ABSTRACT

The SARS-CoV-2 pandemic has presented new challenges to food manufacturers. During the early phase of the pandemic, several large outbreaks of coronavirus disease 2019 (COVID-19) occurred in food manufacturing plants resulting in deaths and economic loss, with approximately 15% of personnel diagnosed as asymptomatic for COVID-19. Spread by asymptomatic and presymptomatic individuals has been implicated in large outbreaks of COVID-19. In March 2020, we assisted in implementation of environmental monitoring programs for SARS-CoV-2 in zones 3 and 4 of 116 food production facilities. All participating facilities had already implemented measures to prevent symptomatic personnel from coming to work. During the study period, from 17 March to 3 September 2020, 1.23% of the 22,643 environmental samples tested positive for SARS-CoV-2, suggesting that infected individuals were actively shedding virus. Virus contamination was commonly found on frequently touched surfaces such as doorknobs, handles, table surfaces, and sanitizer dispensers. Most processing plants managed to control their environmental contamination when they became aware of the positive findings. Comparisons of positive test results for plant personnel and environmental surfaces in one plant revealed a close correlation. Our work illustrates that environmental monitoring for SARS-CoV-2 can be used as a surrogate for identifying the presence of asymptomatic and presymptomatic personnel in workplaces and may aid in controlling infection spread.

HIGHLIGHTS
  • Environmental contamination by SARS-CoV-2 was found in food processing plants.

  • Of 22,643 environmental swabs, 278 (1.23%) were positive for SARS-CoV-2.

  • Frequently touched surfaces had the most contamination.

  • Doorknobs, computer devices, tabletops, and sanitizers had the most contamination.

  • Surface testing may indicate the presence of asymptomatic virus carriers.

Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), a highly infectious novel coronavirus, has been identified as the causative agent of the global coronavirus disease 2019 (COVID-19) pandemic originating from a food market in Wuhan, People's Republic of China in December 2019 (6). As of 13 December 2020, nearly 70 million COVID-19 cases have been confirmed globally, with 1.6 million deaths (18).

The transmission of COVID-19 occurs mainly through direct personal contact and respiratory droplets (3). In addition to infection spread by symptomatic individuals, disease spread by both asymptomatic and presymptomatic individuals can be a major cause for large epidemics (1, 4, 12). Contaminated surfaces were reported as another mode of transmission (911). SARS-CoV-2 remains viable on surfaces for days (15) and may be stable for up to 9 days on surfaces such as metal, glass, and plastic (7). Surface disinfection with 62 to 71% ethanol, 0.5% hydrogen peroxide, or 0.1% sodium hypochlorite can efficiently inactive the virus within 1 min (7).

During the early phase of the COVID-19 pandemic, high rates of SARS-CoV-2–positive samples from environmental surfaces were associated with a large number of COVID-19 cases in built environments such as hospitals and living spaces (19). At one hospital in Italy, the most positive samples were collected from the air and surfaces within the areas designated for patients (13). In a study of 112 surface samples taken from the living quarters of 13 laboratory-confirmed COVID-19 case patients, Wei et al. (17) found that 44 (39.3%) of the samples were positive for SARS-CoV-2 RNA. In a controlled prospective study, Marshall et al. (8) screened both environmental surfaces and employees for SARS-CoV-2 and found that a high prevalence of SARS-CoV-2 RNA in environments was positively correlated with the presence of asymptomatic employees infected with the virus. Their results suggested that environmental monitoring may be used to predict the presence of asymptomatic and presymptomatic individuals. Research in built environments has revealed the importance of proper disinfection of toilet areas, sanitization of surfaces, creation of open spaces, and window ventilation for effectively reducing the levels of SARS-CoV-2 in enclosed areas (6).

According to the U.S. Centers for Disease Control and Prevention (CDC), of the 130,578 people employed in the food industry who were tested for COVID-19 in April, 3% tested positive (5). In a more comprehensive analysis, the CDC analyzed COVID-19 cases in the food industry in 30 states from March to May 2020. Some food processing plants had infection rates as high as 43%. Most workers who were COVID-19 positive were ethnic minorities (83.2%). The asymptomatic rate was about 15%, indicating that screening for COVID-19 symptoms alone is not adequate to combat infection spread (16). Although it is highly likely that airborne virus transmission substantially contributed to observed infection outcomes in the CDC study, transmission also could have occurred via contaminated surfaces (14). However, the extent of virus contamination in the food industry has not been reported. Here, we present the analysis of 22,643 surface samples from food processing facilities in the United States that were tested for the presence of SARS-CoV-2 RNA. These data may help food processing plants evaluate their decontamination protocols, and the surveillance method described here can be used for detecting virus shedding by workers with asymptomatic and presymptomatic infections.

