key: cord-0747169-ebwczvr0
authors: Lucan, Sean C.; Goodwin, Stephanie K.; Lozano, Mariano; Pak, Serina; Freitas, Miguel
title: SARS-CoV-2 Testing for Essential Food-Production Workers: Evolving Thinking, Pilot Testing, and Lessons Learned
date: 2021-06-23
journal: Public Health
DOI: 10.1016/j.puhe.2021.06.014
sha: aaaa7b55598a083ffc2cb919283a692bace6cf2f
doc_id: 747169
cord_uid: ebwczvr0

The food-production workforce is an essential part of U.S. coronavirus-19 (COVID-19) critical infrastructure. Keeping food-production workers safe is essential. During the COVID-19 pandemic, safety has meant added workplace protections. Guidance about protections came early from the Federal Government. Absent from such guidance were strategies to screen workers for the causative virus. Without viral screening, some food companies had outbreaks; some facilities had to close. Companies interested in worker screenings had to devise their own strategies. One company devised a strategy having three main goals: (1) detecting asymptomatic infections, before opportunity for spread; (2) identifying workplace clusters, to indicate potential protection breakdowns; (3) comparing company results to community rates. The company decided on pilot screenings at two U.S. production plants. Screenings involved mandatory viral testing (through reverse-transcription polymerase chain reaction) and optional antibody testing (both immunoglobulins G and M). Pilot screenings showed benefits along with limitations: (1) detecting asymptomatic infections, but at questionably relevant time points; (2) identifying infection clusters, but with uncertain sites of transmission; (3) showing relatively low rates of infection, but absent details for meaningful community comparisons. Establishing a worker screening process was an enormous undertaking. Company employees had to stretch job roles and were distracted form usual responsibilities. Whether other companies would find sufficient benefits to justify screening costs is unclear. Moving forward, new Federal leadership could provide greater support for, and assistance with, worker screenings. Additionally, new technologies could make future screenings more feasible, and valuable. The worker-screening experience from this pandemic offers learnings the next.

interested in worker screenings had to devise their own strategies. One company devised a strategy 10 having three main goals: (1) detecting asymptomatic infections, before opportunity for spread; (2) 11 identifying workplace clusters, to indicate potential protection breakdowns; (3) comparing company 12 results to community rates. The company decided on pilot screenings at two U.S. production plants. An essential part of U.S. coronavirus-19 (COVID-19) critical infrastructure is the food-production 26 workforce. 1 While food production is a priority at any time, it is particularly important during a global 27 pandemic 2 -especially one so strongly linked to diet-related diseases. 3,4 28 29 Access to food has been challenged in the time of COVID-19; food insecurity has surged from nearly 30 three out of every 10 Americans to more than four out of 10. 5 Children have been effected 31 disproportionately. 6,7 So have Black and Latinx populations. 5-7 Many Americans are experiencing 32 hunger for the first time. If food production wanes, the problem can only worsen. 33

To keep our food supply thriving, it is imperative to keep production workers safe. During the COVID-35 19 pandemic, production-worker safety has meant additional protections beyond the routine: added 36 engineering controls (e.g., ventilation, air filtration, physical barriers); new procedures (e.g., staggered 37 work shifts, symptoms screenings, contact tracing); and extra personal safeguards (e.g., hand sanitizer, 38 face shields, universal masking). 39

Early guidance about such protections came from several sources: the World Health Organization 41 (WHO); 8,9 the Occupational Safety and Health Administration (OSHA); 10 and jointly from the U.S. 42

Department of Health and Human Services (HHS) and the Centers for Disease Control and Prevention 43 (CDC). 11 However, completely lacking from early COVID-19 guidance were recommendations around 44 an essential issue-testing for the causative virus, SARS-CoV-2. 45 to situations where a COVID-19 case had already been identified. 12 Other CDC testing guidance was 48 general in nature, not specific to a food-production workforce. 13 Additionally, testing to screen for 49 asymptomatic infections was not addressed. Toward identifying asymptomatic/pre-symptomatic cases, one company, Danone North America, 59 thought a worker-screening strategy could be of benefit. Danone North America (from here forward, 60 "the company") has approximately 6,000 employees across the U.S, with approximately 3,000 61 production workers in 16 U.S. food-production facilities. In deciding to undertake a worker testing pilot, 62 the company had several aims: first, enhancing worker safety; second, keeping plants open to produce 63 needed food; third, generating knowledge to benefit other critical-infrastructure workers-including 64 employees at other food companies. While consideration was given to different SARS-CoV-2 tests, reverse-transcription polymerase chain 75 reaction (PCR)-specifically with nasopharyngeal sampling-seemed to be the emerging test 76 standard. 18 Nonetheless, for worker comfort, less-invasive nasal sampling was thought to be preferably. 77

