The role of papillomavirus and herpesvirus infections in the origins and genesis of genital endometriosis. A literature review

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Abstract

Endometriosis is a chronic multifactorial disease that affects one in ten women of reproductive age. Genetic, endocrine and immunological factors play an important role in the pathogenesis of endometriosis. In recent years, an increasing number of studies have been devoted to the role of vaginal microbiota in the pathogenesis of endometriosis. However, the role of viral infections, such as papillomavirus and herpesvirus infections, in the development of the disease has not been sufficiently studied. The review highlights current ideas about the role of human papillomavirus and herpesvirus infections in the genesis of endometriosis. The data obtained have convinced us of the need to further search for new relationships between papillomavirus and herpesvirus infections, microbiota of reproductive organs and pathogenesis of such a complicated disease as endometriosis.

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About the authors

Aigul M. Khanova

The Research Institute of Obstetrics, Gynecology and Reproductology named after D.O. Ott

Author for correspondence.
Email: musannifovna@gmail.com
ORCID iD: 0000-0002-6438-5195
Russian Federation, Saint Petersburg

Armine R. Khachaturian

The Research Institute of Obstetrics, Gynecology and Reproductology named after D.O. Ott

Email: armine2709@mail.ru
ORCID iD: 0000-0003-2141-6307
SPIN-code: 2691-3910

MD, Cand. Sci. (Med.)

Saint Barthélemy, Saint Petersburg

Tatiana A. Khusnutdinova

The Research Institute of Obstetrics, Gynecology and Reproductology named after D.O. Ott

Email: husnutdinovat@yandex.ru
ORCID iD: 0000-0002-2742-2655
SPIN-code: 9533-9754

MD, Cand. Sci. (Med.)

Russian Federation, Saint Petersburg

Alevtina M. Savicheva

The Research Institute of Obstetrics, Gynecology and Reproductology named after D.O. Ott

Email: savitcheva@mail.ru
ORCID iD: 0000-0003-3870-5930
SPIN-code: 8007-2630

MD, Dr. Sci. (Med.), Professor, Honored Worker of Science of the Russian Federation

Russian Federation, Saint Petersburg

Maria I. Yarmolinskaya

The Research Institute of Obstetrics, Gynecology and Reproductology named after D.O. Ott

Email: m.yarmolinskaya@gmail.com
ORCID iD: 0000-0002-6551-4147
SPIN-code: 3686-3605

