CC BY
90
läum
Foods and Raw Materials. 2023;11(1)
ISSN 2308-4057 (Print) ISSN 2310-9599 (Online)
Review Article Open Access
<S>
Available online at http://jfrm.ru/en https://doi.org/10.21603/2308-4057-2023-1-559 https://elibrary.ru/JKSWOT
Cold chain relevance in the food safety of perishable products
Pedro Arriaga-Lorenzo1 , Erna de Jesús Maldonado-Simán1* , Rodolfo Ramírez-Valverde1 , Pedro Arturo Martínez-Hernández1 , Deli Nazmín Tirado-González2 , Luis Antonio Saavedra-Jiménez3
1 Chapingo Autonomous University"0", Texcoco, Mexico 2 National Technological Institute of Mexico"0", Mexico, Mexico 3 Autonomous University of Guerrero"0", Acapulco de Juarez, Mexico
* e-mail: emamaldonado@correo.chapingo.mx
Received 17.05.2022; Revised 27.06.2022; Accepted 05.07.2022; Published online 30.01.2023
Abstract:
The food cold chain is an effective tool that allows food markets to maintain food quality and reduce losses. Poor logistics may
result in foodborne disease outbreaks and greenhouse gas emissions caused by organic matter decay. The ongoing pandemic of
COVID-19 makes it necessary to study the chances of SARS-CoV-2 transmissions in food products.
This study reviews cold chain logistics as a handy tool for avoiding food safety risks, including COVID-19.
The cold chain of perishables and its proper management make it possible to maintain quality and safety at any stage of the food
supply chain. The technology covers each link of the food chain to prevent microbial spoilage caused by temperature fluctuations
and the contamination with SARS-CoV-2 associated with perishable foods. Given the lack of knowledge in this field in Latin
America, the region needs new research to determine the impact of the cold chain on perishable foodstuffs.
The perishable cold chain is only as strong as its weakest link, and the national and international markets require new traceability
protocols to minimize the effect of COVID-19.
Keywords: Cold chain, meat, food safety, temperature, COVID-19
Funding: This review study did not receive any specific grant from the public, commercial, or not-for-profit funding agencies.
Please cite this article in press as: Arriaga-Lorenzo P, de Jesús Maldonado-Simán E, Ramírez-Valverde R, Martínez-Hernández PA, Tirado-González DN, Saavedra-Jiménez LA. Cold chain relevance in the food safety of perishable products. Foods and Raw Materials. 2023;11(1):116-128. https://doi.org/10.21603/2308-4057-2023-1-559
INTRODUCTION
Food safety and environmental protection are one of the most important issues in the global scientific and technological agenda, as well as the subjects of the growing concern and awareness of final consumers. An effective farm-to-table cold chain is a tool that provides food safety by uninterrupted refrigeration. This process maintains a controlled temperature of the perishable product in a given time and space, thus promoting a constant heat transfer coefficient and particular temperature of the dissipation medium [1]. Product temperatures have to remain within a certain range to avoid microbial proliferation, tissue damage, and excessive emission of CO2 caused by inefficient refrigeration devices and food wastage [2, 3]. Therefore, the industries responsible for cold chain logistics must
find better alternatives to reduce CO2 emissions [4, 5] because perishables require appropriate management, equipment, and facilities at each stage of the food supply chain [3].
Efficient cold chain management uses reliable data on temperature modes for various foods: for instance, low temperatures that are suitable for meat products may damage tropical fruits and reduce their sensory quality [6]. Accurate data on optimal storage temperature for each product could reduce the volume of food waste caused by inadequate cold chain management and mitigate the alarming food loss worldwide [7, 8]. The cold chain technology provides various benefits by limiting the proliferation of microorganisms and avoiding food waste. Efficient cold chain logistics extends shelf life, thus providing the final
Copyright © 2023, Arriaga-Lorenzo et al. This is an open access article distributed under the terms ofthe Creative Commons Attribution 4.0 International License (https://creativecommons.org/licenses/by/4.0/), allowing third parties to copy and redistribute the material in any medium or format and to remix, transform, and build upon the material for any purpose, even commercially, provided the original work is properly cited and states its license.
consumer with a safe product with an optimal sensory profile [9]. Therefore, companies must provide the necessary conditions and equipment for the entire cold chain with its weakest links, not only in the manufacturer's facilities, which are often certified by international standards, such as ISO 9001, ISO 22000, or HACCP [10].
During the current pandemic, food supply chains must reinforce their hygiene measures because SARS-CoV-2 might be transmitted by fomites, although few reports are available on this subject [11, 12]. Nevertheless, in Qingdao, SARS-CoV-2 was revealed in the packaging of cod imported to China via the cold food chain, where the low temperature and humidity increased the stability of the virus [13]. Consequently, disinfection strategies were implemented for packaging cold-chain imported products [14]. This paper highlights the effect of temperature fluctuations on the perishable food cold chain, as well as on the potential presence of SARS-CoV-2 in perishable foods.
RESULTS AND DISCUSSION
Food supply chain. Food products require a variety of handling throughout the food supply chain, from the primary production to the consumer's plate, and each stage involves a large number of people. Assessing the number of people in food production is a difficult task by itself. The European Union alone has at least 11 million establishments engaged in food production, including 300 000 food and beverage companies. Their products are purchased by 2.8 million distribution and food service businesses, whose principal objective is to supply products to some 500 million EU citizens [15].
Considerable food losses and waste are unavoidable because every single stage of the food supply chain involves numerous difficulties. An estimated one-third of the global food production is wasted for various reasons. Approximately 1.3 billion tons are reported as waste every year. The ratios usually differ, depending on the food supply chain link and the conditions within each country [8, 16, 17]. The United Nations Environment Program has estimated that about 931 million tons of food waste were generated by retail, food service, and household waste [18]. While food waste reduction is on the global agenda, Latin America can hardly offer any data on food wastage in the region. Only four countries in Latin America can provide information on food loss and waste. They are Belize, Brazil, Mexico, and Colombia [19-21].
Food cold chain. Cold chain is one of the main tools of the food industry. It ensures the optimal conditions for food meant for human consumption. Cold chain is a system that keeps food under a controlled temperature from the moment of its production or harvest until it reaches the final consumer [22-24]. However, the International Dictionary of Refrigeration describes it as "a series of actions and equipment applied to maintain a product within a specified low-temperature range, from harvest/production to consumption" [25].
Highly perishable food products retain acceptable safety and quality throughout the whole supply chain provided that certain factors are maintained, e.g., temperature and relative humidity [24]. Perishables may suffer an adverse variation when the storage temperature is outside the ideal temperature range [23]. Therefore, cold chain monitoring is critical to identify any weaknesses for successful intervention [26]. Consequently, food science develops various ways to monitor the temperature of a product in realtime and access its temperature history throughout the process [23]. Some of the frequently employed options include radio frequency identification (RFID) tags, time and temperature integrators (TTIs), and wireless sensor networks (WSNs) [27, 28].
Several studies (Table 1) used various monitoring tools to test food temperature along the cold chain and registered temperature abuse at all chain stages [9, 23]. Therefore, food distribution is a complex process that takes into account the effect of environmental conditions on the food temperature throughout the cold chain [29]. Transportation, storage, and retail stages demonstrated the highest temperature abuse rate [30-32].
Temperature abuse can happen in all cold chain links, especially at the last stages. The logistics management definitely requires improvement, given that temperature fluctuations may occur during inspection procedures at customs or ports [35, 42]. A uniform temperature distribution in the refrigeration equipment is crucial to avoid disruptions related to product position within the refrigerator [47].
Technologies employed. The farm-to-table food product chain requires significant resources. Both developed and developing countries keep increasing their refrigeration energy consumption in an attempt to reduce food spoilage [51]. Monforti-Ferrario et al. estimated that about 30% of the electrical energy used in the European Union food industry is spent on cooling and freezing [52].