MATERIALS AND METHODS

Sampling plan

The study period lasted from 17 March to 3 September 2020 and included 116 food processing plants. As for a typical environmental monitoring program, processing plants were directed to identify high-touch areas in high traffic zones (zones 3 and 4), which included entrances, break rooms, lunchrooms, restrooms, and office spaces. Food production areas designated as zones 1 and 2 were not part of the sampling plan. The surfaces tested included high-touch surfaces such as doorknobs and handles, computer accessories, time clocks, and sanitizer dispensers. A total of 22,643 environmental samples were collected from the 116 food processing plants.

Environmental sampling methods

Institute for Environmental Health (IEH) SARS-CoV-2 surface swab kits (P/N: PS-S02, Microbiologique, Seattle, WA) were used for sampling environmental surfaces. All food processing plants instituted frequent sanitation (spraying and wiping) of surfaces with an approved sanitizer every 2 to 4 h. Sampling was done randomly during the day. Sampling was performed by plant personnel according to the manufacturer's instructions. The swab kit contained a sterile polyester-tip swab, a vial containing sampling buffer, and a vial containing viral inactivating transport medium (IEH VTM). A dry swab was removed from the package and wetted with the sampling reagent. Samples were collected by swabbing an area (ca. 2 by 2 in.) with bidirectional movement while rotating the swab stick. The sample swab was then placed in the transport tube containing IEH VTM, which was placed in a self-sealing bag supplied in the kit. The exterior of the sealed bag was sanitized with a 60 to 80% ethanol, 80% isopropyl alcohol, or 5% hypochlorite solution and dried prior to leaving the tested area. The surface area that was swabbed was also cleaned with a sanitizer solution. Sealed bags were shipped to Molecular Epidemiology Inc. (Seattle, WA) for testing.

RNA extraction

Total nucleic acids were extracted and purified from the swabs using the IEH nucleic acid extraction reagent kit (P/N: PM-23, Microbiologique) in a semiautomated KingFisher-96 (Thermo Fisher Scientific, Waltham, MA) nucleic acid purification system following the manufacturer's instruction. The nucleic acid extraction kit contained buffers for nucleic acid isolation and silica functionalized paramagnetic beads for nucleic acid capture. For each environmental sample, 200 μL was mixed with an equal volume of pure ethanol, 3 μL of carrier RNA, and 10 μL of magnetic beads in a 96-well deep plate (Thermo Fisher Scientific). Plates were then mixed and washed with wash buffers in the automated system. Nucleic acids were eluted with 100 μL of nuclease-free water. Eluted total nucleic acids were immediately subjected to a reverse transcription (RT) PCR assay, and remaining samples were stored at or below −20°C for further use.

RT-PCR

The IEH SARS-CoV-2 RT-PCR test kit (P/N: PM-22, Microbiologique) was used for the detection of SARS-CoV-2 RNA in environmental samples. This test kit was derived from the SARS-CoV-2 diagnostic test developed by the CDC (2). This kit contains N1, N2, and RPP primer-probe sets to detect the viral nucleocapsid gene and the human RNase P RNA (internal control). For amplification of viral RNA, 5 μL of RNA sample was added to 20 μL of RT-PCR buffer master mix, and the reaction was run in a real-time PCR machine (Stratagene MX-3005P, Agilent Technologies, Santa Clara, CA). A DNA fragment containing the N1 target region was used as the positive control. MS2-RPP, an engineered MS2 phage particle encapsulating an RNA fragment from the human RNase P gene, was the external extraction control in every set of samples. The cycling parameters were set to 50°C for 10 min for reverse transcription, 95°C for 10 min for RT inactivation, and 45 cycles of 95°C for 10 s and 55°C for 30 s. A cycle threshold value of <38 was considered indicative of a virus-positive sample for environmental testing.

Clinical specimen analysis

Clinical specimens (nasopharyngeal samples taken from employees) from establishment E were processed at Molecular Epidemiology Inc. clinical testing laboratory (certified by the Clinical Laboratory Improvement Amendments) using the same RNA extraction and RT-PCR methods with both the N1-RPP and N2 primers-probes. Protected health information was completely removed from all clinical results before they were given to the researchers. The Western Institutional Review Board (Puyallup, WA) provided institutional biosafety committee services to Molecular Epidemiology Inc. by approving consent forms and human research safety protocols.

Data analysis

Descriptive statistical analyses were used to present data as numbers and percentages of positive samples. The median was used to describe the central tendency for the skewed histogram. Statistical analyses were performed with SigmaPlot 14.0 (Systat Software, Palo Alto, CA).

