Human papillomavirus and pregnancy: A narrative review study

Document Type : Review Article

Authors

1 M.Sc. of Clinical Biochemistry, Blood Borne Infections Research Center, Academic Center for Education, Culture and Research (ACECR), Razavi Khorasan Branch, Mashhad, Iran.

2 Professor, Department of Parasitology and Mycology, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran. Iranian Academic Center for Education, Culture and Research (ACECR), Mashhad Branch, Iran.

3 Professor, Department of Obstetrics and Gynecology, Supporting the Family and the Youth of Population Research Core, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran.

4 PhD of Molecular Medicine, Blood Borne Infections Research Center, Academic Center for Education, Culture and Research (ACECR), Razavi Khorasan Branch, Mashhad, Iran.

Abstract

Introduction: Human papillomavirus (HPV) is the most common sexual transmitted infection. The persistence of HPV infection causes different types of anogenital and oropharyngeal cancer. HPV infection during pregnancy may be associated with several adverse consequences, such as preterm birth and miscarriage. The present study was performed with aim to investigate the relationship between HPV infection and adverse pregnancy outcomes in different studies.
Methods: In this narrative review, to find relevant articles, PubMed and Google Scholar databases were searched using the keywords HPV, Papillomavirus, HPV in Pregnancy, HPV Transmission and Adverse outcomes from 2000 to 2022. For this purpose, original research articles, clinical trials, reviews and case reports related to the subject of this review were included in the study and unrelated studies were excluded. The review of the articles was done by reading the title, abstract and content, respectively. The language on the admission papers was English.
Results: The results of the different studies have shown that the risk of HPV infection in pregnant women is higher than in non-pregnant women. Also, the risk of preterm birth and preterm premature rupture of the membranes is reported to be higher in HPV positive pregnant women in comparison with HPV negative women. Some studies have also pointed to the relationship between HPV infection and spontaneous fetal death.
Conclusion: Considering many complications of HPV infection in pregnant women, it is better to ensure about non-infection with this virus before pregnancy.

