Epidemiology of Human Papillomavirus (HPV) Infection among Iranian Women Identified with Cervical Infections: A Systematic Review and Meta-Analysis of National Data

Authors
M. Dadashi 1
M. Vaezjalali 1
F. Fallah 2
H. Goudarzi 1
M. J. Nasiri 1
P. Owlia 3
A. Hashemi 1
D. Darban-Sarokhalil 4
1 Department of Microbiology, School of Medicine, Shahid Beheshti University of Medical Sciences, Tehran, IR Iran
2 Pediatric Infections Research Center, Mofid Hospital, Shahid Beheshti University of Medical Sciences, Tehran, IR Iran
3 Molecular Microbiology Research Center, Shahed University, Tehran, IR Iran
4 Department of Microbiology, Faculty of Medicine, Iran University of Medical Sciences, Tehran, IR Iran
Abstract
Background: Human papillomavirus (HPV) is one of the most common causes of sexually transmitted disease (STD) in humans. HPV is associated with gynecologic malignancy and cervical cancer among women worldwide. In the current study we sought to determine the prevalence rate of HPV in Iranian women identified with cervical infections.
Materials and Methods: Prevalence rate of HPV in Iran was investigated from 2000-2016 using several databases including Medline, Web of Science, Embase, Google Scholar, Iranmedex, and Scientific Information Database. Statistical analysis was performed by Comprehensive Meta-Analysis (V2.2, Biostat) software. Random effects models were used by taking into account the possibility of the heterogeneity between the studies, which was tested through the Cochran’s Q-statistic.
Results: The meta-analyses showed that the prevalence rate of HPV infections was 38.6 % (95% CI, 27.9-50.5) among Iranian women with cervical infections. The further stratified analyses indicated that the prevalence rate of HPV was higher in the studies conducted during the 2000-2008 years.
Conclusion: The results of the present study underscore the need for further enforcement of STD control strategies in Iran. Establishing advanced diagnostic facilities for HPV, vaccination of high risk groups, and continuous monitoring of HPV are recommended for HPV prevention and control.

Keywords

1.    Vinodhini  K, Shanmughapriya S, Das BC, Natarajaseenivasan K. Prevalence and risk factors of HPV infection among women from various provinces of the world. Arch Gynecol Obstet. 2012; 285(3):771-7.
2.    Liu X, Zhang S, Ruan Q, Ji Y, Ma L, Zhang Y. Prevalence and type distribution of human papillomavirus in women with cervical lesions in Liaoning Province, China. Int J Gynecol Cancer. 2010; 20(1):147-53.
3.    Steben M, Duarte-Franco E. Human papillomavirus infection: epidemiology and pathophysiology. Gynecol Oncol. 2007; 107(2 Suppl 1):S2-5.
4.    De Sanjosé S, Diaz M, Castellsagué X, Clifford G, Bruni L, Muñoz N, et al. Worldwide prevalence and genotype distribution of cervical human papillomavirus DNA in women with normal cytology: a meta-analysis. Lancet Infect Dis. 2007; 7(7):453-9.
5.    Chen W, Zhang X, Molijn A, Jenkins D, Shi J-F, Quint W, et al. Human papillomavirus type-distribution in cervical cancer in China: the importance of HPV 16 and 18. Cancer Causes Control. 2009; 20(9):1705-13.
6.    Munoz N, Bosch F, De Sanjosé S, Vergara A, Del Moral A, Munoz M, et al. Risk factors for cervical intraepithelial neoplasia grade III/carcinoma in situ in Spain and Colombia. Cancer Epidemiol Biomarkers  Prev. 1993; 2(5):423-31.
7.    Muñoz N, Bosch FX, de Sanjosé S, Herrero R, Castellsagué X, Shah KV, et al. Epidemiologic classification of human papillomavirus types associated with cervical cancer. N Engl J Med. 2003; 348(6):518-27.
