Seriprevalense to SARS-CoV-2 in Tyumen Region

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392
ORIGINAL RESEARCHES
© Authors, 2020
Distribution of SARS-CоV-2 seroprevalence among residents
of the Tyumen Region during the COVID-19 epidemic period
Anna Yu. Popova 1, Elena B. Ezhlova 1, Albina A. Melnikova 1, Tatiana F. Stepanova 2,
Galina V. Sharukho 3, Aleksandr N. Letyushev 2,3, Aleksandr Ya. Folmer 4, Anna A. Shepotkova 2,
Lyudmila V. Lyalina 5, Vyacheslav S. Smirnov 5, Kseniya B. Stepanova 2, Tsakhik A. Panina 2,
Olga N. Sidorenko 2, Natalia A. Ivanova 2, Svetlana S. Smirnova 2, Inna N. Malchenko 2,
Elena V. Okhotnikova 2, Elena G. Stakhova 2, Areg A. Totolian 5
1Federal Service for Surveillance on Consumer Rights Protection and Human Wellbeing, 127994, Moscow, Russia;2Tyumen Region Infection Pathology Research Institute, 625026, Tyumen, Russia;3Department of the Federal Service for Surveillance on Consumer Rights Protection and Human Wellbeing
for Tyumen Region, 625026, Tyumen, Russia;
4Center for Hygiene and Epidemiology in the Tyumen Region, 625000, Tyumen, Russia;5Saint Petersburg Pasteur Institute, 197101, Saint Petersburg, Russia
Introduction. In late 2019 – early 2020, an outbreak of infection caused by a nove
l strain of beta coronavirus
SARS-CoV-2 was reported. The World Health Organization defined the disease as coronavirus disease 2019
(COVID-19). In the TXPHQ Region, the first case of COVID-19 was diagnosed on 31/1/2020. The source of
infection was a female student who came from Jinan, Shandong province (China). The number and rate of cases
were steadily increasing from the 16
th week through 28 th week in 2020. The highest rate was 36.87 cases per
100 thousand people. Afterwards, the cumulative incidence kept increasing gradually, but not as quickly.
The purpose of the seroepidemiological study was to measure the level and to identify the structure of herd
immunity against the SARS-CoV-2 virus among the population of the Tyumen Region during the rapid spread of
the COVID-19 outbreak.
Materials and methods. Volunteers for participation in the study were selected through questionnaire surveys
and random sampling. The exclusion criterion was an active COVID-19 infection at the time of
the survey. A total
of 2,758 individuals were tested for SARS-CoV-2 specific antibodies. The age of the surveHGYROXQWHHUVUDQJHG
from 1 HDUWRears and older.
Results of the study. During the active phase of the COVID-19 incidence, the population of the Tyumen Region
showed moderate (24.5%) seroprevalence of SARS-CoV-2. At the same time, the tests revealed a high (97.8%)
rate of asymptomatic infection cases in seropositive individuals who had never been diagnosed with COVID-19
and did not have history of positive PCR test results or acute respiratory infection symptoms on the day of testing.
The maximum level of herd immunitZDVLGHQWLHGLQFKLOGUHQDJHGears (34.7%), which was significantl
higher compared to the average level of seroprevalence in the entire cohort. In recovered COVID-19 patients,
antibodies were detected in 68.2%. In individuals with positive PCR test results, antibodies were detected in 64%.
Conclusion. The results of the assessment of the level of herd immunity against the SARS-CoV-2 virus are crucial
for prediction of the development trend of the epidemic and for planning specific and non-specific COVID-19
prevention measures.
Keywords: coronavirus; epidemic; seroprevalence; Tyumen Region; population.
Acknowledgments. The study had no sponsorship.
Conflict of interest. The authors declare no apparent or potential conflicts of interest related to the publication
of this article.
For citation: Popova A.Yu., Ezhlova E.B., Melnikova A.A., Stepanova T.F., Sharukho G.V., Letyushev A.N.,
Folmer A.Ya., Shepotkova A.A., Lyalina L.V., Smirnov V.S., Stepanova K.B., Panina Ts.A., Sidorenko O.N.,
Ivanova N.A., Smirnova S.S., Malchenko I.N., Okhotnikova E.V., Stakhova E.G., Totolian A.A. Distribution
of SARS-CоV-2 seroprevalence among residents of the TXPHQ5HJLRQGXULQJWKH&29,'HSLGHPLF
period. Journal of microbiology, epidemiology and immunobiology = Zhurnal mikrobiologii, èpidemiolog
ii i
immunobiologii. 2020; 97(5): 392–400.
