Dynamics of formation of anti- bodies to SARS-CoV-2 after coronavirus infection in children

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Abstract

Objective. To estimate the level of antibodies to SARS-CoV-2-IgM and SARS-CoV-2-IgG in children with COVID-19 in acute period and during 1 year period of follow-up after coronavirus infection.

Materials and methods. Blood samples for the presence of IgM and IgG antibodies to SARS-CoV-2 were analyzed in 119 children aged 11.0 [10.1; 11.2] with COVID-19 in the acute period (29.4 % asymptomatic, 51.3 % mild and 19.3 % moderate), and SARS–CoV-2-IgG in the dynamics of the follow-up after 1 (n=55), 6 (n=33) and 12 (n=32) months from the moment of discharge from the hospital in a prospective cohort study. The levels of SARS-CoV-2 surface glycoprotein S, including the receptor-binding domain – RBD were measured at different time by using enzyme-linked immunosorbent assay.

Results. The level of IgM positive rate for SARS-CoV-2 was initially negative in 86.6 % of children with COVID-19. The original seroconversion (on admission to the hospital) was 38.7 % and it increased to 96.7 % in 1 month and to 100 % in 12 months of observation. There were no statistically significant differences in IgG persistence depending on the age and course of COVID-19.

Conclusions. The new coronavirus infection causes a long-term response of IgG antibodies to SARS-CoV-2 which persists for one year of observation and increases by 12 months after the infection regardless of the severity of COVID-19.

Full Text

INTRODUCTION

The novel human coronavirus SARS-CoV-2 is highly contagious, and the disease it causes, COVID-19, can lead to significant morbidity and mortality in some patients [1]. In children, SARS-CoV-2 infection is asymptomatic or mild; however, children are susceptible to severe COVID-19 manifestations and the associated post-infectious multisystem inflammatory syndrome [2]. Moreover, the severity of COVID-19 is associated with the host’s immune response against SARS-CoV-2, and children and adolescents with mild or asymptomatic coronavirus infection can produce a strong and persistent antibody response [3].

Laboratory methods for diagnosing SARS-CoV-2 are based on the detection of viral RNA in patient secretions using the polymerase chain reaction (PCR) method and of antibodies (immunoglobulins M and G) in blood serum [4].

The immune response against SARS-CoV-2 plays a critical role in determining clinical outcome in adults and children [5]. Immunity to SARS-CoV-2 induced by natural infection may be mediated by a combination of humoral and cellular immunity [6]. A study comparing children to adults revealed different immune profiles during coronavirus infection, indicating less severe outcomes in pediatric patients [7].

Immune protective factors against SARS-CoV-2 have not been identified, although neutralizing antibodies are increasingly recognized as major mediators of protection [8].

Studies of severe acute respiratory syndrome (SARS) and Middle East respiratory syndrome showed that virus-specific antibodies were detected in 80 %–100 % of patients 2 weeks after symptom onset [9; 10].

Most adults with coronavirus infection produce an IgG response that can persist for at least 12 months [11]. Recovered seropositive adults have up to 89 % protection against reinfection with the same strain [12]. In contrast, the proportion of children infected with SARS-CoV-2 with seroconvertion is unknown, particularly among patients with asymptomatic or mild COVID-19. Furthermore, children may have distinct immune responses that modulate clinical severity [7]. Additionally, preexisting antibodies to seasonal human coronaviruses may contribute to some level of protection against SARS-CoV-2 in children [13]. Several innate and adaptive immune response aspects in children are not yet fully characterized owing to the limited number of studies in this population. The humoral response to SARS-CoV-2 remains poorly understood, whereas the immunological response to vaccines is well described in clinical trials, the characteristics and persistence of seroconversion are unclear, and follow-up data on IgG levels after COVID-19 are limited.

This study aimed to assess the level of SARS-CoV-2-IgM and SARS-CoV-2-IgG in pediatric patients with COVID-19 in the acute period and during 1-year follow-up after coronavirus infection.

MATERIALS AND METHODS

The prospective cohort study involved 119 children with COVID-19 from the City Clinical Hospital No. 1 of Chita, which at the time of the work was the single hospital accepting patients with coronavirus infection in the Trans-Baikal Territory.

Government authorities have taken preventive measures and given recommendations for the hospitalization of all pediatric patients with COVID-19, including asymptomatic forms to maintain social distance between people and prevent the spread of the SARS-CoV-2 virus.

Inclusion criteria were age 0–17 years, positive result for SARS-CoV-2, and parent/child consent to participate in the study. Non-inclusion criteria were children aged >17 years, negative test result for SARS-CoV-2, and refusal of parents (legal representatives) or children to participate in the study.

The diagnosis of COVID-19 is based on the criteria according to the methodological recommendations “Aspects of clinical manifestations and treatment of the disease caused by a new coronavirus infection (COVID-19) in pediatric patients” (version 1 dated April 24, 2020).