8.    Paul MP, Iannuzzi MC. Sarcoidosis and immunoligic lung. 2011.
9.    Zhao FH, Lewkowitz AK, Hu SY, Chen F, Li LY, Zhang QM, et al. Prevalence of human papillomavirus and cervical intraepithelial neoplasia in China: A pooled analysis of 17 population‐based studies. Int J cancer. 2012; 131(12):2929-38.
10.  Clifford G, Gallus S, Herrero R, Munoz N, Snijders P, Vaccarella S, et al. Worldwide distribution of human papillomavirus types in cytologically normal women in the International Agency for Research on Cancer HPV prevalence surveys: a pooled analysis. Lancet. 2005; 366(9490):991-8.
11.  Peto J, Gilham C, Deacon J, Taylor C, Evans C, Binns W, et al. Cervical HPV infection and neoplasia in a large population-based prospective study: the Manchester cohort. Br J Cancer. 2004; 91(5):942-53.
12.  Maucort-Boulch D, Franceschi S, Plummer M. International correlation between human papillomavirus prevalence and cervical cancer incidence. Cancer Epidemiol Biomarkers Prev. 2008; 17(3):717-20.
13.  Radojicic J, Zaravinos A, Spandidos DA, Agostini M, Bedin C, Pucciarelli S, et al. HPV, KRAS mutations, alcohol consumption and tobacco smoking effects on esophageal squamous-cell carcinoma carcinogenesis. Int J Biol Markers. 2012; 27(1):1-12.
14.  Parkin DM, Monteleone P, Maj M, Fusco M, Orazzo C, Kemali D, et al. The global health burden of infection-associated cancers in the year 2002. J Prev Med Public Health. 2001; 34(4):372-8.
15.  Nakashima K, Shigehara K, Kawaguchi S, Wakatsuki A, Kobori Y, Nakashima K, et al. Prevalence of human papillomavirus infection in the oropharynx and urine among sexually active men: a comparative study of infection by papillomavirus and other organisms, including Neisseria gonorrhoeae, Chlamydia trachomatis, Mycoplasma spp., and Ureaplasma spp. BMC Infect Dis. 2014; 14(1):43.
16.  Park H, Sim S-m, Lee G. The presence of Chlamydia is associated with increased leukocyte counts and pain severity in men with chronic pelvic pain syndrome. Urology. 2015; 85(3):574-9.
17.  Dadashi M, Eslami G, Ghalavand Z, Goudarzi H, Fallah F, Owlia P, et al. Prevalence of chlamydia trachomatis and mycoplasma genitalium in patients with benign and malignant ovarian cancer by nested PCR method. Novel Biomed. 2016; 4(1):18-23.
18.  Sankaranarayanan R, Qiao Y-l, Keita N. The next steps in cervical screening. Women Health. 2015; 11(2):201-12.
19.  León-Maldonado L, Wentzell E, Brown B, Allen-Leigh B, Torres-Ibarra L, Salmerón J, et al. Perceptions and experiences of human papillomavirus (HPV) infection and testing among low-income Mexican women. PloS One. 2016; 11(5):e0153367.
20.  Joura EA, Giuliano AR, Iversen O-E, Bouchard C, Mao C, Mehlsen J, et al. A 9-valent HPV vaccine against infection and intraepithelial neoplasia in women. N Engl J Med. 2015; 372(8):711-23.
21.  Printz C. FDA approves Gardasil 9 for more types of HPV. Cancer. 2015;121(8):1156-7.
22.  Bzhalava D, Eklund C, Dillner J. International standardization and classification of human papillomavirus types. Virology. 2015;476:341-4.
23.  Tjalma WA. There are two prophylactic human papillomavirus vaccines against cancer, and they are different. J Clin Oncol. 2015: 33(8):964-65.
