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High prevalence of human papillomaviruses in Ghanaian pregnant women

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Data about the prevalence of human papillomaviruses (HPV) in African women with normal and abnormal cervical cytology are still scarce. Current HPV vaccines contain HPV types, which mainly represent the HPV epidemiology of industrial countries. As further developments of HPV vaccines are going on, it is necessary to regard regional differences in HPV type prevalence to ensure optimal protection by the vaccine. Vaginal swabs of Ghanaian pregnant women, routinely collected before delivery to rule out bacterial infections causing early onset sepsis, were screened for 12 high-risk (HR), 13 probably/possibly (pHR), and 18 low-risk (LR) HPV types. Most pregnant women come for delivery to the hospital. This was considered as appropriate possibility to have an unselected group of women. HPV DNA were detected in 55/165 women (33.3, 95 % CI 26.3–41.1 %). Thirty-four out of fifty-five (61.8, 95 % CI 47.7–74.3 %) of HPV-positive women were infected with HR and/or pHR HPV types. The five most prevalent HR or pHR HPV types were HPV-52 and HPV-67 (7 women each, 4.2, 95 % CI 1.9–8.9 %), HPV-53 (six women, 3.6, 95 % CI 1.5–8.1 %), HPV-45 (five women, 3.0, 95 % CI 1.1–7.3 %), and HPV-18 (four women, 2.4, 95 % CI 0.8–6.5 %), respectively. HPV-16 was found in two women only (1.2, 95 % CI 0.2–4.8 %). Future HPV vaccine research may devote special interest to HPV-67 and HPV-53 provided further studies confirm their high prevalence in the general population of Sub-Saharan African countries. The true carcinogenic potential of HPV-67, which is a member of species alpha9 including HPV-16, and so far categorized as pHR, should be clarified.

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  1. International Agency for Research on Cancer (IARC) (2012) Biological agents. Volume 100 B. A review of human carcinogens. IARC Monogr Eval Carcinog Risks Hum 100:1–441

    Google Scholar 

  2. Jamieson DJ, Theiler RN, Rasmussen SA (2006) Emerging infections and pregnancy. Emerg Infect Dis 12:1638–1643

    Article  PubMed  PubMed Central  Google Scholar 

  3. Szekeres-Bartho J (2002) Immunological relationship between the mother and the fetus. Int Rev Immunol 21:471–495

    Article  CAS  PubMed  Google Scholar 

  4. Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D, Bray F (2015) Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer 136:E359–E386

    Article  CAS  PubMed  Google Scholar 

  5. Bruni L, Barrionuevo-Rosas L, Albero G, Aldea M, Serrano B, Valencia S, Brotons M, Mena M, Cosano R, Muñoz J, Bosch FX, de Sanjosé S, Castellsagué X. ICO Information Centre on HPV and Cancer (HPV Information Centre) (2016) Human papillomavirus and related diseases in Ghana. Summary Report 2016-02-26. Accessed 2016-08-24

  6. Czegledy J, Rogo KO, Evander M, Wadell G (1992) High-risk human papillomavirus types in cytologically normal cervical scrapes from Kenya. Med Microbiol Immunol 180:321–326

    Article  CAS  PubMed  Google Scholar 

  7. Brandful JAM, Bonney EY, Asmah RH, Apea-Kubi KA (2014) Oncogenic human papillomavirus (HPV) in women from Ghana. J Cancer Res Exp Oncol 6:31–38

    Google Scholar 

  8. Yar DD, Salifu SP, Darko SN, Annan AA, Gyimah AA, Buabeng KO, Owusu-Dabo E (2016) Genotypic characterisation of human papillomavirus infections among persons living with HIV infection; a case–control study in Kumasi, Ghana. Trop Med Int Health 21:275–282

    Article  PubMed  Google Scholar 

  9. Attoh S, Asmah R, Wiredu EK, Gyasi R, Tettey Y (2010) Human papilloma virus genotypes in Ghanaian women with cervical carcinoma. East Afr Med J 87:345–349

    CAS  PubMed  Google Scholar 

  10. Denny L, Adewole I, Anorlu R, Dreyer G, Moodley M, Smith T, Snyman L, Wiredu E, Molijn A, Quint W, Ramakrishnan G, Schmidt J (2014) Human papillomavirus prevalence and type distribution in invasive cervical cancer in sub-Saharan Africa. Int J Cancer 134:1389–1398

