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Original Article

SARS-CoV-2 IgG Seroprevalence Detected by Chemiluminescence Immunoassay Among Healthcare Personnel and Patients in a Province With a Low Incidence Rate of COVID-19 During the First Wave of COVID-19 in Thailand

Patamatamkul, Samadhi MD; Rawangban, Pratya MD; Prommongkol, Bhurapol MD; Potongcamphan, Maythinee MD

Author Information
Infectious Diseases in Clinical Practice: May 2022 - Volume 30 - Issue 3 - e1150
doi: 10.1097/IPC.0000000000001150
  • Open

Abstract

Although COVID-19 cases in Thailand are currently surging amid a new wave, there is still limited evidence addressing seroprevalence from past waves of COVID-19. During the first wave of COVID-19, there was concern regarding inadequate nucleic acid tests in many suburban areas due to limited capacity of molecular laboratories. Undetected asymptomatic transmission of COVID-19 during the first wave of COVID-19 was proposed by a recently published seroprevalence study conducted in Ranong, a province without polymerase chain reaction (PCR)–confirmed COVID-19 cases during that study period.1 The study showed 0.8% IgM seropositivity among 844 staff members in Ranong Hospital from April 17 to May 17, 2020, in which most cases were asymptomatic without COVID-19 exposure risk.1 Another large-scale nationwide seroprevalence survey in Thailand from April 8 to June 26, 2020, showed 0.2% IgG seropositivity and 5.5% combined IgG and/or IgM seropositivity among healthcare personnel (HCP) and patients without COVID-19 symptoms in 52 hospitals.2

The strength of these studies is that they were performed during the first wave of COVID-19, during which antibody levels were still high. The rapid antibody test used in both studies had a specificity of >98%, compared with the enzyme-linked immunosorbent assay (ELISA) method with 99.2% to 100% specificity, and therefore, false positives are unlikely.3 However, another study performed in Bangkok, which had the highest COVID-19 incidence rate, found only 0.015% IgG seropositivity among army personnel aged 20 to 60 years using the ELISA method.4 All these studies used only single time-point testing without follow-up serum testing. Thus, there are still conflicting data regarding the actual seroprevalence rates in different areas of Thailand.

In seroprevalence studies conducted in Europe during the early COVID-19 pandemic, there was a 1% prevalence of symptomatic COVID-19 among 9705 HCPs in the Netherlands in March 2020 and a combined SARS-CoV-2 IgM and IgG seropositivity of 4.04% among 29,295 HCPs in Denmark in April 2020.5,6 Meanwhile, there was a low incidence of confirmed COVID-19 infection in these countries during the study period: 614 and 8073 cases in the Netherlands and Denmark, respectively.7 In addition, a seroprevalence study in Malawi, a resource-constrained country in sub-Saharan Africa, showed a high seroprevalence among healthcare workers of 12.3% in May 22 to June 19, 2020, with only 749 reported COVID-19 cases in the country by the end of the study period.8 These data support the hypothesis of hidden SARS-CoV-2 transmission among high-risk exposure groups. Addressing the seroprevalence rate in asymptomatic individuals may help in the decision to actively screen for COVID-19 in the community to control undetected ongoing transmission.

In this study, we used a quantitative chemiluminescence immunoassay (CLIA) approved by the US Food and Drug Administration to screen for SARS-CoV-2 antibodies in a population with a wide range of exposure risk and underlying health conditions. The aim was to estimate SARS-CoV-2 seroprevalence in Mahasarakham Province during the first wave of COVID-19 in Thailand. In addition, the study addressed possible cross-reaction with other common infectious or immunologic diseases among patients who attended our hospital.

MATERIALS AND METHODS

Study Participants and Sample Recruitment

We conducted cross-sectional serologic testing for SARS-CoV-2 antibodies among HCPs and patients in Suddhavej Hospital, Mahasarakham University. There were 250 HCPs during the study period. This is a secondary care hospital with a 104-bed capacity, covering a population of at least 60,000. It is situated in the downtown of a city with a total population in the province of 974,534 (data as of 2015).

The samples used in the study were serum collected from February 20 to April 30, 2020, at the start and during the first wave of COVID-19 in Thailand. Inclusion criteria were as follows: (1) HCP without any previous symptoms compatible with COVID-19 within 14 days and (2) patients with another confirmed diagnosis, including infectious and immunologic diseases, who visited outpatient or inpatient clinics and had regular blood tests. We excluded cases with a previously diagnosed COVID-19 infection. An IgG antibody test was done in all included cases, and an IgM antibody test was done only in the patient group.

