A HERD IMMUNITY TO RUBELLA VIRUS IN SELECTED GEOGRAPHICAL REGIONS


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Abstract

Since 2017, the incidence rate of rubella in the Russian Federation has been below 1 case per million total population. In addition, no circulation of endemic strains of the rubella virus is recorded evidencing about achieving infection elimination phase. In modern conditions, it is important to constantly monitor the level of herd immunity to the rubella virus to identify epidemically significant population groups, especially in countries lacking rubella vaccination or featured with insufficient disease control. Purpose: to study herd immunity to the rubella virus in selected countries in Eurasia and Africa. Materials and methods. Between 2018 and 2021, 15,594 samples of blood sera were tested for IgG and IgM antibodies to the rubella virus from subjects of different ages obtained from regional measles and rubella surveillance centers in the Northwestern Federal District (NWFD) of the Russian Federation, the Republic of Serbia, South Vietnam, and the Republic of Guinea. The 'Anti-Rubella Virus ELISA (IgМ)' and 'Anti-Rubella Virus ELISA (IgG)' (Euroimmun, Germany) test kits were used. Statistical data processing was carried out using the MS Excel, Prizm 5.0 (GraphPad Software Inc.), and Statistica 8.0 (StatSoft Inc.) software package. Results. During the observation period (2018-2020) the population seroprevalence of the to the rubella virus in the NWFD of the Russian Federation was 96.6% - 97.7% and fluctuated slightly both in separate years and among individual age groups evidencing about high coverage of rubella vaccination. In the Republic of Serbia conducting two-fold immunization against rubella the overall seroprevalence rate was lower than in the Russian Federation and comprising 86.8%. The minimum number of IgG-positive sera was recorded in the 2–4-year-old age group pointing to the shortcomings of routine vaccination. In South Vietnam, children aged 1-3 years (41.9%) predominated among those recovering from rubella, i.e. the age cohort that should be protected by vaccination at the age of 18 months. No rubella vaccination is carried out in Guinea. The total proportion of seropositive individuals was 75%; herd immunity to the rubella virus was established mainly among children and adolescents, reaching 90% only in the older age group. 30% of unprotected subjects of the most active reproductive age were identified among the females surveyed in Guinea. Conclusion. Insufficient herd immunity to the rubella virus, identified in a number of countries, may contribute to the maintenance of the infectious process and the spread of infection. Globalization contributes to the virus importation into regions being at the stage of measles and rubella elimination. The results obtained suggest about a need to continue efforts aimed at maintaining epidemiological wellbeing regarding rubella in diverse countries of the world.

Full Text

Introduction. The Strategic Program for Measles and Congenital Rubella Prevention was developed by WHO in 2002, and in 2004 it also included the rubella elimination target. [18, 19].

Postnatal rubella is a mild infectious disease, predominantly of childhood, characterized by a maculopapular rash and an unexpressed syndrome of general intoxication. Congenital rubella infection is a severe systemic lesion of organs and tissues with intrauterine fetal damage in a pregnant woman sick with rubella.

In 1999, about 800,000 cases of rubella were reported in Europe, by 2008 their number dropped to 18,000. Such a significant decrease in the spread of infection in the region was primarily due to rubella vaccination campaigns in the Russian Federation and CIS countries [14]. However, against the background of a general reduction in incidence in 2009, there was a large outbreak in the Republic of Bosnia and Herzegovina (523 cases). A large number of rubella cases in 2015-2020 were reported in several countries in East, South-East and South Asia, as well as in the WHO African Region [1, 3, 4, 5, 16, 17, 21].

Rubella cases continued to decline in countries in the WHO European Region in 2020–2021. In 2020, 184 cases were detected in only 15 out of 53 states; the largest number of cases was registered in Poland, Ukraine, Germany, Turkey and Italy [15]. In 2021, 102 cases of rubella were registered in Europe, and 7136 cases of rubella in the world. It is likely that Covid-19 prevention and control measures taken in 2020-2021, and above all the complete or partial lockdown that took place in many countries, contributed to a further decrease in the number of reported rubella cases.