    Article  CAS  PubMed  Google Scholar 

  11. Awua AK, Sackey ST, Osei YD, Asmah RH, Wiredu EK (2016) Prevalence of human papillomavirus genotypes among women with cervical cancer in Ghana. Infect Agents Cancer 11:4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. de Sanjose S, Diaz M, Castellsague X, Clifford G, Bruni L, Munoz N, Bosch FX (2007) Worldwide prevalence and genotype distribution of cervical human papillomavirus DNA in women with normal cytology: a meta-analysis. Lancet Infect Dis 7:453–459

    Article  PubMed  Google Scholar 

  13. Bruni L, Diaz M, Castellsague X, Ferrer E, Bosch FX, de Sanjose S (2010) Cervical human papillomavirus prevalence in 5 continents: meta-analysis of 1 million women with normal cytological findings. J Infect Dis 202:1789–1799

    Article  PubMed  Google Scholar 

  14. Liu P, Xu L, Sun Y, Wang Z (2014) The prevalence and risk of human papillomavirus infection in pregnant women. Epidemiol Infect 142:1567–1578

    Article  CAS  PubMed  Google Scholar 

  15. Wagner M, Bennetts L, Patel H, Welner S, de Sanjose S, Weiss TW (2015) Global availability of data on HPV genotype-distribution in cervical, vulvar and vaginal disease and genotype-specific prevalence and incidence of HPV infection in females. Infect Agents Cancer 10:13

    Article  PubMed  PubMed Central  Google Scholar 

  16. Bernard E, Pons-Salort M, Favre M, Heard I, Delarocque-Astagneau E, Guillemot D, Thiebaut AC (2013) Comparing human papillomavirus prevalences in women with normal cytology or invasive cervical cancer to rank genotypes according to their oncogenic potential: a meta-analysis of observational studies. BMC Infect Dis 13:373

    Article  PubMed  PubMed Central  Google Scholar 

  17. de Sanjose S, Quint WG, Alemany L, Geraets DT, Klaustermeier JE, Lloveras B, Tous S, Felix A, Bravo LE, Shin HR, Vallejos CS, de Ruiz PA, Lima MA, Guimera N, Clavero O, Alejo M, Llombart-Bosch A, Cheng-Yang C, Tatti SA, Kasamatsu E, Iljazovic E, Odida M, Prado R, Seoud M, Grce M, Usubutun A, Jain A, Suarez GA, Lombardi LE, Banjo A, Menendez C, Domingo EJ, Velasco J, Nessa A, Chichareon SC, Qiao YL, Lerma E, Garland SM, Sasagawa T, Ferrera A, Hammouda D, Mariani L, Pelayo A, Steiner I, Oliva E, Meijer CJ, Al-Jassar WF, Cruz E, Wright TC, Puras A, Llave CL, Tzardi M, Agorastos T, Garcia-Barriola V, Clavel C, Ordi J, Andujar M, Castellsague X, Sanchez GI, Nowakowski AM, Bornstein J, Munoz N, Bosch FX (2010) Human papillomavirus genotype attribution in invasive cervical cancer: a retrospective cross-sectional worldwide study. Lancet Oncol 11(11):1048–1056

    Article  PubMed  Google Scholar 

  18. Castellsague X, de Sanjose S, Aguado T, Louie KS, Bruni L, Munoz J, Diaz M, Irwin K, Gacic M, Beauvais O, Albero G, Ferrer E, Byrne S, Bosch FX (2007) HPV and cervical cancer in the world: 2007 report. Section I. Continents and regions. Vaccine 25(Suppl 3):C1–C26

    Google Scholar 

  19. Louie KS, de Sanjose S, Mayaud P (2009) Epidemiology and prevention of human papillomavirus and cervical cancer in sub-Saharan Africa: a comprehensive review. Trop Med Int Health 14:1287–1302

    Article  PubMed  Google Scholar 

  20. Guan P, Howell-Jones R, Li N, Bruni L, de Sanjose S, Franceschi S, Clifford GM (2012) Human papillomavirus types in 115,789 HPV-positive women: a meta-analysis from cervical infection to cancer. Int J Cancer 131:2349–2359

