COVID-19: evolution of the pandemic in Russia. Report II: dynamics of the circulation of SARS-CoV-2 genetic variants

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Abstract

Background. The ongoing pandemic of the novel coronavirus infection (COVID-19) draws attention to the significance of molecular and genetic monitoring of the SARS-CoV-2 spread among the population of the Russian Federation. The aim of the study was to analyze the dynamics of circulation of SARS-CoV-2 genetic variants in Russia.

Materials and methods. The analysis of the circulation dynamics for SARS-CoV-2 genetic variants in Russia was carried out, covering the period from 28/12/2020 to 26/6/2022. The analysis included the data from Rospotrebnadzor Report No. 970 "Information about Infectious Diseases in Individuals with Suspected Novel Coronavirus Infection" and the Virus Genome Aggregator of Russia (VGARus). The presence of SARS-CoV-2 RNA was confirmed by the real-time reverse transcription polymerase chain reaction. The primer panels developed at the Central Research Institute of Epidemiology were used for amplification of genomic fragments and the subsequent sequencing.

Results and discussion. Using the Russian VGARus platform developed by the Central Research Institute of Epidemiology, we received the data on mutational variability of SARS-CoV-2. By monitoring the circulation of SARS-CoV-2 genetic variants in Russia from 28/12/2020 to 26/6/2022, we found that Delta and Omicron genetic variants prevailed at different stages of the epidemic.

Conclusion. The data of molecular and genetic studies are an essential component of epidemiological surveillance, being critically important for making executive decisions aimed at prevention of further spread of SARS-CoV-2 and laying the groundwork for creating new vaccines.

Full Text

INTRODUCTION

The rapid development of the epidemic process of the novel COVID-19 infection (Corona Virus Disease 2019), which is etiologically related to the SARS-CoV-2 coronavirus (Severe acute respiratory syndrome-related coronavirus 2), has created favorable evolutionary conditions worldwide for emerging genetic variants of the pathogen, which acquire new pathogenic properties. This evolutionary trend of SARS-CoV-2, on the one hand, is supported by the advantages of the virus variants that are actively transmitted from human to human and, on the other hand, it is driven by the constraining of the spread of the virus variants that can cause severe disease and, consequently, result in hospitalization of patients and fewer numbers of effective contacts. It should be noted that at present, the global COVID-19 epidemic process is in unstable dynamic equilibrium; even a slight increase in the transmissibility of the pathogen, other things being equal, can cause a rise in the incidence [1–7].

Like other RNA viruses, SARS-CoV-2, adapting to its new hosts – humans, undergoes genetic evolution, which, consequently, results in mutations in the viral genome, and these mutations can alter the pathogenic potential of the virus. Addressing the problem of the growing number of SARS-CoV-2 variants, the U.S. Center for Disease Control and Prevention and the World Health Organization (WHO), independently of each other, have developed classification systems to divide emerging mutations of the virus into several subgroups based on their impact on transmissibility, fatality, and response to treatment.

Although there are differences between these two classifications, the first group of variants of concern (VOCs) can also include variants with proven characteristics such as enhanced transmissibility, severe disease, the increased number of fatal outcomes, and a significant decrease in neutralization by antibodies generated in response to the previous infection or vaccination. Currently, according to the WHO classification, the above category includes Delta (B.1.617.2) and Omicron (B.1.1.529) variants1. The second group is composed of variants of interest (VOIs) and includes variants with specific genetic markers associated with changes in receptor binding, reduced neutralization by antibodies, increased transmissibility, reduced efficacy of treatment, and the predicted increase in disease severity. The third group is represented by variants under monitoring (VUM), which are described as having potential effect on the virus transmission rate and treatment efficacy; however, over time, their percentage decreased almost to zero. The classification offered by the U.S. Center for Disease Control and Prevention has one more category – variants of high consequence (VOHC), which have clear evidence that the existing strategies of diagnosis, prevention, and treatment are significantly less effective for them than for previously circulating variants. In the meantime, currently there are no strains falling into the VOHC category2. The above abbreviations have become commonly used terms to define variants of the coronavirus causing COVID-19.

The analysis of the dynamics of the spread of the known and new genetic variants of SARS-CoV-2 circulating in Russia is of critical importance. In accordance with RF Government Decree No. 448 "On Approval of the Temporary Procedure for Provision of Decoded Genome Data for the Novel Coronavirus Infection (COVID-19)" dated 23/3/2021, the Central Research Institute of Epidemiology has developed and launched the Virus Genome Aggregator of Russia (VGARus)3. The VGARus database contains information about nucleotide sequences of SARS-CoV-2 viruses and their mutations prevailing in different regions of Russia and can be used for storage, systematization, and retrieval of data for detection of mutations and identification of virus strains.

VGARus offers the possibility for continuous monitoring of mutational variability of SARS-CoV-2, providing critically important data for detection of new genetic variants and tracing their prevalence in Russia. Molecular and genetic studies are essentially important for making executive decisions on preventive and epidemic control measures aimed to prevent the further spread of SARS-CoV-2 and create the platform for development of new vaccines [8–10].

The aim is to analyze the dynamics of circulation of SARS-CoV-2 genetic variants in Russia.

MATERIALS AND METHODS

The study was performed at the Central Research Institute of Epidemiology of Rospotrebnadzor. The dynamics of circulation of SARS-CoV-2 genetic variants in Russia was analyzed, covering the period from 28/12/2020 to 24/4/2022. The information about patients was retrieved from the database incorporating data from Rospotrebnadzor Report No. 970 "Information about Infectious Diseases in Individuals with Suspected Novel Coronavirus Infection". The ICD-10 U07.1 "COVID 19, identified virus" code was assigned to the above patients: COVID-19 was confirmed by laboratory tests, regardless of the severity of clinical manifestations or symptoms. The study included materials from VGARus, the national platform for aggregated data on SARS-CoV-2 genomes, the centralized database for epidemiological analysis on the novel coronavirus infection (COVID-19) and software "Epidemiological Analytics for the Novel Coronavirus Infection (COVID-19)" [11][12].

The laboratory tests were performed in compliance with Guidelines MR 3.1.0169-20 "Laboratory Diagnostics of COVID-19" and other regulatory documents. The biological material used in the study included nasal, nasopharyngeal, and/or throat swabs, bronchial washings collected during fibrobronchoscopy (bronchoalveolar lavage), (endo)tracheal and nasopharyngeal aspirate, sputum, biopsy or autopsy material of the respiratory tract.