In the Russian Federation, an increase in the number of people vaccinated against rubella, both through routine immunization and the supplementary immunization campaign conducted in 2006-2007 as part of the national «Health» project, contributed to a sharp decrease in the incidence of this infection. As a result of the measures taken, the number of people vaccinated against rubella increased by more than 15 million people, which not only significantly reduced the incidence of rubella, but also prevented the occurrence of new cases of CRS [9, 14].

Since 2017, the rubella incidence rate in the Russian Federation has been below 1 case per 1’000’000 population. There was also no circulation of endemic strains of the rubella virus. All this testified to the achievement of the rubella elimination phase in Russia [14].

At the same time, during the Covid-19 pandemic, routine vaccination against a number of infections, including measles and rubella, could be disrupted due to the increased number of medical exemptions. In addition, there was an interruption or temporary suspension of epidemiological surveillance due to the diversion of medical staff and other resources to counter the Covid-19 pandemic. Achieving optimal coverage (≥95%) with two doses of measles and rubella-containing vaccine at all subnational levels (provinces, regions and districts), along with addressing gaps in population immunity, is considered as critical by experts from different countries and WHO experts [10, 15, 16, 19].

In modern conditions of globalization, it is important to constantly monitor the level of herd immunity to pathogens of certain infections, including the rubella virus, in order to identify epidemically significant population groups [7, 8, 12, 20]. It is especially important to organize such monitoring in countries where rubella vaccination is not conducted, or control by methods of specific prophylaxis is not sufficient. Such studies help limit the spread of rubella to WHO regions being at measles and rubella elimination stage.

The purpose of the study: to study herd immunity to the rubella virus in a number of countries in Eurasia and Africa.

MATERIALS AND METHODS

A total of 15594 blood serum samples from individuals aged 3 months to 82 years, obtained in the period from 2017 to 2021, were studied. The samples were provided by the virological laboratories of the regional measles and rubella surveillance centers in the Northwestern Federal District of the Russian Federation, in the Republic of Serbia, in South Vietnam, and in the Republic of Guinea.

15272 samples obtained from apparently healthy individuals of different ages were tested for IgG antibodies to the rubella virus. 322 samples obtained from patients of different ages with general infectious syndrome and maculopapular rash were tested for IgM antibodies to the rubella virus.

To determine IgM antibodies to the rubella virus, the Euroimmun Anti-Rubella Virus ELISA IgM diagnostic kit (Germany) was used; for the determination of IgG antibodies - diagnostic kits "Anti-Rubella Virus ELISA (IgG) Euroimmun (Germany), according to the manufacturer's instructions.

Statistical processing of the results was carried out using the MSExcel, Prizm 5.0 (GraphPad Software Inc.), Statistica 8.0 (StatSoftInc) software package. Parametric and nonparametric methods were in use. The probability value p<0.05 was determined as the threshold for the significance of differences [13].

RESULTS

The study of herd immunity to rubella virus within the framework of vaccine prevention of infection

          Among the regions included in the study, rubella vaccination is conducted in the Russian Federation, the Republic of Serbia, and the Socialist Republic of Vietnam [2, 6, 14]. In Russia and Serbia, routine vaccination includes two vaccinations: for children aged 12 months and six years old in the Russian Federation; children 15 months and 7 years old - in Serbia. Vaccination in both countries is carried out by combined vaccines, including measles and rubella components. In Viet Nam, the National Immunization Schedule includes one rubella vaccination for children aged 18 months.

In the NWFD of the Russian Federation in 2018-2020, the proportion of seropositive individuals out of 13,511 examined patients was 96.9% and fluctuated slightly over three years (Table 1).

Table 1

The intensity of immunity to the rubella virus in a cohort of the population in NWFD aged 3 to 49 years, divided into six age groups, was determined in total over three years of observation (Table 2). Among those surveyed aged 4 to 29, including four age groups, significant fluctuations in the proportion of persons immune to the rubella virus were not detected.

Table 2

The differences between the number of seropositive individuals under the age of 29 and those of older (30-49 years) age were statistically significant (p<0.05). The proportion of the protected from rubella in the older age group was considerably lower (95.27%) than among children and young adults (97.0% - 98.0%), as well as compared with the average seropositivity rate (96.9%).

