Epidemiology and Infectious Diseases » COVID-19 and the risk of herpesvirus reactivation

COVID-19 and the risk of herpesvirus reactivation

DOI: https://dx.doi.org/10.18565/epidem.2021.11.2.55-62

Solomay T.V., Semenenko T.A., Isaeva E.I., Vetrova E.N., Chernyshova A.I., Romenskaya E.V., Karazhas N.V.
1) Interregional Department One, Federal Biomedical Agency of Russia, Moscow, Russia; 2) I.I. Mechnikov Research Institute of Vaccines and Sera, Ministry of Education and Science of Russia, Moscow, Russia; 3) Honorary Academician N.F. Gamaleya National Research Center for Epidemiology and Microbiology, Ministry of Health of Russia, Moscow, Russia; 4) I.M. Sechenov First Moscow State Medical University (Sechenov University), Ministry of Health of Russia, Moscow, Russia; 5) N.N. Burdenko Main Military Clinical Hospital, Ministry of Defense of Russia, Khimki, Moscow Region, Russia

Objective. To study the features of the epidemic process of infections caused by herpes simplex virus types 1 and 2 (HSV-1, HSV-2), Epstein-Barr virus (EBV), cytomegalovirus (CMV), and human herpes virus type 6 (HHV6) during the COVID-19 pandemic.
Materials and methods. The incidence of COVID-19 and recorded herpesvirus infections was retrospectively analyzed. Ninety-two blood donors and 95 COVID-19 patients without respiratory failure were examined for herpes virus infection markers.
Results. There was an earlier and longer surge in the incidence of infectious mononucleosis in 2020 versus 2019; there were no significant differences between the groups of patients and donors in the detection rate of IgG to HSV-1 (88–91.6%), HSV-2 (20–20.7%), EBV (98.9–100%), CMV (82.1–83.7%), HHV6 (48.4–51.1%); low-avidity IgG to HSV (6.5–8.4%); EBV (2.2–6.3%) and CMV (0–1.1%); IgM to HSV-1 (0%), HSV-2 (0–1.1%,), CMV (0–2.2%), and HHV6 (5.4–8.4%). EBV reactivation markers (VCA IgM and EA IgG in the presence of VCA IgG and EBNA IgG) were significantly more frequently detected in patients (70.5% and 56.8%) than in donors (0 and 2.2%) (p < 0.05).
Conclusion. SARS-CoV-2 is a factor that triggers the mechanism of EBV transition from latency to lytic reproduction in the human body, whereas COVID-19 patients are at risk for reactivation of chronic EBV infection.

Keywords: SARS-CoV-2, COVID-19, Epstein–Barr virus, human herpes virus type 6, herpes viruses, reactivation, herpesvirus infection, herpes simplex virus, cytomegalovirus

Read entire article

Literature

1. Johnson R.W., Bouhassira D., Kassianos G., Leplège A., Schmader K.E., Weinke T. The impact of herpes zoster and post-herpetic neuralgia on quality-of-life. BMC Med. 2010; (8): 37. doi: 10.1186/1741-7015-8-37

2. Damm O., Witte J., Wetzka S., Prosser C., Braun S., Welte R., Greiner W. Epidemiology and economic burden of measles, mumps, pertussis, and varicella in Germany: a systematic review. Int. J. Public. Health 2016; 61(7): 847–60. doi: 10.1007/s00038-016-0842-8

3. Ablashi D., Agut H., Alvarez-Lafuente R., Clark D.A., Dewhurst S., DiLuca D. et al. Classification of HHV-6A and HHV-6B as distinct viruses. Arch. Virol. 2014; 159(5): 863–70. doi: 10.1007/s00705-013-1902-5

4. Мелехина Е.В., Лысенкова М.Ю., Свитич О.А., Музыка А.Д., Каражас Н.В., Рыбалкина Т.Н. и др. Особенности течения инфекции ВГЧ-6А и ВГЧ-6В у детей, проживающих в Московском регионе. Эпидемиол. инфекц. болезни. Актуал. вопр. 2018; (2): 42–9. doi: 10.18565/epidem.2018.2.42-9
Melehina E.V., Lysenkova M.Yu., Svitich O.A., Muzyka A.D., Karazhas N.V., Rybalkina T.N. et al. [Features of the course of HHV-6A and HHV-6B infection in children living in the Moscow Region]. Èpidemiologiâ i infekcionnye bolezni. Аktual’nye voprosy 2018; (2): 42–9. (In Russ.). doi: 10.18565/epidem.2018.2.42-9