RESULTS

The 22,643 environmental samples collected in zones 3 and 4 from 116 food manufacturing plants were received with source information between 17 March and 3 September 2020. Because food is not considered a vehicle for transmission of SARS-CoV-2, most food production lines are automated, and no bare-hand contact with foods occurs, we decided not to include zone 1 and zone 2 for sampling in this study. Of the total environmental samples collected during the study period, 278 (1.23%) were positive for SARS-CoV-2 (Table 1). Samples were analyzed by grouping them into workplace area and surface type. The workplace samples were divided into three groups: welfare area, working area, and entrance. The welfare area and working area swabs came from different locations based on usage and were thus subdivided. The welfare area was split into three categories: bathrooms, lunchrooms, and locker rooms. The working area was composed of offices and conference rooms, training rooms, and receiving rooms. The entrance and other ingress points had the highest prevalence of SARS-CoV-2–positive swabs among tested areas: 1.57% (38 of 2,439 samples) (Table 1). In the working area group, 32 (1.42%) of 2,255 samples were positive, with 25 (1.33%) positive results from 1,883 samples from offices and conference rooms and 1 (0.38%) positive result from 265 samples from training rooms. The receiving room had the highest prevalence: 5.61% (6 of 107 samples). Overall, 1.36% (139 of 10,226) of samples were positive in the welfare area; samples from bathrooms, lunchrooms, and locker rooms had positive rates of 1.17% (31 of 2,640 samples), 1.33% (70 of 5,260), and 1.63% (38 of 2,326), respectively.

TABLE 1

Results of environmental testing for SARS-CoV-2 in work areas in food processing plants

Results of environmental testing for SARS-CoV-2 in work areas in food processing plants
Results of environmental testing for SARS-CoV-2 in work areas in food processing plants

We also determined which surface types yielded the most virus-positive samples (Table 2). Among the positive samples, 46 (16.55%) had no specified surface information, and 93 (33.45%) were from doorknobs or handles, the surfaces with the highest prevalence of positive samples. Other surfaces that frequently tested positive for SARS-CoV-2 were tables and counters (21 positive samples), computer devices (20), sanitizer dispensers (17), switches (12), rails (12), chairs and benches (11), and timeclocks (10). Thirty-six positive samples were collected from other surfaces.

TABLE 2

Results of environmental testing for SARS-CoV-2 on surfaces in food processing plants

Results of environmental testing for SARS-CoV-2 on surfaces in food processing plants
Results of environmental testing for SARS-CoV-2 on surfaces in food processing plants

We next analyzed to what extent these 116 food processing plants were affected by SARS-CoV-2 contamination. Figure 1 shows the frequency distribution of the percentage of positive cases for each processing plant. A total of 53% (62 of 116) of processing plants had at least one positive sample through the observational period. The positive rate for individual plants was 0 to 30%, with a median of 0.25%.

FIGURE 1

Percentage of SARS-CoV-2–positive environmental samples collected from 116 food processing plants. The upper bounds of each interval ranges are inclusive, whereas the lower bounds are exclusive; 0% has no interval range because it contained only one value.

FIGURE 1

Percentage of SARS-CoV-2–positive environmental samples collected from 116 food processing plants. The upper bounds of each interval ranges are inclusive, whereas the lower bounds are exclusive; 0% has no interval range because it contained only one value.

As the pandemic progressed from its early phase in February, almost all food manufacturing companies implemented a variety of safety measures such as vigorous decontamination, mandatory personal protective equipment (including face masks), symptom screening, and in some companies SARS-CoV-2 screening (using the PCR method), which ranged from testing the exposed individuals to widespread screening of all personnel. All personnel who tested positive for SARS-CoV-2 were required to quarantine for 14 days. Most companies required a negative test result before an individual was allowed to come back to work. We next undertook a longitudinal observational study of five food companies and conducted a timeline data analysis to determine the outcomes of SARS-CoV-2 preventive measures (Fig. 2). During the study period (17 March to 3 September 2020), 1,477, 1,577, 912, 867, and 433 surface samples were received from establishments A, B, C, D, and E, respectively. A decreasing trend of daily positive rates was observed in establishments A, B, and E after reaching peaks on 9 May, 19 May, and 7 May, respectively. The other two establishments continued to have sporadic environmental contamination with SARS-CoV-2.

FIGURE 2

Percentage of SARS-CoV-2–positive samples collected from five food processing establishments during the study period. Daily positive rate = number of daily positive samples/number of daily total samples × 100.

FIGURE 2

Percentage of SARS-CoV-2–positive samples collected from five food processing establishments during the study period. Daily positive rate = number of daily positive samples/number of daily total samples × 100.