Demographic data, information about positive PCR tests for SARS-COV-2, medical history, comorbidities, and heredity were obtained from the electronic database of medical records.

All cases were confirmed by PCR using nasal and oropharyngeal swabs. During the study period, children and adolescents were not vaccinated against COVID-19. No reinfections were recorded during the follow-up period.

The severity of coronavirus infection was classified as asymptomatic but with a positive test for SARS-CoV-2 in 35 (29.4 %) pediatric patients (group I), as mild in 61 (51.3 %) pediatric patients (group II), and moderate in 23 (19.3 %) patients (group III). The median age of the pediatric patients was 11 (10.1; 11.2) years old; 53.8 % of those examined were boys. Additionally, children were distributed by age (subgroup 1, 0–6 years (n = 21); subgroup 2, 7–17 years (n = 98)).

To analyze the intensity of humoral immunity after coronavirus infection, SARS-CoV-2-IgG was determined by monitoring patients 1 month (n = 55), 6 months (n = 33), and 12 (n = 32) months after discharge from the hospital.

Blood samples were collected within 48 hours of hospitalization from all 119 pediatric patients and tested for the presence of IgM and IgG antibodies to the surface glycoprotein S of SARS-CoV-2, including the receptor-binding domain (RBD) in the blood serum. The study was conducted using an enzyme immunoassay with a set of reagents SARS-CoV-2-IgM-ELISA-BEST and SARS-CoV-2-IgG-ELISA-BEST (Vector-Best, Novosibirsk region) according to manufacturer instructions. Antibody levels were expressed in S/CO (Signal/Cut-off) as signal/ critical value: positive, results higher than 1.1 S/CO; questionable, those higher than 0.8 S/CO and lower than 1.1 S/CO; and negative, results lower than 0.8 S/CO.

Written voluntary informed consent to participate in the study was obtained from participants aged >15 years or from parents (legal representatives) of pediatric patients aged <15 years.

The study was approved by the local ethics committee of the Chita State Medical Academy (protocol no. 101; April 15, 2020) and was conducted in accordance with the Declaration of Helsinki.

Statistical processing of the research results was performed using IBM SPSS Statistics Version 25.0 software (International Business Machines Corporation, USA). The normality of distribution was tested using the Kolmogorov–Smirnov test. Quantitative variables were presented as median (Me) and interquartile range (Q1; Q3) and categorical variables as absolute values and percen­tages (%). The assessment of variations in the levels of the studied markers in the blood serum between two independent groups was performed using the Mann–Whitney test (U). Intergroup differences in one quantitative sign for comparisons of three or more independent groups were analyzed using the Kruskal–Wallis rank analysis of variance (H). The significant differences in pairwise comparisons between dependent samples were assessed using the Wilcoxon test. P < 0.05 was considered statistically significant.

RESULTS AND DISCUSSION

Serological testing for SARS-CoV-2 upon hospital admission demonstrated a lack of IgM antibody response in pediatric patients with COVID-19 in majority (86.6 %) of cases (Table 1).

 

Table 1

Level of positivity rate of SARS-CoV-2-IgM and SARS-CoV-2-IgG depending on the severity of COVID-19 in pediatric patients of different ages upon admission

COVID-19 severity

IgM PC* level, n/ %

IgG PC level, n/ %

Negative

 < 0.8 S/CO

Questionable

³0.8

and < 1.1 S/CO

Positive

 > 1.1 S/CO

Negative

 < 0.8 S/CO

Questionable ³0.8

and < 1.1 S/CO

Positive

 > 1.1 S/CO

Asymptomatic, n = 23

19/82.6

3/13

1/4.3

15/65.2

0/0

8/34.8

Mild, n = 61

54/88.5

4/6.6

3/4.9

35/57.4

1/1.6

25/40.9

Moderate, n = 35

30/85.7

1/2.9

4/11.4

17/48.6

5/14.3

13/37.1

Total, n = 119

103/86.6

8/6.7

8/6.7

67/56.3

6/5.0

46/38.7

Note: *, level of positivity coefficient (PC).

 

The median level of SARS-CoV-2-IgM in asymptomatic coronavirus infection was 0.37 [0.35; 0.55] S/CO and corresponded to the values for mild (0.27 [0.27; 0.56] S/CO; p = 0.533) and moderate (0.28 [0.27; 0.73] S/CO; p = 0.661) severity of COVID-19. The asymptomatic course of SARS-COV-2 infection was characterized by a serum IgG concentration of 0.41 [0.39; 2.86] and did not differ from the indicators for mild (0.49 [0.37, 2.99] S/CO; p = 0.439) and moderate (0.75 [1.76, 3.14] S/ CO; p = 0.551) forms. No statistical difference was found in the IgM and IgG levels between patients of groups II and III (p = 0.734 and p = 0.894 S/CO, respectively).