5. Соломай Т.В., Семененко Т.А., Каражас Н.В., Рыбалкина Т.Н., Корниенко М.Н., Бошьян Р.Е. и др. Оценка риска инфицирования герпесвирусами при переливании донорской крови и ее компонентов. Анализ риска здоровью 2020; (2): 135–42 doi: 10.21668/health.risk/2020.2.15.eng
Solomay T.V., Semenenko T.A., Karazhas N.V., Rybalkina T.N., Kornienko M.N., Bosh’yan R.E. et al. [Assessing risks of infection with herpes viruses during transfusion of donor blood and its components]. Health Risk Analysis 2020; (2): 135–42. (In Russ.). doi: 10.21668/health.risk/2020.2.15.eng

6. Соломай Т.В., Семененко Т.А. Вирусные гепатиты В, С и инфекционный мононуклеоз: эпидемиологическое сходство и различия. Вопросы вирусологии 2020; 65(1): 27–34 doi: https://doi.org/10.36233/0507-4088-2020-65-1-27-34
Solomay T.V., Semenenko T.A. [Viral hepatitis B, C and infectious mononucleosis: epidemiological similarities and differences]. Voprosy virusologii 2020; 65(1): 27–34. (In Russ.). doi: 10.36233/0507-4088-2020-65-1-27-34 (in Russian)

7. Sharifipour S., Davoodi Rad K. Seroprevalence of Epstein–Barr virus among children and adults in Tehran, Iran. New Microbes New Infect. 2020; 34: 100641. doi: 10.1016/j.nmni.2019.100641

8. Cui J., Yan W., Xu S., Wang Q., Zhang W., Liu W., Ni A. Anti-Epstein–Barr virus antibodies in Beijing during 2013<2017: What we have found in the different patients. PLoS One 2018; 13(3): e0193171. doi: 10.1371/journal.pone.0193171

9. Beader N., Kolarić B., Slačanac D., Tabain I., Vilibić-Čavlek T. Seroepidemiological Study of Epstein–Barr Virus in Different Population Groups in Croatia. Isr. Med. Assoc. J. 2018; 20(2): 86–90.

10. Smatti M.K., Yassine H.M., Abu Odeh R., Al Marawani A., Taleb S.A., Althani A.A., Nasrallah G.K. Prevalence and molecular profiling of Epstein–Barr virus (EBV) among healthy blood donors from different nationalities in Qatar. PLoS One 2017; 12(12): e0189033. doi: 10.1371/journal.pone.0189033

11. Соломай Т.В., Семененко Т.А., Каражас Н.В., Рыбалкина Т.Н., Веселовский П.А., Пульнова Н.Л. и др. Особенности изменения показателей иммунного статуса лиц с активными и латентными формами герпесвирусных инфекций. Пермский медицинский журнал.2021; 38 (1): 46–63. doi: 10.17816/pmj38146%63
Solomay T.V., Semenenko T.A., Karazhas N.V., Rybalkina T.N., Veselovsky P.A., Pulnova N.L. et al. [Features of changes in the immune status of individuals with active and latent forms of herpesvirus infections]. Permskij medicinskij zhurnal.2021; 38 (1): 46–63. (In Russ.). doi: 10.17816/pmj38146%63

12. Wang F., Nie J., Wang H., Zhao Q., Xiong Y., Deng L. et al. Characteristics of Peripheral Lymphocyte Subset Alterationin COVID-19 Pneumonia. J. Infect. Dis. 2020; 221(11): 1762–9. doi: 10.1093/infdis/jiaa150

13. Matsubara H., Konishi T., Saito K., Naito A., Sugisawa J., Nakayama S. et al.. Zoster duplex in a patient with influenza a and bacterial superinfection. J. Dermatol. 2020; 47(1): e32–e33. doi: 10.1111/1346-8138.15099

14. Pereiro T., Lourido T., Ricoy J., Valdés L. Influenza Virus, Herpes Simplex Virus and Methicillin-Resistant Staphylococcus aureus in an Immunocompetent Patient. Arch. Bronconeumol. 2018; 54(3): 159–60. doi: 10.1016/j.arbres.2017.07.005

15. Li C., Li Y., Yang Y., Wang J., Zhu C., Tang S. et al. The Detection and Characterization of Simplex Virus Type 1 in Confirmed Cases. Sci. Rep. 2019; 9(1): 12785. doi: 10.1038/s41598-019-48994-5