In the Republic of Serbia 1400 blood sera of apparently healthy individuals aged 2 to 76 years, divided into four age groups, were examined for the presence of IgG antibodies to the rubella virus in the period 2018-2019 (Table 3).

Table 3

In the first group (2-4 years), the smallest number of IgG-positive sera (72.0%) was recorded in relation to the other three age groups (89.0%-90.0%). Differences are statistically significant (p<0.05). Among 8-14 year-old children, adolescents and 15-49 year-old adults, seroprevalence rate increased to 87.2% - 89.0% and reached its maximum (90.8%) in people aged 50 years and older.

When studying the intensity of immunity to the rubella virus (table 4), it was found that a low level of IgG-rubella antibodies (11.0-50.0 IU/ml) was generally determined in 41.8% of the examined, mainly in the age groups of 8- 14 (49%) and 15-25 (57.3%) year-old. Presumably, these are post-vaccination antibodies. High antibody titers (>150 IU/ml), indicating a recent illness, were detected in 18.9% of the examined, mainly among people over 50 years old.

Table 4

In the socialist Republic of Vietnam, rubella vaccination is also included in the National Calendar. As mentioned earlier, children at the age of 18 months should be vaccinated once.

In this study, 322 blood sera from the sera bank of the Virology Laboratory of the Measles and Rubella Surveillance Center in South Vietnam were used. Sera was received in 2020-2021 from patients with exanthemic manifestations of the infectious process aged from 3 months to 63 years and divided into 5 age groups. In accordance with the protocol adopted in the laboratory, the sera were tested only for IgM antibodies to rubella virus. The obtained results are presented in Table 5. In 9.7% of the studied sera, virus-specific IgM antibodies were detected. The cases of the disease were unevenly distributed between the groups, with a significant predominance of children aged 1-3 years (41.9%) and 7-14 years (22.6%) in the overall structure of cases.

Table 5

Children of preschool and primary school age (7-14 years old) form the second most important group. Among adolescents from 15 years old and adults, single cases of the disease were recorded.

Study of herd immunity to rubella virus in the absence of vaccination.

Among the countries included in the study, the Republic of Guinea is a region where routine rubella vaccination is not conducted, that is, herd immunity is formed in the conditions of the natural spread of the infection.

Herd immunity to the rubella virus was determined by the presence of IgG antibodies in the blood sera of apparently healthy residents of the capital of Guinea - Conakry in 2017-2018. The results are presented in table 6.

Table 6

 

The smallest amount of blood sera (n=42) was obtained from persons under 20 years of age due to the difficulty of obtaining clinical samples from apparently healthy children and adolescents in the GR.

In the first four age groups (up to 50 years of age), the proportion of seropositive patients did not differ significantly and ranged from 71.4% to 75.0%, rising to 95% only in the age group of 50 years and older. 

When determining seroprevalence among women (n=109), it turned out that in general the proportion of those seropositive to the rubella virus was 80.7%, which is somewhat higher than in the population as a whole, apparently due to closer contact with female children. The proportion of seropositive patients ranged from 70% (20-29 years old) to 86% (40-49 years old). It is important to emphasize that among the surveyed young women (20-29 years old), about a third were seronegative to the rubella virus.

DISCUSSION

Rubella is an infection controlled by means of specific prophylaxis.

The WHO proposal to include rubella in the measles elimination program is based on the fact that rubella is less contagious than measles; in most countries, combination vaccines are in use that include a rubella-containing component [16, 17, 18, 19]. Thus, the elimination of rubella can be achieved during the implementation of the measles elimination program. It should be taken into account that the rubella elimination strategy is based primarily on achieving and maintaining a high level (>95%) of routine vaccination coverage, which means, on creating strong herd immunity.

