Abstract

Background and objectives: Children comprised a significant part of the population during the second and third waves of the COVID-19 pandemic. The objectives of this study were to estimate the seroprevalence of COVID-19 IgG antibody among the children aged 6 to 14 years and to determine, if any, the factors associated with seropositivity.

Methods: This cross-sectional study was conducted in a selected block of West Bengal, India over a period of 1 year (April 2022-March 2023) among children. Thirty villages in the block were selected by cluster sampling technique. COVID-19 IgM/IgG Rapid Antibody Test Kit (ICMR approved) was used for the detection of SARS-CoV-2 IgG antibodies.  Data were analyzed by appropriate statistical tests.

Results: Total 600 children were enrolled in the study.SARS-CoV-2 IgG antibody was positive in 57.2% children. The seropositivity rate (91.8%) was significantly (p<0.001) high among children of age group 12 to 14 years. Seropositivity rate was not significantly different between male and female children (46.4% vs. 53.6%; p>0.05).

Conclusion: SARS-COV-2 IgG antibody was positive in a high proportion of children residing in rural areas indicating asymptomatic coronavirus infections among rural population. Socio-demographic factors such as higher age group and father’s education were significantly associated with seropositivity.

July 2024; Vol. 18(2):010.  DOI:https://doi.org/10.55010/imcjms.18.022

*Correspondence: Vineeta Shukla, Department of Community Medicine, Infectious Diseases and Beliaghata General Hospital, Kolkata, India. Email: [email protected]

Introduction

Children are the foundation of any nation, and the health and welfare of its child population determines the progress of any country. The COVID-19 pandemic, which hasn't been formally declared over yet, has led to some significant advancement in the worldwide health care industry. Since children constituted a significant portion of the unprotected population during the second and third waves of the COVID-19 pandemic, their vulnerability was an important consideration. Children and adolescents are also susceptible to the infection and thus form a part of the transmission chain. In late 2021, different nations had reported COVID-19 outbreaks in schools and child care facilities. What is more striking is that children were often reported to have asymptomatic infections than adults in case of COVID-19 [1].

Even though SARS-CoV-2 was thought to impact children and adolescents more mildly than adults, it nonetheless affects a variety of systems, with the cardiovascular signs being most noticeable [2]. In addition to being extremely unwell and necessitating Intensive Care Unit (ICU) admissions, child death rate, particularly in those with Multisystem Inflammatory Syndrome in Children (MIS-C), have been reported as high as 9% [3]. According to the World Health Organization (WHO), children under five years of age represented 2% of reported global COVID-19 cases during January 2020 to October 2021 and older children (5 to 14 years) accounted for 7% of the cases [4]. There was limited seroprevalence data among children in late 2021. Also, the antibody response to SARS-CoV-2 among children was poorly characterized.

Very few studies related to SARS-CoV-2 antibody detection among children were carried out in India in the years 2020 and 2021 and literature from West Bengal was scarce [5]. Following the second wave of COVID-19 cases in 2021, George et al. conducted a study in a rural area of Karnataka, India, and found that children's seroprevalence of antibodies to SARS CoV-2 was 45.9% [6]. In 2021, a multicenter study conducted by Misra et al. [7] found the prevalence of SARS-CoV-2 antibody among under-18-year-olds in both urban and rural areas as 55.7%, with a higher seropositivity rate among females. In another study, about 48.3% of children aged 5 to 17 in both urban and rural Kerala were found positive for COVID-19 antibody [8]. But there was no significant association with gender. In Delhi, India, seroprevalence of immunoglobulin G antibodies against SARS-CoV-2 among children aged 5 to 17 rose from 52.8% in January 2021 to 81.8% in September and October 2021, according to a repeated cross-sectional study [9]. Age and seropositivity correlated positively, but not with gender.

There was a dearth of information about the status of seroprevalence of SARS-COV-2 IgG antibody among people of rural Bengal, especially among children. Therefore,, the present study was conducted in a block of West Bengal, India with objectives to estimate the seroprevalence of SARS-CoV-2 IgG antibody among rural children aged 6 to 14 years and to find the factors associated (if any) with seropositivity among them.

Materials and methods

This descriptive cross-sectional study was carried out in Budge-Budge II block, West Bengal over a period of 12 months from April 2022 to March 2023. The study was approved by Institutional Ethics Committee (IPGME&R/IEC/2022/006, dated 21.01.2022). For children 7-11 years, informed oral assent in presence of parents and for children 12 - 14 years old, informed written assent was taken. Informed written consent was taken from all parents.

Study population: Children aged 7 to 14 years who had been residing with their families in the block for last one year or more were included.Those who had a laboratory confirmed COVID-19 infection in the past or who had any symptoms of COVID-19 infection during the time of data collection were excluded.