MD, Dr. Sci. (Med.), Professor of the Russian Academy of Sciences

Russian Federation, Saint Petersburg

References

  1. Yarmolinskaya MI, Aylamazyan EK. Genital’nyi ehndometrioz. Razlichnye grani problemy. Saint Petersburg: Eco-Vector; 2017. (In Russ.)
  2. Bulun SE, Yilmaz BD, Sison C, et al. Endometriosis. Endocr Rev. 2019;40(4):1048–1079. doi: 10.1210/er.2018-00242
  3. Becker CM, Bokor A, Heikinheimo O, et al. ESHRE guideline: endometriosis. Hum Reprod Open. 2022;2022(2). doi: 10.1093/hropen/hoac009
  4. Gheit T. Mucosal and cutaneous human papillomavirus infections and cancer biology. Front Oncol. 2019;9:355. doi: 10.3389/fonc.2019.00355
  5. Robadi IA, Pharaon M, Ducatman BS. The importance of high-risk human papillomavirus types other than 16 and 18 in cervical neoplasia. Arch Pathol Lab Med. 2018;142(6):693–695. doi: 10.5858/arpa.2017-0563-RA
  6. Zarochentseva NV, Krasnopolsky V., Belaya YuM. Рrogress in vaccination of HPV-associated diseases and cervical cancer in the world and in Russia. Literature review. Colposcopy Issues and Genital Infections. 2022;(1):8–16. (In Russ.) doi: 10.46393/27826392_2022_1_8
  7. Jeršovienė V, Gudlevičienė Ž, Rimienė J, et al. Human papillomavirus and infertility. Medicina (Kaunas). 2019;55(7):377. doi: 10.3390/medicina55070377
  8. Capra G, Schillaci R, Bosco L, et al. HPV infection in semen: results from a new molecular approach. Epidemiol Infect. 2019;147. doi: 10.1017/S0950268819000621
  9. Isaguliants M, Krasnyak S, Smirnova O, et al. Genetic instability and anti-HPV immune response as drivers of infertility associated with HPV infection. Infect Agent Cancer. 2021;16(1):29. doi: 10.1186/s13027-021-00368-1
  10. Zacharis K, Messini CI, Anifandis G, et al. Human Papilloma Virus (HPV) and fertilization: a mini review. Medicina (Kaunas). 2018;54(4):50. doi: 10.3390/medicina54040050
  11. Henneberg AA, Patton WC, Jacobson JD, et al. Human papilloma virus DNA exposure and embryo survival is stage-specific. J Assist Reprod Genet. 2006;23(6):255–259. doi: 10.1007/s10815-006-9030-8
  12. Hong LJ, Oshiro BT, Chan PJ. HPV-16 exposed mouse embryos: a potential model for pregnancy wastage. Arch Gynecol Obstet. 2013;287(6):1093–1097. doi: 10.1007/s00404-013-2711-5
  13. Gomez LM, Ma Y, Ho C, et al. Placental infection with human papillomavirus is associated with spontaneous preterm delivery. Hum Reprod. 2008;23(3):709–715. doi: 10.1093/humrep/dem404
  14. Hermonat PL, Han L, Wendel PJ, et al. Human papillomavirus is more prevalent in first trimester spontaneously aborted products of conception compared to elective specimens. Virus Genes. 1997;14(1):13–17. doi: 10.1023/a:1007975005433
  15. Niyibizi J, Zanré N, Mayrand MH, et al. Association between maternal human papillomavirus infection and adverse pregnancy outcomes: systematic review and meta-analysis. J Infect Dis. 2020;221(12):1925–1937. doi: 10.1093/infdis/jiaa054
  16. Dassi L, Annunziata C, Botti C, et al. Detection of human papillomaviruses in the nasopharynx of breastfed infants: new findings and meta-analysis. Viruses. 2020;12(10):1119. doi: 10.3390/v12101119
  17. Prilepskaya VN, Dovlethanova ER. Papillomavirusnaya infektsiya: teoreticheskie I prakticheskie aspekty. Moscow: GEOTAR-Media; 2018. (In Russ.)
  18. Kiselev VI, Ashrafyan LA, Budarina CO, et al. Ehtiologicheskaya rol’ virusa papillomy cheloveka v razvitii raka sheiki matki: gene ticheskie i patogeneticheskie mekhanizmy, vozmozhnosti terapii i profilaktiki. Gynecology. 2004;6(4):174–180. (In Russ.)
  19. Shipulina OYu, Abramova MS, Korolenkova LI. Сomparative analysis of modern reagent kits on the basis of real time PCR for detection of HPV with a high carcinogenic risk in the framework of cervical screening. Issues of Practical. Colposcopy and Genital Infections. 2022;(3):26–32. (In Russ.) doi: 10.46393/27826392_2022_3_26
