Introduction

Food loss and waste (FLW), alongside unsustainable resource use associated with the traditional model of food production and consumption1,2, as well as its important global environmental and socioeconomic impacts3, have outlined the critical need for a paradigm shift in our global resource management strategies4. Within this context, the circular economy (CE) has been conceived as a transformative approach focused on the restorative use of resources, emphasizing on efficiency, waste reduction, and sustainability5. The global food systems face significant challenges, with an alarming 25–30% of FLW of the total food produced worldwide, contributing to ~8–10% of total anthropogenic GHG emissions and costing about 1 trillion USD per year between 2010 and 20163. The CE model inspires a vision of a food circular economy (FCE)6, promising to alleviate the strain on limited resources by endorsing a model of production and consumption, where waste and loss are minimized through the continuous prevention of waste, and the reuse, recycling, and regeneration of resources in a closed-loop system7,8.

Yet, as we evolve into this transformative landscape towards more sustainable systems, the imperative of food safety cannot be overstated. Significantly, food manufacturing side streams (FMSS) present a growing area of interest for reutilization as viable materials and products that are reinserted into the food supply chain, including valuable food ingredients9. However, the reintegration of these substances into the food supply chain potentially carries the inherent risk of introducing chemical, biological, physical hazards and allergens10,11.

This potential public health concern, while limitedly addressed in literature that primarily focuses on the valorization of side streams12,13,14,15,16, remains a crucial discussion on the potential food hazards emerging from their reuse within a FCE framework. However, the comprehensive reviews by Rao et al.12, Focker et al.11, and Socas-Rodríguez et al.13, alongside other related studies, notably bridge this gap by highlighting the valorization of FMSS, addressing the balance between food safety and sustainability, with an orientation to the European Union (EU) context. They establish a foundation in understanding the valorization process’s complexities, particularly emphasizing the importance of food safety, by identifying food hazards related to products derived from food side streams, which will be reissued in different stages of the food supply chain.

As has been explored by the available body of evidence, as the food system moves towards more sustainable and circular models, understanding the full spectrum of food safety risk factors associated with FMSS becomes paramount, including the food hazards dynamics along closed-loop chains. However, as has also been briefly noted, the food safety implications of reintroducing FMSS into the food supply chain expand beyond a hazard-based perspective. This critical overview highlights a pressing need for adopting holistic perspectives on control strategies.

To do so, here we provide our perspective seeking to broaden the discussion on the multiple considerations in the complex interplay of food safety and circular economy principles. Illustrated at a very general level, we discuss the intersections that we envision for the scope of food side streams, via an integrative and food-chain approach. By advocating for a quad-modal approach grounded in the evidence available, we propose to delve into and elucidate some pathways through which food safety hazards in circular systems may emerge, particularly focusing on the reintroduction of FMSS into the food value chain. Enriched with targeted case studies, we seek to not only present some potential food safety risks but also to discuss strategies and interventions that may fortify our food control systems.

Interlink between food safety and food circular economy: a quad-modal approach to describe dynamics of food safety hazards

Within the circular economy (CE) paradigm, waste is avoided and resources are continuously reused, recycled and regenerated in a closed-loop system5. In the context of the food circular economy (FCE), these principles will be applied to address sustainability issues associated with FLW throughout the multiple stages of the food supply chain.

As previously reported14, there is a high heterogeneity on the definition of FLW, resulting in not only conceptual differences, but also substantial differences in root-causes and driving factors, mitigation strategies and challenges applicable to different types of FLW. This may be led by their inherent nature and characteristics of the waste, the stage of the food chain where they are generated, as well as the specific national context3,14,15. The United Nations built a harmonized conceptual and monitoring framework for FLW, which recognizes differences in the terms of food loss and food waste, establishing scopes based on the stages of the food chain that each covers16,17,18 (Table 1).