Sample size and sampling method: Considering 61.1%  seroprevalence of anti- SARS-CoV-2 IgG antibody rate [10]  and at 95% confidence interval (CI) and with 10% margin of error, the total sample size was calculated as  591 (after multiplying by 2 for design effect for cluster sampling and adding 20% as inconclusive). A total of 30 clusters were selected. Therefore, from each cluster (village) 591/30=19.7≈20 children were enrolled. Thirty villages were selected from a total of 61 villages using probability proportional to size method.

Data collection: Before commencing data collection, an orientation cum training session was conducted involving the Block Medical Officer, Accredited Social Health Activists (ASHA), Auxiliary Nurse Midwives (ANMs) and other health workers followed by pretesting among 20 children of the same age group who were not included in the final sample. Information on socio-demographic, clinical, COVID-19 exposure related questions and vaccination details were collected in a predesigned, pretested, and structured questionnaire. Socio-demographic variables included: age, gender, type of family, socio-economic status, as per Modified BG Prasad Scale 2022 [11], parents’ education, and occupation. Information on COVID-19 related infection included: history of COVID-19 infection in family, vaccination status of family members, and number of doses of vaccine received.

Collection of blood and test: About 30µL of whole blood was collected aseptically by finger prick and tested immediately for SARS-CoV-2 IgM or IgG antibodies by Oscar Covid-19 Rapid Antibody Test Kit (ICMR approved).The measurement range of the assay was from 0.40 U/ml to 250 U/ml. Levels of <0.80 and ≥0.80 U/ml were considered as negative and positive respectively according to the manufacturer’s recommendations. Blood sample was placed in the specimen well of the test kit. Two drops (100µL) of buffer solution (provided with the kit) were added to the specimen. The results were read after 15 minutes. If a coloured line appeared at the IgG level along with the control line, the results were interpreted as positive.

Data analysis: Descriptive statistical measures such as frequencies, mean, standard deviation and confidence interval (CI) were determined. Z test for proportion was applied to test for significant difference between age groups and gender. Multivariable binary logistic regression was performed to find predictors of IgG positive test among the study population.

 Results

Out of 600 children, about 40.5% belonged to age group of 12-14 years and their mean age was 10.36 ± 2.53 years. A little more than half were females (54.7%) and more than 80% followed Hinduism by faith. About 86.3% resided in joint households and half of the families belonged to upper middle class (50.2%).There was a health care worker in only 1.2% of the families (Table-1). None of the children had undergone any kind of COVID-19 detection test prior to the study. A small proportion (64, 10.7%) of the families had a laboratory confirmed history of COVID-19 infection within last one year in at least one of the members. Out of those who tested positive, 4 required hospitalizations and 1 of them died (Table-2).

Table-1: Distribution of the study participants according to the socio-demographic profile (N=600)

Table-2: Distribution of the study participants according to COVID-19 related information (N=600)

About 73% of the families had all their members vaccinated against COVID-19. Out of the 64 people infected with COVID-19 in past one year, 49 had received two doses of vaccine prior to getting the infection. Most common reason for not taking the vaccine was fear of side effects (Table-3).

Table-3: Distribution of the study participants according to COVID-19 vaccination related information (N=600)

Out of 600 children, 343 (57.2%) were SARS-CoV-2 IgG antibody positive by rapid antibody test kit. There were no IgM positive cases and none of the tests were inconclusive. The seropositivity was found to be significantly high (91.8%; p<0.001)) in 12 to 14 years old children compared to other age groups. Sero-positivity rate did not differ significantly between male and female across all age groups (p >0.05; Table- 4).

Table-4:  Seroprevalence of SARS-CoV-2 IgG antibodies among the study participants (N=600)

On performing Pearson’s Chi Square test, socio-demographic categories such as age group and father’s education were found to be significantly associated with seroprevalence. The variables which were considered biologically plausible to be included for multivariable binary logistic regression were age group, family type, father’s education, father’s occupation, and mother’s education. However, on multiple regression analysis only higher age group, 9 to 11 years and 12 to 14 years had statistically significant higher adjusted odds ratio of seropositivity (Tables-5 and 6).

Table-5: Association between seroprevalence of SARS-CoV-2 IgG antibodies and socio-demographic and other factors (N=600)

 Table-6: Multivariable binary logistic regression showing predictors of SARS-CoV-2 IgG seropositivity (N=600)

Discussion

In India, the total number of COVID-19 positive children in the second wave was reported higher than that of the first wave [12]. Murhekar et al., [10] in a study conducted in 70 districts throughout India, which included both urban and rural areas, reported increased rate of seropositivity to SARS-CoV-2 with age [10]. Antibodies against SARS-CoV-2 were 57.2% children aged 6 to 9 years which was greater than the present study. Seroprevalence was 61.6% among 10 to 17 year old children which was lower than the findings of this study for children aged 12 to 14 years. They also reported higher seroprevalence among females (69.2%) than males (65.8%), a finding similar to the current study. The increased seroprevalence in rural areas indicated that infection in the second wave was widespread in rural areas.

