Molecular characterisation of genital human papillomavirus among women in Southwestern, Nigeria
Autoři:
Yewande T. Nejo aff001; David O. Olaleye aff002; Georgina N. Odaibo aff002
Působiště autorů:
Department of Biological Sciences, Bowen University, Iwo, Osun State, Nigeria
aff001; Department of Virology, College of Medicine, University of Ibadan, Ibadan, Nigeria
aff002
Vyšlo v časopise:
PLoS ONE 14(11)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0224748
Souhrn
Background
Persistent infections with high-risk genital Human papillomavirus (HPV) especially types 16 and 18, are associated with cervical cancer. However, distribution of HPV types varies greatly across geographical regions and the available vaccines target only few types. This study was designed to determine the HPV types circulating in Southwestern Nigeria, thereby providing necessary information for effective control of the virus.
Methods
Endocervical swab samples were collected from a total of 295 consenting women attending routine cervical cancer screening, STI clinics and community-based outreach programme. Viral DNA was extracted from the samples and the consensus region of the HPV DNA was amplified by PCR using GP-E6/E7 primers. Type-specific nested multiplex PCR and Sanger sequencing were used to genotype the HPV isolates.
Results
In this study, 51 (17.3%) individuals were positive for HPV DNA using consensus primers that target the E6/E7 genes but only 48 (16.3%) were genotyped. A total of 15 HPV types (HPV-6, 16, 18, 31, 33, 35, 42, 43, 44, 52, 58, 66, 74, 81, 86) were detected, with HPV-31 being the most predominant (32.8%), followed by HPV-35 (17.2%) and HPV-16 (15.5%). Two rare HPV types; 74 and 86 were also detected. The HPV-74 isolate had three nucleotide (CCT) insertions at E7 gene that translated into amino acid proline. Highest nucleotide substitutions (n = 32) were found in HPV-44 genotype. Among positive individuals, 20.8% had dual infections and 86.2% had High-risk HPV types.
Conclusions
Multiple Human papillomavirus types co-circulated in the study. Most of the circulating Human papillomavirus are high-risk type with type 31 being the most predominant. Although the implication of HPV-74 with proline insertion detected for the first time is unknown, it may have effect on the transformation potential of the virus. Polyvalent HPV vaccine will be more effective for the infection control in Nigeria.
Klíčová slova:
Polymerase chain reaction – Human papillomavirus – Human papillomavirus infection – HPV-16 – HPV-18 – HPV-31 – HPV-6 – HPV-1
Zdroje
1. Georgieva S, Iordanov V, Sergieva S. Nature of cervical cancer and other HPV-associated cancers. Journal of BUON. 2009; 14: 391–398. 19810128
2. Bernard HU, Burk RD, Chen Z, van Doorslaer K, Hausen HZ, de Villiers EM. Classification of papillomaviruses (PVs) based on 189 PV types and proposal of taxonomic amendments. Virology. 2010; 401(1): 70–79. doi: 10.1016/j.virol.2010.02.002 20206957
3. Bosch FX, Lorincz A, Muñoz N, Meijer CJLM, Shah KV. The causal relation between human papillomavirus and cervical cancer, Journal of Clinical Pathology. 2002; 55(4): 244–265. doi: 10.1136/jcp.55.4.244 11919208
4. WHO/ICO HPV information centre on HPV and cervical cancer (HPV information centre). Human papillomavirus and related cancers in Nigeria. Summary report 2010. Available: www.who.int/hpvcentre.