Such refrigerants as chlorofluorocarbon and hydrochlorofluorocarbon dominated the refrigeration field in the 1930s, and vapor compression refrigeration gained ground as an alternative throughout the food supply chain. In the 1980s, the growing environmental awareness resulted in a number of international agreements with timescale applications for eliminating hydrochlorofluorocarbon. Later, the European Union proposed introducing regulations on fluorinated gases, including all hydrofluorocarbon refrigerants, e.g., R134A, and mixes containing fluorinated gases, e.g., R407C, R410A and R404A [53].
Multiple compressor refrigeration packs or air-cooled condenser racks are regularly used in commercial refrigeration systems in food distribution centers. In the United Kingdom, modern systems normally use scroll compressors and R404A refrigerants [53]. Supermarkets use open refrigerators that have
Arriaga-Lorenzo P. et al. Foods and Raw Materials. 2023;11(1):116-128 Table 1 Temperature fluctuations observed throughout the cold chain
Country Link Product Recommended temperature, °C Temperature abuse Sensor Reference
Belgium Harvest to restaurant Endive 0 16°C Data loggers [34]
Canada Processing to retail Lettuce < 5 7°C Temperature recorders [35]
China Processing to distribution Meat < 4 8-10°C Data loggers [36]
Transport Fish -18 ± 2 < 18.6°C RFID [37]
Finland Retail Fish and meat < 4 < 105 min with temperatures above recommended Data from the inspector's office, data logger, infrared thermometer [32]
France All links Dairy and meat products < 4 9°C Temperature recorder [38]
All links Smoked salmon < 8 Temperatures above the recommended Data loggers [39]
Transport/storage Milk < 4 < 11.7°C Data loggers [40]
Iceland Transport Fish 5 The temperature was > 5°C during 31.1% of transportation time Data loggers [41]
Japan Farm to retail Lettuce < 5 3-15 Data loggers [42]
Slovenia Retail Miscellaneos products Different temperature ranges Temperatures above recommended for different products Infrared thermometer [31]
South Cold store to haven Fruits 2 < 81% temperature abuse Data loggers [43, 44]
Africa for 1.5 h
Spain Storage Ham < 5 < 12.2°C Data loggers [45]
Retail Meat, dairy, fishery products and vegetables 2-8 Temperatures above the recommended for different products Infrared thermometer [46]
Taiwan Transport to home Frozen shrimps -20 < 17.2°C Data loggers [47]
Thailand Transport/storage -20 < 17°C at different times Infrared thermal camera/ data logger [48]
USA Harvest to retail Live oyster 1.7-10 < 14.4°C Temperature sensors [49]
Transport to display Lettuce < 5 < 18.2°C TempTale4 sensors [50]
Transport Fresh-cut leafy greens < 5 5-10°C Data loggers [51]
no physical barrier between goods and people, except for an air screen that keeps out humidity and warm air [54].
A refrigerated container, also called an integral reefer container, is required to transport perishable foodstuffs. It usually refers to a metal box with polyurethane insulation and a refrigeration unit, typically approved by the International Organization on Standardization, i.e., it is of ISO quality [55]. The container comprises three main components: an air circulation system, a microprocessor controller, and a cooling system. The microprocessor controls the refrigeration unit, records the data obtained by the maintenance system, performs diagnostics, and generates the temperature database during transportation. The refrigeration unit must have a power source supplied by land equipment or container vessels [56].
Different alternatives are available throughout the cold chain, some of which are low-cost, whereas others are more complex and sophisticated, depending on the product's link. Economical alternatives, e.g., ice, or more expensive options, e.g., forced air, vacuum cooling, or hydro-cooling systems, can be used for pre-cooling at the production site. Storage usually occurs in cold rooms, in small or large warehouses with traditional refrigeration equipment, in controlled air conditioning systems, e.g., CoolBot™, or in cold evaporation rooms. The food processing stage may include some alternatives, e.g., refrigerators, individual quick freezing (IQF), blast freezing, freeze-drying, etc. The transportations stage usually includes such alternatives as ice, refrigeration units in trailers, evaporative coolers, or passive cooling [57].
Cold chain in transportation. Cold chain food transportation involves land, air, and maritime resources. Until 2005, trucks used to be the most popular land transport vehicle. Estimates suggest that more than 90% of foods are moved by land in the United Kingdom [2, 58]. The distance that vehicles travel to deliver a food product to the retailer is highly variable [37, 59]. A lot of different factors must be considered during food transportation to keep the cold chain undisturbed. Seasonal temperature can strongly affect the food supply chain, being as low as -10°C in winter or as high as 35°C in summer [7].
Trucks must be able to provide favorable temperature for the perishable foodstuffs they transport, considering that they travel up to 2500 km [37, 59, 60]. Many studies report temperature rises during transportation of milk, strawberries, and fresh-cut leafy greens, as well as during the loading and unloading of fish [39, 50, 61, 62]. Additionally, temperature control deficiencies can be potentiated by the impact of the environment on the temperature fluctuations of the transported products [60].
The advantage of air transport is that food can be quickly moved to locations far from being produced or harvested. However, this transportation method is not very popular, except for high-cost foods and products with a short shelf life that must reach their destination quickly [2]. The cold chain by air transport is extremely complex. Only half of the time required is actually the flight time: the other half is spent on the management procedures to load and unload the product into and out of the aircraft, which results in poor temperature control [2, 63].
In contrast to air transport, shipping products by sea is slower, although more profitable in cases of meat, dairy products, fish, fruits, and vegetables. Therefore, the type of transportation generally depends on the type of the product to be moved. Specialized vessels are usually used to transport bananas. For most products, reefer containers are more cost-effective and can provide a better logistics [2, 64, 65].
Transport to home, which is the last transportation link in the cold chain, is often the weakest one, with the highest temperature increase [66]. Passive cooling devices are a viable alternative to avoid this problem, e.g., phase change material in easily portable insulated boxes [67, 68].
Cold chain in warehouses. Achieving that perishable food reaches the last link of the food supply chain in optimal conditions is complex and expensive. The food industry invests millions of dollars in order to attain this goal and avoid having to recall a product due to contamination during the cold chain [69]. A food product can remain stored in distribution centers for many days [70]. Its shelf life depends on the right conditions, and the optimal temperature control is essential. Unfavorable temperature deviation during the storage of perishable products is related to the corresponding link in the supply chain. Derens et al. revealed that the biggest temperature problems in France
were related to display cabinets, transport to the home, and domestic refrigerator storage [37].
Unfavorable fluctuations occur less frequently during storage at the distribution center. Multiple studies conducted on such perishables as meat, dairy products, and vegetables confirmed temperature records below 4°C at the storage stage in distribution centers [37, 60, 70]. However, these data were obtained from developed countries. Developing countries have less favorable conditions in terms of equipment, energy sources, and environment, which is often due to their geographical location.
Retail cold chain. Derens-Bertheau et al. reported that such stages of the cold chain as display, transport to home, and domestic refrigerator storage are also highly problematic. Retail distribution link appears to be one of the main problems, which can be related to various reasons. Firstly, product information often lacks temperature specifications [31]. Secondly, open refrigeration equipment sometimes fails to maintain the required temperature as a result of an uneven distribution of the airflow throughout the rack [45, 71, 72].
The latter occurs when the equipment lacks capacity or configuration to achieve an effective air curtain [73, 74]. Therefore, refrigeration equipment with doors is a viable option to achieve greater efficiency in cooling of perishables and electricity consumption [54].
Some recent studies pointed to the need for improving the cold chain control during retail: they detected adverse temperature deviations in meat products, poultry, and pork [30, 32, 72]. Even within retail distributors, position of the product in the refrigeration equipment might result in temperature fluctuations caused by design, configuration, or services. Baldera et al. reported a 25, 40, and 57% shelf-life reduction for cheese, salmon, and chicken because they were positioned at the highest point inside the refrigerator.
Within the retail food industry, refrigeration systems are responsible for a significant amount of greenhouse gas emissions, which could be reduced by using improved equipment [75]. The electricity consumed by a supermarket generates approximately 50% of these emissions [76]. Moreover, some supermarkets still use hydrofluorocarbons as refrigerants. This refrigeration method is responsible for 30% of greenhouse gas emissions caused by refrigerant leakage, but it still remains quite popular in the United Kingdom [77]. As a result, standards have been implemented to decrease its use in favor of natural options, such as CO2 [78].