16. Rathore S.K., Dwibedi B., Pati S.S., Panda S., Panda M., Sabat J., Kar S.K. An Investigation on the Coinfection Measles and HSV-1 in Hospitalized Acute Encephalitis Syndrome Patients in Eastern India. Neurol. India 2019; 67(5): 1358–9. doi: 10.4103/0028-3886.271247

17. Anaedobe C.G., Ajani T.A. Co Simplex Virus Type 2 and HIV Infections among Pregnant Women in Ibadan, Nigeria. J. Glob. Infect. Dis. 2019; 11(1): 19–24. doi: 10.4103/jgid.jgid_56_18

18. Ferreira A.C., Romão T.T., Macedo Y.S., Pupe C., Nascimento O.J.M.; Fellow of the American Academy of Neurology (FAAN). COVID-19 and Herpes zoster co-infection presenting with trigeminalneuropathy.Eur J Neurol.2020;27(9):1748-1750. doi: 10.1111/ene.14361.

19. Tartari F., Spadotto A., Zengarini C., Zanoni R., Guglielmo A., Adorno A. et al. Herpes zoster in COVID-19-positive patients. In. J. Dermatol. 2020; 59(8): 1028–9. doi: 10.1111/ijd.15001

20. Elsaie M.L., Youssef E.A., Nada H.A.. Herpes zoster might be an indicator for latent COVID-19 infection. Dermatol. Ther. 2020; 33(4): e13666. doi: 10.1111/dth.13666

21. Le Balc’h P., Pinceaux K., Pronier C., Seguin P., Tadié J.M., Reizine F. Herpes simplex virus and cytomegalovirus reactivations among severe COVID-19 patients. Crit. Care 2020; 24(1): 530. doi: 10.1186/s13054-020-03252-3

22. Sinadinos A., Shelswell J. Oral ulceration and blistering in patients with COVID-19. Evid. Based. Dent. 2020; 21(2): 49. doi: 10.1038/s41432-020-0100-z

23. Bond P. Ethnicity and the relationship between covid-19 and the herpes simplex viruses. Med. Hypotheses 2021; 146: 110447. doi: 10.1016/j.mehy.2020.110447

24. Amorim Dos Santos J., Normando A.G.C., Carvalho da Silva R.L., De Paula R.M., Cembranel A.C. et al. Oral mucosal lesions in a COVID-19 patient: New signs or secondary manifestations? Int. J. Infect. Dis. 2020; 97: 326–8. doi: 10.1016/j.ijid.2020.06.012

25. Xu R., Zhou Y., Cai L., Wang L., Han J., Yang X. et al. Co-reactivation of the human herpesvirus alpha subfamily (herpes simplex virus-1 and varicella zoster virus) in a critically ill patient with COVID-19. Br. J. Dermatol. 2020; 183(6): 1145–7. doi: 10.1111/bjd.19484

26. Cao X., Zhang X., Meng W., Zheng H. Herpes Zoster and Postherpetic Neuralgia in an Elderly Patient with Critical COVID-19: A Case Report. J. Pain. Res. 2020; 13: 2361–5. doi: 10.2147/JPR.S274199

27. Dursun R., Temiz S.A. The clinics of HHV-6 infection in COVID-19 pandemic: Pityriasisrosea and Kawasaki disease. Dermatol. Ther. 2020; 33(4): e13730. doi: 10.1111/dth.13730

28. Brambilla L., Maronese C.A., Tourlaki A., Veraldi S. Herpes zoster following COVID-19: a report of three cases. Eur. J. Dermatol. 2020; 30(6): 754–6. doi: 10.1684/ejd.2020.3924

29. Kadambari S., Klenerman P., Pollard A.J. Why the elderly appear to be more severely affected by COVID-19: The potential role of immunosenescence and CMV. Rev. Med. Virol. 2020; 30(5): e2144. doi: 10.1002/rmv.2144

30. Amaral P.H., Ferreira B.M., Roll S., Neves P.D., Pivetta L,G,, Mohrbacher S. et al. COVID-19 and Cytomegalovirus Co-infection: A Challenging Case of a Critically Ill Patient with Gastrointestinal Symptoms. Eur. J. Case Rep. Intern. Med. 2020; 7(10): 001911. doi: 10.12890/2020_001911

31. García-Martínez F.J., Moreno-Artero E., Jahnke S. SARS-CoV-2 and EBV. Med. Clin. (Engl). 2020; 155(7): 319–20. doi: 10.1016/j.medcle.2020.06.010