5. Woodman CBJ, Stuart I, Collins SI, Young LS. The natural history of cervical HPV infection: unresolved issues. Nature Reviews Cancer. 2007; 7: 11–22. doi: 10.1038/nrc2050 17186016
6. Fernandes J, Carvalho M, de Fernandes T, Araújo J, Azevedo P, Azevedo J, et al. Prevalence of Human Papillomavirus Type 58 in Women With or Without Cervical Lesions in Northeast Brazil. Annals of Medical and Health Sciences Research. 2013; 3(4): 504–510. doi: 10.4103/2141-9248.122060 24379999
7. HPV Center http://www.hpvcenter.se/html/refclones.html. Accessed 29 Dec 2017. Last modified by: Davit Bzhalava 2016-05-24 email: davit.bzhalava@ki.se
8. de Villiers EM, Fauquet C, Broker TR, Bernard HU, zur Hausen H. Classification of papillomaviruses. Virology. 2004; 324: 17–27. doi: 10.1016/j.virol.2004.03.033 15183049
9. Lee K, Magalhaes I, Clavel C, Briolat J, Birembaut P, Tommasino M, et al. Human papillomavirus 16 E6, L1, L2 and E2 gene variants in cervical lesion progression. Virus Res. 2008; 131: 106–110. doi: 10.1016/j.virusres.2007.08.003 17869365
10. Villa LL, Sichero L, Rahal P, Caballero O, Ferenczy A, Rohan T, et al. Molecular variants of human papillomavirus types 16 and 18 preferentially associated with cervical neoplasia. J Gen Virol. 2000; 81: 2959–2968. doi: 10.1099/0022-1317-81-12-2959 11086127
11. Xi LF, Koutsky LA, Hildesheim A, Galloway DA, Wheeler CM, Winer RL, et al. Risk for high-grade cervical intraepithelial neoplasia associated with variants of human papillomavirus types 16 and 18. Cancer Epidemiol. Biomarkers Prev. 2007; 16: 4–10 doi: 10.1158/1055-9965.EPI-06-0670 17220325
12. Zuna RE, Moore WE, Shanesmith RP, Dunn ST, Wang SS, Schiffman M., et al. Association of HPV16 E6 variants with diagnostic severity in cervical cytology samples of 354 women in a US population. Int. J. Cancer. 2009; 125: 2609–2613 doi: 10.1002/ijc.24706 19569178
13. Muñoz N, Bosch FX, de Sanjosé S, Herrero R, Castellsagué X, Shah KV, et al. Epidemiological classification of human papillomavirus types associated with cervical cancer. N. Engl.J.Med. 2003; 348: 518–27. doi: 10.1056/NEJMoa021641 12571259
14. Clifford G, Franceschi S, Diaz M, Munoz N, Villa LL. Chapter 3: HPV type-distribution in women with and without cervical neoplastic diseases. Vaccine. 2006; 24 (Suppl 3): S3/26–34.
15. Odetola TD, Ekpo K. Community Medicine & Health Education Nigerian Women’s Perceptions about Human Papillomavirus Immunisations. J Community Med Health Educ. 2012; 2(11): 1–5.
16. Food and Drug Administration (FDA) 2014. Approval letter—GARDASIL 9. Silver Spring, MD: US Department of Health and Human Services, Food and Drug Administration; December 10, 2014. Available at http://www.fda.gov/BiologicsBloodVaccines/Vaccines/Approved Products/ucm426520.htm
17. Charan J, Biswas T. How to calculate sample size for different study designs in medical research. Indian J Psychol Med. 2013; 35(2): 121–126. doi: 10.4103/0253-7176.116232 24049221
18. Thomas JO, Herrero R, Omigbodun AA, Ojemakinde K, Ajayi IO, Fawole A, et al. Prevalence of papillomavirus infection in women in Ibadan, Nigeria: a population-based study. British Journal of Cancer. 2004; 90: 638–645 doi: 10.1038/sj.bjc.6601515 14760378
19. Sotlar K, Diemer D, Dethleffs A, Hack Y, Stubner A, Vollmer N, et al. Detection and typing of human papillomavirus by E6 nested multiplex PCR. Journal of Clinical Microbiology. 2004; 42: 3176–3184. doi: 10.1128/JCM.42.7.3176-3184.2004 15243079
20. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution. 2013; 30: 2725–2729. doi: 10.1093/molbev/mst197 24132122
21. Tamura K, Nei M. Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in Humans and chimpanzees. Molecular Biology and Evolution. 1993; 10: 512–526. doi: 10.1093/oxfordjournals.molbev.a040023 8336541
22. Nejo YT, Olaleye DO, Odaibo GN. Prevalence and Risk Factors for Genital Human Papillomavirus Infections Among Women in Southwest Nigeria. Archives of basic and applied medicine. 2018; 6(1): 105–112. 29905313
23. Schnatz PF, Markelova NV, Holmes D, Mandavilli SR, O’Sullivan DM. The prevalence of cervical HPV and cytological abnormalities in association with reproductive factors of rural Nigerian women. Journal of Womens Health (Larchmt). 2008; 17: 279–285.