DOI: https://doi.org/10.36233/0372-9311-2020-97-5-1
Received 23 September 2020
Аccepted 1 October 2020
JOURNAL OF MICROBIOLOGY, EPIDEMIOLOGY AND IMMUNOBIOLOGY. 2020; 97(5) DOI: https://doi.org/10.36233/0372-9311-2020-97-5-1
ORIGINAL RESEARCHES

393
ЖУРНАЛ МИКРОБИОЛОГИИ, ЭПИДЕМИОЛОГИИ И ИММУНОБИОЛОГИИ. 2020; 97(5)
DOI: https://doi.org/10.36233/0372-9311-2020-97-5-1
ОРИГИНАЛЬНЫЕ ИССЛЕДОВАНИЯ
Распределение серопревалентности к SARS-CоV-2
среди жителей Тюменской области в эпидемическом
периоде COVID-19
Попова А.Ю. 1, Ежлова Е.Б. 1, Мельникова А.А. 1, Степанова Т.Ф. 2, Шарухо Г.В. 3, Летюшев А.Н. 2,3,
Фольмер А.Я. 4, Шепоткова А.А. 2, Лялина Л.В. 5, Смирнов В.С. 5, Степанова К.Б. 2, Панина Ц.А. 2,
Сидоренко О.Н. 2, Иванова Н.А. 2, Смирнова С.С. 2, Мальченко И.Н. 2, Охотникова Е.В. 2,
Стахова Е.Г. 2, Тотолян А.А. 5
1Федеральная служба по надзору в сфере защиты прав потребителей и благополучия человека,
127994, Москва, Россия;
2ФБУН «Тюменский научно-исследовательский институт краевой инфекционной апатологии» Роспотребнадзора,
625026, Тюмень, Россия;
3Управление Федеральной службы по надзору в сфере защиты прав потребителей и благополучия человека
по Тюменской области, 625026, Тюмень, Россия;
4ФБУЗ «Центр гигиены и эпидемиологии в Тюменской области», 625000, Тюмень, Россия;5ФБУН «Санкт-Петербургский научно-исследовательский институт эпидемиологии и микробиологии им. Пастера»
Роспотребнадзора, 197101, Санкт-Петербург, Россия
Введение. В конце 2019 г. — начале 2020 г. была зарегистрирована вспышка инфекции, ua\ZggZyghым
штаммом бета-коронаbjmkZ6$56&R9<HAhij_^_ebeZb^_glbnbpbjh\Zggh_aZ[he_\Zgb_dZddhjh-
наbjmkgZy[he_agv &29,' <Lxf_gkdhch[eZklbi_jый случай заболевания COVID-19 был
диагностирован 31.01.2020 г. Источником инфекции была студентка, приехаrZybaPabgZgyijhинция
Шаньдун (КНР). С 16-й по 28-ю неделю 2020 г. наблюдался устойчиucjhklaZ[he_\Z_fhklbFZdkbfZev-
ный уровень состаbegZlukq_eh\_d<ihke_^klии кумулятиgZyaZ[he_\Z_fhklvihkl_i_g-
но увеличивалась, хотя и с меньшей интенсиghklvx.
Целью сероэпидемиологического исследования было определение уроgy и структуры популяционного
иммунитета к bjmkm SARS-CoV-2 среди населения Тюменской области  период интенсиgh]h распро-
странения COVID-19.
Материалы и методы. Отбор добровольце^eybkke_^h\Zgbyijh\h^bekyiml_fZgd_lbjh\ZgbybjZg-
домизации. Критерием неdexq_gbyy\eyeZkvZdlbная инфекция COVID-19 на момент обследования. На
наличие специфических антител к SARS-CoV-2 были обследованы 2758 человек. Возраст опрошенных
добровольцеkhklZ\eyehl]h^Z^he_lbklZjr_.
Результаты исследования. Среди населения Тюменской области  актиghc фазе заболеваемости
COVID-19 наблюдалась умеренная (24,5%) серопревалентность к SARS-CoV-2. Одноj_f_gghkwlbfы-
явлена ukhdZy  qZklhlZkemqZ_ бессимптомной инфекции у серопозитиguoex^_cmdhlhjuo
анамнезе не было заболевания COVID-19, положительного результата ПЦР и симптомо острых респи -
раторных bjmkguo инфекций  день обследования. Максимальные показатели коллектиgh]h иммуни-
тета, установленные у детей 1–6 лет (34,7%), были статистически значимыми по сраg_gbx со средним
уроg_fk_jhij_\Ze_glghklb^ey\k_cdh]hjluMj_dhg\Ze_kp_glh COVID-19 антитела обнаруживались
kemqZ_. У лиц с положительным результатом ранее проведенного ПЦР-анализа антитела uyy-
ляются kemqZ_.
Вывод. Результаты исследования состояния коллектиgh]hbffmgbl_lZdирусу SARS-CoV-2 необходимы
для разработки прогноза разblby эпидемиологической ситуации, а также для планирования мероприя-
тий по специфической и неспецифической профилактике COVID-19.
Ключеu_keh\Z: коронаbjmkwib^_fbyk_jhij_\Ze_glghklvLxf_gkdZyh[eZklvgZk_e_gb_.
Источник финансирования. Авторы заявляют об отсутстbbnbgZgkbjh\Zgbyijbijh\_^_gbbbkke_-
дования.
Конфликт интересо Авторы декларируют отсутстb_yных и потенциальных конфликтоbgl_j_-
соk\yaZgguokim[ebdZpb_cgZklhys_cklZlvb
Для цитирования: Попова А.Ю., Ежлова Е.Б., Мельникова А.А., Степанова Т.Ф., Шарухо Г.В., Летюш-
ев А.Н., Фольмер А.Я., Шепоткова А.А., Лялина Л.В., Смирно<KKl_iZgh\ZD;IZgbgZP:Kb^h -
ренко О.Н., Иванова Н.А., Смирнова С.С., Мальченко И.Н., Охотникова Е.В., Стахова Е.Г., Тотолян А.А.