In the Russian Federation, during the observation period (2018-2020), seroprevalence among the NWFD population of  the rubella virus was 96.6% -97.7% and fluctuated slightly both in specific years and among specific age groups. However, the proportion of the protected from rubella in the older age group was significantly lower (95.27%) than among children and young adults (97.0% - 98.0%), as well as compared with the average seropositivity rate (96,9%). Perhaps these differences are due to the fact that within the framework of the National Project "Health" (2007), girls and women aged 15-17 and 18-25 were subject to revaccination against rubella; males were not immunized, which could affect the overall level of IgG-positive sera among older age groups. In general, the consistently high seroprevalence rates identified in this study in the Northwestern Federal District of the Russian Federation indicate a high vaccination coverage against rubella and the effectiveness of specific infection prevention, both being part of routine and additional immunization of the population.

In the Republic of Serbia, overall seroprevalence was significantly lower than in the Russian Federation and amounted to 86.8%. At the same time, the smallest number of IgG-positive sera (72.0%) was recorded in the first age group (2-4 years). Further, the proportion of seropositive persons consistently increased with age, reaching a maximum (90.8%) in persons aged 50 years and older. Such an age distribution of persons protected from infection is more typical for the formation of herd immunity in the conditions of the natural spread of rubella. The smallest proportion of young children (2-4 years) protected from infection indicates the disadvantages of rubella vaccination. This is confirmed by low intensity of immunity, mainly in the age groups of 8-14 (49%) and 15-25 (57.3%) years, that is, among people who should have received not only the first, but also the booster vaccination against rubella. The insufficient level of immunization coverage with the MMR vaccine, which includes the rubella component, was revealed by us earlier, when studying humoral immunity to the measles virus among the population of Serbia [2, 11].

A similar trend was found in South Vietnam when analyzing rubella cases that occurred in 2019-2020. Among those who recovered, children aged from 1 to 3 (41.9%) predominated, which represent the age cohort that should be protected by vaccination as much as possible. The second age group, where a large number of cases were observed, is represented by children of primary and secondary school age (22.6%).Thus, it can be assumed that herd immunity to rubella in Vietnam is most actively formed due to the involvement of children and adolescents in the infectious process. Consequently, routine rubella vaccination that children 18 months of age are subject to in Viet Nam does not provide adequate control of the infection.

In the Republic of Guinea, unlike the other regions included in this study, there is no specific prophylaxis for rubella. It was of undoubted interest to estimate the herd immunity formation in the population as a whole as well as in a socially significant group (women of reproductive age) under the conditions of natural spread of rubella.

The proportion of seropositive individuals both under 20 years and in the range from 20 to 49 years old was 73% and increased to 95% only in the age group of 50 and older. That is, herd immunity to the rubella virus in Guinea is formed mainly among children and adolescents and remains at the same level in the population. The exception is the elderly, where a higher proportion of seropositive individuals is apparently due to their closer contact with children in families. At the same time, 30% of unprotected people of the most active reproductive age were identified among the examined women, which indicates the potential for their becoming infected during pregnancy and the birth of children with congenital rubella infection. In general, under conditions of natural distribution, 75.2% of the examined persons had IgG antibodies to the rubella virus, which corresponds to the characteristics of the infection as a widespread disease with low contagiousness.

Conclusion

The study showed that vaccination has a significant impact on the formation of to the rubella virus. In the Russian Federation, where for a long period of time there has been a high coverage of the population with prophylactic rubella vaccinations, seroprevalence rates remain high, significantly exceeding 95% of persons protected from the infection in all surveyed age groups. This is illustrated by the example of such a large region as the Northwestern Federal District.

Indirectly, by identified cases of rubella infection, one can judge the insufficient coverage of routine rubella vaccination in South Vietnam. Infectious process in this region developed mainly among children who should have received a routine rubella vaccination according to the age.

In Serbia, where double rubella immunization is carried out, there seem to be shortcomings and failures of routine vaccination as well. This is evidenced by the lowest seroprevalence among other age groups, found in children between 2 and 4 years, who should be protected by rubella vaccination.

The smallest proportion of seropositive individuals was registered in Guinea, which is associated with the lack of specific rubella prophylaxis and its low contagiousness. Under these conditions, women of reproductive age represent the most vulnerable group of the population, among whom up to 30% of persons susceptible to infection with the rubella virus have been identified.