Establishment E additionally submitted 1,248 human nasopharyngeal specimens from plant personnel for SARS-CoV-2 analysis from 4 May to 18 June 2020. During the same period, they also submitted environmental samples, of which 9.21% (21 of 228 samples) tested positive. Our results indicated that 10.90% of human samples were positive for SARS-CoV-2 (Fig. 3). Thus, even with screening for symptomatic individuals and strict environmental decontamination, asymptomatic and presymptomatic individuals presumably contaminated their surroundings with the virus.

FIGURE 3

Daily SARS-CoV-2–positive rate among clinical samples and environmental samples collected from food processing establishment E from 30 April to 18 July 2020.

FIGURE 3

Daily SARS-CoV-2–positive rate among clinical samples and environmental samples collected from food processing establishment E from 30 April to 18 July 2020.

DISCUSSION

The goal of our study was to provide a tool for monitoring the presence of SARS-CoV-2 in food production facilities. Environmental monitoring for foodborne pathogens such as Listeria and Salmonella is routinely conducted in food production facilities to document the sanitary conditions under which food is produced. The environmental monitoring results provide feedback that the sanitation and food safety teams can use to determine corrective actions. The COVID-19 pandemic has presented a new challenge to food manufacturers. Although food production is focused on preventing the spread of microbial contamination of foods, with SARS-CoV-2 there is an additional focus on continuing operations while protecting personnel from the virus. Early in the pandemic, a consensus developed around using personal protective equipment (face masks, face shields, gloves, and plastic and Plexiglas barriers), monitoring the health of personnel, reducing density in otherwise crowded areas, sanitizing surfaces frequently, closing down or reducing the capacity in break rooms, contact tracing, quarantine of exposed personnel, and testing for the virus.

Currently little information is available about the level of workplace contamination due to asymptomatic and presymptomatic COVID-19 cases. Marshall et al. (8) conducted a prospective observational study of nine Eurofins Microbiology Laboratories locations. The study involved testing 841 employees and analyzing 5,500 environmental samples. A weak correlation was found between positive human and positive environmental samples in three of the nine laboratories. In March 2020, we assisted in implementation of environmental monitoring programs for SARS-CoV-2 in several food production facilities. All facilities had implemented measures to prevent symptomatic and presymptomatic personnel from coming to work. During the study period, 278 (1.23%) of the 22,643 samples were positive for SARS-CoV-2; at least one positive sample was obtained from 62 of the 116 food production facilities. The prevalence of positive samples among the production facilities was 0 to 30%.

The data (Tables 1 and 2) clearly indicate that all frequently touched areas can be contaminated. Doorknobs and handles had the highest rate of contamination (33.5%), followed by computers, desks and tables, sanitizer dispensers, handrails, switches, chairs and benches, and timeclocks. Figure 2 shows the course of contamination in five plants over the study period. Because environmental contamination with SARS-CoV-2 reflects infections among personnel, contamination would be expected to occur sporadically over time. In establishments A and B, contamination was detected early, and all subsequent samples were negative for SARS-CoV-2, whereas in the other establishments virus contamination appeared and disappeared over time. Although a positive SARS-CoV-2 RT-PCR test result for an environmental sample does not necessarily mean that the sampling site is contaminated with infectious viral particles, the presence of virus is a clear indication of active shedding of viral RNA by infected individuals. SARS-CoV-2 contamination occurred even with decontamination protocols in place, indicating that either these protocols were inadequate or high numbers of asymptomatic and presymptomatic individuals were present. Conversely, negative results could have been due to more rigorous decontamination protocols, inadequate sampling techniques, or timing of sampling in relation to the surface decontamination schedule. During the course of this study, our findings enabled all participating production facilities to fine-tune their COVID-19 safety protocols and to make decisions regarding personnel testing.

In establishment E where we performed environmental testing, initial high positive rates (ca. 40%) prompted testing of personnel. The human and environmental samples were collected in the same facility at the same time, and 10.90% of human and 8.54% of the environmental samples were positive for the virus. This finding indicates that in the absence of personnel testing, environmental testing for SARS-CoV-2 could indicate the presence of active human infections. Other companies that tested employees used testing programs sponsored by either state government or a health care provider. Therefore, those data were not available for our analyses.

Our results clearly show that monitoring for SARS-CoV-2 in workplaces can be a valuable tool in the control of the spread of SARS-CoV-2. A limitation of this study is that we were not able to determine the role of environmental contamination in the spread of COVID-19 because an RT-PCR test cannot differentiate between infectious and noninfectious virus particles. Our results indicate the utility of environmental monitoring for SARS-CoV-2 in food production facilities as an indicator of the presence of infected personnel and as a trigger for human testing in these facilities.

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This is an open access article under the CC BY-NC-ND license (https://creativecommons.org/licenses/cc-by-nc-nd/4.0/)