24. Akarolo-Anthony SN, Al-Mujtaba M, Famooto AO, Dareng EO, Olaniyan OB, Offiong R, et al. HIV associated high-risk HPV infection among Nigerian women. BMC Infectious Diseases. 2013; 13: 521. doi: 10.1186/1471-2334-13-521 24192311
25. Dareng EO, Ma B, Famooto AO, Akarolo-Anthony SN, Offiong RA, Olaniyan O, et al. Prevalent high-risk HPV infection and vaginal microbiota in Nigerian women. Epidemiology and Infection. 2016; 144(1): 123–137. doi: 10.1017/S0950268815000965 26062721
26. Fadahunsi OO, Omoniyi-Esan GO, Banjo AA, Esimai OA, Osiagwu D, Clement F, et al. Prevalence of High Risk oncogenic HPV types in cervical smears of women attending well women clinic in Ile-Ife. Gynaecology Obstetrics. 2013; 3(6): 1000185.
27. Nweke IG, Banjo AAF, Abdulkareem FB, Nwadike VU. Prevalence of Human Papilloma virus DNA in HIV positive women in Lagos University Teaching Hospital (LUTH) Lagos, Nigeria. British Microbiology Research Journal. 2013; 3(3): 400–413.
28. Adegbesan-Omilabu MA, Okunade KS, Omilabu SA. Oncogenic human papillomavirus infection among women attending the cytology clinic of a tertiary hospital in Lagos, South-West Nigeria. International Journal of Research in Medical Sciences. 2014; 2(2): 625–630.
29. Ezechi OC, Ostergren PO, Nwaokorie FO, Ujah IAO, Odberg PK. The burden, distribution and risk factors for cervical oncogenic Human papillomavirus infection in HIV positive Nigerian women. Virology Journal. 2014; 11:15. doi: 10.1186/1743-422X-11-15
30. Piras F, Piga M, De Montis A, Zannou AR, Minerba L, Perra MT, et al. Prevalence of human papillomavirus infection in women in Benin, West Africa. Virology Journal. 2011; 8: 514. doi: 10.1186/1743-422X-8-514 22074103
31. Kuhn L, Denny L, Pollack A, Lorincz A, Richart RM, Wright TC. Human papillomavirus DNA testing for cervical cancer screening in low-resource settings. Journal of National Cancer Institute. 2000; 92: 818–825.
32. Zohoncon TM, Bisseye C, Djigma FW, Yonli AT, Compaore TR, Sagna T, et al. Prevalence of HPV High-Risk Genotypes in Three Cohorts of Women in Ouagadougou (Burkina Faso). Mediterranean Journal of Hematology and Infectious Diseases. 2013.