32. Соломай Т.В., Филатов Н.Н. Сезонность инфекции, вызванной вирусом Эпштейна–Барр. Журнал инфектологии 2020; 12(4): 93–100. doi: 10.22625/2072-6732-2020-12-4-93-100
Solomay T.V., Filatov N.N. [Seasonality of infection caused by the Epstein–Barr virus]. Zhurnal infektologii 2020; 12(4): 93–100. (In Russ.). doi: 10.22625/2072-6732-2020-12-4-93-100

33. Huang W., Berube J., McNamara M., Saksena S., Hartman M., Arshad T. et al. Lymphocyte subset counts in COVID-19 Patients: a meta-analysis. Cytometrya 2020; 97(8): 772–6. doi: 10.1002/cyto.a.24172

34. Mehta S.K., Bloom D.C., Plante I., Stowe R., Feiveson A.H., Renner A. et al. Reactivation of Latent Epstein-Barr Virus: A Comparison after Exposure to Gamma, Proton, Carbon, and Iron Radiation. Int. J. Mol. Sci. 2018;b19(10): pii: E2961. doi: 10.3390/ijms19102961

35. Баженова Л.Г., Ботвиньева И.А., Ренге Л.В., Полукаров А.Н. Динамика распространенности TORCH-инфекций у беременных. Оценка риска первичного инфицирования плода. Мать и дитя в Кузбассе 2012; (1): 22–6.
Bazhenova L.G., Botvinyeva I.A., Renge L.V., Polukarov A.N. [Dynamics of the prevalence of TORCH infections in pregnant women. Assessment of the risk of primary infection of the fetus]. Mat’ i ditya v Kuzbasse 2012; (1): 22–6. (In Russ.).

36. Островская О.В., Власова М.А., Наговицына Е.Б., Морозова О.И., Ивахнишина Н.М. Распространенность TORCH-инфекций у женщин Приамурья. Бюллетень физиологии и патологии дыхания 2008; 30: 72–7.
Ostrovskaya O.V., Vlasova M.A., Nagovitsyna E.B., Morozova O.I., Ivakhnishina N.M. [Prevalence of TORCH infections in women of the Amur Region]. Bulleten’ fiziologii i patologii dyhaniya 2008; 30: 72–7. (In Russ.).

37. Herrera-Ortiz A., Conde-Glez C.J., Vergara-Ortega D.N., García-Cisneros Olamendi-Portugal M.L., Sánchez-Alemán M.A. Avidity of antibodies against HSV-2 and risk to neonatal transmission among Mexican pregnant women. Infect. Dis. Obstet. Gynecol. 2013; 140–2. doi: 10.1155/2013/140142

38. Reward E.E., Muo S.O., Orabueze I.N.A., Ike A.C. Seroprevalence of herpes simplex virus types 1 and 2 in Nigeria: a systematic review and meta-analyses. Pathog. Glob. Health 2019; 113(5): 229–37. doi: 10.1080/20477724.2019.1678938

39. Dargham S.R., Nasrallah G.K., Al-Absi E.S., Mohammed L.I., Al-Disi R.S., Nofal M.Y., Abu-Raddad L.J. Herpes Simplex Virus Type 2 Seroprevalence Among Different National Populations of Middle East and North African Men. Sex. Transm. Dis. 2018; 45(7): 482–87. doi: 10.1097/OLQ.0000000000000791

40. Beader N., Kolarić B., Slačanac D., Tabain I., Vilibić-Čavlek T. Seroepidemiological Study of Epstein–Barr virus in Different Population Groups in Croatia. Isr. Med. Assoc. J. 2018; 20 (2): 86–90.

41. Fourcade G., Germi R., Guerber F., Lupo J., Baccard M., Seigneurin A. et al. Evolution of EBV seroprevalence and primary infection age in a French hospital and a city laboratory network, 2000–2016. PLoS One 2017; 12(4): e0175574. doi: 10.1371/journal.pone.0175574

42. Lachmann R., Loenenbach A., Waterboer T., Brenner N., Pawlita M., Michel A. et al. Cytomegalovirus (CMV) in the adult population of Germany. PLoS One 2018; 13(7): e0200267. doi: 10.1371/journal.pone.0200267

43. Cannon M.J., Schmid D.S., Hyde T.B.. Review of cytomegalovirus seroprevalence and demographic characteristics associated with infection. Rev. Med .Virol. 2010; 20(4): 202–13. doi: 10.1002/rmv.655

44. Aimola G., Beythien G., Aswad A., Kaufer B.B. Current understanding of herpesvirus 6 (HHV-6) chromosomal integration. Antiviral Res. 2020; 176: 104720. doi: 10.1016/j.antiviral.2020.104720

