quantitative research about food industry

A systematic literature review of food sustainable supply chain management (FSSCM): building blocks and research trends

The TQM Journal

ISSN : 1754-2731

Article publication date: 6 December 2021

Issue publication date: 19 December 2022

The purpose of this paper is to explore the increased research attention gained by sustainability in food supply chain management. Although previous review studies have focused on aspects such as traceability, food safety, and performance measurement, sustainability has rarely been considered as a means of integrating these issues.

Design/methodology/approach

The paper presents a comprehensive review of the literature on food sustainable supply chain management (FSSCM). Using systematic review methods, relevant studies published from 1997 to early 2021 are explored to reveal the research landscape and the gaps and trends.

The paper shows the building blocks and the main research directions in FSSCM, particularly considering the opportunities in “neglected” emerging countries. Insights are provided into the various elements of the sustainability supply chain in the food industry, which have previously been analysed separately.

Originality/value

Only a few researchers have systematically reviewed the literature or taken a bibliometric approach in their analyses to provide an overview of the current trends and links between sustainability and food supply chain management.

• Systematic literature review
• Food sustainable supply chain management (FSSCM)
• Food industry
• Global supply chain
• Emerging countries
• Sustainability

Palazzo, M. and Vollero, A. (2022), "A systematic literature review of food sustainable supply chain management (FSSCM): building blocks and research trends", The TQM Journal , Vol. 34 No. 7, pp. 54-72. https://doi.org/10.1108/TQM-10-2021-0300

Emerald Publishing Limited

Copyright © 2021, Maria Palazzo and Agostino Vollero

Published by Emerald Publishing Limited. This article is published under the Creative Commons Attribution (CC BY 4.0) licence. Anyone may reproduce, distribute, translate and create derivative works of this article (for both commercial and non-commercial purposes), subject to full attribution to the original publication and authors. The full terms of this licence may be seen at http://creativecommons.org/licences/by/4.0/legalcode

1. Introduction

The debate over the approach to sustainability has become central to most businesses, as a proper sustainability perspective holistically considers all of a company's functions and business relationships along supply chains, which are increasingly interconnected globally ( Carter and Rogers, 2008 ; Solér et al. , 2010 ). Managing the integration of sustainable environmental, social and economic criteria along the multiple aspects of the supply chain represents a major challenge for manufacturers and producers ( Massaroni et al. , 2015 ).

Supply chain management (SCM) has been defined as “the configuration and operation of efficient and effective production and logistics networks and the intra- and inter-organizational management of supply, transformation and delivery processes” ( Brandenburg and Rebs, 2015 ). A revolution in SCM has occurred in recent years, which has been noted by many scholars and researchers, as its focus has shifted from economic performance to an integrated social and environmental approach ( Seuring and Müller, 2008 ; Ahi and Searcy, 2013 ; Khan et al. , 2020 ).

Exploring the intersection between sustainability and SCM involves considering different viewpoints, as SCM is based on both downstream and upstream flows of goods ( Cosimato and Troisi, 2015 ; Fahimnia et al. , 2015 ; Maditati et al. , 2018 ). The downstream flows of goods (towards the final customer) has been traditionally viewed as involving responsibility and ethical issues ( Seuring and Müller, 2008 ), while upstream flows of products/services (towards the supplier) are explored from manufacturing, product recovery and reverse logistics perspectives ( Feng et al. , 2017 ), and thus more concerned with environmental issues, such as energy and waste reduction ( Naik and Suresh, 2018 ; Kumar et al. , 2020 ; Kumari et al. , 2021 ). There is general agreement that the sustainable management of a supply chain requires an integrated approach to social, environmental and economic goals ( Carter and Rogers, 2008 ; Hassini et al. , 2012 ; Juettner et al. , 2020 ). Thus, the means by which SCM can develop sustainable features and follow the path of sustainable development have been considered ( Manning, 2013 ; Zhu et al. , 2018 ). This can be challenging in industries such as food, in which the SCM can have a strong effect on not only the final consumer but also other stakeholders in the value chain ( Matopoulos et al. , 2015 ; Ghadge et al. , 2017 ; Mangla et al. , 2019 ).

A food supply chain (FSC) is particularly complex, as it connects different sectors of the economy (agriculture and the food-processing industry and distribution sector) in a market dominated by rapidly changing customer preferences ( Beske et al. , 2014 ). Food types can affect the natural environment, due to the food production systems, transport distances from producers and consumers, waste management, and workers' conditions in the sectors involved ( Beer and Lemmer, 2011 ). The situation is even more complicated in the agri-fresh food sector due to the perishability of products and the short shelf-life ( Siddh et al. , 2017 ). Thus, examining sustainable development in the FSC is extremely complex due to the high level of unpredictability in terms of demand and cost, the fragile nature of food and consumers' increased awareness of risks and safety issues associated with diets and eating disorders ( Siddh et al. , 2018 ). Finally, many firms in the FSC are small or medium-sized enterprises (SMEs) ( Beer and Lemmer, 2011 ; Ghadge et al. , 2017 ) that may find it difficult to address sustainability challenges and implement practices. The various FSC duties and tasks are often perceived as more demanding when sustainability is applied to enrich conventional profit-oriented models ( Allaoui et al. , 2018 ). Studies in this area have addressed issues such as the triple bottom line, ethics and corporate social responsible principles in their analyses ( Siddh et al. , 2018 ; Allaoui et al. , 2018 ), but few have provided an integrated overview of the phenomenon.

Only a few researchers have systematically reviewed the literature or taken a bibliometric approach in their analyses to provide an overview of the current trends and links between sustainability and food supply chain management (FSCM). However, many articles have applied specific methods to explore particular themes or typical processes. These themes and processes include sustainable sourcing ( Ghadge et al. , 2017 ), food traceability ( Bosona and Gebresenbet, 2013 ), approaches for enhancing sustainability in SCM ( Sharma et al. , 2017 ; Dania et al. , 2018 ), sustainable supply chain strategies and tactics ( Beske et al. , 2014 ; Zhong et al. , 2017 ), food safety ( Siddh et al. , 2018 ), controls of the level of sustainability ( Sharma et al. , 2017 ), measurements of sustainable items ( Sharma et al. , 2021 ) and the circular economy ( Corallo et al. , 2020 ).

Bosona and Gebresenbet (2013) , for example, presented a literature review that focussed mainly on food traceability, which highlights several features, definitions, items and measurements of the food traceability system. The bibliometric approach was also taken by Beske et al. (2014) , who described how sustainable supply chain management tactics allow organizations to manage their supply chain while putting into practice dynamic capabilities. Zhong et al. (2017) used the bibliometric approach to review the FSCM, and considered it in terms of systems and implementations. Siddh et al. (2017) explored the agri-fresh food supply chain quality features and definitions, by collecting and analysing relevant academic papers. Using the same method, Sharma et al. (2017) analysed the performance indicators and sub-indicators of green SCM implementation. Dania et al. (2018) proposed a systematic review of sustainable agri-food supply chains to assess and manage collaborative performances, while Govindan (2018) focused on the influence of stakeholders in the food industry.

Thomé et al . (2020) recently provided several insights into food supply chains and short food supply chains based on a bibliometric analysis, while Kamble et al. (2020) proposed a framework for managers in the agri-food supply chain based on an extensive literature review, to increase supply chain visibility and resources. Finally, Sharma et al. (2020) applied a systematic literature review of machine learning applications in agricultural supply chains.

These studies demonstrate the pressing need to examine the “green” side of SCM in the food sector. They show that the number of empirical papers in this area is increasing, but that there is a lack of an integrated perspective for holistically linking recent trends and facets of the FSCM. The focus is on very specific viewpoints rather than a broader exploration. To increase our understanding of the intellectual progress and knowledge structure of food sustainable supply chain management (FSSCM), a comprehensive analysis is required. Thus, in the present paper, we aim to outline a comprehensive framework of the research and current trends in the FSSCM, and to identify specific research gaps that must be addressed.

To achieve this, earlier review analyses of FSSCM and broad research trends are identified objectively and systematically, by providing an analysis of the evolution of FSSCM over the past years, exploring the international research, studying the mainly empirical FSSCM research, examining the research tools applied, identifying any issues that arise, and by identifying the main gaps and directions for future research in the field of FSSCM.

The remainder of this paper is organized as follows. Section 2 presents the methodology used for the literature review. Section 3 provides the results and analyses of the selected papers. Sections 4 and 5 present the findings, a discussion and the implications in terms of FSSCM that can enrich further research. Finally, a conclusion and limitations are presented in Section 6 .

2. Methodology

As other studies take various specific perspectives, we applied a comprehensive analysis of the literature focussing on the link between sustainability and FSCM. This offers a complete view and several insights for further studies in various emerging business contexts.

Unlike other conventionally structured literature reviews, a systematic review was selected as this can be effective in managing the exploration of a huge number of academic publications and enables the development of a complex framework for the research subjects ( Garcia-Buendia et al. , 2021 ). The method can also help researchers and scholars explore the literature by considering its bibliographic elements ( Xu et al. , 2020 ). This analytical approach also helps in terms of recognizing the main features and definitions of specific research field(s), identifying the main research questions and gaps, identifying the theoretical area in which the analyses will have an effect, understanding the theoretical concepts and their terminology, providing a list of the relevant resources available, and highlighting the research designs, methodologies and approaches that can be applied ( Soni and Kodali, 2011 ; Fahimnia et al. , 2015 ; Feng et al. , 2017 ).

Time horizon: The first step is the selection of a time period. The exploration period for academic and research articles is between 1997 and early 2021, as SCM and corporate social responsibility (CSR) were implemented in the food industry to a greater extent after 1997 ( Henk and Hans, 1997 ). We end our paper collection in early 2021.

Selection of publications: Only papers written in English were selected, and the articles were selected in Scopus. This database is commonly used by management science researchers (or in related fields) for bibliometric analyses or systematic literature review methods in SCM ( Soni and Kodali, 2011 ; Fahimnia et al. , 2015 ). The Scopus database has greater coverage than the Web of Science, and it was deemed more appropriate for exploring complex research areas that are constantly changing and developing ( Feng et al. , 2017 ).

The keywords used for the selection of the publications: The keywords chosen for developing the search of the main publications in Scopus were “supply”, “food”, and “sustainabl*”. In total, after using the “title, abstract, keywords” search in the Scopus, 1,930 papers were found by searching with these keywords. “Sustainabl*” involves environmental, economic, and social facets, and thus papers identified by searching for “sustainabl*” and “supply” were examined. The papers resulting from the searches were then analysed for information including title, author(s), affiliation(s), source title, number of citations, keywords, abstract and references.

The categorization of academic publications according to the Association of Business Schools (ABS) 2018 list: The number of papers was further reduced by selecting only academic and well-referred journals that were considered in this list. Of the 1,930 papers, some were non-referred publications appearing in 0-star journals, magazines and conference proceedings that did not follow a rigorous scientific editorial approach. Chapters of books and whole books were also not selected for the analysis. After deleting these, 733 articles remained and were filtered from the total number of downloaded publications.

Categorization of academic publications: After reading the abstracts and the complete papers, the number was further reduced by considering the relevance of the publications. The sample size was condensed in this phase to create a representative data set. The rule for selecting the articles was that they had to be related to the food sector, supply chain management and sustainability. Thus, 176 papers remained.

Systematic classifications of the papers: The articles were then categorized according to leading journals in FSSCM research and journal name per number of published articles; number of published articles in FSSCM research per field; number of publications; trending articles about the food sustainable supply chain; geographical locations by region of the first author's affiliation; the methodology used; theoretical frameworks; tool/research methods; data collection; the entity of analysis and sustainability issues.

3. Results and analysis

All of the identified papers are presented, discussed and analysed in the following sections in terms of their various aspects and features.

3.1 Year-based classification of number of publications

The number of articles about FSSCM has increased, probably due to the increased interest and awareness of managers and academics in the area of sustainability and SCM. The annual number of published articles has increased in recent times (2017–2020) to three times that of the 2015–2016 period (in fact, in 2017, 26 papers were published; in 2018, 29 articles were proposed; while in 2019 and 2020, 23 and 27 studies were focused on the selected topics).

3.2 Journal-based categorization of papers

This categorization illustrates the frequency of papers presented in various leading academic journals. Many of these appear to be very interested in issues and problems related to FSSCM. These include Business Strategy and the Environment (BSE), the British Food Journal (BFJ), Corporate Social Responsibility and Environmental Management (CSREM), Food Policy (FP), Industrial Management and Data Systems (IMDS), International Journal of Production Economics (IJPE), International Journal of Production Research (IJPR), Journal of Cleaner Production (JCP), Journal of Manufacturing Technology Management (JMTM), Production Planning and Control (PPC), and Supply Chain Management – An International Journal (SCM-IJ).

In total, 176 papers that focused on SCM definitions and features in the food industry from the perspective of sustainability were selected. This demonstrates that a considerable number of papers were published in the relevant fields of study. Table 1 shows the number of total articles published (PSC) and average global citations received per paper (AGC), and most are from JCP (49 PSC, 28.24 AGC), followed by IJPE (18 PSC, 94.56 AGC), PPC (7 PSC, 4.14 AGC), SCM-IJ (7 PSC, 17.29 AGC), and BSE (6 PSC, 21.67 AGC). Considering the average global citations received per paper (AGC), the journals with the highest are IJPE (18 PSC, 94.56 AGC), IJPR (5 PSC, 81.60 AGC), FP (4 PSC, 75.50 AGC), CSREM (4 PSC, 41.25 AGC) and JCP (49 PSC, 28.24 AGC).

Moreover, the distribution of published articles in FSSCM research per field (economics; ethics-csr management; international business and area; information management; marketing; operations research and management science; organizational studies; regional studies; sector; social studies), based on how they are ranked in the ABS Journal Guide of 2018 was analysed.

It was highlighted that, especially, in the fields of “Operations Research and Management Science” and “Sector”, there were many articles published in 2018, 2019 and 2020 in the realm of FSSCM.

3.3 Categorization of publications based on the geographical location of first authors

Publications are classified based on the first authors' affiliated regions and include developed and emerging economies. This classification clearly shows that most papers are from developed countries in Europe (63%), Asia (18%) and North America (8%), with less attention paid to FSSCM in developing areas such as South America (5%) and Africa (1%), although many countries in these regions are still mainly agrarian.

3.4 Categorization of trending articles in the field of FSSCM

Several of the papers achieved a remarkable number of total citations. The data presented in Table 2 show that two papers gained more than 300 total citations, four achieved over 200, and the remaining four publications gained more than 100 total citations.

3.5 Categorization based on methodology and tools/research methods

FSSCM papers can be analysed according to the methodology (approach) applied. Most publications utilized a qualitative approach (78%) and only 22% take a quantitative approach.

Table 3 shows that theoretical and empirical explorations of SCM sustainability in the food sector have been conducted ( Pohlmann et al. , 2020 ; Yakavenka et al. , 2020 ; Khan et al. , 2021 ).

Case study analysis is the most used (26%: 46 papers) followed by statistical analysis (22%: 38 papers), conceptual analysis and/or frameworks (19%: 34 articles), mathematical models (13%: 23 articles), quality tool (11%: 19 articles) and finally bibliometric analysis and/or literature review (9%: 16 papers). Examples of the methodologies and tools applied to this complex concept include the following: Taghikhah et al. (2020) used several mathematical models to explore the relation between consumer preferences and environmental factors related to food production. Morley (2020) used case studies to analyse the impact of public procurement on various food company strategies. Thomé et al . (2020) used a structured literature review to examine studies of short food supply chains. Sharma et al. (2020) statistically analysed aspects of food and other industries during the coronavirus disease 2019 (COVID-19) pandemic.

3.6 Research publications categorization on the basis of data collection

We first examine the data collection (data sources) applied in the FSSCM papers and find that the majority of the publications use primary data (i.e. survey, experiment, interviews, focus groups, observation, etc.) (56%: 99 papers). Secondary data (i.e. archival, content extraction, bibliometric records, etc.) are used in 46 papers (26%), a combination of primary and secondary data is used in 10 (6%), and 21 papers (12%) do not use data collection as they are based on conceptual analyses, viewpoint research, etc.

3.7 Research publications categorization based on issues of FSSCM

We then categorize the papers based on the FSSCM issues addressed, as shown in Figure 2 . FSSCM involves multiple sustainability issues, and the majority of articles focused on “supplier management” (20%: 36 papers). “Sustainable development” was the next most common (17%: 30 papers), followed by “collaboration and coordination management” in 25 (14%), “performance management” in 17 (10%), “circular economy” in 15 (9%), “logistic management” in 14 (8%), “strategic management” in 11 (6%), “innovation” in 10 (6%), “agriculture” in 6 (3%), a “comprehensive view” (involving more than one issue) in 5 (3%), “quality management” in 4 (2%), and “other issues” were analysed in 3 papers (2%).

Thus, “supplier management”, “sustainable development” and “collaboration and coordination management” were the most common issues, covered by over half of the total selected publications. Other issues are also significant in the area of FSSCM, but not to the same extent, while others are mainly neglected (i.e. “agriculture” and “quality management”)

3.8 Research publications categorization on the basis of theoretical framework

The theoretical framework applied to develop the selected papers was then explored. Nearly two-thirds (114) of the articles did not follow any specific theoretical approach. The stakeholder approach was considered in 11 articles, 8 papers were based on the triple bottom line, 8 took the life cycle approach, 7 the circular economy approach, 6 applied resource-based view (RBV) and knowledge-based view (KBV) frameworks, 6 the institutional theory, 4 applied the resource dependency theory and 2 the decision theory-based framework. Other approaches (i.e. country of origin, TOE, critical success factors, etc.) were taken in ten articles.

3.9 Publications categorization on the basis of entity of analysis

Finally, we examined the main perspectives taken when exploring FSSCM issues.

Many research publications use the supply chain as the entity of analysis (EOA) (70 papers). However, a significant number (23) consider the whole supply network or the manufacturer's point of view (21); 18 are mainly conceptual; 10 are based on the distributor's perspective; 10 take a dyadic view (more than 1 EOA); 9 take the suppliers'/farmers' perspectives; the logistic industry is examined in 7; consumers in 5; and the remaining 3 papers do not use any of these EOA.

4. Discussion: main themes and trends in FSSCM

The increase and evolution of FSSC studies suggests that supply chains in the food sector are moving towards a sustainable approach. Several new trends have emerged in the field, which focus on both intra- and inter-firm dimensions ( Figure 3 ).

Increasingly, the multiplicity of stakeholders in FSSCM and the collaboration/coordination challenges this brings have been explored throughout the food supply chain phases. These include the sustainable purchasing relationships of food retailers ( Chkanikova, 2016 ); increasing legitimacy in the food industry ( Czinkota et al. , 2014 ); strategies for reducing food waste within the circular economy framework ( Dora, 2019 ); and tools for increasing collaboration and coordination throughout the food supply chain ( Vodenicharova, 2020 ). Collaboration has gained the attention of researchers exploring the competitive advantages derived from a sustainable approach by leveraging environmental information along the supply chain ( Solér et al. , 2010 ), the alignment of sourcing with marketing and branding strategies ( Croom et al. , 2007 ), and dynamic capabilities ( Beske et al. , 2014 ).

“Collaboration and coordination management”, “supplier management” and “sustainable development” are the most common issues, covered by over half of the total publications. These include collaboration with partners along the supply chain ( Pakdeechoho and Sukhotu, 2018 ), the criteria for selecting suppliers ( Wilhelm et al. , 2016 ), the alignment of supplier-producer procedures ( Vodenicharova, 2020 ), the overall efficiency of the supply chain ( Danny and Priscila, 2004 ), and collaborations adopting mandatory and voluntary standards when assessing environmental, social and economic performances ( Glover et al. , 2014 ; Touboulic and Walker, 2015 ; Govindan, 2018 ). Other recent emerging challenges include more general sustainability-related aspects, such as innovation and the circular economy. On the other hand, the inclusion of quality management in the field of FSCM seems to be scarce in academic literature ( Ting et al. , 2014 ; Siddh et al. , 2018 ; Feng et al. , 2020 ), even though, there are several authors who tried to build a more centred approach in reviewing quality issues inside the analysis of sustainable supply chain. For example, Manzini et al. (2014) highlighted the existing connection between food quality and environmental sustainability of supply chain strategies and tactics, while Winter and Knemeyer (2013) explored how sustainability can be included in supply chain quality and, Ilbery and Maye (2005) presented a list of important sustainable food standards linked with environmental quality, socially inclusiveness and other relevant items.

Besides, the findings suggest that an integration of intra- and inter-firm processes can be crucial for the effective sustainable performance of organizations, as if FSSCM is based on sustainability it can have a positive effect on all stages of the supply chain ( Erol et al. , 2011 ; Kahi et al. , 2017 ). Unlike traditional performance measurements, sustainable performance involves comprehensively considering social, economic, and environmental factors ( Sharma et al. , 2017 ; Siddh et al. , 2018 ). Pullman et al. (2009) focussed on how to improve the quality performance of the food supply chain, which in turn improves cost performance. Raut et al. (2019) analysed operational/technology-based and human resource-based performance indicators of the sustainable value chain that help those in the food sector minimize their effect on the environment while boosting their economic performance. Thus, when proposing new “green” performance measurements, food industry researchers should include the bases of sustainability in their analyses of FSSCM.

The development of these new FSSCM trends suggests that this field of research will continue to grow as many scholars and academics explore the specific features and perspectives applicable to developed countries. The literature review shows that few studies consider less developed countries, with just 1% having African authors. Developing economies, such as those in Asia, have however had more attention in recent years. Some studies show that a lack of infrastructure or inefficient logistics could result in more food waste and inefficient processes ( Naik and Suresh, 2018 ; Kumar et al. , 2020 ). This is a major issue in FSSCM, as it is expected that 90% of the global population will live in developing countries by 2050 ( PRB, 2020 ). Sustainability is therefore vital in the food global supply chains of these countries, which are characterized by strong interdependencies along the north-south axis.

Most scholars investigating the sustainability of the food supply chain directly collect their data using tools such as surveys, experiments, interviews, and focus groups. The case study is the most common method for these explorations, as indicated in previous research ( Ashby et al. , 2012 ; Massaroni et al. , 2015 ). This emphasis on case studies indicates the novel and fast-changing nature of the field, and that more in-depth investigations are required to identify its boundaries and foundations. However, modelling-based studies are increasing in number (e.g. Chen et al. , 2018 ) as they address the need for a more integrated understanding of sustainable supply chains ( Brandenburg et al. , 2014 ). In addition, the lack of specific theoretical frameworks in two-thirds of the studies indicates that the research field is still emerging, and thus extensive opportunities for research that bridges the gap between theory and practice are presented.

5. Implications and research directions

This systematic literature review offers several implications for practitioners, and insights for further research in the field of FSSCM.

Food supply chains make a significant contribution to the global economy and sustainable development, as they involve suppliers and other stakeholders from various industries working together so food can reach the final consumer ( Joshi et al. , 2020 ; Kamble et al. , 2020 ; Thomé et al. , 2020 ). Kamble et al. (2020) suggest that better economic performance and social wellbeing can be achieved by food suppliers, retailers and others only if critical post-harvest losses can be avoided by applying new methods linked with supply chain visibility and sustainable resources. Thus, the focus should be on the upstream of the supply chain, particularly in many under-developed and developing nations where agriculture is still the essential basis of the economy ( Taghikhah et al. , 2020 ). Some studies were identified as being conducted in developing geographic areas, but more should be encouraged due to the greater potential FSSCM can bring.

The specific directions identified include those of Kumar Sharma et al. (2019) , who stated that the circular economy and sustainability are complex and must be managed by decision makers and practitioners in both developed and developing nations. They proposed a model that can inform the implementation of circular economy-driven sustainability FSC activities in emerging and under-developed economies, particularly in India.

Asian et al. (2019) examined how the increasing costs of logistics, lower yields, and strategic barriers have a negative impact on the level of competitiveness of farmers in developing countries. The authors proposed an algorithm to help key decision makers address the challenges of the FSC and sustainable development. Further studies can also develop theories and practical tools based on specific features, as these geographic areas can support the food industry through new sustainable strategies and tactics.

Such strategies and tactics are high on the agendas of many types of companies, but the business models of start-ups differ from those of other organizations and thus affect their creation and implementation. Larger companies may be able to better sustain the impact of the evolving trends of FSSCM, but they may also be less flexible than start-ups in finding opportunities and innovating ( Suchek et al. , 2021 ).

As suggested in previous sections, researchers must also focus on assessing the reliability and trustworthiness of FSSCM theories, as we found that many papers focussed on theory building. However, these theories generally address specific facets and thus the results cannot be easily generalized. Our study enriches the research by reviewing the most common theoretical approaches (e.g. the stakeholder approach, triple bottom line, the life cycle approach), and others that are less used (i.e. RBV and KBV, institutional theory, resource dependency theory, decision theory-based framework, etc.). This requires further exploration as a need to build a more solid conceptual framework for FSSCM research has also emerged.

In terms of FSSCM measurement and control, our analysis reveals an increase in the development of standardized constructs, which can be used to monitor and control how companies involved in the FSC achieve a successful level of sustainable development ( Folkerts and Koehorst, 1998 ; Yakovleva et al. , 2012 ; Sharma et al. , 2017 ). This is required as most aspects of FSSCM are associated with government regulation, incentive policies, stakeholders' approval of pioneering “green” products/services and the associated cultural and social consequences, and entrepreneurs' inclinations to follow ground-breaking sustainable principles. These trends are often related to the market, and involve accessibility, the costs of raw materials, and new technology, which require specific knowledge and thus may incur huge costs that many companies cannot afford.

