Evaluation of age-related distribution of measles cases with primary and secondary immune response in Russian Federation, 2010-2016

Cover Page


Cite item

Full Text

Abstract

In 2010—2016, blood serum samples were examined from 5539 patients, aged < 1—60 years, with clinically and laboratory confirmed measles. Primary or secondary type of immune response was determined for all measles cases. Studies were performed with children aged < 1—14 years (2381), adolescents, 15—17 years old (189), and adults aged 18—60 years (2969). Serum measles-specific IgM antibodies were measured by “VektoKor’ IgM” ELISA test system (Russia), concentration and avidity of specific IgG — by using “Anti-Measles Viruses ELISA/IgG” and “Avidity: Anti-Measles Viruses ELISA/ IgG” (Euroimmun, Germany). Primary immune response was identified based on the presence of serum measles-specific low avidity IgM and IgG antibodies, whereas secondary immune response was characterized by detecting high avidity IgM and IgG antibodies at concentration of ≥ 5.0 IU/ml. Analyzing measles-specific IgM antibodies in 2010—2016 demonstrated that measles morbidity was mainly due to children, aged 1—2 years reaching up to 39.9% of the total number of children with measles aged < 1—14 years as well as adults aged 18—40 years old comprising as high as 80.1% total number of patients aged 15—60 years. Serum measles-specific IgG testing showed that in 15.0% of cases they were detected at concentration of ≥ 5.0 IU/ml. Further serum dilution resulted in finding IgG titer ranging within 8.5—45.0 IU/ml (21.4+0.36) and high avidity antibodies in 80—100% (92.5+0.2) cases. The remaining 85.0% cases found low avidity measles-specific IgG antibodies (< 30%) at concentration of 0.2—3.46 IU/ml (1.73+0.03). An age-related analysis of our data demonstrated that all children under 14 with laboratory-confirmed measles developed primary immune response. Moreover, in 73.7% of measles patients aged 15—60 with primary immune response measles might be prevented by timely vaccination, whereas persons with “vaccine failure” comprised 26.3%. In 2010 (0.09 per 100,000 subjects) and 2016 (0.12 per 100,000 subjects), frequency of patients with “vaccine failure” during relative epidemic well-being was 35.3% and 18.2%, respectively, exceeding 9.9% (p < 0.001) serving as a hallmark 2014 high measles incidence rate (3.24 per 100,000 subjects).The data obtained indicate that measles virus circulate among people with “vaccine failure,” which may account for potential to spread and infect unprotected population cohorts as well as cause measles outbreaks during periods of epidemic well-being.

About the authors

T. A. Mamaeva

Gabrichevsky Research Institute for Epidemiology and Microbiology

Author for correspondence.
Email: 4522826@bk.ru

Tamara A. Mamaeva - PhD (Biology), Leading Researcher, Laboratory of Immunochemistry.

125212, Moscow, Admiral Makarov str.,10, Phone: +7 (495) 452-28-26 (office); +7 903 558-10-70 (mobile)

Russian Federation

N. V. Zheleznova

St. Petersburg Pasteur Institute

Email: nzhel@mail.ru

PhD (Biology), Leading Researcher, Laboratory of Viral Hepatitis.

St. Petersburg

M. A. Bichurina

St. Petersburg Pasteur Institute

Email: nzhel@mail.ru

PhD, MD (Medicine), Head of the Virological Laboratory of Measles and Rubella Elimination.

St. Petersburg

M. A. Naumova

Gabrichevsky Research Institute for Epidemiology and Microbiology

Email: naumova@gabrich.ru

PhD (Medicine), Senior Researcher, Laboratory of Immunochemistry.

Moscow

M. V. Govoruhina

Center of Hygiene and Epidemiology in the Rostov Region

Email: virus@donses.ru

PhD (Medicine), Head of the Laboratory of Virology.

Rostov-on-Don

A. P. Toptygina

Gabrichevsky Research Institute for Epidemiology and Microbiology

Email: toptyginaanna@rambler.ru

PhD, MD (Medicine), Head of the Laboratory of Cytokine.