Food spoilage induced by microorganisms. Shelf life is the time food keeps its physical, chemical, and microbiological properties and is safe for human consumption. Food spoilage can be associated with environment, composition, packaging, human handling, microorganisms, etc. All these factors reduce shelf life [79, 80]. Potential factors that affect shelf life can be divided into intrinsic and extrinsic. Therefore, a microorganism can be considered an extrinsic factor if it
does not belong to the product. Meat products constitute a highly favorable food source for various bacteria since meat has a lot of nutrients and high water activity, which promote microbial growth. As a result, meat products easily acquire unpleasant texture, odor, and flavor [80].
Food contains a great wide variety of microorganisms, e.g., Campylobacter, Pseudomonas, Enterococ-cus, Acinetobacter, Psychrobacter, Moraxella, etc., as well as numerous kinds of bacteria, fungi, yeasts, protozoa, and viruses [81-85]. Food in general and meat products in particular are susceptible to a wide range of potential spoilage microorganisms. Meat products have been reported as foods with the highest temperature abuse [86]. Therefore, this kind of food must be handled, stored, and transported at a temperature range of 2-7°C, depending on the type of meat product [87].
However, strict temperature control throughout the cold chain is just another tool that minimizes the risk of microbial contamination. Additional measures can help avoid other contamination sources and reduce the chance of microbiological growth. Some psychrotrophs, for example, can grow at temperatures below 7°C [84, 88]. This group of microorganisms includes such high-risk species as Listeria monocytogenes and Yersinia enterocolitica, both of which can grow at temperatures below 5°C [89]. However, the European Union reports a low incidence of outbreaks related to psychrotrophs compared to bacteria, e.g., Campylobacter and Salmonella [90]. Meanwhile, a higher incidence of norovirus cases with a meager mortality rate was reported in the USA through 2017. It was followed by Salmonella and, with fewer cases, Listeria. However, these bacteria could be considered equally dangerous since 3-8 and 3-35 people die from Salmonella and Listeria each year, respectively [81].
Food loss and waste are not only a concern for economic and environmental reasons, but they also present a high risk of an outbreak due to contaminated food. Pathogens, such as Salmonella enterica serovar Typhi, Shigella dysenteriae, Yersinia pestis, and most Escherichia coli, are found within the Ente-robacteriaceae family [91]. Some of them can grow when temperatures are above 7.2°C, e.g., E. coli O157: H7 [82]. Some strains of these bacteria are natural to the digestive tract of warm-blooded animals [92]. However, strains classified as Diarrheal E. coli (DEC) are becoming more aggressive as a result of their improved resistance to different antibiotics [93]. They are subdivided by their virulence into shiga toxin-producing E. coli (STEC), enteropathogenic E. coli (EPEC), ente-roaggregative E. coli (EAEC), enteroinvasive E. coli (EIEC), enterotoxigenic E. coli (ETEC), and diffusely adherent E. coli (DAEC).
COVID-19 and its relevance to food safety. Throughout 2019, the world faced a danger that severely impacted public health and hit the worldwide economy. Coronavirus disease (COVID-19) is caused by Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2). Up to early November 2021, it caused
247 968 227 confirmed cases, of which 5 020 204 deaths were reported in at least 200 countries. Consequently, vaccines are reported to have been applied in 7 027 377 238 doses among the world's population [94]. Vaccination works in conjunction with recommended safety measures, but the number of cases reported vary from region to region in each country.
A 55-day period without viral transmission was achieved in the Beijing region, which was interrupted on June 11, 2022 when a SARS-CoV-2 case was reported and continued to spread. The virus was detected on different surfaces on a wholesale seafood and meat market, particularly on a board used to slice salmon imported from Europe. The virus could be transmitted through food in the cold chain, cross-contamination by workers, or packaging, but the sequences found were consistent with those of infected Chinese citizens who returned from Europe [95, 96].
Moreover, the Chinese Center for Disease Control and Prevention carried out different studies that detected the presence of SARS-CoV-2 nucleic acid in samples of chicken and shrimp imported from South America and marketed in various Chinese cities [97]. Consequently, several studies (Table 2) proved the presence of SARS-CoV-2 in food products and raw materials. Whether food is a direct transmission route remains unclear, which does not eliminate the possibility of cross-contamination [98]. Therefore, strict control measures are required to reduce outbreaks, particularly in large slaughtering and meat-processing companies, where outbreaks have been reported in Portugal, Australia, The United Kingdom, and Ghana [99].
Food products receive little scientific attention in COVID-19 research since they are not considered a potential transmission route of SARS-CoV-2. Studies conducted on fresh vegetables, e.g., cucumbers, revealed that the virus might remain infectious for up to 72 h [107]. Castrica et al. commented that researchers are increasing the number of studies on wastewater based on the understanding that monitoring the pathogen in this environment could create a real-time pandemic model [110, 111]. Moreover, communal areas must not be overlooked as a source of contact infection, although no positive samples have been found from different regions, potentially due to adequate sanitation measures [106].
Since the jury is still out on the foodborne transmission of COVID-19, inoculations were carried out on pork, beef, and salmon samples with different concentrations of SARS-CoV-2 to investigate the stability of the virus after controlled cold-chain management (4 and -20°C) [112]. Viral RNA was detected in all samples stored at 4°C for 72 h after infection, with a higher average number of RNA copies in the pork meat at the lowest concentration. At the highest concentration, viral RNA could be detected in all samples up to 216 h after infection. Viral RNA remained detectable up to 20 days after infection in the samples stored at -20°C in both inoculum
Table 2 Detection of SARS-COV-2 virus in food-safety-related samples
Country Sample Type of study Detection method Reference
USA Water and wastewater Persistence evaluation RT-qPCR and Vero E6 cells [102]
South Korea Tap water Stability in water samples qRT-PCR [103]
China Salmon Viability of SARS-CoV-2 under different conditions Vero E6 cells [104]
Bangladesh Wastewater Detection of SARS-CoV-2 genetic material RT-PCR [105]
Finland Wastewater influent Presence and stability of SARS-CoV-2 RNA RT-qPCR, N2 assay, ABI BigDye™ v3.1 Chemistry [106]
Brazil River water Viability of SARS-COV-2 under different temperature conditions Plaque assay [107]
Canada Surfaces in food retailers Detection of SARS-CoV-2 (all of them negative) RT-qPCR [108]
Apple, tomato, cucumber, and Preservation of infectivity (HCoV-229E) Plaque assay (MRC-5 cells) [109]
lettuce
France Zebra mussel SARS-CoV-2 genome detection in zebra mussels as bioindicators of water contamination RT-qPCR Genes tested: RdRP: RNA-dependent RNA polymerase gene; E, an envelope protein gene and N, nucleocapsid protein gene [110]
Italy Polyethylene and Persistence of SARS-CoV-2 (ATCC® VR- RNA extracted with QIAamp® Viral [111]
polystyrene food trays 1986HK™) RNA Mini Kit RT-qPCR using the VETfinder detection kit
concentrations, being present to a greater measure in pork and beef, probably because of their fat content and texture.
The actual routes of SARS-CoV-2 transmission are not entirely clear [113, 114]. Currently, the closest relationship is to viruses reported in bats [115]. Given the variety of information about possible COVID-19 transmission routes, people reacted by increasing food safety and hygiene measures, e.g., washing and sanitizing kitchen surfaces, food, and hands [116]. Additionally, animal foods should undergo proper cooking procedures before consumption [117]. Unfortunately, people might fail to link security measures to food safety and give up these practices after the pandemic if their importance is not promoted [118]. Another critical point is the correct washing and disinfecting methods, e.g., using of detergent residues or inefficient disinfecting with vinegar, as was observed in Brazil [119-122].
On the other hand, food could be a transmission route for SARS-CoV-2, as it has been linked to meat processing plants, wherefrom viral particles could be transported to meat through the chain links. Some publications reported worrying data on the survival of viral surrogates, depending on the food and temperature. The SARS-CoV-2 viral surrogates remained in chilled and frozen meat and fish for a long time at refrigeration and freezing temperatures, possibly because the low temperatures allowed the virus to survive [123]. Low temperatures and humidity increased the survival of SARS-CoV-2 and contributed to its long-distance spread during logistics and trade [124]. The widespread
recommendation to prevent contamination of food and processing surfaces focuses on disinfection protocols at every stage of food processing.
