Distribution of human papillomavirus genotypes in suspected women cytological specimens from Tehran, Iran
-
Alireza Tabibzadeh
,
Mahshid Panahi
,
Behnaz Bouzari
,
Mohammad Taghi Haghi Ashtiani
,
Farhad Zamani
,
Hadi Teimoori Arzati
,
Mohammad Hadi Karbalaie Niya
Abstract
Background and Objectives: The human papillomavirus (HPV) is associated with more than 70% of the cervical neoplasm. The current study aims to evaluate the distribution of HPV genotypes in suspected women cytological specimens from Tehran, Iran.
Materials and Methods: In the current cross-sectional study, HPV genotype prevalence was investigated in 433 subject women. DNA extraction was performed by High Pure Viral Nucleic Acid kit. A semi-automatically hybriSpot 24™ (HS24) setting was used for HPV typing and data interpreted by hybriSoft™ software according to instructions.
Results: Pathologic data showed 181 (41.8%) had non-malignant lesions, 212 (49%) had inflammation and 40 (9.2%) reported LSIL in primary Pap-smear result. HPV was found in 143 (33%) specimens and the most comment high-risk and low-risk HPV types were HPV-16 and -6, respectively. Also, 62 (43%) were co-infected with multiple genotypes includes, 34 (24%) cases had co-infection with two HPV types, 17 (12%) cases had co-infection with three HPV types, 6 (4%) cases had co-infection with four HPV types and 5 (3%) cases had co-infection with five HPV types. There was statistically different domination on high-risk genotype in most of the co-infected samples (p<0.01).
Conclusion: Current study indicates that the lesion pathology assessment was significantly associated with the HPV infection (p<0.01). Furthermore, the age group assessment shows that most of the HPV positive cases were 21 to 40 (p<0.01). The HPV infection prevalence in the current study was 33% and the most frequently reported high-risk and low-risk HPV types were 16 and 6, respectively.
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3. Alam TM, Khan MM, Iqbal MA, Abdul W, Mushtaq M. Cervical cancer prediction through different screening methods using data mining. Int J Adv Comput Sci Appl 2019;10:388-396.
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6. Burchell AN, Winer RL, de Sanjosé S, Franco EL. Chapter6: Epidemiology and transmission dynamics of genital HPV infection. Vaccine 2006;24 Suppl 3:S3/52-61.
7. Roberts JN, Buck CB, Thompson CD, Kines R, Bernardo M, Choyke PL, et al. Genital transmission of HPV in a mouse model is potentiated by nonoxynol-9 and inhibited by carrageenan. Nat Med 2007;13:857-861.
8. Baseman JG, Koutsky LA. The epidemiology of human papillomavirus infections. J Clin Virol 2005;32 Suppl 1:S16-24.
9. Moscicki AB, Schiffman M, Burchell A, Albero G, Giuliano AR, Goodman MT, et al. Updating the natural history of human papillomavirus and anogenital cancers. Vaccine 2012;30 Suppl 5(0 5):F24-F33.
10. Bouvard V, Baan R, Straif K, Grosse Y, Secretan B, El Ghissassi F, et al. A review of human carcinogens--part B: biological agents. Lancet Oncol 2009;10:321-322.
11. Cogliano V, Baan R, Straif K, Grosse Y, Secretan B, El Ghissassi F, et al. Carcinogenicity of human papillomaviruses. Lancet Oncol 2005;6:204.
12. Doorbar J, Quint W, Banks L, Bravo IG, Stoler M, Broker TR, et al. The biology and life-cycle of human papillomaviruses. Vaccine 2012;30 Suppl 5:F55-F70.
13. 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;348:518-527.
14. Bulkmans NW, Berkhof J, Bulk S, Bleeker MC, van Kemenade FJ, Rozendaal L, et al. High-risk HPV type-specific clearance rates in cervical screening. Br J Cancer 2007;96:1419-1424.