Moscow

References

  1. Ашмарин И.П., Воробьев А.А. Статистические методы в микробиологических исследованиях. М.: Медицина, 1962. 182 с.
  2. Мамаева Т.А., Железнова Н.В., Наумова М.А., Говорухина М.В., Калашникова Н.А, Бичурина М.А., Мукомолов С.Л. Алгоритм лабораторного подтверждения и дифференциальной диагностики коревой инфекции в период элиминации кори в Российской Федерации // Инфекция и иммунитет. 2015. Т. 5, № 1. С. 55-62. doi: 10.15789/2220-7619-2015-1-55-62 (In Russ.)
  3. Мамаева Т.А., Липская Г.Ю., Наумова М.А., Шульга С.В., Mulders M., Featherstone D.A., Завьялова Л.А., Чернышова Е.В., Замятина Е.П., Кузнецова Н.Н. Особенности лабораторной диагностики кори у больных с разным прививочным анамнезом // Вопросы вирусологии. 2012. № 5. С. 21-26.
  4. Мамаева Т.А, Наумова М.А., Железнова Н.В., Липская Г.Ю., Mulders M., Featherstone D.A. Оценка коммерческих тестсистем ИФА разного формата для определения уровня специфических IgM и IgG в сыворотках больных корью // Вопросы вирусологии. 2013. № 5. С. 43-48.
  5. Мамаева Т.А., Тихонова Н.Т., Наумова М.А., Шульга С.В. Национальная лабораторная сеть Российской Федерации по диагностике кори и ее роль в выполнении программы ВОЗ по ликвидации кори // Здоровье населения и среда обитания. 2007. № 11 (176). С. 4-7.
  6. Об обследовании больных с экзантемой и лихорадкой в рамках реализации Программы ликвидации кори. Приказ Роспотребнадзора № 33 от 05.02.2010. URL: http://docs.cntd.ru/document/902201050
  7. Онищенко Г.Г., Попова А.Ю., Алешкин В.А. Корь в России: проблемы ликвидации. М.: Династия, 2017. 552 с.
  8. СмердоваМ.А., Топтыгина А.П.,АндреевЮ.Ю.,СенниковС.В., ЗеткинА.Ю., КлыковаТ.Г.,БеляковС.И. Гуморальный и клеточный иммунитет к антигенам вируса кори и краснухи у здоровых людей // Инфекция и иммунитет. 2019. Т. 9, № 3-4. С. 607-611. doi: 10.15789/2220-7619-2019-3-4-607-611 (In Russ.)
  9. Тихонова Н.Т., Мамаева Т.А., Шульга С.В., Ежлова Е.Б., Лыткина И.Н., Цвиркун О.В., Герасимова А.Г. Лабораторное обеспечение Программы ликвидации эндемичной кори в Российской Федерации // Эпидемиология и вакцинопрофилактика. 2011. № 1. С. 36-39.
  10. Топтыгина А.П., Мамаева Т.А., Алешкин В.А. Особенности специфического гуморального иммунного ответа против вируса кори // Инфекция и иммунитет. 2013. № 3. С. 243-250. doi: 10.15789/2220-7619-2013-3-243-250(In Russ.)
  11. Топтыгина А.П., Смердова М.А, Наумова М.А, Владимирова Н.П, Мамаева Т.А. Влияние особенностей популяционного иммунитета на структуру заболеваемости корью и краснухой // Инфекция и иммунитет. 2018. Т. 8, № 3. С. 341-348. doi: 10.15789/2220-7619-2018-3-341-348(In Russ.)
  12. Цвиркун О.В., Герасимова А.Г., Тихонова Н.Т., Ежлова Е.Б., Мельникова А.А., Дубовицкая Е.Л., Орлова О.С., Басов А.А., Фролов Р.А. Заболеваемость корью в разных возрастных группах в период элиминации инфекции // Эпидемиология и вакцинопрофилактика. 2017. № 3 (94). С. 18—25.
  13. Atrasheuskaya A.V., Kulak M.V., Neverov A.A., Rubin S.A., Ignatyev G.M. Measles cases in highly vaccinated population of Novosibirsk, Russia, 2000—2005. Vaccine, 2008, vol. 26, pp. 2111—2118. doi: 10.1016/j.vaccine.2008.02.028