The presence of SARS-CoV-2 RNA was confirmed by using the real-time reverse transcription polymerase chain reaction together with AmpliSens® CovBat-FL (No. RZN 2014/1987 of 7/4/2020) and LAMP AmpliSens® SARS-CoV-2 (No. RZN 2021/13357 of 3/2/2021) test systems. The AmpliSens® COVID-19-FL (No. RZN 2021/14026 of 09.04.2021) reagent kit was used to quantify SARS-CoV-2 RNA during RT-PCR. The sequencing was performed at the Central Research Institute of Epidemiology using the Illumina MiSeq platform and MiSeq Reagent Kit v2 (PE 150+150 or PE 250+250 cycles) or MiSeq Reagent Kit v3 (PE 300+300 cycles) as well as Illumina NextSeq 2000 and NextSeq 1000/2000 P2 reagents (300 cycles) v3. All sequences obtained during the study were deposited to the VGARus database. In addition to the above techniques, other organizations participating in building the VGARus database used other methods of amplification of nucleic acids and high-throughput sequencing techniques.

The statistical analysis was conducted using standard methods of descriptive statistics in Microsoft Excel and Statistica v.12.0 (StatSoft).

RESULTS

The implementation of RF Government Decree No. 448 of 23/3/2021 resulted in establishment of the Consortium made up of scientific organizations of Rospotrebnadzor and scientific organizations of other agencies. Currently, it combines 131 organizations, 40 of them are engaged in sequencing [13].

The implementation of the decree produced the resource that is unique in the territorial coverage and completeness of supporting information including data required for epidemiological analysis. The operation algorithm used for VGARus data can be effectively used for real-time and retrospective analysis of prevalence of SARS-CoV-2 genetic variants, taking advantage of the latest information about the genetic diversity of the COVID-19 pathogen.

At present, the evolution of the virus is continuously monitored to provide prompt response to its emerging and potentially dangerous variants as well as to revise and adopt measures aimed at prevention of COVID-19. The compulsory registration is performed in accordance with RF Government Decree No. 448 "On Approval of the Temporary Procedure for Provision of Decoded Genome Data for the Novel Coronavirus Infection (COVID-19)".

Scientists from the Central Research Institute of Epidemiology have designed bioinformatical analytical tools for detection of mutations and identification their affinity to epidemiologically significant strains. Sequencing data, including metadata, are steadily being deposited.

Clinical specimens registered in the database automatically receive registration numbers; the information about specimens includes the data obtained by sequencing of the nucleotide sequence of the SARS-CoV-2 variant. The algorithms used in the database automatically analyze mutations and identify the SARS-CoV-2 variant in each specimen. After the nucleotide sequence of the virus is downloaded, the system automatically launches the process of sequence validation, analyzing the identity with the specific genetic variant and (in case of a whole genome) identifying the genetic variant in accordance with the PANGOLIN nomenclature. The platform collects information from different sources: VGARus, epidemiological data from Rospotrebnadzor, data from the StopCoronavirus portal, WHO, demographic and social data for Russia (statistical data, reference materials). In addition, the VGARus platform provides the software program "Epidemiological Analytics for Novel Coronavirus Infection", which offers real-time analysis of data downloaded to the VGARus database.

The dynamic monitoring of mutation changes in coronaviruses detected in Russia, has been conducted since December 2020 when the first case of Alpha genetic variant (B.1.1.7) importation (28/12/2020) was detected.

Based on the data from the national VGARus database, a total of 130,355 sequences of SARSCoV-2 have been registered, including 67,451 (51.7%) whole-genome sequences and 62,904 (48.3%) partial sequences.

Among the sequences deposited to the VGARus database, 112,344 (86.2%) belong to VOC variants according to the WHO classification (the revised version of 26/11/2021). Each of these variants differs from the Wuhan variant by a specific set of mutations; 1,217 (0.9%) sequences belong to the Alpha variant; 94 (< 1%) belong to the Beta variant; 26 (< 1%) – to the Gamma variant; 58,530 (44.9%) and 52, 477 (40.2%) are classified as Delta and Omicron variants, respectively. 18,011 (13.8%) of the deposited sequences do not belong to VOC variants.

The Alpha genetic variant circulated in Russia in winter 2021. The Beta and Gamma genetic variants also occurred at the beginning of 2021; however, their occurrence was limited. The Delta genetic variant started spreading in Russia during the second half of April 2021 and prevailed till January 2022. The Omicron genetic variant was detected in Russia in December 2021, and since January 2022 it has been dominant in Russia. The dynamics of detected genetic variants of SARSCoV-2 during 2020-2022 and the COVID-19 incidence rates (per 100,000 population) in Russia are presented in Fig. 1.

 

Fig. 1. Dynamics of genetic variants of SARS-CoV-2 and COVID-19 incidence rates (per 100,000 population) in Russia (2020–2022).

 

After the whole-genome sequencing performed from 30/3/2020 to 26/6/2022, a total of 67,451 identified specimens were deposited to the VGARus database. 724 (1.07%) specimens were classified as the B.1.1.523 genetic variant; 1,329 (1.97%) were classified as B.1.1.317, 3,903 (5,79%) as B.1.1, 802 (1.19%) as Alpha (B.1.1.7), 3,678 (5.45%) as other genetic variants, 22,818 (33.83%) were classified as Omicron (B.1.1.529+BA*), 34,197 (50.69%) specimens were classified as Delta (B.1.617.2+AY*) (Fig. 2).

 

Fig. 2. The distribution of genetic variants in biomaterial specimens collected from 28/12/2020 to 26/6/2022.

 

The distribution of SARS-CoV-2 genetic variants by periods of the epidemic increase in the COVID-19 incidence rates in Russia during 2020-2022 as the evidence of dominance of Delta (B.1.617.2+AY*) and Omicron (B.1.1.529+BA*) genetic variants is shown in Table 1.