33. Traore IMA, Zohoncon TM, Dembele A, Djigma FW, Obiri-Yeboah D, Traore G, et al. Molecular Characterization of High-Risk Human Papillomavirus in Women in Bobo-Dioulasso, Burkina Faso. BioMed Research International. 2016; 7092583. doi: 10.1155/2016/7092583 27525275
34. 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 Infectious Diseases. 2007; 7(7): 453 59. doi: 10.1016/S1473-3099(07)70158-5 17597569
35. Bruni L, Diaz M, Castellsagué X, Ferrer E, Bosch FX, de Sanjosé S. Cervical Human Papillomavirus Prevalence in 5 Continents: Meta‐Analysis of 1 Million Women with Normal Cytological Findings. The Journal of Infectious Diseases. 2010; 202(12): 1789–1799. doi: 10.1086/657321 21067372
36. de Sanjose S, Quint WG, Alemany L, Geraets DT, Klaustermeier JE, Lloveras B, et al. Human papillomavirus genotype attribution in invasive cervical cancer: a retrospective cross-sectional worldwide study. Lancet Oncology. 2010; 11:1048–1056. doi: 10.1016/S1470-2045(10)70230-8 20952254
37. Li N, Franceschi S, Howell-Jones R, Snijders PJ, Clifford GM. Human papillomavirus type distribution in 30,848 invasive cervical cancers worldwide: variation by geographical region, histological type and year of publication. International Journal of Cancer. 2011; 128: 927–935. doi: 10.1002/ijc.25396 20473886
38. 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. International Journal of Cancer. 2014; 134: 1389–1398. doi: 10.1002/ijc.28425 23929250
39. Ali-Risasi C, Verdonck K, Padalko E, Vanden BD, Praet M. Prevalence and risk factors for cancer of the uterine cervix among women living in Kinshasa, the Democratic Republic of the Congo: a cross-sectional study. Infectious Agents and Cancer. 2015; 10: 20. doi: 10.1186/s13027-015-0015-z 26180542
40. Kennedy NT, Ikechukwu D, Goddy B. Risk factors and distribution of oncogenic strains of human papilloma virus in women presenting for cervical cancer screening in Port Harcourt, Nigeria. The Pan African medical journal. 2016; 23: 85. doi: 10.11604/pamj.2016.23.85.8510 27222684
41. Gravitt PE, Kamath AM, Gaffikin L, Chirenje ZM, Womack S, Shah KV. Human papillomavirus genotype prevalence in high-grade squamous intraepithelial lesions and colposcopically normal women from Zimbabwe. International Journal of Cancer. 2002; 100: 729–732. doi: 10.1002/ijc.10538 12209615
42. Yamada T, Manos MM, Peto J, Greer CE, Munoz N, Bosch FX, et al. Human papillomavirus type 16 dsequence variation in cervical cancers: a worldwide perspective. J Virol Methods. 1997; 71: 2463–2472.
43. Cornet I, Gheit T, Iannacone MR, Vignat J, Sylla BS, Del Mistro A, et al. HPV16 genetic variation and the development of cervical cancer worldwide. Br J Cancer. 2013; 108: 240–244. doi: 10.1038/bjc.2012.508 23169278
44. Cornet I, Gheit T, Franceschi S, Vignat J, Burk RD, Sylla BS, et al. Human Papillomavirus Type 16 Genetic Variants: Phylogeny and Classification Based on E6 and LCR. J Virol. 2012; 86: 6855–6861. doi: 10.1128/JVI.00483-12 22491459
45. Boumba LMA, Assoumou SZ, Hilali L, Mambou JV, Moukassa D, Ennaji MM. Genetic variability in E6 and E7 oncogenes of human papillomavirus Type 16 from Congolese cervical cancer isolates. Infectious Agents and Cancer. 2015; 10(1):15.