Распределение серопревалентности к SARS-CоV-2 среди жителей Тюменской области wib^_fbq_kdhf
периоде COVID-19. Журнал микробиологии, эпидемиологии и иммунобиологии. 2020; 97(5): 392–400.
DOI: https://doi.org/10.36233/0372-9311-2020-97-5-1
Поступила 23.09.2020
Принята i_qZlv0

394
Introduction
The COVID-19 pandemic, which began on
11/2/2020, is an unprecedented event in the modern his-
tory of human civilization. Having started with a single
infected case at the seafood market in Wuhan (China),
the infection spread rapidly around the world, having
affected almost everUHJLRQRIWKHJOREH,WKDVVSDUHG
a few small countries in Africa so far. Besides, there
is no information about COVID-19 cases in Turkmen-
istan and North Korea. As of the first decade of Jul
2020, the global case tall hit 12.5 million confirmed
COVID-19 cases, out of which 6.89 million patients
had recovered and 560 thousand patients had died
1.
In Russia, according to official data from the Rus-
sian Federal Service for Surveillance on Consumer
Rights Protection and Human Wellbeing (Rospotreb-
nadzor), as of 12/7/2020, a total of 727,162 cases were
reported; the number of recovered patients was 561,061
and the number of the deceased was 11,335. Coronavirus
cases are recorded across the country. The highest inci-
dence is recorded in Moscow; the lowest number of cas-
es is recorded in the Chukotka District, Yamalo-Nenets
District and Arctic islands of the Russian Federation. In the Tumen Region, the first case was detected
on 31/1/2020; the source of infection was a female Chi-
nese citizen who came from Jinan, Shandong province.
Sporadic cases had been recorded till April 9, 2020.
The steady increase in the incidence started from the
16
th week in 2020; the peak was reached during the
28th week with 36.87 cases per 100 thousand people.
Afterwards, the cumulative incidence rose gradually to
demonstrate a 195% increase during the period from the 26
th to the 30 th week (Fig. 1).
Therefore, any an-
nouncement of the successful breakthrough in elimina -
tion of the COVID-19 outbreak in the Tyumen Region
would be premature. Both the current COVID-19 situation and the ur -
gent need for effective epidemic control measures bring
herd immunity assessment studies to the fore. The
herd immunity threshold can be reached in two ways:
through natural infection by increasing the number of
people who had the infectious disease, i.e. COVID-19,
in a symptomatic or asymptomatic form, or through
vaccination covering at least 60% of susceptible people
[1, 2]. No matter how fast scientists and manufacturers
are moving to create a vaccine, its development takes
time; its safety, specificitDQGH
vFDF require thorough
examination [3]. Then, the only realistic solution is to
rely on developing herd immunity resulting from ap-
parent symptomatic infection or inapparent seroconver -
sion. The common assumption is that at least 50–60%
of the vulnerable population must develop immunity to
a particular infection to stop the spread of infection [2].
Careful attention should be given to the dynamics of the
process and to the degree of population heterogeneity,
which can significantlD
uHFWWKHGHYHORSPHQWRIERWK
individual and community resistance to infection with
SARS-CoV-2 [4]. Considering the aforesaid, the purpose of the
conducted seroepidemiological study was to measure
the level and to identify the structure of herd immunity
against the SARS-CoV-2 virus among the population
of the Tyumen Region during the rapid spread of the
COVID-19 outbreak.
Fig. 1. COVID-19 incidence in Tyumen Region.
The arrows show the period when the seroprevalence study was conducted (
the 24 th–25 th week of the year).
1https://www.who.int/ru/emergencies/diseases/novel-coronavirus-2019
0 5
10
15
20 25 30
35 40 5
678910 111213141516171819202122232425262728
0,0 7
0 0
00 1
0
0,0 7 0
,0 7
0,0 7
0,4 6 2
,7 7 13,
24
9,5 5 10,
67
17,
84 22,
98
17, 58
14, 0318,
83 21,
223,
18 24,
14
35,
69 36,
87 In cidenc e per 100 thous and peopl e
Num ber o f week
JOURNAL OF MICROBIOLOGY, EPIDEMIOLOGY AND IMMUNOBIOLOGY. 2020; 97(5)
DOI: https://doi.org/10.36233/0372-9311-2020-97-5-1
ORIGINAL RESEARCHES

395
Materials and methods
The studZDVFRQGXFWHGGXULQJWKHUVWVWDJHRI
Rospotrebnadzor’s large-scale project aimed at assess-
ment of herd immunity to the SARS-CoV-2 virus in
the population of Russia, following the protocol rec-
ommended by the World Health Organization
[5] . The
study was approved by the research ethics committee
of the Pasteur Research Institute of Epidemiology and
Microbiology. Prior to the study, all the participants or
their legal representatives were informed about the pur -
pose and methods of the study; all of them signed the
informed consent. Volunteers for participation in the study were se-
lected through questionnaire surveVDQGUDQGRPVDm-
pling. The exclusion criterion was an active COVID-19
infection at the time of the survey. The sample size was
calculated by using the formula:
t2 × p(1 – p)
n = ,
m 2
where:
n — a sample size;
t — a precision level (for a 95% CI t = 1.96);
p — expected prevalence of the studied phenomenon
(at 50% p = 0.5);
m — a margin of error of 5% [6]. A total of 7,163 volunteers were surveyed; out of
them, 3,030 people had their venous blood samples col-
lected for further tests for SARS-CoV-2 specific anti -
bodies. A total of 2,758 samples had been tested. The age of the examined volunteers ranged from 1
to 70 years and older ( Table 1).
