Profile of human papillomavirus genotypes in breast and oesophageal cancer patients in Pretoria, South Africa
DOI:
https://doi.org/10.7196/SAMJ.2023.v113i7.560Keywords:
breast carcinoma, oesophagus carcinoma, multiple HPV genotypes, expanded HPV vaccineAbstract
Background. The association between human papillomavirus (HPV) and cervical cancer is well established, and cervical cancer can be prevented through HPV vaccination. Little has been reported on the association between HPV and breast carcinoma (BC) or oesophageal squamous cell carcinoma (OSCC) in Africa. It is possible that use of appropriate HPV vaccines against genotypes responsible for these cancers may also prevent their development.
Objectives. To investigate HPV genotype prevalence in BC and OSCC patients in Pretoria, South Africa (SA).
Methods. A retrospective cross‐sectional study of BC and OSCC patients managed at Steve Biko Academic Hospital from 2015 to 2019 was undertaken. Patient medical records were analysed, and DNA was extracted from their archived pathology material and amplified by polymerase chain reaction before hybridisation for HPV genotypes.
Results. There were 101 patients with BC and 50 with OSCC. The prevalence of HPV infection in BC patients was 77.2%, with 35.6% high‐ risk (HR) genotypes, and that in OSCC patients 90.0%, with 56.0% HR genotypes. The most prevalent HPV genotypes (>20% each) were HPV 16, 70 and 51 for BC and HPV 51, 70, 16 and 82 for OSCC, with 31.7% and 60.0% of patients, respectively, having co‐infection with ≥2 genotypes.
Conclusion. The high prevalence of infection with multiple HPV genotypes in BC and OSCC patients, with HPV 16, 51, 70, 35 and 82 the most common genotypes in these cancers, warrants expansion of the current SA bivalent HPV 16/18 vaccine for girls to include boys, and inclusion of HPV 51, 70, 35 and 82, in order to prevent BC and OSCC as well as cervical cancer.
References
Bray F, Ferlay J, Soerjomataram I, Seigel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2018;68(6):394‐424. https://doi.org/10.3322/caac.21492
Fitzmaurice C, Abate D, Abbasi N, et al. Global, regional, and national cancer incidence, mortality, years of life lost, years lived with disability, and disability‐adjusted life‐years for 29 cancer groups, 1990 to 2017: A systematic analysis for the global burden of disease study. JAMA Oncol 2019;5(12):1749‐ 1768. https://doi.org/10.1001/jamaoncol.2019.2996
Burd EM. Human papillomavirus and cervical cancer. Clin Microbiol Rev 2003;16(1):1‐17. https://doi. org/10.1128/CMR.16.1.1‐17.2003
Forman D, de Martel C, Lacey CJ, et al. Global burden of human papillomavirus and related diseases. Vaccine 2012;30 Suppl 5:F12‐F23. https://doi.org/10.1016/j.vaccine.2012.07.055
Li N, Bi X, Zhang Y, Zhao P, Zheng T, Dai N. Human papillomavirus infection and sporadic breast carcinoma risk: A meta‐analysis. Breast Cancer Res Treat 2011;126(2):515‐520. https://doi. org/10.1007/s10549‐010‐1128‐0
Bae J‐M, 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/1186/s13027‐016‐0058‐9
Kan C‐Y, Iacopetta BJ, Lawson JS, Whitaker NJ. Identification of human papillomavirus DNA gene sequences in human breast cancer. Br J Cancer 2005;93(8):946‐948. https://doi.org/10.1038/ sj.bjc.6602778
WredeD,LuqmaniYA,CoombesRC,VousdenKH.AbsenceofHPV16and18DNAinbreastcancer. Br J Cancer 1992;65(6):891‐894. https://doi.org/10.1038/bjc.1992.186
Zhou Y, Li J, Ji Y, et al. Inconclusive role of human papillomavirus infection in breast cancer. Infect Agent Cancer 2015;10:36. https://doi.org/10.1186/s13027‐015‐0029‐6