The insufficient level of herd immunity to rubella, identified in a number of regions included in this study, may contribute to the maintenance of the infectious process and the spread of infection, and conditions of globalization contribute to the virus importation into regions at the stage of measles and rubella elimination. This indicates the need for continued efforts for maintaining the epidemiological freedom from rubella in different countries of the world.

 

TABLES

 

Таблица 1. Выявление IgG-антител к вирусу краснухи  унаселения СЗФО в период с 2018 по 2020 гг.

Table 1. Detection of IgG antibodies to rubella virus in the population of the NWFD in the period from 2018 to 2020.

Годы

Years

Всего исследовано сывороток

Total sera tested

Изних IgG-краснуха +

Of them IgG-rubella +

абс. числа

abs. numbers

Доля (%) М±m

Share (%)М±m

2018

4989

4827

96,9±0,28

2019

4780

4639

97,05±0,24

2020

3772

3644

96,61±0,29

Всего

Total

13541

1310

96,9±0,15

 

Таблица 2. Выявление IgG-антител к вирусу краснухи в разных возрастных группах населения СЗФО (2018-2020 гг)

Table 2. Detection of IgG antibodies to rubella virus in different age groups of the NWFD population (2018-2020)

Возрастные группы (лет)

Age groups (years)

Всего исследовано сывороток

Total sera tested

Из них IgG-краснуха +

Of them IgG-rubella +

абс. числа

abs. numbers

Доля (%)М±m

Share (%)М±m

3-4

2632

2579

98,0±0,27

9-10

3133

3069

97,0±0,30

16-17

2859

2754

96,33±0,35

25-29

1957

1896

97,2±0,37

30-35

1745

1669

95,6±0,49

40-49

1191

1128

94,7±0,65

Всего

Total

13511

13094

96,9±0,15

 

Таблица 3. Выявление IgG-антител к вирусу краснухи  в разных возрастных группах населения Республики Сербия

Table 3. Detection of IgG antibodies to rubella virus in different age groups of the population of the Republic of Serbia

Возраст (лет)

Age (years)

Число обследованных лиц

Number of persons surveyed

Изних IgG-краснуха +

Of these IgG-rubella +

абс. числа

abs. numbers

Доля (%) М±m

Share (%)М±m

2-4

200

144

72,0±3,2

8-14

200

178

89,0±1,6

15-49

400

349

87,2±1,6

≥50

600

545

90,8±1,2

Всего

Total

1400

1216

86,8±0,9

 

Таблица 4. Напряженность гуморального иммунитета к вирусу краснухи у населения Сербии в разных возрастных группах

Table 4. Intensity of humoral immunity to rubella virus in the population of Serbia in different age groups.

Воз-

раст (лет)

Age (years)

Число обследованных лиц

Number of persons surveyed

Из них уровень IgG-краснуха (МЕ/мл)

Of these, the IgG level is rubella (IU/ml)

<11,0

11,0-50,0

>50,0-100,0

>100,0-150,0

>150,0

абс./%

abs./%

абс./%

abs./%

абс./%

abs./%

абс./%

abs./%

абс./%

abs./%

2-4

200

56/ 28,0

66 / 32,5

27 / 13,5

17 /8,5

35 / 17,5

8-14

200

22 / 11,0

98 / 49,0

40 / 20,0

18 / 9,0

22 / 11,0

15-25

200

30 / 4,9

115 / 57,3

12 / 5,0

15 / 7,5

29 / 14,4

≥50

400

81 / 20,2

140 / 35,0

44 / 11,0

32 / 8,0

103 / 25,7

Итого

Total

1000

189 / 18,9

418 / 41,8

123 / 12,3

82 / 8,2

189 / 18,9

 

Таблица 5. Распределение случаев кори в Южном Вьетнаме в зависимости от возраста

Table 5. Distribution of measles cases in South Vietnam by age

Возраст (лет)

Age (years)

Всего обследовано

Total examined

Изних IgM +

Of these IgM +

Доля заболевших в данной возрастной группе от общего числа

The proportion of cases in this age group of the total number

Абс.