    Article  CAS  PubMed  Google Scholar 

  21. Ogembo RK, Gona PN, Seymour AJ, Park HS, Bain PA, Maranda L, Ogembo JG (2015) Prevalence of human papillomavirus genotypes among African women with normal cervical cytology and neoplasia: a systematic review and meta-analysis. PLoS One 10:e0122488

    Article  PubMed  PubMed Central  Google Scholar 

  22. Doerr HW, Berger A (2014) Vaccination against infectious diseases: what is promising? Med Microbiol Immunol 203:365–371

    Article  CAS  PubMed  Google Scholar 

  23. Garland SM, Kjaer SK, Muñoz N, Block SL, Brown DR, DiNubile MJ, Lindsay BR, Kuter BJ, Perez G, Dominiak-Felden G, Saah AJ, Drury R, Das R, Velicer C (2016) Impact and effectiveness of the quadrivalent human papillomavirus vaccine: a systematic review of 10 years of real-world experience. Clin Infect Dis 63:519–527

    Article  PubMed  PubMed Central  Google Scholar 

  24. Gross U, Amuzu SK, de Ciman R, Kassimova I, Gross L, Rabsch W, Rosenberg U, Schulze M, Stich A, Zimmermann O (2011) Bacteremia and antimicrobial drug resistance over time, Ghana. Emerg Infect Dis 17:1879–1882

    Article  PubMed  PubMed Central  Google Scholar 

  25. Schmitt M, Bravo IG, Snijders PJ, Gissmann L, Pawlita M, Waterboer T (2006) Bead-based multiplex genotyping of human papillomaviruses. J Clin Microbiol 44:504–512

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Schmitt M, Dondog B, Waterboer T, Pawlita M (2008) Homogeneous amplification of genital human alpha papillomaviruses by PCR using novel broad-spectrum GP5 + and GP6+ primers. J Clin Microbiol 46:1050–1059

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Schmitt M, Dondog B, Waterboer T, Pawlita M, Tommasino M, Gheit T (2010) Abundance of multiple high-risk human papillomavirus (HPV) infections found in cervical cells analyzed by use of an ultrasensitive HPV genotyping assay. J Clin Microbiol 48:143–149

    Article  CAS  PubMed  Google Scholar 

  28. Silling S, Kreuter A, Hellmich M, Swoboda J, Pfister H, Wieland U (2012) Human papillomavirus oncogene mRNA testing for the detection of anal dysplasia in HIV-positive men who have sex with men. J Clin Virol 53:325–331

    Article  CAS  PubMed  Google Scholar 

  29. Wieland U, Ritzkowsky A, Stoltidis M, Weissenborn S, Stark S, Ploner M, Majewski S, Jablonska S, Pfister HJ, Fuchs PG (2000) Communication: papillomavirus DNA in basal cell carcinomas of immunocompetent patients: an accidental association? J Invest Dermatol 115:124–128

    Article  CAS  PubMed  Google Scholar 

  30. Castle PE, Rodriguez AC, Porras C, Herrero R, Schiffman M, Gonzalez P, Hildesheim A, Burk RD (2007) A comparison of cervical and vaginal human papillomavirus. Sex Transm Dis 34:849–855

    Article  PubMed  PubMed Central  Google Scholar 

  31. Roberts CC, Liaw KL, Skjeldestad FE, Jansen KU, Bryan JT (2009) Importance of specimen type in detecting human papillomavirus DNA from the female genital tract. J Med Virol 81:1620–1626

    Article  CAS  PubMed  Google Scholar 

  32. Gravitt PE (2011) The known unknowns of HPV natural history. J Clin Invest 121:4593–4599

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Wheeler CM, Hunt WC, Cuzick J, Langsfeld E, Pearse A, Montoya GD, Robertson M, Shearman CA, Castle PE (2013) A population-based study of human papillomavirus genotype prevalence in the United States: baseline measures prior to mass human papillomavirus vaccination. Int J Cancer 132:198–207

    Article  CAS  PubMed  Google Scholar 

  34. Ghana Statistical Service (GSS), Ghana Health Service (GHS), and ICF International (2015) Ghana Demographic and Health Survey 2014. Rockville, Maryland, USA: GSS, GHS, and ICF International. Accessed 2016-08-24

