Comprehensive Risk Pathway of the Qualitative Likelihood of Human Exposure to Severe Acute Respiratory Syndrome Coronavirus 2 from the Food Chain

ABSTRACT

A group of experts from all Canadian federal food safety partners was formed to monitor the potential issues relating to severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) food contamination, to gather and consider all of the relevant evidence and to determine the impact for Canadian food safety. A comprehensive risk pathway was generated to consider the likelihood of a SARS-CoV-2 contamination event at any of the relevant steps of the food processing and handling chain and the potential for exposure and transmission of the virus to the consumer. The scientific evidence was reviewed and assessed for each event in the pathway, taking into consideration relevant elements that could increase or mitigate the risk of contamination. The advantage of having an event-wise contextualization of the SARS-CoV-2 transmission pathway through the food chain is that it provides a systematic and consistent approach to evaluate any new data and communicate its importance and impact. The pathway also increases the objectivity and consistency of the assessment in a rapidly evolving and high-stakes situation. Based on our review and analysis, there is currently no comprehensive epidemiological evidence of confirmed cases of SARS-CoV-2, or its known variants, causing coronavirus disease 2019 from transmission through food or food packaging. Considering the remote possibility of exposure through food, the likelihood of exposure by ingestion or contact with mucosa is considered negligible to very low, and good hygiene practices during food preparation should continue to be followed.

At the end of 2019, a new coronavirus strain emerged, causing an outbreak of respiratory illness in China. This new strain was identified as severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), a Betacoronavirus that causes the disease known as coronavirus disease 2019 (COVID-19). In March 2020, the World Health Organization declared the situation a pandemic when more than 118,000 cases and 4,200 deaths were reported among 114 countries ( 53 ). Within a year, the number of reported cases increased to more than 144 million, with more than 3.07 million deaths worldwide, as reported on 23 April 2021 ( 55 ).

A worldwide concentrated research effort began working toward understanding SARS-CoV-2 and its associated disease. This effort was reflected in the increasing rate of journal publications, especially during the period from January to May 2020. In March 2021, the LitCovid literature hub reported more than 110,000 articles related to the novel coronavirus in PubMed ( 7 ). Furthermore, an increase of preprints related to COVID-19 became a significant factor to expedite knowledge sharing during this pandemic ( 12 , 15 ). However, the elevated influx of articles comes with challenges for accurate interpretation stemming from either an expedited and/or a lack of peer review process and uncertainties associated with preliminary reports. The validity and value of the shared information have been uncertain because of multiple factors, including studies with small sample numbers, a lack of reproducibility and consistency in methodology and results, the relevance of results obtained using SARS-CoV-2 surrogates and other human coronaviruses and the relevance of experimental results in controlled settings compared with real-world scenarios.

Scientists worldwide continue to investigate SARS-CoV-2 infection and transmission, COVID-19 diagnosis and treatment, and prevention and control measures. Because COVID-19 has been characterized as a respiratory disease transmitted via virus-containing human secretions, limited comprehensive information is available regarding the likelihood of transmission of SARS-CoV-2 through food or food packaging.

In Canada, the safety of the food supply is maintained via a collaborative effort between federal food safety partners: the Canadian Food Inspection Agency, Health Canada, the Public Health Agency of Canada, and Agriculture and Agri-Food Canada. From the beginning of the pandemic, there was a need to ensure these departments were able to evaluate the increasing amount of scientific information that became rapidly available, contextualize its importance and impact on food safety, and identify knowledge gaps and uncertainties that would affect decision-making. To this end, a group of experts from the federal food safety partners developed a comprehensive risk pathway to estimate the potential exposure and transmission of the virus through the food chain. This risk pathway takes into consideration a recently published exposure profile of SARS-CoV-2 in Canadian food sources that described the exposure routes considered most relevant in the context of food contamination ( 42 ).