Bonlokke S, Blaakaer J, Steiniche T, et al. Evidence of no association between human papillomavirus and breast cancer. Front Oncol 2018;8:209. https://doi.org/10.3389/fonc.2018.00209
Livanage SS, Rahman B, Ridda I, et al. The aetiological role of human papillomavirus in oesophageal squamous cell carcinoma: A meta‐analysis. PLoS ONE 2013;8(7):e69238. https://doi.org/10.1371/ journal.pone.0069238
Rajendra S, Pavey D, McKay O, Merrett N, Gautam SD. Human papillomavirus infection in esophageal squamous cell carcinoma and esophageal adenocarcinoma: A concise review. Ann N Y Acad Sci 2020;1482(1):36‐48. https://doi.org/10.1111/nyas.14509
Sur M, Cooper K. The role of the human papillomavirus in esophageal cancer. Pathology 1998;30(4):348‐354. https://doi.org/10.1080/00313029800169616
Petrik JL, Wyss AB, Butler AM, et al. Prevalence of human papillomavirus among oesophageal squamous cell carcinoma cases: Systematic review and meta‐analysis. Br J Cancer 2014;110(9):2369‐ 2377. https://doi.org/10.1038/bjc.2014.96
Zhang S‐K, Guo L‐W, Chen Q, et al. The association between human papillomavirus 16 and esophageal cancer in Chinese population: A meta‐analysis. BMC Cancer 2015;15:99. https://doi.org/10.1186/ s12885‐015‐1096‐1
Mohammadpour B, Rouhi S, Khodabandehloo M, Moradi M. Prevalence and association of human papillomavirus with esophageal squamous cell carcinoma in Iran: A systematic review and meta‐ analysis. Iran J Public Health 2019;48(7):1215‐1226.
Li X, Gao C, Yang Y, et al. Systematic review with meta‐analysis: The association between human papillomavirus infection and oesophageal cancer. Aliment Pharmacol Ther 2014;39(3):270‐281. https://doi.org/10.1111/apt.12574
Alsop BR, Sharma P. Esophageal cancer. Gastroenterol Clin North Am 2016;45(3):399‐415. https:// doi.org/10.1016/j.gtc.04.001
Feller L, Wood NH, Khammissa RAG, Lemmer J. Human papillomavirus‐mediated carcinogenesis and HPV‐associated oral and oropharyngeal squamous cell carcinoma. Part 1: Human papillomavirus‐ mediated carcinogenesis. Head Face Med 2010;6:14. https://doi.org/10.1186/1746‐160X‐6‐14
Shai A, Pitot HC, Lambert PF. p53 Loss synergizes with estrogen and papillomaviral oncogenes to induce cervical and breast cancer. Cancer Res 2008;68(8):2622‐2631. https://doi.org/10.1158/0008‐ 5472.CAN‐07‐5266
Amellem O, Sandvik JA, Stokke T, Pettersen EO. The retinoblastoma protein‐associated cell cycle arrest in S‐phase under moderate hypoxia is disrupted in cells expressing HPV18 E7 oncoprotein. Br J Cancer 1998;77(6):862‐872. https://doi.org/10.1038/bjc.1998.143
Wang Y‐W, Zhang K, Zhao S, et al. HPV status and its correlation with BCL2, p21, p53, Rb, and survivin expression in breast cancer in a Chinese population. Biomed Res Int 2017;2017:6315392. https://doi.org/10.1155/2017/6315392
Zhou C, Tuong ZK, Frazer IH. Papillomavirus immune evasion strategies target the infected cell and the local immune system. Front Oncol 2019;9:682. https://doi.org/10.3389/fonc.2019.00682
Litwin TR, Clarke MA, Dean M, Wentzensen N. Somatic host cell alterations in HPV carcinogenesis. Viruses 2017;9(8):206. https://doi.org/10.3390/v9080206
Ohba K, Ichiyama K, Yajima M, et al. In vivo and in vitro studies suggest a possible involvement of HPV infection in early stage of breast carcinogenesis via APOBEC3B induction. PLoS ONE 2014;9(5):e97787. https://doi.org/10.1371/journal.pone.0097787
Cooper K, Taylor L, Govind S. Human papillomavirus DNA in oesophageal carcinomas in South Africa. J Pathol 1995;175(3):273‐277. https://doi.org/10.1002/path.1711750304
Matsha T, Erasmus R, Kafuko AB, Mugwanya D, Stepien A, Parker MI. Human papillomavirus associated with oesophageal cancer. J Clin Pathol 2002;55(8):587‐590. https://doi.org/10.1136/ jcp.55.8.587