Keywords

Main Subjects


  1. Alotaibi HJ, Almajhdi FN, Alsaleh AN, Obeid DA, Khayat HH, Al-Muammer TA, et al. Association of sexually transmitted infections and human papillomavirus co-infection with abnormal cervical cytology among women in Saudi Arabia. Saudi Journal of Biological Sciences 2020; 27(6):1587-95.
  2. Wierzbicka M, San Giorgi MR, Dikkers FG. Transmission and clearance of human papillomavirus infection in the oral cavity and its role in oropharyngeal carcinoma–A review. Reviews in medical virology 2023; 33(1):e2337.
  3. De Villiers EM, Fauquet C, Broker TR, Bernard HU, Zur Hausen H. Classification of papillomaviruses. Virology 2004; 324(1):17-27.
  4. Egawa N, Egawa K, Griffin H, Doorbar J. Human papillomaviruses; epithelial tropisms, and the development of neoplasia. Viruses 2015; 7(7):3863-90.
  5. Chilaka VN, Navti OB, Al Beloushi M, Ahmed B, Konje JC. Human papillomavirus (HPV) in pregnancy–An update. European Journal of Obstetrics & Gynecology and Reproductive Biology 2021; 264:340-8.
  6. Winer RL, Kiviat NB, Hughes JP, Adam DE, Lee SK, Kuypers JM, et al. Development and duration of human papillomavirus lesions, after initial infection. The Journal of infectious diseases 2005; 191(5):731-8.
  7. de Sanjose S, Brotons M, Pavon MA. The natural history of human papillomavirus infection. Best practice & research Clinical obstetrics & gynaecology 2018; 47:2-13.
  8. Jee B, Yadav R, Pankaj S, Shahi SK. Immunology of HPV-mediated cervical cancer: current understanding. International Reviews of Immunology 2021; 40(5):359-78.
  9. Oh HY, Seo SS, Kim MK, Lee DO, Chung YK, Lim MC, et al. Synergistic effect of viral load and alcohol consumption on the risk of persistent high-risk human papillomavirus infection. PLoS One 2014; 9(8):e104374.
  10. Chan DP, Cheung TH, Tam AO, Cheung JL, Yim SF, Lo KW, et al. Risk Association between Human Leukocyte Antigen–A Allele and High-Risk Human Papillomavirus Infection for Cervical Neoplasia in Chinese Women. The Journal of infectious diseases 2005; 192(10):1749-56.
  11. Xu HH, Yan WH, Lin A. The role of HLA-G in human papillomavirus infections and cervical carcinogenesis. Frontiers in immunology 2020; 11:1349.
  12. Shahi M, Shamsian SA, Ghodsi M, Shafaei A. Prevalence of Different Human Papillomavirus Genotypes and Their Relationship with Pap Smear Test Results in Mashhad, Iran. Journal of Mazandaran University of Medical Sciences 2021; 31(200):149-55.
  13. Shahi M, Shamsian SA, Ghodsi M, Shafaei A. Prevalence and Genotype Distribution of Human Papillomavirus in a Population of Iranian Men. Journal of Mazandaran University of Medical Sciences 2022; 32(212):147-54.
  14. Ntanasis-Stathopoulos I, Kyriazoglou A, Liontos M, Dimopoulos M, Gavriatopoulou M. Current trends in the management and prevention of human papillomavirus (HPV) infection. J. BUON 2020; 25(3):1281-5.
  15. Jamieson DJ, Theiler RN, Rasmussen SA. Emerging infections and pregnancy. Emerging infectious diseases 2006; 12(11):1638.
  16. Grce M, Husnjak K, Matovina M, Milutin N, Magdic L, Husnjak O, et al. Human papillomavirus, cytomegalovirus, and adeno-associated virus infections in pregnant and nonpregnant women with cervical intraepithelial neoplasia. Journal of clinical Microbiology 2004; 42(3):1341-4.
  17. Pandey D, Solleti V, Jain G, Das A, Shama Prasada K, Acharya S, et al. Human papillomavirus (HPV) infection in early pregnancy: prevalence and implications. Infectious diseases in obstetrics and gynecology 2019; 2019.
  18. Condrat CE, Filip L, Gherghe M, Cretoiu D, Suciu N. Maternal HPV infection: Effects on pregnancy outcome. Viruses 2021; 13(12):2455.
  19. Ardekani A, Taherifard E, Mollalo A, Hemadi E, Roshanshad A, Fereidooni R, et al. Human papillomavirus infection during pregnancy and childhood: a comprehensive review. Microorganisms 2022; 10(10):1932.