 

Table 1. Distribution of SARS-CoV-2 genetic variants by periods of the epidemic increase in the COVID-19 incidence in Russia (2020–2022)

Period

Number of samples

Genovariants, abs. (%)

B.1.1

B.1.1.317

B.1.1.523

Alpha

(B.1.1.7)

Delta

(B.1.617.2+AY.*)

Omicron

(B.1.1.529+BA.*)

other

I period 30.03.2020­30.08.2020

1701

1056 (62,08)

55 (3,28)

-

-

-

-

590 (34,69)

II period 31.08.2020­09.05.2021

7417

2497 (33,67)

1202 (16,21)

378 (5,10)

536 (7,23)

121 (1,63)

-

2683 (36,17)

III period 10.05.2021­12.09.2021

10 602

126 (1,19)

67 (0,63)

345 (3,25)

266 (2,51)

9502 (89,62)

-

296 (2,79)

IV period 19.09.2021­09.01.2022

23 315

21 (0,09)

2 (0,009)

1 (0,004)

-

21 795 (93,48)

1420 (6,09)

76 (0,33)

V period 10.01.2022­26.06.2022

24 416

203 (0,83)

3 (0,012)

-

-

2779 (11,38)

21 398 (87,64)

33 (0,14)

Total

67 451

3903 (5,79)

1329 (1,97)

724 (1,07)

802 (1,19)

34 197 (50,69)

22 818 (33,83)

3678 (5,45)

 

From May to December 2021, the Delta genetic variant (B.1.617.2 + AY.*) prevailed in Russia, reaching 100% occurrence among the detected variants. The variant, which was named AY.122 by the PANGOLIN nomenclature on 26/11/2021, has been dominant (83.3%) during all months of monitoring since the Delta genetic variant was registered.

In addition to AY.122, the most frequently occurred Delta subvariants were represented by the "parental" B.1.617.2 (9.1%), AY.126 (3,0%), and others. Other subvariants were of rare occurrence, accounting for 4.6% of the total Delta sequences (Fig. 3).

 

Fig. 3. Subvariants of the Delta lineage (B.1.617.2+AY.*) isolated in Russia.

 

A total of 30 sublineages of the Delta genetic variant were isolated in Russia; 5% of the analyzed whole genomes of the Delta lineage (B.1.617.2 + AY.*) are presented in Fig. 4.

 

Fig. 4. Subvariants of the B.1.617.2. (Delta) lineage, except for basic variant B.1.617.2 and subvariants AY.122, AY.126, AY.121, AY.43 isolated in Russia.

 

The analysis of the dynamics of subvariants of the Delta lineage (B.1.617.2 + AY.*), which were isolated in Russia, showed that in May 2021, the Delta lineage was mainly represented by B.1.617.2 (38.7%) and AY.122 (33.8%) sublineages and less frequently occurring sublineages; after their dissociation, the AY.122 sublineage accounted for 80% of the total population (Fig. 5).

 

Fig. 5. Dynamics of subvariants of the Delta lineage (B.1.617.2+AY.*), which were isolated in Russia, based on the data from the national VGARus database.

 

The Omicron variant has been rapidly spreading since December 2021; currently, it is the dominant variant in Russia (100% of all the studies specimens). The analysis of the data from the national VGARus database helped reveal the dissociation of the gentic Omicron lineage in Russia with the most frequently circulating subvariants BA.1 (54.5%), BA.1.1 (21.7%), and BA.2 (23.8%). Subvariant BA.3 was of rare occurrence and currently accounts for less than 0.1% of the total Omicron population (Fig. 6).

 

Fig. 6. Subvariants of the Omicron lineage (B.1.1.529+BA.*), which were isolated in Russia, based on the data from the national VGARus database as of 26/6/2022.

 

It should be noted that since 1/3/2022 subvariant BA.2 has been dominating in the Omicron lineage (B.1.1.529 + BA.*); its dominance coincided with the decrease in the COVID-19 incidence. It accounts for more than 80% of the total population of subvariants (Fig. 7).

 

Fig. 7. Dynamics of subvariants of the Omicron lineage (B.1.1.529 + BA.*), which were isolated in Russia, based on the data from the national VGARus database.

 

Thus, having analyzed the structure of the dominant genetic variants of the Delta lineage (B.1.617.2 + AY.*) and the Omicron lineage (B.1.1.529 + BA.*), we can conclude that heterogeneity and rapid changes in the pathogenic properties and transmissibility of the virus have a clear impact on the development of the epidemic process. This conclusion is supported by the dynamics of the epidemic process manifestations and by severity of the disease (Table 2). The highest incidence rate in 2020 (the dominance of the Wuhan strain) was 51.31 (per 100,000 population); the highest incidence rate in 2021 (the dominance of the Delta strain) was 192.45 (per 100,000 population); the highest incidence rate in 2022 (the dominance of the Omicron strain) was 905.37 (per 100,000 population).

 

Table 2. Comparative analysis (dynamics) of the manifestations of the COVID-19 epidemic process, considering the evolution of the pathogen

Manifestations of the epidemic process

Wuhan genetic variant

Delta genetic variant

Omicron genetic variant

Incidence per 100,000 population

51,31

192,45

905.37 (a 17.6-fold increase; p < 0.05)

Percentage of severe cases of infection, %

4,5

2,6

0.4% (a 11.3-fold decrease; p < 0.05)

Percentage of circulating coronaviruses among relatively healthy population, %*

10-12

13-16

30-37% (a 3-fold increase; p < 0.05)

Percentage of children among affected individuals, %

10

12

18% (a 1.8-fold increase; p < 0.05)

*Based on the data for Moscow and Moscow Region (n = 2,366,527).

 

DISCUSSION

During the first year of SARS-CoV-2 presence in the human population, its genome did not demonstrate any nucleotide substitutions, which could cause noticeable changes in the properties of the pathogen. However, as the survival of the pathogen as a biological species is impossible without evolutionary growth, the range of coronavirus population heterogeneity starts expanding through circulation of low-virulent and high-virulent variants; the expansion is followed by stabilizing selection and establishment of the epidemic variant of the pathogen. The first significant VOCs were detected at the end of 2020 – at the beginning of 2021: Alpha (B.1.1.7) in Great Britain, Beta (B.1.351) in South Africa, Gamma (P.1) in Brazil, and Delta (B.1.617.2) in India4. The emerging mutations altered the amino acid sequence of the spike (S) protein, which binds to the ACE2 receptor and facilitates the entry of the virus into sensitive human host cells, thus becoming the main factor of the COVID-19 pathogenesis. Such mutations raise reasonable concerns, as the aggressiveness of the virus depends on them.