Another relevant factor indicates that contaminated food and packaging imported from areas of active outbreaks of COVID-19 were located in China [125]. In contrast, low levels of SARS-CoV-2 were detected on stainless steel and cardboard surfaces under room temperature and constant humidity [126, 127]. Frozen foods were reported to carry SARS-CoV-2 without human contact, thus necessitating procedures for safe transport. Scientists reported incidents related to cold chains in frozen meat and fish. An improvement system for food cold chain management includes information detection, chain linkage, and credible traceability [128]. We identified two areas of improved cold chain management practices. The first one focuses on the analysis of requirements for the prediction of transmission risk and temperature ranges. The other concentrates on the documentation regarding critical control points throughout the cold chain, thus implementing objective traceability.
For high-quality food to reach the final chain link, the food industry needs qualified staff who are aware of the relevance of their work. All workers along the cold chain should possess a solid food safety culture, be able to identify the hazards of food mishandling, and understand the importance of hygienic measures both before and after the handling of animal products, tools, etc. [129, 130]. In addition, whole and retail vendors must be tightly supervised by government and nongovernment certification agencies [131, 132]. However,
Nyarugwe et al. conducted surveys of employees from diverse areas in food companies located in China, Greece, Tanzania, and Zambia [133]. They found that workers in African compared lacked training and safety culture in comparison to those in China and Greece.
Unfortunately, the statistics of foodborne disease outbreaks in developing countries are scarce, and adequate product resources for safe food are few [134]. Therefore, the safety culture and personal training identified by Nyarugwe et al. in African companies could be extrapolated to those in Latin America [133]. In addition, the challenges of the COVID-19 pandemic require better hygiene practices in the general population. For instance, male workers were reported to have a greater sense of risk of contracting SARS-CoV-2, but they took fewer safety measures to protect themselves, compared to female employees [118].
Mohammadi-Nasrabadi et al. assessed the knowledge on health and food safety during the COVID-19 pandemic in restaurant personnel only to discover that none of them had received any training on this topic [135]. The authors classified the level of COVID-19 awareness in restaurant workers as low (17%), moderate (35.2%), and good (47.2%). After the training, these percentages increased.
CONCLUSION
Food safety has the potential to have a strong impact on different sectors of each nation. By supplying healthy food to the population, governments can reduce the occurrence of foodborne diseases. Companies that produce, transport, or trade in perishables should raise the awareness of their employees about refrigeration equipment, its maintenance, calibration,
and temperature monitoring. This simple measure is especially important in developing countries, where it could improve food handling at each supply chain step.
The present work stresses the need to use refrigeration equipment that ensures temperature control at each stage of the cold chain because various potential microorganisms may affect meat products' safety and shelf life. An appropriate cold chain management could reduce food wastage, especially in developing countries, thus decreasing carbon print. An effective cold chain possesses a reliable traceability and contributes to international efforts against the COVID-19 pandemic. Therefore, effective food cold chain management standards increase food safety and prevent the spread of SARS-CoV-2.
CONTRIBUTION
P. Arriaga-Lorenzo compiled the bibliography and initiated the research. P. Arriaga-Lorenzo, E. de Jesús Maldonado-Simán, R. Ramírez-Valverde, P.A. Martínez-Hernández, D.N. Tirado-González, and L.A. Saavedra-Jiménez participated in the analysis and discussion of each topic. All the authors approved the final version of the manuscript.
CONFLICT OF INTEREST
The authors declare that there are no conflicts of interest regarding the publication of this article.
ACKNOWLEDGEMENTS
The support of the Consejo Nacional de Ciencia y Tecnología (CONACyT) of Mexico is gratefully acknowledged.
REFERENCES
1. Buaynova IV. Simulating the refrigeration of batch dairy products in a multizone cold supply system. Foods and Raw Materials. 2014;2(2):121-129. https://doi.org/10.12737/5469
2. Mercier S, Villeneuve S, Mondor M, Uysal I. Time-temperature management along the food cold chain: A review of recent developments. Comprehensive Reviews in Food Science and Food Safety. 2017;16(4):647-667. https://doi. org/10.1111/1541-4337.12269
3. Li X, Zhou K. Multi-objective cold chain logistic distribution center location based on carbon emission. Environmental Science and Pollution Research. 2021;28(25):32396-32404. https://doi.org/10.1007/s11356-021-12992-w
4. Kaur H, Singh SP. Modeling low carbon procurement and logistics in supply chain: A key towards sustainable production. Sustainable Production and Consumption. 2017;11:5-17. https://doi.org/10.1016Zj.spc.2017.03.001
5. Mariano EB, Gobbo JA, Camioto FC, Rebelatto DAN. CO2 emissions and logistics performance: A composite index proposal. Journal of Cleaner Production. 2017;163:166-178. https://doi.org/10.1016/jjclepro.2016.05.084
6. Liu J, Li F, Li T, Yun Z, Duan X, Jiang Y. Fibroin treatment inhibits chilling injury of banana fruit via energy regulation. Scientia Horticulturae. 2019;248:8-13. https://doi.org/10.1016/j.scienta.2018.12.052
7. East A, Smale N, Kang S. A method for quantitative risk assessment of temperature control in insulated boxes. International Journal of Refrigeration. 2009;32(6):1505-1513. https://doi.org/10.1016/j.ijrefrig.2009.01.020
8. The state of food and agriculture 2019. Moving forward on food loss and waste reduction. Rome: FAO; 2019. 182 p.
9. Loisel J, Duret S, Cornuéjols A, Cagnon D, Tardet M, Derens-Bertheau E, et al. Cold chain break detection and analysis: Can machine learning help? Trends in Food Science and Technology. 2021;112:391-399. https://doi. org/10.1016/j.tifs.2021.03.052
10. Skawinska E, Zalewski RI. Economic impact of temperature control during food transportation - A COVID-19 perspective. Foods. 2022;11(3). https://doi.org/10.3390/foods11030467
11. Cai J, Sun W, Huang J, Gamber M, Wu J, He G. Indirect virus transmission in cluster of COVID-19 cases, Wenzhou, China, 2020. Emerging Infectious Diseases. 2020;26(6):1343-1345. https://doi.org/10.3201/eid2606.200412
12. Xie C, Zhao H, Li K, Zhang Z, Lu X, Peng H, et al. The evidence of indirect transmission of SARS-CoV-2 reported in Guangzhou, China. BMC Public Health. 2020;20(1). https://doi.org/10.1186/s12889-020-09296-y
13. Aboubakr HA, Sharafeldin TA, Goyal SM. Stability of SARS-CoV-2 and other coronaviruses in the environment and on common touch surfaces and the influence of climatic conditions: A review. Transboundary and Emerging Diseases. 2021;68(2):296-312. https://doi.org/10.1111/tbed.13707
14. Ji W, Li X, Chen S, Ren L. Transmission of SARS-CoV-2 via fomite, especially cold chain, should not be ignored. Proceedings of the National Academy of Sciences of the United States of America. 2021;118(11). https://doi. org/10.1073/pnas.2026093118
15. The Food Supply Chain [Internet]. [cited 2022 Apr 15]. Available from: https://www.fao.org/family-farming/detail/ es/c/1116584
16. Global food losses and food waste - extent, causes and prevention [Internet]. [cited 2022 Apr 15]. Available from: https://www.fao.org/sustainable-food-value-chains/library/detalles/es/c/266053
17. Xue L, Liu G, Parfitt J, Liu X, Van Herpen E, Stenmarck Á, et al. Missing food, missing data? A critical review of global food losses and food waste data. Environmental Science and Technology. 2017;51(12):6618-6633. https://doi. org/10.1021/acs.est.7b00401
18. Food waste index report 2021. United Nations Environment Programme; 2021. 100 p.
19. Araujo GP, Lourengo CE, Araújo CML, Bastos A. Intercambio Brasil-Uniao Europeia sobre desperdicio de alimentos: relatório final. Brasilia: Diálogos Setoriais Uniao Europeia - Brasil; 2018. 40 p. (In Portuguese).