  35. Thomas JO, Herrero R, Omigbodun AA, Ojemakinde K, Ajayi IO, Fawole A, Oladepo O, Smith JS, Arslan A, Munoz N, Snijders PJ, Meijer CJ, Franceschi S (2004) Prevalence of papillomavirus infection in women in Ibadan, Nigeria: a population-based study. Br J Cancer 90:638–645

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Piras F, Piga M, De Montis A, Zannou AR, Minerba L, Perra MT, Murtas D, Atzori M, Pittau M, Maxia C, Sirigu P (2011) Prevalence of human papillomavirus infection in women in Benin, West Africa. Virol J 8:514

    Article  PubMed  PubMed Central  Google Scholar 

  37. Smith JS, Lindsay L, Hoots B, Keys J, Franceschi S, Winer R, Clifford GM (2007) Human papillomavirus type distribution in invasive cervical cancer and high-grade cervical lesions: a meta-analysis update. Int J Cancer 121:621–632

    Article  CAS  PubMed  Google Scholar 

  38. Bzhalava D, Guan P, Franceschi S, Dillner J, Clifford G (2013) A systematic review of the prevalence of mucosal and cutaneous human papillomavirus types. Virology 445:224–231

    Article  CAS  PubMed  Google Scholar 

  39. Andersson S, Mints M, Sallstrom J, Wilander E (2005) The relative distribution of oncogenic types of human papillomavirus in benign, pre-malignant and malignant cervical biopsies. A study with human papillomavirus deoxyribonucleic acid sequence analysis. Cancer Detect Prev 29:37–41

    Article  CAS  PubMed  Google Scholar 

  40. Gudleviciene Z, Didziapetriene J, Ramael M, Uleckiene S, Valuckas KP (2006) Human papillomavirus and p53 polymorphism in Lithuanian cervical cancer patients. Gynecol Oncol 102:530–533

    Article  CAS  PubMed  Google Scholar 

  41. Gargiulo F, De Francesco MA, Schreiber C, Ciravolo G, Salinaro F, Valloncini B, Manca N (2007) Prevalence and distribution of single and multiple HPV infections in cytologically abnormal cervical samples from Italian women. Virus Res 125:176–182

    Article  CAS  PubMed  Google Scholar 

  42. Wentzensen N, Schiffman M, Dunn T, Zuna RE, Gold MA, Allen RA, Zhang R, Sherman ME, Wacholder S, Walker J, Wang SS (2009) Multiple human papillomavirus genotype infections in cervical cancer progression in the study to understand cervical cancer early endpoints and determinants. Int J Cancer 125:2151–2158

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Petrosky E, Bocchini JA Jr, Hariri S, Chesson H, Curtis CR, Saraiya M, Unger ER, Markowitz LE (2015) Use of 9-valent human papillomavirus (HPV) vaccine: updated HPV vaccination recommendations of the advisory committee on immunization practices. MMWR Morb Mortal Wkly Rep 64:300–304

    PubMed  Google Scholar 

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We would like to thank Nabila Ristow and Monika Junk from the German National Reference Centre for Papilloma- and Polyomaviruses, University of Cologne, for their excellent technical assistance. We are also grateful to Klaus Jung, Ph.D., and his colleagues from the Department of Medical Statistics, University of Göttingen, for their valuable support in statistical analysis of the data. This study was presented in part as a poster at the 30th International Papillomavirus Conference, Lisbon, Portugal, 17–21 September 2015, in part as a talk at the 55th Interscience Conference on Antimicrobial Agents and Chemotherapy, San Diego, United States, 17–21 September 2015, and in part as a poster at the 26th Annual Meeting of the Society of Virology, Münster, Germany, 6–9 April 2016.

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Correspondence to Marco H. Schulze.

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The authors declare that they have no conflicts of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. The study was approved by the ethical committee of the University Medical Center Göttingen, Germany (number 14/10/11), and the authority of the St. Martin de Porres Hospital in Eikwe, Ghana.

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Informed consent was obtained from all individual participants included in the study.

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Marco H. Schulze and Fabian M. Völker have equally contributed to this work.

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Schulze, M.H., Völker, F.M., Lugert, R. et al. High prevalence of human papillomaviruses in Ghanaian pregnant women. Med Microbiol Immunol 205, 595–602 (2016).

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