Analysis of human coronaviruses circulation

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Abstract

Introduction. The novel SARS-CoV-2 coronavirus, which emerged at the end of 2019 and caused a worldwide pandemic, triggered numerous questions about the epidemiology of the novel COVID-19 disease and  about wellknown coronavirus infections, which used to be given little attention due to their mild symptoms.

The purpose: The routine screening-based multiyear retrospective observational study of prevalence and circulation patterns of epidemic-prone human coronaviruses in Moscow.

Material and methods. The real-time polymerase chain reaction was used to detect RNA of human coronaviruses (HCoVs) in nasal and throat swabs from 16,511 patients with an acute respiratory infection (ARI), aged 1 month to 95 years (children accounted for 58.3%) from January 2016 to March 2020, and swabs from 505 relatively healthy children in 2008, 2010 and 2011.

 

Results. HCoVs were yearly found in 2.6–6.1% of the examined patients; the detection frequency was statistically higher in adults than in children, regardless of sex. At the height of the disease incidence in December 2019, HCoVs were detected in 13.7% of the examined, demonstrating a two-fold increase as compared to the multi-year average for that month. The statistical frequency of HCoV detection in ARI pediatric patients under 6 years was significantly higher than in their healthy peers (3.7 vs 0.7%, p = 0.008).

Conclusion. HCoVs circulate annually, demonstrating a winter-spring seasonal activity pattern in the Moscow Region and reaching peak levels in December. Over the years of observation, the HCoV epidemic activity reached maximum levels in December 2019–February 2020 and decreased in March to the multi-year average. Amid a growing number of SARS-CoV-2 cases imported to Moscow in March 2020, the HCoV detection frequency dropped sharply, which can be explained by the competition between different coronaviruses and by the specificity of HCoV detection with the diagnostic test kit used in this study.

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Introduction

Coronaviruses causing infectious diseases in animals and humans are common throughout the world. They belong to the family Coronaviridae, the subfamily Orthocoronavirinae, which is further divided into four genera: Alphacoronavirus, Betacoronavirus, Deltacoronavirus and Gammacoronavirus [1]. Representatives of Gammacoronavirus and Deltacoronavirus genera primarily infect birds. Viruses belonging to Alphacoronavirus and Betacoronavirus genera are found in mammals.

Human coronaviruses (HCoVs) circulating year-round in the human population, i.e. epidemic-prone coronaviruses, cause acute respiratory infections (ARI) [2] generally affecting an upper respiratory tract [3][4][5][6]. In rare cases, they are associated with a lower respiratory tract disease [7]; there were cases reported when human coronaviruses were isolated from patients with pneumonia [8].

Currently, there are four types of epidemic-prone human coronaviruses (HCoVs) that circulate continuously in the human population.

Human coronavirus 229E (the genus Alphacoronavirus, the subgenus Duvinacovirus) and Betacoronavirus 1 (formerly referred to as HCoV-OC43; the genus Betacoronavirus, the subgenus Embecovirus) have been known since the mid-1960s. Human coronavirus NL63 (the genus Alphacoronavirus, the subgenus Setracovirus) and Human coronavirus HKU1 (the genus Betacoronavirus, the subgenus Embecovirus) were discovered in 2004 and 2005, respectively.

Coronavirus virions are spherical particles with diameters of 120 nm; they contain helical nucleocapsid (genomic RNA bound to nucleoprotein (N)) coated with a lipid membrane with integral proteins: spike glycoprotein (S) forming a monolayer of club-shaped protrusions; hemagglutinin-esterase (HE); membrane protein (M) and envelope small membrane protein (E) [9]. Viruses enter cells of mucous membranes by using their spike proteins that bind to specific receptors; moreover, coronaviruses of animals and different types of HCoVs target different receptors [10].

The coronavirus genome, the largest genome among all RNA-containing viruses, consists of a linear, positive-sense, single-stranded RNA molecule, 27–32 kb in size.