Abs.

Доля (%)

Share (%)

Догода

Up to a year

165

4

2,4

12,9

1-3

74

13

17,6

41,9

4-6

15

2

13,3

6,5

7-14

38

8

18,4

22,6

15-29

10

3

30,0

9,7

30-39

7

1

14,3

3,2

40 и >

40 and >

12

3

8,1

3,2

Всего

Total

322

31

9,7

100

 

Таблица 6. Выявление IgG-антител к вирусу краснухи  в разных возрастных группах населения Гвинейской республики

Table 6. Detection of IgG antibodies to rubella virus in different age groups of the population of the Republic of Guinea

Возраст (лет)

Age (years)

Обследовано

(человек)

Examined (person)

IgG краснуха «+», абс.

IgGrubella «+», abs.

IgG краснуха «+» %М±m

IgG-rubella «+»,

%М±m

До 20

42

30

71,4±6,97

20 – 29

143

102

71,3±3,78

30 – 39

64

48

75,0±5,41

40 – 49

42

31

73,8±6,78

50 и старше

40

38

95,0±3,45

ИТОГО

TOTAL

331

249

75,2±2,37

 

×

About the authors

Irina Nikolaevna Lavrentieva

ФБУН «Санкт-Петербургский научно-исследовательский институт эпидемиологии и микробиологи имени Пастера»

Email: pasteur.lawr@mail.ru
ORCID iD: 0000-0002-2188-6547

д.м.н., зав. лабораторией экспериментальной вирусологии

197101, г. Санкт-Петербург, ул. Мира, дом 14

Maina Alexandrovna Bichurina

ФБУН «Санкт-Петербургский научно-исследовательский институт эпидемиологии и микробиологи имени Пастера»

Email: poliospb@nr3854.spb.edu
ORCID iD: 0000-0001-5184-0315

д.м.н., зав. вирусологической лабораторией центра по элиминации кори и краснухи

197101, г. Санкт-Петербург, ул. Мира, дом 14

Анастасия Юрьевна Антипова

ФБУН НИИЭМ имени Пастера

Email: anti130403@mail.ru
ORCID iD: 0000-0002-7763-535X

к.б.н. научный сотрудник лаборатории детских вирусных инфекций

Jacob Camara

Университет Гамаля Абдель Насера

Email: Jacob2240@gmail.com
ORCID iD: 0000-0003-4837-0206

researcher, laboratory of hemorrhagic hemorrhagic fevers

Minh Hoang

Pasteur Institute of Ho Chi Minh City

Email: hoangminh_bio@yahoo.com
ORCID iD: 0000-0002-3444-1360

Researcher, Department of microbiology and immunology

Maja Dragorad Bancevic

Institute for Virology, Vaccine and Sera «TORLAK»

Email: mbancevic@torlak.rs
ORCID iD: 0000-0003-2364-9980

MD, Specialist in Medical microbiology, Head of National Reference Laboratory for measles and rubella, Department of Serology and Molecular Diagnostics

Belgrade, Serbia

Nina Vsevolodovna Zheleznova

St-Petersburg Pasteur Institute

Email: nzhel@mail.ru
ORCID iD: 0000-0002-7072-1714

PhD, Leading Scientific Reseacher, Laboratory of Viral Hepatitis

Svetlana Alexandrovna Egorova

Saint Petersburg Pasteur Institute

Email: egorova72@mail.ru
ORCID iD: 0000-0002-7589-0234

D. Sc. (Medicine), Deputy Director for Innovation, Senior Researcher at the Laboratory of Intestinal Infections, bacteriologist of the highest qualification category

Areg Artyomovich Totolyan

Saint Petersburg Pasteur Institute

Author for correspondence.
Email: totolian@spbraaci.ru
ORCID iD: 0000-0003-4571-8799

D. Sc. (Medicine),  Chief, Director

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Copyright (c) Lavrentieva I.N., Bichurina M.A., Антипова А.Ю., Camara J., Hoang M., Bancevic M.D., Zheleznova N.V., Egorova S.A., Totolyan A.A.

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