In all the age groups, the number of volunteers
was comparable, except for the significantl smaller
number of volunteers in the senior-age group. Tak- ing into account the specifics of child development,
the first group was divided into three subgroups:
1–6, 7–13 and 14–17 years. The individuals who had
COVID-19 in the past accounted for 0.7% (22 peo-
ple) of the total number of volunteers. On the testing
day, no volunteer had clinical symptoms of acute re-
spiratory infections.
Blood samples were collected in EDTA-contain -
ing vacutainer tubes and centrifuged. Plasma was sepa-
rated from cellular elements, collected in plastic tubes
and stored at 4°C till the commencement of the test. The
amount of antibodies to SARS-CoV-2 was measured
with an enzyme-linked immunosorbent assay (ELISA)
kit for human blood serum or plasma tests for detecting
SARS-CoV-2 nucleocapsid specific immunoglobulin G
(IgG) antibodies; the kit is made bWKH6WDWH5HVHDUFK
Center for Applied Microbiology and Biotechnology of
Rospotrebnadzor. The results were assessed by using
qualitative methods and were deemed positive when
the cut-off level was exceeded. The statistical processing included variation sta-
tistics methods, an Excel statistical package and Win-
Pepi software (version 11.65). Due to the absence of a
representative sample for districts of the Tyumen Re-
gion, most of the statistical indicators were calculated
by using the results obtained from the volunteers from
Tyumen. The probability value of p < 0.05 was used to
assess significant differences between variables.
Results
Assessment of seroprevalence
The seroprevalence among the residents of the
Tyumen Region totaled 24.5 ± 1.6% (677 out of 2,758);
in the age groups, it ranged from 13.4 ± 5.5% to
Table 1. Seroprevalence in residents of TXPHQ5HJLRQGLHUHQWDJHJURXSs
Age group, yearsNumber of the examined,
persons Including
Seroprevalence, %
(M ± m)
seropositive seronegative
1–17 35694262 26.4 ± 4.6
Including: 1–6 75264934.7 ± 10.8
7–13 1443311122.9 ± 6.9
14–17 13735102 25.5 ± 6.3
18–29 48512536025.8 ± 3.9
30–39 45211 933326.3 ± 4.1
40–49 44710833924.2 ± 4.0
50–59 48212635626.1 ± 3.9
60–69 38785302 22.0 ± 4.1
70 and older 14920129 13.4 ± 5.5
Total 27586772081 24.5 ± 1.6
ЖУРНАЛ МИКРОБИОЛОГИИ, ЭПИДЕМИОЛОГИИ И ИММУНОБИОЛОГИИ. 2020; 97(5)
DOI: https://doi.org/10.36233/0372-9311-2020-97-5-1
ОРИГИНАЛЬНЫЕ ИССЛЕДОВАНИЯ

396 26.4 ± 4.6% (Table 1). The maximum level of sero-
conversion was detected in the child-age group (mostly
in the subgroup of 1–6 years). The senior age group
(70 years and older) had the lowest level of seropreva-
lence (13.4 ± 5.5%), which can be explained by the in-
sufficient size of the sample. The seropositivitGLGQRW
show an significant gender differences and amounted
to 21.5 ± 2.7% in the males and 26.0 ± 2.0% (p > 0.05)
in the females, though the females demonstrated a clear
trend to seroconversion prevalence. The seroprevalence
level was 24.5 ± 1.6% in city of Tyumen, exclusive of
non-representative data from regional districts.
Assessment of risk factors
Among the participants who had symptomatic
COVID-19, the proportion of seropositive individuals
was 68.2 ± 19.5%, while among the participants who
had not been previously diagnosed with this infection,
the proportion was significantl lower — 24.2 ± 1.6%
(p < 0.05), and completely correlated with the results
obtained during the examination of residents from other
regions [5, 7]. In the group of individuals who had never been
exposed to COVID-19 patients, the proportion of sero-
positive people amounted to 21.1 ± 1.6%, while among
the individuals who had work or household contacts
with those who were diagnosed with COVID-19, the
proportion of volunteers with detected anti-SARS-
CoV-2 antibodies increased to 32.1 ± 7.2%. It suggests
the possibility of household development of an immune
response resulting from transmission of the pathogen
from a COVID-19 patient, though in small amounts.
The absence of significant differences, while the pro-
portion of seropositive people increased by 1.5 times, is
indicative of the insufficient size of the sample. The assessment of the seropositivity level among
volunteers who had positive PCR test results for virus
RNA is of particular interest. The test results showed
that among PCR positive individuals the seroprevalence
level was 64%, while among PCR-negative volunteers,
the seroprevalence level is 24.24%. The differences are
significant at probabilit of p < 0.05. The obtained re-
sults convincingly demonstrate the presence of a strong
functional relationship between the virus RNA circula-
tion and antibodies to the SARS-CoV-2 virus. The above
assumption was verified through the analVLVRIWKHUHOa-
tionship between incidence and seroprevalence (Fig. 2 ).