Table 1 Definition and scope of food waste and food loss concepts under UN framework
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In this article, food manufacturing side streams (FMSS) refer to substances or residual materials generated from primary food production that are not the primary intended food product. These may include waste, by-products, and initially inedible “fragments” as defined in the conceptual framework for FLW proposed by FAO16. However, cultural, economic, and technological factors should also be considered when assessing the categorization of these food fragments as edible or inedible. For instance, soybean residue (okara), often viewed as inedible residue of soy beverage or tofu production, is a valued food ingredient in some countries, such as unohana in Japan, kongbiji jjigae in Korea and xiao doufu in China. Considering this, defining side streams based on their production processes may provide a more inclusive approach. In addition, it is also important to note the distinction between side streams and by-products. While side streams encompass a broader category of materials with varying degrees of commercial viability, the term “by-products” is frequently used, often interchangeably with “side streams”, though it is a subset of side streams characterized by their immediate commercial value and are desired products. In this article, we use FMSS to include both materials with current commercial applications and those in the research stage that may hold potential for future utilization.

To narrow our discussion within the established scope of this perspective article, our examination will be focused on the food safety implications related to food loss scope FMSS. Globally, around 14% of food produced, valued at $400 billion per year, is lost during post-harvest up to the point just before retail19, reaching over 20% in regions like Central and Southern Asia16. In that sense, it is imperative to sustainably manage these food losses and FMSS. Specifically for food loss, some interlinks are distinguished between food safety and the management measures applied. During routine food safety monitoring, several issues can arise from various points of the food supply chain, such as the detection of pathogens or breaks in the cold chain, compromising on food safety and quality and hence generating production discards, which are considered as food loss. This relationship highlights that adhering to general principles of food hygiene16 is a way to minimize food loss. On the contrary, certain measures applied by food business operators to minimize food loss, such as the excessive use of pesticides and preservatives, may represent practices that compromise food safety.

On the other hand, within the facets of reusing, recycling and regenerating food loss and FMSS in a closed-loop system of FCE, specific food safety implications are also identified. Conventionally used in animal feed and fertilizers, FMSS are increasingly recognized for their potential in the production of materials and compounds, demonstrating the expansive scope of upcycling within the food manufacturing industry20,21,22. Furthermore, the growing interest in converting FMSS into valuable food ingredients, packaging materials, underscores the potential to increase the longevity of these resources while maximizing their value9. However, this raises distinct and multifaceted challenges, particularly concerning food safety in the instance where the reintegration of these materials carries the risk of introducing food safety hazard into the food chain10,11. The intrinsic variability in foods due to diverse factors, including genetic variation, is further compounded in FMSS generated from secondary food processing that have undergone various food processing. This variability imparts FMSS with diverse properties and hazards prior to their reuse (Table 2).

Table 2 Summary of major sources of food manufacturing side streams and their associated intrinsic hazards and valuable ingredients
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To effectively mitigate potential food safety risk associated with these cases, it is essential to recognize the potential and varied dynamics in the occurrence and levels of food safety hazards that could happen throughout the stages of transformation of side streams to by-products that will be reintroduced into the food chain. These dynamics would depend on several factors, such as the occurrence and previous levels of hazards in the raw material, raw material characteristics, reprocessing methods, and handling conditions. Each side stream and by-product have distinctive characteristics that influence their specific considerations for its reuse and consumption. Throughout various stages of reprocessing and rehandling, they undergo transformations, including in food hazard aspects, termed the ‘quad-modal hazard dynamic approach’. This comprises four key modalities through which food safety hazards can evolve in food circular systems, defined in Table 3.

Table 3 Definition of key terms in the ‘Quad-Modal hazard dynamic’ approach
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Figure 1 provides a cohesive illustration of the interconnection between food safety and food loss and FMSS within the framework of a food circular economy. At its core, the diagram represents solely the stages of the food supply chain (highlighted in green tones) where food loss occurs (shown in red tones), and the FMSS are generated. The links with preceding and succeeding stages of the chain are represented in gray. The chain becomes circular via the FCE’s closed-loop approach. Encircling this core, the diagram presents the primary components of the food circular economy in orange. This layer is divided into two primary objectives: preventing food losses at all stages of the supply chain, and the reintroduction of reclaimed food loss and FMSS back into the cycle, highlighting the potential to repurpose valuable food ingredients derived. The outermost layer, in yellow, depicts the crucial considerations for food safety pertinent to each component of the FCE, integrating a quad-modal approach for comprehensive coverage.