Sung H, Ferlay J, Siegel RL, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2021;719(3):209‐249. https:// doi.org/10.3322/caac.21660
Mbulawa ZZA, van Schalkwyk C, Hu N‐C, et al. High human papillomavirus (HPV) prevalence in South African adolescents and young women encourages expanded HPV vaccination campaigns. PLoS ONE 2018;13(1):e0190166. https://doi.org/10.1371/journal.pone.0190166
Delany‐Moretlwe S, Kelley KF, James S, et al. Human papillomavirus vaccine introduction in South Africa: Implementation lessons from an evaluation of the national school‐based vaccination campaign. Glob Health Sci Pract 2018;6(3):425‐438. https://doi.org/10.9745/GHSP‐D‐18‐00090
Qiagen QIAamp DNA Mini and Blood Mini Handbook Fifth Edition, May 2016. https://www.bing. com/ck/a?!&&p=1dbc8b17e3e72bddJmltdHM9MTY4NjUyODAwMCZpZ3VpZD0xMjljOTA3OC1 hMzkwLTYyNDktMTNlMC04MzU2YTJhMzYzY2UmaW5zaWQ9NTE4Mw&ptn=3&hsh=3&fclid =129c9078‐a390‐6249‐13e0‐8356a2a363ce&psq=Qiagen+QIAamp+DNA+Mini+and+Blood+Mini+ Handbook+Fifth+Edition%2c+May+2016.&u=a1aHR0cHM6Ly93d3cucWlhZ2VuLmNvbS91cy9y‐ XNvdXJjZXMvZG93bmxvYWQuYXNweD9pZD02MmEyMDBkNi1m YWY0LTQ2OWItYjUwZi0y YjU5Y2Y3Mzg5NjImbGFuZz1lbg&ntb=1 (accessed 15 June 2023).
Islam S, Dasgupta H, Roychowdhury A, et al. Study of association and molecular analysis of human papillomavirus in breast cancer of Indian patients: Clinical and prognostic implication. PLoS ONE 2017;12(2):e0172760. http://doi.org/10.1371/journal.pone.0172760
Akil N, Yasmeen A, Kassab A, Ghabreau L, Darnel AD, Al Moustafa A‐E. High‐risk human papillomavirus in breast cancer in Syrian women and their association with Id‐1 expression: A tissue microarray study. Br J Cancer 2008;99(3):404‐407. https://doi.org/10.1038/sj.bjc.6604503
Khodabandehlou N, Mostafaei S, Etemadi A, et al. Human papilloma virus and breast cancer: The role of inflammation and viral expressed proteins. BMC Cancer 2019;19(1):61. https://doi.org/10.1186/ s12885‐019‐5286‐0
Fernandes A, Bianchi G, Feltri AP, Pérez M, Correnti M. Presence of human papillomavirus in breast cancer and its association with prognostic factors. Ecancermedicalscience 2015;9:548. https://doi. org/10.3332/ecancer.2015.548
Salman NA, Davies G, Majidy F, et al. Association of high risk human papillomavirus and breast cancer: A UK based study. Sci Rep 2017;7:43591. https://doi.org/10.1038/srep43591
ElAmrani A, Gheit T, Benhessou M, et al. Prevalence of mucosal and cutaneous human papillomavirus in Moroccan breast cancer. Papillomavirus Res 2018;5:150‐155. https://doi. org/10.1016/j.pvr.2018.04.003
Khan NA, Castillo A, Koriyama C, et al. Human papillomavirus detected in female breast carcinomas in Japan. Br J Cancer 2008;99(3):408‐414. https://doi.org/10.1038/sj.bjc.6604502
Choi J, Kim C, Lee HS, et al. Detection of human papillomavirus in Korean breast cancer patients by real‐time polymerase chain reaction and meta‐analysis of human papillomavirus and breast cancer. J Pathol Translat Med 2016;50(6):442‐450. https://doi.org/10.4132/jptm.2016.07.08
Lawson JS, Glenn WK, Salyakina D, et al. Human papilloma viruses and breast cancer. Front Oncol 2015;5:277. https://doi.org/10.3389/fonc.2015.00277
Herrera‐Goepfert R, Vela‐Chávez T, Carrillo‐García A, et al. High‐risk human papillomavirus (HPV) DNA sequences in metaplastic breast carcinomas of Mexican women. BMC Cancer 2013;13:445. https://doi.org/10.1186/1471‐2407‐13‐445
Suarez ALP, Lorenzetti MA, Lucano RG, et al. Presence of human papilloma virus in a series of breast carcinoma from Argentina. PLoS ONE 2013;8(4):e61613. https://doi.org/10.1371/journal. pone.0061613