The conducted analysis shows that there is a direct
linear relationship between the variables. The Pearson
correlation coefficient and the Spearman rank correla -
tion coefficient amounted to 0.44 (p < 0.1). Although
the significance of the revealed relationship is not high,
it leads to the obvious conclusion implied by the direct
relationship between the variables: аn increase in the
incidence rate is accompanied by an increase in the se-
roprevalence ( Fig. 2).
Estimation of the proportion of asymptomatic cases The asymptomatic infection is typical of
COVID-19 and, as assumed, can act as significant fac-
tor of virus transmission [8]. From this perspective,
estimation of the percentage of asymptomatic cases in
the population is highly important for the analysis of in-
fection transmission among healthy individuals [9] and
can help significantl in adjusting the range and focus
of epidemic prevention measures [10]. The proportion of asymptomatic cases among se-
ropositive individuals was estimated through measur -
ing the proportion of individuals who did not have at
least one of the following: the COVID-19 diagnosis
Fig. 2. Correlation between the incidence rate and seroprevalence.
The vertical axis shows seroprevalence, %; the horizontal axis shows the incidence per 100 thousand people.
JOURNAL OF MICROBIOLOGY, EPIDEMIOLOGY AND IMMUNOBIOLOGY. 2020; 97(5)
DOI: https://doi.org/10.36233/0372-9311-2020-97-5-1
ORIGINAL RESEARCHES

397
or a positive PCR test result or acute respiratory infec
-
tion (ARI) symptoms. Among residents of the Tyumen
Region, the asymptomatic cases accounted for 97.8 ±
1.1%, reaching the highest levels in two age groups:
40–49 year-old and over 70 years old ( Table 2).
Thus, similar to other regions, the absolute number
of seropositive individuals demonstrates asymptomatic
infection. Keeping in mind that seropositivity is not
necessarily connected with the virus RNA circulation,
we can reasonably assume that asymptomatic infection
has more advantages than downsides, as it is highly
probable that the presence of antibodies to the SARS-
CoV-2 nucleocapsid protein can be connected with the
increased resistance to infection with a pathogenic vi-
rus and can contribute to reduction in the epidemic ten-
sion among people. The same tendency underlies the
relationship between the seroprevalence to the SARS-
CoV-2 virus and COVID-19 incidence ( Fig. 1).
Discussion
The examination of the population of the Tyu-
men Region represented mainly by Tyumen residents
showed that the seroprevalence level among the volun-
teers ranged from 13.4 ± 5.5 to 34.7 ± 10.8%. Similar to
other regions (St. Petersburg and Leningrad Region) [1,
2], the highest seroprevalence was detected among chil -
dren. At present, this phenomenon cannot be explained
adequatelDQGWRWKHIXOOHVW,WFDQEHDVVXPHGWKDWWKH
development of the landscape of antibodies to corona-
virus in children is affected b cross-reactive antibod -
ies resulting from acute respiratory infections caused
bRWKHUWpes of β-coronaviruses, which have common
determinants in nucleocapsid proteins [11]. The other
age groups did not show anVXEVWDQWLDOGL
uHUHQFHVLQ
seroprevalence levels. The fairly low proportion of indi-
viduals with SARS-CoV-2 antibodies in the senior-age
group can be explained by the small number of people
of this age in the group. The analysis of other parameters of seropreva-
lence did not reveal anXQXVXDOQGLQJV$V expected, the seroprevalence level was significantl higher
among people recovered after COVID-19, people
who had work or household contact with COVID-19
patients, and viral RNA carriers having positive PCR
test results.
As for asymptomatic cases, they demonstrate a
high level of seroprevalence. The phenomenon can be
caused by two factors: On the one hand, it is a typical
characteristic of SARS-CoV-2 [10, 11]; on the other
hand, it can be produced by inapparent seroconversion
when a humoral immune response can develop even
without manifest symptoms of the infection [5, 7].
Conclusions
1. The herd immunity of the total population of
the Tyumen Region was 24.5%. The highest level of
seroprevalence was found in individuals aged 1–6 years
(34.7%); the lowest level was identified in the group of
individuals aged 70 years and older (13.4%). 2. After the symptomatic COVID-19 infection,
antibodies are detected in 68% of the patients. 3. Antibodies were detected in 64% of individuals
with positive PCR test results. 4. The COVID-19 incidence rate has a strong rela -
tionship with SARS-CoV-2 seroprevalence. 5. The proportion of asymptomatic cases totaled
97.8% of the seropositive residents of the Tyumen Re-
gion.
Acknowledgements
The authors would like to express their gratitude
to G.V. Parfenova, A.Z. Umbitova, E.N. Dolgushina,
and A.S. Khismatullina, employees of the Tyumen Re-
search Institute of Regional Infectious Pathology; to
A.K. Kupina and I.V. Metafonova, employees of the
Neftyanik Health Facility; to A.E. Suvorova, an em-
ployee of Municipal Clinic No. 12; to A.N. Dimadieva,
N.A. Smagina and Yu.R. Dautova, employees of the
Tyumen Regional Infection Hospital, for their technical
support during the study.