In rural Karnataka, George et al. [6] conducted a cross-sectional study involving 412 children aged between 11 months to 18 years. The study's findings indicated an overall seroprevalence of antibodies to SARS-CoV-2 as 45.9%. Compared to the current study, the seropositivity to SARS-CoV-2 was comparatively lower in their children. Seroprevalence in the age group 6-10 years was 35.9% while it was 50.4% among 11-15 years old children.In Karnataka, the seropositive status of the parents, any family members who tested positive, and a history of symptoms suggestive of COVID-19 were substantially associated with the seropositivity among children. In the current study, seropositivity was significantly associated with age and father's educational attainment.

A multicentre seroepidemiological study conducted by Misra et al. [7] in selected urban and rural areas of five sites selected from four Indian regions (Delhi, Odisha, Uttar Pradesh, Tripura) reported a seroprevalence of 55.7% (using IgG ELISA) among children. This was slightly less than the prevalence found in the current study. The prevalence of SARS-CoV-2 infection among female and male children (58.6% and 53%) in their study was almost same as the current study. Age group wise distribution showed higher seroprevalence among 5-9 years old children (43.8%) compared to this study. About 60.3% of 10-17 years old children were seropositive. Saanuet al. [8] also reported COVID-19 antibody seroprevalence of 48.3% in children of Ernakulam district of Kerala. The seroprevalence of COVID-19 antibody was higher among children of mothers with skilled/unskilled occupation, residents of rural area, above poverty line category children, positive history of COVID-19, and those with history of contact with COVID-19-positive patients. None of these factors were found to have a statistically significant association with seroprevalence in this study. According to a repeated cross-sectional analyses study conducted by Sharma et al.[9] in Delhi, India, the seroprevalence of antibodies to SARS-CoV-2 among children aged 5 to 17 climbed to 81.8% in September and October 2021 from 52.8% in January 2021. Jahan et al. [13] conducted a meta-analysis on the seroprevalence of IgG antibodies against SARS-CoV-2 in the general population in India from March 2020 to August 2021. The overall pooled seroprevalence was 20.7% in the first wave and 69.2% in the second wave, with higher seroprevalence in urban regions than rural. Also, seroprevalence did not differ by age and gender. In a Bangladesh study among general population by Rahman et al. [14], the overall adjusted seroprevalence was 48.3%, which did not differ by gender. Children up to 17 years had a significantly lower seroprevalence 38.6% compared to adults. Increasing age and education were identified as risk factors for seropositivity. A very low IgG seropositivity (3.9% in children aged less than 9 years) was reported from a cross-sectional study in Pakistan by Ahmad et al. [15]. Also, the seroprevalence was higher in urban than rural areas. Seropositivity was around twice as common in the older age group (20 years and above) than in the 0–9 age group. In our study the seropositivity rate for SARS-CoV-2 was 91.8% among children aged 12-14 years. Seroprevalence of IgG antibodies to SARS-CoV-2 positively correlated with participants’ age.The high rate of seroconversion among children who were not vaccinated suggested the existence of naturally occurring immunity generated by prior exposure to SARS-CoV-2.

The present study had some limitations. The study was conducted in only one block of West Bengal, thus limiting the generalization of the findings on a nationwide scale. A high proportion of children were SARS-CoV-2 IgG positive in the present study. Socio-demographic factors such as higher age group and father’s education were significantly associated with seropositivity. In addition to usual infection prevention measures, full vaccination coverage is may be considered as nearly half of the children were still at risk of contracting the disease.

Acknowledgement

The authors would like to send their deepest regards and gratitude to the Block Medical Officer and all the health workers of the block for their prompt help and unconditional support throughout the study.

Authors’ contributions

VS, VS MB, AM, MR and RS: Conception, design of the study, analysis, and interpretation of data, drafting and revising the article critically and final approval of the version.

Conflict of interest

There is no conflict of interest.

Financial support

 This study was funded by IJCM Ford Foundation, India. Travel and other logistics support were provided by the institute.

References

1.     Asrani P, Eapen MS, Hassan MI, Sohal SS. Implications of the second wave of COVID-19 in India. The Lancet Respir Med. 2021; 9: e93–4. DOI:https://doi.org/10.1016/S2213-2600(21)00312-X.