Lebelo RL, Bogers JJ, Thys S, et al. Detection, genotyping and quantitation of multiple HPV infections in South African women with cervical squamous cell carcinoma. J Med Virol 2015;87(9):1594‐1600. https://doi.org/10.1002/jmv.24132
Lawson JS, Glenn, WK, Salyakina D, et al. Human papillomavirus identification in breast cancer patients with previous cervical neoplasia. Front Oncol 2016;5:298. https://doi.org/10.3389/ fonc.2015.00298
SitasF,UrbanM,SteinL,etal.Therelationshipbetweenanti‐HPV‐16IgGseropositivityandcancer of the cervix, anogenital organs, oral cavity and pharynx, oesophagus and prostate in a black South African population. Infect Agent Cancer 2007,2:6 https://doi.org/10.1186/1750‐9378‐2‐6
Wang X, Tian X, Liu F, et al. Detection of HPV DNA in esophageal cancer specimens from different regions and ethnic groups: A descriptive study. BMC Cancer 2010;10:19. https://doi. org/10.1186/1471‐2407‐10‐19
Takalashi A, Ogoshi S, Ono H, et al. High‐risk human papillomavirus infection and overexpression of p53 protein in squamous cell carcinoma of the esophagus from Japan. Dis Esophagus 1998;11(3):162‐167. https://doi.org/10.1093/dote/11.3.162
Park E, Kim J‐Y, Choi S, Kim DS, Oh YL. Carcinogenic risk of human papillomavirus (HPV) genotypes and potential effects of HPV vaccines in Korea. Sci Rep 2019;9(1):12556. https://doi. org/10.1038/s41598‐019‐49060‐w
Castellsague X, Diaz M, de Sanjose S, et al. Worldwide human papillomavirus etiology of cervical adenocarcinoma and its co‐factors: Implications for screening and prevention. J Natl Cancer Inst 2006;98(5):303‐315. https://doi.org/10.1093/jnci/djj067
Wong MYW, Wang B, Yang A, Khor A, Xuan W, Rajenda S. Human papillomavirus exposure and sexual behaviour are signficant risk factors for Barrett’s dysplasia/esophageal adenocarcinoma. Dis Esophagus 2018;31(12). https://doi.org/10.1093/dote/doy051
KamolratanakulS,PitisuttithumP.Humanpapillomavirusvaccineefficacyandeffectivenessagainst cancer. Vaccines (Basel) 2021;9(12):1413. https://doi.org/10.3390/vaccines9121413
Costa APF, Cobucci RNO, da Silva JM, da Costa Lima PH, Giraldo PC, Goncalves AK. Safety of human papillomavirus 9‐valent vaccine: A meta‐analysis of randomised trials. J Immunol Res 2017;2017;3736201. https://doi.org/10.1155/2017/3736201
Downloads
Published
Issue
Section
License
Copyright (c) 2023 Taole Mokoena, Nomasondo Maroga, Neo Ledibane, Alfred Musekiwa, Meshack Bida, Mpho Kgomo, Ramokone Lebelo
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
Licensing Information
The SAMJ is published under an Attribution-Non Commercial International Creative Commons Attribution (CC-BY-NC 4.0) License. Under this license, authors agree to make articles available to users, without permission or fees, for any lawful, non-commercial purpose. Users may read, copy, or re-use published content as long as the author and original place of publication are properly cited.
Exceptions to this license model is allowed for UKRI and research funded by organisations requiring that research be published open-access without embargo, under a CC-BY licence. As per the journals archiving policy, authors are permitted to self-archive the author-accepted manuscript (AAM) in a repository.
Publishing Rights
Authors grant the Publisher the exclusive right to publish, display, reproduce and/or distribute the Work in print and electronic format and in any medium known or hereafter developed, including for commercial use. The Author also agrees that the Publisher may retain in print or electronic format more than one copy of the Work for the purpose of preservation, security and back-up.