24.  Delany-Moretlwe S, Cowan FM, Busza J, Bolton-Moore C, Kelley K, Fairlie L. Providing comprehensive health services for young key populations: needs, barriers and gaps. HIV and adolescents: focus on young key populations. J Int AIDS Soc. 2015:8(2 suppl1);19833.
25.  Owsianka B, Gańczak M. Evaluation of human papilloma virus (HPV) vaccination strategies and vaccination coverage in adolescent girls worldwide. Przegl Epidemiol. 2015; 69(1):53-8.
26.  Anttila M, Syrjänen S, Ji H, Saarikoski S, Syrjänen K. Failure to demonstrate human papillomavirus DNA in epithelial ovarian cancer by general primer PCR. Gynecol Oncol. 1999;72(3):337-41.
27.  Atalay F, Taskiran C, Taner MZ, Pak I, Or M, Tuncer S. Detection of human papillomavirus DNA and genotyping in patients with epithelial ovarian carcinoma. J Obstet Gynaecol Res. 2007; 33(6):823-8.
28.  Idahl A, Lundin E, Elgh F, Jurstrand M, Møller JK, Marklund I, et al. Chlamydia trachomatis, Mycoplasma genitalium, Neisseria gonorrhoeae, human papillomavirus, and polyomavirus are not detectable in human tissue with epithelial ovarian cancer, borderline tumor, or benign conditions. Am J Obstet Gynecol. 2010; 202(1):71. e1-. e6.
29.  Rosa MI, Silva GD, de Azedo Simões PWT, Souza MV, Panatto APR, Simon CS, et al. The prevalence of human papillomavirus in ovarian cancer: a systematic review. Int J Gynecol Cancer. 2013; 23(3):437-41.
30.  Allameh T, Moghim S, Asadi-Zeidabadi M. A survey on the prevalence of high-risk subtypes of human papilloma virus among women with cervical neoplasia in Isfahan University of Medical Science. Arch Gynecol Obstet. 2011; 284(6):1509-13.
31.  Eslami G, Golshani M, Rakhshan M, Fallah F, Goudarzi H, Taghavi A. PCR detection and high risk typing of human papillomavirus DNA in cervical cancer in Iranian women. Cancer Ther. 2008;6:361-6.
32.  Esmaeili M, Bonyadi M, Dastranj A, Alizadeh M, Melli MS, Shobeiri MJ. HPV typing in women with cervical precancerous and cancerous lesions in northwestern Iran. Gynecol obstet invest. 2008;66(1):68-72.
33.  Ghaffari SR, Sabokbar T, Mollahajian H, Dastan J, Ramezanzadeh F, Ensani F, et al. Prevalence of human papillomavirus genotypes in women with normal and abnormal cervical cytology in Iran. Asian Pac J Cancer Prev. 2006;7(4):529-32.
34.  Hamkar R, Azad TM, Mahmoodi M, Seyedirashti S, Severini A, Nategh R. Prevalence of human papillomavirus in Mazandaran province, Islamic Republic of Iran. East Mediterr Health J. 2002; 8(6):805-11.
35. 
Esmaeili M, Bonyadi M, Dastranj A, Alizadeh M, Melli M, S, Shobeiri M, J, HPV Typing in Women with Cervical Precancerous and Cancerous Lesions in Northwestern Iran. Gynecol Obstet Invest 2008;66:68-72
36.  Maleknejad P, Rakhshan M, Kazemi B, Farokh F, Shahsava S. Detection of human papilomavirus types 16 and 18 in pathologic samples from patients with cervical cancer by PCR and RFLP methods. DARU J Pharm Sci. 2006; 14(2):78-81.
37.  Mortazavi S, Zali M, Raoufi M, Nadji M, Kowsarian P, Nowroozi A. The prevalence of human papillomavirus in cervical cancer in Iran. Asian Pac J Cancer Prev. 2002;3(1):69-72.