20. Kemper K, Voegele J, Hickey V, Ahuja PS, Poveda R, Edmeades S, et al. A conceptual framework for a national strategy on food loss and waste in Mexico. 2019.
21. Project on master plan study for integrated solid waste management in Bogota D.C. Bogota: Kokusai Kogyo, Ex Research Institute; 2013. 428 p.
22. Montanari R. Cold chain tracking: A managerial perspective. Trends in Food Science and Technology. 2008;19(8):425-431. https://doi.org/10.1016/j.tifs.2008.03.009
23. Ndraha N, Hsiao H-I, Vlajic J, Yang M-F, Lin H-TV. Time-temperature abuse in the food cold chain: Review of issues, challenges, and recommendations. Food Control. 2018;89:12-21. https://doi.org/10.1016/j.foodcont.2018.01.027
24. Taoukis PS, Gogou E, Tsironi T, Giannoglou M, Dermesonlouoglou E, Katsaros G. Food cold chain management and optimization. In: Nedovic V, Raspor P, Levic J, Saponjac VT, Barbosa-Cánovas GV, editors. Emerging and traditional technologies for safe, healthy and quality food. Cham: Springer; 2016. pp. 285-309. https://doi.org/10.1007/978-3-319-24040-4_16
25. International Dictionary of Refrigeration [Internet]. [cited 2022 Apr 15]. Available from: https://dictionary.iifiir.org/p? inputLang=en&truncPos=right&srchTerm=cold+chain&outputLang=xx&defnLang=en&submit=View+results&disp Lang=en&_ga=2.155921083.12016883.1632520040-1547586917.1632520040
26. Tromp S-O, Haijema R, Rijgersberg H, van der Vorst JGAJ. A systematic approach to preventing chilled-food waste at the retail outlet. International Journal of Production Economics. 2016;182:508-518. https://doi.org/10.1016/j. ijpe.2016.10.003
27. Koutsoumanis KP, Gougouli M. Use of time temperature Integrators in food safety management. Trends in Food Science and Technology. 2015;43(2):236-244. https://doi.org/10.1016Zj.tifs.2015.02.008
28. Kumari L, Narsaiah K, Grewal MK, Anurag RK. Application of RFID in agri-food sector. Trends in Food Science and Technology. 2015;43(2):144-161. https://doi.org/10.1016/j.tifs.2015.02.005
29. Joshi K, Warby J, Valverde J, Tiwari B, Cullen PJ, Frias JM. Impact of cold chain and product variability on quality attributes of modified atmosphere packed mushrooms (Agaricus bisporus) throughout distribution. Journal of Food Engineering. 2018;232:44-55. https://doi.org/10.1016/jjfoodeng.2018.03.019
30. Likar K, Jevsnik M. Cold chain maintaining in food trade. Food Control. 2006;17(2):108-113. https://doi.org/10.1016/ j.foodcont.2004.09.009
31. Lundén J, Vanhanen V, Kotilainen K, Hemminki K. Retail food stores' internet-based own-check databank records and health officers' on-site inspection results for cleanliness and food holding temperatures reveal inconsistencies. Food Control. 2014;35(1):79-84. https://doi.org/10.1016/jibodcont.2013.06.050
32. Lundén J, Vanhanen V, Myllymaki T, Laamanen E, Kotilainen K, Hemminki K. Temperature control efficacy of retail refrigeration equipment. Food Control. 2014;45:109-114. https://doi.org/10.1016/j.foodcont.2014.04.041
33.
34.
35.
36.
37.
38.
39.
40
41
42
43
44
45
46
47
48
49
50
51
52
Rediers H, Claes M, Peeters L, Willems KA. Evaluation of the cold chain of fresh-cut endive from farmer to plate. Postharvest Biology and Technology. 2009;51(2):257-262. https://doi.org/10.1016/j.postharvbio.2008.07.017
McKellar RC, LeBlanc DI, Lu J, Delaquis P. Simulation of Escherichia coli O157:H7 behavior in fresh-cut lettuce under dynamic temperature conditions during distribution from processing to retail. Foodborne Pathogens and Disease. 2012;9(3):239-244. https://doi.org/10.1089/fpd.2011.1025
Frank D, Zhang Y, Li Y, Luo X, Chen X, Kaur M, et al. Shelf life extension of vacuum packaged chilled beef in the Chinese supply chain. A feasibility study. Meat Science. 2019;153:135-143. https://doi.org/10.1016/j.meatsci.2019.03.006
Tingman W, Jian Z, Xiaoshuan Z. Fish product quality evaluation based on temperature monitoring in cold chain. African Journal of Biotechnology. 2010;9(37):6146-6151.
Derens E, Palagos B, Guilpart J. The cold chain of chilled products under supervision in France. IUFoST. 2006;19:51-64. https://doi.org/10.1051/IUFoST:20060823
Morelli E, Derens E. Temperature evolution of the smoked salmon during the logistical circuits. Revue Générale Du Froid et Du Conditionnement d'Air. 2009:51-56.
Koutsoumanis K, Pavlis A, Nychas G-JE, Xanthiakos K. Probabilistic model for Listeria monocytogenes growth during distribution, retail storage, and domestic storage of pasteurized milk. Applied and Environmental Microbiology. 2010;76(7):2181-2191. https://doi.org/10.1128/AEM.02430-09
Mai NTT, Margeirsson B, Margeirsson S, Bogason SG, Sigurgísladóttir S, Arason S. Temperature mapping of fresh fish supply chains - air and sea transport. Journal of Food Process Engineering. 2012;35(4):622-656. https://doi. org/10.1111/j.1745-4530.2010.00611.x
Koseki S, Isobe S. Prediction of pathogen growth on iceberg lettuce under real temperature history during distribution from farm to table. International Journal of Food Microbiology. 2005;104(3):239-248. https://doi.org/10.1016/ j.ijfoodmicro.2005.02.012
Goedhals-Gerber LL, Haasbroek L, Freiboth H, van Dyk FE. An analysis of the influence of logistics activities on the export cold chain of temperature sensitive fruit through the Port of Cape Town. Journal of Transport and Supply Chain Managemen. 2015;9(1). https://doi.org/10.4102/jtscm.v9i1.201
Goedhals-Gerber LL, Stander C, van Dyk FE. Maintaining cold chain integrity: Temperature breaks within fruit reefer containers in the Cape Town Container Terminal. Southern African Business Review. 2017;21(1):362-384.