By looking at the pathway of exposure, and considering uncertainty surrounding the state of knowledge for the various steps, our analysis clearly communicates the risk of exposure and transmission throughout the food processing chain and can guide and contextualize future research in this field. Taken together, the exposure profile of SARS-CoV-2 in Canadian food sources and this comprehensive risk pathway of the likelihood of exposure in the food chain provide a clear indication of the Canadian process for understanding the potential food safety risks during this pandemic ( 42 ).

APPROACH

In April 2020, a Food Safety COVID-19 working group (WG), consisting of approximately 30 experts and partners from the Canadian Food Inspection Agency, Health Canada, the Public Health Agency of Canada, Agriculture and Agri-Food Canada, and other Government of Canada departments, was convened to review and assess the information linked to food safety and SARS-CoV-2. This information was assessed to ensure actions, control measures, and communications were prompt and appropriate and based on the most recent and credible science. As part of the WG, a subgroup of five experts was created to develop a risk pathway for potential routes of exposure related to the food chain. These experts were selected based on their expertise in virology, risk assessment, public health, and food safety. Through an iterative process, the risk pathway (Fig. 1 ) was developed based on the literature, potential hypotheses, and the relevant expertise of the group. Each box in the pathway represents a necessary or potential event of exposure if SARS-CoV-2 were to be transmitted through the food chain.

FIGURE 1.

Flow diagram pathway illustrating the events of potential food contamination by SARS-CoV-2 and human exposure to the virus through food and food packaging chain. The figure represents three levels: at establishment (white boxes 1 to 6), at consumer level (light gray box 7), and in the human body (dark gray boxes 8 and 9). Each event represented is expressed as an event that could occur and contribute to exposure from food and food packaging. Dashed lines represent the possibility of introduction of the virus at different events. Dashed boxes represent events that could be applicable depending on the context of the specific scenario being evaluated.

Scientific literature from various sources (e.g., ProMed, PubMed, Scopus, BioRxiv) was reviewed in real time on a weekly basis to identify newly published information. The search strategy was broader than the usual models associated with systematic reviews, given the novelty and multiple sources of information. A variety of keywords were used to ensure that any relevant studies or papers written in English that were linked to SARS-CoV-2 (including other human coronaviruses and/or surrogates) and food safety were considered. The title, abstract, and if needed, full article were screened to identify whether the information was new and supporting the scope of the WG. Although most publications focused on SARS-CoV-2 characterization, infection, transmission, and other health- and public safety–related research, relevant data about food safety were extrapolated when deemed applicable and relevant (e.g., susceptibility to disinfectants, persistence on a variety of surfaces). Because a large proportion of the information assessed had not been peer reviewed, the experts considered all information and retained what was deemed credible and well supported by appropriate study design, sound hypothesis, and data analysis. Articles were excluded if they did not provide sufficient details to inform the pathway or the assignment of likelihood. When unsure of the acceptability of an article, experts consulted more broadly with the other experts of the sub-WG to establish whether the article was within scope and should be included. The real-time notification strategy used returned approximately 100 to 150 articles per week over a period of 1 year. Overall, more than 5,000 articles were screened and relevant articles were used to support the development of the pathway.

The supporting information for each event of the pathway was reviewed and documented to describe the current state of knowledge on, the risk factors and interventions that could increase or reduce the likelihood of exposure and transmission of SARS-CoV-2 via the food chain. To ensure proper interpretation of the likelihood levels, definitions were derived from existing qualitative risk characterizations and assessments ( 5 , 14 ). Table 1 lists the definitions used in this article to characterize the likelihood of each event identified as a possible contributing factor in the potential exposure and transmission of the virus through the food chain. The relevant information that was considered and the likelihoods can be found in Table 2 , broken down by each event in the risk pathway.

TABLE 1.