Fig. 1: Interconnection between food safety, food loss and food manufacturing side streams (FMSS) within the framework of a circular food economy.
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The diagram illustrates three key components: (1) Food supply chain segment, represented by gray sectors near the center of the circle. The critical food chain stages from which food loss and FMSS (in red tones) originate are highlighted in dark gray tones. (2) The orange sections represent the components of the circular food economy integrated throughout various stages of the food chain, emphasizing the reintegration of valuable ingredients from FMSS into the food chain through closed-loop systems. (3) The yellow sectors denote considerations for food safety within the context of food circular economy.

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Case studies: Assessment of food safety hazards in high-volumeFMSS using the ‘Quad-Modal hazard dynamics’ approach

To illustrate the ‘Quad-Modal hazard dynamics’ approach to evaluate food safety hazards in food circular systems, we assess selected hazards within three FMSS that have gained significance in the food industry due to its large production quantities. By analyzing these FMSS as case studies, we gain critical insights into the complex nature of food safety hazards present in these materials when reintegrated into circular food system. The focus is on discerning the nuanced interplay of chemical, biological, and physical hazards within these FMSS, given their extensive utilization and the consequent potential for widespread impacts on food safety within FCE.

Seafood side streams

Seafood side streams, encompassing large quantities of unused fish and crustacean parts, are rich in high value nutrients like omega-3 fatty acids and proteins23,24. In fish processing, the side streams constitute a considerable portion of the total weight of fish (~50%), comprising unused parts of the fish such as viscera, heads, trimmings, skin, scale, fin, bone, and damaged or unsuitable fish25. These seafood side streams are economical sources of useful ingredients for culinary applications26,27,28. However, reutilizing seafood side streams is not without its food safety challenges, and it necessitates an assessment of the associated food safety hazards that may arise from its reintegration within the FCE. Seafood is subject to various food safety hazards, among which chemical hazards are predominant, and seafood side streams that are reprocessed for foods, feed and supplements are no exception29,30.

Introduction

Biogenic amines (BAs) may be introduced into seafood side streams during improper handling, storage, and processing29. Seafood side streams are highly perishable, with their quick spoilage driven largely by processes such as microbial metabolism, autolysis, and lipid oxidation31. Factors such as higher temperatures can promote the growth and enzymatic activities of decarboxylase-producing bacteria like Enterobacteriaceae, Pseudomonas, and lactic acid bacteria, favoring formation of BAs32. In addition, during the processing of the seafood side streams, processes like fermentation can result in increased levels of BAs33. In a study of Korean fermented foods by Moon et al.33, elevated levels of histamine, a derivative of histidine identified as a key causative toxin of scombroid poisoning, were found to have increased across all tested fermented food samples29,33. The formation of histamine poses as a food hazard as it cannot be easily eliminated due to its thermal stability34.

Accumulation

The bioaccumulation of heavy metals is particularly pronounced in seafood side streams. Some types of fishmeal produced using fish parts that are unsuitable for human consumption, may be fed to farmed finfish and shellfish, leading to the bioaccumulation of contaminants such as methylmercury (MeHg) in muscle35. Fishmeal is also often used as feed for poultry and swine, and can lead to significant mercury accumulation in these livestock, exceeding safety limits36. Mercury that is present in the feed may then accumulate further in chicken feathers, a poultry side stream often repurposed into feather meal for livestock and aquaculture, thus perpetuating the cycle of contamination within the closed loop of FCE37.

Reduction

Depending on the food processing methods utilized, food safety hazards may be reduced in the process, which is a crucial step in ensuring the safe use of seafood side streams. Techniques like ultrasonic cleaning have proven effective in reducing heavy metals and other contaminants in shellfish side streams, enhancing their suitability for various applications, such as in calcium supplements38,39. Depending on the technological interventions used for food processing, food safety hazards may be lowered, and hence reducing the need to dispose of waste, aligning with the goals of circular food systems.