Written consent was obtained from all HCPs and outpatients. Inpatients underwent routine in-hospital blood tests, and leftover serum was used for COVID-19 testing, meaning that the need for consent was waived. This study was approved by the Ethics Committee of Mahasarakham University (approval number 265/2563).

Antibody Detection

IgG and IgM antibodies against SARS-CoV-2 were measured using the Food and Drug Administration–approved MAGLUMI 2019-nCoV IgG/IgM indirect CLIA kit (Shenzhen New Industries Biomedical Engineering Co, Ltd, Shenzhen, China). According to the instructions, the sensitivity and specificity of the kits were 91.21% and 97.33% for IgG and 48.28% and 96.27% for IgM, respectively. As a screening assay for COVID-19, combined nucleocapsid (N) protein and spike (S) glycoprotein were used as coated antigens to increase the sensitivity. The levels of IgG and IgM antibodies were positively correlated with Relative Luminescence Units (RLU) and were calculated as arbitrary units per milliliter (AU/mL). The tests for IgG and IgM were considered reactive with RLU level ≥1.0 AU/mL according to the manufacturer's declaration.9

Specimen Collection and Handling

A 5-mL sample of venous blood was collected into an EDTA-coated tube. Leftover serum volume varied, but 2 mL was deemed adequate to perform the test. The specimens allowed for only a single freeze-thaw cycle. Each tube was labeled with a unique participant ID. Samples from both venous blood and leftover serum were immediately stored at −20°C.

Sample Size Calculation and Statistical Analysis

Assuming seroprevalence of ≤1%, a sample size of at least 75 was required given the sensitivity and specificity of the IgG antibody. The assumed seroprevalence was based on the estimation for a rare disease of 1% because of the lack of seroprevalence study for SARS-CoV-2 in Thailand before the start of our study.10 Ninety-five percent confidence intervals (CIs) for unadjusted seroprevalence were estimated using exact binomial models. A Mann-Whitney U test was used to compare IgG and IgM values between and within each group. All statistical analyses were done with SPSS software version 23 (SPSS, Chicago, Illinois).

RESULTS

There were 112 HCPs and 78 patients included in this study. No case had a previous positive SARS-CoV-2 nucleic acid test result or was previously diagnosed with COVID-19. The flow of case selection is shown in Figure 1. The median age of participants was 29 years (interquartile range [IQR], 25–40 years), and 35.8% were male. The median age of the HCPs was 29 years (IQR, 26.25–34 years), and there were 16.1% male participants included in the HCP group. The HCPs included 89 nurse-assistants (79.5%), 14 doctors (12.5%), and 9 laboratory personnel (8%). The patient cohort included 35 outpatients and 43 inpatients; their median age was 31 years (IQR, 23–59 years), and 64.1% were male. Most HIV cases were virologically suppressed (87.1% [27 of 31]) with a mean CD4 of 452.48 ± 201.28 cell/mm3 (21.4% ± 8.61%). Three patients did not have HIV RNA data, and CD4 counts were unavailable in 1 patient. All HIV-infected patients were currently on combination antiretroviral therapy, except for 1 IgG-positive case, which is described later. The detailed characteristics of all patients are described in Table 1.

F1
FIGURE 1:
Flow of case selection.
TABLE 1 - Baseline Characteristics of All Participants in the Study
Baseline Characteristics HCP (112) Patient
Total (78) Non-HIV (44) HIV (34)
Age (IQR), y 29 (26.25–34) 31 (23–59) 52.5 (40–73.75) 24 (22.75–26)
Male, % 16.1 64.1 43.2 91.2
CD4, cell/mm3 452.48 ± 201.28
CD4, % 21.4 ± 8.61
Virologic suppression, % 87.1
Presenting conditions, %
 Infectious diseases
  Bacterial infection
  Respiratory tract infection 11.5 20.5
  Urinary tract infection 1.3 2.3
  Gastrointestinal infection  (gastroenteritis, cholangitis) 5.1 9.1
  Unspecified sepsis 3.8 6.8
  Other bacterial infection 6.4 11.4
 Viral infection
  Respiratory tract infection 10.3 18.2
  Dengue infection 5.1 9.1
  Other viral infection 3.8 6.8
  HIV infection 43.6 100
 Immunologic diseases
  Interferon-γ autoantibody with or without  opportunistic infections 2.6 4.5
  Active systemic lupus erythematosus 1.3 2.3
  Rheumatoid arthritis 1.3 2.3
 Other infectious or immunologic diseases 1.3 2.3
None 2.6 4.5
 IgM RLU value (IQR), AU/mL 0.359 (0.058–0.483) 0.412 (0.256– 0.493) 0.090 (0.000–0.483)
 IgG RLU value (IQR), AU/mL 0.059 (0.0296–0.0828) 0.0650 (0.0470–0.1050) 0.0735 (0.0565–0.1185) 0.0545 (0.0000–0.1210)
 Positive IgG, no. 1 2 1 1
 Positive IgM, no. 0 0 0 0
†One case was initially diagnosed as systemic lupus erythematosus but later confirmed as non-specific dermatitis, and another case presented with nasal congestion with suspected respiratory tract infection, but was later confirmed to be a deviated nasal septum