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16. Cutts FT, Franceschi S, Goldie S, Castellsague Xd, de Sanjose S, Garnett G, et al. Human papillomavirus and HPV vaccines: a review. Bull World Health Organ 2007;85:719-726.
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18. Zhai L, Tumban E. Gardasil-9: A global survey of projected efficacy. Antiviral Res 2016;130:101-109.
19. Piñeros M, Saraiya M, Baussano I, Bonjour M, Chao A, Bray F. The role and utility of population-based cancer registries in cervical cancer surveillance and control. Prev Med 2021;144:106237.
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21. Arbyn M, Ronco G, Anttila A, Meijer CJ, Poljak M, Ogilvie G, et al. Evidence regarding human papillomavirus testing in secondary prevention of cervical cancer. Vaccine 2012;30 Suppl 5:F88-F99.
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23. Sasieni PD, Cuzick J, Lynch-Farmery E. Estimating the efficacy of screening by auditing smear histories of women with and without cervical cancer. The National Co-ordinating Network for Cervical Screening Working Group. Br J Cancer 1996;73:1001-1005.
24. 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 lesion. Iran Red Crescent Med J 2016;18(4):e24458.
25. Salehi-Vaziri M, Sadeghi F, Alamsi-Hashiani A, Haeri H, Monavari SH, Keyvani H. Merkel cell polyomavirus and human papillomavirus infections in cervical disease in Iranian women. Arch Virol 2015;160:1181-1187.
26. Kavita SN, Shefali M. Visual inspection of cervix with acetic acid (VIA) in early diagnosis of cervical intraepithelial neoplasia (CIN) and early cancer cervix. J Obstet Gynaecol India 2010;60:55-60.
27. Liu L, Wang D, Dong H, Jin C, Jiang L, Song H, et al. Characteristics of carcinogenic HPV genotypes in North China plain and the association with cervical lesions. Medicine (Baltimore) 2019;98(37):e17087.
28. Liao G, Jiang X, She B, Tang H, Wang Z, Zhou H, et al. Multi-infection patterns and co-infection preference of 27 human Papillomavirus types among 137,943 gynecological outpatients across China. Front Oncol 2020;10:449.
29. Brant AC, Menezes AN, Felix SP, Almeida LM, Moreira MAM. Preferential expression of a HPV genotype in invasive cervical carcinomas infected by multiple genotypes. Genomics 2020;112:2942-2948.
30. Colpani V, Soares Falcetta F, Bacelo Bidinotto A, Kops NL, Falavigna M, Serpa Hammes L,, et al. Prevalence of human papillomavirus (HPV) in Brazil: A systematic review and meta-analysis. PLoS One 2020;15(2):e0229154.
31. Wang J, Tang D, Wang K, Wang J, Zhang Z, Chen Y, et al. HPV genotype prevalence and distribution during 2009–2018 in Xinjiang, China: Baseline surveys prior to mass HPV vaccination. BMC Womens Health 2019;19:90.
32. Wheeler CM, Hunt WC, Joste NE, Key CR, Quint WG, Castle PE. Human papillomavirus genotype distributions: implications for vaccination and cancer screening in the United States. J Natl Cancer Inst 2009;101:475-487.
33. Zhu B, Liu Y, Zuo T, Cui X, Li M, Zhang J, et al. The prevalence, trends, and geographical distribution of human papillomavirus infection in China: The pooled analysis of 1.7 million women. Cancer Med 2019;8:5373-5385.
34. Denny L, Adewole I, Anorlu R, Dreyer G, Moodley M, Smith T, et al. Human papillomavirus prevalence and type distribution in invasive cervical cancer in sub‐Saharan Africa. Int J Cancer 2014;134:1389-1398.
35. Iljazović E, Mena M, Tous S, Alemany L, Omeragić F, Sadiković A, et al. Human papillomavirus genotype distribution in invasive cervical cancer in Bosnia and Herzegovina. Cancer Epidemiol 2014;38:504-510.