  14. Breackwell L., Moturi E., Helgenberger L., Gopalani S.V., Hales G., Lam E., Sharapov U., Larzeller M., Johnson E., Masao C., Setik E., Barrow L., Dolan S., Chen T.H., Patel M., Rota P., Hickman C., Bellini W., Seward J., Wallace G., Papania M. Measles outbreak assocated with vaccine failure in adults — Federated States of Micronesia February-August 2014. Morb. Mortal. Wkly Rep, 2015, vol. 64, pp. 1088-1092.
  15. Chen R.T., Markowitz L.E., Albrect P., Stewart J.A., Mofenson L.M., Preblud S.R., Orenstein W.A. Measles antibody: reevaluation of protective titers. J. Infect. Dis., 1990, vol. 162 (5), pp. 1036-1042. doi: 10.1093/infdis/162.5.1036
  16. Cherry J.D., Zahn M. Clinical characteristics of measles in previously vaccinated and unvaccinated patients in California. Clin. Infect. Dis, 2018, vol. 67, pp. 1315-1319. doi: 10.1093/cid/ciy286
  17. Christenson B., Botting M. Measles antibody: comparison of long-term vaccination titres, early vaccination titres and naturally acquired immunity to and booster effects on the measles virus. Vaccine, 1994, vol. 12, no. 2, pp. 129-133. doi: 10.1016/0264-410X(94)90049-3
  18. Davidkin I., Jokinen S, Broman M., Leinkki P., Peltola H. Persistence of measles, mumps, and rubella antibodies in an MMR-vaccinated cogort: a 20-years follow-up. J. Infect. Dis., 2008, vol. 197(7), pp. 950-956. doi: 10.1086/528993
  19. De Vries R.D., de Swart R.L., Lamouille B., Astier A., Rabourdin-Combe C. Measles immune suppression: functional impairment or numbers game? PLoS Pathog., 2014, vol. 10, no. 12: e1004482. doi: 10.1371/journal.ppat.1004482
  20. Durrhem D.N. Measles virus is unforgiving where immunity gaps exist. J. Infect. Dis., 2017, vol. 216 (10), pp. 1183-1184. doi: 10.1093/infdis/jix452
  21. Durrhem D.N., Crowcroft N.S. The price of delaying measles eradication. The Lancet Public Health, 2017, vol. 2(3), pp. e130-e131. doi: 10.1016/S2468-2667(17)30026-9
  22. Eaton L. Measles cases in England and Wales rise sharply in 2008. BMJ, 2009, vol. 338, p. b533.
  23. Enders J.F., Peebles T.C. Propagation in tissue cultures of cytopathogenic agents from patients with measles. Proc. Soc. Exp. Biol. Med, 1954, vol. 86, no. 2, pp. 277-286. doi: 10.3181/00379727-86-21073
  24. Funk S., Knapp J.K., Lebo E., Reef S.E., Dabbagh A., Kretsinger K., Jit M., Edmunds W.J., Strebel P.M. Combining serological and contact data to derive target immunity levels for achieving and maintaining measles elimination. BMC Med., 2019, vol. 17, no. 1:180. doi: 10.1186/s12916-019-1413-7
  25. Griffin D.E. The immune response in measles: virus control, clearance and protective immunity. Viruses, 2016, vol. 8, no. 10:282. doi: 10.3390/V8100282
  26. Griffin D.E., Lin W.H., Pan C.H. Measles virus, immune control and persistence. FEMS Microbiol. Rev., 2012, vol. 36, no. 3, pp. 649-662. doi: 10.1111/j.1574-6976.2012.00330.x
  27. Hahne S.J.M., Nic Lochlainn L.M,. van Bugel N.D. Measles outbreak among previously immunized helthcae works, The Netherlands, 2014. J. Infect. Dis., 2016, vol. 214, no. 12, pp. 1980-1986. doi: 10.1093/infdis/jiw480
  28. Hickman C.J., Hyde T.B., Sovers S.B., Mercader S., McGrew M., Williams N.J., Beeler J.A., Audet S., Kiehl B., Nandy R., Tamin A., Bellini W.J. Laboratory characterization of measles virus infection in previously vaccinated and unvaccinated individuals. J. Infect. Dis., 2011, vol. 204, no. 1, pp. 549-558. doi: 10.1093/infdis/jir106