In terms of the EOA, we suggest that future empirical research should focus on intra-functional and intra-firm exploration at corporate and network levels, or on dyads that reveal the relationships between pairs of organizations (i.e. farms, manufacturers, distributors, etc.). Similarly, Siddh et al. (2017) also emphasized that empirical research should focus on exploring intra-firm and intra-functional relations, as integration between companies should be encouraged before sustainability at different levels of the FSC is achieved. Finally, the role of end consumers in the FSSCM is still largely unexplored but important, as they can prompt organizations, dyads and networks to adopt more efficient and effective methods of introducing sustainable innovations and identifying new niche opportunities in this area.

6. Conclusion

In this paper we provide a literature review of papers focussed on the various facets of the FSSCM. We identify relevant papers published over the past 23 years (1997 to early 2021), with the aim of informing academics and practitioners about the research landscape, gaps, and current and future trends in the FSSCM. The literature review considers 176 influential peer-reviewed articles using accurate selection procedures and content investigation.

The majority of the selected papers were published in the last eight years (2014–2021), probably due to the increased awareness of environmental problems and of the need to reduce hunger globally (Zero Hunger is Goal Two of the Sustainable Development Goals of the 2030 Agenda), the increased food risks, an awareness of the benefits of decreasing food wastage, health management and of the well-being of people in all geographical areas (Goal Three: Good Health and Well-being).

FSSCM research is undoubtedly increasing, but few studies succeed in combining the various sustainability constructs with the main elements of the FSCM, particularly in the context of developing/under-developed countries. Thus, there are opportunities to increase our understanding of the integrative factors, particularly in less-developed regions of the world.

Our research has various limitations, like most studies. First, we used the specific keywords “supply”, “food”, and “sustainabl*” to select the articles from the Scopus database. While this identified nearly 2000 articles, using different keywords may have a different outcome. Additionally, only one database was used, so researchers can explore others such as Web of Science and compare their findings to ours, and although many analyses were identified, other methods of bibliometric analysis and systematic literature review may offer different insights into the specific context. Thus, we suggest that researchers apply different bibliometric methods when addressing this research domain.

Steps of the systematic literature review

Main sustainability issues in the field of FSSCM

Trends in FSSCM research

Leading journals in FSSCM research

Applied tools/research methods in the field of FSSCM

Ahi , P. and Searcy , C. ( 2013 ), “ A comparative literature analysis of definitions for green and sustainable supply chain management ”, Journal of Cleaner Production , Vol.  52 , pp.  329 - 341 .

Allaoui , H. , Guo , Y. , Choudhary , A. and Bloemhof , J. ( 2018 ), “ Sustainable agro-food supply chain design using two-stage hybrid multi-objective decision-making approach ”, Computers and Operations Research , Vol.  89 , pp.  369 - 384 .

Ashby , A. , Leat , M. and Hudson-Smith , M. ( 2012 ), “ Making connections: a review of supply chain management and sustainability literature ”, Supply Chain Management , Vol.  17 No.  5 , pp.  497 - 516 .

Asian , S. , Hafezalkotob , A. and John , J.J. ( 2019 ), “ Sharing economy in organic food supply chains: a pathway to sustainable development ”, International Journal of Production Economics , Vol.  218 , pp.  322 - 338 .

Beer , S. and Lemmer , C. ( 2011 ), “ A critical review of ‘green’ procurement: life cycle analysis of food products within the supply chain ”, Worldwide Hospitality and Tourism Themes , Vol.  3 No.  3 , pp.  229 - 244 .

Beske , P. , Land , A. and Seuring , S. ( 2014 ), “ Sustainable supply chain management practices and dynamic capabilities in the food industry: a critical analysis of the literature ”, International Journal of Production Economics , Vol.  152 , pp.  131 - 143 .

Bosona , T. and Gebresenbet , G. ( 2013 ), “ Food traceability as an integral part of logistics management in food and agricultural supply chain ”, Food Control , Vol.  33 No.  1 , pp.  32 - 48 .

Brandenburg , M. and Rebs , T. ( 2015 ), “ Sustainable supply chain management: a modeling perspective ”, Annals of Operations Research , Vol.  229 No.  1 , pp.  213 - 252 .

Brandenburg , M. , Govindan , K. , Sarkis , J. and Seuring , S. ( 2014 ), “ Quantitative models for sustainable supply chain management: developments and directions ”, European Journal of Operational Research , Vol.  233 No.  2 , pp.  299 - 312 .

Carter , C.R. and Rogers , D.S. ( 2008 ), “ A framework of sustainable supply chain management: moving toward new theory ”, International Journal of Physical Distribution and Logistics Management , Vol.  38 No.  5 , pp.  360 - 387 .

Chen , Y. , Wang , S. , Yao , J. , Li , Y. and Yang , S. ( 2018 ), “ Socially responsible supplier selection and sustainable supply chain development: a combined approach of total interpretive structural modeling and fuzzy analytic network process ”, Business Strategy and the Environment , Vol.  27 No.  8 , pp.  1708 - 1719 .

Chkanikova , O. ( 2016 ), “ Sustainable purchasing in food retailing: inter-organizational relationship management to green product supply ”, Business Strategy and the Environment , Vol.  25 No.  7 , pp.  478 - 494 .

Corallo , A. , Latino , M.E. , Menegoli , M. and Pontrandolfo , P. ( 2020 ), “ A systematic literature review to explore traceability and lifecycle relationship ”, International Journal of Production Research , Vol.  58 No.  15 , pp.  4789 - 4807 .

Cosimato , S. and Troisi , O. ( 2015 ), “ Green supply chain management: practices and tools for logistics competitiveness and sustainability. The DHL case study ”, The TQM Journal , Vol.  27 No.  2 , pp.  256 - 276 .

Croom , S. , Cox , A. , Chicksand , D. and Yang , T. ( 2007 ), “ The proactive alignment of sourcing with marketing and branding strategies: a food service case ”, Supply Chain Management: An International Journal , Vol.  12 No.  5 , pp.  321 - 333 .

Czinkota , M. , Kaufmann , H.R. and Basile , G. ( 2014 ), “ The relationship between legitimacy, reputation, sustainability and branding for companies and their supply chains ”, Industrial Marketing Management , Vol.  43 No.  1 , pp.  91 - 101 .

Dania , W.A.P. , Xing , K. and Amer , Y. ( 2018 ), “ Collaboration behavioural factors for sustainable agri-food supply chains: a systematic review ”, Journal of Cleaner Production , Vol.  186 , pp.  851 - 864 .

Danny , P.C. and Priscila , B.D.O.C. ( 2004 ), “ Coordinating B2B cross-border supply chains: the case of the organic coffee industry ”, The Journal of Business and Industrial Marketing , Vol.  19 No.  6 , pp.  405 - 414 .

Dora , M. ( 2019 ), “ Collaboration in a circular economy: learning from the farmers to reduce food waste ”, Journal of Enterprise Information Management , Vol.  33 No.  4 , pp.  769 - 789 .

Erol , I. , Sencer , S. and Sari , R. ( 2011 ), “ A new fuzzy multi-criteria framework for measuring sustainability performance of a supply chain ”, Ecological Economics , Vol.  70 No.  6 , pp.  1088 - 1100 .

Fahimnia , B. , Sarkis , J. and Davarzani , H. ( 2015 ), “ Green supply chain management: a review and bibliometric analysis ”, International Journal of Production Economics , Vol.  162 No.  c , pp.  101 - 114 .

Feng , Y. , Zhu , Q. and Lai , K.H. ( 2017 ), “ Corporate social responsibility for supply chain management: a literature review and bibliometric analysis ”, Journal of Cleaner Production , Vol.  100 No.  158 , pp.  296 - 307 .

Feng , H. , Wang , X. , Duan , Y. , Zhang , J. and Zhang , X. ( 2020 ), “ Applying blockchain technology to improve agri-food traceability: a review of development methods, benefits and challenges ”, Journal of Cleaner Production , Vol.  260 , 121031 .

Folkerts , H. and Koehorst , H. ( 1998 ), “ Challenges in international food supply chains: vertical co-ordination in the European agribusiness and food industries ”, British Food Journal , Vol.  100 No.  8 , pp.  385 - 388 .

Garcia-Buendia , N. , Moyano-Fuentes , J. , Maqueira-Marín , J.M. and Cobo , M.J. ( 2021 ), “ 22 Years of lean supply chain management: a science mapping-based bibliometric analysis ”, International Journal of Production Research , Vol.  59 No.  6 , pp.  1901 - 1921 .

Ghadge , A. , Kaklamanou , M. , Choudhary , S. and Bourlakis , M. ( 2017 ), “ Implementing environmental practices within the Greek dairy supply chain drivers and barriers for SMEs ”, Industrial Management and Data Systems , Vol.  117 No.  9 , pp.  1995 - 2014 .

Glover , J.L. , Champion , D. , Daniels , K.J. and Dainty , A.J. ( 2014 ), “ An institutional theory perspective on sustainable practices across the dairy supply chain ”, International Journal of Production Economics , Vol.  152 No.  C , pp.  102 - 111 .

Govindan , K. ( 2018 ), “ Sustainable consumption and production in the food supply chain: a conceptual framework ”, International Journal of Production Economics , Vol.  195 No.  C , pp.  419 - 431 .

Hassini , E. , Surti , C. and Searcy , C. ( 2012 ), “ A literature review and a case study of sustainable supply chains with a focus on metrics ”, International Journal of Production Economics , Vol.  140 No.  1 , pp.  69 - 82 .

Henk , F. and Hans , K. ( 1997 ), “ Challenges in international food supply chains: vertical co-ordination in the European agribusiness and food industries ”, Supply Chain Management: An International Journal , Vol.  2 No.  1 , pp.  11 - 14 .

Ilbery , B. and Maye , D. ( 2005 ), “ Food supply chains and sustainability: evidence from specialist food producers in the Scottish/English borders ”, Land Use Policy , Vol.  22 No.  4 , pp.  331 - 344 .

Joshi , S. , Singh , R.K. and Sharma , M. ( 2020 ), “ Sustainable agri-food supply chain practices: few empirical evidences from a developing economy ”, Global Business Review , Vol.  1 No.  24 .

Juettner , U. , Windler , K. , Podleisek , A. , Gander , M. and Meldau , S. ( 2020 ), “ Implementing supplier management strategies for supply chain sustainability risks in multinational companies ”, The TQM Journal , Vol.  32 No.  5 , pp.  923 - 938 .

Kahi , V.S. , Yousefi , S. , Shabanpour , H. and Saen , R.F. ( 2017 ), “ How to evaluate sustainability of supply chains? A dynamic network DEA approach ”, Industrial Management and Data Systems , Vol.  117 , pp.  1866 - 1889 .

Kamble , S.S. , Gunasekaran , A. and Gawankar , S.A. ( 2020 ), “ Achieving sustainable performance in a data-driven agriculture supply chain: a review for research and applications ”, International Journal of Production Economics , Vol.  219 , pp.  179 - 194 .

Khan , S.A.R. , Yu , Z. , Golpîra , H. , Sharif , A. and Mardani , A. ( 2020 ), “ A state-of-the-art review and meta-analysis on sustainable supply chain management: future research directions ”, Journal of Cleaner Production , Vol. 278 , 123357 .

Khan , S.A. , Mubarik , M.S. , Kusi‐Sarpong , S. , Zaman , S.I. and Kazmi , S.H.A. ( 2021 ), “ Social sustainable supply chains in the food industry: a perspective of an emerging economy ”, Corporate Social Responsibility and Environmental Management , Vol.  28 No.  1 , pp.  404 - 418 .

Kumar , A. , Mangla , S.K. , Kumar , P. and Karamperidis , S. ( 2020 ), “ Challenges in perishable food supply chains for sustainability management: a developing economy perspective ”, Business Strategy and the Environment , Vol.  29 No.  5 , pp.  1809 - 1831 .

Kumar Sharma , Y. , Mangla , S. , Patil , P. and Liu , S. ( 2019 ), “ When challenges impede the process: for circular economy driven sustainability practices in food supply chain ”, Management Decision , Vol.  57 No.  4 , pp.  995 - 1017 .

Kumari , S. , Raghuram , P. , Venkatesh , V.G. and Shi , Y. ( 2021 ), “ Future perspectives on progressive farming with adoption of virtual reality technology for sustainable quality in agriculture ”, The TQM Journal , Vol. ahead-of-print No. ahead-of-print , doi: 10.1108/TQM-06-2021-0191 .

Maditati , D.R. , Munim , Z.H. , Schramm , H.J. and Kummer , S. ( 2018 ), “ A review of green supply chain management: from bibliometric analysis to a conceptual framework and future research directions ”, Resources, Conservation and Recycling , Vol.  139 , pp.  150 - 162 .

Mangla , S.K. , Sharma , Y.K. , Patil , P.P. , Yadav , G. and Xu , J. ( 2019 ), “ Logistics and distribution challenges to managing operations for corporate sustainability: study on leading Indian diary organizations ”, Journal of Cleaner Production , Vol.  238 , 117620 .

Manning , L. ( 2013 ), “ Corporate and consumer social responsibility in the food supply chain ”, British Food Journal , Vol.  115 No.  1 , pp.  9 - 29 .

Manzini , R. , Accorsi , R. , Ayyad , Z. , Bendini , A. , Bortolini , M. , Gamberi , M. , Valli , E. and Toschi , T.G. ( 2014 ), “ Sustainability and quality in the food supply chain. A case study of shipment of edible oils ”, British Food Journal , Vol.  116 No.  12 , pp.  2069 - 2090 .

Massaroni , E. , Cozzolino , A. and Wankowicz , E. ( 2015 ), “ Sustainability in supply chain management-a literature review ”, Sinergie Italian Journal of Management , Vol.  33 , pp.  331 - 355 .

Matopoulos , A. , Barros , A.C. and van der Vorst , J.G.A.J. ( 2015 ), “ Resource-efficient supply chains: a research framework, literature review and research agenda ”, Supply Chain Management: An International Journal , Vol.  20 No.  2 , pp.  218 - 236 .

Morley , A. ( 2020 ), “ Procuring for change: an exploration of the innovation potential of sustainable food procurement ”, Journal of Cleaner Production , Vol.  279 , 123410 .

Naik , G. and Suresh , D.N. ( 2018 ), “ Challenges of creating sustainable agri-retail supply chains ”, IIMB Management Review , Vol.  30 , pp.  270 - 282 .

Pakdeechoho , N. and Sukhotu , V. ( 2018 ), “ Sustainable supply chain collaboration: incentives in emerging economies ”, Journal of Manufacturing Technology Management , Vol.  29 No.  2 , pp.  273 - 294 .

Pohlmann , C.R. , Scavarda , A.J. , Alves , M.B. and Korzenowski , A.L. ( 2020 ), “ The role of the focal company in sustainable development goals: a Brazilian food poultry supply chain case study ”, Journal of Cleaner Production , Vol.  245 , 118798 .

PRB ( 2020 ), “ 2020 world population data sheet. World population data sheet (population reference bureau, July 2020) ”, available at: https://www.prb.org/2020-world-population-datasheet .

Pullman , M.E. , Maloni , M.J. and Carter , C.R. ( 2009 ), “ Food for thought: social versus environmental sustainability practices and performance outcomes ”, Journal of Supply Chain Management , Vol.  45 No.  4 , pp.  38 - 54 .

Raut , R.D. , Luthra , S. , Narkhede , B.E. , Mangla , S.K. , Gardas , B.B. and Priyadarshinee , P. ( 2019 ), “ Examining the performance oriented indicators for implementing green management practices in the Indian agro sector ”, Journal of Cleaner Production , Vol.  215 , pp.  926 - 943 .

Seuring , S. and Muller , M. ( 2008 ), “ From a literature review to a conceptual framework for sustainable supply chain management ”, Journal of Cleaner Production , Vol.  16 No.  15 , pp.  1699 - 1710 .

Sharma , A. , Adhikary , A. and Borah , S.B. ( 2021 ), “ Covid-19's impact on supply chain decisions: strategic insights from NASDAQ 100 firms using Twitter data ”, Journal of Business Research , Vol.  117 , pp.  443 - 449 .

Sharma , R. , Kamble , S.S. , Gunasekaran , A. , Kumar , V. and Kumar , A. ( 2020 ), “ A systematic literature review on machine learning applications for sustainable agriculture supply chain performance ”, Computers and Operations Research , Vol.  119 , 104926 .

Sharma , V.K. , Chandna , P. and Bhardwaj , A. ( 2017 ), “ Green supply chain management related performance indicators in agro industry: a review ”, Journal of Cleaner Production , Vol.  141 , pp.  1194 - 1208 .

Siddh , M.M. , Soni , G. , Jain , R. and Sharma , M.K. ( 2018 ), “ Structural model of perishable food supply chain quality (PFSCQ) to improve sustainable organizational performance ”, Benchmarking: An International Journal , Vol.  25 No.  7 , pp.  2272 - 2317 .

Siddh , M.M. , Soni , G. , Jain , R. , Sharma , M.K. and Yadav , V. ( 2017 ), “ Agri-fresh food supply chain quality (AFSCQ): a literature review ”, Industrial Management and Data Systems , Vol.  117 No.  9 , pp.  2015 - 2044 .

Solér , C. , Bergström , K. and Shanahan , H. ( 2010 ), “ Green supply chains and the missing link between environmental information and practice ”, Business Strategy and the Environment , Vol.  19 No.  1 , pp.  14 - 25 .

Soni , G. and Kodali , R. ( 2011 ), “ A critical analysis of supply chain management content in empirical research ”, Business Process Management Journal , Vol.  17 No.  2 , pp.  238 - 266 .

Suchek , N. , Fernandes , C.I. , Kraus , S. , Filser , M. and Sjögrén , H. ( 2021 ), “ Innovation and the circular economy: a systematic literature review ”, Business Strategy and the Environment , Vol. ahead-of-print No. ahead-of-print , pp. 1 - 17 , doi: 10.1002/bse.2834 .

Taghikhah , F. , Voinov , A. , Shukla , N. , Filatova , T. and Anufriev , M. ( 2020 ), “ Integrated modeling of extended agro-food supply chains: a systems approach ”, European Journal of Operational Research , Vol.  288 No.  3 , pp.  852 - 868 .

Thomé , K.M. , Cappellesso , G. , Ramos , E.L.A. and de Lima Duarte , S.C. ( 2020 ), “ Food supply chains and short food supply chains: coexistence conceptual framework ”, Journal of Cleaner Production , Vol. 278 , 123207 .

Ting , S.L. , Tse , Y.K. , Ho , G.T.S. , Chung , S.H. and Pang , G. ( 2014 ), “ Mining logistics data to assure the quality in a sustainable food supply chain: a case in the red wine industry ”, International Journal of Production Economics , Vol.  152 , pp.  200 - 209 .

Touboulic , A. and Walker , H. ( 2015 ), “ Love me, love me not: a nuanced view on collaboration in sustainable supply chains ”, Journal of Purchasing and Supply Management , Vol.  21 No.  3 , pp.  178 - 191 .

Vodenicharova , M.S. ( 2020 ), “ Supply chain study in food industry in Bulgaria ”, International Journal of Retail and Distribution Management , Vol.  48 No.  9 , pp.  921 - 938 .

Wilhelm , M. , Blome , C. , Wieck , E. and Xiao , C.Y. ( 2016 ), “ Implementing sustainability in multi-tier supply chains: strategies and contingencies in managing sub-suppliers ”, International Journal of Production Economics , Vol.  182 , pp.  196 - 212 .

Winter , M. and Knemeyer , A.M. ( 2013 ), “ Exploring the integration of sustainability and supply chain management: current state and opportunities for future inquiry ”, International Journal of Physical Distribution and Logistics Management , Vol.  43 No.  1 , pp.  18 - 38 .

Xu , S. , Zhang , X. , Feng , L. and Yang , W. ( 2020 ), “ Disruption risks in supply chain management: a literature review based on bibliometric analysis ”, International Journal of Production Research , Vol.  58 No.  11 , pp.  3508 - 3526 .

Yakavenka , V. , Mallidis , I. , Vlachos , D. , Iakovou , E. and Eleni , Z. ( 2020 ), “ Development of a multi-objective model for the design of sustainable supply chains: the case of perishable food products ”, Annals of Operations Research , Vol.  294 No.  1 , pp.  593 - 621 .

Yakovleva , N. , Sarkis , J. and Sloan , T. ( 2012 ), “ Sustainable benchmarking of supply chains: the case of the food industry ”, International Journal of Production Research , Vol.  50 No.  5 , pp.  1297 - 1317 .

Zhong , R. , Xu , X. and Wang , L. ( 2017 ), “ Food supply chain management: systems, implementations, and future research ”, Industrial Management and Data Systems , Vol.  117 No.  9 , pp.  2085 - 2114 .

Zhu , Z. , Chu , F. , Dolgui , A. , Chu , C. , Zhou , W. and Piramuthu , S. ( 2018 ), “ Recent advances and opportunities in sustainable food supply chain: a model-oriented review ”, International Journal of Production Research , Vol.  56 No.  17 , pp.  5700 - 5722 .

Acknowledgements

Although the views and ideas expressed in this article are those of Maria Palazzo and Agostino Vollero; “sections 1; 3; 3.1; 3.2; 3.6; 3.8; 4” are attributed to Maria Palazzo; while “sections 2; 3.3; 3.4; 3.5; 3.7; 3.9; 5; 6” are attributed to Agostino Vollero.

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Towards the Quantitative Management of Food Allergens in the Food Industry

• Published: 13 November 2023
• Volume 1 , pages 99–107, ( 2023 )

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• Gustavo A. Polenta 1 , 2 , 3  

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Purpose of Review

This paper reviews different aspects related to recently proposed threshold values for priority food allergens, which are expected to guide food business operator (FBO) and regulatory agencies towards a quantitative management of allergens, providing transparency and trust to the different stakeholders, especially in controverted aspects such as the (over) use of precautionary allergen label (PAL) in food products, and the potential application of quantitative risk analysis, to improve the current management of food allergens.

Recent Findings

Recently, groups of reports were published from an Expert Committee on Risk Assessment of Food Allergens convened by FAO and WHO, to provide the Codex Committee on Food Labelling (CCFL) scientific advice on different topics related to allergen management such as the establishment of threshold levels for priority allergens, recommendations on the potential use of these thresholds by the food industry, and the proposal of a risk-based process to scientifically support the inclusion of precautionary allergen labelling (PAL) in foods. These reports are expected to provide internationally harmonized basis to ensure that food labelling is accurate and informative for consumers with food allergies, and that food companies would be able to comply with food safety standards.

Quantitative allergen management will be increasingly important for different stakeholders such as the food industry and regulatory agencies. In this regard, allergen thresholds, defined as the levels of allergens in food products below which the risk of an allergic reaction is considered negligible, can help ensure that food products are safe for consumers with food allergies. FAO and WHO have recently addressed this topic and proposed allergen thresholds for the priority allergens. One of the most important uses of thresholds is in the implementation of PAL, which can help allergic consumers make an informed decision. The use of sound analytical methods represents a key element, which allows to measure the amount of allergens in raw materials, finished products, and food processing environments. This information can be used to identify and address any potential allergen risks. Quantitative risk assessment allows the food industry to identify and assess the risks of allergen cross-contamination. This information can be used to develop, implement, and improve control measures to reduce the risk of cross-contamination and comply with regulations.

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Introduction

Food allergies have emerged as one of the most relevant food safety hazards of the last decades, with an important impact on public health. In fact, in countries such as the UK, food anaphylaxis admissions in hospitals experimented an annual increase of around 6%, from 1.23 to 4.04 per 100,000 population per year (from 1998 to 2018) [ 1 ]. Although current allergen management practices have made food products safer for allergic consumers, there is not yet a harmonized approach to risk assessment and management among different manufacturers. This has led to an increase in precautionary allergen labelling (PAL), eroding consumer trust and making people more likely to take unnecessary risks. Minimizing the risk of allergenic foods is a shared responsibility of all stakeholders. Allergen cross-contact leading to unintended allergen presence (UAP) constitutes a relevant challenge for food business operators (FBO), for which priority allergens must be effectively managed throughout the manufacturing process [ 2 ].

A recent report of FDA comprising the period 2013–2019 indicates that allergens were responsible for most regulated recalls, with milk being the most involved allergen (37.5%). Most allergen recalls (89.4%) were classified as class I, which means that they posed a serious or life-threatening health hazard [ 3 ]. These data are coincident with other global food safety incidents reported by different regulatory agencies (CFIA — Canada, FSANZ — Australia and New Zealand, FSA — UK, etc.), where almost half of the identified hazards ending in recalls were related to allergens (1354 out of 2932) [ 4 ].

The evaluation of quantitative data related to UAP leads to the conclusion that the detected amounts undoubtedly represent a serious concern. In this regard, a study with dark chocolate bars found that 87% of chocolate products with a PAL for milk contained levels of this allergen above 100 parts per million (ppm), and more than half even above 1000 ppm [ 5 ]. These high levels represent a serious risk of triggering anaphylactic reactions.