46. Schlecht NF, Burk RD, Palefsky JM, Minkoff H, Xue X, Massad LS, et al. Variants of human papillomaviruses 16 and 18 and their natural history in human immunodeficiency virus-positive women. Journal of General Virology. 2005; 86: 2709–2720. doi: 10.1099/vir.0.81060-0 16186224
47. Smith B, Chen Z, Reimers L, van Doorslaer K, Schiffman M, DeSalle R, et al. Sequence imputation of HPV16 genomes for genetic association studies. PLoS ONE. 2011; 6: doi: 10.1371/journal.pone.0021375 21731721
48. Burk RD, Harari A, Chen Z. Human papillomavirus genome variants. Virology. 2013; 445: 232–243. doi: 10.1016/j.virol.2013.07.018 23998342
49. Pérez S, Cid A, Iñarrea A, Pato M, Lamas MJ, Couso B, et al. Prevalence of HPV 16 and HPV 18 Lineages in Galicia, Spain. PLoS ONE. 2014; 9(8): e104678. doi: 10.1371/journal.pone.0104678 25111834
50. Tu JJ, Kuhn L, Denny L, Beattie KJ, Lorincz A, Wright TC. Molecular variants of human papillomavirus type 16 and risk for cervical neoplasia in South Africa. Int J Gynecol Cancer. 2006; 16: 736–742. doi: 10.1111/j.1525-1438.2006.00401.x 16681754
51. Qmichou Z, Ennaji MM, Amrani M, Fahime EM, Meloul M, Meftah EL, et al. Molecular Characterization of HPV16 E6 and E7 Variants among Women with Cervical Cancer in Moroco. Britsh Microbiol Res J. 2013; 3: 692–705
52. Bernard HU, Calleja-Macias IE, Dunn ST. Genome variation of human papillomavirus types: phylogenetic and medical implications. Int J Cancer. 2006; 118: 1071–1076. doi: 10.1002/ijc.21655 16331617
53. Sichero L, Ferreira S, Trottier H, Duarte-Franco E, Ferenczy A, Franco EL, et al. High grade cervical lesions are caused preferentially by non-European variants of HPVs 16 and 18. Int J Cancer. 2007; 120: 1763–1768. doi: 10.1002/ijc.22481 17230525
54. Freitas LB, Chen Z, Muqui EF, Boldrini NAT, Miranda AE, Spano LC, et al. Human Papillomavirus 16 Non-European variants are preferentially associated with high-grade cervical lesions. PLoS One. 2014; 9(7): e100746. doi: 10.1371/journal.pone.0100746 24983739
55. Crook T, Tidy JA, Vousden KH. Degradation of p53 can be targeted by HPV E6 sequences distinct from those required for p53 binding and trans-activation. Cell. 1991; 67: 547–556. doi: 10.1016/0092-8674(91)90529-8 1657399
56. Stöppler MC, Ching K, Stöppler H, Clancy K, Schlegel R, Icenogle J. Natural variants of the human papillomavirus type 16 E6 protein differ in their abilities to alter keratinocyte differentiation and to induce p53 degradation. J Virol. 1996; 70: 6987–6993. 8794343
57. Ellis JRM, Etherington I, Galloway D, Luesley D, Young LS. Antibody responses to HPV16 virus-like particles in women with cervical intraepithelial neoplasia infected with a variant HPV16. The Lancet. 1997; 349: 1069–1070.
58. Chow VT, Loh E, Yeo WM, Tan SY, Chan R. Identification of multiple genital HPV types and sequence variants by consensus and nested type-specific PCR coupled with cycle sequencing. Pathology. 2000; 32: 204–208. 10968397
59. Shen M, Ding X, Li T, Chen G, Zhou X. Sequence Variation Analysis of HPV-18 Isolates in Southwest China. PLoS ONE. 2013; 8: doi: 10.1371/journal.pone.0056614 23451059
60. Arroyo SL, Basaras M, Arrese E, Hernáez S, Andía D, Esteban V, et al. Human Papillomavirus (HPV) genotype 18 variants in patients with clinical manifestations of HPV related infections in Bilbao, Spain. Virology Journal. 2012; 9: 258. doi: 10.1186/1743-422X-9-258 23121839
61. Kovelman R, Bilter GK, Roman A, Brown DR, Barbosa MS. Human papillomavirus type 6: classification of clinical isolates and functional analysis of E2 proteins. Journal of General Virology. 1999; 80: 2445–2451. doi: 10.1099/0022-1317-80-9-2445 10501500
62. Kocjan BJ, Poljak M, Cimerman M, Gale N, Potočnik M, Bogovac Ž, et al. Prevaccination genomic diversity of human papillomavirus genotype 6 (HPV 6). Virology 2009; 391: 274–283. doi: 10.1016/j.virol.2009.06.030 19596128
63. Danielewski JA, Garland SM, McCloskey J, Hillman RJ, Tabrizi SN. Human Papillomavirus Type 6 and 11 Genetic Variants Found in 71 Oral and Anogenital Epithelial Samples from Australia. PLoS ONE. 2013; 8(5).