 Positive test results for IgM antibodies to the surface glycoprotein S (Spike) of SARS-CoV-2 in the blood serum were detected in 6.7 % of patients with confirmed SARS-CoV-2 infection, whereas 4.3 % of them were asymptomatic and 4.9 % and 11.4 % of patients had a mild and moderate form of the disease, respectively.

The seroprevalence (positive IgG antibodies to SARS-CoV-2) at the time of hospitalization was 38.7 %. Additionally, 56.3 % of patients with positive PCR for SARS-CoV-2 did not have IgG antibodies, and questionable results were recorded in 5 % of pediatric patients. It was revealed that 34.8 % of patients in group 1, 40.9 % of patients in group 2, and 37.1 % of pediatric patients in group 3 tested positive for SARS-CoV-2-IgG.

 

Table 2

Antibody titers upon admission depending on the severity of coronavirus infection in pediatric patients of different ages

Ig

(S/CO)

Study group

Test statistics

I, n = 23

II, n = 61

III, n = 35

0–6 years,

n = 7

7–17 years,

n = 16

0–6 years,

n = 7

7–17 years,

n = 54

7–17 years,

n = 28

Kruskal–Wallis,

df = 3

Mann–Whitney

Intragroup

comparison

Comparison of

subgroups studied

1

2

3

4

6

IgM

0.49

[0.40; 0.65]

0.30

[0.30; 0.55]

0.27

[0.27; 0.54]

0.27

[0.27; 0.58]

0.28

[0.28; 0.67]

U = 3.45;

p = 0.632

U1–2 = 43.5, p1–2 = 0.402;

U3–4 = 185.5, p3–4 = 0.937;

U5–6 = 65.0, p5–6 = 0.172

 

U1–3 = 20.0, p1–3 = 0.562;

U1–5 = 21.5, p1–5 = 0.701;

U3–5 = 18.0, p3–5 = 0.404;

U2–4 = 427.5, p2–4 = 0.950;

U2–6 = 216.0, p2–6 = 0.845;

U4–6 = 739.0, p4–6 = 0.868

IgG

0.44

[0.44; 4.08]

0.37

[0.36; 2.85]

0.31

[0.30; 1.68]

0.49

[0.49; 3.23]

0.69

[0.67; 2.13]

U = 3.90;

p = 0.564

U1–2 = 46.5, p1–2 = 0.524;

U3–4 = 151.5, p3–4 = 0.396;

U5–6 = 62.5, p5–6 = 0.143

 

U1–3 = 20.0, p1–3 = 0.564;

U1–5 = 16.0, p1–5 = 0.277;

U3–5 = 15.0, p3–5 = 0.225;

U2–4 = 363.0, p2–4 = 0.334;

U2–6 = 211.5, p2–6 = 0.760;

U4–6 = 696.0, p4–6 = 0.557

 

Table 2 presents the antibody titers used depending on the coronavirus infection severity in pediatric patients of different ages. The study results showed an increase in the titer of IgG antibodies to SARS-CoV-2 in patients aged 0–6 years with moderate COVID-19 compared to that in asymptomatic patients and those with mild forms of the disease, whereas no significant differences were noted in the levels of antibodies of the IgM and IgG classes depending on the age of the pediatric patients and disease severity (p > 0.05). Because no significant differences were observed in IgM and IgG levels between pediatric patients of different ages, further dynamic follow-up of the study groups was performed among pediatric patients aged 0–17 years.

Median level of SARS-CoV-2-IgG during dynamic follow-up 1 month after coronavirus infection was 9.55 [8.15; 10.90], which is significantly higher by 12 times than similar data in the acute period (0.81 [0.79, 3.74]; p = 0.000). By month 6 from the date of discharge from the hospital, the IgG level to SARS-CoV-2 was 10.38 [8.97; 10.25], which is significantly higher than that in the initial study (0.92 [0.87, 2.48]; p = 0.000).

The proportion of seropositive patients (IgG to SARS-CoV-2) reached its maximum (100 %) values of 10.12 [8.63; 10.34] when determined after 12 months, compared to the results obtained 1 month and 6 months after coronavirus infection (96.4 % and 96.9 %, respectively; Table 3).

 

Table 3

Dynamics of SARS-CoV-2-IgG antibody titer in pediatric patients after COVID-19

Post-COVID term

IgG PC level, n/%

Negative

 < 0.8 S/CO

Questionable

>0.8 and < 1.1 S/CO

Positive

 > 1.1 S/CO

1 month, n = 55

2/3.6

0/0

53/96.4

6 months, n = 33

1/3,0

0/0

32/96.9

12 months, n = 32

0/0

0/0

32/100.0

 

 

Serological testing for COVID-19 demonstrated IgG seroconversion in all pediatric patients after 12-month follow-up, including asymptomatic patients, and in the acute period of the disease, SARS-CoV-2-IgG was recorded in 38.7 %.