In November 2021, the emergence of the new variant of SARS-CoV-2 coronavirus put an end to cautious optimism and hopes of experts for the soon coming winding-down of the COVID-19 pandemic; the new variant was first identified in Botswana and the Republic of South Africa. The new lineage was designated as BA.2, the main lineage of the recently detected variant of the coronavirus was designated as BA.1, while the umbrella name of the variant remained unchanged — B.1.1.529 according to the PANGO classification. On 26/11/2021, WHO classified the mutated virus as VOC and assigned the Omicron (B.1.1.529 + BA.*) code to it.

In the opinion of experts, SARS-COV-2 has undergone evolution, and the genomic changes promoted such characteristics as the ability to cause intensive transmission of the virus, to change the clinical symptoms of the disease, to evade the immune response, diagnostic techniques or therapeutical agents. The existence of multiple COVID-19 cluster on different continents can affect the epidemiological situation, lead to a new source of risk for the health of the global population and to a new wave of infection. Therefore, all countries should improve their epidemiological surveillance; perform genome sequencing for effective monitoring of circulating variants of SARS-CoV-2; deposit whole-genome sequences of the virus and supporting metadata to the publicly accessible database such as GISAID. The global dominance of the Omicron genetic variant calls for exploration of its impact on disease severity, effectiveness of epidemic control measures, immune response, neutralizing activity of antibodies, and other significant parameters5.

Today, there is a significant amount of data on evolutionary changes in the SARS-CoV-2 genome, including its tendencies to acquire new epidemiological properties. During its circulation in the human population, the SARS-CoV-2 genome, adapting to the new host, has acquired a certain number of nucleotide substitutions.

The COVID-19 pandemic once again confirmed the theory offered by academician V.D. Belyakov who believed that the development of the epidemic process was based on the phase changes in the heterogeneity of biological properties of interacting populations of the pathogen and human, involving the reverse negative relations in the process of self-regulation with an important role played by social and natural factors [14][15]. In accordance with the theory of self-regulation of parasitic systems, changes are associated not only with genetic variability, but also with other polydeterminant characteristics of the pathogen: With emergence of new genetic variants, SARS-CoV-2 has become less pathogenic, though more contagious for human. This specific characteristic is important not only for theoretical, but also for practical epidemiology, making it possible to predict the pattern of development of the epidemic situation.

CONCLUSION

The whole-genome sequencing of SARSCoV-2 genetic variants was performed in Russia from 28/12/2020 to 26/6/2022, using the VGARus database. It confirmed the dominance of Delta and Omicron genetic variants and demonstrated that from May to December 2021, the Delta genetic variant (B.1.617.2 + AY.*) was dominant in Russia, while subvariant AY.122 prevailed (83.3%). The Omicron variant started its rapid spread in December 2021, including dissociation of the Omicron genetic lineage and dominance of subvariants BA.1, BA.1.1, and BA.2. The BA.3 sublineage was of rare occurrence and currently accounts for less than 0.1% of the total Omicron population. The proportion of the BA.2 sublineage is gradually increasing (accounting for 80% of the Omicron sublineages isolated during the 16th–17th week in 2022). In Russia, a few BA.4 and BA.5 genetic variants have been detected; they have not developed into epidemic forms, causing asymptomatic or mild cases of acute respiratory viral infection.

It has been found that with emergence of new genetic variants, SARS-CoV-2 has become less pathogenic, though more contagious for human. This statement is supported by the dynamics of epidemic process manifestations and severity of the disease.

The SARS-CoV-2 virus is going through evolution, thus calling for continuous scientific studies involving advanced methods of the whole genome analysis of its genetic sequences.

Currently, the molecular and genetic monitoring of the SARS-CoV-2 circulation is a high-priority area of the epidemiological surveillance over COVID-19, being of critical importance for development and implementation of epidemic control measures.

The authors express their gratitude to the organizations participating in sequencing:

  • National Research Center of Epidemiology and Microbiology named after Honorary Academician N.F. Gamaleya, Moscow, Russia;
  • The Pirogov Russian National Research Medical University, Moscow, Russia;
  • The Mechnikov Research Institute of Vaccines and Sera, Moscow, Russia;
  • The National Medical Research Center for Hematology, Moscow, Russia;
  • The Federal Research Center of Fundamental and Translational Medicine, Novosibirsk, Russia;
  • The Kulakov National Medical Research Center for Obstetrics, Gynecology and Perinatology, Moscow, Russia;
  • The Tyumen Research Institute of Regional Infectious Pathology, Tyumen, Russia;
  • The Center of Hygiene and Epidemiology, Perm, Russia;
  • The Federal Research Center for Virology and Microbiology, Volginsky, Russia;
  • The Chumakov Federal Scientific Center for Research and Development of Immunobiological Products, Moscow, Russia;
  • Centre for Strategic Planning and Management of Biomedical Health Risks of the Federal Medical Agency, Moscow, Russia.

 

1. WHO. Tracking SARS-CoV-2 variants. 2021. URL: https://www.who.int/ru/activities/tracking-SARS-CoV-2-variants/tracking-SARS-CoV-2-variants

2. CDC. SARS-CoV-2 Variant Classifications and Definitions; 2022. URL: https://www.cdc.gov/coronavirus/2019-ncov/variants/variant-classifications.html

3. VGARus (Virus Genome Aggregator of Russia) Project. URL: https://genome.crie.ru/app/index

4. WHO. Weekly epidemiological update on COVID-19 – 22 March 2022. URL: https://www.who.int/publications/m/item/weeklyepidemiological-update-on-covid-19---22-march-2022

5. WHO. Classification of Omicron (B.1.1.529): SARS-CoV-2 Variant of Concern; 2021. URL: https://www.who.int/news/item/26-11-2021-classificationof-omicron-(b.1.1.529)-sars-cov-2-variant-of-concern