  20. Rogovskaya SI, Trofimov DY, Kogan EA, et al. Clinical value of molecular markers in papillomavirus infection. Obstetrics and Gynecology. 2011;(4):4–10. (In Russ.)
  21. Hibma MH. The immune response to papillomavirus during infection persistence and regression. Open Virol J. 2012;6:241–248. doi: 10.2174/1874357901206010241
  22. Skinner SR, Wheeler CM, Romanowski B, et al. Progression of HPV infection to detectable cervical lesions or clearance in adult women: analysis of the control arm of the VIVIANE study. Int J Cancer. 2016;138(10):2428–2438. doi: 10.1002/ijc.29971
  23. Prilepskaya VN, Gusakov KI, Nazarova NM. Vaccination as an effective method of prevention for cervical diseases associated with human papillomavirus (literature review). Gynecology. 2019;21(2):23–27. (In Russ.) doi: 10.26442/20795696.2019.2.190396
  24. Lavagna A, Auger JP, Girardin SE, et al. Recognition of lipoproteins by Toll-like receptor 2 and DNA by the AIM2 inflammasome is responsible for production of interleukin-1β by virulent suilysin-negative streptococcus suis serotype 2. Pathogens. 2020;9(2):147. doi: 10.3390/pathogens9020147
  25. Lebedeva OP, Kalutsky PV, Pakhomov SP, et al. Toll-like raceptors of female reproductive tract and their ligands. Challenges in modern medicine. 2010;12(22,93):31–35. (In Russ.)
  26. Amador-Molina A, Hernández-Valencia JF, Lamoyi E, et al. Role of innate immunity against human papillomavirus (HPV) infections and effect of adjuvants in promoting specific immune response. Viruses. 2013;5(11):2624–2642. doi: 10.3390/v5112624
  27. Song D, Li H, Li H, et al. Effect of human papillomavirus infection on the immune system and its role in the course of cervical cancer. Oncol Lett. 2015;10(2):600–606. doi: 10.3892/ol.2015.3295
  28. Kedrova AG, Levakov SA, Tsarenko MD. Long-term results of treatment for benign cervical epithelial changes associated with human papillomavirus. Gynecology. 2016;12(2):77–83. (In Russ.) doi: 10.17650/1994-4098-2016-12-2-77-83.
  29. Daud II, Scott ME, Ma Y, et al. Association between toll-like receptor expression and human papillomavirus type 16 persistence. Int J Cancer. 2011;128(4):879–886. doi: 10.1002/ijc.25400
  30. Gumilevskaya OP, Kiseleva TS, Ritter MA, et al. The role of allelic polymorphism of receptor genes of innate immunity in the persistence of human papillomavirus. Journal Infectology. 2016;8(4):46–49. (In Russ.) doi: 10.22625/2072-6732-2016-8-4-46-49
  31. Proshin SN, Glushakov RI, Shabanov PD, et al. The value of the expression of TLR-receptors for the selection of pharmacological correction of pathology of the cervix and endometrium. Genes and Cells. 2011;6(1):91–97. (In Russ.)
  32. Wahid B, Ali A, Idrees M, Rafique S. Immunotherapeutic strategies for sexually transmitted viral infections: HIV, HSV and HPV. Cell Immunol. 2016;310:1–13. doi: 10.1016/j.cellimm.2016.08.001
  33. Rossiyskoe obshchestvo akusherov-ginekologov. Klinicheskie rekomendatsii po diagnostike i lecheniyu zabolevaniy, soprovozhda yushchikhsya patologicheskimi vydeleniyami iz polovykh putey. 2nd edition. Moscow; 2019. (In Russ.) [cited 2023 Aug 13]. Available from: https://minzdrav.midural.ru/uploads/19.pdf
  34. Allaband C, McDonald D, Vázquez-Baeza Y, et al. Microbiome 101: studying, analyzing, and interpreting gut microbiome data for clinicians. Clin Gastroenterol Hepatol. 2019;17(2):218–230. doi: 10.1016/j.cgh.2018.09.017
  35. Turnbaugh PJ, Ley RE, Hamady M, et al. The human microbiome project. Nature. 2007;449(7164):804–810. doi: 10.1038/nature06244
  36. France MT, Ma B, Gajer P, et al. VALENCIA: a nearest centroid classification method for vaginal microbial communities based on composition. Microbiome. 2020;8(1):166. doi: 10.1186/s40168-020-00934-6