  20. Nobbenhuis MA, Helmerhorst TJ, Van den Brule AJ, Rozendaal L, Bezemer PD, Voorhorst FJ, et al. High-risk human papillomavirus clearance in pregnant women: trends for lower clearance during pregnancy with a catch-up postpartum. British journal of cancer 2002; 87(1):75-80.
  21. Abu-Raya B, Michalski C, Sadarangani M, Lavoie PM. Maternal immunological adaptation during normal pregnancy. Frontiers in immunology 2020: 2627.
  22. Liu P, Xu L, Sun Y, Wang Z. The prevalence and risk of human papillomavirus infection in pregnant women. Epidemiology & Infection 2014; 142(8):1567-78.
  23. Luo D, Peng M, Wei X, Pan D, Xue H, Xu Y, et al. Prevalence of human papillomavirus and genotype distribution in pregnant and non-pregnant Women in China. Risk Management and Healthcare Policy 2021: 3147-57.
  24. Chen J, Gopala K, Puthatta A, Struyf F, Rosillon D. Prevalence and incidence of human papillomavirus (HPV) infection before and after pregnancy: pooled analysis of the control arms of efficacy trials of HPV-16/18 AS04-adjuvanted vaccine. InOpen Forum Infectious Diseases 2019; 6(12):ofz486.
  25. Ardekani A, Sepidarkish M, Mollalo A, Afradiasbagharani P, Rouholamin S, Rezaeinejad M, et al. Worldwide prevalence of human papillomavirus among pregnant women: A systematic review and meta‐analysis. Reviews in Medical Virology 2023; 33(1):e2374.
  26. Gomez LM, Ma Y, Ho C, McGrath CM, Nelson DB, Parry S. Placental infection with human papillomavirus is associated with spontaneous preterm delivery. Human reproduction 2008; 23(3):709-15.
  27. Liu Y, You H, Chiriva-Internati M, Korourian S, Lowery CL, Carey MJ, et al. Display of complete life cycle of human papillomavirus type 16 in cultured placental trophoblasts. Virology 2001; 290(1):99-105.
  28. You H, Liu Y, Carey MJ, Lowery CL, Hermonat PL. Defective 3A trophoblast-endometrial cell adhesion and altered 3A growth and survival by human papillomavirus type 16 oncogenes. Molecular Cancer Research 2002; 1(1):25-31.
  29. You H, Liu Y, Agrawal N, Prasad CK, Chiriva-Internati M, Lowery CL, et al. Infection, replication, and cytopathology of human papillomavirus type 31 in trophoblasts. Virology 2003; 316(2):281-9.
  30. Wetherill LF, Holmes KK, Verow M, Müller M, Howell G, Harris M, et al. High-risk human papillomavirus E5 oncoprotein displays channel-forming activity sensitive to small-molecule inhibitors. Journal of virology 2012; 86(9):5341-51.
  31. Nieto-Torres JL, Verdiá-Báguena C, Castaño-Rodriguez C, Aguilella VM, Enjuanes L. Relevance of viroporin ion channel activity on viral replication and pathogenesis. Viruses 2015; 7(7):3552-73.
  32. Gibbs RS. The relationship between infections and adverse pregnancy outcomes: an overview. Annals of periodontology 2001; 6(1):153-63.
  33. Huang QT, Zhong M, Gao YF, Huang LP, Huang Q, Wang W, et al. Can HPV vaccine have other health benefits more than cancer prevention? A systematic review of association between cervical HPV infection and preterm birth. Journal of Clinical Virology 2014; 61(3):321-8.
  34. Niyibizi J, Mayrand MH, Audibert F, Monnier P, Brassard P, Laporte L, et al. Association between human papillomavirus infection among pregnant women and preterm birth. JAMA Network Open 2021; 4(9):e2125308.
  35. Wiik J, Nilsson S, Kärrberg C, Strander B, Jacobsson B, Sengpiel V. Associations of treated and untreated human papillomavirus infection with preterm delivery and neonatal mortality: A Swedish population-based study. PLoS medicine 2021; 18(5):e1003641.
  36. Ambühl LM, Baandrup U, Dybkær K, Blaakær J, Uldbjerg N, Sørensen S. Human papillomavirus infection as a possible cause of spontaneous abortion and spontaneous preterm delivery. Infectious diseases in obstetrics and gynecology 2016; 2016.
