Top

Published in:

01-12-2021 | Human Papillomavirus | Research article

Viral load and high prevalence of HR-HPV52 and 58 types in black women from rural communities

Authors: Lays Paula Bondi Volpini, Jerusa Araújo Dias, Luciana Bueno de Freitas, Maria Carmen Lopes Ferreira Silva, Angélica Espinosa Miranda, Liliana Cruz Spano

Published in: BMC Infectious Diseases | Issue 1/2021

Abstract

Background

The high-risk human papillomavirus (HR-HPV) infection is the main cause of cervical cancer development, and the most common types were included in the last approved nonavalent vaccine (9vHPV). Geographical, socioeconomic and ethnic barriers in developing countries challenge primary and secondary prevention measures of cervical cancer. We aimed to determine the prevalence of HPV infection and the viral load of HR-HPV 9vHPV-related types black women resident in rural semi-isolated communities.

Methods

A descriptive study was conducted with 273 cervical samples of women from rural communities of Southeastern Brazil. Viral DNA was amplified by PCR, the genotype was identified by Reverse Line Blot (RLB) and Restriction Fragment Length Polymorphism (RFLP), and real-time PCR was applied to determine the viral load.

Results

HPV frequency was 11.4% (31/273), associated with the presence of cytological abnormalities (32.3%; p < 0.001). Thirty-one distinct genotypes were detected; HR-HPV occurred in 64.5% (20/31) of the samples and the most prevalent type were HPV52 > 58, 59. Multiple infections occurred with up to nine different genotypes. The viral load of HR-HPV 9vHPV-related types was higher in lesions than in normal cytology cases (p = 0.04); “high” and “very high” viral load occurred in HSIL and LSIL, respectively (p = 0.04).

Conclusions

We highlight that despite the low HPV frequency in the black rural women population, the frequency of HR-HPV was high, particularly by the HR-HPV52 and 58 types. Moreover, the HR-HPV viral load increased according to the progression from normal to lesion, being a potential biomarker to identify those women at higher risk of developing cervical lesions in this population.

Centers for Disease Control and Prevention. Genital HPV infection—CDC fact sheet, vol. 1. Atlanta, GA: CDC; 2012. CDC Fact Sheets 2014;1–2 [cited 2019 Dec 16]. Available from: https://www.cdc.gov/std/hpv/HPV-FS-July-2017.pdf

Muñoz N, Castellsague X, de Gonzalez AB, Gissmann L. Chapter 1: HPV in the etiology of human cancer. Vaccine. 2006;24:1–10.CrossRef

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(3):621–32. https://doi.org/10.1002/ijc.22527.CrossRefPubMed

Bruni L, Albero G, Serrano B, Mena M, Gómez D, Muñoz J, et al. ICO/IARC Information Centre on HPV and Cancer (HPV Information Centre). Human Papillomavirus and Related Diseases in the World. Summary Report 17 June 2019 [cited 2020 Mar 9]. Available from: https://www.hpvcentre.net/statistics/reports/XWX.pdf.

Arbyn M, Weiderpass E, Bruni L, de Sanjosé S, Saraiya M, Ferlay J, et al. Estimates of incidence and mortality of cervical cancer in 2018: a worldwide analysis. Lancet Glob Health. 2020;8(2):e191–203. https://doi.org/10.1016/S2214-109X(19)30482-6.CrossRefPubMed

Arbyn M, Raifu AO, Weiderpass E, Bray F, Anttila A. Trends of cervical cancer mortality in the member states of the European Union. Eur J Cancer. 2009;45(15):2640–8. https://doi.org/10.1016/j.ejca.2009.07.018.CrossRefPubMed

Wentzensen N, Arbyn M, Berkhof J, Bower M, Canfell K, Einstein M, et al. Eurogin 2016 roadmap: how HPV knowledge is changing screening practice. Int J Cancer. 2017;140(10):2192–200. https://doi.org/10.1002/ijc.30579.CrossRefPubMed

Brasil, Ministério da Saúde/INCA [Internet]. Câncer do colo do útero, estatísticas. 2019 [cited 2019 Dec 17]. Available from: https://www.inca.gov.br/tipos-de-cancer/cancer-do-colo-do-utero.