  37. Mitra A, MacIntyre DA, Marchesi JR, et al. The vaginal microbiota, human papillomavirus infection and cervical intraepithelial neoplasia: what do we know and where are we going next? Microbiome. 2016;4(1):58. doi: 10.1186/s40168-016-0203-0
  38. De Seta F, Lonnee-Hoffmann R, Campisciano G, et al. The vaginal microbiome: III. The vaginal microbiome in various urogenital disorders. J Low Genit Tract Dis. 2022;26(1):85–92. doi: 10.1097/LGT.0000000000000645
  39. Watts DH, Fazzari M, Minkoff H, et al. Effects of bacterial vaginosis and other genital infections on the natural history of human papillomavirus infection in HIV-1-infected and high-risk HIV-1-uninfected women. J Infect Dis. 2005;191(7):1129–1139. doi: 10.1086/427777
  40. Norenhag J, Du J, Olovsson M, et al. The vaginal microbiota, human papillomavirus and cervical dysplasia: a systematic review and network meta-analysis. BJOG. 2020;127(2):171–180. doi: 10.1111/1471-0528.15854
  41. Di Paola M, Sani C, Clemente AM, et al. Characterization of cervico-vaginal microbiota in women developing persistent high-risk Human Papillomavirus infection. Sci Rep. 2017;7(1). doi: 10.1038/s41598-017-09842-6
  42. Machado A, Cerca N. Influence of biofilm formation by gardnerella vaginalis and other anaerobes on bacterial vaginosis. J Infect Dis. 2015;212(12):1856–1861. doi: 10.1093/infdis/jiv338
  43. Iakov DV, Isakov VA. New aspects in pathogenesis of herpes simplex infection (Review). The Bulletin of Hematology. 2016;12(4):13–18. (In Russ.)
  44. Meditsinskaya mikrobiologiya, virusologiya i immunologiya. Ed. by V.V. Zverev, M.N. Boychenko. Moscow: GEOTAR-Media; 2010. (In Russ.)
  45. Anogenital’naya gerpeticheskaya virusnaya infektsiya. Klini cheskie rekomendatsii. 2021. (In Russ.) [cited 13 Aug 2023]. Available from: https://roag-portal.ru/recommendations_gynecology
  46. James C, Harfouche M, Welton NJ, et al. Herpes simplex virus: global infection prevalence and incidence estimates, 2016. Bull World Health Organ. 2020;98(5):315–329. doi: 10.2471/BLT.19.237149
  47. Speck SH, Ganem D. Viral latency and its regulation: lessons from the gamma-herpesviruses. Cell Host Microbe. 2010;8(1):100–115. doi: 10.1016/j.chom.2010.06.014
  48. Zhu S, Viejo-Borbolla A. Pathogenesis and virulence of herpes simplex virus. Virulence. 2021;12(1):2670–2702. doi: 10.1080/21505594.2021.1982373
  49. Shannon B, Gajer P, Yi TJ, et al. Distinct effects of the cervicovaginal microbiota and herpes simplex type 2 infection on female genital tract immunology. J Infect Dis. 2017;215(9):1366–1375. doi: 10.1093/infdis/jix088
  50. Kaul R, Nagelkerke NJ, Kimani J, et al. Prevalent herpes simplex virus type 2 infection is associated with altered vaginal flora and an increased susceptibility to multiple sexually transmitted infections. J Infect Dis. 2007;196(11):1692–1697. doi: 10.1086/522006
  51. Cherpes TL, Meyn LA, Krohn MA, et al. Association between acquisition of herpes simplex virus type 2 in women and bacterial vaginosis. Clin Infect Dis. 2003;37(3):319–325. doi: 10.1086/375819
  52. Cherpes TL, Melan MA, Kant JA, et al. Genital tract shedding of herpes simplex virus type 2 in women: effects of hormonal contraception, bacterial vaginosis, and vaginal group B Streptococcus colonization. Clin Infect Dis. 2005;40(10):1422–1428. doi: 10.1086/429622
  53. Tapilskaya NI, Vorobtsova IN, Glushakov RI. Spontaneous clearance of the human papilloma virus as a result of suppressive therapy with acyclic nucleosides of a recurrent herpes-viral infection. Gynecology. 2017;19(3):55–61. (In Russ.) doi: 10.26442/2079-5696_19.3.55-61
  54. Horne AW, Missmer SA. Pathophysiology, diagnosis, and management of endometriosis. BMJ. 2022;379. doi: 10.1136/bmj-2022-070750
  55. Evans MB, Decherney AH. Fertility and endometriosis. Clin Obstet Gynecol. 2017;60(3):497–502. doi: 10.1097/GRF.0000000000000295