The seroprevalence rates of SARS-CoV-2 IgG for the HCP and patient groups were 0.9% (1 of 112; 95% CI, 0.0226–4.9) and 2.6% (2 of 78; 95% CI, 0.3–9), respectively. The overall IgG seroprevalence in this study was 1.6% (3 of 190; 95% CI, 0.3–4.5). For the 3 positive cases, the RLU values were 5.400, 1.340, and 1.001 AU/mL, respectively. Repeated sampling from each case 3 months after the first samples were taken resulted in positivity only in 1 case, an HCP. The second RLU values for each case were 5.542, 0.329, and 0.872 AU/mL, respectively.

Investigations of these 3 positive cases found potential risk for SARS-CoV-2 exposure. The first case was a 30-year-old man who worked as an assistant laboratory technician. His potential exposure was that 4 weeks before specimen collection; he traveled to and from Buriram Province in a crowded bus with many people from Bangkok during the nationwide lockdown. During that period, the estimated incidence rate of COVID-19 in Buriram was 0.81 per 100,000 population, compared with 0.1 per 100,000 population in Mahasarakham. He denied any COVID-19–associated symptoms. The index first serum was also tested for IgM antibody, which was nonreactive (RLU = 0.347 AU/mL).

Another case was a 51-year-old asymptomatic woman who attended regular outpatient department visits for health checkup. The possible exposure risk was that her daughter, who was living in the same house, came back from China with an upper respiratory tract infection 8 weeks before the sample collection. The case's daughter was not tested for SARS-CoV-2 by real-time reverse transcription–PCR (rRT-PCR) during that time because the city was not on the list of possible widespread COVID-19.

The last case was a 52-year-old woman who presented with pneumocystis pneumonia and was found to have AIDS. She had a CD4 of 14 cell/mm3 (5%). She recently traveled back from Bangkok but did not recall any exposure to a person with a COVID-19–like illness.

The IgM antibody test was done only in the patient group, and 4 cases did not have adequate leftover serum for IgM testing. No seropositivity for IgM was found (0/74). Characteristics of patients who were tested for both IgM and IgG are shown in Table 1.

There was no significant difference in IgG RLU level between the HCP and patient groups (P = 0.356). Among the patient group, IgG and IgM levels in patients without HIV were significantly higher than in HIV patients (P = 0.003 and 0.027, respectively; Table 1).

At the end of the collection period, a total of 277 respiratory specimens had been tested by rRT-PCR in our province, yielding only 1 positive test result. This was confirmed as the only COVID-19 case during the study period.

DISCUSSION

This study found a low overall seroprevalence for SARS-CoV-2 among HCPs and patients in Suddhavej Hospital, Mahasarakham Province, during the first wave of COVID-19 in Thailand. However, we found that the estimated seroprevalence was higher in the lower-exposure-risk patient group. It is noteworthy that all positive cases had a potential exposure risk from provinces with a higher COVID-19 prevalence than our province. This observation suggests that in-community asymptomatic transmission or in-hospital transmission during the first COVID-19 wave in Thailand was unlikely. A strength of our study is that we were able to obtain follow-up IgG antibody levels to confirm persistent positivity, which is indicative of true past infection with SARS-CoV-2.