  37. Bober L, Guzowski G, Moczulska H, Sieroszewski P. Influence of human Papilloma Virus (hPV) infection on early pregnancy. Ginekologia polska 2019; 90(2):72-5.
  38. Conde-Ferráez L, May AD, Carrillo-Martínez JR, Ayora-Talavera G, del Refugio González-Losa M. Human papillomavirus infection and spontaneous abortion: a case–control study performed in Mexico. European Journal of Obstetrics & Gynecology and Reproductive Biology 2013; 170(2):468-73.
  39. Tognon M, Tagliapietra A, Magagnoli F, Mazziotta C, Oton-Gonzalez L, Lanzillotti C, et al. Investigation on spontaneous abortion and human papillomavirus infection. Vaccines 2020; 8(3):473.
  40. Slatter TL, Hung NG, Clow WM, Royds JA, Devenish CJ, Hung NA. A clinicopathological study of episomal papillomavirus infection of the human placenta and pregnancy complications. Modern Pathology 2015; 28(10):1369-82.
  41. McDonnold M, Dunn H, Hester A, Pacheco LD, Hankins GD, Saade GR, et al. High risk human papillomavirus at entry to prenatal care and risk of preeclampsia. American journal of obstetrics and gynecology 2014; 210(2):138-e1.
  42. Cho G, Min KJ, Hong HR, Kim S, Hong JH, Lee JK, et al. High-risk human papillomavirus infection is associated with premature rupture of membranes. BMC pregnancy and childbirth 2013; 13(1):1-4.
  43. Nimrodi M, Kleitman V, Wainstock T, Gemer O, Meirovitz M, Maymon E, et al. The association between cervical inflammation and histologic evidence of HPV in PAP smears and adverse pregnancy outcome in low risk population. European Journal of Obstetrics & Gynecology and Reproductive Biology 2018; 225:160-5.
  44. Suhag A, Berghella V. Intrauterine growth restriction (IUGR): etiology and diagnosis. Current Obstetrics and Gynecology Reports 2013; 2(2):102-11.
  45. Korteweg FJ, Erwich JJ, Holm JP, Ravisé JM, van der Meer J, Veeger NJ, et al. Diverse placental pathologies as the main causes of fetal death. Obstetrics & Gynecology 2009; 114(4):809-17.
  46. Subramaniam A, Lees BF, Becker DA, Tang Y, Khan MJ, Edwards RK. Evaluation of human papillomavirus as a risk factor for preterm birth or pregnancy-related hypertension. Obstetrics & Gynecology 2016; 127(2):233-40.
  47. Rombaldi RL, Serafini EP, Mandelli J, Zimmermann E, Losquiavo KP. Perinatal transmission of human papilomavirus DNA. Virology journal 2009; 6:1-12.
  48. Syrjänen S. Current concepts on human papillomavirus infections in children. Apmis 2010; 118(6‐7):494-509.
  49. Zouridis A, Kalampokas T, Panoulis K, Salakos N, Deligeoroglou E. Intrauterine HPV transmission: a systematic review of the literature. Archives of Gynecology and Obstetrics 2018; 298:35-44.
  50. Syrjänen S, Rintala M, Sarkola M, Willberg J, Rautava J, Koskimaa H, et al. Oral human papillomavirus infection in children during the first 6 years of life, Finland. Emerging Infectious Diseases 2021; 27(3):759.
  51. Louvanto K, Sarkola M, Rintala M, Syrjänen K, Grenman S, Syrjänen S. Breast milk is a potential vehicle for human papillomavirus transmission to oral mucosa of the spouse. The Pediatric Infectious Disease Journal 2017; 36(7):627-30.
  52. Workowski KA, Bolan GA. Sexually transmitted diseases treatment guidelines, 2015. MMWR. Recommendations and reports: Morbidity and mortality weekly report. Recommendations and reports 2015; 64(RR-03):1.
  53. Steben M, LaBelle D. Genital warts: Canadians’ perception, health-related behaviors, and treatment preferences. Journal of lower genital tract disease 2012; 16(4):409-15.
  54. Rob F. Genital Warts. Diagnostics to Pathogenomics of Sexually Transmitted Infections 2018: 119.
  55. Wiley DJ, Douglas J, Beutner K, Cox T, Fife K, Moscicki AB, et al. External genital warts: diagnosis, treatment, and prevention. Clinical Infectious Diseases 2002; 35(Supplement_2):S210-24.