RNA recombination of different types of coronaviruses can generate new viral variants characterized by altered tissue tropism, increased virulence and the ability to overcome the interspecies barrier [11][12][13]. When occurred between coronavirus genomes of bats and other animals, such recombination events, which are established by natural selection, triggered the emergence of coronaviruses highly virulent for humans: SARS-CoV, the virus causing severe acute respiratory syndrome (SARS) [14][15], MERS-CoV, the virus causing Middle East respiratory syndrome [16], and SARS-CoV-2, the virus causing COVID-19 [17]; the viruses emerged in 2002, 2012 and 2019, respectively.

Apparently, HCoVs also emerged as a result of recombination events involving different types of coronaviruses of mammals [18][19] with whom they share a common ancestor that existed millions of years ago [20].

The data about the epidemiology of infection caused by HCoVs are fragmentary: having been obtained in groups of patients in different years, they do not give decisive answers to questions regarding seasonality of coronavirus infection and HCoVs prevalence in different age groups of ARI patients. Different researchers inform about winter, spring or summer incidence peaks [21][22][23][24][25][26][27].

No long-term studies of human coronaviruses circulation have been performed in Russia.

The purpose of this work is to present the multiyear retrospective observational study of the prevalence of epidemic-prone human coronaviruses in Moscow. The study is based on the routine screening by using real-time polymerase chain reaction (PCR) method.

Materials and methods

Nasal and throat swabs from 16,511 patients with ARI symptoms were examined. The swabs were collected from January 2016 to March 2020 during the routine screening aimed at the identification of ARI etiology in Moscow. There are data on the age of 16,385 individuals and on the sex of 16,404 individuals. The age of the patients ranged from 1 month to 95 years; children aged 1 month through 18 years accounted for 58.3% of the examined.

The analysis also included the test findings for nasal and throat swabs collected from 505 relatively healthy children aged 1 month to 18 years (children under 6 years accounted for 56.2%); the swabs were collected in 2008, 2010 and 2011; the children had no symptoms of respiratory infection at the time of examination [28].

The RNA HCoVs detection based on real-time PCR test included differentiation by genera: Alphacoronavirus (HCoV NL63 and HCoV 229E) and Betacoronavirus (HCoV HKUI, HCoV OC43) and was performed with an AmpliSens ARVI-screen-FL kit (The Central Research Institute of Epidemiology of Rospotrebnadzor) according to the manufacturer’s instructions on the real-time PCR instruments: Rotor-Gene 6000 (Corbett Research, Australia), Rotor-Gene Q (QIAGEN GmbH, Germany), and DT-96 (OOO NPO DNA-Technology, Russia).

Nasal and throat swabs were taken in accordance with the instructional guidelines «Laboratory Diagnostics of Influenza and Other ARVI by Using Polymerase Chain Reaction» MR 3.1.0117-17 and the clinical guidelines «Laboratory Diagnostics of Influenza and Other ARVI using Polymerase Chain Reaction» (2016)1. 

The collected swabs were placed in tubes with 0.5 ml of transport medium and stored at the temperature ranging from +4 to +8 C for a maximum of 3 days. The statistical analysis included verification of the distributions for normality and calculation of the Pearson chi-square (χ2) statistic by using the SPSS Statistics v. 18 software package; the 95% confidence interval (CI) was calculated by the Wald method [29].

Results

HCoVs were detected annually; the percentage of positive cases demonstrated exponential growth by 2020, from 2.6% to 6.1% of the total number of the examined patients. The annual occurrence of viruses belonging to the genus Alphacoronavirus (Alpha-HCoV) exceeded that of Betacoronavirus (Beta-HCoV) by 1.5–3 times (Fig. 1).

Fig. 1. Prevalence of epidemic-prone coronaviruses over five years.

The horizontal line – years of observation (from January 2016 to March 2020); the vertical line, on the left – the absolute number of the observed and positive
cases; on the right – the proportion of positive cases.

The HCoVs circulation demonstrated a distinct winter-spring seasonal pattern (Fig. 2). The incidence surge was observed from November to May when HCoVs were detected in more than 3% of the ARI patients; the peak levels were reached in December–February (7.4–5.5%). In summer months, the proportion of the HCoV-infected did not exceed 0.5% (Fig. 2). The Alpha-HCoV monthly detection frequency was several times as high as that of Beta-HCoV.

Fig. 2. Seasonal prevalence of epidemic-prone coronaviruses over 5 years of observation (from January 2016 to March 2020).