Our results demonstrated higher IgG seropositivity than previous seroprevalence studies in Thailand, where the rate ranged from 0.2% to 0.61%. Comparing similar population of HCPs and patients with Nopsopon et al,1 our study revealed a higher estimated IgG seroprevalence of 1.6% (95% CI, 0.3%–4.5%) versus 0.2% (95% CI, 0.1%–0.8%). This finding is likely due to the smaller sample size in our study, or different exposure or adherence to preventive measures. In addition, we used the CLIA method to detect IgG, which is more sensitive and specific than a rapid antibody test. The Infectious Diseases Society of America suggests testing for SARS-CoV-2 IgG or total antibodies for epidemiological purposes and recommends against using both SARS-CoV-2 IgM and IgG to detect past SARS-CoV-2 infection.11 In addition, the time after infection after which the MAGLUMI 2019-nCoV IgG/IgM indirect CLIA kit can first detect IgM and IgG is similar.11 IgG persists at a level detectable using this kit for >30 days, rendering a false-negative test during the study period very unlikely.12 Thus, the sole use of SARS-CoV-2 IgG antibody for determining SARS-CoV-2 serostatus by CLIA or ELISA is adequate.11 Overall, our result suggests that it is possible that seroprevalence may be higher than previously reported in lower-exposure-risk group.

It is noteworthy that the large seroprevalence studies conducted early during the COVID-19 pandemic revealed higher seropositivity rates among high-exposure-risk groups such as HCP than in the general population.6,13 In a study conducted in London, at Whittington Health NHS Trust, in May and June 2020, 31.6% tested positive for SARS-CoV-2 antibodies from 2167 individuals tested, compared with an estimated seroprevalence of 17.5% for London's general population.13 In this study, working in the COVID-19 ward was associated with a higher rate of seropositivity.13 The findings were concordant with the study by Iversen et al6 conducted in Denmark during a similar period and a recent meta-analysis combining many seroprevalence studies.13,14 All these data suggest that high seropositivity among HCPs is mainly attributable to patient-to-HCP transmission, possibly due to shortages of personal protective equipment (PPE) and/or poor adherence to infection prevention and control measures.14

However, there are also conflicting results demonstrating that in-hospital COVID-19 transmission from patient-to-HCP and seropositivity are not associated.15,16 These studies suggest that community SARS-CoV-2 exposure or household contact plays the major role in seropositivity among HCPs.15,16 A large, multicenter seroprevalence study including 24,749 HCPs in the United States revealed a seropositivity of 4.4% (95% CI, 4.1%–4.6%). In multivariable analysis, community COVID-19 contact and community COVID-19 cumulative incidence were associated with seropositivity.15 Moreover, there was a seropositivity of 6.4% (95% CI, 5.5%–7.3%) reported in a single-center study from Belgium in which 3056 HCPs participated.16 In agreement with the US data, household contact with suspected or confirmed COVID-19 was associated with antibody positivity. A recent focused review by Shenoy and Weber17 supports these studies, showing that the risk of nosocomial transmission from patient to HCP and from HCP to patient is relatively low, 1.2% and 0.4%, respectively.

Several factors contribute to differences in seropositivity among studies, including the study design, the populations and dates of data collection, use of antibody tests with variation in sensitivity and specificity, lockdown and quarantine measures in the respective territories where the studies were conducted, and adherence to infection prevention measures, especially the appropriate use of PPE.

Our results show that seropositivity in the HCP in our study population was most likely due to recent travel to areas with a higher COVID-19 incidence rate than our province where COVID-19 infection may have been acquired by community exposure. This is similar to the findings of the US and Belgian studies where community transmission was associated with high COVID-19 seropositivity among HCPs.15,16 These findings should be reassuring for most HCPs working in the frontline, in that the currently used PPE is adequate for protecting against infection if other preventive measures outside patient care, such as physical distancing, universal mask wearing, and regular hand washing, are also strictly implemented.17

Of note, considering that transient low-titer positivity was found in only 2 patients, a false-positive IgG test is still possible. Unfortunately, a nucleic acid test of respiratory samples from the 2 positive cases was not available at the time of serum testing. Another explanation is a rapid waning of antibody response, which is commonly found among asymptomatic or mild COVID-19 patients.18 In addition, the IgG antibody test using the MAGLUMI 2019-nCoV antibody assay demonstrates a significant decline in IgG level 45 days after onset, and false IgG negativity is found in up to 20% of cases compared with other quantitative antibody assays.19,20 Cross-reaction with recent infection with non–SARS-CoV-2 coronavirus strains, such as coronavirus HKU1, NL63, OC43, or 229E, are very unlikely according to multiple studies regarding the use of the MAGLUMI 2019-nCoV antibody assay from prepandemic sera.21,22 Combining testing for IgM and IgG antibodies from convalescent serum 17 days after the onset of symptoms can modestly increase the assay sensitivity, from 90.9% to 95.5%.23 Unfortunately, detection of IgM using the MAGLUMI 2019-nCoV kit peaks 12 to 13 days after symptom onset and continues to decline thereafter.12 The IgM level is also related to the severity of SARS-CoV-2 infection.24 Given possible SARS-CoV-2 exposure more than 1 month ago in both asymptomatic cases in our cohort, the IgM level may have declined to an undetectable level. All these pieces of evidence suggest that, even without IgM positivity, the IgG positivity of both patients in our study likely reflects a true past infection.