Interaction

Besides histamine, the formation of other BAs, notably putrescine and cadaverine, are also closely linked to spoilage of seafood, which can affect the resulting quality of the seafood side streams that would be made into by-products. Putrescine and cadaverine are formed by bacterial decarboxylation of ornithine and lysine, respectively29. More importantly, the presence of putrescine and cadaverine can aggravate the toxicity effects of histamine poisoning through synergistic interactions29. These BAs have been found to facilitate histamine transport across the intestinal lumen and enhance its absorption, increasing histamine bioavailability, or may inhibit histamine-metabolizing enzymes like diamine oxidase (DAO), leading to reduced histamine breakdown and clearance from the body40.

Whey from dairy processing

The dairy industry generates an estimated 180 to 190 million tons of whey each year, a valuable side stream utilized as a by-product derived from cheese and casein-based dairy production41. Whey constitutes a substantial proportion of the total milk volume and retains a significant amount of nutrients, such as protein, lactose, minerals and vitamins, making it a nutritious and functional resource for various applications in food and beverage products42,43.

Accumulation

The repercussions of veterinary drug use in dairy production become increasingly evident in the context of whey utilization44. The reliance of the dairy industry on heat treatment to ensure the safety of milk products falls short when it comes to antibiotics. Studies report that the extent of heat degradation, a standard process in milk treatment, is insufficient for removing antibiotic residues45. This shortfall means that these substances can remain present despite the heat treatment. The correlation between antibiotic levels in milk and its derivatives such as whey and fresh cheese is remarkably direct. Research indicates that the levels of antibiotics in whey and fresh cheese closely mirror those found in the original milk, with as much as 85.9% of these substances being transferred from the milk source to whey46,47. This suggests a predictable and consistent contamination of whey when originating from antibiotic-laden milk.

Interaction

The persistence and transfer of antibiotic residues from milk to whey not only concentrate these substances but also elevate the potential risk of fostering antimicrobial resistance (AMR). Moreover, the acquisition of antimicrobial resistance genes (ARGs) by pathogens through horizontal gene transfer poses severe health and environmental risks48. For instance, Fraiture et al.‘s study highlights this concern, identifying ARGs from Bacillus subtilis in a notable percentage of vitamin B2-enriched feed samples49. Similarly, the investigation conducted by Lányi et al. into raw milk samples from public markets reveals the alarming presence of various bacterial genetic materials, including complete ARGs46. These ARGs have the capacity to compromise the effectiveness of a broad spectrum of antibiotics, including cephalosporin, cephamycin, fluoroquinolone, peptide antibiotics, and tetracycline46. The accumulated presence of antibiotic residues in whey, stemming from standard dairy processing practices, emerges as a critical issue. It not only represents a direct threat to food safety but also contributes to the broader, more complex challenge of AMR.

Brewer’s spent grain from breweries

Brewer’s spent grain (BSG) is a significant side stream of the brewing industry, accounting for about 85% of the solid waste generated, reaching an annual production of 39 million tons worldwide50. BSG is composed of various valuable components such as hemicellulose, cellulose, lignin, and proteins51. Despite its potential value, BSG presents food safety challenges that need to be addressed. For instance, the prevalence of fungal secondary metabolites, namely mycotoxins, in BSG pose as a hazard that might affect human health, due to their toxicity to cause various health issues. Pereyra et al.52 evaluated the mycotoxins content in 33 brewer’s spent grain samples and found that all the samples are contaminated with fumonisin B1 (FB1) (104 – 145 μg kg-1), with 18% of the samples containing aflatoxin B1 (AFB1) at levels between 19 and 44.52 μg kg−152.

Introduction

Mycotoxins can also be introduced after its production, due to the fungi contamination. The high moisture and nutritional contents of BSG makes it especially susceptible to microbial growth and spoilage, in particular common fungal species such as Fusarium53. This genus is known for producing mycotoxins, including deoxynivalenol (DON) and fumonisins (FBs), which pose significant risks to animal and human health54,55,56. In the study by Penagos-Tabares et al., compounds like Zearalenone (ZEA), T-2, and HT-2 toxins were detected, even though they were found to be below European maximum limits for animal feeds57,58. Their persistent presence, however, is a stark reminder of the potential dangers if accumulated. BSG may initially meet acceptable standards for food use, however its microbial profile is subject to rapid alteration post-production, characterized by increases in microaerophilic bacteria and anaerobes59. Particularly disturbing are the high levels of Penicillium-derived metabolites, often indicative of post-production contamination during storage, which exacerbate the already serious issue of toxin accumulation58.