Likelihood interpretation for each event included in the pathway and applied to SARS-CoV-2 transmission through the food chain

Likelihood	Interpretation
Negligible	The event is considered to be virtually zero—it is so rare that it does not merit to be considered
Very low	The event is considered to be very unlikely—very rare but cannot be excluded
Low	The event is considered to be unlikely—rare but does occur
Moderate	The event is considered to be fairly likely—occurs regularly or often
High	The event is considered to be likely—occurs almost certainly

TABLE 2.

Likelihood assigned to each event of the pathway that represents an event in the potential food contamination by SARS-CoV-2 based on current knowledge and interventions having an impact on the likelihood

Pathway event	Current knowledge	Interventions that could reduce the likelihood	Elements that could increase the likelihood	Likelihood
1. Infected individual in food establishment	Asymptomatic and presymptomatic individuals could infect others and/or contaminate environment (4,50). Outbreaks of COVID-19 among workers in food establishments have been documented (48).	Operational barriers and measures in place (symptoms self-monitoring, facility screen-in protocols, sick leave policies, quarantine, contact tracing, COVID-19 testing, vaccination).	No operational barriers or measures in place, large establishments with numerous employees, history of positive cases in the establishment. Factors outside the establishment could contribute to the transmission among workers (shared housing and/or transportation, frequent community contacts, social disparities (48).	Low to moderate if operational barriers in place.Moderate to high if no operational barriers.
2. Infected individual sheds or propagates virus in the food establishment	Person-to-person transmission of SARS-CoV-2 occurs primarily through coughing, respiratory droplets, and sneezing (52). COVID-19 can cause gastrointestinal manifestations, and SARS-CoV-2 RNA was detected in fecal material from COVID-19 patients (57,62). However, very few studies have been able to isolate infectious viral particles from feces (8,30).SARS-CoV-2 may cause ocular manifestations such as viral conjunctivitis and viral RNA was detected in ocular fluids (29,56).	Operational barriers in place (personal protective equipment [PPE], reduced workers density, physical distancing, adequate ventilation). Worker education and training, compliance with hygiene practices.	No operational barriers in place. Noncompliance with hygiene practices.	Very low to low if operational barriers in place. Moderate if no operational barriers.
3. Virus survives in the food establishment environment and on fomites	SARS-CoV-2 persists a few hours to days on certain surfaces under different conditions (9,24,38,41,47), and frequently touched surfaces could be contaminated with SARS-CoV-2 in food establishments (33). Coronaviruses, including SARS-CoV-2, are sensitive to standard surface washing and disinfection protocols (21,23). Transmission of SARS-CoV-2 by fomites in real-life conditions does not appear to occur when standard cleaning procedures and precautions are applied (34).	Worker education and training, standard cleaning and disinfection protocols. Monitoring of SARS-CoV-2 on environmental surfaces could predict the presence of asymptomatic and presymptomatic personnel at the workplace (32,33). This could allow for response and control measures to be implemented for these personnel.	Poor or nonexistent cleaning and disinfection procedures.	Low with interventions in place to moderate if no protective measures in place.
4. Virus contaminates and survives on the following in the food establishment:  (A) Food product  (B) Packaging  (C) Food contact surface	The presence of a protein-rich medium or organic soil load can promote the survival of SARS-CoV-2 on certain surfaces (24,38). SARS-CoV-2 RNA was detected on food contact surface, packaging, and chilled and frozen foods (17,31).	Operational barriers in place (PPE, reduced workers density, physical distancing). Education, training; hygiene practices in place. Good hygiene practices and hazard analysis (and) critical control point protocols already in place in food establishments to prevent contamination by foodborne pathogens could also be effective against SARS-CoV-2.	Ready-to-eat products (RTE) or foods involving a higher level of human manipulation (handled by workers, more possible contacts), poor cleaning and disinfection practices of food contact surfaces, establishments with more manual handling and packaging.	For A, B, and C—very low to low. The range represents consideration of the presence of protective measures and the absence of protective measures.