Jofré A, Latorre-Moratalla ML, Garriga M, Bover-Cid S. Domestic refrigerator temperatures in Spain: Assessment of its impact on the safety and shelf-life of cooked meat products. Food Research International. 2019;126. https://doi. org/10.1016/j.foodres.2019.108578
Baldera Zubeldia B, Nieto Jiménez M, Valenzuela Claros MT, Mariscal Andrés JL, Martin-Olmedo P. Effectiveness of the cold chain control procedure in the retail sector in Southern Spain. Food Control. 2016;59:614-618. https://doi. org/10.1016/j.foodcont.2015.06.046
Ndraha N, Sung W-C, Hsiao H-I. Evaluation of the cold chain management options to preserve the shelf life of frozen shrimps: A case study in the home delivery services in Taiwan. Journal of Food Engineering. 2019;242:21-30. https:// doi.org/10.1016/j.jfoodeng.2018.08.010
Chaitangjit P, Ongkunaruk P. The study of cold storage and temperature controlled transportation: A case study of a chain restaurant in Thailand. Pamukkale University Journal of Engineering Sciences. 2019;25(9):1014-1019. https:// doi.org/10.5505/pajes.2019.81231
Love DC, Kuehl LM, Lane RM, Fry JP, Harding J, Davis BJK, et al. Performance of cold chains and modeled growth of Vibrio parahaemolyticus for farmed oysters distributed in the United States and internationally. International Journal of Food Microbiology. 2020;313. https://doi.org/10.1016/j.ijfoodmicro.2019.108378
Zeng W, Vorst K, Brown W, Marks BP, Jeong S, Pérez-Rodríguez F, et al. Growth of Escherichia coli O157:H7 and Listeria monocytogenes in packaged fresh-cut romaine mix at fluctuating temperatures during commercial transport, retail storage, and display. Journal of Food Protection. 2014;77(2):197-206. https://doi.org/10.4315/0362-028X.JFP-13-117
Brown W, Ryser E, Gorman L, Steinmaus S, Vorst K. Transit temperatures experienced by fresh-cut leafy greens during cross-country shipment. Food Control. 2016;61:146-155. https://doi.org/10.1016/j.foodcont.2015.09.014 Duret S, Hoang H-M, Guillier L, Derens-Bertheau E, Dargaignaratz C, Oriol S, et al. Interactions between refrigeration temperatures, energy consumption in a food plant and microbiological quality of the food product: Application to refrigerated stuffed pasta. Food Control. 2021;126. https://doi.org/10.1016/j.foodcont.2021.108076 Monforti-Ferrario F, Dallemand J-F, Pinedo Pascua I, Motola V, Banja M, Scarlat N, et al. Energy use in the EU food sector: State of play and opportunities for improvement. European Union; 2015. 176 p. https://doi.org/10.2790/ 266295
53. Tassou SA, Lewis JS, Ge YT, Hadawey A, Chaer I. A review of emerging technologies for food refrigeration applications. Applied Thermal Engineering. 2010;30(4):263-276. https://doi.org/10.1016/j.applthermaleng.2009.09.001
54. Laguerre O, Chaomuang N. Closed refrigerated display cabinets: Is it worth it for food quality? Research anthology on food waste reduction and alternative diets for food and nutrition security. IGI Global; 2021. pp. 99-121. https://doi. org/10.4018/978-1-7998-5354-1.ch005
55. Hundy GF, Trott AR, Welch T. The cold chain - transport, storage, retail. In: Hundy GF, Trott AR, Welch TC, editors. Refrigeration, air conditioning and heat pumps. Butterworth-Heinemann; 2016. pp. 273-287. https://doi.org/10.1016/ B978-0-08-100647-4.00017-6
56. Brecht PE, Brecht JK, Saenz JE. Temperature-controlled transport for air, land, and sea. In: Yahia EM, editor. Postharvest technology of perishable horticultural commodities. Woodhead Publishing; 2019. pp. 591-637. https:// doi.org/10.1016/B978-0-12-813276-0.00018-3
57. Kitinoja L. Use of cold chains for reducing food losses in developing countries. PEF White Paper No 13-03 [Internet]. [cited 2022 Apr 16]. Available from: http://www.postharvest.org/Cold_chains_PEF_White_Paper_13_03.pdf
58. The validity of food miles as an indicator of sustainable development. Final Report produced for DEFRA [Internet]. [cited 2022 Apr 16]. Available from: https://library.uniteddiversity.coop/Food/DEFRA_Food_Miles_Report.pdf
59. Pirog RS, Van Pelt T, Enshayan K, Cook E. Food, fuel, and freeways: An Iowa perspective on how far food travels, fuel usage, and greenhouse gas emissions [Internet]. [cited 2022 Apr 16]. Available from: https://www.leopold.iastate. edu/files/pubs-and-papers/2011-06-food-fuel-and-freeways-iowa-perspective-how-far-food-travels-fuel-usage-and-greenhouse-gas-emissions.pdf
60. McKellar RC, LeBlanc DI, Rodriguez FP, Delaquis P. Comparative simulation of Escherichia coli O157:H7 behaviour in packaged fresh-cut lettuce distributed in a typical Canadian supply chain in the summer and winter. Food Control. 2014;35(1):192-919. https://doi.org/10.1016/jibodcont2013.06.002
61. Pelletier W, Brecht JK, Nunes, MCN, Emond J-P. Quality of strawberries shipped by truck from California to Florida as influenced by postharvest temperature management practices. HortTechnology. 2011;21(4):482-493. https://doi. org/10.21273/H0RTTECH.21.4.482
62. Abad E, Palacio F, Nuin M, Zarate AG, Juarros A, Gomez JM, et al. RFID smart tag for traceability and cold chain monitoring of foods: Demonstration in an intercontinental fresh fish logistic chain. Journal of Food Engineering. 2009;93(4):394-399. https://doi.org/10.1016/j.jfoodeng.2009.02.004
63. Pelletier W, Nunes do Nascimento MC, Emond J-P. Air transportation of fruits and vegetables: An update. Stewart Postharvest Review. 2005;1(1). https://doi.org/10.2212/spr.2005.L5
64. Arduino G, Carrillo Murillo D, Parola F. Refrigerated container versus bulk: Evidence from the banana cold chain. Maritime Policy and Management. 2015;42(3):228-245. https://doi.org/10.1080/03088839.2013.851421
65. Jedermann R, Praeger U, Geyer M, Lang W. Remote quality monitoring in the banana chain. Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences. 2014;372(2017). https://doi.org/10.1098/ rsta.2013.0303
66. Laguerre O, Hoang HM, Flick D. Experimental investigation and modelling in the food cold chain: Thermal and quality evolution. Trends in Food Science and Technology. 2013;29(2):87-97. https://doi.org/10.1016/j.tifs.2012.08.001
67. Leungtongkum T, Flick D, Hoang HM, Steven D, Delahaye A, Laguerre O. Insulated box and refrigerated equipment with PCM for food preservation: State of the art. Journal of Food Engineering. 2022;317. https://doi.org/10.1016/ j.jfoodeng.2021.110874
68. Robertson J, Franzel L, Maire D. Innovations in cold chain equipment for immunization supply chains. Vaccine. 2017;35(17):2252-2259. https://doi.org/10.1016/j.vaccine.2016.11.094
69. Singh S, Gaikwad KK, Lee M, Lee YS. Temperature sensitive smart packaging for monitoring the shelf life of fresh beef. Journal of Food Engineering. 2018;234:41-49. https://doi.org/10.1016/j.jfoodeng.2018.04.014
70. Derens-Bertheau E, Osswald V, Laguerre O, Alvarez G. Cold chain of chilled food in France. International Journal of Refrigeration. 2015;52:161-167. https://doi.org/10.1016/jijrefrig.2014.06.012
71. Goransson M, Nilsson F, Jevinger A. Temperature performance and food shelf-life accuracy in cold food supply chains -Insights from multiple field studies. Food Control. 2018;86:332-341. https://doi.org/10.1016/j.foodcont.2017.10.029
72. Morelli E, Noel V, Rosset P, Poumeyrol G. Performance and conditions of use of refrigerated display cabinets among producer/vendors of foodstuffs. Food Control. 2012;26(2):363-368. https://doi.org/10.1016/j.foodcont. 2012.02.002