  56. Wolf M. The Vulva in Pregnancy and Delivery. Vulvar Disease: Breaking the Myths 2019: 73-9.
  57. Wilkerson EC, Van Acker MM, Bloom BS, Goldberg DJ. Utilization of laser therapy during pregnancy: a systematic review of the maternal and fetal effects reported from 1960 to 2017. Dermatologic surgery 2019; 45(6):818-28.
  58. Arena S, Marconi M, Frega A, Villani C. Pregnancy and condyloma. Evaluation about therapeutic effectiveness of laser CO2 on 115 pregnant women. Minerva ginecologica 2001; 53(6):389-96.
  59. Allison RR, Moghissi K. Photodynamic therapy (PDT): PDT mechanisms. Clinical endoscopy 2013;46(1):24-9.
  60. Yang YG, Zou XB, Hua ZH, Zhang YJ, Li HJ. Photodynamic therapy of condyloma acuminata in pregnant women. Chinese Medical Journal 2012; 125(16):2925-8.
  61. Sugai S, Nishijima K, Enomoto T. Management of condyloma acuminata in pregnancy: a review. Sexually transmitted diseases 2021; 48(6):403-9.
  62. Bonde U, Joergensen JS, Lamont RF, Mogensen O. Is HPV vaccination in pregnancy safe?. Human vaccines & immunotherapeutics 2016; 12(8):1960-4.
  63. Du J, Ährlund-Richter A, Näsman A, Dalianis T. Human papilloma virus (HPV) prevalence upon HPV vaccination in Swedish youth: A review based on our findings 2008–2018, and perspectives on cancer prevention. Archives of gynecology and obstetrics 2021; 303:329-35.
  64. Shimabukuro TT, Su JR, Marquez PL, Mba-Jonas A, Arana JE, Cano MV. Safety of the 9-Valent Human Papillomavirus Vaccine. Pediatrics 2019; 144(6):e20191791.
  65. Bruni L, Saura-Lázaro A, Montoliu A, Brotons M, Alemany L, Diallo MS, et al. HPV vaccination introduction worldwide and WHO and UNICEF estimates of national HPV immunization coverage 2010–2019. Preventive medicine 2021; 144:106399.
  66. Spînu AD, Anghel RF, Marcu DR, Iorga DL, Cherciu A, Mischianu DL. HPV vaccine for men: Where to?. Experimental and therapeutic medicine 2021; 22(5):1-6.
  67. Centers for Disease Control and Prevention. HPV (Human Papilloma Virus) Vaccine What You Need to Know; 2021.
  68. Ambühl LM, Leonhard AK, Widen Zakhary C, Jørgensen A, Blaakær J, Dybkær K, et al. Human papillomavirus infects placental trophoblast and Hofbauer cells, but appears not to play a causal role in miscarriage and preterm labor. Acta obstetricia et gynecologica Scandinavica 2017; 96(10):1188-96.
  69. Ticconi C, Pietropolli A, Fabbri G, Capogna MV, Perno CF, Piccione E. Recurrent miscarriage and cervical human papillomavirus infection. American Journal of Reproductive Immunology 2013; 70(5):343-6.
  70. Cotton-Caballero A, Dudley D, Ferguson J, Pettit K, Boyle A. Maternal human papillomavirus infection increases the risk of premature rupture of membranes [19M]. Obstetrics & Gynecology 2017; 129(5):S137.
  71. Medeiros LR, Ethur AB, Hilgert JB, Zanini RR, Berwanger O, Bozzetti MC, et al. Vertical transmission of the human papillomavirus: a systematic quantitative review. Cadernos de saude publica 2005; 21:1006-15.
  72. Freitas AC, Mariz FC, Silva MA, Jesus AL. Human papillomavirus vertical transmission: review of current data. Clinical infectious diseases 2013; 56(10):1451-6.
  73. Chatzistamatiou K, Sotiriadis A, Agorastos T. Effect of mode of delivery on vertical human papillomavirus transmission–A meta-analysis. Journal of Obstetrics and Gynaecology 2016; 36(1):10-4.
  74. Smith EM, Ritchie JM, Yankowitz J, Swarnavel S, Wang D, Haugen TH, et al. Human papillomavirus prevalence and types in newborns and parents: concordance and modes of transmission. Sexually transmitted diseases 2004: 57-62.
  75. Mammas IN, Sourvinos G, Spandidos DA. Human papilloma virus (HPV) infection in children and adolescents. European journal of pediatrics 2009; 168:267-73.