Musselwhite LW, Oliveira CM, Kwaramba T, Pantano NDP, Smith JS, Reis RM, et al. Racial/ethnic disparities in cervical Cancer screening and outcomes. Acta Cytol. 2016;60(6):518–26. https://doi.org/10.1159/000452240.CrossRefPubMed

10.

Batista JE, Saddi VA, Carvalho KPA, Ribeiro AA, Segati KD, Carneiro MADS, et al. Human papillomavirus genotypes 68 and 58 are the most prevalent genotypes in women from Quilombo communities in the state of Maranhão. Brazil Int J Infect Dis. 2017;55:51–5. https://doi.org/10.1016/j.ijid.2017.01.001.CrossRefPubMed

11.

Nascimento SD, Brandão VFCB, da Silva MAC N, Batista JE, MCL LB, et al. prevalence of human papillomavirus infection among women from Quilombo communities in northeastern Brazil. BMC Womens Health. 2018;18(1):1–10. https://doi.org/10.1186/s12905-017-0499-3.CrossRefPubMedPubMedCentral

12.

Schiffman M, Wentzensen N, Wacholder S, Kinney W, Gage JC, Castle PE. Human papillomavirus testing in the prevention of cervical cancer. J Natl Cancer Inst. 2011;103(5):368–83. https://doi.org/10.1093/jnci/djq562.CrossRefPubMedPubMedCentral

13.

Marongiu L, Godi A, Parry JV, Beddows S. Human papillomavirus 16, 18, 31 and 45 viral load, integration and methylation status stratified by cervical disease stage. BMC Cancer. 2014;14(1):384. https://doi.org/10.1186/1471-2407-14-384.CrossRefPubMedPubMedCentral

14.

Solomon D, Davey D, Kurman R, Moriarty A, O’Connor D, Prey M, et al. The 2001 Bethesda system: terminology for reporting results of cervical cytology. JAMA. 2002;287(16):2114–9. https://doi.org/10.1001/jama.287.16.2114.CrossRefPubMed

15.

Gravitt PE, Peyton CL, Alessi TQ, Wheeler CM, Hildesheim A, Schiffman MH, et al. Improved amplification of genital human papillomaviruses improved amplification of genital human papillomaviruses. J Clin Microbiol. 2000;38(1):357–61.PubMedPubMedCentral

16.

Huang SZ, Sheng M, Zhao JQ, Qiu XK, Zeng YT, Wang QS, et al. Detection of sickle cell gene by analysis of amplified DNA sequences. Yi Chuan Xue Bao. 1989;16(6):475–82.PubMed

17.

Bernard HU, Chan SY, Manos MM, Ong CK, Villa LL, Delius H, et al. Identification and assessment of known and novel human papillomaviruses by polymerase chain reaction amplification, restriction fragment length polymorphisms, nucleotide sequence, and phylogenetic algorithms. J Infect Dis. 1994 Nov;170(5):1077–85. https://doi.org/10.1093/infdis/170.5.1077.CrossRefPubMed

18.

Estrade C, Menoud PA, Nardelli-Haefliger D, Sahli R. Validation of a low-cost human papillomavirus genotyping assay based on PGMY PCR and reverse blotting hybridization with reusable membranes. J Clin Microbiol. 2011 Oct;49(10):3474–81. https://doi.org/10.1128/JCM.05039-11.CrossRefPubMedPubMedCentral

19.

Gravitt PE, Peyton C, Wheeler C, Apple R, Higuchi R, Shah KV. Reproducibility of HPV 16 and HPV 18 viral load quantitation using TaqMan real-time PCR assays. J Virol Methods. 2003 Sep;112(1–2):23–33. https://doi.org/10.1016/S0166-0934(03)00186-1.CrossRefPubMed

20.