One of the most relevant aspects of allergens, leading to consistent and transparent managing and clear communication of the allergenic status, would be the establishment of globally accepted threshold values, which should be based on scientifically sound methodologies [ 2 ]. In this regard, the recurrent question referred to allergens “how much is too much?”, first posed by Taylor et al . [ 6 ], has thereafter received considerable attention. Despite its increasing concern, this topic had not been officially addressed until recently [ 7 •, 8 ], when an Expert Committee on Risk Assessment of Food Allergens was convened by FAO and WHO to provide the Codex Committee on Food Labelling (CCFL) with scientific advice on different topics related to allergen management, such as the establishment of threshold levels for priority allergens and recommendations on the potential use of these thresholds by the food industry [ 9 , 10 ••, 11 ]. The general approach on this subject as well as different recommendations from the FAO/WHO committee is currently being evaluated by different regulatory agencies [ 12 , 13 ]. From these and other international discussions, it becomes clear that scientists have currently enough information on threshold doses for the most relevant allergenic foods, to guide food manufacturers on how to protect allergic consumers.

Globally harmonized regulations based on threshold values are expected to improve the quality of life for food-allergic consumers, focussing on the real risks that exist to these consumers. Therefore, considering that PAL is a voluntary labelling system that informs consumers with food allergies about the potential presence of allergens in food, the establishment of harmonized allergen threshold values will allow for a more rational assessment of the real need to include it. However, up to the present, PAL has not always been effective in mitigating risks, due to inconsistencies in its application. This paper reviews several aspects related to threshold values for priority food allergens, which can now guide FBO and regulatory agencies towards a quantitative management of allergens, providing transparency and trust to the different stakeholders.

Rational Use of PAL in Food Products

It is important to consider that allergen management has two main protection goals: minimizing the risk of allergy episodes in sensitive people (food safety objective) and maximizing the possibilities of choice for healthy foods by allergic consumers (food security objective). In this regard, stakeholders agree that PAL should be used based on the actual risk of allergic reaction, with transparent and consistent decision-making criteria, when there is an unacceptable risk of significant but unavoidable allergen cross-contamination, without unduly restricting food choices to allergic consumers [ 2 , 14 •]. Contrarily, current use of PAL has shown limited effectivity to protect people with food allergies. Therefore, different studies recommend a risk-based approach to decide its inclusion, which should be based on the amount of allergen likely to cause a reaction as well as in the potential severity of reactions [ 15 ]. In this regard, it was reported that reactions to small amounts of allergens are usually mild, while the most severe allergic reactions are usually caused by significant quantities of allergens, added intentionally as an ingredient to the food [ 16 , 17 ].

PAL was developed by the food industry as an ultimate tool to mitigate the risk of unavoidable UAP due to the complexity of food manufacturing (different ingredients and raw materials, shared equipment, cleaning protocols that could be not entirely effective to remove all traces of allergens) [ 18 ]. Ideally, the inclusion of PAL should be decided according to the so-called action levels, objectively determined (a topic that will be later discussed in more detail). Thus, a concentration of the potential UAP higher than the action level would trigger the use of PAL, while no PAL would be necessary for concentrations equal to or lower than this cut-off [ 16 ].

According to this conception, the conduction of a formal allergen risk assessment can be considered as an improvement in the use of PAL, since it will provide the basis for a more informative labelling scheme, ultimately contributing to a transparent allergen management and communication [ 19 ]. One of the first and most widely used schemes using this approach has been the VITAL program (Voluntary Incidental Trace Allergen Labelling), established by the Allergen Bureau of Australia and New Zealand [ 20 ].

In summary, the rational use of PAL is important to ensure that it be used in a transparent, clear, and concise way, avoiding unnecessary risk or confusion to consumers. Therefore, FBO should only use PAL when there is a genuine risk of cross-contamination and, in turn, allergic consumers should be aware of the limitations of PAL and not rely on it as the only way to avoid food allergies, for which they should be educated about the real meaning of precautionary labelling [ 11 ].

The Way for Threshold Values of Food Allergens

Allergen threshold is defined as the minimum amount of an allergenic food that can trigger an allergic reaction. One of the problems associated to allergen threshold is that this expression may have different significance and connotation for the different stakeholders such as allergic individuals, health professionals, the food industry, and regulatory authorities. For allergic individuals and health professionals, threshold data can help them manage allergies by identifying safe food choices and preventing allergic reactions [ 21 ], since they provide information on how much allergen can be tolerated by (most of) allergic individuals before they experience a reaction. In turn, the food industry and regulatory authorities can use thresholds to assess the public health risk of food allergies and design appropriate food safety measures [ 22 ].

A term closely related to allergen threshold and useful for public health purposes, i.e. eliciting dose (ED), can be used to set safety limits for foods potentially containing allergens [ 23 ]. With this purpose, standardized clinical challenges from a large number of allergic patients can help estimate population thresholds through statistical modelling of the dose-distribution of individual responses to the target allergen. From these models, ED or population threshold can be therefore defined as the amount of the allergenic food which will cause an objective reaction in a specified proportion of an allergic population (EDp). Thus, the ED05 is the dose predicted to elicit an allergic reaction in the 5% most sensitive individuals. For example, if the ED05 for peanuts is 1 mg, then a portion of food (to be consumed in one eating occasion) containing 1 mg of peanuts would be safe for 95% of people with peanut allergies. Although the ED acknowledges that it is impossible to guarantee absolute safety, a value that protects a certain percentage (ideally the vast majority) of allergic people could be agreed [ 10 ••, 23 ].

Several bibliographic references addressed the topic of threshold values. The following list includes the most significant and representative publications in the way to a global consensus:

Alternative criteria to establish threshold values for food allergens [ 24 ]

Establishment of reference doses for different allergenic foods based on oral provocation studies and probabilistic models [ 25 ]

Establishment of population minimal eliciting dose-distributions of priority allergens based on clinical data with a more extensive database [ 26 ]

Full range of population eliciting doses for priority allergenic foods also based on the previous database [ 7 •]

International scientific consensus on reference values, action levels, and current analytical capabilities in relation to the recommended thresholds for priority allergens [ 10 ••]

Some of these thresholds have been already used with success in Australia and New Zealand, to develop reference dose limits for the voluntary, risk-based VITAL program for food manufacturers [ 20 ].

The Concepts of Reference Dose and Action Level

Four main components should be addressed for the establishment of allergen thresholds in food: (a) the estimation of reference doses from the modelling of dose–response curves of individual allergens, obtained from a sufficient numbers of allergic individuals subjected to provocation tests; (b) the agreement of the required level of (minimum) eliciting dose obtained from these models (ED01, ED05, etc.); (c) sound consumption databases for different types of food; and (d) commercially available analytical methods to quantify allergens at the required levels [ 10 ••].

Based on EDp values, risk managers can set reference doses (RfD) at any risk level considered to be acceptable [ 8 ]. Remington et al . [ 26 ] reported ED01 and ED05 values (considered the candidate values for the establishment of thresholds) for fourteen different allergenic foods. Based on these values, the VITAL program chose the ED01 (protection levels of 99%) as the basis for the RfD for taking risk management decisions within the VITAL 3.0 framework [ 27 ]. Other regulatory agencies such as the Belgium Federal Safety Agency adopted the lower limit of the 95% confidence interval of ED05 [ 28 ], while the Dutch Office BuRO established the ED01 value [ 29 ]. Recently, FAO/WHO [ 10 ••] agreed a tolerable safety objective associated to a threshold value as that capable (literally) “to minimise, to a point where further refinement does not meaningfully reduce health impact, the probability of any clinically relevant objective allergic response as defined by dose-distribution modelling of minimum eliciting doses (MED) …”. The committee responsible for this publication agreed that ED05 values will meet this objective. Full range of allergic population dose-distributions such as those presented by Houben et al . [ 7 •] can be further used for characterizing the risk and number of predicted reactions for different scenarios or specific situations [ 8 ].

Table 1 presents the most important threshold values (RfDs), either expressed as absolute amounts (mg) of concentrations (ppm), presented by different regulatory agencies and/or organizations such as FAO/WHO and VITAL. It becomes evident that there is a wide range of values and different ways of expression (mg or ppm) for each individual allergen among the different agencies, organizations such as FAO/WHO, and programs like VITAL. However, it has been recognized, after the publication of FAO/WHO reports, the validity of methodologies such as the dose-distribution analysis to determine the reference values, and the consumption database to calculate action levels. It is also acknowledged that data sources reported in the studies from Remington et al . [ 26 ] and Houben et al . [ 7 •] constitute the best described and most comprehensive bibliographic sources available up to the present, in terms of content and curation and validation by highly regarded peer-reviewed publications. The main difference is due to what can be considered by the regulatory agencies and organization as a tolerable risk to protect consumers, according to the concept of Madsen et al . [ 15 ], and the difficulty to find a right compromise between the food safety and food security protection goals, as previously described.

To apply RfD in practical terms and determine the limits for different types of foods, these values should be converted into concentrations (ideally expressed as mg of total protein of the allergenic food per kg food product) by simply dividing them by the estimated serving size of food eaten in a single occasion. This would provide the target concentration limit to decide a PAL inclusion and the required limits of quantification of analytical methods to monitor compliance of food products [ 10 ••, 11 ]. These target values, termed action levels, can be defined as the maximum concentration of each specific allergen that can be present in a food product without causing a severe reaction in most people with allergies to that allergen. The allergen concentration unintentionally remaining in a product, even with the best allergen management practices, can be estimated by different methodologies. These estimated concentrations can then be compared to allergen threshold values [ 2 ]. Different information sources and calculus related to these values have been recently proposed by the International Life Science Institute (ILSI) [ 14 •].

To provide reference serving amounts, Birot et al . [ 29 ] combined data from consumption surveys accomplished in different European countries (France, Denmark, and Netherlands) into a common database, which resulted in 61 food groups. They calculated for each food group the mean consumption value, as well as the 75th percentile (P75) and the 90th percentile (P95), which are useful for allergen risk assessment. The 50th percentile is considered as the optimal consumption amount to be used confidently for probabilistic risk assessments with an acceptable risk level [ 30 , 31 ]. Intake data from the general population can also be used for food allergen risk assessment since, as evidenced, no statistically significant difference of consumption exists between the allergic and the general populations [ 32 ].

Quantitative Management of Food Allergens

As previously explained, the use or absence of PAL currently shows a limited correlation with the real level of UAP and the consequent risk of an allergic reaction. This concomitant risk after the consumption of a product that unintendedly contains an allergen can be estimated by quantitative risk assessment (QRA) [ 33 ]. This tool complements allergen management practices by quantitatively estimating the risk that face an allergic consumer due to an UAP in a food. It can thereby provide information as input into the risk management decision-making process, such as whether a PAL inclusion is necessary [ 14 •].

QRA can be based on fixed numerical data (deterministic), probabilities (probabilistic), or a combination of both. In food manufacturing, deterministic assessments are often used because they are simple and provide enough information to make risk management decisions [ 34 ].

In practical terms, once established the different parameters previously mentioned (reference doses, real serving sizes, action levels), the next step is to review, in a comprehensive assessment, the potential for allergens to be present in a food product, which will constitute a relevant input to make decisions about allergen labelling. The review process should identify the presence of allergens either by direct incorporation or by (unintended) cross-contact, and should include the entire manufacturing process, from raw materials to the finished product, identifying and quantifying any accumulated residues within the manufacturing line. The output will be the establishment of the allergen status of all materials, including the estimation of the amount of unintentionally added allergens [ 14 •, 35 ]. Based on this information, the likelihood and severity of reactions in allergic people who consume food containing allergens can be systematically evaluated.

It is expected that QRA be increasingly adopted by FBO because of its utility to develop more effective control measures, or eventually decide in a coherent and transparent manner the inclusion of PAL, both conducting to reduce the risk of allergic reactions without unnecessary and unrealistic warnings. Among the advantages for FBO to adopt a decision-making process based on QRA, it can be mentioned a reduced liability in the event of an allergic reaction, the enhancement of the brand reputation, an increased efficiency by identifying and eliminating inefficient practices, which can lead to cost savings, an improved compliance with government regulations on food allergens, and a more efficient and transparent communication with stakeholders.

In summary, a quantitative risk-based approach to allergen management considers the likelihood and severity of an allergic reaction when determining whether to use precautionary labelling, leading to a wider range of food choices for allergic consumers and a lower risk of nutritional deficiencies. By taking this approach, the vast majority of allergic consumers will be able to tolerate foods that do not carry precautionary labelling [ 2 ].

Analytical Requirement for the Quantitative Management of Food Allergens

The establishment of thresholds for food allergens requires the availability of sound analytical methods, which constitute a critical component to support compliance with the established values, as potentially required by certification systems, internal standards, and/or regulations. Allergen analysis can assist in different activities such as verifying allergen profile and potential UAP in raw materials, assessing cleaning efficacy and validations, confirming assumptions of the risk assessment process, and monitoring the effect of critical changes [ 20 ].

Three techniques (polymerase chain reaction — PCR, ELISA, and mass spectrometry —MS) are currently considered as being the best options for compliance and enforcement related to allergen management [ 36 ]. Because the availability of reference material for the analysis of allergens is still scarce, one important problem is that different analytical methods for food allergen can lead to inconsistent quantification results, which can hinder accurate quantitative risk assessment and its regulatory implementation. Therefore, there is still a clear need to improve, standardize, and harmonize allergen analysis [ 37 , 38 ]. Cubero-Leon et al . [ 39 ] proposed a concept called reference measurement system for food allergens. This system consists of three components: a primary reference measurement method, a certified reference material, and a reference laboratory. Recently, a European project addressed the development of a MS method able to analyse six priority allergens (milk, egg, peanut, hazelnut, almond, and soybean), validated by immunoassay and DNA-based methods. This method has the required sensitivity to quantify these allergens with the performance established by the recent FAO/WHO expert consultation [ 40 ].

A recent study investigated if current methods have the required analytical performance to assess the recommended doses established by VITAL 2.0 and 3.0 for different serving sizes (between 5 and 500 g). Data on published and commercial ELISA, PCR, and MS methods were reviewed for the analysis of peanuts, soy, hazelnut, wheat, milk, and egg. It was found that available methods can successfully detect peanut, soy, hazelnut, and wheat allergens at or below the doses of both versions of the VITAL program, even in large serving sizes. However, some difficulties can be found for milk and egg due to matrix/processing incompatibility. In coincidence with the above mentioned, this study also remarks the need for harmonized reporting units, available reference materials, and ring-trials to enable validation and the provision of comparable measurement results [ 38 ].

The report on the establishment of threshold levels published by FAO/WHO [ 10 ••] recommends assessing the method performance requirement on the limits of quantification (LoQ), which should be around threefold lower than the action level for each food. This would account for the practical variability, assuring that the analytical values obtained are at or below the action levels. This report provides a table showing the required LoQ recommended to meet the action levels, as calculated for the different allergens, and serving sizes of foods. It is important to mention that the study from Holzhauser et al . (39) considers limits of detection (LoD), which are lower than LoQ, but the assessment was made for ED01 reference doses of allergens.

The Relevance of Allergen Cleaning

Allergen QRA can provide critical allergen protein concentrations above which a risk can be verified. To attain such low or negligible amount of UAP, cleaning represents a key allergen control measure in food facilities. Allergen cleaning is the process of removing food allergens from surfaces, equipment, and other areas where they may have come into contact with food. However, it is usually difficult to link the results of allergen tests on non-food materials (such as surface swabs and rinse water) to the amount of allergen in finished products, since it is unclear how much of the allergen would be transferred. Current allergen tests for non-food materials are mostly used to validate and verify control measures. If allergens are detected, control measures need to be reviewed and improved [ 34 ].

In some situations, potential carry-over could be estimated through knowledge of the line(s) and equipment, together with easy measurements, such as the mass of preceding product that may be left within the equipment. Carry-over QRA can then be combined with analytical data to provide additional assurance [ 14 •].

Appropriate analysis to assess cleaning efficacy plays an essential role for the effective risk management and harmonization of mitigation measures such as PAL. Four crucial issues to be addressed have been identified: (a) sampling method, (b) analysis accomplishment, (c) analysis performance, and (d) interpretation of the results [ 41 ]. Protocols designed to remove food allergens should include the following steps: identifying the allergens that need to be removed, selecting the appropriate cleaning methods and materials, cleaning surfaces and equipment thoroughly, and verifying that the cleaning has been effective.

The Development of “Free-From Allergens” Products

Free-from-allergen foods are a special type of products initially devoted to a small number of highly sensitive and reactive allergic people. They would not provoke even mild reactions in the vast majority of highly sensitive allergic consumers, based on the guarantee of analytical absence of allergenic proteins and a robustly designed food safety system (GMP, HACCP, etc.) [ 2 ].

Free-from allergens is considered a claim, although its definition and requirements are not covered in most of the legislations of EU and countries such as the UK and Argentina, except for “gluten-free” products [ 42 ]. Because of its absolute connotation, a product should be labelled as “free-from” only after a stringent assessment of the ingredients, environment, and the assurance that processes and controls have been followed. According to the British Retail Consortium (BRC) [ 42 ], a “free-from” claim should observe the following principles: (a) no ingredient with the specified allergen should be included in the product recipe; (b) the production environment should observe strict manufacturing practices and the most stringent allergen management practices; (c) a robust analytical program with specified sampling and testing methods should be established and followed; and (d) a clear labelling and other communication tools should be considered, all of them complying with legal requirements. In some countries, these requirements are supported by independent (third-party) certification bodies. These products are particularly scrutinized and frequently monitored by regulatory authorities, and sometimes inconsistencies are found. For instance, products labelled as “milk- and gluten-free” has been detected to positively contain milk and gluten [ 43 ], and in 15% of chocolates with dairy-free statement and in 25% of vegan chocolates the presence of milk was detected [ 5 ].

In addition to more stringent management practices (for instance, some certification systems require that no ingredient with the target allergen be present in the powder form within the entire facility), the analytical absence of the allergen should be verified by any of the most sensitive commercial methods available. Actually, a very frequent use of analytical test kits by the food industry is in the context of certification or to support “free-from” labelling [ 44 ].

The market for free-from allergen foods has experimented a significant growth in the last years, especially in North America and Western Europe, mainly because of the increasing number of people with food allergies or intolerances. However, even non-allergic consumers wrongly perceive eating these products as a way to improve their overall health and digestion [ 45 ]. This suggests that the market for free-from foods will continue to grow and expand in the future, for which it will be increasingly important to have in place robust analytical programs, and a consistent quantitative management system for food allergens. In this case, a zero-risk approach would be particularly relevant, differently from regular foods, where a tolerable-risk approach would be more adequate.

Conclusions

This review shows that quantitative allergen management will be increasingly important for different stakeholders such as the food industry and regulatory agencies. In this regard, internationally agreed allergen thresholds such as those proposed by FAO/WHO will be of utmost importance to ensure that food products are safe for allergic consumers. One of the most relevant uses of thresholds is in the process to assess the need to include PAL. Within this framework, the availability of sound analytical methods represents a key element. An increased adoption of QRA is therefore expected because of its efficacy to identify and address potential allergen risks, especially the existence and impact of cross-contamination and the consequent labelling decision. However, it should be emphasized that QRA does not substitute the compliance with good manufacturing practices (GMPs) and prerequisite programs (PRPs).

Data Availability

Not applicable.

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

Baseggio Conrado A, Ierodiakonou D, Gowland MH, Boyle RJ, Turner PJ. Food anaphylaxis in the United Kingdom: analysis of national data, 1998-2018. BMJ (former British Medical Journal). 2021;372(251):1–10. https://doi.org/10.1136/bmj.n251 .

Article   Google Scholar  

Ward R, Crevel R, Bell I, Khandke N, Ramsay C, Paine S. A vision for allergen management best practice in the food industry. Trends Food Sci Technol. 2010;21(12):619–25. https://doi.org/10.1016/j.tifs.2010.09.004 .

Article   CAS   Google Scholar  

Sharma GM, Ma Y, Luccioli S. Recalls associated with food allergens and gluten in FDA-regulated foods from fiscal years 2013 to 2019. J Food Prot. 2023;86(4):100069. https://doi.org/10.1016/j.jfp.2023.100069 .

Article   PubMed   Google Scholar  

Soon JM, Brazier AKM, Wallace CA. Determining common contributory factors in food safety incidents – a review of global outbreaks and recalls 2008–2018. Trends Food Sci Technol. 2020;97:76–87. https://doi.org/10.1016/j.tifs.2019.12.030 .

Bedford B, Yu Y, Wang X, Garber EAE, Jackson LS. A limited survey of dark chocolate bars obtained in the United States for undeclared milk and peanut allergens. J Food Prot. 2017;80(4):692–702. https://doi.org/10.4315/0362-028x.jfp-16-443 .

Article   CAS   PubMed   Google Scholar  

Taylor SL, Hefle SL, Bindslev-jensen C, Atkins FM, Andre C, Bruijnzeel-koomen C, et al. A consensus protocol for the determination of the threshold doses for allergenic foods: how much is too much? Clin Exp Allergy. 2004;34(5):689–95. https://doi.org/10.1111/j.1365-2222.2004.1886.x .

Houben GF, Baumert JL, Blom WM, Kruizinga AG, Meima MY, Remington BC, et al. Full range of population eliciting dose values for 14 priority allergenic foods and recommendations for use in risk characterization. Food Chem Toxicol. 2020;146:111831–111831. https://doi.org/10.1016/j.fct.2020.111831 .  This paper provides the full range of ED values for the 14 most relevant  allergenic foods, predicted to elicit objective allergic symptoms in different  percentages of the allergic population, as well as recommendations for their  use, specifically in the context of characterizing risks of unintended allergenic  proteins in food products. Values were based on the largest threshold  database worldwide.

Remington BC, Baumert J, Blom WM, Bucchini L, Buck N, Crevel R, et al. Allergen quantitative risk assessment within food operations: concepts towards development of practical guidance based on an ILSI Europe workshop. Food Control. 2022;138(108917):108917. https://doi.org/10.1016/j.foodcont.2022.108917 .

Food Agricultural Organization and World Health Organization. Risk assessment of food allergens. In: Part 1 – review and validation of Codex Alimentarius priority allergen list through risk assessment. Meeting report. Food safety and quality series No. 14. Rome; 2022. https://doi.org/10.4060/cb9070en . Accessed 10 Oct 2023.

Food Agricultural Organization and World Health Organization. Risk assessment of food allergens. In: Part 2 - Review and establish threshold levels in foods for the priority allergens. Meeting Report. Food Safety and Quality Series No. 15. Rome; 2022. https://doi.org/10.4060/cc2946en . Accessed 3 Oct 2023. This report provides reference doses (RfD, expressed as milligrams of total protein from the allergenic source) for the most relevant food allergens, as defined by an Ad hoc Joint FAO/WHO Expert Consultation on Risk Assessment of Food Allergens convened by FAO/WHO, which constitutes a critical requirement to assessing the risk from allergens. RfDs were based on dose-distribution modelling according to the ED05 values, and those foods with close ED05 values grouped together and a single value.

Food Agricultural Organization and World Health Organization. Risk assessment of food allergens. In: Part 3 – Review and establish precautionary labelling in foods of the priority allergens. Meeting report. Food safety and quality series No. 15. Rome; 2023. https://doi.org/10.4060/cc6081en . Accessed 10 Oct 2023.

Livsmedelsverket. Sjögren Bolin Y, Warensjö Lemming E. Undeclared allergens in food – Guide on how to assess the risk of allergic reactions in the population. Livsmedelsverkets rapportserie. Uppsala. L 2022 nr 13. https://www.livsmedelsverket.se/globalassets/publikationsdatabas/rapporter/2022/l-2022-nr-13-undeclared-allergens-in-food-risk-assessment-guide.pdf . Accessed 10 Oct 2023.

Committee on Toxicity Codex Subgroup. Food Standards Agency. Assessment of the Codex report on food allergen thresholds; 2023. 12 pp. https://doi.org/10.46756/sci.fsa.rif459 . Accessed 10 Oct 2023.

Remington BC, Baumert J, Blom MW, Bucchini L, Buck N, Crevel R, De Mooij, F, Flanagan, S, Stavropoulou, DA, van den Dungen, M, van Ravenhorst, M, Wang, S, Walker, M. Practical guidance on the application of food allergen quantitative risk assessment. International Life Sciences Institute (ILSI) Belgium; 2022. https://doi.org/10.5281/zenodo.6651934 . Accessed 10 Oct 2023. This is a very detailed guidance which provides tools and approaches to harmonize the data gathering process for food allergen risk assessments and their implementation, promoting consistency in documentation, decision-making, and application of allergen quantitative risk

Madsen CB, van den Dungen MW, Cochrane S, Houben GF, Knibb RC, Knulst AC, et al. Can we define a level of protection for allergic consumers that everyone can accept? Regul Toxicol Pharmacol. 2020;117(104751):104751. https://doi.org/10.1016/j.yrtph.2020.104751 .

Turner PJ, Patel N, Ballmer-Weber BK, Baumert JL, Blom WM, Brooke-Taylor S, et al. Peanut can be used as a reference allergen for hazard characterization in food allergen risk management: a rapid evidence assessment and meta-analysis. J Allergy Clin Immunol Pract. 2022;10(1):59–70. https://doi.org/10.1016/j.jaip.2021.08.008 .

Article   PubMed   PubMed Central   Google Scholar  

Turner PJ, Baumert JL, Beyer K, Brooke-Taylor S, Comberiati P, Crevel RWR, et al. ‘Too high, too low’: the complexities of using thresholds in isolation to inform precautionary allergen (‘may contain’) labels. Allergy. 2022;77(6):1661–6. https://doi.org/10.1111/all.15202 .

DunnGalvin A, Chan C-H, Crevel R, Grimshaw K, Poms R, Schnadt S, et al. Precautionary allergen labelling: perspectives from key stakeholder groups. Allergy. 2015;70(9):1039–51. https://doi.org/10.1111/all.12614 .

