Prevalence and Current Scenario of HPV in Pakistan: A Systematic Review and Meta-analysis

Sadia Minhas; Aneequa Sajjad; Rabia Mushtaq Chaudhry; Zobaria Rehman; Batool Syeda; Muhammad Kashif

doi:10.3889/oamjms.2022.9036

Authors

Sadia Minhas Department of Microbiology, University of Lahore, Lahore, Pakistan; Department of Oral Pathology, Akhtar Saeed Dental College, Lahore, Pakistan
Aneequa Sajjad Department of Oral Pathology, Akhtar Saeed Dental College, Lahore, Pakistan
Rabia Mushtaq Chaudhry Department of Oral Medicine, Akhtar Saeed Dental College, Lahore, Pakistan
Zobaria Rehman Center of Applied Molecular Biology, University of Punjab, Lahore, Pakistan
Batool Syeda Department of Community Medicine, Peoples University of Medical and Health Sciences, Nawabshah, Pakistan
Muhammad Kashif Department of Oral Pathology, Bakhtawar Amin Medical and Dental College, Multan, Pakistan

DOI:

https://doi.org/10.3889/oamjms.2022.9036

Keywords:

Human papillomavirus, Pakistan, Cervical cancer, Oral cancer, Prevalence

Abstract

AIM: The present study was designed to compile and screen data regarding HPV-related reported diseases to evaluate the status of HPV infection in Pakistan.

METHODS: The literature on the prevalence of HPV in Pakistan was searched in Google Scholar and other search engines using various keywords.

RESULTS: A total of 39 studies published from 2007 to 2018 were reviewed. About 7341 participants have been screened for HPV in Pakistan for the past 11 years, and according to this meta-analysis, the reported HPV prevalence was 23.1%. The highest HPV prevalence rate was observed among cervical cancer cases (80.4%) followed by normal cervical region (61.8%) and oral cancer (40.4%), respectively.

CONCLUSION: The high prevalence of HPV in Pakistan reflects the raised burden of HPV-associated diseases. The health-care system needs to be more organized in terms of awareness and screening programs, diagnosis, and treatment of the disease to reduce the burden of HPV in Pakistan.

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References

Markowitz LE, Dunne EF, Saraiya M, Chesson HW, Curtis CR, Gee J, et al. Human papillomavirus vaccination: Recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep. 2014;63(5):1-30. PMid:25167164

Milner DA. Diagnostic Pathology: Infectious Diseases E-Book. Amsterdam, The Netherlands: Elsevier Health Sciences; 2019.

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:F55-70. https://doi.org/10.1016/j.vaccine.2012.06.083 PMid:23199966 DOI: https://doi.org/10.1016/j.vaccine.2012.06.083

Ferris DG, Brown DR, Giuliano AR, Myers E, Joura EA, Garland SM, et al. Prevalence, incidence, and natural history of HPV infection in adult women ages 24 to 45 participating in a vaccine trial. Papillomavirus Res. 2020;10:100202. https://doi.org/10.1016/j.pvr.2020.100202 PMid:32464334 DOI: https://doi.org/10.1016/j.pvr.2020.100202

Kojima A, Maeda H, Sugita Y, Tanaka S, Kameyama Y. Human papillomavirus type 38 infection in oral squamous cell carcinomas. Oral Oncol. 2002;38(6):591-6. https://doi.org/10.1016/s1368-8375(01)00112-9 PMid:12167437 DOI: https://doi.org/10.1016/S1368-8375(01)00112-9

Stelzle D, Tanaka LF, Lee KK, Khalil AI, Baussano I, Shah AS, et al. Estimates of the global burden of cervical cancer associated with HIV. Lancet Glob Health. 2021;9(2):e161-9. https://doi.org/10.1016/S2214-109X(20)30459-9 PMid:33212031 DOI: https://doi.org/10.1016/S2214-109X(20)30459-9

De Martel C, Ferlay J, Franceschi S, Vignat J, Bray F, Forman D, et al. Global burden of cancers attributable to infections in 2008: A review and synthetic analysis. Lancet Oncol. 2012;13(6):607-15. https://doi.org/10.1016/S1470-2045(12)70137-7 PMid:22575588 DOI: https://doi.org/10.1016/S1470-2045(12)70137-7

de Martel C, Georges D, Bray F, Ferlay J, Clifford GM. Global burden of cancer attributable to infections in 2018: A worldwide incidence analysis. Lancet Glob Health. 2020;8(2):e180-90. https://doi.org/10.1016/S2214-109X(19)30488-7 PMid:31862245 DOI: https://doi.org/10.1016/S2214-109X(19)30488-7