5. If applicable, virus survives processing events in food establishment	SARS-CoV-2 survives at 4°C for several days, and freezing does not affect this persistence (6,9). In laboratory experiments, SARS-CoV-2 variant S-G614 at high initial viral titers seems more stable and infectious after 30 days of storage at −20 and at 4°C (20). SARS-CoV-2 was inactivated after 5 min at 70°C in media (9) and less than 30 and 15 min at 56 and 65°C, respectively, in cell culture supernatant (49). Holder pasteurization (63°C, 30 min) is effective to inactivate SARS-CoV-2 inoculated in human milk (10). SARS-CoV-2 is sensitive to pH extremes (6,9).	Thermal and nonthermal processing that could lead to inactivation such as, chemical treatments, desiccation, fermentation, pasteurization (39,44). In laboratory experiments, at low concentrations, similar to real viral titers found in the environment, the stability and infectivity of the virus may be affected during storage at 4° and −20°C (20).	Refrigeration or freezing, uncooked RTE products.	Negligible for foods that undergo treatment resulting in inactivation. Low to moderate for uncooked or RTE products and fresh produces. Moderate for frozen products.
6. If applicable, virus survives during the following at the food establishment  (A) Transport  (B) Handling and preparation  (C) Display	The cold chain could contribute to extended survival of the virus (13,27,31,58). No infectious SARS-CoV-2 particles were detected on fresh produce following a low-dose experimental aerosol exposure to simulate an airborne transmission (16) nor after direct exposure through hand manipulation by COVID-19 patients (43). SARS-CoV-2 inoculated on swine skin, substitute for human skin, can remain infectious for up for 96 h at room temperature and 8 h at 37°C, which could lead to possible fomite transmission of the virus in indoor environments in the absence of good hand hygiene practices (18).	Cooking, desiccation, fermentation, and other.	Refrigeration or freezing.	For A, B, and C—negligible for foods that undergo treatment resulting in inactivation Very low for products at room temperature. Low for refrigerated products. Moderate for frozen products.
7a. Virus survives consumer preparation/cooking	See events 5 and 6	Cooking, desiccation, fermentation, and other. Washing of fresh products under running water could reduce overall load (19,51).	Refrigeration or freezing, uncooked RTE products. Possibility of reintroduction of the virus by the consumer (e.g., poor hand hygiene, inadequate food safety habits).	Negligible for heat-processed foods. Low to moderate for RTE uncooked products and fresh produces. Moderate for frozen products.
7b. Ingestion of viral particles	Ingestion of SARS-CoV-2 does not appear to be a route of transmission (1).	Consumer education, respect of hygiene practices.	Noncompliance with hygiene practices.	Negligible to very low both with and without interventions.
7c. Virus contaminates food surfaces and/or hands	Frequently touched surfaces could be contaminated with SARS-CoV-2 in food and health care establishments (33,59). SARS-CoV-2 is removed by effective hand washing and is inactivated by the use of gel with an alcohol content of 62–71% (9,26).	Consumer education, respect of hygiene practices.	Noncompliance with hygiene practices.	Negligible both with and without interventions considering the required transfer prior to this event.
7d. Virus transfer to mucosa (mouth, nose, eyes) via hands	See event 7c.			Negligible both with and without interventions considering the required transfer before this event.
8a. Virus survives through stomach an replicates in intestinal cells	There is no evidence to suggest that COVID-19 can be contracted through food or food packaging (51).	Consumer education, respect of hygiene practices.	Noncompliance with hygiene practices.	Negligible both with and without interventions.
	The SARS-CoV-2 receptor ACE2 protein has been shown to be expressed in gastric, duodenal and rectal epithelial cells (57). In vitro human small intestinal organoid model was used to demonstrate SARS-CoV-2 replication in human enterocytes (28). SARS-CoV-2 RNA was detected in esophagus, stomach, duodenum, and rectum specimens from COVID-19 patients with severe symptoms (30). The SARS-CoV-2 virus particles released in the intestinal lumen were inactivated by the simulated human colonic fluid, which could significantly reduce the infectivity of the virus in the human gastrointestinal tract (61).		Medication and some foods reducing gastric acidity may create a more favorable environment for SARS-CoV-2 survival through the digestive tract (6,45).	Negligible both with and without interventions.
8b. Infection via contact with mucous membranes	Current studies suggest that the eye is a potential route for SARS-CoV-2 transmission and infection (2,40).	Consumer education, respect of hygiene practices.	Nonrespect of hygiene practices.	Negligible when interventions are in place. Very low to low without interventions.
9. Virus propagates in host	This would be dependent on human health considerations of host susceptibility, risk factors, infectious dose, etc., that are beyond the scope of this pathway which is limited to considering the overall likelihood of exposure through the food chain.			Not applicable.