  29. Hubschen J.M., Bork S.M., Brown K.E., Mankertz A., Santibanez S., Ben Mamou M., Mulders M.N., Muller C.P. Challenges of measles and rubella laboratory diagnostic in the era of elimination. Clin. Microbiol. Infect., 2017, vol. 23, no. 8, pp. 511-515. doi: 10.1016/j.cmi.2017.04.009
  30. Huiss S., Damien B. Schneider F., Muller C.P. Characteristics of asymptomatic secondary immune responces to MeV in late convalescent donors. Clin. Exp. Immunol., 1997, vol. 109, no. 3, pp. 416-420. doi: 10.1046/j1365-2249.1997.00137.x
  31. Javelle E., Colson P., Parola P., Raoult D. Measles, the need for a paradigm shift. Eur. J. Epidemiol., 2019, vol. 34, no. 10, pp. 897915. doi: 10.1007/S10654-019-00569-4
  32. Komabayashi K., Seto J., Tanaka S., Suzuki Yu., Ikeda T., Onuki N., Yamada K., Ahiko T., Ishikawa H., Mizuta K. The largest measles outbreak, including 38 modified measles and 22 typical measles cases in its elimination Era in Yamagata, Japan. 2017. Jpn. J. Infect. Dis, 2018, vol. 71,pp. 413-418. doi: 10.7883/yoken.JJID.2018.083
  33. Manual for the laboratory diagnosis of measles and rubella virus infection; 2nd ed. Geneva, Switzerland: WHO, 2006.
  34. Manual for the laboratory-based surveillance of measles, rubella, and congenital rubella syndrome; 3rd ed. Geneva, Switzerland: WHO, 2018.
  35. Measles in Europe: record number of both sick and immunized. WHO Europe, Copenhagen, 7 February 2019. URL: https://www.euro.who.int/en/media-centre/sections/press-releases/2019/measles-in-europe-record-number-of-both-sick-and-immunized
  36. McKee A., Ferrari M.J., Shea K. Correlation between measles vaccine doses: implications for the maintenance of elimination. Epidemiol. Infect, 2018, vol. 146, pp. 468-475. doi: 10.1017/S950268817003077
  37. Mercades S., Garcia P., Bellini W.J. Measles virus IgG avidity assay for use in classification of measles vaccine failure in measles elimination setting. Clin. Vaccine Immunol, 2012, vol. 19, no. 11, pp. 1810-1817. doi: 10.1128/CVI.00406-12
  38. Mina M.J. Measles, immune suppression and vaccination: direct and indirect nonspecific vaccine benefits. J. Infect., 2017, vol. 74, pp. 10-17. doi: 10.1016/S0163-4453(17)30185-8
  39. Mina M.J., Metcalf C.J.E., de Swart R.L., Osterhaus A.D.M.E., Grenfell B.T. Long-term measles-induced immunomodulation increases overall childhood infectious disease mortality. Science, 2015, vol. 348, no. 6235, pp. 694-699. doi: 10.1126/science.aaa3662. Epub 2015 8 may
  40. Mitchell P., Turner N., Jennings L., Dong H. Previous vaccination modifies both the clinical disease and immunological features in children with measles. J. Prim. Health Care, 2013, vol. 5 (2), pp. 93—98.
  41. Parent du Chatelet I., Floret D., Antona D., Levy-Bruhl D. Measles resurgence in France in 2008, a preliminary report. Euro Surveill., 2009, vol. 14:19118.
  42. Patel M.K., Orenstein W.A. Classification of global measles cases in 2013—2017 as due to policy or vaccination failure:a retrospective rewiev of global surveilence data. Lancet Glob. Health, 2019, vol. 7, pp. e313-e320. doi: 10.1016/S2214-109X(18)30492-3
  43. Paunio M., Hedman K., Davidkin I., Peltola H. IgG avidity to distinguish secondary from primary measles vaccination failures: prospects for a more effective global measles elimination strategy. Expert Opin. Phamacother., 2003, vol. 4 (8), pp. 1215—1225. doi: 10.1517/14656566.4.8.1215