Dempsey AF. Human papillomavirus: The usefulness of risk factors in determining who should get vaccinated. Rev Obstet Gynecol. 2008;1(3):122-8. PMid:19015763

Moher D, Liberati A, Tetzlaff J, Altman DG, PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. Int J Surg. 2010;8(5):336-41. https://doi.org/10.1016/j.ijsu.2010.02.007 PMid:20171303 DOI: https://doi.org/10.1016/j.ijsu.2010.02.007

Abdullah A, Qasim M, Shafiq M, Ijaz M, Parveen S, Murtaza S, et al. Molecular diagnosis and phylogenetic analysis of human papillomavirus type-16 from suspected patients in Pakistan. Infect Agent Cancer. 2016;11:1. https://doi.org/10.1186/s13027-016-0047-z PMid:26766963 DOI: https://doi.org/10.1186/s13027-016-0047-z

Aziz H, Iqbal H, Mahmood H, Fatima S, Faheem M, Sattar AA, et al. Human papillomavirus infection in females with normal cervical cytology: Genotyping and phylogenetic analysis among women in Punjab, Pakistan. Int J Infect Dis. 2018;66:83-9. https://doi.org/10.1016/j.ijid.2017.11.009 PMid:29138009 DOI: https://doi.org/10.1016/j.ijid.2017.11.009

Khan S, Noonari AA, Zehra F, Yousaf W, ul Huda N, Qureshi A. Prevalence of HPV in Pakistani women. Pathology. 2016;48:S133. DOI: https://doi.org/10.1016/j.pathol.2015.12.359

Raza S, Franceschi S, Pallardy S, Malik F, Avan B, Zafar A, et al. Human papillomavirus infection in women with and without cervical cancer in Karachi, Pakistan. Br J Cancer. 2010;102(11):1657-60. https://doi.org/10.1038/sj.bjc.6605664 PMid:20407442 DOI: https://doi.org/10.1038/sj.bjc.6605664

Shahid M, Kazmi SU, Rehman A, Ainuddin J, Furqan S, Nazeer S. Cervical cancer screening and HPV genotype distribution among asymptomatic patients of Karachi Pakistan. Pak J Med Sci. 2015;31(3):493-8. https://doi.org/10.12669/pjms.313.8004 PMid:26150831 DOI: https://doi.org/10.12669/pjms.313.8004

Akbar S, Pervez SN, Shah W. Manual liquid based cytology for Pap smear preparation and HPV detection by PCR in Pakistan. Asian Pac J Cancer Prev. 2015;16(2):579-83. https://doi.org/10.7314/apjcp.2015.16.2.579 PMid:25684490 DOI: https://doi.org/10.7314/APJCP.2015.16.2.579

Loya A, Serrano B, Rasheed F, Tous S, Hassan M, Clavero O, et al. Human Papillomavirus genotype distribution in invasive cervical cancer in Pakistan. Cancers (Basel). 2016;8(8):72. https://doi.org/10.3390/cancers8080072 PMid:27483322 DOI: https://doi.org/10.3390/cancers8080072

Saba K, Bukhari MH, Khaleel E, Imam SF, Zainab M, Siddiqa A, et al. Detection of HPV and its association with different known risk factors for neoplastic cervical lesions. Acta Med Int. 2015;2(2):92-9. DOI: https://doi.org/10.5530/ami.2015.3.9

Khan S, Jaffer NN, Khan MN, Rai MA, Shafiq M, Ali A, et al. Human papillomavirus subtype 16 is common in Pakistani women with cervical carcinoma. Int J Infect Dis. 2007;11(4):313-7. https://doi.org/10.1016/j.ijid.2006.06.007 PMid:17291804 DOI: https://doi.org/10.1016/j.ijid.2006.06.007

Gul S, Murad S, Javed A. Prevalence of high risk human papillomavirus in cervical dysplasia and cancer samples from twin cities in Pakistan. Int J Infect Dis. 2015;34:14-9. https://doi.org/10.1016/j.ijid.2015.02.018 PMid:25725135 DOI: https://doi.org/10.1016/j.ijid.2015.02.018

Siddiqa A, Zainab M, Qadri I, Bhatti MF, Parish JL. Prevalence and genotyping of high risk human papillomavirus in cervical cancer samples from Punjab, Pakistan. Viruses. 2014;6(7):2762-77. https://doi.org/10.3390/v6072762 PMid:25036463 DOI: https://doi.org/10.3390/v6072762

Yousuf S, Syed S, Moazzam A, Lucky MH. Frequency of high risk human papillomavirus types in squamous cell carcinoma of cervix among women. J Pak Med Assoc. 2010;60(3):193-6. PMid:20225776

Zahid A, Shakoori AR. Frequency of E6 and E7 Oncogenes of Human Papillomavirus Types 16 and 18 in Cervical Cancer Patients in Pakistani Women. Pak J Zool. 2016;48(6):1911-7.