The main goal of the pathway is to assess the potential likelihood of the virus reaching the end consumer through the food chain. The risk—defined as a product of the likelihood and the consequence of developing COVID-19—is not specifically addressed herein. However, it could be assessed by incorporating additional events into this pathway to identify, develop, and assess the public health elements associated with the development of an infection after exposure based on identified factors, including infective dose, susceptibility, and other relevant risk factors.

The sub-WG experts independently reviewed the pathway and assigned a likelihood level to each event, based on its contribution to the potential transmission of SARS-CoV-2 through the food chain as identified in the literature assessment (Table 2). The likelihood levels were collated and discrepancies were reviewed and discussed until a consensus was reached based on the scientific evidence. A range of likelihood was assigned to encompass any variability that remained after discussion. The initial level of agreement between the experts was high, and the number of discrepancies was minimal. This exercise was repeated with the larger WG, to validate the process and ensure minimal variability. There was also a strong level of agreement with the assigned levels of likelihood among the experts of the WG.

The resulting risk pathway and associated likelihood levels were reviewed periodically and adjusted as needed based on newly available scientific evidence. New scientific evidence was compared with the previously reviewed literature and integrated in the pathway to determine the following: (i) whether the assigned likelihood changed for the specific event and how it impacted the overall likelihoods assigned and (ii) whether it addressed any research or knowledge gaps that were previously identified. The likelihoods presented in this article are a reflection of the scientific information from the literature available up to 25 April 2021 and may evolve as new science becomes available.

PATHWAY AND SUPPORTING INFORMATION

The pathway depicted in Figure 1 highlights the relevant events for viral transmission along the food chain. For increased clarity, the pathway was separated into three distinct levels along the food chain: food establishments, consumer environment, and human body. All of the levels are differentiated by shades of gray.

Table 2 summarizes the key knowledge elements as well as the likelihood assigned to each event in the pathway. Table 2 also provides examples of interventions or measures that could have an impact on the potential exposure of the consumer to SARS-CoV-2 through the food chain, resulting in an infection. Table 2 is complementary to the pathway and provides a summary of the supporting information analysis of information that was used by the sub-WG experts to determine the likelihood levels.

Level 1: food establishment

General terminology was used in this pathway to be applicable and useful to a large variety of scenarios and situations. The first event in this pathway is “an infected individual in a food establishment,” where food establishment can refer, for example, to a farm, restaurant, food manufacturing facility, grocery store, or farmers' market. Given that the virus could also be introduced at subsequent steps within food establishments, these possibilities were also considered and added to the pathway. These events at the food establishment level (events 2 to 6), are listed as follows: the propagation of the virus by an infected individual; the survival of the virus on surfaces and/or fomites; the contamination of food packaging or surfaces; and the survival of the virus through processing steps, transport, preparation, and display. For example, conditions of temperature and relative humidity in a food establishment could have an impact on the virus survival on surfaces. Survival rates are higher at a lower temperature (10°C) than at a higher temperatures (22 and 27°C) when the relative humidity is 40%. Likewise, at 22 and 27°C survival is higher at 40 and 85% relative humidity versus 65% relative humidity ( 35 ). As the pathway allows for various scenarios, not all the events presented in Figure 1 will occur; those that are considered optional, depending on specific circumstances, are indicated by boxes in dashed lines. Examples of optional circumstances that may or may not be considered in the estimation of likelihood include processing steps (e.g., cooking) or asymptomatic people who enter a grocery store and contaminate the food items on display (Fig. 1, events 5 and 6).