45. Drago F., Ciccarese G., Rebora A., Parodi A. Human herpesvirus-6, -7, and Epstein–Barr virus reactivation in pityriasisrosea during COVID-19. J. Med. Virol. 2021; 93(4): 1850–1. doi: 10.1002/jmv.26549

46. Paolucci S., Cassaniti I., Novazzi F., Fiorina L., Piralla A., Comolli G. et al. DNA increase in COVID-19 patients with impaired lymphocyte subpopulation count. Int. J. Infect. Dis. 2020; 104: 315–9. doi: 10.1016/j.ijid.2020.12.051

47. Ablashi D., Agut H., Alvarez-Lafuente R., Clark D.A., Dewhurst S., DiLuca D., Flamand L., Frenkel N., Gallo R., Gompels U.A. Classification of HHV-6A and HHV-6B as distinct viruses. Arch. Virol. 2014; 159(5): 863–70. DOI: 10.1007/s00705-013-1902-5

48. Мелехина Е.В., Лысенкова М.Ю., Свитич О.А., Музыка А.Д., Каражас Н.В., Рыбалкина Т.Н. и др. Особенности течения инфекции ВГЧ-6А и ВГЧ-6В у детей, проживающих в Московском регионе. Эпидемиол. инфекц. болезни. Актуал. вопр. 2018; (2): 42–9. DOI: 10.18565/epidem.2018.2.42-9
Melekhina E.V., Lysenkova M.Yu., Svitich O.A., Muzyka A.D., Karazhas N.V., Rybalkina T.N. et al. [Features of HHV-6A and HHV-6B infections in children living in the Moscow Region]. Èpidemiologiâ i infekcionnye bolezni. Аktual’nye voprosy 2018; (2): 42–9 (In Russ.). DOI: 10.18565/epidem.2018.2.42-9

About the Autors

Tatiana V. Solomay, Сand. Med. Sci., Deputy Head, Interregional Department №. 1 of the FMBA of Russia; Senior Researcher, Laboratory and Epidemiological Analysis and Monitoring of Infectious Diseases, I.I. Mechnikov Research Institute of Vaccines and Serums, Moscow, Russia; solomay@rambler.ru; https://orcid.org/0000-0002-7040-7653
Professor Tatiana A. Semenenko, MD, Head, Department of Epidemiology, Honorary Academician N.F. Gamaleya National Research Center for Epidemiology and Microbiology, Ministry of Health of Russia; Professor, Department of Infectology and Virology, I. M. Sechenov First Moscow State Medical University, Ministry of Health of the Russia (Sechenov University), Moscow, Russia; semenenko@gamaleya.org; https://orcid.org/0000-0002-6686-9011
Elena I. Isayeva, Cand. Biol. Sci., Leading Researcher, Laboratory of Immunology, D.I. Ivanovsky Research Institute of Virology, Honorary Academician N.F. Gamaleya National Research Center for Epidemiology and Microbiology, Ministry of Health of Russia, Moscow, Russia; immunol.lab@mail.ru; https://orcid.org/0000-0002-2523-0692
Elizaveta N. Vetrova, Researcher, Laboratory of Immunology, D. I. Ivanovsky Research Institute of Virology, Honorary Academician N.F. Gamaleya National Research Center for Epidemiology and Microbiology, Ministry of Health of Russia, Moscow, Russia; immunol.lab@mail.ru; https://orcid.org/0000-0003-1902-5278
Alyona I. Chernyshova, Junior Researcher, Laboratory of Immunology, D. I. Ivanovsky Research Institute of Virology, Honorary Academician N.F. Gamaleya National Research Center for Epidemiology and Microbiology, Ministry of Health of Russia, Moscow, Russia; immunol.lab@mail.ru; https://orcid.org/0000-0003-1290-4042
Elina V., Romenskaya, Epidemiologist, Branch № 8, N.N. Burdenko Main Military Clinical Hospital, Ministry of Defense of the Russia, Moscow Region, Khimki, Russia; elinaromenskaya@yandex.ru; https://orcid.org/0000-0001-8097-9412
Professor Nataliya V. Karazhas, BD, Head, Laboratory of Epidemiology of Opportunistic Infections, Honorary Academician N.F. Gamaleya National Research Center for Epidemiology and Microbiology, Ministry of Health of Russia, Moscow, Russia; karazhas@inbox.ru; https://orcid. org / 0000-0003-3840-963X

COVID-19 and the risk of herpesvirus reactivation

Literature

About the Autors

Similar Articles