2.     Rajapakse N, Dixit D. Human and novel coronavirus infections in children: a review. Paediatr Int Child Health. 2021; 41: 36–55. DOI: 10.1080/20469047.2020.1781356.

3.     Acevedo L, Piñeres-Olave BE, Niño-Serna LF, Vega LM, Gomez I, Chacón S,et al. Mortality and clinical characteristics of multisystem inflammatory syndrome in children (MIS-C) associated with COVID-19 in critically ill patients: an observational multicenter study (MISCO study). BMC Pediatr. 2021; 21: 516.DOI: 10.1186/s12887-021-02974-9.

4.     World Health Organization. COVID-19 disease in children and adolescents. Scientific Brief [Internet]. Available at: https://www.who.int/publications/i/item/WHO-2019-nCoV-Sci_Brief-Children_and_adolescents-2021.1 [Accessed on April 12, 2024].

5.     Xu W, Li X, Dozier M, He Y, Kirolos A, Lang Z, et al. What is the evidence for transmission of COVID-19 by children in schools? A living systematic review. J Glob Health. 2020; 10: 021104. DOI: 10.7189/jogh.10.021104.

6.     George CE, Inbaraj LR, Rajukutty S, Joan RF, Muthuraj S, Chandrasingh S. Seroprevalence of SARS CoV-2 among children after the second surge (June 2021) in a rural district of South India: Findings and lessons from a population-based survey. Front Pediatr. 2022; 10: 997684. DOI: 10.3389/fped.2022.997684.

7.     Misra P, Kant S, Guleria R, Rai SK, Kishore S, Baidya S, et al. Serological prevalence of SARS-CoV-2 antibody among children and young age group (between 2 and 17 years) in India: an interim result from a large multicentric population-based seroepidemiological study. J Family Med Prim Care. 2022; 11: 2816–2823. DOI:10.4103/jfmpc.jfmpc_2274_21.

8.     Sidharthan S, Shaik S, Tomy C, Mohandas KS, Poornima B, Paediatric COVID19, Seroconversion group. Seroprevalence of COVID-19 antibody among children aged 5–17 years in an urban and rural area of Ernakulam District, Kerala. Indian J Public Health. 2022; 66: S66-70. DOI: 10.4103/ijph.ijph_1082_22.

9.     Sharma P, Basu S, Mishra S, Singh MM. Seroprevalence of immunoglobulin G antibodies against SARS-CoV-2 in children and adolescents in Delhi, India, from January to October 2021: a repeated cross-sectional analysis. Osong Public Health Res Perspect. 2022; 13: 184-190. DOI:10.24171/j.phrp.2022.0014.

10.  Murhekar MV, Bhatnagar T, Thangaraj JWV, Saravanakumar V, Santhosh Kumar M, Selvaraju S, et al. Seroprevalence of IgG antibodies against SARS-CoV-2 among the general population and healthcare workers in India, June–July 2021: A population-based cross-sectional study. PLoS Med. 2021; 18: e1003877. DOI: 10.1371/journal.pmed.1003877.

11.  Pentapati SSK, Debnath DJ. Updated BG Prasad's classification for the year 2022. J Family Med Prim Care. 2023; 12: 189-190. DOI:10.4103/jfmpc.jfmpc_1478_22

12.  Muthusamy S, Sarojam B, Sugunan S, Krishna G, S B, A S AK. Clinical Profile and Short-Term Outcome of Children with Acute SARS-CoV-2 Infection during the first and second waves of the pandemic. Indian J Pediatr. 2023; 90: 443-449. DOI: 10.1007/s12098-022-04193-1.

13.  Jahan N, Brahma A, Kumar MS, Bagepally BS, Ponnaiah M, Bhatnagar T, et al. Seroprevalence of IgG antibodies against SARS-CoV-2 in India, March 2020 to August 2021: a systematic review and meta-analysis. Int J Infect Dis. 2022; 116: 59-67. DOI: 10.1016/j.ijid.2021.12.353.

14.  Rahman M, Khan SR, Alamgir ASM, Kennedy DS, Hakim F, Evers ES, et al. Seroprevalence of SARS-CoV-2 antibodies among forcibly displaced Myanmar nationals in Cox's Bazar, Bangladesh 2020: a population-based cross-sectional study. BMJ Open. 2022; 12: e066653. DOI: 10.1136/bmjopen-2022-066653.

15.  Ahmad AM, Shahzad K, Masood M, Umar M, Abbasi F, Hafeez A. COVID-19 seroprevalence in Pakistan: a cross-sectional study. BMJ Open. 2022; 12: e055381. DOI: 10.1136/bmjopen-2021-055381.

Cite this article as: