key: cord-0907494-s5nmonaf
authors: Fwoloshi, Sombo; Hines, Jonas Z; Barradas, Danielle T; Yingst, Samuel; Siwingwa, Mpanji; Chirwa, Lameck; Zulu, James E; Banda, Dabwitso; Wolkon, Adam; Nikoi, Kotey I; Chirwa, Bob; Kampamba, Davies; Shibemba, Aaron; Sivile, Suilanji; Zyambo, Khozya D; Chanda, Duncan; Mupeta, Francis; Kapina, Muzala; Sinyange, Nyambe; Kapata, Nathan; Zulu, Paul M; Makupe, Alex; Mweemba, Aggrey; Mbewe, Nyuma; Ziko, Luunga; Mukonka, Victor; Mulenga, Lloyd B; Malama, Kennedy; Agolory, Simon
title: Prevalence of Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) among Health Care Workers—Zambia, July 2020
date: 2021-03-30
journal: Clin Infect Dis
DOI: 10.1093/cid/ciab273
sha: 250ecad181d803f0f23f332abb2dd35488d68399
doc_id: 907494
cord_uid: s5nmonaf

INTRODUCTION: Healthcare workers (HCWs) in Zambia have become infected with SARS-CoV-2, the virus that causes coronavirus disease (COVID-19). However, SARS-CoV-2 prevalence among HCWs is not known in Zambia. METHODS: We conducted a cross-sectional SARS-CoV-2 prevalence survey among Zambian HCWs in twenty health facilities in six districts in July 2020. Participants were tested for SARS-CoV-2 infection using polymerase chain reaction (PCR) and for SARS-CoV-2 antibodies using enzyme-linked immunosorbent assay (ELISA). Prevalence estimates and 95% confidence intervals (CIs), adjusted for health facility clustering, were calculated for each test separately and a combined measure for those who had PCR and ELISA performed. RESULTS: In total, 660 HCWs participated in the study, with 450 (68.2%) providing nasopharyngeal swab for PCR and 575 (87.1%) providing a blood specimen for ELISA. Sixty-six percent of participants were females and the median age was 31.5 years (interquartile range 26.2–39.8 years). The overall prevalence of the combined measure was 9.3% (95% CI 3.8%–14.7%). PCR-positive prevalence of SARS-CoV-2 was 6.6% (95% CI 2.0%–11.1%) and ELISA-positive prevalence was 2.2% (95% CI 0.5%–3.9%). CONCLUSIONS: SARS-CoV-2 prevalence among HCWs was similar to a population-based estimate (10.6%) during a period of community transmission in Zambia. Public health measures such as establishing COVID-19 treatment centers before the first cases, screening for COVID-19 symptoms among patients accessing health facilities, infection prevention and control trainings, and targeted distribution of personal protective equipment based on exposure risk might have prevented increased SARS-CoV-2 transmission among Zambian HCWs.

As with other respiratory viruses, severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), the virus that causes coronavirus disease 2019 (COVID-19) is transmitted primarily through respiratory droplets from symptomatic and asymptomatic persons infected with the virus (1) . Given the possibility of transmission of SARS-CoV-2 regardless of presence of symptoms, healthcare workers (HCWs) can be at elevated risk of acquiring the virus due to their role in patient care and treatment (2) . Use of personal protective equipment (PPE) such as face masks and face shields, and other public health measures such as triage of patients accessing health facilities and immediate isolation of those with COVID-19 symptoms can limit the spread of COVID-19 among HCWs (3) . However, shortages of PPE were commonplace in the early response to the SARS-CoV-2 outbreak in many countries, potentially placing healthcare workers at higher risk of infection with SARS-CoV-2 (4) (5) (6) . Shortages of PPE have been particularly pronounced in resource-limited settings where PPE are generally imported.

Determining the extent of spread and the prevalence of the virus among HCWs can be challenging in resource-limited settings because testing capacity is limited and many people with SARS-CoV-2 infection are asymptomatic or have only mild symptoms (1, (7) (8) (9) (10) .

Some of the available data indicate that seroprevalence of SARS-CoV-2 among HCWs in resource-rich countries is dependent on the type of work performed and can range from lower to higher prevalence compared with what is observed among the general public (2, (11) (12) (13) (14) (15) (16) (17) . For instance, in the U.S., nurses had the highest risk of SARS-CoV-2 infection among HCWs (2) . However, there are limited data about the prevalence of SARS-CoV-2 among HCWs in Africa where there have been severe shortages of PPE, testing for SARS-CoV-2 continues to be limited, and there tend to be shortages of HCWs in general (5, 18) . Small studies from Malawi and Nigeria found SARS-CoV-2 seroprevalence of 12.3%-45.1% among HCWs in urban settings (19) (20) (21) , whereas, in Togo, there was a low prevalence of SARS-CoV-2 (1.6%) among high-risk populations including HCWs (22) .

Zambia reported the first cases of COVID-19 in March 2020. By the end of July, over 13,000 Zambians were diagnosed with SARS-CoV-2, with most cases reported during July (Supplemental Figure) . Like other countries in the region, Zambia relies on imported PPE, and the Ministry of Health (MOH) realized that supply chain disruptions could diminish COVID-19 control and prevention efforts among HCWs. To reduce transmission of SARS-CoV-2 in healthcare settings, Zambian MOH implemented mitigation measures aimed at limiting introduction and spread of SARS-CoV-2 in health facilities.

Before the first confirmed COVID-19 cases, Zambia established COVID-19 isolation and treatment M a n u s c r i p t 5 5 facilities with the capacity to cohort patients with confirmed SARS-CoV-2 infection. At COVID-19 isolation and treatment facilities, clinicians trained in caring for COVID-19 patients worked for set periods of times (i.e., one month) after which they would quarantine for 14 days. In April, MOH introduced measures that required HFs to establish COVID-19 mitigation procedures including screening patients for symptoms of COVID-19 before patients could enter HFs (23); patients who screened positive for any COVID-19 symptoms were immediately isolated, given cloth masks, and were prioritized for COVID-19 testing. In addition, MOH officials conducted multiple infection prevention and control (IPC) trainings for HCWs using virtual platforms and distributed available PPE to HCWs based on risk of exposure to SARS-CoV-2. For example, HCWs who were directly managing COVID-19 patients were prioritized to receive face masks, goggles or face shields, gloves, and gowns.

Moreover, MOH modified criteria for COVID-19 testing eligibility to include HCWs who managed COVID-19 patients, were exposed to patients with COVID-19, or worked in facilities with COVID-19 patients irrespective of symptoms (23) . Additionally, health facilities increased outdoor waiting areas (given Zambia's favorable climate), and restricted visitors for inpatients. Furthermore, the Government of the Republic of Zambia introduced strict measures to limit the spread of SARS-CoV-2 in the community, including closing schools, bars and taverns, restaurants, and movie theatres; restricting large gatherings; prompt isolation of anyone who tested positive for SARS-CoV-2 and immediate contact tracing; mandated mask wearing or face covering in public; and mandatory quarantine of all travelers to Zambia for 14 days or pending a negative PCR-based test result.

SARS-CoV-2 prevalence was 10.6% during a cross-sectional, cluster sample, household survey conducted in six districts Zambia during July 2020, which was during the first wave in the country (Supplemental Figure) (24) . With widespread community transmission of SARS-CoV-2 in July 2020, many HCWs were also diagnosed with COVID-19. However, the extent of spread of SARS-CoV-2 among HCWs in Zambia and the risk factors for acquisition of the virus remained unclear. We assessed the prevalence of SARS-CoV-2 infection among Zambian HCWs in selected districts with known widespread community transmission.

A cross-sectional survey of SARS-CoV-2 prevalence among HCWs was conducted during July 2-31, 2020, at 20 health facilities in six districts across Zambia. The districts were purposefully selected based on high rates of confirmed COVID-19 cases, mixture of urban and rural setting, and being travel corridors to and from the neighboring countries. As of June 2020, these six A c c e p t e d M a n u s c r i p t 6 6 districts accounted for more than 90% of confirmed COVID-19 cases in Zambia and are home to onequarter of the 18 million people in Zambia. The districts have a total of 2,056 health facilities (HFs) and 25 ,865 professional HCWs (e.g., doctors, nurses, etc.) (. * Based on available resources, a total of 20 HFs were selected from the six districts (Supplemental Table) . The proportion of HFs in each district out of the total HFs in the six districts were calculated and a proportional number of HFs from each district were selected for inclusion. Facilities were then purposefully selected to represent the different types of HFs in Zambia (hospitals and urban or rural health centers). Three of 20 selected facilities were also COVID-19 treatment centers. All but one HF were in areas designated as urban. A convenience sample of HCWs at the selected HFs who were present during the survey dates were recruited with the goal of reaching 600 participants. For smaller HFs (e.g., health centers), all HCWs were included; for larger HFs (e.g., hospitals), 50 HCWs were invited to participate. This HCW survey was conducted simultaneously to a population-based household survey in the same districts (24) . The study was approved by the Zambia National Health Research Authority and the University of Zambia Biomedical Research Ethics Committee. The activity was reviewed by CDC and was conducted consistent with applicable federal law and CDC policy. † The study methods were aligned with those of the WHO Unity Studies (25) .

Variables. Participants were administered a standardized questionnaire by trained personnel that included information about demographics, past medical history, contact with a person with confirmed COVID-19, and history of recent illness on a tablet using REDCap (Research Electronic Data Capture, Nashville, Tennessee) hosted at the Zambia Ministry of Health. SARS-CoV-2 exposures included known contact with a laboratory-confirmed case, travel (domestic or international), typical means of transportation, past month health facility utilization, in-person attendance to work or school, and the number of visits to markets/grocery stores. Recent illness was assessed by asking if the participant had experienced any illnesses since February 2020 (before the first reported case in Zambia); if they responded affirmatively, symptomology was ascertained. HCWs were categorized as medical doctors, mid-level providers (clinical officers, nurse practitioners), nurses (registered/enrolled nurses and midwives), allied health (including physical therapists, nutritionists, psychosocial counselors, laboratory * Estimates that included all types of HCWs (as were included in this study) were not available. technicians/workers, and pharmacists) and non-clinical staff (including clerks, cashiers, laundry staff, porters, drivers, and security).

Sample collection. Nasopharyngeal swabs (one per participant) were collected into a cryovial with viral transport medium for detection of SARS-CoV-2 Ribonucleic acid (RNA) using real-time reverse transcription polymerase chain reaction (PCR). Blood samples were collected by finger prick using the BD microtainer EDTA cryovial tube system for detection of SARS-CoV-2 antibodies using enzymelinked immunosorbent assay (ELISA (Table 3) .

There were no differences in the prevalence by sex, age group, presence of a medical comorbid condition, known contact with a COVID-19 case, travel, or typical means of transportation (Table 3) . 

During the month of July when confirmed cases of COVID-19 were rapidly increasing in Zambia, the overall prevalence of SARS-CoV-2 among Zambian HCWs was similar to what was being observed among the general Zambian public (24) . The PCR prevalence was high in both populations, which was compatible with observed community-wide transmission during the study period. The similarity between the SARS-CoV-2 prevalence among HCWs and the general population was rather unexpected given