Reassuringly, such nasal sampling seemed to have similar sensitivity. 19 Regardless, with either type of 78 sampling, in relying on a PCR-only strategy, it was recognized that SARS-CoV-2 infections could be 79 missed. 20 A potential solution was thought to be add-on antibody testing. 80

Early thinking was that add-on antibody testing could serve three purposes: (i) capturing active but later-82 stage infections missed by PCR; (ii) establishing who may have already been infected and how recently, 83

(iii) suggesting who may have some degree of protective immunity. 21 The first and second purposes 84 might be served by earlier-developing Immunoglobulin M (IgM); the second and third purposes might 85 be served by later-developing Immunoglobulin G (IgG). 22 To proceed, the company explored three logistical options. First was purchasing testing equipment for 100 in-house screening. However, cost, administration, and regulatory restrictions were prohibitive. The 101 second option was partnering with local health departments. Unfortunately, government testers were not 102 amenable to conducting screenings for private companies. Additionally, health departments were 103 focused mostly on testing only in cases of symptoms or exposures. The third option was outsourcing 104 screening to private companies. This seemed the most viable option. 105

Ultimately though, there was no single "end-to-end" solution. For specimen collection, processing, and 107

reporting, worker screening would require a multi-partner approach. Building the approach would 108 necessitate job-role stretch; food-company employees would have to make assessments in unfamiliar 109 areas-e.g., related to laboratory medicine and clinical epidemiology. More than 10 laboratories and 110 testing companies were investigated. The best combination of price, experience, credibility, and 111 logistical feasibility seemed to be a solution involving a laboratory-support service working side-by-side 112 5 123

Only after pilot testing was completed did company leadership recognize an omission in their employee 124 communication: There was no mention of sharing screening results externally. In order to publish pilot 125 findings, a retrospective, voluntary, op-in consent form was designed by company attorneys. The 126 consent form noted that individual results would be de-identified. 127

In COI, 70% of 347 workers provided consent to share findings; in FW, 86% of 219 workers did. Figure  129 1 shows test results for workers giving consent (Of note, for considerations of representativeness, data 130 from workers declining consent would not have meaningfully changed reported findings). (Table 2) . 143 144 Presuming all test results were true results (i.e., no false positives, no false negatives), any non-negative 145

IgM (IgM-positive or IgM-indeterminant) could represent recent infection (Table 2) . Thus, at COI, the 146 number of asymptomatic infected workers could have been as high as seven ( Figure 1 ); at FW, the 147 number could have been as high as four (counting the worker who tested PCR-positive but who declined 148 antibody testing). Nonetheless, any asymptomatic infections detected by IgM would necessarily be 149

'longer-established' as opposed to 'newly acquired' (Table 2) . Once IgM starts to emerge, the chance of 150 contagiousness might be small; the window for preventing spread to other workers might have already 151 passed. In other words, while the pilot may have detected a few cases of asymptomatic infection, the net 152 benefit of removing later-detected cases from production plants would be unclear.

Only in FW (where the PCR-positive individual did not have antibody testing), is it possible that case 155 removal could have substantively reduced the chance of SARS-CoV-2 spread. Based on PCR testing 156 alone though, it is not possible to know if the individual was early or late in infection. 157

Identifying workplace clusters 159 160

The combination of results for PCR, IgM, and IgG can reflect infection at a specific stage (Table 2) Unfortunately, unlike workplace screenings where testing represents a full census, community testing is 228 not generally population-representative. Rather, community testing is likely to over-represent 229 symptomatic disease-and, thus, over-estimate prevalence. Also, age-sex distributions for tested 230 community members likely differ from age-sex distributions for production-plant workers. To account 231 for differences, standardization by age-sex categories is one approach. 28 But age-and sex-specific strata 232 for community rates are not generally available. Another approach, using linear regression, is to 233 correlate asymptomatic worker prevalence with weekly community incidence rates. 29 Such approach, 234 however, is only meaningful with more than two data points-i.e., more than two pilot sites (it is always 235 possible to draw a perfect line between two points, even if correlation is actually poor). 236