Gichki AS, Buajeeb W, Doungudomdacha S, Khovidhunkit SP. Detection of human papillomavirus in normal oral cavity in a group of Pakistani subjects using real-time PCR. Asian Pac J Cancer Prev. 2012;13(5):2299-304. https://doi.org/10.7314/apjcp.2012.13.5.2299 PMid:22901210 DOI: https://doi.org/10.7314/APJCP.2012.13.5.2299

Baig S, Rubab Z, Arif MM, Lucky M. Chewable risk factors-Threatened oral cancer HPV’s Looming Epidemic in Pakistan. European J Biotechnol Biosci. 2015;3(1):39-45.

Khyani IA, Qureshi MA, Mirza T, Farooq MU. Salivary detection of human Papilloma virus 16 & 18 in pre-malignant and malignant lesions of oral cavity: Is it feasible in Pakistani context of Socio-Cultural Taboos? Pak J Med Sci. 2015;31(5):1104. https://doi.org/10.12669/pjms.315.7093 PMid:26648995 DOI: https://doi.org/10.12669/pjms.315.7093

Irshad F, Baig S, Syed S, Lucky MH. High risk HPV detected in oral cavity of children in a set population of Karachi. Int STD Res Rev. 2015;3(1):27-32. DOI: https://doi.org/10.9734/ISRR/2015/14841

Baig S, Zaman U, Lucky MH. Human papilloma virus 16/18: Fabricator of trouble in oral squamous cell carcinoma. Int J Infect Dis. 2018;69:115-9. https://doi.org/10.1016/j.ijid.2018.02.003 PMid:29432879 DOI: https://doi.org/10.1016/j.ijid.2018.02.003

Castillo A, Koriyama C, Higashi M, Anwar M, Bukhari MH, Carrascal E, et al. Human papillomavirus in upper digestive tract tumors from three countries. World J Gastroenterol. 2011;17(48):5295-304. https://doi.org/10.3748/wjg.v17.i48.5295 PMid:22219599 DOI: https://doi.org/10.3748/wjg.v17.i48.5295

Perveen F, Baig S, Ahmad F, Majeed N. Detecting human papillomavirus 6 & 11 in a set of Pakistani population. J Adv Med Med Res. 2016;17(9):1-9. https://doi.org/10.9734/BJMMR/2016/28578 DOI: https://doi.org/10.9734/BJMMR/2016/28578

Ali SA, Awan MS, Atif S, Ali N, Mirza Y. Correlation of human papillomavirus infection and clinical parameters with five-year survival in oral squamous cell carcinoma. J Laryngol Otol. 2018;132(7):628-35. https://doi.org/10.1017/S0022215118000361 PMid:29888686 DOI: https://doi.org/10.1017/S0022215118000361

Akram S, Shabbir A, Mirza T. Association of high risk human papilloma virus (HPV-16/18) with P16 protein in oral premalignant lesions and oral squamous cell carcinoma. Pak J Med Dent. 2019;9:4-11. DOI: https://doi.org/10.36283/PJMD8-4/002

Azhar J, Salahuddin S, Qadri I. The role of human papilloma virus in the development of oral squamous cell carcinoma in Pakistani population. Advances in Dentistry and Oral Health. 2018;9(5):27-34. DOI: https://doi.org/10.19080/ADOH.2018.10.555778

Kashif M, Sadia M, Romeeza T, Shah J, Nadeem A. PO-080 prevalence of human papilloma virus and its phylogenetic analysis in patients with head and neck squamous cell carcinoma in Pakistan. ESMO Open. 2018;3:A257. DOI: https://doi.org/10.1136/esmoopen-2018-EACR25.608

Awan MS, Irfan B, Zahid I, Mirza Y, Ali SA. Comparison of polymerase chain reaction and immunohistochemistry assays for analysing human papillomavirus infection in oral squamous cell carcinoma. J Clin Diagn Res. 2017;11(6):XC10-3. https://doi.org/10.7860/JCDR/2017/24742.10119 PMid:28764278 DOI: https://doi.org/10.7860/JCDR/2017/24742.10119