38.  Safaei A, Khanlari M, Momtahen M, Monabati A, Robati M, Amooei S, et al. Prevalence of high-risk human papillomavirus types 16 and 18 in healthy women with cytologically negative pap smear in Iran. Indian J Pathol Microbiol. 2010; 53(4):681.
39.  Shahramian I, Heidari Z, Mahmoudzadeh-Sagheb H, Moradi A, Forghani F. Prevalence of HPV Infection and high risk HPV genotypes (16, 18), among monogamous and polygamous women, In Zabol, Iran. Iran J Public Health. 2011; 40(3):113-121.
40.  Shahsiah R, Khademalhosseini M, Mehrdad N, Ramezani F, Nadji SA. Human papillomavirus genotypes in Iranian patients with cervical cancer. Pathol Res Pract. 2011; 207(12):754-7.
41.  Zavarei MJZJ, Hamkar R, Dana VG, Delforoosh M, Shojamoradi M, Gilani MM. Prevalence of HPV infection and its association with cytological abnormalities of Pap smears in Tehran. Iran J Public Health. 2008; 37(3):101-6.
42.  Eghbali M, Sadeghi F, Mirinargesi M, Mohseni R. Frequency of human papillomavirus among pregnant women by PCR technique. Int J Mol Clin Microbiol. 2013; 2:285-8.
43.  Haghshenas M, Golini-Moghaddam T, Rafiei A, Emadeian O, Shykhpour A, Ashrafi GH. Prevalence and type distribution of high-risk human papillomavirus in patients with cervical cancer: a population-based study. Infect Agent Cancer. 2013; 8(1):20.
44.  Hamidi-Fard M, Fattahi-Abdizadeh M, Makvandi M, Ranjbari N, Mansoori E, Samarbaf-Zadeh A. Detection and genotyping of human papillomavirus in cervical tissue samples in Ahvaz, Southwest Iran. Jundishapur J Microbiol. 2013;6(7): e4569.
45.  Khodakarami N, Clifford GM, Yavari P, Farzaneh F, Salehpour S, Broutet N, et al. Human papillomavirus infection in women with and without cervical cancer in Tehran, Iran. Int J Cancer. 2012; 131(2):E156-61.
46.  Mahmoodi P, Motamedi H, Shapouri MRSA, Shehni MB, Kargar M. Molecular detection and typing of human papillomaviruses in paraffin-embedded cervical cancer and pre-cancer tissue specimens. Iran J Cancer Prev. 2016;9(1): e3752.
47.  Moradi A, Nosrat SB, Besharat S. Molecular epidemiology of high-risk types of human papillomaviruses (16, 18) in pap-smear, the North East of Iran. Iran J Cancer Prev. 2011;4(3):135-40.
48.  Salehi-Vaziri M, Sadeghi F, Hashemi FS, Haeri H, Bokharaei-Salim F, Monavari SH, et al. Distribution of human papillomavirus genotypes in Iranian women according to the severity of the cervical Llsion. Iran Red Crescent Med J. 2016; 18(4): e24458.
49.  Shafaghi B, Jarollahi A, Yousefzadeh B, Ameri A, Moghadam S, Mostafavi M. Human papilloma virus prevalence and types among Iranian women attending regular gynecological visits. Rep Radiother Oncol. 2013;1(2).
50.  Piroozmand A, Mostafavi Zadeh SM, Niakan M, Madani A, Soleimani R, Nedaeinia R, et al. The association of high risk human papillomaviruses in patients with cervical cancer: an evidence based study on patients with squamous cell dysplasia or carcinoma for evaluation of 23 human papilloma virus genotypes. Cervical Cancer. 2016; 17; 9(4):e32728..
51.  Zandi K, Eghbali SS, Hamkar R, Ahmadi S, Deilami I, Nejad HA, et al. Prevalence of various human papillomavirus (HPV) genotypes among women who subjected to routine pap smear test in Bushehr city (South west of Iran) 2008-2009. Virol J. 2010;7(1):65.