IgM provides the first line of defense in viral infections, whereas IgG production lags behind IgM and is responsible for long-term immunity and memory [14]. According to a previous report on SARS in 2003, IgM was detected in the blood of patients 3–6 days after disease onset, and IgG could be detected 8 days after the onset of infection [15]. Other studies [16; 17] on seropositivity for antibodies to SARS-CoV-2 in pediatric patients reported lower rates than those detected in this study. Thus, in a meta-analysis, Rostami et al. revealed that the prevalence of antibodies to SARS-CoV-2 in the population aged <19 years was 2.3 % [16]. According to the Spanish national registry, seropositivity for SARS-CoV-2 was registered in 12.5 % of adults and 7.7 % of children [17]. The present study showed that the level of anti-SARS-CoV-2-IgG at the time of hospitalization is already relatively high (38.7 %), which is consistent with a previous study that found an early and high level of IgG response against SARS-CoV-2 [18]. The high incidence of positive IgG in the early stage of SARS-CoV-2 infection may be due to the fact that some patients with COVID-19 are asymptomatic in the first days after infection [19]. A study showed that in 97.5 % of people, symptoms appear within 11.5 days [20]. The recorded date of disease onset may be later than the date of infection because of the asymptomatic course, which explains the high level of IgG during week 1 of illness [21].

The long-term immune response of SARS-CoV-2, demonstrated during the dynamic follow-up of pediatric patients who had coronavirus infection in our study, coincides with that of the coronavirus associated with SARS-CoV [22]. The researchers reported that IgG antibodies were continuously detected for 2 years in patients who recovered from SARS-CoV [23].

Additionally, previous studies confirm our findings of high IgG positivity rate for SARS-CoV-2 [21; 24; 25]. Thus, IgG antibody titers remained elevated against protein S and RBD in 96 % and 99 % of cases, respectively [24]. In 95.3 % of patients included in the study by Li, IgG against SARS-CoV-2 was detected 5 weeks after symptom onset [21]. Iyer et al. examined 343 patients and showed that IgG persisted for 90 days after symptom onset [25]. Moreover, Zhu et al. reported that over 60 % of adults remained IgG positive 7 months after symptom onset, regardless of COVID-19 severity [26]. In the study by Whitcombe, 96 % of patients had anti-S protein IgG levels above baseline 4–8 months after infection [24]. In children in the Irkutsk Region, after recovery from a confirmed new coronavirus infection, antibodies were detected in 66.1 % of cases and persisted for up to 10–15 months to the nucleocapsid and up to 15–18 months to the RBD of SARS-CoV-2 [27]. An assessment of IgG levels to SARS-CoV-2 after COVID-19 in pediatric patients demonstrated that the highest antibody levels persisted for 2–4 months after the illness [28].

Thus, longer follow-up of pediatric patients infected with SARS-CoV-2 is crucial to establish the duration of humoral protection in this population. Further research is required to elucidate the role of long-term humoral responses in pediatric patients following SARS-CoV-2 infection and their relationship with protection against recurrent infections.

Tracking dynamic changes in SARS-CoV-2-IgG can provide additional information for diagnosing, monitoring, and predicting COVID-19 and developing new vaccines.

CONCLUSIONS

In 6.7 % of pediatric patients with coronavirus infection at the time of hospitalization, positive levels of the positivity coefficient of IgM antibodies to SARS-CoV-2 were detected, whereas the overall seroconversion rate was 38.7 %. Children who have had COVID-19, starting from month 1 after discharge from the hospital, demonstrated increased SARS-CoV-2-IgG antibody titer. Most pediatric patients with SARS-CoV-2 infection remain serologically positive 6 months after infection. IgG antibodies to SARS-CoV-2 persist up to 12 months after infection, regardless of the severity of COVID-19.

×

About the authors

Irina K. Bogomolova

Chita State Medical Academy

Email: bogomolova_ik@mail.ru
ORCID iD: 0000-0003-4668-6071
Scopus Author ID: 57205157038
ResearcherId: R-2691-2017

MD, PhD, Professor, Head of the Department of Pediatrics of Medical and Dental Faculties

Russian Federation, Chita

Valentina N. Peregoedova

Chita State Medical Academy

Author for correspondence.
Email: v.peregoedova@mail.ru
ORCID iD: 0000-0002-9684-2864
SPIN-code: 1346-0396
Scopus Author ID: 57205157061
ResearcherId: Q-5166-2017

Candidate of Medical Sciences, Associate Professor of the Department of Pediatrics of Medical and Dental Faculties

Russian Federation, Chita

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