  56. Kolanska K, Alijotas-Reig J, Cohen J, et al. Endometriosis with infertility: a comprehensive review on the role of immune deregulation and immunomodulation therapy. Am J Reprod Immunol. 2021;85(3). doi: 10.1111/aji.13384
  57. Jarmolinskaja MI. Genital’nyj jendometrioz: vlijanie gormonal’nyh, immunologicheskih i geneticheskih faktorov na razvitie, osobennosti techenija i vybor terapii. [dissertation]. SaintPetersburg; 2009. (In Russ.) [cited 2023 Sept 26]. Available from: https://www.dissercat.com/content/genitalnyi-endometrioz-vliyanie-gormonalnykh-immunologicheskikh-i-geneticheskikh-faktorov-na
  58. Králíčková M, Vetvicka V. Immunological aspects of endometriosis: a review. Ann Transl Med. 2015;3(11):153. doi: 10.3978/j.issn.2305-5839.2015.06.08
  59. Osuga Y, Koga K, Hirota Y, et al. Lymphocytes in endometriosis. Am J Reprod Immunol. 2011;65(1):1–10. doi: 10.1111/j.1600-0897.2010.00887.x
  60. Riccio LDGC, Santulli P, Marcellin L, et al. Immunology of endometriosis. Best Pract Res Clin Obstet Gynaecol. 2018;50:39–49. doi: 10.1016/j.bpobgyn.2018.01.010
  61. Lebovic DI, Mueller MD, Taylor RN. Immunobiology of endometriosis. Fertil Steril. 2001;75(1):1–10. doi: 10.1016/s0015-0282(00)01630-7
  62. Symons LK, Miller JE, Kay VR, et al. The immunopathophysiology of endometriosis. Trends Mol Med. 2018;24(9):748–762. doi: 10.1016/j.molmed.2018.07.004
  63. Kobayashi H, Higashiura Y, Shigetomi H, et al. Pathogenesis of endometriosis: the role of initial infection and subsequent sterile inflammation (Review). Mol Med Rep. 2014;9(1):9–15. doi: 10.3892/mmr.2013.1755
  64. Sobstyl M, Niedźwiedzka-Rystwej P, Grywalska E, et al. Toll-like receptor 2 expression as a new hallmark of advanced endometriosis. Cells. 2020;9(8). doi: 10.3390/cells9081813
  65. Almasi MZ, Hosseini E, Jafari R, et al. Evaluation of Toll-like receptor 3 (TLR3) signaling pathway genes and its genetic polymorphisms in ectopic and eutopic endometrium of women with endometriosis. J Gynecol Obstet Hum Reprod. 2021;50(9). doi: 10.1016/j.jogoh.2021.102153
  66. Hernandes C, Gueuvoghlanian-Silva BY, Monnaka VU, et al. Regulatory T cells isolated from endometriotic peritoneal fluid express a different number of Toll-like receptors. Einstein (Sao Paulo). 2020;18. doi: 10.31744/einstein_journal/2020AO5294
  67. de Azevedo BC, Mansur F, Podgaec S. A systematic review of toll-like receptors in endometriosis. Arch Gynecol Obstet. 2021;304(2):309–316. doi: 10.1007/s00404-021-06075-x
  68. Salliss ME, Farland LV, Mahnert ND, et al. The role of gut and genital microbiota and the estrobolome in endometriosis, infertility and chronic pelvic pain. Hum Reprod Update. 2021;28(1):92–131. doi: 10.1093/humupd/dmab035
  69. Chang CY, Chiang AJ, Lai MT, et al. A more diverse cervical microbiome associates with better clinical outcomes in patients with endometriosis: a pilot study. Biomedicines. 2022;10(1):174. doi: 10.3390/biomedicines10010174
  70. Hsu CY, Ke DS, Lin CL, et al. To investigate the risk of herpes zoster in women with endometriosis: a taiwan national population-based cohort study. Front Med (Lausanne). 2021;8. doi: 10.3389/fmed.2021.584322
  71. Oppelt P, Renner SP, Strick R, et al. Correlation of high-risk human papilloma viruses but not of herpes viruses or Chlamydia trachomatis with endometriosis lesions. Fertil Steril. 2010;93(6):1778–1786. doi: 10.1016/j.fertnstert.2008.12.061
  72. Heidarpour M, Derakhshan M, Derakhshan-Horeh M, et al. Prevalence of high-risk human papillomavirus infection in women with ovarian endometriosis. J Obstet Gynaecol Res. 2017;43(1):135–139. doi: 10.1111/jog.13188
  73. Rocha RM, Souza RP, Gimenes F, et al. The high-risk human papillomavirus continuum along the female reproductive tract and its relationship to infertility and endometriosis. Reprod Biomed Online. 2019;38(6):926–937. doi: 10.1016/j.rbmo.2018.11.032

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