The bottom line is that without additional data-i.e., doing worker screenings at a greater number of 238 production plants or having further details about community data-it is not possible to meaningfully 239 compare worker results to population results. Such realities complicate the design of any test-and-240 response algorithm, as attempted by the company prior to starting the screening pilot (Appendix -241 Figure) . Beyond sizable financial outlays for sampling, processing, and results delivery, there are monetary costs 247 related to shifting job roles; in figuring out testing complexity, some company employees will 248 necessarily be distracted from their usual responsibilities. Productivity may suffer. The potential costs 249 (and benefits) of a screening program need to be weighed against the potential costs (and benefits) of not 250 screening (Table 1) . 251 9 If companies do decide to screen, paper-strip antigen tests could be a "game changer." Such tests would 253 allow for cheap, rapid, frequent (even daily) testing without need for a processing lab. 30 The tests could 254 be performed by workers themselves and, while having lower sensitivity than PCR-based assays, greater 255 testing frequency would help ensure fewer missed cases. 30 Additionally, positive results would more 256 definitively suggest actual contagiousness rather than inconsequential past infection. 30 257 258

Another "game changer" is vaccination. As of this writing, two COVID-19 vaccines have just received 259 emergency use authorization. Essential food workers will be prioritized for receipt. 31 A vaccinated 260

workforce changes the calculus about the value of asymptomatic-worker screening-at least until the 261 emergence of the next pandemic. 262 263 For any future pandemic, the same issues will inevitably arise again. In what has been described as a 264 "leadership vacuum" for COVID-19, 32 testing was neither prioritized nor coordinated; individual 265 companies were largely left to fend for themselves. Hopefully, under a new administration, government 266 will place greater importance on testing-particularly testing of critical infrastructure workers. 267

In the interim, individual companies will continue to have to determine whether asymptomatic-worker 269 screening makes sense. The decision will continue to be one of consequence. Critical-infrastructure 270 workers are critical for a reason. Screening may not be essential, but food production is. 271 J o u r n a l P r e -p r o o f 

the Essential Critical Infrastructure Workforce: Ensuring Community and National 273 Resilience in COVID-19 Response

Nutrition amid the COVID-19 pandemic: a multi-level framework for 277 action

COVID-19): People with Certain Medical Conditions

Covid-19 and 282 Disparities in Nutrition and Obesity

Racial/Ethnic Disparities in Household Food Insecurity 284

During the COVID-19 Pandemic: a Nationally Representative Study

Getting your workplace ready for COVID-19: How COVID-19 spreads

COVID-19): Overview of Testing for SARS-CoV-2

Update: COVID-19 Among Workers in Meat

Mapping Covid-19 outbreaks in the food system

Meat processing plants are closing due to covid-19 outbreaks. Beef shortfalls may 312 follow. The Washington Post

Prevalence of Asymptomatic SARS-CoV-2 Infection: A Narrative Review

Systematic review with 316 meta-analysis of the accuracy of diagnostic tests for COVID-19

Nasal Swab Sampling for SARS-CoV-2: a Convenient 318

Alternative in Times of Nasopharyngeal Swab Shortage

Variation in False-Negative Rate of

Reverse Transcriptase Polymerase Chain Reaction-Based SARS-CoV-2 Tests by Time Since Exposure

The Role of Antibody 323

Interpreting Diagnostic Tests for SARS-CoV-2

COVID-19 and the Path to Immunity

COVID-19 Cases and Deaths in Federal 336 and State Prisons

CoV-2 Infection in Children Without Symptoms of Coronavirus Disease

Rethinking Covid-19 Test Sensitivity -A Strategy for

ACIP COVID-19 Vaccines Work Group -Phased Allocation of COVID-19 Vaccines

Dying in a Leadership Vacuum

= indeterminant test result (including "quantity not sufficient"), Alt. = Alternative Rows shaded gray are possible scenarios not realized at either site of the pilot trial

both PCR and IgG could also have indeterminant results, adding more possible combinations. b for example, due to cross-contamination during specimen collection, shipping, or aliquoting c "Healthy -continue working" is always an alternative possibility given any/all positive tests results could be false positives d Exact duration of self-isolation would not be defined by CDC guidance; company would have to decide what is most reasonable e for example, due to other circulating human beta coronaviruses

Created by Danone North America staff prior to start of testing pilot