Accumulation

Grains, which serve as the raw materials for the brewery industry, are frequently contaminated with mycotoxins. However, the concentration of mycotoxins in beer is usually reduced as they are primarily absorbed and accumulated in the spent grains during the brewing process60. This was also corroborated by another study, in which 60% of the ZEA and 18% of the 15-acetyldeoxynivalenol (15-ADON) presented on the malt grist before the brewing process were found remaining in the spent grains61. Cumulatively, the gradual accumulation of mycotoxins in brewer’s spent grain, together with the newly produced mycotoxins after BSG production, can escalate to concentrations that pose acute health risks, underscoring the necessity for continuous monitoring and strict control measures in the management of BSG.

Reduction

Interestingly, research indicates that biological detoxification can effectively reduce the production and concentration of mycotoxin. Gomaa et al. demonstrated the ability of lactic acid bacteria, Lactobacillus brevis, to reduce the production of aflatoxin B1 by Aspergillus flavus and Aspergillus parasiticus, by 96.31% and 90.43%62. Luz et al. successfully reduced ochratoxin A (OTA) by 97% and 95% using Lactobacillus rhamnosus and Lactobacillus plantarum63. Several cutting-edge technologies, such as cold plasma, moderate electric field (MEF), pulsed electric field (PEF), ultrasound, and ohmic heating, have shown significant positive outcomes together with fermentation for mycotoxin detoxification, suggesting these technologies may interact synergistically to degrade mycotoxins in food64.

Interaction

BSG is likely to be co-contaminated by several mycotoxins during complex processing and storage. The interaction between different mycotoxins might result in more severe toxic effects than exposure to individual mycotoxin. The simultaneous presence of, AFB1 and ZEA, or, AFB1 and DON, in agricultural products, for example, could be more hepatotoxic than either mycotoxin acting alone65.

Overall, these case studies of high-volume FMSS demonstrate that while these resources present a valuable opportunity for resource reutilization in circular food systems, they require a good assessment and understanding of the potential food safety hazards arising from food circularity. The ‘Quad-Modal hazard dynamics’ offers a structured approach to identify, characterize, and therefore able to manage these hazards through a targeted manner, ensuring the safe integration of FMSS into the food value chain while aligning with the principles of a sustainable circular economy.

Food control implications and advancing research on food safety risk in food circular economy: A critical imperative

In the transition towards a circular food economy, aimed at sustainability and resource efficiency, the various aspects of food safety that we have described, particularly the multiple dynamics that food safety hazards could experience, underscore the critical need for a deeper understanding of these phenomena. Based on this, tailoring appropriate approaches to mitigate food safety risks associated with food loss and waste (FLW) across diverse stages of the food supply chain is imperative. These insights, grounded in scientific evidence and a risk-based perspective, are pivotal for developing effective food control strategies to ensure food safety within circular economy frameworks.

As highlighted in previous studies11,12,13, food safety challenges inherent in FCE practices remain inadequately understood or addressed, particularly in the reuse of food side streams for food ingredient purposes. While the reuse of these side streams within the food supply chain effectively reduces losses, it also may pose a risk of (re)introducing contaminants into the food stream. Our ‘Quad-Modal hazard dynamic’ approach aims to illustrate that the occurrence and concentration levels of both new and pre-existing contaminants in raw materials depend largely on the nature and composition of the food Table 4 by-products, the processes employed to transform them into food ingredients, and the hygiene conditions maintained by operators during these processes. These dynamics of food hazards within the closed-loop section of the FCE model contribute to the complexities of ensuring effective food safety control measures.