64. Gagnon S, Hankins C, Tremblay C, Pourreaux K, Forest P, Rouah F, et al. Polymorphism of human papillomavirus type 31 isolates infecting the genital tract of HIV-seropositive and HIV-seronegative women at risk for HIV infection. Journal of Medical Virology. 2005; 75: 213–221. doi: 10.1002/jmv.20259 15602735
65. Calleja-Macias IE, Kalantari M, Allan B, Williamson AL, Chung LP, Collins RJ, et al. Papillomavirus subtypes are natural and old taxa: phylogeny of human papillomavirus types 44 and 55 and 68a and -b. Journal of virology. 2005; 79: 6565–6569. doi: 10.1128/JVI.79.10.6565-6569.2005 15858044
66. Chen Z, Schiffman M, Herrero R, DeSalle R, Anastos K, Segondy M, et al. Evolution and taxonomic classification of human papillomavirus 16 (HPV16)-related variant genomes: HPV31, HPV33, HPV35, HPV52, HPV58 and HPV67. PLoS ONE. 2011; 6: doi: 10.1371/journal.pone.0020183 21673791
67. Maver PJ, Kocjan BJ, Seme K, Poljak M. Genomic diversity of low-risk human papillomavirus genotypes HPV 40, HPV 42, HPV 43, and HPV 44. Journal of Medical Virology. 2014; 86(2), 272–282. doi: 10.1002/jmv.23822 24155245
68. de Villiers EM. Heterogeneity of the human papillomavirus group. Journal of Virology. 1989; 63: 4898–4903.4. 2552162
69. Prado JC, Calleja-Macias IE, Bernard HU, Kalantari M, Macay SA, Allan B, et al. Worldwide genomic diversity of the human papillomaviruses-53, 56, and 66, a group of high-risk HPVs unrelated to HPV-16 and HPV-18. Virology. 2005; 340: 95–104. doi: 10.1016/j.virol.2005.06.024 16039686
70. Chang YJ, Chen HC, Lee BH, You SL, Lin CY, Pan MH, et al. Unique variants of human papillomavirus genotypes 52 and 58 and risk of cervical neoplasia. International Journal of Cancer. 2011; 129(4): 965–973. doi: 10.1002/ijc.25724 20949622
71. Choi YD, Han CW, Chung WJ et al., “Analysis of HPV-other samples by performing HPV DNA sequencing,” Korean Journal of Pathology. 2009; 43(3): 250–253.
72. Ngai Na Chloe Co, Lai-On C, Joseph KFC, Joseph WOT, Enders KON. HPV Prevalence and Detection of Rare HPV Genotypes in Hong Kong Women from Southern China with Cytological Abnormalities. ISRN Virology. 2013. https://doi.org/10.5402/2013/312706.
73. Molden T, Feiring B, Ambur OH, et al. Human papillomavirus prevalence and type distribution in urine samples from Norwegian women aged 17 and 21 years: A nationwide cross-sectional study of three non-vaccinated birth cohorts. Papillomavirus Res. 2016;2:153–158. doi: 10.1016/j.pvr.2016.05.002 29074174
74. Longuet M, Cassonnet P, Orth G. A novel genital human papillomavirus (HPV), HPV type 74, found in immunosuppressed patients. J Clin Microbiol. 1996; 34(7): 1859–1862. 8784613
75. Terai M, and Burk RD. Characterization of a novel genital human papillomavirus byoverlapping PCR: candHPV86 identified in cervicovaginal cells of a woman with cervical neoplasia. Journal of General Virology. 2001; 82: 2035–2040. doi: 10.1099/0022-1317-82-9-2035 11514712
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