  44. Paunio M., Hedman K., Davidkin I., Valle M., Heinonen O.P., Leinikiki P., Salmi A., Peltola H. Secondary measles vaccine failures identified by measurement of IgG avidity: high occurrence among teenagers vaccinated at a young age. Epidemiol. Infect., 2000, vol. 124, pp. 263-271. doi: 10.1517/S0950268899003222
  45. Ramssay M., Brown K. The public health implication of secondary measles vaccine failure. J. Prim. Health Care, 2013, vol. 5 (2), pp. 92-94. doi: 10.1071/HC13092
  46. Ratnam S., Tipples G., Head C., Fauvel M., Fearon M., Ward B.J. Perfomance of indirect immunoglobulin M (IgM) serology test and IgM capture assays for laboratory diagnosis of measles. J. Clin. Mic., 2000, no. 38, pp. 99-104.
  47. Rosen J.B., Rota J.S., Hickman C.J., Sovers S.B., Mercader S., Rota P.A., Bellini W.J., Huang A.J., Doll M.K., Zucker J.R., Zimmerman C.M. Outbreak of measles among persons with prior evidence of ummunity, New York City, 2011. Clin. Infect. Dis., 2014, vol. 58 (9), pp. 1205-1210. doi: 10.1093/cid/ciu105
  48. Rota J.S., Hickman C.J, Sovers S.B., Rota P.A., Mercader S., Bellini W.J. Two case studies of modified measles in vaccinated physicians exposed to primary measles case: high risk of infection but low risk of transmission. J. Infect. Dis., 2011, vol. 204 (1), pp. 5559-5563.
  49. Rota P.A., Moss W.J., Takeda M, de Swart R.L., Thompson K.M., Goodson J.L. Measles. Nat. Rev. Dis. Primers, 2016, no. 2: 16049. doi: 10.1038/nrdp.2016.49
  50. Sovers S.B., Rota J.S., Hickman C.J., Mercader S., Redd S., McNall R.J., Williams N., McGrew M., Walls M.L., Rota P.A., Bellini W.J. High concentration of measles neutralizing antibodies and high-avidity measles IgG accurately identify measles reinfection cases. Clin. Vaccine Immunol., 2016, vol. 23, no. 8, pp. 707- 716. doi: 10.1128/CVI.00268-16
  51. Sugerman D.E., Barskey A.E., Delea M.G., Ortega-Sanchez I.R., Bi D., Ralston K.G., Rota P.A., Waters-Montijo K., Lebaron C.W. Measles outbreak in a highly vaccinated population, San Diego, 2008: role internationally under vaccinated. Pediatrics, 2010, vol. 125, pp. 747-755.
  52. Tahara M.,Burchert J.-P., Maena K., Muller C.P., Taceda M. Measles virus hemagglutinin protein epitopes: the basis of antigenic stability. Viruses, 2016, vol. 8:216. doi: 10.3390/V8080216
  53. Vaccine Preventable Diseases Surveillance Standards, 2018. URL: http://www.who.int/immunization/monitoring_surveillance/bur-den/vpd/standards/en
  54. Yang L., Grenfell B.T., Mina M.J. Measles vaccine immune escape: should we be concerned? Eur. J. Epidemiol., 2019, vol. 34, pp. 893-896. doi: 10.1007/s10654-019-00574-7
  55. Zhang Z., Chen M., Ma R., Pan J., Suo L., Lu L. Outbreak ofmeasles among persons with secondary vaccine failure, China, 2018. Hum. Vaccin. Immunother., 2020, vol. 16, no. 2, pp. 358-362. doi: 10.1080/21645515.2019.1653742

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

Copyright (c) 2020 Mamaeva T.A., Zheleznova N.V., Bichurina M.A., Naumova M.A., Govoruhina M.V., Toptygina A.P.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.
СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: серия ПИ № ФС 77 - 64788 от 02.02.2016.


This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies