Port Harcourt Medical Journal

REVIEW ARTICLE
Year
: 2020  |  Volume : 14  |  Issue : 3  |  Page : 95--99

Human papillomavirus and cervical cancer


Firdous Ansari 
 Department of Mathematics and Statistics, Jai Narain Vyas University, Jodhpur, Rajasthan, India

Correspondence Address:
Firdous Ansari
Ansari Bldg 1st 'B' Road, Sardarpura Jodhpur - 342 001, Rajasthan
India

Abstract

Background: According to the World Health Organization, human papillomavirus (HPV) causes cervical cancer, which is the fourth most common cancer in women, with an estimated 266,000 deaths and 528,000 new cases in 2012. Usually, HPV infections cause no symptoms but it is also reported that 99% cervical cancer cases are linked to genital infection with HPV and it is the most common viral infection of the reproductive tract. Aim: The aim of the study is to review the literature to describe what research has been done and what can be the future prospect. Methods: To search for the literature search engine, PubMed and Google were searched by inputting different key words, for example, HPV and cervical cancer. Studies considered were broadly associated with either HPV and cervical cancer or its worldwide scenario and socio-economic status. Results: Considered studies showed that Genital HPV is the most common sexually transmitted infection in the United States, whereas a considerable number i.e., 90% cases of cervical cancer, HPV was detected. The largest proportion attributable to HPV reported were about 75%, 70%, 70% and 60% of vaginal cancers, oropharyngeal cancers, vulvar cancers and penile cancers, respectively. Various identified risk factors as well as different suggested methods are also described to protect against HPV. Conclusion: We may conclude that as it is sexually transmitted infection and causes no symptoms, so proper care should be taken in intimate hygiene management.



How to cite this article:
Ansari F. Human papillomavirus and cervical cancer.Port Harcourt Med J 2020;14:95-99


How to cite this URL:
Ansari F. Human papillomavirus and cervical cancer. Port Harcourt Med J [serial online] 2020 [cited 2021 Apr 17 ];14:95-99
Available from: https://www.phmj.org/text.asp?2020/14/3/95/311928


Full Text



 Introduction



Human papilloma viruses (HPVs) are a small group of nonenveloped viruses belonging to the Papillomaviridae family with strong similarities to polyoma viruses.[1],[2],[3],[4],[5],[6] The Center for Disease Control and Prevention highlights the fact that the majority of sexually active individuals become infected with HPV at least once in their lifetime.[7],[8],[9],[10] HPV is the most prevalent sexually transmitted infection worldwide,[11],[12],[13],[14],[15] associated with approximately 5.2% of human cancer burden worldwide.[16],[17],[18] Types of human papillomavirus (HPV) are phylogenetically classified into alpha (a), beta (ß) or gamma (γ) genera, with a HPVs displaying tropism for mucosal epithelium and ß-and γ-HPVs displaying tropism for cutaneous epithelium.[19],[20] Cutaneous HPVs have also been detected in the anal canal, genital, cervical epithelia and in oral and nasal mucosa.[21],[22],[23],[24],[25],[26],[27],[28],[29],[30] HPV types 16 and 18 are the most common high-risk types and are considered to be responsible for >70% of all cervical cancer cases.[5]

 Methods of Review



For the development purpose of this article different key words in different search engines such as PubMed and Google were searched. Key words used were HPV, cervical cancer, risk factors of cervical cancer, low socio-economic status, etc. Studies included in this review article were broadly associated either with HPV and cervical cancer or with its worldwide scenario and socio-economic status.

 Results



Considered studies showed that genital HPV is the most common sexually transmitted infection in the United States, whereas a considerable number i.e., 90% cases of cervical cancer, HPV was detected. The largest proportion attributable to HPV reported were about 75%, 70%, 70% and 60% of vaginal cancers, oropharyngeal cancers, vulvar cancers and penile cancers, respectively. Rates of oropharyngeal squamous cell carcinomas (SCC) were reported amongst 7.6% males than amongst 1.7% of females whereas rates of anal SCC were found amongst 1.8% females than amongst 1.1% males. In South Asia, India has the highest age standardised incidence of cervical cancer at 22 years of age, compared to 19.2 years in Bangladesh, 13 years in Sri Lanka and 2.8 years in Iran. Whereas in India, according to ICO/IARC Information Centre on HPV and Cancer(HPV Information Centre) 2019; 122,844 women were diagnosed with cervical cancer and 67,477 died from the disease. In India, the 5 years prevalence was found to be 1.8 million individuals with cancer which was figured to be 5.52% of global prevalence.

Various risk factors identified are infection with certain oncogenic types of HPVs, sexual intercourse at an early age, multiple sexual partners, multiparity, long-term oral contraceptive use, multiple childbirths, tobacco smoking, low socioeconomic status, infection with Chlamydia trachamatis, micronutrient deficiency and a diet deficient in vegetables and fruits, that contribute to the development of cervical cancer.

Different methods are also suggested to protect against HPV such as sexual abstinence, consistent and correct use of condoms, limiting the number of lifetime sexual partners, cultivating a monogamous relationship and having safe sexual habits. It is also observed that all prophylactic vaccines work through the induction of virus-neutralising antibodies, and reduce the number of cells that are infected after challenge with virus, and so prevent the clinical disease associated with infection. In many African countries, self-reported screening rates were found between 8.3% and 64%, whereas screening rates were observed ranging between 9.4% and 80% among women accessing HIV care.

 Discussion



First, we will discuss worldwide scenario of HPV and its association with cervical cancer, genital HPV is reported to be the most common sexually transmitted infection in the United States with an estimated incidence of 14 million annually.[11],[31],[32],[33],[34],[35],[36],[37],[38],[39] According to a study, HPV was detected in about 90% cases of cervical cancers in the United States. From the same study, the largest proportion attributable to HPV were of anal cancers, about 75% of vaginal cancers, followed by about 70% oropharyngeal cancers, an estimated of about 70% vulvar cancers, and about 60% of penile cancers.[40],[41],[42],[43],[44] Among HPV-attributable cancers, oropharyngeal SCCs were observed the most common from 2009 to 2013.[45],[46],[47],[48],[49],[50],[51],[52],[53] Rates of oropharyngeal SCC were found higher among males (7.6%) than females (1.7%) whereas rates of anal SCC were found higher among females (1.8%) than males (1.1%).[54] In South Asia, India has the highest age standardised incidence of cervical cancer at 22 years of age, compared to 19.2 years in Bangladesh, 13 years in Sri Lanka and 2.8 years in Iran. Whereas in India, according to ICO/IARC Information Centre on HPV and Cancer (HPV Information Centre) 2019; 122,844 women were diagnosed with cervical cancer and 67,477 died from the disease.[55],[56] In India, the 5-year prevalence was found to be 1.8 million individuals with cancer which was figured to be 5.52% of global prevalence.[57] If we talk about risk factors associated with HPV, some of the risk factors identified by various studies are infection with certain oncogenic types of HPVs, sexual intercourse at an early age, multiple sexual partners, multiparity, long-term oral contraceptive use, multiple childbirths, tobacco smoking, low socioeconomic status, infection with Chlamydia trachomatis, micronutrient deficiency and a diet deficient in vegetables and fruits, that contribute to the development of cervical cancer.[33],[58],[59],[60],[61]

Regarding HPV Prevention, numerous studies suggested various methods to protect against HPV such as sexual abstinence, consistent and correct use of condoms,[7],[10] limiting the number of lifetime sexual partners, cultivating a monogamous relationship and having safe sexual habits.[62] Various studies have reported that viral vaccines that are licensed for use in humans are prophylactic against future challenge with the virus.[63],[64],[65],[66],[67],[68] According to Frazer, it is believed that all prophylactic vaccines work through the induction of virus-neutralising antibodies, and markedly reduce the number of cells that are infected after challenge with virus, and so prevent the clinical disease associated with infection.[63] If we put our concentration on vaccination and screening, we came across various studies, reporting that the WHO also recommends the inclusion of HPV vaccination in national immunisation programs provided HPV represents a public health priority and vaccine delivery is feasible and cost-effective.[69],[70],[71],[72],[73],[74] In another study, screening was found to be another way for early detection and treatment and is a cornerstone of prevention. It is also revealed that early diagnosis and treatment of cervical precancerous lesions prevents up to 80% of cervical cancers in high resource countries where cervical cancer screening is routine.[75] In a population-based study, conducted in 57countries in 2008 disclosed that 19% of women in developing countries were screened for cervical cancer in the preceding 3 years.[76] Although cervical cancer screening are not found available for many African countries, but a number of studies reported self-reported screening rates to be low ranging between 8.3% and 64%.[77],[78],[79] Screening rates were observed ranging between 9.4% and 80% among women accessing HIV care.[80],[81],[82],[83],[84],[85],[86],[87],[88],[89],[90],[91]

On the basis of studies considered, cervical cancer is becoming an epidemic, especially in developing countries. As HPV infections cause no symptoms, it is not easy to identify the disease so to improve the awareness about the disease and virus, government should initiate awareness campaign. As far as further research is concerned, research should be done keeping in view a combination of risk factors, for example, a women who had first cohabitation at early age and has many children, but she does not belong to low socioeconomic status then what would be the probability of getting the disease? Can it be controlled or diagnosed early if any combination of risk factor is taken into consideration?

 Conclusion



We may conclude that as it is sexually transmitted infection and causes no symptoms, so proper care should be taken in intimate hygiene management.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

References

1zur Hausen H. Papillomaviruses and cancer: From basic studies to clinical application. Nat Rev Cancer 2002;2:342-50.
2Ramqvist T, Grün N, Dalianis T. Human papillomavirus and tonsillar and base of tongue cancer. Viruses 2015;7:1332-43.
3Lacey CJ, Lowndes CM, Shah KV. Chapter 4: Burden and management of non-cancerous HPV-related conditions: HPV-6/11 disease. Vaccine 2006;24 Suppl 3:S3/35-41.
4Cogliano V, Baan R, Straif K, Grosse Y, Secretan B, El Ghissassi F, et al. Carcinogenicity of human papillomaviruses. Lancet Oncol 2005;6:204.
5Clifford GM, Smith JS, Plummer M, Muñoz N, Franceschi S. Human papillomavirus types in invasive cervical cancer worldwide: A meta-analysis. Br J Cancer 2003;88:63-73.
6Hoots BE, Palefsky JM, Pimenta JM, Smith JS. Human papillomavirus type distribution in anal cancer and anal intraepithelial lesions. Int J Cancer 2009;124:2375-83.
7Workowski KA. Centers for Disease Control and Prevention (CDC): Sexually transmitted diseases treatment guidelines, 2010. MMWR Recomm Rep 2010;59:1-110.
8Mammas IN, Sourvinos G, Spandidos DA. The paediatric story of human papillomavirus (Review). Oncol Lett 2014;8:502-6.
9Mammas IN, Vageli D, Spandidos DA. Geographic variations of human papilloma virus infection and their possible impact on the effectiveness of the vaccination programme. Oncol Rep 2008;20:141-5.
10Workowski KA, Bolan GA; Centers for Disease Control and Prevention. Sexually transmitted diseases treatment guidelines, 2015. MMWR Recomm Rep 2015;64:1-37.
11Satterwhite CL, Torrone E, Meites E, Dunne EF, Mahajan R, Ocfemia MC, et al. Sexually transmitted infections among US women and men: Prevalence and incidence estimates, 2008. Sex Transm Dis 2013;40:187-93.
12Doorbar 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:F55-70.
13International Human Papillomavirus Reference Center. Reference clones, Stockholm: Karolinska Institutet; Updated 2016.
14Nielsen A, Kjaer SK, Munk C, Iftner T. Type-specific HPV infection and multiple HPV types: Prevalence and risk factor profile in nearly 12,000 younger and older Danish women. Sex Transm Dis 2008;35:276-82.
15Skaaby S, Kofoed K. Anogenital warts in Danish men who have sex with men. Int J STD AIDS 2011;22:214-7.
16Owusu-Edusei K Jr., Chesson HW, Gift TL, Tao G, Mahajan R, Ocfemia MC, et al. The estimated direct medical cost of selected sexually transmitted infections in the United States, 2008. Sex Transm Dis 2013;40:197-201.
17Tota JE, Chevarie-Davis M, Richardson LA, Devries M, Franco EL. Epidemiology and burden of HPV infection and related diseases: Implications for prevention strategies. Prev Med 2011;53 Suppl 1:S12-21.
18Chaturvedi AK, Engels EA, Pfeiffer RM, Hernandez BY, Xiao W, Kim E, et al. Human papillomavirus and rising oropharyngeal cancer incidence in the United States. J Clin Oncol 2011;29:4294-301.
19Chouhy D, Bolatti EM, Pérez GR, Giri AA. Analysis of the genetic diversity and phylogenetic relationships of putative human papillomavirus types. J Gen Virol 2013;94:2480-8.
20de Villiers EM. Cross-roads in the classification of papillomaviruses. Virology 2013;445:2-10.
21Smelov V, Hanisch R, McKay-Chopin S, Sokolova O, Eklund C, Komyakov B, et al. Prevalence of cutaneous beta and gamma human papillomaviruses in the anal canal of men who have sex with women. Papillomavirus Res 2017;3:66-72.
22Ronco G, Arbyn M, Segnan N. Cervical screening according to age and HPV status. BMJ 2009;339:b3005.
23Moscicki AB, Widdice L, Ma Y, Farhat S, Miller-Benningfield S, Jonte J, et al. Comparison of natural histories of human papillomavirus detected by clinician- and self-sampling. Int J Cancer 2010;127:1882-92.
24Torres M, Gheit T, McKay-Chopin S, Rodríguez C, Romero JD, Filotico R, et al. Prevalence of beta and gamma human papillomaviruses in the anal canal of men who have sex with men is influenced by HIV status. J Clin Virol 2015;67:47-51.
25Donà MG, Gheit T, Latini A, Benevolo M, Torres M, Smelov V, et al. Alpha, beta and gamma Human Papillomaviruses in the anal canal of HIV-infected and uninfected men who have sex with men. J Infect 2015;71:74-84.
26Pierce Campbell CM, Messina JL, Stoler MH, Jukic DM, Tommasino M, Gheit T, et al. Cutaneous human papillomavirus types detected on the surface of male external genital lesions: A case series within the HPV Infection in Men Study. J Clin Virol 2013;58:652-9.