Table 2. Proportion of asPSWRPDWLFFDVHVLQWKHWRWDOQXPEHURIVHURSRVLWLYHUHVLGHQWVRIGLHUHQWDJHJURXSVLQ TXPHQ
Region
Age group, years Total number

of seropositives Asymptomatic seropositives Proportion of asPSWRPDWLFFDVHV
(M ± m)
1–17 9493 98.9 ± 2.1
18–29 12511 9 95.2 ± 3.8
30–39 11 911 5 96.6 ± 3.3
40–49 108108 100.0 ± 1.9
50–59 126123 97.6 ± 2.7
60–69 8584 98.8 ± 2.3
70 and older 2020 100.0 ± 4.4
Total 677662 97.8 ± 1.1
ЖУРНАЛ МИКРОБИОЛОГИИ, ЭПИДЕМИОЛОГИИ И ИММУНОБИОЛОГИИ. 2020; 97(5)
DOI: https://doi.org/10.36233/0372-9311-2020-97-5-1
ОРИГИНАЛЬНЫЕ ИССЛЕДОВАНИЯ

398
JOURNAL OF MICROBIOLOGY, EPIDEMIOLOGY AND IMMUNOBIOLOGY. 2020; 97(5) DOI: https://doi.org/10.36233/0372-9311-2020-97-5-1
ORIGINAL RESEARCHES
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Information about the authors
Anna Yu. Popova — D. Sci. (Med.), Prof., Head, Federal Service for
Surveillance on Consumer Rights Protection and Human Wellbeing,
127994, Moscow, Russia.
ORCID ID: http://orcid.org/0000-0003-2567-9037.
Е-mail: depart@gsen.ru
Elena B. Ezhlova — Cand. Sci. (Med.), Deput+HDG)HGHUDO
Service for Surveillance on Consumer Rights Protection and Human
Wellbeing, 127994, Moscow, Russia.
E-mail: ezhlova_eb@gsen.ru
Albina A. Melnikova — Cand. Sci. (Med.), Deput+HDG
Epidemiological surveillance department, Federal Service for Информация об авторах
Попова Анна ЮрьеgZ
— д.м.н., проф., руководитель
Федеральной службы по надзору kn_j_aZsbluijZ
потребителей и благополучия человека, 127994, Москва,
Россия. ORCID ID: http://orcid.org/0000-0003-2567-9037.
Е-mail: depart@gsen.ru
Ежлова Елена БорисоgZ — к.м.н., зам. руководителя
Федеральной службы по надзору kn_j_aZsbluijZ
потребителей и благополучия человека, 127994, Москва,
Россия. Е-mail: ezhlova_eb@gsen.ru
Мельникова Альбина АндрееgZ — к.м.н., зам. начальника
Управления эпидемиологического надзора Федеральной

399
ЖУРНАЛ МИКРОБИОЛОГИИ, ЭПИДЕМИОЛОГИИ И ИММУНОБИОЛОГИИ. 2020; 97(5)
DOI: https://doi.org/10.36233/0372-9311-2020-97-5-1
ОРИГИНАЛЬНЫЕ ИССЛЕДОВАНИЯ
Surveillance on Consumer Rights Protection and Human Wellbeing,
127994, Moscow, Russia.
ORCID ID: http://orcid.org/0000-0002-5651-1331.
Е-mail: melnikova_aa@gsen.ru
Tatiana F. Stepanova — D. Sci (Med.), Prof., Director, TXPHQ
Region Infection Patholog5HVHDUFK,QVWLWXWH7umen,
Russia.
ORCID ID: https://orcid.org/0000-0002-6289-6274.
Е-mail: stepanovatf@tniikip.rospotrebnadzor.ru
Galina V. Sharukho — D. Sci (Med.), Head, Department of the
Federal Service for Surveillance on Consumer Rights Protection and
Human Wellbeing in the TXPHQ5HJLRQ7umen, Russia.
ORCID ID: https://orcid.org/0000-0003-0772-8224.
Е-mail: nadzor72@tXPHQVHUYLFHUu
Aleksandr N. Letyushev — Cand. Sci. (Med.), leading researcher,
TXPHQ5HJLRQ,QIHFWLRQ3DWKRORJ Research Institute, 625026,
Tyumen, Russia; Head, Epidemiological surveillance department,
Department of the Federal Service for Surveillance on Consumer
Rights Protection and Human Wellbeing in the Tyumen Region,
625026, TXPHQ5XVVLD.
ORCID ID: https://orcid.org/0000-0002-4185-9829.
Е-mail: nadzor72@tXPHQVHUYLFHUu
Aleksandr Ya. Folmer — Cand. Sci. (Med.), chief phVLFLDQ&HQWHU
for HJLHQHDQG(SLGHPLRORJ in the TXPHQ5HJLRQ
Tyumen, Russia.
ORCID ID: https://orcid.org/0000-0001-8321-5637.
Е-mail: tocgsen@fguz-tXPHQUu
Anna A. Shepotkova — medical statistician of the laboratorRI
epidemiological analysis and mathematical modeling, Tyumen
Region Infection Patholog5HVHDUFK,QVWLWXWH
Tyumen, Russia.
ORCID ID: https://orcid.org/0000-0002-1930-5635.
Е-mail: shepotkovaaa@tniikip.rospotrebnadzor.ru
Lyudmila V. Lyalina — D. Sci. (Med.), Prof., Head, Laborator
of epidemiology of infectious and non-infectious diseases,
Saint Petersburg Pasteur Institute, 197101, St. Petersburg, Russia.