The horizontal line – months of observation. The vertical line, on the left – the total absolute number of the observed and positive cases; on the right – the
proportion of positive cases per month for the entire observation period.

From November 2019 to February 2020, there was an increase in the HCoV epidemic activity: The detection frequency doubled as compared to the multi-year average (MYA) in each month of observation. In December 2019, at the height of the surge (Fig. 3), the frequency of HCoV detection was 13.7% (7.0% MYA); in January– February – 8% (3.1 and 4.2% MYA); in March it dropped sharply to 4.1% (4.2% MYA).

Fig. 3. Prevalence of epidemic-prone coronaviruses from September 2019 to March 2020.

Infection prevalence among patients of different sex and age deserves attention.

The cumulative proportion of coronavirus infection among ARI female patients was higher than the proportion of coronavirus-infected ARI males (4.6 vs 3.7; p = 0.013), though the proportions varied across years (Table 1), thus giving no proof of statistically significant differences in HCoV prevalence among females and males.

Table 1. Coronavirus detection frequency in female and male patients with an acute respiratory infection


Note. *Here and in table 2: CI – confidence interval.

The prevalence of coronavirus infection in ARI patients of different age is shown in Table 2. Despite the absence of a distinct age peak, HCoVs were detected more often among adults than among children (5.43%; 95% CI 4.92– 6.0 vs 3.19%, 95% CI 2.86–3.56; p < 0.01) (Fig. 4).

Table 2. Coronavirus prevalence in different age groups of patients with an acute respiratory infection

 

Fig. 4. Prevalence of epidemic-prone coronaviruses in children and adults.

The vertical line – the proportion of positive cases.

During the examination of a group of children without ARI symptoms, HCoVs were detected in 12 (2.1%; 95% CI 1.23–4.11%) out of 505 cases; positive test results were reported throughout the year, though more than half of them (seven cases) were identified in spring.

In relatively healthy children under 6 years, HCoVs were detected significantly more rarely than in children of the same age, but with ARI symptoms (0.7% vs 3.7%; p = 0.008). The prevalence of HCoVs in pediatric ARI patients older than 6 years and in relatively healthy children of the same age did not have any statistically significant differences: 66 (2.4%) out of 2,803 vs 10 (4.5%) out of 221 (p = 0.047).

Discussion

The obtained data suggest that HCoVs circulate annually and their activity in the Moscow Region tends to increase in the winter-spring period, reaching the peak level in December. The seasonality pattern identified during our study corresponds to the data of the research performed in Norway [30], whereas studies performed in Israel and Hong Kong prove spring-and-summer activity of HCoVs [27][31]. Apparently, it can be explained by region-specific climatic features affecting the circulation of HCoVs and other respiratory viruses [32].

The frequency of HCoV detection in our study is similar to the frequency in other countries [2][27][30][33].

Unfortunately, most of the published studies focused on the child population. The only published study conducted in the United States among patients aged 0–96 years showed the average age of 22 years for the HCoV-infected patients [33]. In our study, the average age of HCoV-infected patients is 24 years and the median age is 23 years.

We detected HCoVs in 2.1% of the relatively healthy children. Similar results (1.9%) were obtained by researchers in Slovenia [25]. In the Netherlands, HCoVs were detected in children of the control group at higher frequency (10%) [30].

In our study, the HCoV detection frequency among children under 6 years and with ARI symptoms was significantly higher than among healthy children of the same age, thus corresponding to the data obtained by researchers in Slovenia [25]. As for children aged 6–18 years, the frequency of HCoV detection in the sick and healthy was almost identical, demonstrating similarity to the data obtained by Norwegian researchers [30].

These age-related differences can be explained by a milder and asymptomatic course of infection in older children due to the acquired anamnestic immune response. The prevalence of coronavirus infection in adult ARI patients was higher than in children, presumably, due to the age-related weakening of anamnestic immune response.

Both genera of HCoVs demonstrated the identical circulation seasonality, but seasonal surges of Beta-HCoV incidence were not as pronounced as those of Alpha-HCoV, while the prevalence of Beta-HCoV among children and adults was almost the same.