DunnGalvin A, Roberts G, Schnadt S, Astley S, Austin M, Blom WM, et al. Evidence-based approaches to the application of precautionary allergen labelling: report from two iFAAM workshops. Clin Exp Allergy. 2019;49(9):1191–200. https://doi.org/10.1111/cea.13464 .

Brooke-Taylor S, Christensen G, Grinter K, Sherlock R, Warren L. The Allergen Bureau VITAL program. J AOAC Int. 2018;101(1):77–82. https://doi.org/10.5740/jaoacint.17-0392 .

Crevel RWR, Ballmer-Weber BK, Holzhauser T, Hourihane JO, Knulst AC, Mackie AR, et al. Thresholds for food allergens and their value to different stakeholders. Allergy. 2008;63(5):597–609. https://doi.org/10.1111/j.1398-9995.2008.01636.x .

Saab IN, Jones W. Trends in food allergy research, regulations and patient care. Nutr Today. 2022;57(2):64–9. https://doi.org/10.1097/nt.0000000000000530 .

Crevel RWR, Briggs D, Hefle SL, Knulst AC, Taylor SL. Hazard characterisation in food allergen risk assessment: the application of statistical approaches and the use of clinical data. Food Chem Toxicol. 2007;45(5):691–701. https://doi.org/10.1016/j.fct.2006.09.005 .

Buchanan R, Dennis S, Gendel S, Acheson D, Assimon SA, Beru N, et al. Approaches to establish thresholds for major food allergens and for gluten in food. J Food Prot. 2008;71(5):1043–88. https://doi.org/10.4315/0362-028x-71.5.1043 .

Taylor SL, Baumert JL, Kruizinga AG, Remington BC, Crevel RWR, Brooke-Taylor S, et al. Establishment of reference doses for residues of allergenic foods: report of the VITAL Expert Panel. Food Chem Toxicol. 2014;63:9–17. https://doi.org/10.1016/j.fct.2013.10.032 .

Remington BC, Westerhout J, Meima MY, Blom WM, Kruizinga AG, Wheeler MW, et al. Updated population minimal eliciting dose distributions for use in risk assessment of 14 priority food allergens. Food Chem Toxicol. 2020;139(111259):111259. https://doi.org/10.1016/j.fct.2020.111259 .

Article   CAS   PubMed   PubMed Central   Google Scholar  

Allergen Bureau. The Food Industry Guide to the Voluntary Incidental Trace Allergen Labelling (VITAL®) Program. Version 3.0. Allergen Bureau. Australia New Zealand. 18 pp. https://allergenbureau.net/wp-content/uploads/2021/04/Food_Industry_Guide_VITAL_Program_Version_April_2021_VF1.pdf . Accessed 10 Oct 2023.

Federaal Agentschap voor de Veiligheid van de Voedselketen - SciCom. (Federal Agency for the Safety of the Food Chain – Belgium). Referentiedosissen voor de allergenen die zijn opgenomen in bijlage II van de Verordening. (EU) nr. 1169/2011 van 25 oktober 2011. ADVIES 24–2017 Betreft. 37 pp. 2017. https://www.favv-afsca.be/wetenschappelijkcomite/adviezen/2022/_documents/Advies08-2022_SciCom2021-22_Referentiedosisallergenen.pdf . Accessed 10 Oct 2023.

Birot S, Madsen CB, Kruizinga AG, Crépet A, Christensen T, Brockhoff PB. Food groups for allergen risk assessment: combining food consumption data from different countries in Europe. Food Chem Toxicol. 2018;118:371–81. https://doi.org/10.1016/j.fct.2018.05.042 .

Blom WM, Remington BC, Baumert JL, Bucchini L, Crépet A, Crevel RWR, et al. Sensitivity analysis to derive a food consumption point estimate for deterministic food allergy risk assessment. Food Chem Toxicol. 2019;125:413–21. https://doi.org/10.1016/j.fct.2019.01.025 .

Blom WM, Westerhout J, Houben GF. The 50th percentile of the general population single eating occasion intake of food is optimal for the calculation of action levels for precautionary allergen labelling. Food Chem Toxicol. 2023;179(113953):113953. https://doi.org/10.1016/j.fct.2023.113953 .

Blom WM, van Os-Medendorp H, Bijlsma S, van Dijk A, Kruizinga AG, Rubingh C, et al. Allergen risk assessment: food intake levels of the general population represent those of food allergic patients. Food Chem Toxicol. 2020;146(111781):111781. https://doi.org/10.1016/j.fct.2020.111781 .

Remington BC, Baumert JL, Blom MW, Houben GF, Taylor SL, Kruizinga AG. Quantitative risk assessment of UK food products cross‐contaminated with allergens. Clin Transl Allergy. 2015;5(S3) https://doi.org/10.1186/2045-7022-5-s3-o10

Food Allergy Canada, Food Risk Analysis and Regulatory Excellence Platform (PARERA – Universite Laval). Allergen management guidelines for food manufacturers. 2022. https://parera.ulaval.ca/fileadmin/Fichiers/Formation_FAC/FAC_ManufacturersGuide_EN.pdf . Accessed 10 Oct 2023.

Allergen Bureau & Australian Food and Grocery Council. Food industry guide to allergen management and labelling for Australia and New Zealand. 55 pp. 2023. https://www.afgc.org.au/download/2023-food-industry-guide-to-allergen-management-and-labelling-for-australia-and-new-zealand . Accessed 10 Oct 2023.

Diaz-Amigo C, Popping B. Analytical testing as a tool for the enforcement of future regulatory thresholds for food allergens. J AOAC Int. 2010;93(2):434–41. https://doi.org/10.1093/jaoac/93.2.434 .

Cordeiro F, Cubero-Leon E, Nørgaard J, Martinez-Esteso MJ, Brohée M, Breidbach A, et al. Total cow’s milk protein in cookies: the first interlaboratory comparison with a well-defined measurand fit for food allergen risk assessment. Accred Qual Assur. 2021;26(3):177–81. https://doi.org/10.1007/s00769-021-01470-y .

Holzhauser T, Johnson P, Hindley JP, O’Connor G, Chan C-H, Costa J, et al. Are current analytical methods suitable to verify VITAL® 2.0/3.0 allergen reference doses for EU allergens in foods? Food Chem Toxicol. 2020;145(111709):111709. https://doi.org/10.1016/j.fct.2020.111709 .

Cubero-Leon E, Emons H, O’Connor G, Nørgaard J, Robouch P. Food allergen analysis: considerations for establishing a reference measurement system to implement EU legislation. Food Chem. 2023;424(136391):136391. https://doi.org/10.1016/j.foodchem.2023.136391 .

Mills ENC, Adel-Patient K, Bernard H, De Loose M, Gillard N, Huet A-C, et al. Detection and quantification of allergens in foods and minimum eliciting doses in food-allergic individuals (ThRAll). J AOAC Int. 2019;102(5):1346–53. https://doi.org/10.1093/jaoac/102.5.1346 .

Littleton P, Walker M, Ward R. Controlling cross-contamination by food allergens. Food Sci Technol. 2021;35(2):47–51. https://doi.org/10.1002/fsat.3502_14.x .

BRC (British Retail Consortium). Guidance on “free-from” allergen claims . 2015. https://www.fdf.org.uk/globalassets/resources/publications/brc-free-from-guidance.pdf

Martínez-Pineda M, Yagüe-Ruiz C. The risk of undeclared allergens on food labels for pediatric patients in the European Union. Nutrients. 2022;14(8):1571. https://doi.org/10.3390/nu14081571 .

Dupuis, C, Tchounkeu, F. Certification programs for foods labeled as “ free-from” specific allergens. In: Allergen management in the food industry. John Wiley & Sons, Inc.; 2010. p. 473–94.

Hattersley S, Ward R. Regulatory controls for food allergens. In: Madsen CB, Crevel R, Mills C, Taylor S, editors. Risk management for food allergy. Academic Press; 2014. p. 273–89. https://doi.org/10.1016/B978-0-12-381988-8.00017-8 .

Chapter   Google Scholar  

Office for Risk Assessment & Research (BuRO). Netherlands Food and Product Safety Authority (NVWA). In: Advice of BuRO on preliminary doses for food allergens. 17 pp. 2016. NVWA/BuRO/2016/150. https://english.nvwa.nl/about-us/documents/consumers/food/safety/documents/advice-of-buro-on-preliminary-reference-doses-for-food-allergens . Accessed 10 Oct 2023.

Akiyama H, Adachi R. Japanese food allergy-labeling system and comparison with the international experience; detection and thresholds. Food Safety. 2021;9(4):101–16. https://doi.org/10.14252/foodsafetyfscj.d-21-00008 .

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The present study received the support from Instituto Nacional de Tecnología Agropecuaria, INTA (INTA 1.6.2.7.PT.I161 – Plataforma Alergenos en Alimentos, and 2023-PE-L04-I088).

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Food regulatory bodies play an important role in public health, and in reducing the costs of food borne illness that are absorbed by both industry and government. Regulation in the food industry involves a relationship between regulators and members of the industry, and it is imperative that these relationships are built on trust. Research has shown in a variety of contexts that businesses find the most success when there are high levels of trust between them and their key stakeholders. An evidence-based understanding of the barriers to communication and trust is imperative if we are to put forward recommendations for facilitating the (re)building of trusting and communicative relationships.

We present data from 72 interviews with regulators and industry representatives regarding their trust in and communication with one another. Interviews were conducted in the UK, New Zealand, and Australia in 2013.

Data identify a variety of factors that shape the dynamic and complex relationships between regulators and industry, as well as barriers to communication and trust between the two parties. Novel in our approach is our emphasis on identifying solutions to these barriers from the voices of industry and regulators.

Conclusions

We provide recommendations (e.g., development of industry advisory boards) to facilitate the (re)building of trusting and communicative relationships between the two parties.

Peer Review reports

Food regulatory bodies play an important role in the field of public health, and contribute significantly to the health of populations in a variety of ways [ 1 ]. In particular, their role involves both developing food safety standards, and/or enforcing these standards to monitor food safety risks. There are two main types of food risks for consumers. The first relates to hygiene and is specific to foods being unsafe for consumers to consume. The second relates to food standards which includes nutrition labelling (e.g., consumers are misled over fat content), safety labelling (e.g., use by dates are incorrect), and composition labelling (e.g., labelling misleads the consumer because contents do not meet compositional standards) [ 2 ]. As such, food safety risks refer to those that directly affect human health, but also risks regarded as “food fraud incidents”, relating to deception or malintent [ 3 ]. As a result, the role of food regulators is broad and can range from enforcing food standards in restaurants to organising large scale food recalls. Regardless of role, food regulation is essential for ensuring public safety as well as developing and maintaining public trust in food [ 4 ].

Enforcement involves engagement with members of the food industry who are required to comply with such standards, with penalties occurring if noncompliance is identified. Food safety incidents, for example Garibaldi (Australia), bovine spongiform encephalopathy (BSE) (UK) and toxic levels of iodine (New Zealand) [ 5 – 7 ] have brought to light the importance of regulation of the food industry [ 8 , 9 ]. The costs associated with foodborne illness are important for both regulators and industry. Using Australia as an example, an estimated 4.1 million domestically acquired cases of foodborne gastroenteritis occur annually, costing an estimated $1.2 billion AUD per year [ 10 ]. These costs are absorbed by a variety of actors with a stake in food safety, including businesses (food safety recall costs total $14 million AUD) and the Australian government ($10 million AUD) [ 11 ]. As such, both regulators and members of industry have a stake in maintaining food safety standards and avoiding food scares.

Regulation in the food industry involves a relationship between regulators and members of the industry, and it is imperative that these relationships are built on trust. At its core, trust is described by social theorists as existing in three parts: A trusts B to do X [ 12 , 13 ]. In this context, A and B are the regulators and members of industry, and “doing X” (either A for B, or B for A) can be described as acting in each other’s best interests. No matter the industry, trust has been shown to play a very important role in regulation-industry relationships, enhancing cooperation and leading to better outcomes for both parties [ 14 ]. Research has shown in a variety of contexts that businesses find the most success when there are high levels of trust between them and their key stakeholders [ 15 ]. Indeed, it is in the best interest that the two parties cooperate. Industry’s trust in regulation, and subsequent compliance with food safety standards may minimize food safety incidents that have the potential to reduce consumer trust, reducing their profits. For regulators, having a trusting relationship with industry may lead to greater transparency in times of food scares or when industry are finding it challenging to meet food safety standards.

Trust is a complex multidimensional concept consisting of both a rational component (arising from experience) and an irrational component based on instinct and emotion [ 16 , 17 ]. Importantly, trust can be understood to occur at two distinct levels – institutional [ 18 ] and interpersonal [ 19 ]. Institutional trust is that which is placed in one or more social systems or institutions (e.g., Food Standards Australia New Zealand). Interpersonal trust is negotiated between individuals; for example, between a consumer and a grocer. Both forms of trust are important for understanding where and how trust can be (re)developed and maintained in the context of food safety regulation and compliance. Both the reputation and knowledge of the institution (e.g., Food Standards Agency or McDonalds), as well as the personal relationships with those who represent it (Food Safety Manager or Restaurant Owner), are vital to the pursuit of trust between members of industry and regulators.

The relationship between regulators and industry can be complicated by a variety of factors, including the varying sizes of businesses involved, as they can range from multinational corporations to small, family-owned businesses [ 20 ]. Therefore, it is important to recognise both the perceived and real barriers that the food industry face when aiming to comply with food safety standards, and the level of understanding of these challenges from the perspective of regulators. An evidence-based understanding of the barriers to communication and trust is imperative if we are to put forward recommendations for facilitating the (re)building of trusting and communicative relationships with the aim of increasing compliance in the interest of public health.

This paper presents the views of regulators and members of industry regarding their trust in and communication with one another within three countries (UK, New Zealand, and Australia), which necessities a brief overview of the policy and institutional context within each locale. Food Standards Australia New Zealand (FSANZ) is a bi-national body that is responsible for the Australia New Zealand Food Standards Code which forms the basis of much of the food law in each country. FSANZ is an independent science-based organization that is managed by a Board whose members are experts in various aspects of food (e.g., toxicology, nutrition, microbiology, food technology, food industry etc.). FSANZ is not responsible for the enforcement of the Code, nor is it responsible for the policy that informs the direction of the Code – this is undertaken by the states and territories of Australia, and the Government of New Zealand. In the case of policy this is generally the departments of health and/or agriculture, while enforcement may be undertaken by local authorities. In the UK, the Food Standards Agency is generally responsible for the development of food safety policy and controls, while enforcement of these are devolved to local authorities. In England the nutrition components of food regulation are administered through the Department of Health.

For the purposes of this paper, the use of the term regulator is inclusive of both individuals responsible for developing food safety standards and for enforcing food safety standards. The term industry is inclusive of a variety of individuals and organisation types (e.g., grocers, small business owners, and large corporations). Our analysis of these perspectives has allowed us to identify barriers and facilitators to communication and trust, and potential areas of conflict that are problematic from a public health perspective that may be amenable to change. A variety of data-driven solutions are provided for (re)building trusting and communicative relationships between the two parties, with the end goal of protecting the public.

The data presented in this in this paper comes from a larger study examining trust in the food system from the perspectives of food regulators, the food industry and the media, conducted across three countries – UK, New Zealand (NZ) and Australia (AU). A protocol paper outlining this wider study has been published elsewhere [ 20 ].

Recruitment

Individuals working in the food regulation and food industry were recruited for this research. Recruitment was through purposive sampling, which enabled participation of individuals who were information rich [ 21 ] and had relevant experiences to share [ 22 ]. An initial list of people to contact was developed by the research team, based on their own contacts and knowledge of food industry and regulatory settings. Considering the varied roles of representatives working in the food regulation settings, a sampling strategy was developed to ensure coverage of participants working in different areas including policy development, standards setting, implementation, inspection and enforcement. Likewise, the sampling strategy for industry was developed to ensure coverage of a range of business types including local food industry, franchise food industry, supermarkets, industry advocacy groups and consumer advocacy groups. Potential participants and organisations were contacted by one researcher in AU and NZ and two researchers in the UK. Initial contact was made through e-mail. If no response was received, a second email was sent and this was followed up by a phone call if a response to the second email was not received. In total, 80 individuals were contacted. Eight declined participation or did not respond to requests for participation. The email/ phone call outlined the purpose of the study and invited the individual to participate in an interview. An information sheet and letter of introduction was also included. Table  1 provides an overview of the participant sample.

As noted above, the actors within the food industry, as well as regulation vary, which is an important consideration in the interpretation of the results. Table  2 provides an overview of participant characteristics as they relate to the participant’s role within regulation or industry.

Data collection

Data were collected using semi-structured interviews. The interview guide was piloted separately in the UK, NZ and AU to check for usability and relevance to the cultural context. Minor changes were made to increase flow of the interview schedule based on feedback from piloting. The interview schedule was used as a guide for discussion during interviews. Relevant to this paper, the interview guide was designed to discuss food regulator and food industry representatives’ ideas about food safety, responses to food incidents in general, regulation and maintaining safety standards, as well as challenges to compliance with food regulation. The interview guide has been published elsewhere [ 23 ].

Interviews were conducted face-to-face or over the telephone at a time and location convenient for the participant. Phone interviews were used when participants were geographically distant from the interviewers. Interviews ranged from 30-60 min. Three interviewers collected data, one in Australia and NZ and two in the UK. The three interviewers met fortnightly via Skype during the data collection period to ensure consistency in questioning. Interviews were conducted in AU and the UK between July and November 2013 and in NZ in October 2013 until saturation of themes was reached [ 24 ]. Interviews were digitally recorded using a voice recorder after consent to conduct the interview had been obtained.

Data analysis

Digital voice files were de-identified and transcribed verbatim. In this study, nonverbal cues, emphasis and pace were deemed less important and were not transcribed. Interview transcripts were checked by each interviewer for accuracy. De-identified transcripts were then imported into NVivo 10.0 (QSR International, Doncaster). A start list of codes was developed by the research team (including academics and industry partners working in the food regulation setting). Transcripts were then coded by one researcher using this start list of codes following six stages of thematic analysis [ 25 ]. Central to this paper are the codes developed from the research objectives that included role of interviewees in regulation, industry and maintaining safety standards. As coding progressed, further themes and sub-themes were added based on the objectives of the research and information in the data. Coding was checked and agreed upon by team members at fortnightly team meetings and at two data analysis workshops during the data analysis phase of the research. Other members of the research team reviewed up to five transcripts each to confirm the themes arising from the primary researcher’s analysis.

Information regarding participant sample characteristics, as outlined in Table  2 , have been included when reporting participant quotes if this information was deemed useful for the purpose of data interpretation.

The two themes identified in interviews with regulators related to their role in engagement with the food industry, and conflict and understanding in their relationships with industry. Not surprisingly, the regulator voices across all three countries represented below are from what we have categorized as ‘state-based food regulation’ (see Table  2 ), while those in the national food regulatory bodies did not comment on their engagement with the food industry. This is likely because it is the state-based regulators who are responsible for the enforcement of the code and therefore have ongoing personal engagement with members of industry.

Perception of role in engagement with food industry

Participants across all three countries discussed their role in food safety, and their relationship with industry. There were clear differences in how AU and NZ described their roles when compared to UK regulators.

AU and NZ regulators identified their role as developers or enforcers of regulation, with the primary focus being public safety. However, they identified conflict with industry, which they perceived to be a misconception on the part of industry that regulators try to cause problems for industry:

I mean I think we’re all after the same end, like we’re all there to protect public health, and I think a lot of the food guys are wanting to do that as well…And, yeah, we don’t want to be shutting people down, we really don’t. If we can identify problems we want to go in and fix them up and I think if that can all be managed well and the people where a problem might be identified, if they’re very keen to do the right thing then often they’re the success stories and they actually – you know, their businesses go on to be stronger and stronger and stronger… There’s a perception perhaps that public health want to close down and anywhere that’s dirty we don’t want them to operate anymore and I don’t think that’s the case. (AU-REG23)

The above comment also identifies recognition of the mutual benefit that can result from compliance with regulation; public safety and making industry stronger. NZ-REG1 echoes this, commenting that while regulators are at times perceived as being the enemy, industry often do value their recommendations and view them as strengthening industry. In recognition of the potential to be viewed as the enemy, the following suggests that NZ regulators make a concerted effort to ensure their behaviours and actions suggest otherwise, and to work with industry to resolve issues:

Whenever we do – in government we tend to be fairly cautious because we’re bureaucrats and sometimes – there’s always a little bit of pushback [from industry]; sometimes there’s quite a bit of pushback. I have to say quite often companies are on the same page when they know that their reputation is at risk so quite often the companies – well, there was one of the companies that we were dealing with in the incident who said – we said ‘this is what we think is affected and this is what we recommend you recall’ and they said ‘we’re not going to quibble, we’re just going to get rid of the stuff. Anything that’s potentially affected we’re just going to withdraw the whole lot’ and the only reason they did that is for commercial reasons, not for trust reasons and I think that was the right thing to do. It will have cost them more money but it was an investment in the brand. (NZ-REG1)

UK regulators also identified their role as being responsible for enforcing regulation. However, within the following quote there is no indication that working with industry may be beneficial for both parties. The quote, among others, is indicative of a more top down approach than identified in NZ and AU interviews:

I think there’s an expectation on their part [industry] that we’re almost viewed as a consultant in many cases and we should be providing them with information and guidance to update their systems when in fact that responsibility lies with them and they’re duty bound, or they need to think about who they engage as a consultant to assist them in their activities. It’s not our role really; our role is to identify what’s not compliant and to advise the businesses that they need to address these issues. You might offer some guidance but our role is not to recreate or reproduce your documentation or your procedures or practices, it’s to make sure that they are correct and advise you of that and then monitor the activity to see that you’ve addressed those issues (UK-REG5)

UK regulator interviews demonstrated a clear division of roles regarding food safety, and little communication or partnership between industry and regulation.

Perceived influences on regulator-industry communication: conflict and understanding

Within the UK specifically, regulator interviewees discussed the reluctance of industry to work with regulators. For example:

They [industry] have the technical knowledge and we may not have the knowledge to deal with some of the stuff because it is quite technical… we have a general understanding of most stuff and if we want to obtain particular information we have to go through loads of regulation and guidance to get that information where they’re actually doing it all the time. Sometimes you may walk in and they’ll say ‘well, what do you know? I know more about this activity than you do’ which they may do but we will look at it objectively and where our powers or where our skill comes in is an ability to audit systems and to look at stuff objectively and make decisions based on the information that’s provided to us. (UK-REG5)

In relation to the recent horsemeat scandal in the UK (2013), the following was stated regarding why communication might lead to conflict between the two parties. A clear explanation is given which relates to the fear of repercussions that may result from transparency between the two.

I think that at the start there was quite a bit of reluctance of industry to work with the < name of regulating body > and that’s sort of quite historic because they were concerned that if they told < name of regulating body > things and they admitted they didn’t do things right they might get punished. (UK-REG10)

UK regulators identified industry as falling into one of four groups; dependent on the extent to which they want to comply with regulation, and the extent to which they actually do comply with regulation. The perception is that these different ‘types’ of industry require differential treatment:

You’ve got those that will know what they need to do and how they need to do it and will do it proactively; you’ve got those that want to comply but don’t really know how to comply and are looking to you for help and advice; you’ve got businesses that don’t want to comply but, you know, with a little bit of sort of help the persuasion will get there. And you’ve got those that don’t care, don’t want to care, are in it for pure profit and are trying to avoid the regulation and trying to avoid being caught making money at the expense of, well, anything really. (UK-REG3)

Those who are trusted to comply were identified as requiring less monitoring:

So the likes of Tesco and Sainsbury’s and McDonald’s, etcetera, you would probably be able to look away from them because they have got generally very good systems in place when they’re implemented…leave the likes of the bigger retailers to their own devices because simply we knew that they would do their own investigation and pull this stuff if they found it on their shelves. (UK-REG3)

However, conflicting with the above quote, the following suggest that larger industry (e.g., McDonalds) are more closely monitored because of the greater impact if a food incident was to occur. UK-REG3 continues:

… if you have somewhere that has the potential to have a bigger impact you visit it more often than you would somebody that has the potential of a smaller impact, like a post office selling a few lollies; that makes common sense. (UK-REG3)

We are unable to explain this inconsistency and further understanding of the flexibility in monitoring and enforcement is required.

Whilst also identifying the conflict between regulators and industry, AU regulators were sympathetic to the fact that compliance with (over)regulation can be burdensome and potentially detrimental to business. The following quote emphasizes the influence that the political economy has on industry food safety management:

A lot of people don’t want to make – no-one really wants to make somebody else sick but there are business imperatives that are pushing some practices, you know, they need to make money to survive because that’s their livelihood but also they need to be doing those things in a safe way that doesn’t make people sick. (AU-REG23)

Difficulties in compliance

Representatives of industry discussed their difficulties with compliance in relation to the changing nature of regulations, the knowledge gap between industry and regulators, a lack of consistency across regulators, and concerns about the potential for over-regulation. Not surprisingly, the majority of the comments regarding difficulties in compliance were from individuals whose primary position in industry was the finance and management of large-scale corporations (see Table  2 ).

NZ and AU industry interviewees discussed the difficulty in abiding by complex and sometimes irrelevant regulations that are constantly updated and changed, requiring more work on the part of the industry to get up-to-speed.