Level 2: consumer

The second category of events is focused on the consumer environment, that is, once a consumer brings food items from the food establishment into their home environment. As with any pathogenic microorganism, cross-contamination with SARS-CoV-2 is considered either through contaminated food contacting other surfaces or the hands (event 7c) and when the virus on food or a surface is transferred to the mucosa via hand contact (event 7d). Similar to the events described in the food establishment category, event 7a considers the survival of the virus through preparation steps that can include cooking, freezing, or preservation. As such, steps 7a through 7d would represent exposure through food and food packaging and its likelihood of happening, not the likelihood of potential infection through that route as described above.

Level 3: human body

The third category of events is related to the routes of exposure through ingestion (event 8a) and contact through the mucosa (event 8b). Currently, the scientific literature is scarce regarding the potential of infection after the ingestion of SARS-CoV-2 viral particles. Elements such as transfer through the respiratory system or tropism would require further research to determine the extent of their potential role in the development of infection with SARS-CoV-2 after ingestion of viral particles. The limited information regarding potential infection with SARS-CoV-2 after exposure through mucosa is primarily related to exposure via the eye. The lack of receptors for SARS-CoV-2 on the conjunctiva and the impact of ocular secretions and tears, both as a barrier and through flushing actions, limit the likelihood of infection through this route of exposure ( 2 , 11 , 40 ). The upper respiratory tract is an important route of entry and infection via respiratory droplets. However, further research is required to determine whether sufficient virus would be transferred to the nasal mucosa through hand contact, for infection to occur.

Mitigating and compounding measures and interventions

The interventions or measures that could mitigate or increase the likelihood of an event contributing to an exposure through the food chain are listed in Table 2.

These interventions primarily have an impact on the survivability of the virus under different conditions (e.g., cooking, freezing, persistence on surfaces) or impact potential exposure through the protective measures linked to hygiene (e.g., washing hands, protective equipment, physical distancing, sanitation). The likelihood levels were assigned by considering the impact of these measures within the Canadian context and could be different in other settings.

Overall likelihood of exposure to SARS-CoV-2 through the food chain

Considering the various events in the pathway and their associated supporting information, the overall likelihood of exposure of a consumer to SARS-CoV-2 through the food chain was considered to be negligible to very low. This likelihood is due in part to the number of sequential and unlikely events that need to happen throughout the food chain, to result in an exposure that might lead to an infection via the explored routes of exposure. In addition, there is currently an absence of comprehensive epidemiological evidence to support infection by ingestion or contact through food or food packaging.

Of note, similar pathways considering, for example, companion animals, food-producing animals and their products and by-products, and animal feed, also could be developed and connected to this food safety pathway at the various relevant events where the introduction of the virus is theoretically possible and could be linked to the food chain. Other factors linked to the likelihood of infection such as susceptibility of the patient, risk factors, immunity, also could be added in parallel to event 9 to refine the overall likelihood of infection through the food chain.

EXAMPLES OF USE OF THE PATHWAY

Contextualization of information is critical when a situation evolves rapidly and tremendous amounts of information become available in a very short time. This importance is magnified when the level of uncertainty of this new information is high. The pathway can be used as a tool to provide a framework to assess, evaluate, and contextualize new scientific information. The likelihood associated with each of the events should be adjusted based on this new scientific information where applicable, and the overall messaging updated accordingly. This tool facilitates the communication of risk to decision makers and identifies research gaps based on areas of higher risk and events at which control measures would have the greatest impact on preventing potential transmission through the food chain.