36. Horn J, Denecke A, Luyten A, Rothe B, Reinecke-Lüthge A, Mikolajczyk R, et al. Reduction of cervical cancer incidence within a primary HPV screening pilot project (WOLPHSCREEN) in Wolfsburg, Germany. Br J Cancer 2019;120:1015-1022.
37. Leite KRM, Pimenta R, Canavez J, Canavez F, de Souza FR, Vara L, et al. HPV genotype prevalence and success of vaccination to prevent cervical cancer. Acta Cytologica 2020;64:420-424.
38. Shetty RS, Pi RP, Kamath VG, Manjunath AP. Screening for pre-malignant lesions of the cervix among rural women in Southern India. Indian J Res Rep Med Sci 2011;1:1-6.
39. Nayar R, Wilbur DC. The bethesda system for reporting cervical cytology: a historical perspective. Acta
Cytol 2017;61:359-372.
40. Ndifon CO, Al-Eyd G. Atypical squamous cells of undetermined significance (ASCUS). StatPearls [Internet]: StatPearls Publishing; 2020.
41. Serrano B, de Sanjose S, Tous S, Quiros B, Munoz N, Bosch X, et al. Human papillomavirus genotype attribution for HPVs 6, 11, 16, 18, 31, 33, 45, 52 and 58 in female anogenital lesions. Eur J Cancer 2015;51:1732-1741.
42. Kim N, Park JS, Kim JE, Park JH, Park H, Roh EY, et al. Fifteen new nucleotide substitutions in variants of human papillomavirus 18 in Korea: Korean HPV18 variants and clinical manifestation. Virol J 2020;17:70.
2. McCredie MR, Sharples KJ, Paul C, Baranyai J, Medley G, Jones RW, et al. Natural history of cervical neoplasia and risk of invasive cancer in women with cervical intraepithelial neoplasia 3: a retrospective cohort study. Lancet Oncol 2008;9:425-434.
3. Alam TM, Khan MM, Iqbal MA, Abdul W, Mushtaq M. Cervical cancer prediction through different screening methods using data mining. Int J Adv Comput Sci Appl 2019;10:388-396.
4. Bosch FX, Lorincz A, Muñoz N, Meijer CJ, Shah KV. The causal relation between human papillomavirus and cervical cancer. J Clin Pathol 2002;55:244-265.
5. Smith JS, Lindsay L, Hoots B, Keys J, Franceschi S, Winer R, et al. Human papillomavirus type distribution in invasive cervical cancer and high‐grade cervical lesions: a meta‐analysis update. Int J Cancer 2007;121:621-632.
6. Burchell AN, Winer RL, de Sanjosé S, Franco EL. Chapter6: Epidemiology and transmission dynamics of genital HPV infection. Vaccine 2006;24 Suppl 3:S3/52-61.
7. Roberts JN, Buck CB, Thompson CD, Kines R, Bernardo M, Choyke PL, et al. Genital transmission of HPV in a mouse model is potentiated by nonoxynol-9 and inhibited by carrageenan. Nat Med 2007;13:857-861.
8. Baseman JG, Koutsky LA. The epidemiology of human papillomavirus infections. J Clin Virol 2005;32 Suppl 1:S16-24.
9. Moscicki AB, Schiffman M, Burchell A, Albero G, Giuliano AR, Goodman MT, et al. Updating the natural history of human papillomavirus and anogenital cancers. Vaccine 2012;30 Suppl 5(0 5):F24-F33.
10. Bouvard V, Baan R, Straif K, Grosse Y, Secretan B, El Ghissassi F, et al. A review of human carcinogens--part B: biological agents. Lancet Oncol 2009;10:321-322.
11. Cogliano V, Baan R, Straif K, Grosse Y, Secretan B, El Ghissassi F, et al. Carcinogenicity of human papillomaviruses. Lancet Oncol 2005;6:204.