We need to be making sure that we produce a product that is safe and we don’t need to complicate that. Especially for small producers let’s just keep it simple. Let’s just make sure that all the criteria is being met but let’s not overcomplicate it. (AU-IND4)

I think they’re updating the current food standards codes. I think it’s been challenged that many times that it’s irrelevant to the industry…Because it’s boring and you have to read ten pages to get to the results. (AU-IND5)

Contrary to regulator beliefs about their proximity to and understanding of industry challenges, industry participants noted that regulators are too far removed from the food industry and therefore, do not relate to the barriers to compliance with regulation:

Well, they need to understand food and they can’t understand food if they don’t understand the food system that’s providing it, particularly if you’re trying to protect consumers, which is their fundamental role, of course. (AU-IND3)

Consistent with comments made by AU industry, UK interviewees also commented that individuals in regulation do not always have the food expertise required to make the decisions they are faced with:

I think it’s very important to have an independent position but you need to work closely because if you want real expertise and technical guidance, technical advice, some of that best knowledge sits within the food chain. You have to find a balance between the two but independent robustness is very important. (UK-IND9)

They get in wrong but in terms, sometimes, of their understanding of the industry. You know, a lot of their expertise has been lost down the years as people have moved around, gone, and they sometimes seem to know remarkably little about how the food supply chains work. (UK-IND13)

This lack of knowledge on the part of regulators was seen as problematic and in some cases, harmful to businesses. For example:

I mean the regulators, sometimes they’re not always as sensitive to the sort of brand issues as food manufacturers are and they can say something which is intended for the best but, you know, plays rather badly in the media and can sometimes make matters worse. Sometimes I’ve had incidences where they have made statements in the media which have required retailers to remove product from shelf completely unnecessarily because they’ve just said the wrong thing completely inadvertently because they’re not trained to deal with the media or they don’t sort of think through what it is they’re actually saying. (UK-IND12)

Another difficulty faced in complying noted by industry was the lack of what they referred to as ‘consistency’ in enforcement, which in some circumstances suggested a conflict of interest or differential treatment:

Environmental Health Officers in different council areas may be administering the law differently – they need to come together and apply the law in the same way in order to get a unified approach. (AU-IND2)

I think also enforcing [regulation] it is quite important as well. I think one of the things that people get upset with – you know, again I refer to my friend who manages a pub – she says ‘oh well I’ve been into restaurants and I’ve walked past their kitchens and I’ve seen their kind of messy floors and how come I’m being pulled up because I didn’t fill in my fridge/freezer temperature gauge for last week and yet they had meat on the floor? When I walked past I could’ – so I think there’s that. (UK-IND4)

Concerns about the extent of regulation, and the potential effects of regulation on smaller industry were also noted:

Also the cost of manufacture in Australia is ridiculous with all the red tape. All the requirements that the government puts in, day in day out, it doesn’t help local manufacturers. If you’re small it’s really hard because you’ve got no volume. It’s easier for bigger players because they can bend the rules in different ways because they’ve got volume. (AU-IND5)

I think farmers are very fed up with red tape and bureaucracy. We don’t want to tie people down with lots of bureaucracy. It makes it harder to run a business with all that, when you’ve got paperwork and bureaucracy so I think – I don’t think it’s an issue of trust, it’s just an issue of focus. So farmers want their focus to be on driving these businesses forward not holding them down by red tape and bureaucracy… regulators in the UK are very – can definitely put a lot of burden on farmers and that’s not always equal to other parts of the world which makes it difficult for us to compete globally. (UK-IND10)

While not a matter of distrust, the above identifies conflict or a lack of communication between the industry and regulators, and the perception or reality that regulation is problematic for business.

Conflict with, and distrust in, regulators

Several participants from NZ and AU industry noted the importance of trust in their relationship with regulators, but indicated that trust between the two is not always present. Among industry representatives, this was largely attributed to poor communication and engagement by the regulators, which in turn led to the perception that regulators are not focused on maintaining public safety, as intended:

I’m not a big fan of food regulators. I think food regulators are there to protect corporate industrialized food systems and not public health and safety. You don’t have to look very long at the regulatory system or at the risks that we are exposed to to start to question the regulatory system and to realize that the regulatory system is letting us down, letting the public down and then the consequence of that is you have low trust in mainstream – a mainstream food system and the regulatory authorities that oversee that food safety regulatory systems to be overhauled, completely overhauled to work on the premise of protecting public health and safety rather than, as we do at the moment, protecting industry…. I mean chemicals used in agriculture, in food production, chemicals used in food processing, GMOs used in foods, radiation being used, these are all issues which we believe are being very poorly assessed. System wide risks that the public is being exposed to that’s being very poorly assessed for public health and safety because the regulatory system is designed to not look at what they don’t want to look at. It’s designed to hide under the carpet many of the consequences of the risk that the food industry is using or technologies that expose the public to risks. Many of those risks, the regulatory system desire to not look at those risks. (AU-IND1)

The interviewee here, whose role in industry is food safety, is not surprisingly focused on ensuring public safety. Their perception is that regulators focus too much on protecting selected industry, suggesting that Australian food regulation is in part at least, driven by the political agenda. Distinct from the role described by regulators, their perception is that the safety of the public is not the primary concern. Similarly, NZ-IND4 discusses their distrust in regulators, but with a different rationalization which may be related to their role in the finance and management of industry. The quote suggests that trusting regulators to take action can have negative implications for industry when the safety of a product is in question:

It’s not just what the company does, it’s also what the regulator does and if I look at the < removed for confidentiality > recall I believe that brand has sustained some damage through no fault of the company at all, purely because < name of regulatory body > pressured into recalling every single batch, its entire brand line, when in fact there were only specific batches involved; that said to consumers there’s something wrong with every product. (NZ-IND4)

UK-IND11, identified as a consumer advocate, also discussed the fallibility of regulators and the consequences of these alleged mistakes on industry. The participant is sympathetic to the dual role of regulators as looking out for consumers but also having to consider the implications for industry if their actions are overly cautious:

The problem I think with regulators is in the Catch 22 where they can take proactive action but if that means that they, for example, go too early and say to companies ‘okay, clear the shelves. Those tens of millions of products, huge amounts of your money, off the shelves, chuck them away, destroy them; it’s your profit’ and then it turns out that it wasn’t really a problem and the regulator had – you know because there’s always uncertainty about these things, the regulator had kind of erred on the side of caution, can cause, you know all kinds of problems and so regulators aren’t allowed to do that because they have to sort of pre-empt things but also know for certain. (UK-IND11)

The dual role of the regulator, as advisor to the consumer and industry, was also identified as a potential source of conflict with regulators. For example, the case above identifies regulators as being perhaps overly cautious for the protection of the consumer, thereby damaging the industry. Below, NZ-IND1 who is involved in the finance and management of industry, identifies the pressure on regulators to serve multiple interests:

I mean food regulators, they can find themselves trying to serve both consumers and manufacturers. We have quite a strong push here for export so a lot of focus on the safety of food exports, so that can mean that the domestic market is – domestic consumers are less well served. (NZ-IND1)

NZ-IND1’s comment might also relate to concerns posed above regarding regulators’ focus on the political agenda, rather than public health. If there is a push to export food and to grow business for economic gain in NZ, there is a potential for conflict of interest – however, this is not empirically supported and is in need of further exploration.

UK industry also noted the importance of an interpersonal relationship between industry and regulators, and the importance of trust. Trust was however identified as having declined over time:

I think it’s [trust] not as good as it was. I mean in days gone by the links were a lot closer with the Minister of Agriculture, as it was then, but a lot of it’s down to personal contacts and that’s why it’s important for companies to have people who build those contacts, that you pick up the phone to people and there’s a level of trust there. (UK-IND7)

This point was further emphasized by UK-IND3 who noted that as the result of a change in government, individuals in food regulation no longer communicate with the food industry:

They had a food policy which was a much more – I mean they never got to their conclusions but at least they started the process of a much more comprehensive food strategy really. This government abandoned all that and went back to, you know, ‘how do we produce more and sell more in Britain?’… the previous government used to hold six monthly discussions with CEOs of food retailers; this government abandoned that straightaway and all they wanted to talk to was farmers all the time, which was fine because actually it means they bother us less, until of course you get an incident and then they’ve got no knowledge of how our sector works or our relationship with consumers and what actually happens on labels and all these kinds of things. (UK-IND3)

The lack of communication with the food sector may be in part due to the means by which the role of regulators is governed. Consistent with comments from AU industry about the role of government in shaping the agenda for the food sector, UK-IND3 (industry food regulator) and UK-IND2 (finance and management) comment:

Well I would say our relationship with the officials is very good… but the ministers are not necessarily focused on our end of the supply chain. They’re very politically driven and they’re politically driven towards farming rather than either manufacturing or retail… (UK-IND3)

I think certainly government and UK government and some of the key government departments we’ve got individual good relationships there but in terms of how much they listen and respond to not just us but lots of other organisations in the food and farming space, so that’s open for debate I think. Certainly we would say it’s difficult to engage UK government on lots of these issues. (UK-IND2)

Here it is presented that the interests of the government, in this case selling more product within Britain, needs to be taken into consideration. UK-IND11’s comment emphasises the power of political agendas:

But also you know, there’s huge legal things and political things because then you know if the politicians lose the trust in the regulators you know they’ll end up restructuring the organisation......So there is a thing where regulators I think are in a very, very difficult position…(UK-IND11)

UK industry viewed the extent of bureaucracy and the fragmented information spread amongst stakeholders as problematic to the functioning of regulation:

You know, regulators and government, it’s so difficult to do that and there is that thing of always, you know, kind of a stereotype civil servant of always passing things up and down the line endlessly checking not only the facts but also whether the boss – and the boss’s boss and maybe the politician’s boss....you know, making sure everybody’s onside…And I think that one of the problems with the – certainly in government and to a certain extent with regulators – is sort of having somebody who can make that kind of authoritative statement …But I think that very often the problem is that they have people in all of the organisations who can’t really just act on 25% information, you know, they have to have 95%....you know, and 95% is incredibly difficult to get. (UK-IND11)

Furthermore, rather that working together, the message that was conveyed by our interviewees was that there is animosity and distrust between the politicians, the regulators and the industry. For example:

…the reason why politicians will get involved is because they will fear that not everybody in the food industry can be trusted, so that’s why regulation exists, is to prevent those that don’t play by the rules or don’t play fair from harming consumers and the general public. (UK-IND14)

The < name of regulatory body > is, sadly, a hollow shell of what it once. I mean food safety is all it does these days so, yes, you would expect the < name of regulatory body > to be a first port of call and to be doing something but they’re so emasculated these days you just think – it was a very, very clever move by the coalition government to not abolish it in the bonfire of the [inaudible] because I think there would have been an outcry and a massive campaign, not only by our campaigning sector but even some bits of the food industry wouldn’t have wanted to see it go. But what they wanted it to be was weaker and it now is. (UK-IND8)

UK-IND8, responsible for finance and management of industry, may be speaking to the recent (2010) changes in England whereby the main regulatory body is no longer responsible for food authenticity and composition, and are solely focused on food safety.

Solutions for improving relationships

In order to address many of the potential areas of conflict mentioned above, participants voiced a variety of potential solutions to improve the relationships between regulators and industry. These included making regulation more flexible and realistic, encouraging information sharing and mutual education between regulators and industry, and generally encouraging more positive relationships through face to face interaction and frequent communication.

AU-REG respondents noted the need for a degree of flexibility in regulation, dependent on the industry involved. The degree of flexibility was identified as industry-specific, with changes in regulation likely affecting industries differently. This may be a potential solution to conflict, but one that needs to be approached with caution, taking into account the confusion and conflict that can result with inconsistency (i.e., differential treatment) and change:

I mean there’s a whole lot to food regulation now and there’s queries being raised by some whether the type of regulation, the outcomes based stuff that’s been put out there, is the best way to go or the prescriptive, or do you go like an island in the middle [allow some self-regulation]? The basis for the outcomes based is – so it gives industry the opportunity to be innovative and seek the outcome by a different means rather than traditional means and that’s fine. We’ve really only got so many businesses that have the capacity to do that, the majority – 99% – of businesses I’m sure, food businesses, haven’t got the capacity to be that innovative with how they comply with food regulation, so it’s – we’ll see over time whether that evolves. I’m sure it will but it’ll evolve to something else. There’s constant change which must be confusing for the industry. (AU-REG20)

As a solution to conflict between regulators and industry, AU and NZ regulation participants also discussed their role in ensuring that the regulations being put into place are realistic, requiring correspondence with and input from industry:

We need to make sure that it [regulation] is achievable by industry. It’s no good putting unrealistic requirements on industry, so we certainly sign off with industry that ‘here’s what we need to put in place and you tell us if you’ve got any concerns or if you think there’s any impracticalities with it and we’ll address those’. (AU-REG20)

Government and regulators can have a role helping the business to comply or knowing what they need to comply with rather than just setting it and hoping that they – or expecting that they do what they’re meant to do. (AU-REG19)

NZ regulator participants discussed the importance of communication to ensure that industry are able to understand, and more importantly, implement guidelines:

Part of having a good regulatory system is being good at voluntary uptake by industry and for us to have ways to assist them to do that by having some good guidance and information available. (NZ-REG6)

The importance of face-to-face interaction was also noted by state regulator AU-REG15:

I guess business owners and those sort of guys that are on the front foot, we have more of a collaborative approach when we work with them, so we’re definitely friendly, have a nice approach and talk with them and try and understand their business, their challenges. Being a smaller community we are quite visible to businesses so, you know, you pop into a shop and you buy an apple or you buy a drink or you get something and you have a chat with them and build a bit of a relationship that way. (AU-REG15)

AU industry also suggested a need for a relationship with regulators, and a means by which relationships can be developed between industry and regulators to facilitate information sharing. They viewed regulators as a resource:

I believe that it has to be win/win and I think when you’re building that relationship with them – I find with the health regulators, if you involve them in your business they will help you and anyone – I think once they know that you’re open to listening to them you build a rapport with them that then they’re willing to work with you but when you come in and see them as the enemy - oh my God the health inspector seen as an enemy - they’re not your enemy. They’re here and if you’re doing everything right - they’re your friend if you’re doing everything right and I think this is where some – I believe in the food industry some people say ‘oh they’re the enemy’. They are not the enemy they are the supposed industry experts and they’re sometimes more up to date than the mum and dad deli or the mum and dad restaurant. They’re more up to date with what’s going on… I think you have to use them as a resource rather than – I think they are a resource to you rather than anything else. (AU-IND9)

The AU industry participants recognised their need to partner with regulators, particularly in times of food safety incidents where government is seen as a credible source of information and arguably the representative of the food system:

In some cases our opinion is that government is going to have far more credibility than a commercial organization. We will always do our best but, you know, to have a government authority presenting the facts in some cases is far more credible than a commercial organization. (AU-IND6)

NZ industry participants spoke about the important role regulators play in the operation of industry. Discussing their role in advising on the recall of products, NZ-IND3 stated:

It was important that as an overarching regulator < name of regulating body > could provide good advice not only to the public but also to industry. (NZ-IND3)

The role of advisor is bidirectional, however. Regarding the lack of knowledge regulators have about the food industry, AU-REG3 (employed by a national food regulatory body) posed the solution of information sharing.

We have a good working relationship with the regulators. We give them information if they ask for it, and sometimes we give them information if they don’t ask for it but if we think it helps their position. I mean I think you need to understand that if the regulators are not close to the industry, if they don’t actually understand the industry itself, then they don’t – you know, they’re restricted in how effective they can be. (AU-REG3)

In the above quote AU-REG3 reflects the importance of a relationship between industry and regulators in the management of risk, with industry playing the role of educator in some circumstances. The regulators, in this case, need to work with industry to obtain the correct information about food safety issues in order to manage the risks.

In summary, AU and NZ regulator participants depicted greater understanding of the difficulties faced by industry in their compliance. This may be the result of their proximity to industry in the way regulation is enforced. For example, they discussed being able to meet face-to-face with industry, and to maintain continuity in regulatory representatives. As a result, they were able to suggest means by which barriers to communication and conflict could be overcome. As reflected by the lack of representation by UK in the above, UK interviewees did not discuss potential solutions for overcoming problems of distrust and lack of communication.

Consumers in industrialised countries increasingly demand foods that are safe and of high quality. This, alongside the interest of public health and an increasingly globalized food system, has led to the development of food safety standards [ 26 ]. This paper presents the views of individuals in food regulation (the regulators), and those in the food industry (the regulated), regarding their trust in and communication with one another within three countries: the UK, New Zealand, and Australia. Our primary aim was to provide recommendations, from representatives of industry and regulation, for facilitating the (re)building of trusting and communicative relationships between the two parties, with the end goal of increasing compliance with regulation and protecting public health. As an outsider, food safety standards may be viewed as a set of rules or best practices, enforced by one or more regulatory body. We may view industry then as compliant, or noncompliant. However, as we have shown, there are a variety of factors that shape the dynamic and complex relationships between regulators and industry, and the nature or extent of partial or (non)compliance. It is by speaking with these actors that we can identify barriers to compliance that are amenable to change. The following outlines key barriers and points of conflict identified in the data, with the primary aim being to propose solutions relevant to improving regulator-industry communication and trust. In doing so, we identify that while trust needs to occur at an interpersonal level between individual actors, trust at an institutional level also needs to occur. At times, participant comments were suggestive of a boarder distrust in either the systems of regulation or industry in general.

While previous research has identified that food safety regulation is trusted by the community [ 27 ], our data suggest this is not the case for individuals working within industry. Primarily, there is concern on the part of some UK and AU interviewees that regulations are based on larger political agendas or serve the interest of selected industry (rather than public health). Although these comments were not consistent across the findings, they are important nonetheless because they point to the need for greater transparency in the development and enforcement of food safety standards, and the need to develop institutional trust in regulation as a system – either at a local/state (e.g., department of health) or national level (e.g., FSA or FSANZ). Furthermore, these comments suggest a lack of, or breakdown in interpersonal trust between industry and regulators; a finding evident elsewhere in the data. Institutional distrust was also evident from the perspective of industry who at times suggested that regulation (rather than individual regulators) ‘holds’ industry down (e.g., red tape). Interestingly, regulator interviewees were aware of this perception and AU and NZ participants identified a need to communicate with industry about their actual intentions; ensuring public safety and safeguarding businesses. However, regulators were not always sympathetic to industry perceptions. There were concerns from regulators that individual industry representatives are at times purposely noncompliant with regulation, which reflected badly on industry generally. From the perspective of regulators, we suggest that interpersonal interactions with industry have tainted the perception of industry as a whole; a finding consistent with the theoretical literature on trust whereby it is argued that that although “the real repository of trust is in the abstract system, rather than the individuals who in specific contexts ‘represent’ it…it is the flesh and blood people (who are potentially fallible) who are its operators” [ 28 ] (p. 85) and who come to represent the system.

In several interviews from AU and NZ, success stories were noted, whereby participants discussed the importance of face-to-face communication between industry and regulators, establishing relationships at the onset of business development, and creating an environment where industry can enquire about food safety issues without fear of repercussion. We argue that these may be viewed as facilitators to the development of interpersonal trust between regulators and industry representatives, which based on our discussion above, may in turn have positive implications for institutional trust. Whilst there are undoubtedly structural and resource barriers to these solutions, they are nonetheless feasible in certain circumstances. For example, having one individual responsible for specific areas would allow for continuity in enforcement and the development of the interpersonal relationships and familiarity needed to foster trust [ 29 ].

Food safety is a complex issue and it is understandable that perspectives on how to manage food safety would differ between practical (industry) and technical (regulators) players. We argue that communication would facilitate a mutually beneficial understanding of these perspectives. For example, previous research has identified that in times of food safety incidents, it is important for public health professionals to work with the media in the construction of their reporting to ensure that information being disseminated to the public is accurate [ 30 ]. The need for information sharing (from industry to regulator) was identified in our interviews, whereby both parties indicated that some regulators lack knowledge about the food system which at times affects their judgement of how to handle food recalls, or their ability to relate to difficulties in meeting food standards. We suggest that a possible way forward is the inclusion in course curricula the study of food laws and standards for Environmental Health degrees, and for individuals in regulation who have not worked within the food system in any other capacity.

Most prominent in the findings from both parties were discussions around barriers to compliance. The perceived differential treatment, difficulty in understanding regulatory requirements, changing requirements and overregulation were concerns posed by industry, and recognised by NZ and AU regulators. Whilst a solution proposed by many to address overregulation was flexibility in enforcement, this may lead to further feelings of differential treatment and lead to confusion and individual interpretation of what/how standards should be met. Also problematic are the barriers to addressing changing requirements, as they are based on best-practice guidelines that are constantly being updated based on emerging research. However, based on the data from all three countries, we do recommend that an audit be conducted of what training, information and support is currently available to industry so that any recommendations made from the perceptions of respondents can be grounded in truth and tailored to complement existing resources. Furthermore, given the variety of industry (e.g., mom n’ pop stores, large corporations), individual communication with regulators could allow for adjustments to regulatory requirements on a case-by-case basis, though again there is room here to create confusion and conflict.

Also noted in the data is the importance of political climate and history in shaping how industry and regulators view one-another. Data from the UK were unique from AU and NZ interviews in that they were indicative of very poor relations between regulators and industry. In addition to conflict noted by AU and NZ participants, UK regulators perceived industry to be reluctant to work with them, while also noting that they did not see themselves as working ‘with’ industry but rather, their role was that of an enforcer. From an industry perspective, relationships with regulators lacked communication and trust. As UK-REG10 noted, this may be a problem rooted in history. We suspect that the findings are related to the restructuring of UK food standard governance over the past 15 years. In 2001, the Food Standards Agency (FAS) was developed in order to “put an end to the climate of confusion and suspicion which has resulted from the way food safety and standards issues have been handled in the past” [ 31 ] (p. 6). It was also created in response to the potential conflict of interest with the Ministry of Agriculture, Fisheries and Food (previously responsible for food safety) that arose from their dual role of protecting the interests of public health and agriculture and food industries [ 31 ]. The FSA was therefore purposefully developed so that it had institutional regulation of safety independence from producer interests, and also separated scientific advice from governmental departments, giving science a measure of institutional independence. These characteristics were deemed to be the features of an authority that helped to restore public trust in the UK food system [ 32 ]. However, in 2010, food authenticity and composition policy was transferred back to government departments. The UK National Audit Office (2013) state that this restructuring has led to confusion amongst food safety stakeholders: “local authorities…continue to be unclear on whom to contact, or get information from, in certain areas of food policy. They find that each department has a different approach and way of working which requires duplication of effort on their part.” (p. 7) [ 2 ]. Our data, consistent with the National Audit Office accounts, lead us to suggest that the delegation of responsibilities of the FSA be reconsidered. It is difficult to recommend further action given the complexity of bureaucratic processes. However, perhaps the use of industry advisory groups to inform the way forward for food standards would help develop or maintain trust. Furthermore, NZ and AU regulatory bodies may wish to look to historical blunders in any future plans for restructure.

Building a strong interdependence between regulators and industry can balance power relationships, reduce misunderstandings, and ensure a reliable flow of information for both parties [ 14 ]. These are all crucial to the development and maintenance of trust and communicative relationships. Although the issues identified by interviewees differ, a common theme is the problematic lack of constructive communication. This points to the complexity of human relationships and the difficulty in streamlining processes that are dependent on context, political climate, individual behaviour, material resources, among other factors. Ideally, there should be greater communication between regulators and industry about why specific food standards are set (e.g., why it is important to have food stored at a particular temperature and to monitor the temperature). Furthermore, development of course curricula that includes increased workplace training for regulators on food practices would provide regulators with a greater understanding of the constraints placed on industry in meeting these regulatory requirements. In an evolving food safety climate, our paper offers insight into some of the barriers that shape noncompliance, and points to the tension and conflict identified between industry and regulators. As identified by participants, many of these conflicts and barriers may be easy to address with very few resources. Most central is the need for interpersonal communication from representatives of both parties. It clearly benefits public health to have transparent, open and communicative channels operating between food regulators and the food industry. We provide these data and insider suggestions as a means of overcoming conflict.

Abbreviations

New Zealand

United Kingdom

Burris S, Wagenaar AC, Swanson J, Ibrahim JK, Wood J, Mello MM. Making the case for laws that improve health: a framework for public health law research. Milbank Q. 2010;88(2):169–210.

Article   PubMed   PubMed Central   Google Scholar  

National Audit Office. Food safety and authenticity in the processed meat supply chain. 2013. 20 July 2016.

O'Mahony PJ. Finding horse meat in beef products - a global problem. Q J Med. 2013;106:595–7.

Article   Google Scholar  

Green JM, Draper AK, Dowler E. Short cuts to safety: risk and 'rules of thumb' in accounts of food choice. Health Risk Soc. 2003;5(1):33–52.

Kriven S. Business risks from food poisioning in food processing: the Garibaldi case. Aust Agribusiness Rev. 1995;3:5.

Google Scholar  

The Guardian: BSE crisis: timeline. The Guardian; 2000. https://www.theguardian.com/uk/2000/oct/26/bse3 . Accessed 10 Feb 2017.

Crawford BA, Cowell CT, Emder PJ, Learoyd DL, Chua EL, Sinn J, Jack MM. Iodine toxicity from soy milk and seaweed ingestion is associated with serious thyroid dysfunction. Med J Aust. 2010;193(7):413–5.

PubMed   Google Scholar  

Knowles T, Moody R, McEachern MG. European food scares and their impact on EU food policy. Br Food J. 2007;109(1):43–67.

Coveney J, Mamerow L, Henderson J, Taylor A, Meyer SB, Ward PR. Comparative examination of trust during times of a food scandal in Europe and Australia. Food Public Health. 2012;6(2):202–12.

The OzFoodNet Working Group. Monitoring the incidence and causes of diseases potentially transmitted by food in Australia: Annual report of teh OzFoodNet network, 2011. OzFoodNet. 2015;39(2):E236–64.