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About the authors

Vasily G. Akimkin

Central Research Institute for Epidemiology

Email: uglevas@bk.ru
ORCID iD: 0000-0003-4228-9044

D. Sci. (Med.), Prof., Full Member of RAS, Director

Россия, Moscow

Anna Yu. Popova

Federal Service for Supervision of Consumer Rights Protection and Human Welfare

Email: uglevas@bk.ru
ORCID iD: 0000-0002-4315-5307

D. Sci. (Med.), Professor, Head, Chief State Sanitary Doctor of the Russian Federation

Россия, Moscow

Kamil F. Khafizov

Central Research Institute for Epidemiology

Email: uglevas@bk.ru
ORCID iD: 0000-0001-5524-0296

PhD, Head, Genomic research laboratory

Россия, Moscow

Dmitry V. Dubodelov

Central Research Institute for Epidemiology

Email: uglevas@bk.ru
ORCID iD: 0000-0003-3093-5731

Cand. Sci. (Med.), senior researcher, Laboratory of viral hepatitis, Department of molecular diagnostics and epidemiology

Россия, Moscow

Svetlana V. Ugleva

Central Research Institute for Epidemiology

Author for correspondence.
Email: uglevas@bk.ru
ORCID iD: 0000-0002-1322-0155

D. Sci. (Med.), Assoc. Prof., consultant, Organizational and methodological department, Administrative division

Россия, Moscow

Tatyana A. Semenenko

National Research Center of Epidemiology and Microbiology named after Honorary Academician N.F. Gamaleya

Email: uglevas@bk.ru
ORCID iD: 0000-0002-6686-9011

D. Sci. (Med.), Professor, Head, Department of epidemiology

Россия, Moscow

Antonina A. Ploskireva

Central Research Institute for Epidemiology

Email: uglevas@bk.ru
ORCID iD: 0000-0002-3612-1889

Antonina A. Ploskireva — D. Sci. (Med.), Deputy director

Moscow

Россия, Moscow

Alexander V. Gorelov

Central Research Institute for Epidemiology

Email: uglevas@bk.ru

D. Sci. (Med.), Professor, RAS Corresponding Member, Deputy Director for Science

Россия, Moscow

Natalia Yu. Pshenichnaya

Central Research Institute for Epidemiology

Email: uglevas@bk.ru
ORCID iD: 0000-0003-2570-711X

D. Sci. (Med.), Deputy director

Россия, Moscow

Elena B. Yezhlova

Federal Service for Supervision of Consumer Rights Protection and Human Welfare

Email: uglevas@bk.ru
ORCID iD: 0000-0002-8701-280X

Cand. Sci. (Med.), Deputy Head

Россия, Moscow

Alexander N. Letyushev

Federal Service for Supervision of Consumer Rights Protection and Human Welfare

Email: uglevas@bk.ru
ORCID iD: 0000-0002-4185-9829

Cand. Sci. (Med.), Head, Department of scientific and analytical support and international activities

Россия, Moscow

Yulia V. Demina

Federal Service for Supervision of Consumer Rights Protection and Human Welfare

Email: uglevas@bk.ru
ORCID iD: 0000-0003-0538-1992

D. Sci. (Med.), Head, Department of epidemiological surveillance

Россия, Moscow

Vladimir V. Kutyrev

Russian Research Anti-Plague Institute "Microbe"

Email: uglevas@bk.ru
ORCID iD: 0000-0003-3788-3452

D. Sci. (Med.), Professor, RAS Full Member, Director

Россия, Saratov

Rinat A. Maksyutov

State Research Centre of Virology and Biotechnology “Vector”

Email: uglevas@bk.ru
ORCID iD: 0000-0003-1314-281X

D. Sci. (Biol.), Director

Россия, Koltsovo

Vadim M. Govorun

Institute of Disinfectology

Email: uglevas@bk.ru
ORCID iD: 0000-0003-0837-8764

D. Sci. (Biol.), Professor, RAS Full Member, Director

Россия, Moscow

Ivan A. Dyatlov

State Research Center for Applied Microbiology and Biotechnology

Email: uglevas@bk.ru
ORCID iD: 0000-0002-3436-0368

D. Sci. (Med.), Professor, RAS Full Member, Director

Россия, Obolensk

Areg A. Totolian

Pasteur St. Petersburg Research Institute of Epidemiology and Microbiology

Email: uglevas@bk.ru
ORCID iD: 0000-0003-4571-8799

D. Sci. (Med.), Professor, RAS Full Member, Head, Laboratory of molecular immunology, Director

Россия, St. Petersburg

Alexandr N. Kulichenko

Stavropol Research Anti-Plague Institute

Email: uglevas@bk.ru
ORCID iD: 0000-0002-9362-3949

D. Sci. (Med.), Professor, RAS Corresponding member, Director

Россия, Stavropol

Sergey V. Balakhonov

Irkutsk Research Anti-Plague Institute of Siberia and the Far East

Email: uglevas@bk.ru
ORCID iD: 0000-0003-4201-5828

Director

Россия, Irkutsk

Nikolay V. Rudakov

Omsk Research Institute of Natural Focal Infections

Email: uglevas@bk.ru
ORCID iD: 0000-0001-9566-9214

D. Sci. (Med.), Professor, Director

Россия, Omsk

Olga E. Trotsenko

Khabarovsk Research Institute of Epidemiology and Microbiology

Email: uglevas@bk.ru
ORCID iD: 0000-0003-3050-4472

D. Sci. (Med.), Director

Россия, Khabarovsk

Alexey K. Noskov

Rostov-on-Don Researsh Anti-Plague Institute

Email: uglevas@bk.ru
ORCID iD: 0000-0003-0550-2221

Cand. Sci. (Med), Director

Россия, Rostov-on-Don

Natalia N. Zaitseva

Nizhny Novgorod Research Institute of Epidemiology and Microbiology

Email: uglevas@bk.ru
ORCID iD: 0000-0001-5370-4026

D. Sci. (Med.), Director

Россия, Nizhny Novgorod

Andrey V. Toporkov

Volgograd Research Anti-Plague Institute

Email: uglevas@bk.ru
ORCID iD: 0000-0002-3449-4657

D. Sci. (Med.), Associate Professor, Direc

Россия, Volgograd

Dmitry A. Lioznov

Smorodintsev Research Institute of Influenza

Email: uglevas@bk.ru
ORCID iD: 0000-0003-3643-7354

D. Sci. (Med.), Director

Россия, St. Petersburg

Elena E. Andreeva

Federal Service for Supervision of Consumer Rights Protection and Human Welfare for the City of Moscow