Naqvi SU, Khan S, Ahmed A, Lail A, Gul S, Ahmed S. Prevalence of EBV, CMV, and HPV in oral squamous cell carcinoma patients in the Pakistani population. J Med Virol. 2020;92(12):3880-83. https://doi.org/10.1002/jmv.25791 PMid:32219873 DOI: https://doi.org/10.1002/jmv.25791

Baig S, Lucky M, Qamar A, Ahmad F, Khan S, Ahmed W. et al. Human papilloma virus and oral lesions in gutka eating subjects in Karachi. J Coll Physicians Surg Pak. 2012;22(3):135-8. PMid:22414350

Tasneem M, Hassan M, Khan A, Arabdin M, Qamar MA. Frequency of human papilloma virus in patients with oesophageal squamous cell carcinoma in Khyber Pakhtunkhwa. J Pak Med Assoc. 2019;69(5):738-40. PMid:31105301

Ilahi NE, Anwar S, Noreen M, Hashmi SN, Murad S. Detection of human papillomavirus-16 DNA in archived clinical samples of breast and lung cancer patients from North Pakistan. J Cancer Res Clin Oncol. 2016;142(12):2497-502. https://doi.org/10.1007/s00432-016-2251-z PMid:27613186 DOI: https://doi.org/10.1007/s00432-016-2251-z

Naushad W, Surriya O, Sadia H. Prevalence of EBV, HPV and MMTV in Pakistani breast cancer patients: A possible etiological role of viruses in breast cancer. Infect Genet Evol. 2017;54:230-7. https://doi.org/10.1016/j.meegid.2017.07.010 PMid:28705719 DOI: https://doi.org/10.1016/j.meegid.2017.07.010

Bruni L, Barrionuevo-Rosas L, Albero G, Serrano B, Mena M, Gómez D, et al.. Human papillomavirus and related diseases in the world. Summary report 27 July 2017. Available from: http://www.hpvcentre.net/statistics/reports/XWX.pdf [Last accessed on 2022 May 20].

Laia B, Mireia D, Xavier C, Elena F, Xavier F, Selviade’S. Cervical human papilloma virus prevalence in 5 continents: Meta-analysis of 1 million women with normal cytological findings. J Infect Dis. 2010;202(12):1789-99. https://doi.org/10.1086/657321 PMid:21067372 DOI: https://doi.org/10.1086/657321

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. https://doi.org/10.1016/S1473-3099(07)70158-5 PMid:17597569 DOI: https://doi.org/10.1016/S1473-3099(07)70158-5

Trottier H, Franco EL. The epidemiology of genital human papillomavirus infection. Vaccine. 2006;24:S4-15. https://doi.org/10.1016/j.vaccine.2005.09.054 PMid:16406226 DOI: https://doi.org/10.1016/j.vaccine.2005.09.054

Partridge JM, Koutsky LA. Genital human papillomavirus infection in men. Lancet Infect Dis. 2006;6(1):21-31. https://doi.org/10.1016/S1473-3099(05)70323-6 PMid:16377531 DOI: https://doi.org/10.1016/S1473-3099(05)70323-6

Moreira ED Jr., Giuliano AR, Palefsky J, Flores CA, Goldstone S, Ferris D, et al. Incidence, clearance, and disease progression of genital human papillomavirus infection in heterosexual men. J Infect Dis. 2014;210(2):192-9. https://doi.org/10.1093/infdis/jiu077 PMid:24495910 DOI: https://doi.org/10.1093/infdis/jiu077

Ishibashi MA, Antunes JA, Aoki MF, Terreri RB, Silva RC, Cunha RF, et al. Human Papillomavirus infection in men residing in Brazil, Mexico, and the USA [Infección por Virus de Papiloma Humano en hombres de Brasil, México y EUA]. Salud Publica Mex. 2008;50(5):408-18. https://doi.org/10.1590/s0036-36342008000500014 PMid:18852938 DOI: https://doi.org/10.1590/S0036-36342008000500014

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. https://doi.org/10.1371/journal.pone.0229154 PMid:32084177 DOI: https://doi.org/10.1371/journal.pone.0229154