Abelson P. The Annual Cost of Foodborne Illness. Sydney: OZFoodNet; 2006.

Baier A. Trust and antitrust. Ethics. 1986;96(2):231–60.

Luhmann N. Trust and Power: Two works by Niklas Luhmann. Brisbane: John Wiley and Sons; 1979.

McCaffery DP, Smith AE, Martinez-Moyano IJ. "Then let's have a dialogue': Interdependence and negotiation in a cohesive regulatory system. J Public Health Adm. 2007;17(2):307–34.

Wicks AC, Berman SL. The effects of context on trust in firm-stakeholder relationships: The institutional enviroment, trust creation and firm performance. Bus Ethics Q. 2004;14(1):141–60.

Henderson J, Ward PR, Coveney J, Meyer SB. Trust in the Australian food supply: innocent until proven guilty. Health, Risk Soc. 2012;14(3):257–72.

Zinn J. Heading into the unknown: everyday strategies for managing risk and uncertainty. Health Risk Soc. 2008;10(5):439–50.

Luhmann N. The Paradox of System Differentiation and the Evolution of Society. In: Alexander J, Colomy P, editors. Differentiation Theory and Social Change. New York: Columbia University Press; 1990. p. 409–40.

Fukuyama F. Trust: The Social Virtues and the Creation of Prosperity. New York: Free Press Paperback; 1995.

Hutter BM, Amodu T. Risk Regulation and Compliance: Food Safety in the UK. London: The London School of Economics and Political Science; 2008.

Patton M. Qualitative Research and Evaluation Methods. Thousand Oaks: Sage; 2002.

Popay J, Rogers A, Williams G. Rationale and standards for the systematic review of qualitative literature in health services research. Qual Health Res. 1998;8:341–51.

Article   CAS   PubMed   Google Scholar  

Wilson A, Coveney J, Henderson J, Meyer SB, Calnan MR, Caraher M, Webb T, Elliot A, Ward PR. Trust makers, breakers and brokers: building trust in the Australian food system. BMC Public Health. 2013;13:229.

Guest G, Bunce A, Johnson L. How many interviews are enough?: an experiment with data saturation and variability. Field Methods. 2006;18(1):59–82.

Braun V, Clarke V. Using thematic analysis in psychology. Qual Res Psychol. 2006;3(2):77–101.

Trienekens J, Zuurbier P. Quality and safety standards in the food industry, developments and challenges. Int J Prod Econ. 2008;113:107–22.

Henderson J, Coveney J, Ward P. Who regulates food? Australians' perceptions of responsibility for food safety. Aust J Prim Health. 2010;16(4):334–51.

Giddens A. The Consequences of Modernity. Stanford: Stanford University Press; 1990.

Luhmann N. Familiarity, Confidence, Trust: Problems and Alternatives'. In: Gambetta D, editor. Trust: Making and Breaking Cooperative Relations. Oxford: University of Oxford; 2000. p. 94–107.

Wilson A, Henderson J, Coveney J, Meyer SB, Webb T, Calnan M, Caraher M, Lloyd S, McCullume D, Elliot A, et al. Media actors’ perceptions of their roles in reporting food incidents. BMC Public Health. 2014;14:1305.

Minister of Agriculrure Fisheries and Food. The Food Standards Agency: A Force for Change. 1998. 20 July 2016.

Wales C, Harvey M, Warde A. Recuperating from BSE: The shifting UK institutional basis for trust in food. Appetite. 2006;47:187–95.

Article   PubMed   Google Scholar  

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Acknowledgements

The authors would like to acknowledge Sian Calnan and Sue Lloyd who undertook data collection in the UK. The authors would also like to acknowledge Professor Elliott and Professor Caraher for their input into the research design and delivery, and Liz Withall for assistance on this project.

This project is funded by an Australian Research Council Linkage Grant (LP120100405) and by industry partners SA Health and Food Standards Australia New Zealand (FSANZ).

Availability of data and materials

Data will not be shared. Ethics approval does not permit the sharing of data due to issues of confientiality.

Authors’ contribitions

JC, PW, JH, SM, TW, and MC contributed to the conceptualisation of the project and to the initial grant application. SM wrote the first draft of the manuscript and it was reviewed by all authors. AW collected data in Australia and NZ, and managed data collection in the UK. SM and AP analysed the data. TW and DM assisted with recruitment of media actors in Australia. All authors read and approved the final manuscript.

Competing interests

The authors declared that they have no competing interests.

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Not applicable.

Ethics approval and consent to participate

This research received ethics approval from Flinders University Social and Behavioural Research Ethics Committee (SBREC) in Australia to collect data in all sites (AU, UK and NZ). However, retrospective ethics approval following data collection was also obtained from the University of Kent Research Ethics Committee. Additionally, the New Zealand Ethics Committee (University of Waikato) reviewed the project and provided a written statement indicating that the project would have been granted ethics approval and that retrospective approval was not required. Written informed consent was obtained from all participants.

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Julie Henderson

Food Safety and Nutrition Branch, SA Health, Adelaide, Australia

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Meyer, S.B., Wilson, A.M., Calnan, M. et al. In the interest of food safety: a qualitative study investigating communication and trust between food regulators and food industry in the UK, Australia and New Zealand. BMC Public Health 17 , 189 (2017). https://doi.org/10.1186/s12889-017-4118-x

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Research Article

Quantitative Analysis of Food and Feed Samples with Droplet Digital PCR

* E-mail: [email protected]

Affiliation Department of Biotechnology and Systems Biology, National Institute of Biology, Ljubljana, Slovenia

• Dany Morisset, 
• Dejan Štebih, 
• Mojca Milavec, 
• Kristina Gruden, 

• Published: May 2, 2013
• https://doi.org/10.1371/journal.pone.0062583
• Reader Comments

In this study, the applicability of droplet digital PCR (ddPCR) for routine analysis in food and feed samples was demonstrated with the quantification of genetically modified organisms (GMOs). Real-time quantitative polymerase chain reaction (qPCR) is currently used for quantitative molecular analysis of the presence of GMOs in products. However, its use is limited for detecting and quantifying very small numbers of DNA targets, as in some complex food and feed matrices. Using ddPCR duplex assay, we have measured the absolute numbers of MON810 transgene and hmg maize reference gene copies in DNA samples. Key performance parameters of the assay were determined. The ddPCR system is shown to offer precise absolute and relative quantification of targets, without the need for calibration curves. The sensitivity (five target DNA copies) of the ddPCR assay compares well with those of individual qPCR assays and of the chamber digital PCR (cdPCR) approach. It offers a dynamic range over four orders of magnitude, greater than that of cdPCR. Moreover, when compared to qPCR, the ddPCR assay showed better repeatability at low target concentrations and a greater tolerance to inhibitors. Finally, ddPCR throughput and cost are advantageous relative to those of qPCR for routine GMO quantification. It is thus concluded that ddPCR technology can be applied for routine quantification of GMOs, or any other domain where quantitative analysis of food and feed samples is needed.

Citation: Morisset D, Štebih D, Milavec M, Gruden K, Žel J (2013) Quantitative Analysis of Food and Feed Samples with Droplet Digital PCR. PLoS ONE 8(5): e62583. https://doi.org/10.1371/journal.pone.0062583

Editor: Joshua L. Heazlewood, Lawrence Berkeley National Laboratory, United States of America

Received: January 29, 2013; Accepted: March 22, 2013; Published: May 2, 2013

Copyright: © 2013 Morisset et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Funding: The work was supported by the Slovenian Research Agency (grant Nos.: P4 0165). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Competing interests: The authors have declared that no competing interests exist.

Introduction

In many aspects of basic research, diagnostic tests, and commercial processes, the advent of modern analytical technologies has provided the ability to detect and quantify nucleic acid targets with unprecedented sensitivity and specificity. Currently, the most common technique for analyzing the presence of nucleic acids in food and feed samples is the polymerase chain reaction (PCR) [1] – [3] . When quantitative analysis is required, the use of real-time quantitative PCR (qPCR) is preferred because of its accuracy and precision [1] . However, its use for target quantification can be seriously limited by a significant bias when the target is present at low concentrations in a background of high numbers of non-target nucleic acids in the sample [4] – [7] . Another important limitation is its sensitivity to the frequent presence of inhibitors co-extracted with nucleic acid from complex matrices [8] .

One example of the need for quantitative nucleic acid analysis in food and feed is the testing for genetically modified organisms (GMOs). Numerous countries have implemented regulations requiring the labeling of products containing GMOs, or materials derived from GMOs, above certain thresholds, therefore emphasizing the requirement for quantification of GMO content [9] .

GMO content in food and feed samples is expressed in relative terms as the ratio of the quantity of the transgene (GM target, i.e . the nucleic acid fragment introduced in the host genome) to that of the endogene (reference gene in the host genome) [10] . Using qPCR–the common technique for GMO quantification-, standard curves for the quantities of endogene and transgene are prepared separately, using serial dilutions of DNA extracted from reference material [8] . qPCR efficiency and hence quantification by qPCR of endogene and transgene, can be influenced by many factors, including inhibitors, present in food and feed samples, leading to significant under- or over-estimation of GMO content [8] , [11] . Much effort has been put into improving the performance of qPCR quantification with respect to the inhibition and matrix effects [8] and the low concentration levels of targets in routine samples [12] , [13] . The lack of certified reference material has also been noted [13] . However, most of the proposed solutions are not practical and reliable quantification of GMOs in food and feed samples still remains a major challenge.

The basis of digital PCR (dPCR) is to quantify the absolute number of targets present in a sample, using limiting dilutions, PCR and Poisson statistics [14] . To do so, the PCR mix is distributed across a large number of partitions containing zero, one or more copies of the target nucleic acid. After end-point PCR amplification, each partition is scrutinized and defined as positive (“1”, presence of PCR product) or negative (“0”, absence of PCR product) hence the term “digital”. The absolute number of target nucleic acid molecules contained in the original sample before partitioning can be calculated directly from the ratio of positive to total partitions, using binomial Poisson statistics [15] .

Currently, two approaches are used in commercially available dPCR systems [15] , [16] . One approach, termed chamber digital PCR (cdPCR), relies on the partitioning of up to a few thousand individual reactions in microfluidic chambers. The second approach, called droplet digital PCR (ddPCR), combines partitioning of the PCR test into several thousands or millions of individual droplets in a water-oil emulsion, with the use of flow cytometry to count positive PCR tests.

dPCR has been adopted for a number of applications, including studies of copy number variation involving allelic discrimination or imbalance, single cell gene expression, hyper-methylation, detection of low copy number nucleic acid targets (reviewed [6] , [17] , [18] ) and of point mutations. Recently, a cdPCR commercial system has been demonstrated that enables suitable metrological performance for the certification of the copy number ratio of reference materials used in GMO testing [11] , [19] . Several advantages are proposed for the use of dPCR instead of qPCR in routine GMO testing: 1) it enables absolute target copy number to be detected and avoids the amplification efficiency bias observed with qPCR [11] , [19] , 2) it overcomes dependence on the availability of references or standards [18] , 3) it provides data with the high precision and confidence necessary for metrological use [11] , [19] , 4) it provides more accurate data at low target copy numbers than qPCR [20] , allowing quantification of low GMO content, and 5), because of its tolerance to inhibitors as an end-point measurement, it can reduce the biases linked to matrix type often observed with qPCR [18] . However, the application of cdPCR is limited by two important factors: the small dynamic range it offers (2–3 logs) and its relatively high price.

Given the larger number of replicates allowed by ddPCR than by cdPCR and the lower price per sample of the former, it has been envisaged that ddPCR could allow better precision [16] , confidence and easier adoption of digital PCR technology in laboratories for daily analysis, all at lower cost per sample [15] . The aim of this study was therefore to evaluate the application of ddPCR for quantitative analysis in food and feed samples. Taking GMO testing as a concrete example, ddPCR key performance parameters, using the QX100 droplet system (Bio-Rad, Pleasanton, CA), were compared with current qPCR performance and with the recently studied performance of cdPCR [11] , [18] . Linearity of response, absolute limits of detection and quantification, repeatability over the dynamic range of the ddPCR endogene and transgene assays were assessed. The applicability of ddPCR with different sample matrices and the practicability of use for routine GMO testing were also evaluated. The results obtained should be applicable to other fields where quantitative testing in food and feed samples is required.

Materials and Methods

Test material.

Several MON-ØØ81Ø-6 (MON810) maize seed powder based, certified reference materials (CRM) were purchased from the EU Joint Research Centre, IRMM (Institute for Reference Materials and Measurements, Geel, Belgium). All these CRMs have certified mass/mass (m/m) GM maize/wild-type maize material ratios. Some of them are also certified for the copy/copy (cp/cp) transgene/endogene ratio (see Appendix S1 and Table S1 ).

Other samples containing the MON810 maize event, and previously assayed by qPCR, were also used in this study. Finally, a limited specificity study was conducted on two samples containing either wild-type maize, or DNA from a milk sample without maize (see Appendix S1 and Table S1 ).

DNA extraction

DNA was extracted and purified from 200 mg of starting material for all samples using the NucleoSpin Food kit (Macherey-Nagel GmbH & Co. KG, Düren, Germany). In parallel, DNA from sample G147/08 was also extracted and purified according to a modified CTAB method (see Appendix S1 ) [21] .

Dilutions of the stock extracted DNA solutions were made with nuclease- and protease-free water (Sigma-Aldrich Chemie Gmbh, Munich, Germany), using pipettes calibrated with a SAG285 precision weighing module (Mettler-Toledo d.o.o., Ljubljana, Slovenia). All samples were stored at −20°C.

Enzymatic restriction of genomic DNA

Enzymatic digestion of MON810 genomic DNA (gDNA) with Taq I (New England Biolabs GmbH, Frankfurt am Main, Germany) was performed as described (see Appendix S1 ) [19] . 6 µL of digested gDNA were analyzed on a 1% agarose gel to confirm complete digestion.

qPCR reactions and data analysis

The hmg gene was used as the endogenous control gene for maize. A unique, single copy DNA integration-border region of the genomic sequence and the inserted sequence element originating from CaMV (35S promoter) were used for specific detection and quantification of the MON810 event. Probe and primer nucleotide sequences were the same as in the inter-laboratory validated protocol [22] but the TAMRA quencher in the probes was replaced by the Black Hole Quencher 1 (BHQ-1). The same primers and probes were used for both qPCR and ddPCR experiments (see Appendix S1 and Table S2 ).

MON810 content was determined by qPCR, using relative quantification according to the standard curve approach. Standard curves were prepared from five serial dilutions of the copy/copy ratio certified reference material ERM-BF413gk (starting from approximately 100 ng to 1 ng DNA per reaction) and used in two replicates. For each sample, the quantification was done based on two replicates of three dilutions. Results of quantification performed with CRM certified for transgene/endogene copy ratio were expressed as percentages of the copy/copy ratio.

Droplet Digital PCR reactions and data analysis

Duplex ddPCR reaction mixes were prepared as follows. 10 µL of 2× ddPCR Master Mix (Bio-Rad, Pleasanton, CA) and 1 µL of each primer (final concentration of 300 nM) and probe (final concentration of 180 nM) were mixed, and 4 µL of DNA template added. For singleplex reactions, 3 µL of nuclease- and protease-free water (Sigma-Aldrich Chemie Gmbh, Munich, Germany) were added to complete a 20 µL reaction volume. Final primer and probe concentrations (purchased at Eurofins MWG Operon, Ebersberg, Germany) in ddPCR mixes were identical to the qPCR conditions used in this study, and to those used in the previously described chamber digital PCR (cdPCR) conditions [11] (see Appendix S1 and Table S2 ).

ddPCR workflow and data analysis were performed as described (see Appendix S1 ) [15] .

Determination of ddPCR key performance parameters

Comparison of singleplex and duplex reactions..

The ddPCR duplex assay was evaluated using three 8-well cartridges containing the singleplex hmg , the singleplex MON810 and the duplex ddPCR assay respectively. In each cartridge, one well was filled with a non template control (NTC) ddPCR mix, while the seven other wells contained ddPCR mixes with DNA extracted from the ERM-BF413ek CRM (average of 46,571 hmg copies and 324 MON810 copies). Droplets were generated for each individual cartridge, and those droplets containing the PCR mixes of the three cartridges were transferred onto a single PCR plate for amplification followed by droplet count.

Dynamic range, repeatability, limits of detection and quantification.

A dilution series was prepared with MON810 maize DNA extracted from the ERM-BF413gk CRM. DNA quantification in the initial MON810 maize DNA solution was estimated by qPCR as described [23] . The dilution series consisted of 14 solutions containing from approximately 118000 to 0.02 copies of hmg , and from 4300 to 0.0008 copies of MON810 per 20 µL, respectively). Five replicates of the dilution series and of a non template control (NTC) were measured by ddPCR. For qPCR, measurements were made in duplicate. Linearity over the dynamic range was determined by the coefficient of correlation R 2 , calculated on the average of the target copy numbers measured in the replicated dilution series for both qPCR and ddPCR. Repeatability over the dynamic range was determined by the coefficient of variation (cv) of the measured target copy number or of the MON810 content between the replicates of the dilution series. The absolute limit of quantification (aLOQ) and absolute limit of detection (aLOD) for qPCR and ddPCR were determined on these experimental results.

An additional set of experiments was performed to establish repeatability between different emulsification runs. Intra- and inter-cartridge (ddPCR 8 well chips) repeatability was determined on five independent series consisting of seven replicates of the ERM-BF413ek (approximately 100 ng and an average of 46571 hmg copies and 324 copies of MON810 per 20 µl reaction) and one NTC. Four series were prepared by two operators and droplet amplification reactions were performed simultaneously on the same 96-well plate. The fifth series was prepared by one operator on a second day and ddPCR reactions were performed on another 96-well plate. A total of 35 replicate positive ddPCR results were then analyzed.

Specificity.

The DNA extracts from samples G053/12 (approximately 6,200 copies of hmg ) and G031/12 (approximately 100 ng DNA) were tested with the duplex MON810/ hmg ddPCR assay. A total of eight replicate reactions per sample were performed (see Appendix S1 for more details).

Applicability.

Samples representative of four different maize-containing matrices from routine GMO testing were used to test the applicability: seed-powder flour, corn flakes, wheat seed-powder flour with maize contamination, and feed containing maize (see Appendix S1 and Table S1 ).

Results and Discussion

Given the limitations of qPCR for the quantification of GMO in food and feed samples, especially at low target levels and in some complex matrices, the use of ddPCR in routine GMO quantification was evaluated, following the generally accepted minimum performance requirements for analytical methods [24] , [25] .

In order to avoid biases as much as possible when comparing qPCR and ddPCR quantification, we transferred the inter-laboratory validated qPCR hmg - and MON810-specific assays to ddPCR technology with the minimum of adaptation. Therefore, apart from the mastermix and settings that are specific to the QX100 droplet system, primers and probe nucleotide sequences and concentrations, DNA concentration, and PCR thermo-profile were kept identical to those in the qPCR assays.

ddPCR can readily be set as a duplex application

Because GMO content is calculated based on the ratio of transgene/endogene quantities, it would be more practical to perform endogene–transgene duplex reactions to reduce costs. For this reason, evaluation of duplex qPCR and ddPCR assays was performed and compared to the performance of singleplex assays. The primers and probes of both the hmg and MON810 systems were mixed in the qPCR or ddPCR volumes to final concentrations equal to those in the original singleplex assays.

Evaluation of qPCR duplex systems has shown that the hmg system performed identically in duplex and singleplex qPCR reactions, while MON810 amplification was significantly affected in the duplex reactions, showing signal values approximately 5.5 Cq higher than in singleplex reactions (data not shown). An attempt to optimize the duplex qPCR assay was made by varying primers and probe concentration of both systems. However, the hmg and MON810 were affected differently under all the tested conditions, resulting in under-estimations of the MON810 content and/or loss of sensitivity (data not shown). These results are not surprising: the difficulty of multiplexing qPCR assays is well documented, including its application to GMO quantification [26] – [28] . One of the limitations is the need to choose target sequences with similar, short lengths. Another difficulty linked to GMO detection is that the event-specific targets needed for reliable and specific GMO quantification are usually the junction regions between the transgene and the host plant genome, leaving a very narrow window for design, and decreasing further the flexibility for a multiplex design. Also, the need is usually to quantify low concentrations of transgene (down to 0.1%) in a background of high endogene quantities. This asymmetry in concentration renders establishment of a qPCR duplex assay targeting both the MON810 transgene and the hmg endogene even more difficult. In the following experiments, results of only the singleplex qPCR assays were used for comparison with ddPCR assay results.

For ddPCR, no significant variation of the measured target copy number was observed between the singleplex and duplex ddPCR assays for both hmg (bias = −1.8%) and MON810 systems (bias = 3.7%). Similarly, no significant variation of the measured MON810 content was observed between the singleplex and the duplex ddPCR assays (bias = 5.8%) ( Table S3 ). Additionally, the repeatability of the duplex assay in measurements of the MON810 content appears slightly better that of the singleplex assays. From these results, it was concluded that the duplex ddPCR assay performs as well as the singleplex ddPCR assays without any additional optimization. This was further confirmed by the successful establishment of several additional duplex ddPCR assays from singleplex qPCR assays, targeting GM events or screening elements, without optimization (data not shown).

It was recently suggested that it is preferable to expose gDNA to endonuclease restriction in order to improve amplification efficiency and to increase the accuracy of GMO target copy number measurement with cdPCR [19] . gDNA endonuclease restriction for ddPCR testing was also evaluated and found unnecessary ( Table S4 ).

Digestion of DNA may be necessary for digital PCR analysis in the case of a possible linkage between targets, such as multiple copies of target physically linked on the same chromosome, or if different targets present on a same plasmid need to be quantified. In the case of GMO quantification, the target of the event-specific assay and the target chosen for endogene quantification are present as unique copies in the host plant genome and are not linked. In the case of MON810 maize, results of the two dimensional analyses of the droplet signals in digested and undigested DNA samples ( Figure S1 in Supporting Information) suggests the absence of linkage between MON810 positive droplets and hmg positive droplets, thus confirming the independence of the two targets. Further, ddPCR performance was evaluated using non-digested gDNA.

Dynamic Range, precision and limits of quantification

A recent study has estimated that the theoretical ddPCR dynamic range is 10 5 target copies, and it has been established experimentally that the dynamic range covers more than 4 orders of magnitude [15] .

The ddPCR duplex assay response was investigated over target concentrations ranging from approximately 0.02 to 118,000 hmg copies and from approximately 0.0008 to 4300 MON810 copies per 20 µL of ddPCR reaction. Due to pipetting errors, that were noted after loading the 8-well cartridges with ddPCR mixes, data from one reaction (1.4% of the total dataset) were excluded from the analysis. The average number of droplets read for each ddPCR reaction included in the data analysis was 13,606 with a standard deviation of 931 droplets (coefficient of variation cv = 6.8%).

The ddPCR response was linear over concentrations ranging from an average of 5 to 118,000 hmg copies (0.02% to 99.5% positive droplets) with a coefficient of correlation (R 2 ) of 0.9990. Similarly, the ddPCR response for MON810 was, on average, linear from 6 to 4,340 MON810 copies (R 2  = 0.9993; 0.03% to 17.9% positive droplets in average) ( Figure 1 ). This performance was similar to those of the two singleplex qPCR assays, which was linear over the same dynamic ranges (R 2 hmg  = 0.9939 and R 2 MON810 = 0.9958) (data not shown). The ddPCR linear response for the MON810/ hmg duplex assays covered a broader range than the same assays tested in cdPCR which was limited to 2–3 orders of magnitude [18] , [19] . This wider range of concentrations can be attributed to the large number of partitions available for reactions in ddPCR (13,606 droplets on average in this work) compared to the number (765) available for cdPCR test. It has already been asserted that qPCR offers a much broader dynamic range than digital PCR [16] . The dynamic range observed for ddPCR covers the whole range of target concentrations usually needed by a laboratory for routine GMO testing (0.1% to 100% transgene/endogene ratio cp/cp).

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Five replicates for each data point. Error bars represent the standard deviation between the five replicates at each target concentration.

https://doi.org/10.1371/journal.pone.0062583.g001

For individual targets and for GMO content, the coefficient of correlation R 2 obtained with ddPCR met the requirements (R 2 >0.98) set by the European Union Reference Laboratory for GM Food and Feed [25] for acceptance of a quantitative PCR-based detection method for GMO.

All samples used for determining the dynamic range came from serial dilution of a single stock MON810 maize DNA sample. At a higher concentration (118,000 hmg copies per 20 µl ddPCR mix), each droplet contained, on average, 5.9 hmg molecules, which is the upper recommended concentration for use of the droplet system (Bio-Rad, personal communication). This finding supports the fact that the duplex MON810/ hmg ddPCR assay can be used over a wide range of target concentrations to determine the MON810 content in a given sample, and that values around 115,000 copies constitute the upper range of quantification with ddPCR.

The absolute limit of quantification (aLOQ) is the lowest target copy number in a sample that can be reliably quantified with an acceptable level of precision and accuracy [25] . The aLOQ of the hmg or MON810 ddPCR systems was estimated as the lowest copy number within the dynamic range with a coefficient of variation (cv) of the measured copy number≤25% [25] . Based on this criterion, aLOQ was estimated to be around 5 copies for the hmg system, and 18 copies for the MON810 system and for the duplex ddPCR assay ( Table S5 ). As a comparison, it is usually agreed that aLOQ of qPCR assays range from 30 to 100 target copies per reaction [12] , [29] . The aLOQ of the qPCR MON810 specific method used in this study was initially estimated at 10 copies of the target MON810 sequence [22] , and at a higher range of 31–63 copies in another recent study [18] . In our laboratory, the aLOQ estimated for the qPCR assay on the same DNA is 18 copies. The aLOQ of the duplex ddPCR assay was therefore equal to or better than that estimated for the qPCR performance. Similarly, the aLOQ of the duplex ddPCR assay was also in a range similar to the aLOQ measured in cdPCR (15–56 transgene copies), assessed only on the MON810 assay [18] .