Email: uglevas@bk.ru
ORCID iD: 0000-0001-6687-7276

Head

Россия, Moscow

Olga M. Mikailova

Federal Service for Supervision of Consumer Rights Protection and Human Welfare in the Moscow Region

Email: uglevas@bk.ru
ORCID iD: 0000-0003-3842-6368

Cand. Sci. (Med.), Chief State Sanitary Doctor in the Moscow Region, Head

Россия, Moscow

Andrey G. Komarov

Diagnostic Center (Center for Laboratory Research) of the Department of Health of the City of Moscow

Email: uglevas@bk.ru

Director

Россия, Moscow

Vasily Yu. Ananyev

Federal Center for Hygiene and Epidemiology

Email: uglevas@bk.ru
ORCID iD: 0000-0002-1670-6791

Cand. Sci. (Med.), Chief physician

Россия, Moscow

Vladimir V. Moldovanov

Center for Hygiene and Epidemiology in the City of Moscow

Email: uglevas@bk.ru
ORCID iD: 0000-0002-5606-4906

D. Sci. (Med.), chief physician

Россия, Moscow

Denis Yu. Logunov

National Research Center of Epidemiology and Microbiology named after Honorary Academician N.F. Gamaleya

Email: uglevas@bk.ru
ORCID iD: 0000-0003-4035-6581

D. Sci. (Biol.), Corresponding Member of RAS, Deputy Director for research

Россия, Moscow

Vladimir A. Gushchin

National Research Center of Epidemiology and Microbiology named after Honorary Academician N.F. Gamaleya

Email: uglevas@bk.ru
ORCID iD: 0000-0002-9397-3762

Cand. Sci. (Biol.), Head, Laboratory of mechanisms of population variability of pathogenic diseases

Россия, Moscow

Vladimir G. Dedkov

Pasteur St. Petersburg Research Institute of Epidemiology and Microbiology

Email: uglevas@bk.ru
ORCID iD: 0000-0002-5500-0169

Cand. Sci. (Med.), Deputy Director for science

Россия, St. Petersburg

Anna S. Cherkashina

Central Research Institute for Epidemiology

Email: uglevas@bk.ru
ORCID iD: 0000-0001-7970-7495

Cand. Sci. (Chem.), Head, Scientific group of genetic engineering and biotechnology, Department of molecular diagnostics and epidemiology

Россия, Moscow

Stanislav N. Kuzin

Central Research Institute for Epidemiology

Email: uglevas@bk.ru
ORCID iD: 0000-0002-0616-9777

D. Sci. (Med.), Professor, Laboratory of viral hepatitis, Department of molecular diagnostics and epidemiology

Россия, Moscow

Elena V. Tivanova

Central Research Institute for Epidemiology

Email: uglevas@bk.ru
ORCID iD: 0000-0003-1286-2612

Head, Directions of laboratory medicine and promotion of laboratory services, Department of molecular diagnostics and epidemiology

Россия, Moscow

Larisa Yu. Kondrasheva

Central Research Institute for Epidemiology

Email: uglevas@bk.ru
ORCID iD: 0000-0002-0147-4262

Head, Laboratory of polymerase chain reaction

Россия, Moscow

Valeria V. Saenko

Central Research Institute for Epidemiology

Email: uglevas@bk.ru
ORCID iD: 0000-0003-0952-0830

Head, Scientific group of genomic technologies

Россия, Moscow

Semyon Yu. Selezov

Central Research Institute for Epidemiology

Email: uglevas@bk.ru
ORCID iD: 0000-0001-9451-4341

bioinformatician, Laboratory of genomic research

Россия, Moscow

Gasan A. Gasanov

Central Research Institute for Epidemiology

Email: uglevas@bk.ru
ORCID iD: 0000-0002-0121-521X

post-graduate student

Россия, Moscow

Nino Kh. Svanadze

Central Research Institute for Epidemiology

Email: uglevas@bk.ru
ORCID iD: 0000-0001-7524-3080

Nino Kh. Svanadze — epidemiologist, Laboratory of viral hepatitis,
Department of molecular diagnostics and epidemiology 

Moscow

Россия, Moscow

Maxim B. Glazov

Central Research Institute for Epidemiology

Email: uglevas@bk.ru
ORCID iD: 0000-0002-2195-1580

Head, Center for the development of information technologies and systems

Россия, Moscow

Aleksey A. Ostroushko

Central Research Institute for Epidemiology

Email: uglevas@bk.ru
ORCID iD: 0000-0003-0803-5630

Head, Information and analytical service

Россия, Moscow

Konstantin O. Mironov

Central Research Institute for Epidemiology

Email: uglevas@bk.ru
ORCID iD: 0000-0001-8207-9215

D. Sci. (Med.), Head, Laboratory of molecular methods for genetic polymorphisms detection

Россия, Moscow

Anna S. Esman

Central Research Institute for Epidemiology

Email: uglevas@bk.ru
ORCID iD: 0000-0002-5456-7649

researcher, Laboratory of Molecular methods for genetic polymorphisms research

Россия, Moscow

Natalia A. Osina

Russian Research Anti-Plague Institute "Microbe"

Email: uglevas@bk.ru
ORCID iD: 0000-0003-0954-5683

Cand. Sci. (Biol.), Head, Laboratory of molecular diagnostics

Россия, Saratov

Sergei A. Bodnev

State Research Centre of Virology and Biotechnology “Vector”