ORCID ID: https://orcid.org/0000-0001-9921-3505.
Е-mail: lDOLQD#SDVWHXURUJUu
Vyacheslav S. Smirnov
— D. Sci. (Med.), Prof., leading researcher,
Saint Petersburg Pasteur Institute, 197101, St. Petersburg, Russia.
ORCID ID: https://orcid.org/0000-0002-2723-1496.
Е-mail: vssmi@mail.ru
Kseniya B. Stepanova — Cand. Sci. (Med.), leading researcher,
TXPHQ5HJLRQ,QIHFWLRQ3DWKRORJ Research Institute, 625026,
Tyumen, Russia.
ORCID ID: https://orcid.org/0000-0002-5420-0919.
Е-mail: stepanovakb@tniikip.rospotrebnadzor.ru
Tsakhik A. Panina — junior researcher, LaboratorRIFOLQLF
and immunology of biohelminthiasis, Tyumen Region Infection
Patholog5HVHDUFK,QVWLWXWH7umen, Russia.
ORCID ID: https://orcid.org/0000-0003-2490-4592.
E-mail: lifa@tniikip.rospotrebnadzor.ru
Olga N. Sidorenko — junior researcher, LaboratorRIFOLQLF
and immunology of biohelminthiasis, Tyumen Region Infection
Patholog5HVHDUFK,QVWLWXWH7umen, Russia.
ORCID ID: https://orcid.org/0000-0002-9032-1603.
E-mail: lifa@tniikip.rospotrebnadzor.ru
Natalia A. Ivanova — junior researcher, LaboratorRIFOLQLF
and immunology of biohelminthiasis, Tyumen Region Infection
Patholog5HVHDUFK,QVWLWXWH7umen, Russia.
ORCID ID: https://orcid.org/0000-0001-6964-0039.
E-mail: lifa@tniikip.rospotrebnadzor.ru
Svetlana S. Smirnova — junior researcher, LaboratorRIFOLQLF
and immunology of biohelminthiasis, Tyumen Region Infection
Patholog5HVHDUFK,QVWLWXWH7umen, Russia.
ORCID ID: https://orcid.org/0000-0002-2797-7570.
E-mail: lifa@tniikip.rospotrebnadzor.ru
Inna N. Malchenko — phVLFLDQ&OLQLFDOGHSDUWPHQW7umen
Region Infection Patholog5HVHDUFK,QVWLWXWH7umen,
Russia.
ORCID ID: https://orcid.org/0000-0003-2550-868X.
E-mail: info@tniikip.rospotrebnadzor.ru службы по надзору kn_j_aZsbluijZ потребителей и
благополучия человека, 127994, Москва, Россия.

ORCID ID: http://orcid.org/0000-0002-5651-1331.
Е-mail: melnikova_aa@gsen.ru
Степанова Татьяна ФедороgZ — д.м.н., проф., директор
ФБУН «Тюменский научно-исследовательский институт краевой
инфекционной патологии» Роспотребнадзора, 625026, Тюмень,
Россия.
ORCID ID: https://orcid.org/0000-0002-6289-6274.
Е-mail: stepanovatf@tniikip.rospotrebnadzor.ru
Шарухо Галина ВасильеgZ — д.м.н., рук. Управления
Федеральной службы по надзору kn_j_aZsbluijZ
потребителей и благополучия человека по Тюменской области,
625026, Тюмень, Россия.
ORCID ID: https://orcid.org/0000-0003-0772-8224.
Е-mail: nadzor72@tXPHQVHUYLFHUu
Летюше:e_dkZg^jGbdheZ_ич — к.м.н., gkN;MG
«Тюменский научно-исследовательский институт краевой
инфекционной патологии» Роспотребнадзора, 625026, Тюмень,
Россия; рук. отдела эпидемиологического надзора Управления
Федеральной службы по надзору kn_j_aZsbluijZ
потребителей и благополучия человека по Тюменской области,
625026, Тюмень, Россия.
ORCID ID: https://orcid.org/0000-0002-4185-9829.
Е-mail: nadzor72@tXPHQVHUYLFHUu
Фольмер Александр Яковлеbq — к.м.н., глаgucрач ФБУЗ
«Центр гигиены и эпидемиологии Lxf_gkdhch[eZklb
625000, Тюмень, Россия.
ORCID ID: https://orcid.org/0000-0001-8321-5637.
Е-mail: tocgsen@fguz-tXPHQUu
Шепоткова Анна АнатольеgZ — медстатистик лаб.
эпидемиологического анализа и математического
моделирования ФБУН «Тюменский научно-исследовательский
институт краевой инфекционной патологии» Роспотребнадзора,
625026, Тюмень, Россия;
ORCID ID: https://orcid.org/0000-0002-1930-5635.
Е-mail: shepotkovaaa@tniikip.rospotrebnadzor.ru
Лялина Людмила ВладимироgZ — д.м.н., проф., заeZ[
эпидемиологии инфекционных и неинфекционных заболеваний
ФБУН НИИ эпидемиологии и микробиологии им. Пастера,
197101, Санкт-Петербург, Россия.
ORCID ID: https://orcid.org/0000-0001-9921-3505.