Winer RL, Xi LF, Shen Z, Stern JE, Newman L, Feng Q, et al. Viral load and short-term natural history of type-specific oncogenic human papillomavirus infections in a high-risk cohort of midadult women. Int J Cancer. 2014;134(8):1889–98. https://doi.org/10.1002/ijc.28509.CrossRefPubMed

21.

Kõressaar T, Lepamets M, Kaplinski L, Raime K, Andreson R, Remm M. Primer3_masker: integrating masking of template sequence with primer design software. Bioinformatics. 2018;34(11):1937–8. https://doi.org/10.1093/bioinformatics/bty036.CrossRefPubMed

22.

Schlecht NF, Trevisan A, Duarte-Franco E, Rohan TE, Ferenczy A, Villa LL, et al. Viral load as a predictor of the risk of cervical intraepithelial neoplasia. Int J Cancer. 2003;103(4):519–24. https://doi.org/10.1002/ijc.10846.CrossRefPubMed

23.

Brasil. Fundação Cultural Palmares [Internet]. Certificação Quilombola [cited 2020 Mar 6]. Available from: http://www.palmares.gov.br/?page_id=37551.

24.

de Lima SV, de Mesquita AM, Cavalcante FG, Silva ZP, Hora V, Diedrich T, et al. Sexually transmitted infections in a female population in rural north-East Brazil: prevalence, morbidity and risk factors. Tropical Med Int Health. 2003;8(7):595–603.CrossRef

25.

Sowjanya AP, Jain M, Poli UR, Padma S, Das M, Shah KV, et al. Prevalence and distribution of high-risk human papilloma virus (HPV) types in invasive squamous cell carcinoma of the cervix and in normal women in Andhra Pradesh. BMC Infect Dis. 2005;5(1):116. https://doi.org/10.1186/1471-2334-5-116.CrossRefPubMedPubMedCentral

26.

Thapa N, Maharjan M, Shrestha G, Maharjan N, Petrini MA, Zuo N, et al. Prevalence and type-specific distribution of human papillomavirus infection among women in mid-western rural , Nepal- A population-based study. BMC Infect Dis. 2018;18(1):338. https://doi.org/10.1186/s12879-018-3175-9 Prevalence and type-specific distribution of human papillomavirus infection among women in mid-western rural, Nepal- A population-based study.CrossRefPubMedPubMedCentral

27.

Pista A, Oliveira A, Verdasca N, Ribeiro F. Single and multiple human papillomavirus infections in cervical abnormalities in Portuguese women. Clin Microbiol Infect. 2011;17(6):941–6. https://doi.org/10.1111/j.1469-0691.2010.03387.x.CrossRefPubMed

28.

Coser J, da Rocha BT, Simon D. Kazantzi Fonseca a S, Ikuta N, lunge VR. Prevalence and genotypic diversity of cervical human papillomavirus infection among women from an urban center in Brazil. Genet Mol Res. 2013;12(4):4276–85. https://doi.org/10.4238/2013.CrossRefPubMed

29.

Wheeler CM, Hunt WC, Cuzick J, Langsfeld E, Pearse A, Montoya GD, et al. A population-based study of human papillomavirus genotype prevalence in the United States: baseline measures prior to mass human papillomavirus vaccination. Int J Cancer. 2013;132(1):198–207. https://doi.org/10.1002/ijc.27608.CrossRefPubMed

30.

Martín P, Kilany L, García D, López-García AM, Martín-Azaña MJ, Abraira V, et al. Human papillomavirus genotype distribution in Madrid and correlation with cytological data. BMC Infect Dis. 2011;11(1):316. https://doi.org/10.1186/1471-2334-11-316.CrossRefPubMedPubMedCentral

31.