Email: uglevas@bk.ru
ORCID iD: 0000-0003-0599-3817

Cand. Sci. (Med.), leading researcher

Россия, Koltsovo

Andrey B. Komissarov

Smorodintsev Research Institute of Influenza

Email: uglevas@bk.ru
ORCID iD: 0000-0003-1733-1255

Head, Laboratory of Molecular Virology

Россия, St. Petersburg

Daria М. Danilenko

Smorodintsev Research Institute of Influenza

Email: uglevas@bk.ru
ORCID iD: 0000-0001-6174-0836

Cand. Sci. (Biol.), Deputy Director for Science

Россия, St. Petersburg

Aleksandr G. Bogun

State Research Center for Applied Microbiology and Biotechnology

Email: uglevas@bk.ru
ORCID iD: 0000-0001-5454-2495

Cand. Sci. (Biol.), leading researcher, Department of Collection Cultures

Россия, Obolensk

Yuriy P. Skryabin

State Research Center for Applied Microbiology and Biotechnology

Email: uglevas@bk.ru
ORCID iD: 0000-0001-5748-995X

Cand. Sci. (Biol.), research scientist, Laboratory of antimicrobial agents

Россия, Obolensk

Kristina V. Lopatovskaya

Irkutsk Research Anti-Plague Institute of Siberia and the Far East

Email: uglevas@bk.ru
ORCID iD: 0000-0002-8772-5842

researcher, Laboratory of natural focal viral infections

Россия, Irkutsk

Sergey V. Shtrek

Omsk Research Institute of Natural Focal Infections

Email: uglevas@bk.ru
ORCID iD: 0000-0002-4509-1212

Cand. Sci. (Med.), senior researcher, Laboratory of Zoonotic Infections

Россия, Omsk

Anna S. Volynkina

Stavropol Research Anti-Plague Institute

Email: uglevas@bk.ru
ORCID iD: 0000-0001-5554-5882

Cand. Sci. (Biol.), Head, Laboratory for Diagnostics of Viral Infections

Россия, Stavropol

Anna S. Gladkikh

Pasteur St. Petersburg Research Institute of Epidemiology and Microbiology

Email: uglevas@bk.ru
ORCID iD: 0000-0001-6759-1907

Cand. Sci. (Biol.), senior researcher, Group of Molecular Genetics of Pathogenic Microorganisms, Department of Epidemiology

Россия, St. Petersburg

Valeria О. Kotova

Khabarovsk Research Institute of Epidemiology and Microbiology

Email: uglevas@bk.ru
ORCID iD: 0000-0001-9824-7025

senior researcher, Head, Laboratory of Epidemiology and Prevention of Viral Hepatitis and AIDS

Россия, Khabarovsk

Alexey S. Vodopyanov

Rostov-on-Don Researsh Anti-Plague Institute

Email: uglevas@bk.ru
ORCID iD: 0000-0002-9056-3231

Cand. Sci. (Med.), Deputy head, Group of virology

Россия, Rostov-on-Don

Nadezhda A. Novikova

Nizhny Novgorod Research Institute of Epidemiology and Microbiology

Email: uglevas@bk.ru
ORCID iD: 0000-0002-3710-6648

D. Sci. (Biol.), Professor, Head, Laboratory of Molecular Epidemiology of Viral Infections

Россия, Nizhny Novgorod

Anna S. Speranskaya

Institute of Disinfectology

Email: uglevas@bk.ru
ORCID iD: 0000-0001-6326-1249

Cand. Sci. (Biol.), senior researcher, Center for Genomics and Mass Spectrometry

Россия, Moscow

Andrey E. Samojlov

Institute of Disinfectology

Email: uglevas@bk.ru
ORCID iD: 0000-0001-8284-3164

Ph.D. (Biology), Senior Researcher Center for Genomics and Mass Spectrometry

Россия, Moscow

Alexey D. Neverov

Central Research Institute for Epidemiology

Email: uglevas@bk.ru
ORCID iD: 0000-0002-3594-1682

Cand. Sci. (Biol.), Head, Group of bioinformatics, Central Research Institute of Epidemiology

Россия, Moscow

Ivan M. Shpak

Volgograd Research Anti-Plague Institute

Email: uglevas@bk.ru
ORCID iD: 0000-0001-6446-0274

Ph.D. (Med.), researcher, Sector of bioinformatics analysis

Россия, Volgograd

References

  1. Акимкин В.Г., Кузин С.Н., Семененко Т.А., Плоскирева А.А., Дубоделов Д.В., Тиванова Е.В. и др. Характеристика эпидемиологической ситуации по COVID-19 в Российской Федерации в 2020 г. Вестник Российской академии медицинских наук. 2021; 76(4): 412-22. https://doi.org/10.15690/vramn1505
  2. Пшеничная Н.Ю., Лизинфельд И.А., Журавлев Г.Ю., Плоскирева А.А., Акимкин В.Г. Эпидемический процесс COVID-19 в Российской Федерации: промежуточные итоги. Сообщение 1. Инфекционные болезни. 2020; 18(3): 7-14. https://doi.org/10.20953/1729-9225-2020-3-7-14
  3. Пшеничная Н.Ю., Лизинфельд И.А., Журавлев Г.Ю., Плоскирева А.А., Еровиченков А.А., Акимкин В.Г. Эпидемический процесс COVID-19 в Российский Федерации: промежуточные итоги. Сообщение 2. Инфекционные болезни. 2021; 19(1): 10-5. https://doi.org/10.20953/1729-9225-2021-1-10-15
  4. Кутырев В.В., Попова А.Ю., Смоленский В.Ю., Ежлова Е.Б., Демина Ю.В., Сафронов В.А. и др. Эпидемиологические особенности новой коронавирусной инфекции (COVID-19). Сообщение 1: Модели реализации профилактических и противоэпидемических мероприятий. Проблемы особо опасных инфекций. 2020; (1): 6-13. https://doi.org/10.21055/0370-1069-2020-1-6-13
  5. Краснов Я.М., Попова А.Ю., Сафронов В.А., Федоров А.В., Баданин Д.В., Щербакова С.А. и др. Анализ геномного разнообразия SARS-CoV-2 и эпидемиологических признаков адаптации возбудителя COVID-19 к человеческой популяции (Сообщение 1). Проблемы особо опасных инфекций. 2020; (3): 70-82. https://doi.org/10.21055/0370-1069-2020-3-70-82
  6. Акимкин В.Г., Кузин С.Н., Семененко Т.А., Шипулина О.Ю., Яцышина С.Б., Тиванова Е.В. и др. Закономерности эпидемического распространения SARS-CoV-2 в условиях мегаполиса. Вопросы вирусологии. 2020; 65(4): 203-11. https://doi.org/10.36233/0507-4088-2020-65-4-203-211
  7. Акимкин В.Г., Кузин С.Н., Семененко Т.А., Плоскирева А.А., Дубоделов Д.В., Тиванова Е.В. и др. Гендерно-возрастная характеристика пациентов с COVID-19 на разных этапах эпидемии в Москве. Проблемы особо опасных инфекций. 2020; (3): 27-35. https://doi.org/10.21055/0370-1069-2020-3-27-35
  8. Щелканов М.Ю., Попова А.Ю., Дедков В.Г., Акимкин В.Г., Малеев В.В. История изучения и современная классификация коронавирусов (Nidovirales: Coronaviridae). Инфекция и иммунитет. 2020; 10(2): 221-46. https://doi.org/10.15789/2220-7619-HOI-1412
  9. Kaptelova V.V., Bukharina A.Y., Shipulina O.Y., Korneenko E.V., Saenko S.S., Lukyanov A.V., et al. Case report: change of dominant strain during dual SARS-CoV-2 infection. BMC Infect. Dis. 2021; 21(1): 959. https://doi.org/10.1186/s12879-021-06664-w
  10. Борисова Н.И., Котов И.А., Колесников А.А., КаптеловаВ.В., Сперанская А.С., Кондрашева Л.Ю. и др. Мониторинг распространения вариантов SARS-CoV-2 (Coronaviridae: Coronavirinae: Betacoronavirus; Sarbecovirus) на территории Московского региона с помощью таргетного высокопроизводительного секвенирования. Вопросы вирусологии. 2021; 66(4): 269-78. https://doi.org/10.36233/0507-4088-72
  11. Дубоделов Д.В., Савельер Е.В., Плоскирева А.А., Акимкин В.Г., Глазов М.Б., Гасанов Г.А. и др. Централизованная база данных для построения эпидемиологической аналитики по новой коронавирусной инфекции (COVID-19). Патент РФ № 2021622334; 2021.
  12. Дубоделов Д.В., Савельер Е.В., Плоскирева А.А., Акимкин В.Г., Глазов М.Б., Гасанов Г.А. и др. Эпидемиологическая аналитика по новой коронавирусной инфекции (COVID-19). Патент РФ № 2021667476; 2021.
  13. Попова А.Ю., ред. COVID-19: научно-практические аспекты борьбы с пандемией в Российской Федерации. Саратов: Амирит; 2021.
  14. Беляков В.Д. Внутренняя регуляция эпидемического процесса (ответы на замечания и вопросы, поднятые при обсуждении теории). Журнал микробиологии, эпидемиологии и иммунобиологии. 1987; 64(10): 78-89.
  15. Беляков В.Д., Голубев Д.Б., Каминский Г.Д., Тец В.В. Саморегуляция паразитарных систем. Ленинград: Медицина; 1987.