12. Doorbar J, Quint W, Banks L, Bravo IG, Stoler M, Broker TR, et al. The biology and life-cycle of human papillomaviruses. Vaccine 2012;30 Suppl 5:F55-F70.
13. 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;348:518-527.
14. Bulkmans NW, Berkhof J, Bulk S, Bleeker MC, van Kemenade FJ, Rozendaal L, et al. High-risk HPV type-specific clearance rates in cervical screening. Br J Cancer 2007;96:1419-1424.
15. Bulkmans NW, Berkhof J, Rozendaal L, van Kemenade FJ, Boeke AJ, Bulk S, et al. Human papillomavirus DNA testing for the detection of cervical intraepithelial neoplasia grade 3 and cancer: 5-year follow-up of a randomised controlled implementation trial. Lancet 2007;370:1764-1772.
16. Cutts FT, Franceschi S, Goldie S, Castellsague Xd, de Sanjose S, Garnett G, et al. Human papillomavirus and HPV vaccines: a review. Bull World Health Organ 2007;85:719-726.
17. Schiller JT, Castellsagué X, Garland SM. A review of clinical trials of human papillomavirus prophylactic vaccines. Vaccine 2012;30 Suppl 5(0 5):F123-F138.
18. Zhai L, Tumban E. Gardasil-9: A global survey of projected efficacy. Antiviral Res 2016;130:101-109.
19. Piñeros M, Saraiya M, Baussano I, Bonjour M, Chao A, Bray F. The role and utility of population-based cancer registries in cervical cancer surveillance and control. Prev Med 2021;144:106237.
20. Arbyn M, Buntinx F, Van Ranst M, Paraskevaidis E, Martin-Hirsch P, Dillner J. Virologic versus cytologic triage of women with equivocal Pap smears: a meta-analysis of the accuracy to detect high-grade intraepithelial neoplasia. J Natl Cancer Inst 2004;96:280-293.
21. Arbyn M, Ronco G, Anttila A, Meijer CJ, Poljak M, Ogilvie G, et al. Evidence regarding human papillomavirus testing in secondary prevention of cervical cancer. Vaccine 2012;30 Suppl 5:F88-F99.
22. Das CR, Mahanta LB, Borah H, Hussain E, Devi A, Choudhury M, et al. A study on epidemiological factors and its association with pathological findings for precancerous symptoms of cervical cancer. Indian J Public Health Res Dev 2019;10:592-597.
23. Sasieni PD, Cuzick J, Lynch-Farmery E. Estimating the efficacy of screening by auditing smear histories of women with and without cervical cancer. The National Co-ordinating Network for Cervical Screening Working Group. Br J Cancer 1996;73:1001-1005.
24. 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 lesion. Iran Red Crescent Med J 2016;18(4):e24458.
25. Salehi-Vaziri M, Sadeghi F, Alamsi-Hashiani A, Haeri H, Monavari SH, Keyvani H. Merkel cell polyomavirus and human papillomavirus infections in cervical disease in Iranian women. Arch Virol 2015;160:1181-1187.
26. Kavita SN, Shefali M. Visual inspection of cervix with acetic acid (VIA) in early diagnosis of cervical intraepithelial neoplasia (CIN) and early cancer cervix. J Obstet Gynaecol India 2010;60:55-60.
27. Liu L, Wang D, Dong H, Jin C, Jiang L, Song H, et al. Characteristics of carcinogenic HPV genotypes in North China plain and the association with cervical lesions. Medicine (Baltimore) 2019;98(37):e17087.
28. Liao G, Jiang X, She B, Tang H, Wang Z, Zhou H, et al. Multi-infection patterns and co-infection preference of 27 human Papillomavirus types among 137,943 gynecological outpatients across China. Front Oncol 2020;10:449.