Sammarco ML, Del Riccio I, Tamburro M, Grasso GM, Ripabelli G. Type-specific persistence and associated risk factors of human papillomavirus infections in women living in Central Italy. Eur J Obstet Gynecol Reprod biol. Eur J Obstet Gynecol Reprod Biol. 2013;168(2):222–6. https://doi.org/10.1016/j.ejogrb.2013.01.012.CrossRefPubMed

32.

Trottier H, Mahmud S, Costa M, Sobrinho JP, Duarte-Franco E, Rohan TE, et al. Human papillomavirus infections with multiple types and risk of cervical Neoplasia. Cancer Epidemiol Biomark Prev. 2006;15(7):1274–80. https://doi.org/10.1158/1055-9965.EPI-06-0129.CrossRef

33.

Adcock R, Cuzick J, Hunt WC, Mcdonald RM, Wheeler CM, Wheeler CM. Role of HPV genotype, multiple infections, and viral load on the risk of high-grade cervical Neoplasia. Cancer Epidemiol Biomark Prev. 2019;28(11):1816–24. https://doi.org/10.1158/1055-9965.EPI-19-0239.CrossRef

34.

Wentzensen N, Schiffman M, Dunn ST, Zuna RE, Gold MA, Allen RA, et al. Multiple HPV genotype infections in cervical cancer progression in the study to understand cervical Cancer early endpoints and determinants (SUCCEED). Int J Cancer. 2009;125(9):2151–8. https://doi.org/10.1002/ijc.24528.CrossRefPubMedPubMedCentral

35.

Sammarco ML, Ucciferri C, Tamburro M, Falasca K, Ripabelli G, Vecchiet J. High prevalence of human papillomavirus type 58 in HIV infected men who have sex with men: a preliminary report in Central Italy. J Med Virol. 2016;88(5):911–4. https://doi.org/10.1002/jmv.24406.CrossRefPubMed

36.

Vidal AC, Smith JS, Valea F, Bentley R, Gradison M, Yarnall KSH, et al. HPV genotypes and cervical intraepithelial neoplasia in a multiethnic cohort in the southeastern USA. Cancer Causes Control. 2014;25(8):1055–62. https://doi.org/10.1007/s10552-014-0406-2.CrossRefPubMedPubMedCentral

37.

Montealegre JR, Varier I, Bracamontes CG, Dillon LM, Guillaud M, Sikora AG, et al. Racial/ethnic variation in the prevalence of vaccine-related human papillomavirus genotypes. Ethn Health. 2019;24(7):804–15. https://doi.org/10.1080/13557858.2017.1373073.CrossRefPubMed

38.

De Vuyst H, Parisi MR, Karani A, Mandaliya K, Muchiri L, Vaccarella S, et al. The prevalence of human papillomavirus infection in Mombasa. Kenya Cancer Causes Control. 2010;21(12):2309–13. https://doi.org/10.1007/s10552-010-9645-z.CrossRefPubMed

39.

Edna Omar V, Orvalho A, Nália I, Kaliff M, Lillsunde-Larsson G, Ramqvist T, et al. Human papillomavirus prevalence and genotype distribution among young women and men in Maputo city. Mozambique BMJ Open. 2017;7(7):e015653. https://doi.org/10.1136/bmjopen-2016-015653.CrossRefPubMed

40.

Mitra a, D a MI, Lee YS, Smith a, Marchesi JR, Lehne B, et al. Cervical intraepithelial neoplasia disease progression is associated with increased vaginal microbiome diversity. Sci Rep. 2015;5:16865. https://doi.org/10.1038/srep16865.CrossRefPubMedPubMedCentral

41.

Huang X, Li C, Li F, Zhao J, Wan X, Wang K, et al. Cervicovaginal microbiota composition correlates with the acquisition of high-risk human papillomavirus types. Int J Cancer. 2018;143(3):621–34. https://doi.org/10.1002/ijc.31342.CrossRefPubMed

42.

Fettweis JM, Brooks JP, Serrano MG, Sheth NU, Girerd PH, Edwards DJ, et al. Differences in vaginal microbiome in African American women versus women of European ancestry. Microbiology. 2014;160(10):2272–82. https://doi.org/10.1099/mic.0.081034-0.CrossRefPubMedPubMedCentral

43.