73. Ben-abdallah R, Leducq D, Hoang HM, Pateau O, Ballot-Miguet B, Delahaye A, et al. Modeling and experimental investigation for load temperature prediction at transient conditions of open refrigerated display cabinet using Modelica environment. International Journal of Refrigeration. 2018;94:102-110. https://doi.org/10.1016/jijrefrig.2018.02.017
74. Navaz HK, Henderson BS, Faramarzi R, Pourmovahed A, Taugwalder F. Jet entrainment rate in air curtain of open refrigerated display cases. International Journal of Refrigeration. 2005;28(2):267-275. https://doi.org/10.1016/ j.ijrefrig.2004.08.002
75. Maouris G, Sarabia Escriva EJ, Acha S, Shah N, Markides CN. CO2 refrigeration system heat recovery and thermal storage modelling for space heating provision in supermarkets: An integrated approach. Applied Energy. 2020;264. https://doi.org/10.1016/j.apenergy.2020.114722
76. Mylona Z, Kolokotroni M, Tsamos KM, Tassou SA. Comparative analysis on the energy use and environmental impact of different refrigeration systems for frozen food supermarket application. Energy Procedia. 2017;123:121-130. https://doi.org/10.1016/j.egypro.2017.07.234
77. Tassou SA, Ge Y, Hadawey A, Marriott D. Energy consumption and conservation in food retailing. Applied Thermal Engineering. 2011;31(2-3):147-156. https://doi.org/10.1016/j.applthermaleng.2010.08.023
78. Efstratiadi M, Acha S, Shah N, Markides CN. Analysis of a closed-loop water-cooled refrigeration system in the food retail industry: A UK case study. Energy. 2019;174:1133-1144. https://doi.org/10.1016Zj.energy.2019.03.004
79. Subramaniam P. The stability and shelf life of food. A volume in Woodhead Publishing series in food science, technology and nutrition. Second Ed. Woodhead Publishing; 2016. 612 p. https://doi.org/10.1016/C2015-0-06842-3
80. Sun XD, Holley RA. Antimicrobial and antioxidative strategies to reduce pathogens and extend the shelf life of fresh red meats. Comprehensive Reviews in Food Science and Food Safety. 2012;11(4):340-354. https://doi.org/10.1111/ j.1541-4337.2012.00188.x
81. Lee H, Yoon Y. Etiological agents implicated in foodborne illness world wide. Food Science of Animal Resources. 2021;41:1-7. https://doi.org/10.5851/kosfa.2020.e75
82.Vorst K, Shivalingaiah N, Monge Brenes AL, Coleman S, Mendonga A, Brown JW, et al. Effect of display case cooling technologies on shelf-life of beef and chicken. Food Control. 2018;94:56-64. https://doi.org/10.1016/ j.foodcont.2018.06.022
83. Dave D, Ghaly AE. Meat spoilage mechanisms and preservation techniques: A critical review. American Journal of Agricultural and Biological Sciences. 2011;6(4):486-510. https://doi.org/10.3844/ajabssp.2011.486.510
84. Jay JM, Loessner MJ, Golden DA. Modern food microbiology. 7th ed. New York: Springer; 2005. 790 p. https://doi. org/10.1007/b100840
85. Kotsiri Z, Vidic J, Vantarakis A. Applications of biosensors for bacteria and virus detection in food and water - A systematic review. Journal of Environmental Sciences. 2022;111:367-379. https://doi.org/10.1016/jjes.2021.04.009
86. Lambert AD, Smith JP, Dodds KL. Shelf life extension and microbiological safety of fresh meat - a review. Food Microbiology. 1991;8(4):267-297. https://doi.org/10.1016/S0740-0020(05)80002-4
87. Raab V, Petersen B, Kreyenschmidt J. Temperature monitoring in meat supply chains. British Food Journal. 2011;113(10):1267-1289. https://doi.org/10.1108/00070701111177683
88. Novoa CP, Restrepo LP. Influence of psichrotrophic bacteria in proteolytic activity of milk. Revista de La Facultad de Medicina Veterinaria y de Zootecnia. 2007;54(1):9-16.
89. James C, Onarinde BA, James SJ. The use and performance of household refrigerators: A review. Comprehensive Reviews in Food Science and Food Safety. 2017;16(1):160-179. https://doi.org/10.1111/1541-4337.12242
90. The European Union One Health 2019 Zoonoses Report. EFSA Journal. 2021;19(2). https://doi.org/10.2903/ j.efsa.2021.6406
91. Wu S, Xu S, Chen X, Sun H, Hu M, Bai Z, et al. Bacterial communities changes during food waste spoilage. Scientific Reports. 2018;8(1). https://doi.org/10.1038/s41598-018-26494-2
92. Kaper JB, Nataro JP, Mobley HLT. Pathogenic Escherichia coli. Nature Reviews Microbiology. 2004;2:123-140. https://doi.org/10.1038/nrmicro818
93. Amir M, Riaz M, Chang Y-F, Ismail A, Hameed A, Ahsin M. Antibiotic resistance in diarrheagenic Escherichia coli isolated from broiler chickens in Pakistan. Journal of Food Quality and Hazards Control. 2021;8(2):78-86. https://doi. org/10.18502/jfqhc.8.2.6472
94. Coronavirus disease (COVID-19) pandemic [Internet]. [cited 2022 Apr 17]. Available from: https://www.who.int/ emergencies/diseases/novel-coronavirus-2019
95. Normile D. Source of Beijing's big new COVID-19 outbreak is still a mystery. Science. 2020. https://doi.org/10.1126/ science.abd3890
96. Yang J, Niu P, Chen L, Wang L, Zhao L, Huang B, et al. Genetic tracing of HCoV-19 for the re-emerging outbreak of COVID-19 in Beijing, China. Protein and Cell. 2021;12(1):4-6. https://doi.org/10.1007/s13238-020-00772-0
97. How to import foreign food safety? [Internet]. [cited 2022 Apr 17]. Available from: https://www.ccdi.gov.cn/ toutiao/202008/t20200815 223796.html
98. Adelodun B, Ajibade FO, Tiamiyu AO, Nwogwu NA, Ibrahim RG, Kumar P, et al. Monitoring the presence and persistence of SARS-CoV-2 in water-food-environmental compartments: State of the knowledge and research needs. Environmental Research. 2021;200. https://doi.org/10.1016/j.envres.2021.111373
99. Waltenburg MA, Victoroff T, Rose CE, Butterfield M, Jervis RH, Fedak KM, et al. Update: COVID-19 among workers in meat and poultry processing facilities - United States, April-May 2020. Morbidity and Mortality Weekly Report. 2020;69(27):887-892. https://doi.org/10.15585/MMWR.MM6927E2
100. Bivins A, Greaves J, Fischer R, Yinda KC, Ahmed W, Kitajima M, et al. Persistence of SARS-CoV-2 in Water and wastewater. Environmental Science and Technology Letters. 2020;7(12):937-942. https://doi.org/10.1021/acs. estlett.0c00730
101. Lee YJ, Kim JH, Choi BS, Choi JH, Jeong YI. Characterization of severe acute respiratory syndrome coronavirus 2 stability in multiple water matrices. Journal of Korean Medical Science. 2020;117(13):7001-7003. https://doi. org/10.3346/jkms.2020.35.e330
102. Dai M, Li H, Yan N, Huang J, Zhao L, Xu S, et al. Long-term survival of SARS-CoV-2 on salmon as a source for international transmission. Journal of Infectious Diseases. 2021;223(3):537-539. https://doi.org/10.1093/infdis/jiaa712
103. Ahmed F, Islam MA, Kumar M, Hossain M, Bhattacharya P, Islam MT, et al. First detection of SARS-CoV-2 genetic material in the vicinity of COVID-19 isolation Centre in Bangladesh: Variation along the sewer network. Science of the Total Environment. 2021;776. https://doi.org/10.1016/j.scitotenv.2021.145724
104. Hokajarvi A-M, Rytkonen A, Tiwari A, Kauppinen A, Oikarinen S, Lehto K-M, et al. The detection and stability of the SARS-CoV-2 RNA biomarkers in wastewater influent in Helsinki, Finland. Science of the Total Environment. 2021;770. https://doi.org/10.1016/j.scitotenv.2021.145274
105. de Oliveira LC, Torres-Franco AF, Lopes BC, Santos BSAS, Costa EA, Costa MS, et al. Viability of SARS-CoV-2 in river water and wastewater at different temperatures and solids content. Water Research. 2021;195. https://doi. org/10.1016/j.watres.2021.117002
106. Singh M, Sadat A, Abdi R, Colaruotolo LA, Francavilla A, Petker K, et al. Detection of SARS-CoV-2 on surfaces in food retailers in Ontario. Current Research in Food Science. 2021;4:598-602. https://doi.org/10.1016/ j.crfs.2021.08.009