HCWs are believed to be at higher risk of SARS-CoV-2 infections because of potential nosocomial exposures in HFs (28) . Yet, a study of HCWs in the U.S. found equivalent and even lower seroprevalence estimates than comparable cumulative incidence estimated in some geographic areas, which could have results from greater access to PPE by HCWs early in the outbreak (2) . SARS-CoV-2 prevalence was higher among allied health and non-clinical staff compared with nurses who provided direct patient care. This is in contrast to a study from Nigeria where there was no prevalence difference by HCW occupation, and another study from Scotland where patient-facing providers had elevated risk (19, 30) . It is possible that these non-clinical HCWs were less familiar with SARS-CoV-2 IPC best practices, as they were not included in the IPC trainings that were conducted by A c c e p t e d M a n u s c r i p t 10 10 MOH. Moreover, non-clinical staff who were perceived to be lower risk than patient-facing providers, might not have been prioritized to receive PPE even though many of them might have come into contact with COVID-19 patients within their HFs. Furthermore, the pattern of SARS-CoV-2 prevalence among different types of HCW in this study could indicate SARS-CoV-2 infections were occurring outside HFs given widespread community transmission in July in Zambia. Thus, both nosocomial and community SARS-CoV-2 transmission were likely both occurring among HCWs in Zambia in July. Providing IPC trainings, optimizing engineering and administrative controls, and ensuring adequate access to PPE for all HCWs-including those without direct clinical roles-can reduce the risk of nosocomial SARS-CoV-2 transmission (3, 8) . Furthermore, universal masking in health facilities is another strategy that can substantially reduce risk of nosocomial transmission (31) .

HCWs in Livingstone District had higher PCR-positive prevalence than HCWs in other districts and, similarly, HCWs in Nakonde District had higher ELISA-positive prevalence than other HCWs in other districts. Moreover, the prevalence estimates in these districts were higher than in the general population (11.2% in Livingstone and 7.0% in Nakonde Districts) (24) . This difference is suggestive of nosocomial outbreaks among HCWs in these districts-potentially ongoing at the time of the study in Livingstone

District. In Nakonde District, a large outbreak was reported in early May 2020 (32), which could explain the higher ELISA-positive prevalence there.

There are several limitations to our study. The HFs included in our survey were purposefully selected and might not be representative of the HFs in Zambia. HFs were largely located in urban areas, and our findings do not reflect SARS-CoV-2 prevalence among rural HCWs; of note, persons residing in rural areas had lower SARS-CoV-2 prevalence in a population-based study in Zambia in July 2020 (24) .

Additionally, HCWs were conveniently sampled. Participants voluntarily participated in each aspect of the study (i.e., interview and nasopharyngeal and blood specimen collection), and the response rate for participants who had both PCR and ELISA tests was low (58% of all participants), which could have led to both less precise and biased estimates; therefore, PCR and ELISA prevalence estimates were also reported separately. Furthermore, the small sample size could have affected the ability to detect significant differences among age groups and other risk factors. The prevalence estimate for the combined measure was greater than the sum of the PCR and ELISA estimates, which was a result of how these estimates were calculated (i.e., the denominator was the number of participants who had data for the given measure). Next, we used Euroimmun ELISA for antibody testing, which is reported to have a sensitivity of about 90% (27) . This would suggest an underestimation of previous infections in A c c e p t e d M a n u s c r i p t 11 11 our survey, which may be further compounded other factors like Ig isotype, waning levels, crossreactivity, and other factors (33, 34) . Lack of access to antibody tests with higher sensitivity continues to be a challenge but future surveys might be able to use improved assays with higher sensitivity.

Despite 

A c c e p t e d M a n u s c r i p t 13 13 M a n u s c r i p t 16 16 Not calculated * Refers to the subset of participants who had both PCR and ELISA tests performed SARS-CoV-2 prevalence and 95% CIs were calculated as the proportion of positive results divided by the total number of tests (for a given test modality), adjusting confidence intervals for clustering by health facility. Participants with facility information missing (PCR=8; ELISA=21; combined measure=6) were excluded from the calculations. The sum of the PCR and ELISA prevalence estimates does not equal the combined measure prevalence estimate because each estimate was independently derived from the subset of study participants who had data for a given modality. CI: confidence interval; OR = odds ratio; ELISA: enzyme-linked immunosorbent assay; PCR: real-time polymerase chain reaction

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