Clifford GM, Smith JS, Plummer M, Munoz N, Franceschi S. Human papillomavirus types in invasive cervical cancer worldwide: A meta-analysis. Br J Cancer. 2003;88(1):63-73. https://doi.org/10.1038/sj.bjc.6600688 PMid:12556961 DOI: https://doi.org/10.1038/sj.bjc.6600688

Tam S, Fu S, Xu L, Krause KJ, Lairson DR, Miao H, et al. The epidemiology of oral human papillomavirus infection in healthy populations: A systematic review and metaanalysis. Oral Oncol. 2018;82:91-9. https://doi.org/10.1016/j.oraloncology.2018.04.005 PMid:29909908 DOI: https://doi.org/10.1016/j.oraloncology.2018.04.005

Shaikh MH, McMillan NA, Johnson NW. HPV-associated head and neck cancers in the Asia Pacific: A critical literature review & meta-analysis. Cancer Epidemiol. 2015;39(6):923-38. https://doi.org/10.1016/j.canep.2015.09.013 PMid:26523982 DOI: https://doi.org/10.1016/j.canep.2015.09.013

Chaitanya NC, Allam NS, Babu DG, Waghray S, Badam R, Lavanya R. Systematic meta-analysis on association of human papilloma virus and oral cancer. J Cancer Res Ther. 2016;12(2):969-74. https://doi.org/10.4103/0973-1482.179098 PMid:27461683 DOI: https://doi.org/10.4103/0973-1482.179098

Jayaprakash V, Reid M, Hatton E, Merzianu M, Rigual N, Marshall J, et al. Human papillomavirus types 16 and 18 in epithelial dysplasia of oral cavity and oropharynx: A metaanalysis, 1985–2010. Oral Oncol. 2011;47(11):1048-54. https://doi.org/10.1016/j.oraloncology.2011.07.009 PMid:21816661 DOI: https://doi.org/10.1016/j.oraloncology.2011.07.009

de la Cour CD, Sperling CD, Belmonte F, Syrjänen S, Verdoodt F, Kjaer SK. Prevalence of human papillomavirus in oral epithelial dysplasia: Systematic review and meta-analysis. Head Neck. 2020;42(10):2975-84. https://doi.org/10.1002/hed.26330 PMid:32573035 DOI: https://doi.org/10.1002/hed.26330

Guo L, Liu S, Zhang S, Chen Q, Zhang M, Quan P, et al. Human papillomavirus-related esophageal cancer survival: A systematic review and meta-analysis. Medicine (Baltimore). 2016;95(46):e5318. https://doi.org/10.1097/MD.0000000000005318 PMid:27861358 DOI: https://doi.org/10.1097/MD.0000000000005318

Li X, Gao C, Yang Y, Zhou F, Li M, Jin Q, et al. Systematic review with meta-analysis: The association between human papillomavirus infection and oesophageal cancer. Aliment Pharmacol Ther. 2014;39(3):270-81. https://doi.org/10.1111/apt.12574 PMid:24308856 DOI: https://doi.org/10.1111/apt.12574

World Health Organization. International Agency for Research on Cancer. Globocan. 2020. Available from: https://gco.iarc.fr/today/data/factsheets/populations/586 -pakistan-fact-sheets.pdf. [Last accessed on 2021 Jul 12].

Aguayo F, Anwar M, Koriyama C, Castillo A, Sun Q, Morewaya J, et al. Human papillomavirus-16 presence and physical status in lung carcinomas from Asia. Infect Agent Cancer. 2010;5:20. https://doi.org/10.1186/1750-9378-5-20 PMid:21080966 DOI: https://doi.org/10.1186/1750-9378-5-20

Zhai K, Ding J, Shi HZ. HPV and lung cancer risk: A metaanalysis. J Clin Virol. 2015;63:84-90. https://doi.org/10.1016/j.jcv.2014.09.014 PMid:25315992 DOI: https://doi.org/10.1016/j.jcv.2014.09.014

Li N, Bi X, Zhang Y, Zhao P, Zheng T, Dai M. Human papillomavirus infection and sporadic breast carcinoma risk: A meta-analysis. Breast Cancer Res Treat. 2011;126(2):515-20. https://doi.org/10.1007/s10549-010-1128-0 PMid:20740311 DOI: https://doi.org/10.1007/s10549-010-1128-0

Bae JM, Kim EH. Human papillomavirus infection and risk of breast cancer: A meta-analysis of case-control studies. Infect Agent Cancer. 2016;11:14. https://doi.org/10.1186/s13027-016-0058-9 PMid:26981149 DOI: https://doi.org/10.1186/s13027-016-0058-9