107. Blondin-Brosseau M, Harlow J, Doctor T, Nasheri N. Examining the persistence of human Coronavirus 229E on fresh produce. Food Microbiology. 2021;98. https://doi.org/10.1016/j.fm.2021.103780
108. Le Guernic A, Palos Ladeiro M, Boudaud N, Do Nascimento J, Gantzer C, Inglard J-C, et al. First evidence of SARS-CoV-2 genome detection in zebra mussel (Dreissena polymorpha). Journal of Environmental Management. 2022;301. https://doi.org/10.1016/j.jenvman.2021.113866
109. Castrica M, Balzaretti C, Miraglia D, Lorusso P, Pandiscia A, Tantillo G, et al. Evaluation of the persistence of SARS-CoV-2 (ATCC® VR-1986HK™) on two different food contact materials: flow pack polyethylene and polystyrene food trays. LWT. 2021;146. https://doi.org/10.1016/j.lwt.2021.111606
110. Rizou M, Galanakis IM, Aldawoud TMS, Galanakis CM. Safety of foods, food supply chain and environment within the COVID-19 pandemic. Trends in Food Science and Technology. 2020;102:293-299. https://doi.org/10.1016/ j.tifs.2020.06.008
111. Can the sewers disclose the scale of COVID-19? [Internet]. [cited 2022 Apr 18]. Available from: https://www.niva. no/en/news/can-the-sewers-disclose-the-scale-of-covid-19
112. Feng X-L, Li B, Lin H-F, Zheng H-Y, Tian R-R, Luo R-H, et al. Stability of SARS-CoV-2 on the surfaces of three meats in the setting that simulates the cold chain transportation. Virologica Sinica. 2021;36(5):1069-1072. https:// doi.org/10.1007/s12250-021-00367-x
113. Ji W, Wang W, Zhao X, Zai J, Li X. Cross-species transmission of the newly identified coronavirus 2019-nCoV Journal of Medical Virology. 2020;92(4):433-440. https://doi.org/10.1002/jmv.25682
114. Paraskevis D, Kostaki EG, Magiorkinis G, Panayiotakopoulos G, Sourvinos G, Tsiodras S. Full-genome evolutionary analysis of the novel corona virus (2019-nCoV) rejects the hypothesis of emergence as a result of a recent recombination event. Infection, Genetics and Evolution. 2020;79. https://doi.org/10.1016/j.meegid.2020.104212
115. Lau SKP, Luk HKH, Wong ACP, Li KSM, Zhu L, He Z, et al. Possible Bat origin of severe acute respiratory syndrome coronavirus 2. Emerging Infectious Diseases. 2020;26(7):1542-1547. https://doi.org/10.3201/eid2607.200092
116. Gorur N, Topalcengiz Z. Food safety knowledge, hygiene practices, and eating attitudes of academics and university students during the coronavirus (COVID-19) pandemic in Turkey. Journal of Food Safety. 2021;41(5). https://doi. org/10.1111/jfs.12926
117. Coronavirus disease 2019 (COVID-19) Situation Report - 32. [Internet]. [cited 2022 Apr 18]. Available from: https://www.who.int/docs/default-source/coronaviruse/situation-reports/20200221-sitrep-32-covid-19. pdf?sfvrsn=4802d089_2
118. Thomas MS, Feng Y. Consumer risk perception and trusted sources of food safety information during the COVID-19 pandemic. Food Control. 2021;130. https://doi.org/10.1016/j.foodcont.2021.108279
119. Chang A, Schnall AH, Law R, Bronstein AC, Marraffa JM, Spiller HA, et al. Cleaning and disinfectant chemical exposures and temporal associations with COVID-19 - National poison data system, United States, January 1, 2020 -March 31, 2020. Morbidity and Mortality Weekly Report. 2020;69(16):496-498. https://doi.org/10.15585/mmwr. mm6916e1
120. Finger JAFF, Lima EMF, Coelho KS, Behrens JH, Landgraf M, Franco BDGM, et al. Adherence to food hygiene and personal protection recommendations for prevention of COVID-19. Trends in Food Science and Technology. 2021;112:847-852. https://doi.org/10.1016/j.tifs.2021.03.016
121. Gil MI, Selma MV, López-Gálvez F, Allende A. Fresh-cut product sanitation and wash water disinfection: Problems and solutions. International Journal of Food Microbiology. 2009;134(1-2):37-45. https://doi.org/10.1016/ j.ijfoodmicro.2009.05.021
122. Pezzuto A, Belluco S, Losasso C, Patuzzi I, Bordin P, Piovesana A, et al. Effectiveness of washing procedures in reducing Salmonella enterica and Listeria monocytogenes on a raw leafy green vegetable (Eruca vesicaria). Frontiers in Microbiology. 2016;7. https://doi.org/10.3389/fmicb.2016.01663
123. Bailey ES, Curcic M, Sobsey MD. Persistence of Coronavirus Surrogates on Meat and Fish Products during Long-Term Storage. Applied and Environmental Microbiology. 2022;88(12). https://doi.org/10.1128/aem.00504-22
124. Chen C, Feng Y, Chen Z, Xia Y, Zhao X, Wang J, et al. SARS-CoV-2 cold-chain transmission: Characteristics, risks, and strategies. Journal of Medical Virology. 2022;94(8):3540-3547. https://doi.org/10.1002/jmv.27750
125. Bai L, Wang Y, Wang Y, Wu Y, Li N, Liu Z. Controlling COVID-19 transmission due to contaminated imported frozen food and food packaging. China CDC Weekly. 2021;3(2):30-33.
126. Anelich LECM, Lues R, Farber JM, Parreira VR. SARS-CoV-2 and risk to food safety. Frontiers in Nutrition. 2020;7. https://doi.org/10.3389/fnut.2020.580551
127. Chin AWH, Poon LLM. Stability of SARS-CoV-2 in different environmental conditions - Authors' reply. The Lancet Microbe. 2020;1(4). https://doi.org/10.1016/S2666-5247(20)30095-1
128. Qian J, Yu Q, Jiang L, Yang H, Wu W. Food cold chain management improvement: A conjoint analysis on COVID-19 and food cold chain systems. Food Control. 2022;137. https://doi.org/10.1016/j.foodcont.2022.108940
129. Alam MK, Keiko Y, Hossain MM. Present working conditions in slaughterhouses and meat selling centres and food safety of workers in two districts of Bangladesh. Pertanika Journal of Social Sciences and Humanities. 2020;28(2):867-881.
130. Mayurnikova LA, Koksharov AA, Krapiva TV. Food safety practices in catering during the coronavirus COVID-19 pandemic. Foods and Raw Materials. 2020;8(2):197-203. DOI: http://doi.org/10.21603/2308-4057-2020-2-197-203
131. Maldonado-Siman E, Bernal-Alcántara R, Cadena-Meneses JA, Altamirano-Cárdenas JR, Martinez-Hernández PA. Implementation of quality systems by Mexican exporters of processed meat. Journal of Food Protection. 2014;77(12):2148-2152. https://doi.org/10.4315/0362-028X.JFP-14-003
132. Maldonado-Siman E, Martínez-Hernández PA, Ruíz-FloresA, García-Muñiz JG, Cadena-Meneses JA. Implementation of HACCP in the Mexican poultry processing industry. IFIP Advances in Information and Communication Technology. 2009;295:1757-1767. https://doi.org/10.1007/978-1-4419-0213-9_26
133. Nyarugwe SP, Linnemann AR, Ren Y, Bakker E-J, Kussaga JB, Watson D, et al. An intercontinental analysis of food safety culture in view of food safety governance and national values. Food Control. 2020;111. https://doi. org/10.1016/j.foodcont.2019.107075
134. Grace D. Food safety in low and middle income countries. International Journal of Environmental Research and Public Health. 2015;12(9):10490-10507. https://doi.org/10.3390/ijerph120910490
135. Mohammadi-Nasrabadi F, Salmani Y, Esfarjani F. A quasi-experimental study on the effect of health and food safety training intervention on restaurant food handlers during the COVID-19 pandemic. Food Science and Nutrition. 2021;9(7):3655-3663. https://doi.org/10.1002/fsn3.2326
ORCID IDs
Pedro Arriaga-Lorenzo https://orcid.org/0000-0001-8061-9986 Erna de Jesús Maldonado-Simán https://orcid.org/0000-0002-1692-3198 Rodolfo Ramírez-Valverde https://orcid.org/0000-0002-3185-8494 Pedro Arturo Martínez-Hernández https://orcid.org/0000-0003-2197-3736 Deli Nazmín Tirado-González https://orcid.org/0000-0002-5668-9025 Luis Antonio Saavedra-Jiménez https://orcid.org/0000-0001-6124-7240