29. Brant AC, Menezes AN, Felix SP, Almeida LM, Moreira MAM. Preferential expression of a HPV genotype in invasive cervical carcinomas infected by multiple genotypes. Genomics 2020;112:2942-2948.
30. Colpani V, Soares Falcetta F, Bacelo Bidinotto A, Kops NL, Falavigna M, Serpa Hammes L,, et al. Prevalence of human papillomavirus (HPV) in Brazil: A systematic review and meta-analysis. PLoS One 2020;15(2):e0229154.
31. Wang J, Tang D, Wang K, Wang J, Zhang Z, Chen Y, et al. HPV genotype prevalence and distribution during 2009–2018 in Xinjiang, China: Baseline surveys prior to mass HPV vaccination. BMC Womens Health 2019;19:90.
32. Wheeler CM, Hunt WC, Joste NE, Key CR, Quint WG, Castle PE. Human papillomavirus genotype distributions: implications for vaccination and cancer screening in the United States. J Natl Cancer Inst 2009;101:475-487.
33. Zhu B, Liu Y, Zuo T, Cui X, Li M, Zhang J, et al. The prevalence, trends, and geographical distribution of human papillomavirus infection in China: The pooled analysis of 1.7 million women. Cancer Med 2019;8:5373-5385.
34. Denny L, Adewole I, Anorlu R, Dreyer G, Moodley M, Smith T, et al. Human papillomavirus prevalence and type distribution in invasive cervical cancer in sub‐Saharan Africa. Int J Cancer 2014;134:1389-1398.
35. Iljazović E, Mena M, Tous S, Alemany L, Omeragić F, Sadiković A, et al. Human papillomavirus genotype distribution in invasive cervical cancer in Bosnia and Herzegovina. Cancer Epidemiol 2014;38:504-510.
36. Horn J, Denecke A, Luyten A, Rothe B, Reinecke-Lüthge A, Mikolajczyk R, et al. Reduction of cervical cancer incidence within a primary HPV screening pilot project (WOLPHSCREEN) in Wolfsburg, Germany. Br J Cancer 2019;120:1015-1022.
37. Leite KRM, Pimenta R, Canavez J, Canavez F, de Souza FR, Vara L, et al. HPV genotype prevalence and success of vaccination to prevent cervical cancer. Acta Cytologica 2020;64:420-424.
38. Shetty RS, Pi RP, Kamath VG, Manjunath AP. Screening for pre-malignant lesions of the cervix among rural women in Southern India. Indian J Res Rep Med Sci 2011;1:1-6.
39. Nayar R, Wilbur DC. The bethesda system for reporting cervical cytology: a historical perspective. Acta
Cytol 2017;61:359-372.
40. Ndifon CO, Al-Eyd G. Atypical squamous cells of undetermined significance (ASCUS). StatPearls [Internet]: StatPearls Publishing; 2020.
41. Serrano B, de Sanjose S, Tous S, Quiros B, Munoz N, Bosch X, et al. Human papillomavirus genotype attribution for HPVs 6, 11, 16, 18, 31, 33, 45, 52 and 58 in female anogenital lesions. Eur J Cancer 2015;51:1732-1741.
42. Kim N, Park JS, Kim JE, Park JH, Park H, Roh EY, et al. Fifteen new nucleotide substitutions in variants of human papillomavirus 18 in Korea: Korean HPV18 variants and clinical manifestation. Virol J 2020;17:70.
| Files | ||
| Issue | Vol 14 No 1 (2022) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v14i1.8812 | |
| Keywords | ||
| Human papillomavirus (HPV); Papillomavirus infections; Uterine cervical neoplasms; In situ hybridization; Co-infection; LSIL | ||
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Tabibzadeh A, Panahi M, Bouzari B, Haghi Ashtiani MT, Zamani F, Teimoori Arzati H, Karbalaie Niya MH. Distribution of human papillomavirus genotypes in suspected women cytological specimens from Tehran, Iran. Iran J Microbiol. 2022;14(1):112-118.