In addition to the studied serum from the IgG-positive healthcare worker, there was a persistently elevated IgG titer of 5.542 AU/mL in the third serum sample taken 10 months after the first test. We examined the IgG level in convalescent serum (10–14 days after illness or first nucleic acid test positivity) of confirmed asymptomatic-to-mild COVID-19 patients in our hospital and found that the median level was 1.53 AU/mL (IQR, 1.39–4.967 AU/mL). This range of IgG level is comparable with that in a previous study of mild COVID-19 using the same assay.19 We concluded that the persistently elevated level of IgG was consistent with previous SARS-CoV-2 infection. This is an interesting finding that even an asymptomatic individual with previous COVID-19 can maintain IgG antibodies for up to a year. Recent immunologic study revealed that spike-IgG can be detected up to 9 to 11 months after COVID-19 infection in most cases.25 Interestingly, a slightly higher percentage of persistent seropositivity was seen in the asymptomatic-to-mild COVID-19 infection group than in the moderate COVID-19 infection group.25 In addition, most cases elicited considerable humoral and cellular immune response at 9 to 11 months after onset.25 These findings are concordant with the persistent antibody response found in our case. However, the determining factors among individuals for a persistent immune response after SARS-CoV-2 infection remain to be explored.

The IgM and IgG assays using CLIA demonstrate no cross-reactivity with multiple acute and chronic infectious and immunologic diseases. Our findings are in agreement with a previous analytical study in which there was no cross-reactivity in the MAGLUMI 2019-nCoV IgM/IgG assay among patients with autoimmune disease.24 However, serologic diagnosis of COVID-19 in the era of COVID-19 vaccination will be challenging. Spike-IgG antibodies are highly elevated after COVID-19 vaccination and remain so for a long period with the use of mRNA or potent viral vector vaccines.26,27 In contrast, the spike IgM antibodies are only modestly elevated and decline more rapidly.26,27 It has been shown that in COVID-19 breakthrough infection in vaccinated individuals, 65% have antinucleocapsid IgM/IgG seroconversion 3 weeks after onset.28 Given the high specificity of the nucleocapsid-based MAGLUMI 2019-nCoV IgM assay (>96%), these findings may support the use of nucleocapsid-protein IgM antibody, especially in vaccinated patients with unexplained subacute pneumonia and an initial negative upper respiratory tract PCR for SARS-CoV-2, to help with the diagnosis of COVID-19 pneumonia.9,23,24 However, more studies are required to validate serologic diagnosis in vaccine breakthrough SARS-CoV-2 infections. Many questions remain to be answered; for example, whether spike-specific, nucleocapsid-specific, or combined spike/nucleocapsid antibodies should be used, and whether IgM, IgA, or IgG alone or in some combination should be used?

This cross-sectional study has several important limitations. Participants who had blood taken for screening may not represent seroprevalence in either the Thai or the overall provincial population. Differences between our studied population and the aforementioned population include underlying health, exposure risk, or adherence to prevention measures, including use of masks and social distancing. All these differences affect seroprevalence in each particular population. In addition, the studied population covers only a small city area, and therefore, overall provincial seroprevalence may be overestimated because of the selection of higher-risk and a more crowded environment. Underestimation of seroprevalence was unlikely because we collected samples during a 2-month period during the first wave of COVID-19, in which waning of antibody detected by CLIA would be unlikely if recent infection had occurred.

Our study suggests that there is a low SARS-CoV-2 seroprevalence in a province outside Bangkok in a population with high risk of exposure. Community acquisition of SARS-CoV-2 from areas with a high COVID-19 incidence rate during travel was the major cause of seropositivity in our study population. These findings imply that preventive measures during the first wave of COVID-19 in Thailand were effective in controlling cross-transmission between provinces, even with the initial limited capacity for PCR testing in some suburban areas. Our study also stresses the need for broad coverage of COVID-19 vaccination in our province, and presumably all other suburban areas in Thailand, to provide adequate herd immunity to protect against the next wave of COVID-19.

ACKNOWLEDGMENTS

We would like to thank all the laboratory staff for providing the tests in the study.

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Keywords:

seroprevalence; chemiluminescence immunoassay; antibody; SARS-CoV-2; COVID-19

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