Data of seroepidemiological studies show that IgG antibodies to different types of HCoVs are detected fairly often, especially in adults. The study conducted in the USA shows that from 91 to 100% of the individuals older than 50 years had IgG antibodies to all the four HCoVs in blood serum and 8–30% of the cases had secretory IgA produced by the nasal mucosa, thus being indicative of high prevalence of the infection and the risk of becoming re-infected with coronaviruses of the same type [34].

Experiments demonstrated the absence of cross-reactivity of neutralizing antibodies to HCoVs of different genera and within one genus Beta-HCoV [35][36].

Our data about the higher frequency of HCoV detection among adults than among children, together with the findings of immunology studies performed by our foreign colleagues suggest the existence of short-term immunological protection after infection and a probability of recurrence of infection with different types of HCoVs.

The seasonal sharp decrease in the HCoV detection frequency in March 2020 amid a growing number of SARSCoV-2 cases imported to Moscow could result from the competition between different coronaviruses and decisively confirms the specificity of RNA HCoVs detection with the diagnostic kit used in this study.

Conclusion

The performed retrospective observational study made it possible to estimate the prevalence and to identify HCoV circulation patterns in Moscow over five years (2016–2020). The HCoV circulation featured a winter-spring seasonal pattern and dominance of Alpha-HCoVs both in females and males. The prevalence of HCoVs ranged from 2.6 to 6.1% of the total number of patients examined a year, and demonstrated a two-fold increase as compared to the multi-year average during the epidemic season in 2019–2020. The frequency of HCoV detection in ARI pediatric patients under 6 years was significantly higher than in their relatively healthy peers, thus proving the significance of pathogens for development of infection. The older children, possibly with a protective history of immunity, being infected whith HCoVs, appears to have mild and asymptomatic disease, that may explain the similar frequency of detection of viruses in individuals of 6-18 years old with and without respiratory symptoms the similar frequency of detection of viruses in individuals with and without respiratory symptoms. The increased HCoV detection frequency in adults, which was revealed during this study, can be explained by the absent cross-reaction of neutralizing antibodies to different HCoVs and by the age-specific decrease in the level of antibodies.

In the last few years, the epidemic activity of human coronaviruses steadily increased to reach its maximum in December 2019–February 2020, i.e. the time coincident with the emergence of the novel SARS-CoV-2 coronavirus (the genus Betacoronavirus) in China. This coincidence could not be accidental; rather, it was a natural consequence of active evolutionary processes in the population of mammals’ coronaviruses, which should be further studied.

1. Clinical guidelines. https://fedlab.ru/upload/medialibrary/b71/_-_-_-_-_06122016.pdf (reference date: 23/6/2020).

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About the authors

S. B. Yatsyshina

Central Research Institute for Epidemiology of the Federal Service for Supervision of Consumer Rights Protection and Human Welfare

Author for correspondence.
Email: svetlana.yatsyshina@pcr.ms
ORCID iD: 0000-0003-4737-941X

PhD. Sci. (Biol.), Head of the Scientific Group on the Development of New Diagnostic Methods of ARI diagnostics

Moscow, 111123

Россия

M. V. Mamoshina

Central Research Institute for Epidemiology of the Federal Service for Supervision of Consumer Rights Protection and Human Welfare

Email: grya@cmd.su
ORCID iD: 0000-0002-1419-7807
Moscow, 111123

Россия

O. Yu. Shipulina

Central Research Institute for Epidemiology of the Federal Service for Supervision of Consumer Rights Protection and Human Welfare

Email: olga.shipulina@pcr.ms
ORCID iD: 0000-0003-4679-6772
Moscow, 111123

Россия

A. T. Podkolzin

Central Research Institute for Epidemiology of the Federal Service for Supervision of Consumer Rights Protection and Human Welfare

Email: apodkolzin@pcr.ru
ORCID iD: 0000-0002-0044-3341
Moscow, 111123

Россия

V. G. Akimkin

Central Research Institute for Epidemiology of the Federal Service for Supervision of Consumer Rights Protection and Human Welfare

Email: akimkin@pcr.ms
ORCID iD: 0000-0003-4228-9044
Moscow, 111123

Россия

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