As an example, this pathway was used as a tool to assess new research and information related to the emerging variants of the SARS-CoV-2. It is theorized that as the rate of infection rises in a population due to the increased transmissibility of the SARS-CoV-2 known variants ( 25 ), it is likely that more infected individuals (asymptomatic or before the appearance of symptoms) could be entering food establishments (event 1) and propagating the virus in the environment, food, and/or food packaging (events 2 to 4). The increase of infected individuals in the food establishment may contribute to a higher viral load and potentially impact virus survivability in the food establishment environment (event 3). This could therefore create further opportunities for virus introduction on food, food packaging, and surfaces during processing steps and/or transport (events 4 to 6). However, considering the various controls and protective measures in place throughout the food chain, in addition to the sequence of subsequent events required for the virus to reach the consumer, it was considered that the variants do not have a significant impact on the overall likelihood of exposure or transmission of the virus through the food chain for the consumer. Nonetheless, considering the very recent emergence of these variants, further research is required to determine whether additional, currently unknown attributes of these viruses could further impact the risk of exposure or transmission through the food chain.

Another example of the use of the pathway was to assess the potential role of the cold chain in the exposure of the consumer to the virus; in this specific case, any potential transmission through packaging of food products that are transported and stored in a cold environment. Because this would be considered surface contamination, the exposure or transmission pathway would be through inhalation or contact with eyes, nose, or mouth. This information would relate to the elements associated with event 5 (virus survives processing steps in food establishment) or any reintroduction of the virus. However, to evaluate whether this information had a direct impact on the potential exposure or transmission of SARS-CoV-2 via food, all other events before and after event 5 also were considered. For example, the mitigation events associated with events 6 to 8 would reduce the potential exposure resulting from increased virus survivability at freezing temperatures, including recommended public health hygiene measures (e.g., washing hands). Via the literature review, articles suggesting infection through food packaging of foods with a cold-chain distribution component were identified ( 3 , 37 , 60 ); however, these articles did not include sufficient epidemiological evidence or investigation data on other routes of exposure to exclude community transmission, other transmission hypotheses, or the adherence to recommended public health measures, such as washing hands ( 3 , 37 , 60 ). As in the initial development of the pathway, that level of evidence and high level of uncertainty were considered when reviewing and incorporating this new information.

The advantage of having an event-wise contextualization of the transmission pathway through the food chain is that it provides a systematic and consistent approach to evaluate any new data and communicate its importance and impact. The pathway also increases the objectivity and consistency of the assessment in a rapidly evolving and high-stakes situation.

RESEARCH AND KNOWLEDGE GAPS

The review of the literature linked to food safety and SARS-CoV-2 and the estimation of likelihood for each event in the risk pathway identified areas where knowledge was limited. Figure 2 depicts the main gaps identified and illustrates how they would impact the knowledge linked to SARS-CoV-2 and potentially the likelihoods assigned to the events in the current article. A significant gap would be addressed by the development of standardized detection and quantification methods for SARS-CoV-2 in food products and on surfaces that would allow for better characterization of the presence, persistence, and survivability of the virus. However, this is not meant to indicate that testing for the presence of SARS-CoV-2 in the food chain sector (on food products, packaging, or environmental surfaces) should be implemented as an effective control measure. In addition, with current molecular detection methods (RNA), the results of environmental sampling would not provide any information on, for example, infectivity, infective load, and transfer rate, thereby limiting the useful of the results and their interpretation for decision-making. Nevertheless, standardized detection and quantification methods would facilitate valid comparison of studies and also would be useful to support studies addressing other knowledge gaps, such as transfer rates throughout the food chain and shedding levels. Transfer rates under various conditions of initial inoculum, temperature, freeze-thaw cycles, humidity, surface type, matrix, and other factors could vary widely and could broadly impact the potential exposure of consumers to the virus through the food chain. The presence of viral RNA has been demonstrated on a variety of food surfaces or food products, and more information on the factors that could influence both the presence of the virus and its relevance from the perspective of human infection would be useful. By itself, detecting the presence of viral RNA on environmental surfaces could not be considered as representing a definitive source of exposure without information on viability and efficiency of transfer rates. This is also in line with recommendations for future work related to the cold chain ( 54 ). Standardized detection methods also would allow for a better characterization of the level of viruses being shed as well as the specific host factors that might contribute to different shedding patterns. This also would contribute to better characterization of the infectivity of the viral particles detected, which would have a large impact on the potential transmission of the virus.