Sensitivity

The absolute limit of detection (aLOD) is the lowest target copy number in a sample that can be reliably detected, but not necessarily quantified [25] . For this study, aLOD was calculated based on experimental data obtained to determine the dynamic range. aLOD was determined as the lowest concentration level for which all five ddPCR replicates resulted in at least two positive droplets per reaction. aLOD was estimated to be five copies for the hmg system, and six copies for the MON810 system, which is suitable for routine GMO testing. The absolute sensitivity is, according to our own assessment (data not shown), lower than the one observed for the MON810 singleplex qPCR assay at around 6–18 copies, and comparable to the one observed in cdPCR [18] .

Repeatability

Intra- and inter-cartridge repeatability of the ddPCR was assessed by two different operators and over two different days for both hmg and MON810 target copy number determinations and for MON810 content determination. Less than 10% variability was observed within each of the five cartridges for the determination of hmg copies, MON810 copies, and MON810 content. Similarly, comparison of the values between the five cartridges showed low variability (cv<10%) for all the three measured parameters ( Figure 2 and Table S6 ).

MON810 content measured by ddPCR in five series of seven replicates. The aggregate represents the sum of the five series. The target certified MON810 content (0.77%) is indicated by a dotted line. Acceptance criterion for repeatability is ±25% of the target content (from 0.58% to 0.96%) represented by the dashed lines. Error bars represent the standard deviation between the replicates for each series or in the aggregate.

https://doi.org/10.1371/journal.pone.0062583.g002

The overall repeatability could also be estimated by analyzing the results of the experiment performed for aLOQ and dynamic range determination. All along the dynamic range, the cv of the determined hmg copies, MON 810 copies, and MON810 content remained below the threshold for acceptance of quantitative methods (cv<25%) ( Table S5 ).

It has already been observed with both ddPCR [15] and cdPCR [19] that the relative uncertainty in target copy number varies across the dynamic range, with higher uncertainty, and consequently higher measurement variability, as the target copy number decreases. In this study, similar variability of the measured target copy numbers ( Table S5 and Figure 1 ) and of the MON810 content was observed at lower target concentrations ( Table S5 and Figure 3 ).

MON810 content measured by ddPCR in five series of seven target concentrations. The target MON810 content (3.85%) is indicated by a dotted line. Acceptance criterion for precision is ±25% of the target content (from 2.89% to 4.81%) represented by the dashed lines. Error bars represent the standard deviation of the measured MON810% by ddPCR at each target concentration (five replicates per target concentration).

https://doi.org/10.1371/journal.pone.0062583.g003

In all experiments and for all three parameters (hmg and MON 810 copy number, MON810 content), the coefficient of variability measured at each point of the dynamic range was far below the 25% threshold set in international guidance documents for validation of GMO testing methods [24] , [25] . These experiments demonstrate that, using ddPCR, one can obtain repeatable and comparable quantitative estimates of GMO target number or content.

Trueness is defined as the closeness of agreement between the average value obtained from a series of test results and an accepted reference value [25] . Acceptance criterion for trueness is that the measured value has to be within ±25% of the accepted reference value over the whole dynamic range [24] , [25] .

To assess trueness, data generated by the experiments for dynamic range determination and for intra- and inter-cartridge repeatability performance were used. In the absence of a DNA reference material certified for absolute copy number concentration, trueness could only be assessed for the MON810 content.

In the experiment performed to determine the intra- and inter-cartridge repeatability (on CRM ERM-BF413ek), the average value of the pooled ddPCR data showed good agreement with the certified value ( Table 1 ) and, in every case, the MON810 content measured by ddPCR (within the dynamic range) was within ±25% of the certified value ( Figure 2 ). By comparison, the MON810 content measured by qPCR was close to the limit of acceptance ( Table 1 ).

https://doi.org/10.1371/journal.pone.0062583.t001

The average value of the pooled ddPCR duplex assay data at each dilution level of the dynamic range showed good agreement with the reference value of 3.85% cp/cp (ERM-BF413gk) ( Table 1 ). The MON810 content measured by qPCR was similar to that of the ddPCR value, the latter being slightly closer to the target value ( Table 1 ). Throughout the dynamic range, each individual ddPCR measurement of the MON810 content fell within ±25% of the certified value ( Figure 3 ). It is noteworthy that the deviation between the MON810 content measured by ddPCR and the reference value tended to increase with lower target copy number. Nevertheless, the MON810/hmg ddPCR duplex assay met trueness acceptance criteria throughout the whole dynamic range. Trueness was also evaluated on two additional CRMs and on samples from the ILC-EURL-GMFF proficiency program: ddPCR results showed better agreement with the target values than qPCR and were in accordance with the trueness acceptance criterion ( Table 1 ).

Specificity

The ddPCR amplicons used for this study are the same as for the qPCR singleplex assays that were subjected to inter-laboratory validation and for which specificity was thoroughly checked at this stage. Moreover, the key assay parameters (primer and probe concentration, thermal profiles) were not modified. Therefore, the specificity of the ddPCR amplicons was not thoroughly verified as it is inferred that specificity should be the same as for the qPCR singleplex assays. A limited specificity study was however conducted on two samples containing either wild-type maize, or DNA from milk sample without maize. In all cases, a false-positive rate far below 5%, which is the generally used acceptance criterion, was observed ( Table S7 ). In addition, for all experiments performed in this study, NTC resulted in no signal (no positive droplet).

Applicability

Another important factor when introducing new methods or technologies for testing GMOs in food and feed is their applicability. More specifically, their ability to perform well with different sample matrices and within a range of concentrations relevant for GMO testing has to be demonstrated [24] .

MON810 contents measured by the ddPCR duplex MON810/ hmg assay in maize seed-powder flour samples and corn flakes samples are in good accordance with the values measured with the qPCR singleplex MON810 and hmg assays ( Table 1 ).

During qPCR tests, we detected the presence of inhibition in the stock DNA solution of two samples (wheat seed-powder flour with maize contamination and maize feed), as indicated by the large differences in MON810 content (cv>25%) calculated from different sample dilutions. Consequently, diluted DNA samples were used to determine the MON810 content with qPCR. In the wheat sample, the generally used NucleoSpin Food kit (NSF) extraction protocol resulted in strong inhibition of the qPCR amplifications, and new DNA extraction following the CTAB protocol was needed. Both stock and diluted DNA solutions from the CTAB extract could be used for MON810 content determination with qPCR. The ddPCR measurements of MON810 content were in agreement with the accepted values obtained with qPCR but with a bias slightly above the acceptance limit for the wheat seed-powder flour sample ( Tables 1 and S6 ). It has to be noted that there is substantial empirical knowledge about the efficacy of DNA extraction methods related to sample matrix. GMO laboratories use adapted DNA extraction methods that in some cases may reduce inhibition during the qPCR analysis. Furthermore, inhibition is already assessed during the screening and identification phases of GMO testing, so there is no risk that substances in a DNA extract would totally inhibit the qPCR or ddPCR amplification reaction, resulting in false negatives.

Interestingly, for the DNA extracts obtained with NSF, very low differences were observed between the MON810 content determined by ddPCR in the stock (presenting inhibition with qPCR) and the diluted DNA solutions for both matrices (Table S8 in Appendix S2 ). This result suggests that the ddPCR duplex assay is more tolerant to inhibitors found in some complex food and feed matrices than the qPCR assays, as suggested earlier [18] .

In summary, the ddPCR MON810/ hmg duplex assay can be applied for routine quantification of the MON810 maize, as demonstrated on a large range of transgene content (experimentally from 0.04% to 29.6%) usually found in samples. Moreover, its use for several types of food, feed and seed matrices commonly found in routine samples has been verified.

Practicability

Before introducing a new technology in a laboratory, one has to verify its practicability for daily use [24] .

To do so, calculations were made based on the simultaneous quantification of four samples-the average number run in parallel in middle-size GMO laboratories. The quantitative analysis of four samples using hmg and MON810 singleplex qPCR assays requires a total of 96 reactions (see set up A, Table S9 in Appendix S2 ). This number of reactions is high, due mainly to the use of inter-laboratory validated singleplex methods, the need for monitor inhibition that requires additional dilutions, and the need for a standard curve. With ddPCR, the standard curve is not needed and a duplex MON810/ hmg assay with a wide dynamic range is used. Since inhibition is assessed during the screening and identification phases of GMO testing and given the demonstrated tolerance of the assay for amplification inhibition, it is not necessary to control the inhibition at the ddPCR quantification stage. Thus, a simple ddPCR testing set-up is proposed (set up B, Table S9 in Appendix S2 ) that included two replicate reactions for each test portion of the sample, in accordance with the ISO 21570:2005 standard [30] . Including NTC and quantification control reactions in the set-up, a total of 20 reactions would be necessary to reliably quantify MON810 in four samples.

Based on the experience acquired during this study and assuming the samples and mixes are already prepared, the simultaneous analysis of these four samples with ddPCR would require approximately 190 minutes. For comparison, qPCR would take 160 minutes to generate results (see Table S10 in Appendix S2 ). In terms of hands-on-time, ddPCR would require approximately 15 min less than qPCR. The main difference between the two approaches can be attributed to the time needed by the droplet reader to analyze individual droplets.

Considering the cost of reagents, consumables and labor at NIB and the above proposed set-ups for GMO testing, the quantification of a given transgene in four samples with ddPCR would cost approximately US$20.9 per sample and US$22.3 using qPCR. If more samples must be handled simultaneously, ddPCR shows even better throughput and smaller cost than qPCR (see Tables S11 and S12 in Appendix S2 ). The use of cdPCR, taking into account prices per chip or plate (from US$150 to US$400 each) [16] and using the proposed set-up for ddPCR (four runs, i.e. chips or plate per sample), would lead to a cost per sample much greater than that required for current routine detection of GMOs in most laboratories.

Quantification of routine samples using ddPCR is therefore practical and has the potential to provide better throughput and cost-effectiveness than qPCR for GMO laboratories. A MIQE checklist is made available in Appendix S3 .

The intention of this study was to demonstrate the usability of ddPCR in real-life routine diagnostics, rather than to re-investigate the recently reported metrological characteristics of this technology [15] . The applicability of ddPCR was investigated for the quantification of GMO in food, feed and seed samples. The ddPCR MON810/ hmg duplex assay presented here and implemented without optimization from the inter-laboratory validated singleplex qPCR assays, achieves a wide dynamic range close to five orders of magnitude with an upper limit of quantification of about 118,000 target copies. It also shows very good sensitivity, suitable for GMO testing. The excellent performance of the tested parameters enables the quantification of samples from different matrices, using DNA extracted with common methods without up-front DNA quantity estimation. The limits of quantification, trueness and repeatability of the duplex assay comply with international recommendations [24] , [25] and are comparable or superior to those of the inter-laboratory validated qPCR singleplex assays ( Table 2 ).

https://doi.org/10.1371/journal.pone.0062583.t002

Applicability of the technology has been verified on representative matrices found in routine samples, and on the range of GMO content usually found in routine samples and relevant to different international labeling requests. Unlike qPCR, quantification by ddPCR has been found to be insensitive to the amplification inhibition present in some DNA extracts. It is also very precise at very low levels of target content. The use of the ddPCR duplex assay in routine GMO analysis was shown to be practical, following the new test set-up proposed in this study.

It was recently discussed as to whether price is a limiting factor to the adoption of dPCR in the laboratory [16] . The data provided here show that, in the context of GMO quantification, ddPCR running costs are lower than those of the standard qPCR technology, given the superior throughput, and especially when numerous samples are handled simultaneously ( Table 2 ). Increasing the multiplexing will certainly give further, additional advantage to ddPCR in terms of cost and throughput, and could allow its use already at the screening and/or identification steps. The establishment of duplex reactions is straightforward and does not need optimization, which is also encouraging. This characteristic has the advantages of reducing the cost of analysis, and of decreasing the uncertainty linked to droplet volume variation and dilution pipetting errors [19] .

To be employed in routine testing, methods based on ddPCR shall be properly validated through ring-trials and verified during their introduction in laboratories to demonstrate their fitness for the purpose. However, the ddPCR performance demonstrated in this study on real routine samples should lead to greater confidence and easier adoption of digital PCR technology, to generating more precise data on everyday tests, and at overall better cost per sample. The demonstrated application of ddPCR for routine quantification of GMO content in food and feed samples should act as an inducement to introduce this technology in other areas where precise analytical testing is required in food and feed samples.

Supporting Information

VIC vs . FAM channel clustering plot of droplets for non-digested and Taq I digested MON810 DNA. Upper frame: Non digested DNA. Lower frame: Taq I digested DNA. Upper left quadrant: FAM ( hmg ) positive-VIC (MON810) negative droplet cluster. Upper right quadrant: FAM ( hmg ) positive-VIC (MON810) positive droplet cluster. Lower left quadrant: FAM ( hmg ) negative-VIC (MON810) negative droplet cluster. Lower right quadrant: FAM ( hmg ) negative-VIC (MON810) positive droplet cluster.

https://doi.org/10.1371/journal.pone.0062583.s001

Test material used in this study.

https://doi.org/10.1371/journal.pone.0062583.s002

Primers and probes used in this study.

https://doi.org/10.1371/journal.pone.0062583.s003

Comparison of quantification using singleplex and duplex ddPCR assays.

https://doi.org/10.1371/journal.pone.0062583.s004

Comparison of duplex ddPCR quantification on digested and non-digested genomic DNA.

https://doi.org/10.1371/journal.pone.0062583.s005

Results from the dilution series used for the dynamic range, the aLOD and aLOQ determination, and the overall repeatability.

https://doi.org/10.1371/journal.pone.0062583.s006

Inter- and intra-cartridge repeatability.

https://doi.org/10.1371/journal.pone.0062583.s007

False-positive rates observed with ddPCR.

https://doi.org/10.1371/journal.pone.0062583.s008

Appendix S1.

Supporting material and methods.

https://doi.org/10.1371/journal.pone.0062583.s009

Appendix S2.

Table S8. Inhibition effect on MON810 quantification in qPCR and ddPCR. Table S9. Set-up and number of reactions needed for simultaneous quantification of four samples with qPCR and ddPCR. Table S10. Time needed for quantification with qPCR and ddPCR. Table S11. Set-up and number of reactions needed for simultaneous quantification of 23 samples with qPCR and ddPCR. Table S12. Set-up and number of reactions needed for quantification with qPCR and ddPCR (full 96 well-plate).

https://doi.org/10.1371/journal.pone.0062583.s010

Appendix S3.

MIQE checklist.

https://doi.org/10.1371/journal.pone.0062583.s011

Acknowledgments

We thank Prof. Dr. Roger Pain for reviewing the manuscript. This work was co-financed by the Slovenian Ministry of Economic Development and Technology, Metrology Institute (MIRS) in the frame of the contract no. 640118/2008/67 on performing activities as holder of the national standard MIRS/NIB/FITO for the amount of substance in food of plant origin.

Author Contributions

Conceived and designed the experiments: DM DS. Performed the experiments: DM DS. Wrote the paper: DM MM KG JZ.

• View Article
• Google Scholar
• 10. Weighardt F (2006) Quantitative PCR for the detection of GMOs. In: Querci M, Jermini.M, Van den Eede G, editors. Training course on the Analysis of Food Samples for the Presence of Genetically Modified Organisms. Luxembourg, Luxembourg: Luxembourg: Office for Official Publications of the European Communities.pp. 1–19.
• 17. Devonshire AS, Sanders R, Wilkes TM, Taylor MS, Foy CA et al.. (2012) Application of next generation qPCR and sequencing platforms to mRNA biomarker analysis. Methods. In press.
• 21. Somma M (2006) Extraction and purification of DNA. In: Querci M, Jermini.M, Van den Eede G, editors. Training Course on the Analysis of Food Samples for the Presence of Genetically Modified Organisms-User Manual.Luxembourg: Office for Official Publications of the European Communities.
• 22. European Union Reference Laboratory for GM Food and Feed (2006) CRL assessment on the validation of an event-specific method for the relative quantitation of maize line MON 810 DNA using real-time PCR as carried out by Federal Institute for Risk Assessment (BfR). Available: http://gmo-crl.jrc.ec.europa.eu/summaries/Mon810_validation_report.pdf . Accessed 29-1-2013.
• 24. Codex Committee On Methods Of Analysis And Sampling (2010) Guidelines On Performance Criteria And Validation Of Methods For Detection, Identification And Quantification Of Specific DNA Sequences And Specific Proteins In Foods. Available: http://www.codexalimentarius.org/download/standards/11667/CXG_074e.pdf . Accessed 29-1-2013.
• 25. European Union Reference Laboratory for GM Food and Feed (2008 October) Definition of minimum Performance requirements for analytical methods of GMO testing. Available: http://gmo-crl.jrc.ec.europa.eu/doc/Min_Perf_Requirements_Analytical_methods.pdf . Accessed 29-1-2 2013.
• 30. International Organization for Standardization (2005) ISO 21570:2005Foodstuffs–Methods of analysis for the detection of genetically modified organisms and derived products–Quantitative nucleic acid based methods. Geneva, Switzerland: International Organization for Standardization.

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A Qualitative Study of Factors Influencing Food Choices and Food Sources Among Adults Aged 50 Years and Older During the Coronavirus Disease 2019 Pandemic

Patrick j. brady.

1 Division of Epidemiology and Community Health, University of Minnesota School of Public Health, Minneapolis, Minnesota

Natoshia M. Askelson

2 Department of Community and Behavioral Health, University of Iowa College of Public Health, Iowa City, Iowa

3 University of Iowa Public Policy Center, Iowa City, Iowa

Helaina Thompson

Sarah kersten, haley hopkins.

4 Iowa Department of Public Health, Des Moines, Iowa

Sato Ashida

Faryle nothwehr, brandi janssen.

5 Department of Occupational and Environmental Health, University of Iowa College of Public Health, Iowa City, Iowa

David Frisvold

6 Department of Economics, Tippie College of Business, University of Iowa, Iowa City, Iowa

The coronavirus disease 2019 pandemic affected food availability and accessibility for many older adults, especially those experiencing food insecurity. Food citizenship is a theoretical framework that encourages the use of alternate over industrial food sources and can characterize where foods are acquired and how food choices are made.

The purpose of this study is to explore how Iowans aged 50 years and older made choices about what foods to acquire and where to acquire foods during the coronavirus disease 2019 pandemic using food citizenship as a theoretical framework.

We used in-depth interviews with Iowans aged 50 years and older (N = 60).

Participants

We recruited respondents through Area Agencies on Aging, food banks, and food pantries. Individuals who contacted the research team, were aged 50 years and older, and spoke English were eligible. Half of the sample screened as food insecure.

Statistical analysis

We conducted a thematic analysis to identify recurring themes.

Food costs, personal preferences, and the healthfulness of food were cited as the most influential factors. Respondents said that the pandemic had not changed how they make choices, but increased prices had made costs more salient. Respondents primarily got their food from industrial food retailers, government programs, or food pantries. More than half of the respondents also acquired food from an alternate food source, such as a farmers’ market. Reasons for not using alternate food sources included cost and transportation barriers.

Conclusions

It is essential to ensure that older adults have access to affordable, healthy foods, especially during crises such as the coronavirus disease 2019 pandemic. Alternate food sources provided supplementary, healthy food for many respondents, but there are opportunities to expand the use of these food sources. Incentivizing the use of alternate food sources through government programs and connecting the emergency food system to local producers could increase the consumption of healthy food.

Research Snapshot

Research Question: How has the coronavirus disease 2019 pandemic influenced the food choices and food sources of adults aged 50 years and older?

Key Findings: Food prices, personal preferences, and a food’s healthfulness were the primary factors driving choices. Although respondents said the pandemic had not changed the factors motivating their choices, they mentioned that food prices had become particularly relevant. Similarly, food sources did not change, and respondents used retailers in the industrial food system, government programs, or food pantries as their primary food source. Many respondents supplemented their diets with foods from the alternate food system, mainly farmers’ markets.

Older adults who experience food insecurity generally consume a poor diet 1 , 2 , 3 , 4 , 5 and are at increased risk for malnutrition. 4 , 6 Older adults who experience food insecurity also have an increased chronic disease burden compared with those who are food secure. 7 Barriers such as poor access to 8 , 9 and high costs of 10 , 11 healthy and sustainably grown food make it difficult to consume a heath-promoting diet. Because of this, government programs and emergency food services offer support to individuals experiencing food insecurity, 12 , 13 , 14 but these services may not be available to all who need them and are underutilized by older adults. 15 , 16 , 17

Food citizenship is a food movement and theoretical framework that has been used to address poor diet and food insecurity by enabling access to healthy, sustainably produced foods. 18 , 19 , 20 , 21 Whereas the food citizenship framework has been more fully described elsewhere, 21 rights and responsibilities are key concepts within food citizenship that should be considered here. Food citizenship is based on the fundamental and inalienable right to access healthy, nutritious foods produced in a just and sustainable way. 21 Based on this right, all members of the food system have responsibilities around food production, distribution, procurement, preparation, and consumption behaviors. 21 For food producers, distributors, and retailers, there is a responsibility to provide whole and truthful information about their foods and to increase equitable access to healthy, nutritious foods. 21 For individual consumers, food citizenship states that they have a responsibility to consider how their food-related behaviors and choices influence themselves and others. 21 By enabling all to practice the right to food and satisfying these responsibilities, we can improve our food system as well as individual dietary intake, health, and well-being.

It is important to reflect on why older adults choose the foods they do. Older adults have been shown to make food choices based on personal beliefs and preference as well as outside factors such as costs, 22 and these choices differ based on socioeconomic status 23 or food security status. 24 Furthermore, changing physiological and social circumstances associated with aging influence food choices. 25 Although food choices among older adults have been studied, 22 , 23 , 24 , 25 they have not been examined using food citizenship, which emphasizes a wide range of responsibilities associated with food choices that often were not considered in previous studies.

One manner in which older adults could engage with their responsibilities around food is utilizing the alternate food system. Alternate food systems often focus on local production and consumption and include food sources outside the industrial food systems such as farmers’ markets, gardens, or community-supported agriculture. This is in contrast to industrial food systems, which are those that are characterized by large-scale operations, often featuring vertical integration and concentration of power, and where the focus is efficiency and increasing profit. 26 , 27 In addition, the emergency food system exists as a safety net to provide food to those in need at no cost, and consists of meal sites, food pantries, food banks, and food rescue programs. 14 These systems are not independent; that is, a producer may sell food directly to consumers as part of the alternate food system but also have products in a grocery store as part of the industrial food system. Furthermore, emergency food systems rely on donations from large, multinational corporations but also receive food from local producers. However, by characterizing different food sources based on their focus and practices (eg, small-scale, local productions vs multinational, vertically integrated production), researchers can broadly understand from what type of institutions or organizations individuals are acquiring their foods. It is important to examine why older adults do or do not use certain food sources and understand what barriers may exist for individuals with food security, such as food costs or transportation. 28 , 29 This is especially true given the increased rates of food insecurity during the coronavirus disease 2019 (COVID-19) pandemic. 30 , 31 , 32

During the COVID-19 pandemic, many barriers to consuming healthy food items have been exacerbated, but little is known about how these barriers influenced food choices or where older adults acquired food. When there are disruptions to the food supply chain or changes in factors that influence food choices, such as price, individuals may respond by seeking to acquire food from new or different sources. This study aimed to answer two general research questions about adults who were approaching older age and older adults. First, we were interested in understanding what factors influenced food choices during the COVID-19 pandemic among adults aged 50 years and older and how these factors align with food citizenship. Second, we were interested in how the COVID-19 pandemic influenced where adults aged 50 years and older get their food and how their food sources align with food citizenship.

This study was part of a larger project conducted in collaboration with the Iowa Department of Public Health’s Supplemental Nutrition Program Education (SNAP-Ed) program and the Iowa Food Bank Association. The goal of the larger project was to increase produce consumption among older Iowans with food insecurity through food bank services.

Study Population, Recruitment, and Sample Size

The population was English-speaking adults aged 50 years and older who were living in Iowa. Iowa’s overall demographic profile can be found elsewhere. 33 We initially chose our population as individuals aged 50 years and older to capture the perspectives of those in near-retirement age as well as older adults, who we define based on the age-eligibility guidelines for Older American Act Nutrition Programs (ie, those older than age 60 years). Although we originally intended to use quota sampling to facilitate comparisons based on age, gender, and rural status, due to limitations introduced by the COVID-19 pandemic, we used a convenience sample. We chose to do this to collect timely data from as many individuals as possible during the data collection period so our results could potentially inform actions aimed to lessen food hardship among Iowans aged 50 years and older. Recruitment occurred between June and November 2020. During our first round of recruitment, we distributed a flyer through the congregate or home-delivered meal programs at four Area Agencies on Aging (AAAs) in Iowa. These four agencies cover 61 of Iowa’s 99 counties. Some individuals who did not participate in the AAA meal programs contacted us after hearing about the study through word of mouth. For the second round of recruitment, the flyer was distributed by three food banks to their partner agencies and mobile pantry programs. The flyer included details about the study and asked interested parties to contact the research team either by telephone or e-mail. This study was approved by the institutional review board at the University of Iowa.