Supplementary files

Supplementary Files
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1. JATS XML
2. Fig. 1. Dynamics of genetic variants of SARS-CoV-2 and COVID-19 incidence rates (per 100,000 population) in Russia (2020–2022).

Download (543KB)
3. Fig. 2. The distribution of genetic variants in biomaterial specimens collected from 28/12/2020 to 26/6/2022.

Download (62KB)
4. Fig. 3. Subvariants of the Delta lineage (B.1.617.2+AY.*) isolated in Russia.

Download (91KB)
5. Fig. 4. Subvariants of the B.1.617.2. (Delta) lineage, except for basic variant B.1.617.2 and subvariants AY.122, AY.126, AY.121, AY.43 isolated in Russia.

Download (297KB)
6. Fig. 5. Dynamics of subvariants of the Delta lineage (B.1.617.2+AY.*), which were isolated in Russia, based on the data from the national VGARus database.

Download (302KB)
7. Fig. 6. Subvariants of the Omicron lineage (B.1.1.529+BA.*), which were isolated in Russia, based on the data from the national VGARus database as of 26/6/2022.

Download (53KB)
8. Fig. 7. Dynamics of subvariants of the Omicron lineage (B.1.1.529 + BA.*), which were isolated in Russia, based on the data from the national VGARus database.

Download (345KB)
9. Fig. 1. Dynamics of genetic variants of SARS-CoV-2 and COVID-19 incidence rates (per 100,000 population) in Russia (2020–2022).

Download (544KB)
10. Fig. 2. The distribution of genetic variants in biomaterial specimens collected from 28/12/2020 to 26/6/2022.

Download (74KB)
11. Fig. 3. Subvariants of the Delta lineage (B.1.617.2+AY.*) isolated in Russia.

Download (60KB)
12. Fig. 4. Subvariants of the B.1.617.2. (Delta) lineage, except for basic variant B.1.617.2 and subvariants AY.122, AY.126, AY.121, AY.43 isolated in Russia.

Download (297KB)
13. Fig. 5. Dynamics of subvariants of the Delta lineage (B.1.617.2+AY.*), which were isolated in Russia, based on the data from the national VGARus database.

Download (295KB)
14. Fig. 6. Subvariants of the Omicron lineage (B.1.1.529+BA.*), which were isolated in Russia, based on the data from the national VGARus database as of 26/6/2022.

Download (50KB)
15. Fig. 7. Dynamics of subvariants of the Omicron lineage (B.1.1.529 + BA.*), which were isolated in Russia, based on the data from the national VGARus database.

Download (303KB)

Copyright (c) 2022 Akimkin V.G., Popova A.Y., Khafizov K.F., Dubodelov D.V., Ugleva S.V., Semenenko T.A., Ploskireva A.A., Gorelov A.V., Pshenichnaya N.Y., Yezhlova E., Letyushev A.N., Demina Y.V., Kutyrev V.V., Maksyutov R.A., Govorun V.M., Dyatlov I.A., Totolian A.A., Kulichenko A.N., Balakhonov S.V., Rudakov N.V., Trotsenko O.E., Noskov A.K., Zaitseva N.N., Toporkov A.V., Lioznov D.A., Andreeva E.E., Mikailova O.M., Komarov A.G., Ananyev V.Y., Moldovanov V.V., Logunov D.Y., Gushchin V.A., Dedkov V.G., Cherkashina A.S., Kuzin S.N., Tivanova E.V., Kondrasheva L.Y., Saenko V.V., Selezov S.Y., Gasanov G.A., Svanadze N.K., Glazov M.B., Ostroushko A.A., Mironov K.O., Esman A.S., Osina N.A., Bodnev S.A., Komissarov A.B., Danilenko D.M., Bogun A.G., Skryabin Y.P., Lopatovskaya K.V., Shtrek S.V., Volynkina A.S., Gladkikh A.S., Kotova V.O., Vodopyanov A.S., Novikova N.A., Speranskaya A.S., Samojlov A.E., Neverov A.D., Shpak I.M.

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