FIGURE 2.

Identification of main knowledge gaps or uncertainty themes that could have an impact on the likelihood evaluation linked to the potential role of the food chain in the exposure to SARS-CoV-2.

Currently, there is no comprehensive evidence that suggests that ingestion of viral particles would be a route to develop infection. This knowledge gap requires gaining a better understanding of the effectiveness of the digestive environment to inactivate SARS-CoV-2, the potential intestinal cell infection mechanism, and tissue tropism that could lead to the development of COVID-19. Additional considerations should be given to the potential infectivity of fecally shed SARS-CoV-2 virus and its survival in wastewater and the environment for agricultural practices. This last knowledge gap would likely have the most impact on the risk characterization of SARS-CoV-2 through the food chain.

LIMITATIONS AND UNCERTAINTIES

The risk pathway depicted in Figure 1 was generated to highlight the likelihood of SARS-CoV-2 contamination of food and the further exposure and transmission at relevant steps of the food processing and handling chain. This pathway is not intended to represent a quantitative risk assessment but rather to serve as a tool to adapt to various situations. The user can take into consideration which events are relevant for different types of food establishments and food products as well as regional and local contexts to identify the potential routes of exposure and transmission. As described in the previous section, there are numerous unknowns associated with each event in the pathway that prevent a full quantification of the probabilities and risks. These uncertainties stem from gaps in knowledge due to the following: knowledge acquired from preliminary reports, knowledge acquired from SARS-CoV-2 surrogates such as other human coronaviruses, lack of reproducibility of published results, lack of consistency in methodologies used, and uncertainties associated with the translation of experimental results to a real-world setting. Research on SARS-CoV-2 and its associated disease is ongoing and will prove useful to refine assumptions and reduce uncertainty. New scientific information on elements that could have an impact on the events depicted in the risk pathway presented here are published daily. This pathway and its conclusions are based on the knowledge at the time of publication and therefore should be considered dynamic, allowing for the integration of new knowledge as it becomes available and the assessment of its impact on the overall likelihood of exposure.

CONCLUSIONS

This risk pathway development process allowed the Canadian food safety partners to readily contextualize available evidence to better communicate complex information to senior management, decision makers, and other partners in a visual format. It highlighted that many sequential events would need to occur for food or food packaging to be successful vectors of transmission of SARS-CoV-2. By combining the likelihood of each event in the continuum from food production to propagation in the host, it also allowed for the identification of areas where additional research and knowledge could inform our conclusions, decrease uncertainty, and provide food safety partners with additional information regarding appropriate interventions to address this potential route of exposure.

Based on our review and analysis, there is currently no comprehensive epidemiological evidence of confirmed cases of SARS-CoV-2 or its new variants causing COVID-19 resulting from transmission through food or food packaging. Despite the theoretical possibility of exposure through food, there remains several critical uncertainties linked to the transfer rates and the infective nature of the virus at certain points in the pathway. Therefore, the likelihood of exposure to and transmission of SARS-CoV-2 that could lead to potential infection with the virus through the food chain, by ingestion or contact, is still considered negligible to very low. Consistent with other scientific opinions linked to the role of food and food packaging in the transmission of SARS-CoV-2, the current controls in place in Canadian food establishments would be considered adequate to mitigate any potential risks outlined in this pathway ( 14 , 22 , 36 , 46 ).