Table 4 Summary of cases presented and food hazards consideration under ‘Quad-Modal hazard dynamic’ approach
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From a food control standpoint, competent authorities and partners can build up on the insights provided here to develop food control strategies tailored to the needs of more sustainable food systems. Adhering to international risk analysis principles for food safety, hazard assessment investigations must meticulously identify and evaluate these hazard dynamics, with particular attention to potential new hazards. This involves comprehensively understanding the adverse health effects associated with these agents and characterizing the relationship between dosage and the likelihood of adverse effects occurring. However, to advance comprehensive risk-based control measures, other elements of risk assessment and management, as well as other food control aspects. Table 5 provides examples demonstrating how these food safety control elements can integrate the quad-modal approach to understanding the dynamics of food safety hazards, along with other pertinent considerations.

Table 5 Examples of considerations in food safety control linked to the ‘Quad-Modal hazard dynamic’ approach and other food safety aspects
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Likewise, the scientific community should engage in rigorous research that examines the entire lifecycle of these by-products within circular systems. The research should focus on understanding how processing, storage, and handling in circular systems contribute to the safety profiles of these FMSS. There is a pressing need to develop and validate new methodologies for contaminant detection and quantification, assessing current decontamination techniques, and exploring innovative approaches to manage these food safety hazards. Furthermore, with better understanding of the food safety hazards, research into the integration of advanced food processing technologies like High Pressure Processing (HPP), Pulsed Electric Fields (PEF), and Atmospheric Cold Plasma (ACP) can offer promising technological solutions to minimize waste within food circular systems, through their capabilities of reducing microbiological activity, chemical contaminants, and food allergens in food products66,67,68,69,70,71. These technologies, alongside advanced detection methods like Next-Generation Sequencing (NGS), quantitative Polymerase Chain Reaction (qPCR), utility of stable isotopes, and various spectroscopy techniques, provide comprehensive tools for tracking and monitoring changes in FMSS in the context of food safety72,73,74,75,76,77. The use of biosensors for real-time monitoring and the combination of multiple detection technologies with chemometric and omics approaches, augmented by artificial intelligence, present innovative avenues for detecting food hazards77,78,79,80,81.

By undertaking this crucial research, the scientific community can provide indispensable insights and guidelines that will aid policymakers, industry stakeholders, and regulatory bodies in harmonizing sustainability goals with uncompromised food safety in circular economy food systems. This alignment is essential for the sustainable and safe growth of our global food systems, ensuring that our pursuit of environmental sustainability goes hand in hand with the protection of public health.

Concluding remarks

This perspective article has examined the interlink between food safety and food circular economy model, with emphasis on the complexities of food hazards dynamic that can occur in the reuse of food manufacturing side streams (FMSS) and their reintegration into the supply food chain.

The transition towards circularity in food systems via the reprocessing of food manufacturing side streams and by-products holds significant promise for waste reduction, resource conservation, and the promotion of more sustainable consumption and production patterns. However, to ensure the success of this transition, it is crucial to thoroughly understand the complexities potential occurrences and harmful alterations of the hazard levels associated with these reprocessing practices. The proposed quad-modal approach addresses these food safety hazards dynamics by describing their potential modalities of introduction, accumulation, reduction, and interaction. This underscores the critical need for a deeper understanding and developing effective management strategies for potential food safety risks to ensure the safety and sustainability of food systems. These strategies should encompass rigorous hazard assessment, but should also address appropriate exposure assessments, risk characterization, and proactive risk management practices. Based on this, the competent authorities must deploy appropriate actions to control food safety, which must be applied within the framework of the food circular economy.

Future research should focus on the compositional changes and risks associated with reprocessing food manufacturing side streams, to develop safer and more efficient processing techniques. The advancement of new detection, monitoring, and analysis technologies will also be essential for assessing and managing risks and ensuring food safety.

As we advance our understanding and implementation of circular food systems, it becomes clear that the goals of environmental sustainability and food safety are not only compatible, but are integral, complementary pillars essential for building a truly sustainable food system. Therefore, we call upon industry stakeholders, policymakers, and researchers to unite in their efforts to innovate on robust solutions that not only advance sustainable food system objectives but also ensure the safety and well-being of consumers. Through such collaborative efforts, we can craft a food system that upholds the principles of sustainability while safeguarding public health, thereby achieving a sustainable future for all.