Ravel J, Gajer P, Abdo Z, Schneider GM, Koenig SSK, McCulle SL, et al. Vaginal microbiome of reproductive-age women. Proc Natl Acad Sci U S A. 2011;108(Suppl. 1):4680–7. https://doi.org/10.1073/pnas.1002611107.CrossRefPubMed

44.

Zhou X, Brown CJ, Abdo Z, Davis CC, Hansmann MA, Joyce P, et al. (2007) differences in the composition of vaginal microbial communities found in healthy Caucasian and black women. ISME J. 2007;1(2):121–33. https://doi.org/10.1038/ismej.2007.12.CrossRefPubMed

45.

Hesselink AT, Berkhof J, Heideman DA, Bulkmans NW, Van Tellingen JE, Meijer CJ, et al. High-risk human papillomavirus DNA load in a population-based cervical screening cohort in relation to the detection of high-grade cervical intraepithelial neoplasia and cervical cancer. Int J Cancer. 2009;124(2):381–6. https://doi.org/10.1002/ijc.23940.CrossRefPubMed

46.

Xi LF, Hughes JP, Castle PE, Edelstein ZR, Wang C, Galloway DA, et al. Viral load in the natural history of human papillomavirus type 16 infection: a nested case-control study. J Infect Dis. 2011;203(10):1425–33. https://doi.org/10.1093/infdis/jir049.CrossRefPubMedPubMedCentral

47.

Flores R, Papenfuss M, Klimecki WT, Giuliano AR. Cross-sectional analysis of oncogenic HPV viral load and cervical intraepithelial neoplasia. Int J Cancer. 2006;118(5):1187–93. https://doi.org/10.1002/ijc.21477.CrossRefPubMed

48.

Kim J, Kim BK, Jeon DS, Lee CH, Roh JW, Kim JY, et al. Type-specific viral load and physical state of HPV type 16, 18, and 58 as diagnostic biomarkers for high-grade squamous intraepithelial lesions or cervical Cancer. Cancer Res Treat. 2019;52(2):396–405. https://doi.org/10.4143/crt.2019.152.CrossRefPubMedPubMedCentral

Title: Viral load and high prevalence of HR-HPV52 and 58 types in black women from rural communities
Authors: Lays Paula Bondi Volpini
Jerusa Araújo Dias
Luciana Bueno de Freitas
Maria Carmen Lopes Ferreira Silva
Angélica Espinosa Miranda
Liliana Cruz Spano
Publication date: 01-12-2021
Publisher: BioMed Central
Keywords: Human Papillomavirus
Cervical Cancer
Cervical Cancer
Published in: BMC Infectious Diseases / Issue 1/2021
Electronic ISSN: 1471-2334
DOI: https://doi.org/10.1186/s12879-021-06042-6

ACC 2024 Congress Coverage

Heart Failure Video

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Viral load and high prevalence of HR-HPV52 and 58 types in black women from rural communities

Abstract

Background

Methods

Results

Conclusions

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page

At a glance: The ONWARDS insulin icodec trials

Springer Medicine

Abstract

Background

Methods

Results

Conclusions

Please log in to get access to this content

Other articles of this Issue 1/2021

The distribution of hepatitis C virus infection in Shanghai, China: a time-spatial study

Bacterial and fungal profile, drug resistance pattern and associated factors of isolates recovered from blood samples of patients referred to Ethiopian Public Health Institute: cross-sectional study

Ambulatory induction phase treatment of cryptococcal meningitis in HIV integrated primary care clinics, Yangon, Myanmar

Evaluation of asymptomatic bacteruria management before and after antimicrobial stewardship program implementation: retrospective study

Seroprevalence of hepatitis B virus infection, anti-HCV antibodies and HIV and knowledge among people who use drugs attending methadone therapy clinic in Tanzania; a cross-sectional study

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page