Е-mail: lDOLQD#SDVWHXURUJUu
Смирно<yq_keZ Сергееbq
— д.м.н., проф., gkN;MG
НИИ эпидемиологии и микробиологии им. Пастера, 197101,
Санкт-Петербург, Россия.
ORCID ID: https://orcid.org/0000-0002-2723-1496.
Е-mail: vssmi@mail.ru
Степанова Ксения БорисоgZ — к.м.н., gkN;MGLxf_gkdbc
научно-исследовательский институт краевой инфекционной
патологии» Роспотребнадзора, 625026, Тюмень, Россия.
ORCID ID: https://orcid.org/0000-0002-5420-0919.
Е-mail: stepanovakb@tniikip.rospotrebnadzor.ru
Панина Цахик АрутоgZ — м.н.с. лаб. клиники и иммунологии
биогельминтозоN;MGLxf_gkdbcgZmqghbkke_^h\Zl_evkdbc
институт краевой инфекционной патологии» Роспотребнадзора,
625026, Тюмень, Россия.
ORCID ID: https://orcid.org/0000-0003-2490-4592.
E-mail: lifa@tniikip.rospotrebnadzor.ru
Сидоренко Ольга НиколаеgZ — м.н.с. лаб. клиники
и иммунологии биогельминтозоN;MGLxf_gkdbcgZmqgh-
исследовательский институт краевой инфекционной патологии»
Роспотребнадзора, 625026, Тюмень, Россия.
ORCID ID: https://orcid.org/0000-0002-9032-1603.
E-mail: lifa@tniikip.rospotrebnadzor.ru
Иванова Наталья АлександроgZ — м.н.с. лаб. клиники
и иммунологии биогельминтозоN;MGLxf_gkdbcgZmqgh-
исследовательский институт краевой инфекционной патологии»
Роспотребнадзора, 625026, Тюмень, Россия.
ORCID ID: https://orcid.org/0000-0001-6964-0039.
E-mail: lifa@tniikip.rospotrebnadzor.ru

400
Elena V. Okhotnikova — phVLFLDQ&OLQLFDOGHSDUWPHQW7umen
Region Infection Patholog5HVHDUFK,QVWLWXWH7umen,
Russia.
ORCID ID: https://orcid.org/0000-0001-8815-0916.
E-mail: info@tniikip.rospotrebnadzor.ru
Elena G. Stakhova — phVLFLDQ&OLQLFDOGHSDUWPHQW7umen
Region Infection Patholog5HVHDUFK,QVWLWXWH7umen,
Russia.
ORCID ID: https://orcid.org/0000-0003-4571-8799.
E-mail: info@tniikip.rospotrebnadzor.ru
Areg A. Totolian — D. Sci. (Med.), Prof., Academician of RAS,
Director, Saint Petersburg Pasteur Institute, 197101,
St. Petersburg, Russia.
ORCID ID: https://orcid.org/0000-0003-4571-8799.
Е-mail: pasteur@pasteurorg.ru
Contribution: the authors contributed equally to this article. Смирнова Светлана СергееgZ
— м.н.с. лаб. клиники
и иммунологии биогельминтозоN;MGLxf_gkdbcgZmqgh-
исследовательский институт краевой инфекционной патологии»
Роспотребнадзора, 625026, Тюмень, Россия.
ORCID ID: https://orcid.org/0000-0002-2797-7570.
E-mail: lifa@tniikip.rospotrebnadzor.ru
Мальченко Инна НиколаеgZ — jZqdebgbq_kdh]hhl^_e_gby
ФБУН «Тюменский научно-исследовательский институт краевой
инфекционной патологии» Роспотребнадзора, 625026, Тюмень,
Россия.
ORCID ID: https://orcid.org/0000-0003-2550-868X.
E-mail: info@tniikip.rospotrebnadzor.ru
Охотникова Елена ВладимироgZ — jZqdebgbq_kdh]h
отделения ФБУН «Тюменский научно-исследовательский
институт краевой инфекционной патологии» Роспотребнадзора,
625026, Тюмень, Россия.
ORCID ID: https://orcid.org/0000-0001-8815-0916.
E-mail: info@tniikip.rospotrebnadzor.ru
Стахова Елена ГеоргиеgZ — jZqdebgbq_kdh]hhl^_e_gby
ФБУН «Тюменский научно-исследовательский институт краевой
инфекционной патологии» Роспотребнадзора, 625026, Тюмень,
Россия.
ORCID ID: https://orcid.org/0000-0002-8436-2409.
E-mail: info@tniikip.rospotrebnadzor.ru
Тотолян Арег Артемоbq — д.м.н., проф., академик РАН,
директор ФБУН НИИ эпидемиологии и микробиологии
им. Пастера, 197101, Санкт-Петербург, Россия.
ORCID ID: https://orcid.org/0000-0003-4571-8799.
Е-mail: pasteur@pasteurorg.ru
Участие авторо: все авторы сделали экb\Ze_glgucклад 
подготоdmim[ebdZpbb.
JOURNAL OF MICROBIOLOGY, EPIDEMIOLOGY AND IMMUNOBIOLOGY. 2020; 97(5)
DOI: https://doi.org/10.36233/0372-9311-2020-97-5-1
ORIGINAL RESEARCHES
X