Because this was a preliminary, qualitative study, the number of participants was guided by the aims of the study and the responses of the participants, specifically, the collection of new, meaningful information throughout the data collection. After conducting 46 interviews in our first round of recruitment, we had reached saturation. 34 , 35 However, we did not have many respondents from the 50- to 59-year old age group, from historically marginalized populations, from the northeastern and western regions of the state, and from those living in more rural areas. From the second round of recruitment, we conducted an additional 14 interviews for a total of 60 interviews. We had participants from 15 counties of which six are considered metropolitan and nine of which are considered nonmetropolitan according to 2013 Rural-Urban Continuum Codes. 36 Each of the state’s four congressional districts (which correspond to the Northeast, Northwest, Southeast, and Southwest of the state) were represented in the sample. Although the second round of recruited participants added diversity to our sample, there were no major differences in the responses between the rounds.

Data Collection Tools

We used in-depth interviews to gather the thoughts, experiences, and perspectives of adults aged 50 years and older. We developed an interview guide to explore where respondents were obtaining their food, why they were obtaining food from those places, and how they chose which foods to get (see Figure 1 , available at www.jandonline.org ). Following 10 pilot interviews, the interview guide was updated by reordering the sequence of the questions, eliminating original stems and replacing them with probes, and rewording questions to be more specific. An example of rewording a question was asking about how choices were made for selecting specific types of food vs generally (eg, “Last time you got fruit, how did you choose which fruits you were going to get?” vs “How do you make choices about what food you get?”). The interview guide asks about two general time periods, before the COVID-19 pandemic began and since the pandemic started because we were interested in exploring changes in these topics influenced by the pandemic.

We also collected demographic information (age, gender, Hispanic ethnicity, race, educational attainment, and monthly income), their living situation (the type of housing, whether they rent or own, and if they lived alone), and the use of food assistance programs and services (eg, SNAP, Older Americans Act nutrition programs, and food pantries/banks). We used a two-item food insecurity screening questionnaire 37 that has been validated in the general US population and for older adults 38 to identify individuals who had experienced food insecurity during the past year.

Data Collection and Management

The data collection team consisted of three interviewers (authors P.J.B., H.T., and S.K.) trained in conducting interviews with older adults. After a potential study participant contacted us to schedule an interview, we verified they were older than age 50 years, obtained verbal consent, and either carried out the interview or scheduled it for a later date. The first 10 interviews served as a pilot and were completed by the first author. Because the changes to the interview guide were minor, the 10 interviews used as a pilot were included in the analysis. Following the pilot interviews, the remaining interviews were split between the three research team members. All interviews were completed over the telephone and were audiorecorded. Participants were compensated with a $25 gift card following the interview. A typical interview lasted approximately 30 minutes, but some lasted longer than an hour. The interviews occurred between June and November 2020. The audio files were transcribed by a third-party transcription service. In the limited cases where participants did not want to be audiorecorded (n = 3) or the audio files were corrupted (n = 1), detailed notes were used instead of an interview transcript. We uploaded the de-identified and cleaned transcripts to the Dedoose software program. 39

Analytic Approach

We used a thematic analysis approach to code each transcript. 40 We developed a codebook using a deductive approach based on the aim of this study, the research questions, and the initial reading of the transcripts. After developing a draft codebook, each member of the research team coded three interviews independently. We then combined the coded interviews and met to discuss code applications and to refine the draft codebook. We finalized the codebook by reaching a consensus on code definitions and rules for code applications. Each member of the research team then independently coded a selection of the remaining transcripts. We reviewed the coded transcripts, met to discuss the code applications, and reached a final consensus. Following the initial coding, the first author categorized the factors that influence food choices as factors outside individual control (eg, food prices or food availability), factors related to responsibilities for themselves (eg, personal health or taste preferences), and factors related to responsibilities to others (eg, supporting farmers or environmental sustainability). We then compared responses between respondents who were food secure and food insecure to identify group differences. We had originally intended to compare emergent themes between adults in each age group to explore differences in experiences by age category (50 to 59 vs 60 to 69 vs ≥70 years) in addition to comparisons between respondents reporting food security and food insecurity, but this was not possible given the number of participants in the age 50 to 59 years category. We also did not observe differences in emergent themes between respondents in the age 60 to 69 years and age 70 years and older groups. Therefore, we do not discuss differences in emergent themes between age categories.

Demographic Characteristics

Respondents’ demographic characteristics are shown in the Table . The sample was mostly older, women, and White. We did not have any respondents who identified as Hispanic or Latino. The vast majority of the respondents were not employed and had completed a high school education or equivalent. Most of the respondents earned <$1,500 per month, lived alone, rented their residence, and lived in an apartment. Half of the sample screened as experiencing food insecurity in the past year. Half the respondents were participating in SNAP at the time of the interview and about two-thirds of the respondents described using a food pantry or food bank during the pandemic.

Demographic characteristics of respondents (N = 60) in an interview study about food-related behaviors and factors contributing to food choices among Iowans aged 50 years and older conducted between June and November 2020

Food Choices during the COVID-19 Pandemic

Overall themes and quotes regarding food choices during the COVID-19 pandemic are shown in Figure 2 and discussed in more detail below. The majority of respondents cited food costs, personal preferences, and health concerns or the food’s healthfulness as the major factors driving food decisions. The respondents frequently discussed balancing these factors; respondents often said they considered their preferences, health, and outside factors such as price together when selecting foods. The pandemic did not seem to introduce new influences on the respondents’ dietary choices, except when they were able to acquire more expensive food items that they would normally not purchase due to pandemic-related efforts to address unmet food needs. Some respondents highlighted factors such as price and healthfulness of foods that have become more relevant. For example, due to increased health risks due to the pandemic, some respondents described trying to eat healthier to strengthen their immune system. Food insecure respondents described prices as the major factor driving their food choices more often and more intensely compared with those who did not experience food insecurity. Respondents with food security were more likely to cite personal preferences. There were no other evident differences in responses based on food security status.

Figure 2

Themes related to food choices emerging from an interview study about food-related behaviors and factors contributing to food choices among Iowans aged 50 years and older conducted between June and November 2020.

Respondents most often discussed that food prices ultimately determined their food choices, regardless of the source of food or other factors they may consider ( Figure 2 ; Theme: Food costs). The respondents noted that this was true prior to the pandemic, but that increased food prices during the pandemic had changed what foods they chose or the quantity of foods they purchased ( Figure 2 ; Theme: Food costs). Respondents often noted that foods from alternate food sources were more expensive than at industrial retailers, but respondents also considered these foods to be healthier ( Figure 2 ; Themes: Food costs and Support for local food). Because price was often the major factor driving food choices and a barrier to selecting certain foods, there is an unmet responsibility under food citizenship in ensuring individual’s food choices are not constrained by systemic factors. Other outside factors influencing food choices were not necessarily framed in reference to outside responsibilities that one would consider as a food citizen even when they were emphasized as important by the respondents. One example of this is seasonality. Although some respondents mentioned picking produce according to the season, it was due to price and food quality and not a responsibility toward environmental sustainability ( Figure 2 ; Theme: Food costs, Subtheme: Seasonality), which would be an important concern under food citizenship. In addition, many of the respondents discussed choosing foods for their shelf life or to prevent food waste, but this was out of economic concerns ( Figure 2 ; Theme: Food costs, Subtheme: Shelf-life).

Many respondents reported that their food choices were influenced by the foods they like to consume and how those foods would influence their health ( Figure 2 ; Themes: Healthfulness and Personal Preferences). Because autonomy of choice is a key concept in food citizenship, it is important for individuals to have access to the foods they would like to consume. Despite this, many respondents experienced cost barriers to purchasing foods they would prefer to eat, such as with foods that were perceived to be healthier ( Figure 2 ; Theme: Food costs). Respondents who discussed the health benefits of certain foods influencing their choices cited both chronic conditions (eg, low sodium for hypertension) and to support an overall healthy lifestyle ( Figure 2 ; Theme: Healthfulness). Food citizenship emphasizes a responsibility to one’s own health, therefore considering individual health in food choices is consistent with food citizenship.

A few respondents mentioned the availability of food items as a challenge ( Figure 2 ; Theme: Availability and Accessibility), but most of the respondents did not describe foods being out of stock or unavailable. In fact, a number of respondents described increased accessibility since the pandemic started, due to increased SNAP benefits, participation in other government programs, or receiving food from a food pantry or food bank ( Figure 2 ; Theme: Availability and Accessibility). Despite the increased accessibility of foods and the ability to choose a wider variety of foods, respondents focused on maximizing their individual benefit, whether that was around price, taste, or health, rather than considering how their food choices influence others or larger systems.

None of the respondents cited outside factors (eg, for environmental sustainability, supporting local producers, other economic benefits to the community) as their primary reason for purchasing food items, but a few respondents did specifically mention these as influencing their food choices. Some respondent mentioned supporting their local food economy ( Figure 2 ; Theme: Support for local food), which is integral to food citizenship. They also discussed how the decision to acquire food from alternate food sources and support local producers was influenced both by increased costs compared to industrial food retailers and responsibilities for protecting individual health through healthier dietary intake ( Figure 2 ; Theme: Support for local food).

Food Sources during the COVID-19 Pandemic

Overall themes and quotes regarding food sources during the COVID-19 pandemic are shown in Figure 3 and discussed in more detail below. All respondents used an industrial food retailer (ie, grocery store, supermarket, or dollar store), government program (in this case, the Commodities Supplemental Food Program or Older Americans Act Nutrition Services), or a food pantry/bank as their primary source of food ( Figure 3 ; Theme: Main food sources). These were often the places that the respondent had acquired food from before the pandemic, but in some cases, respondents moved from one grocery or super store to another for various reasons such as price, offering delivery services, or out of concerns for safety related to COVID-19 ( Figure 3 ; Themes: Main food sources and COVID–19-related barriers to accessing food sources). A few respondents indicated that retailers in the industrial food system were not enforcing safety precautions such as social distancing and mask wearing while others were implementing these precautions ( Figure 3 ; Theme: COVID–19-related barriers to accessing food sources).

Figure 3

Themes related to food sources and use of alternate food sources emerging from an interview study about food-related behaviors and factors contributing to food choices among Iowans aged 50 years and older conducted between June and November 2020. a COVID = coronavirus disease 2019.

More than half of respondents also acquired food from an alternate food source, but this often was not out of a desire to support the local food economy, but instead due to personal preferences ( Figure 3 ; Theme: Alternate food sources) and having financial support ( Figure 3 ; Theme: Alternate food sources, Subtheme: Financial support). The majority of respondents using alternate food sources discussed using farmers’ markets, while a few said that they had their own gardens. The respondents who shopped at farmers’ markets cited the foods’ taste and health profile as reasons for shopping there ( Figure 3 ; Theme: Alternate food sources). In addition, many who attended the farmers’ markets received Senior Farmers’ Nutrition Program (SFMNP) vouchers from their AAA, which reduced price barriers to accessing these food sources ( Figure 3 ; Theme: Alternate food sources, Subtheme: Financial support). Some stated that they would spend their own money at farmers’ markets, whereas others would only use the SFMNP vouchers. Some respondents also started growing their own food in response to the pandemic, whether that was due to worries over food shortages or increasing food prices ( Figure 3 ; Theme: Alternate food sources).

The use of alternate food sources did not differ between respondents who did and did not experience food insecurity, but rather depended on the availability and accessibility of these food sources, financial support to purchase foods from local vendors, and personal preference. Even though there did not appear to be a major factor influencing the use of alternate food sources, the prices of foods were cited by some respondents who were experiencing food insecurity as a reason to not shop at alternate food sources ( Figure 3 ; Theme: Alternate food sources, Subtheme: Accessibility of alternate food sources). In addition, some respondents reported transportation barriers preventing them from using farmers markets ( Figure 2 ; Theme: Alternate food sources, Subtheme: Accessibility of alternate food sources). Similar to retailers in the industrial food system, a few respondents indicated that farmers’ markets were not enforcing safety precautions while others were ( Figure 3 ; Theme: COVID–19-related barriers to accessing food sources). These barriers indicate that there are unfulfilled responsibilities around ensuring alternate food sources are accessible for all. Some respondents who use food pantries discussed how these emergency food providers connected them with locally produced foods ( Figure 3 ; Theme: Alternate food sources, Subtheme: Accessibility of alternate food sources), increasing access to food from the alternate food system.

When examining where the respondents got their food and why through the lens of food citizenship, it is clear these respondents were not actively participating as food citizens, but often due to structural barriers such as physical and financial access. The majority of the respondents who used alternate food sources stated that they only used them because they had financial support to do so. There were a few examples of individuals being connected to local food sources through new programs as a result of the pandemic, which indicates that local producers and emergency food providers were acting on their responsibility to provide access to healthy, nutritious food to all. It was also clear that some retailers, both in the industrial and alternate food systems, were not acting responsibly in regard to the safety of their customers and precautions around the spread of COVID-19. Overall, it does not appear that the respondents moved toward acquiring food from alternate food sources in response to the pandemic. Despite this, farmers’ markets, gardens, and locally produced foods received through the emergency food system were an important source of healthy foods during this time.

This study explored the factors leading to food choices and food sources among Iowans aged 50 years and older during the COVID-19 pandemic using food citizenship as a theoretical framework. These results show that factors such as personal preference, health, and price were consistent determinants of food choices before and during the pandemic and that food acquisition behaviors did not change substantially. Although the pandemic did not cause the issues the respondents described, it exacerbated already existing vulnerabilities regarding food access and security and highlighted various structural and societal barriers to consuming healthy and preferable foods. In addition, the responses to this crisis, such as strengthening SNAP and expanding access to emergency food resources, provide insight on potential paths forward to improve food security and access. It will be critical for practitioners in nutrition, dietetics, public health, and public policy to learn from these times to build a foundation where all people and communities have access to healthy, preferable food.

Food choices among respondents were primarily based on material and personal factors, which is consistent with previous literature, 10 , 11 , 24 , 25 but largely did not consider wider social responsibilities, such as to consume ethically produced and distributed food. Food citizenship is defined by a right to access healthy nutritious foods and a responsibility to promote justice and equity through individual and collective actions. 21 These results show that the actions prescribed under this movement may not be feasible for adults aged 50 years and older given unmet societal responsibilities creating barriers to accessing healthy, nutritious foods produced in a just manner.

Whereas respondents’ sources of food remained fairly consistent during the COVID-19 pandemic, some respondents described increased barriers to accessing healthy food due to increase food prices, whereas others said responses to the pandemic, like increasing SNAP benefits, improved their access. It is clear from these results that Iowans aged 50 years and older, especially those who were experiencing food insecurity, were not actively acting as food citizens when making their food choices. Food prices and personal preference were most often described as what motivated food choices, which agrees with previous qualitative research identifying similar factors, such as taste, monetary, and health considerations. 24 The respondents material situation and personal needs may have been more pressing than loftier motivations described under food citizenship because no respondents cited responsibilities to others or the greater good as their primary reason for choosing food. Despite this, some respondents noted these responsibilities as an additional consideration, indicating that certain responsibilities described under food citizenship may be more salient in this population in the case that current factors such as price that overwhelmingly influenced food choices were addressed. Conceivably, these more immediate needs will have to be met to enable older adults to consider wider, societal obligations they have when choosing their foods, especially in the context of a global pandemic. Dietitians, other food and nutrition practitioners, and health care professionals working in clinical and community settings should aim to address these immediate needs by connecting patients experiencing food insecurity with resources such SNAP and emergency food providers, including aiding in navigating the administrative hurdles to accessing these services.

Food prices are a major influence on food choices and a barrier to healthy eating for food insecure individuals, 10 , 11 and the respondents indicated that rising food prices were a concern. Although COVID-19 may not have been the sole reason for changes in food prices, the respondents here perceived it as the reason for changes in food prices and often discussed how higher food prices had influenced their food choices during this time, particularly for meat and produce. Respondents also described panic buying resulting in less availability of low-cost items, forcing them to choose more expensive options. The respondents described this effect being blunted or eliminated in cases where the increase in SNAP benefits countered the increase in cost. It was clear from the respondents that the increase SNAP benefits were viewed as immensely beneficial and that previous benefits levels were inadequate to support a healthy diet. This study provides initial evidence suggesting that some of the policies enacted in response to the pandemic were effective in improving food security and dietary intake. There is limited information on the influence of the pandemic and accompanying food assistance and economic supports on diet quality of older adults. These results indicate that at least for some, dietary intake may have improved due to policy and nongovernmental responses to the pandemic, and future research is needed to quantify the influence of these policy interventions on food security and dietary intake.

Respondents’ use of multiple food sources agrees with the previous literature showing that households rely on a number of sources for food, including grocery stores, supermarkets, convenience stores, and restaurants, 41 , 42 and that spending at alternate food sources is much lower than at other sources. 43 Alternate food sources provided access to fresh produce, which was perceived by the respondents as healthier and of higher quality compared with foods from industrial food retailers. These perceptions are supported by previous research on consumer perceptions of food from farmers’ markets. 44 , 45 , 46 They also offered the opportunity to obtain foods in season, which were noted as an important factor in food choices by respondents in this study. In previous studies, receiving food from alternate food sources was beneficial to older adults’ fruit and vegetable consumption 47 and diet quality, 48 and because acquiring foods from alternate food sources also has broader societal benefits, 49 facilitating the use of alternate food sources is a vital strategy to improve our food system. Nutrition and dietetics practitioners can facilitative the transition toward consuming more foods from the alternate food system by linking clinical or community services to alternate food systems. For example, in SNAP-Ed nutrition education and produce prescription programs or by connecting patients to resources that increase accessibility to these foods, such as emergency food providers who work with local producers and the SFMNP.

In a few cases, respondents were connected to local food sources through initiatives in the emergency food system. Previous interventions addressing food insecurity using food citizenship have aimed to distribute locally produced foods to low-income individuals through government food programs 19 and nonprofits. 20 Respondents in this study also described benefits from efforts that increased access to locally produced foods, including through food pantries and government programs. Nutrition and dietetics practitioners and health care providers should work with providers in the emergency food system to connect them to local food resource and promote these foods to their clients. Integrating food recovery and redistribution efforts with emergency food systems and incentivizing the purchase of locally produced foods through government programs can provide local produce to individuals who may not be able to afford to shop in the alternate food system, 50 aligns with the goals of food citizenship, 21 and has the potential to improve dietary intake and health for vulnerable households who rely on food pantries to acquire food.

A number of respondents said they were trying to eat healthier food in response to the pandemic, often citing the benefits food has on one’s immune response. The healthfulness of food has been identified as an influential factor motivating food choices in older adults. 25 Furthermore, some respondents discussed being able to eat healthier foods because of increased benefits, participation in government programs, or access to emergency food systems, which were available in response to the pandemic. These results suggest that if foods produced in more just and environmentally sustainable ways were affordable and accessible at comparable levels to food from the industrial food system, it is likely that these respondents would prefer, purchase, and consume them. Nutrition and dietetics practitioners can increase healthy food consumption among adults aged 50 years and older and benefit society by leveraging their desire to eat healthy foods while connecting them to the resources required to access, prepare, and consume foods produced in just and environmentally sustainable ways.

For those who did not use alternate food sources, the barriers to use were also reflected in the previous literature and included factors discussed by the respondents, such as cost and transportation barriers. 31 , 32 Despite these barriers, we believe there are multiple opportunities to improve older adults’ diet through facilitating connections to the alternate food system. This could be done by brining foods from the alternative food system into nutrition education programs, leveraging perceived healthfulness of foods from the alternative food system to reduce intake of ultraprocessed foods, connecting participants to financial support (such as the SMFNP), for acquiring foods from the alternate food system, and connecting the alternate food and emergency food systems. It should also be noted that this study was conducted when alternate food sources were widely available (ie, summer and fall), and the seasonality of these food sources is also likely to be a barrier to using alternate food sources at other times of the year. Additional barriers were introduced by the pandemic, specifically in the case where providers and customers were not following safety precautions (eg, wearing masks and social distancing). Efforts should be made to ensure that older adults are able to safely shop in any outlet because it is a societal responsibility to ensure that all individuals are able to safely access the food retailers of their choice.

Limitations

The recruitment strategy for this study introduces a few limitations. First, because of limitations associated with conducting research during a pandemic with a vulnerable population, we chose to use a convenience sample for this study, which resulted in a sample that was mostly women, and we did not have any respondents who identified as Hispanic. We also recruited the majority of the sample through AAAs. This is likely why we saw such a large proportion of the sample receiving vouchers for the SFMNP because AAAs distribute the SFMNP vouchers in Iowa. A smaller group of our sample was recruited through the food banking system, which increased the geographic, racial, and age diversity of our sample. Because of where we recruited participants, we largely interviewed individuals who were already connected to either an AAA or a food bank, and therefore we do not include the perspective of individuals who are not connected to either a government or nonprofit support system. In other words, this sample likely did not include the most marginalized individuals of any demographic group included in the sample, which should be considered when interpreting these results. Because we had reached saturation, indicating that increasing the sample size would not add new, meaningful data and our results would not change, it is important to consider how the limitations of the recruitment strategy affect who was included in this study. These limitations could be addressed in future research by recruiting outside of food assistance programs and services, using more purposeful selection criteria, and using quota sampling; for example, requiring a certain proportion of the sample is not receiving emergency food or participating in government food assistance. In addition, we were not able to examine differences in emergent themes between respondents in the 50 to 59 ages groups vs other age categories, which are likely given then different circumstances of those in this age group compared with those older than age 60 years. Further research is needed on how changes in food choices and sources differed by age category. Finally, the recruitment strategy relied on participants reaching out to schedule an interview, which would introduce self-selection bias because those who are willing to reach out likely differ from those who are not in some ways. For example, our sample was heavily women, which may be due to self-selection of female-identifying individuals into the sample vs male-identifying individuals.

This study used in-depth interviews with Iowans aged 50 years and older to explore factors influencing food choices and food sources during the COVID-19 pandemic. The factors that determined food choices among respondents were mostly outside of individual control (food prices) and/or related to responsibilities toward one’s self (eg, personal preferences or for health reasons) rather than for responsibilities to the greater good. Acquiring foods from alternate food sources has individual dietary benefits and collective benefits, such as promoting environmental sustainability. Dietitians and food and nutrition practitioners should work to connect eligible clients aged 50 years and older to resources that provide material resources (eg, SNAP) and increase accessibility to alternate food sources (eg, SFMNP and emergency food providers) while providing the knowledge and skills needed to prepare and consume those foods to promote the consumption of these foods. By promoting and incentivizing the use of alternate food sources and consumption of locally produced foods, there is the opportunity to meet the nutrition needs of older adults and improve population health while working toward a more sustainable and just food system.

Acknowledgement

The authors thank Doris Montgomery, MS, RDN, LDN and the Iowa Food Bank Association for advice and assistance. The authors also thank the interview participants for the time and effort they provided.

Biographies

P. Brady is a postdoctoral fellow, Division of Epidemiology and Community Health, University of Minnesota School of Public Health, Minneapolis.

N. Askelson is an associate professor, Department of Community and Behavioral Health, University of Iowa College of Public Health, and a research fellow, University of Iowa Public Policy Center, Iowa City.

H. Thompson are research assistants, and S. Ashida and F. Nothwehr are associate professors, Department of Community and Behavioral Health, University of Iowa College of Public Health, Iowa City.

S. Kersten are research assistants, are associate professors, Department of Community and Behavioral Health, University of Iowa College of Public Health, Iowa City.

S. Ashida are associate professors, Department of Community and Behavioral Health, University of Iowa College of Public Health, Iowa City.

F. Nothwehr are associate professors, Department of Community and Behavioral Health, University of Iowa College of Public Health, Iowa City.

H. Hopkins is a community health consultant, Iowa Department of Public Health, Des Moines.

B. Janssen is a clinical associate professor, Department of Occupational and Environmental Health, University of Iowa College of Public Health, Iowa City.

D. Frisvold is an associate professor, Department of Economics, Tippie College of Business, and a senior research fellow, University of Iowa Public Policy Center, Iowa City.

Supplementary materials: Figure 1 is available at www.jandonline.org

STATEMENT OF POTENTIAL CONFLICT OF INTEREST No potential conflict of interest was reported by the authors.

FUNDING/SUPPORT This study was supported by the USDepartment of Agriculture Supplemental Nutrition Assistance Program and it was developed by the Iowa Department of Public Health and the University of Iowa in partnership with the Iowa Department of Human Services (Iowa Nutrition Network Food Bank Project, grant no. 5880NU29). The first author is supported by Award no. T32DK083250 from the National Institute of Diabetes and Digestive and Kidney Diseases (NIDDK). The content is solely the responsibility of the authors and does not necessarily represent the official view of the NIDDK or National Institutes of Health.

AUTHOR CONTRIBUTIONS All authors meet the International Committee of Medical Journal Editors criteria for authorship. P. Brady, N. Askelson, H. Thompson, S. Kersten, H. Hopkins, S. Ashida, B. Janssen, F. Nothwehr, and D. Frisvold, made substantial contributions to the conception and design of the study. P. Brady, H. Thompson, S. Kersten, and H. Hopkins contributed to the acquisition of the data. P. Brady, N. Askelson, H. Thompson, S. Kersten, S. Ashida, B. Janssen, F. Nothwehr, and D. Frisvold, contributed to the analysis and interpretation of the data. P. Brady, N. Askelson, S. Ashida, B. Janssen, F. Nothwehr, and D. Frisvold, wrote the first draft. All authors revised subsequent drafts and gave final approval of the work.

Supplementary Materials

Older adult interview guide.