27Sichero L, El-Zein M, Nunes EM, Ferreira S, Franco EL, Villa LL, et al. Cervical infection with cutaneous beta and mucosal alpha papillomaviruses. Cancer Epidemiol Biomarkers Prev 2017;26:1312-20.
28Bottalico D, Chen Z, Dunne A, Ostoloza J, McKinney S, Sun C, et al. The oral cavity contains abundant known and novel human papillomaviruses from the Betapapillomavirus and Gammapapillomavirus genera. J Infect Dis 2011;204:787-92.
29Paolini F, Rizzo C, Sperduti I, Pichi B, Mafera B, Rahimi SS, et al. Both mucosal and cutaneous papillomaviruses are in the oral cavity but only alpha genus seems to be associated with cancer. J Clin Virol 2013;56:72-6.
30Forslund O, Johansson H, Madsen KG, Kofoed K. The nasal mucosa contains a large spectrum of human papillomavirus types from the Betapapillomavirus and Gammapapillomavirus genera. J Infect Dis 2013;208:1335-41.
31Markowitz 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;63:1-30.
32Parkin DM, Bray F. Chapter 2: The burden of HPV-related cancers. Vaccine 2006;24 Suppl 3:S3/11-25.
33Hartwig S, Syrjänen S, Dominiak-Felden G, Brotons M, Castellsagué X. Estimation of the epidemiological burden of human papillomavirus-related cancers and non-malignant diseases in men in Europe: A review. BMC Cancer 2012;12:30.
34Mehanna H, Jones TM, Gregoire V, Ang KK. Oropharyngeal carcinoma related to human papillomavirus. BMJ 2010;340:c1439.
35The Joint Committee on Vaccination and Immunisation (JCVI) Interim Statement on Extending HPV Vaccination to Adolescent Boys; 2017.
36Newman PA, Lacombe-Duncan A. Human papillomavirus vaccination for men: Advancing policy and practice. Future Virol 2014;9:1033-47.
37Gottvall M, Stenhammar C, Grandahl M. Parents' views of including young boys in the Swedish national school-based HPV vaccination programme: A qualitative study. BMJ Open 2017;7:e014255.
38Muhwezi WW, Banura C, Turiho AK, Mirembe F. Parents' knowledge, risk perception and willingness to allow young males to receive human papillomavirus (HPV) vaccines in Uganda. PLoS One 2014;9:e106686.
39Lee Mortensen G, Adam M, Idtaleb L. Parental attitudes towards male human papillomavirus vaccination: A pan-European cross-sectional survey. BMC Public Health 2015;15:624.
40Saraiya M, Unger ER, Thompson TD, Lynch CF, Hernandez BY, Lyu CW, et al. US assessment of HPV types in cancers: Implications for current and 9-valent HPV vaccines. J Natl Cancer Inst 2015;107:djv086.
41Sherman SM, Nailer E, Minshall C, Coombes R, Cooper J, Redman CW. Awareness and knowledge of HPV and cervical cancer in female students: A survey (with a cautionary note). J Obstet Gynaecol 2016;36:76-80.
42Perez S, Tatar O, Ostini R, Shapiro GK, Waller J, Zimet G, et al. Extending and validating a human papillomavirus (HPV) knowledge measure in a national sample of Canadian parents of boys. Prev Med 2016;91:43-9.
43Waller J, Ostini R, Marlow LA, McCaffery K, Zimet G. Validation of a measure of knowledge about human papillomavirus (HPV) using item response theory and classical test theory. Prev Med 2013;56:35-40.
44Perez S, Shapiro GK, Tatar O, Joyal-Desmarais K, Rosberger Z. Development and validation of the human papillomavirus attitudes and beliefs scale in a national Canadian sample. Sex Transm Dis 2016;43:626-32.
45Fu TC, Fu Xi L, Hulbert A, Hughes JP, Feng Q, Schwartz SM, et al. Short-term natural history of high-risk human papillomavirus infection in mid-adult women sampled monthly. Int J Cancer 2015;137:2432-42.
46Bernard HU, Burk RD, Chen Z, van Doorslaer K, zur Hausen H, de Villiers EM. Classification of papillomaviruses (PVs) based on 189 PV types and proposal of taxonomic amendments. Virology 2010;401:70-9.
47Burk RD, Harari A, Chen Z. Human papillomavirus genome variants. Virology 2013;445:232-43.
48Pande S, Jain N, Prusty BK. Human papillomavirus type 16 variant analysis of E6, E7, and L1 genes and long control region in biopsy samples from cervical cancer patients in North India. J Clin Microbiol 2008;46:10600-66.
49Ramas V, Mirazo S, Bonilla S, Ruchansky D, Arbiza J. Analysis of human papillomavirus 16 E6, E7 genes and Long Control Region in cervical samples from Uruguayan women. Gene 2018;654:103-9.
50Lehoux M, D'Abramo CM, Archambault J. Molecular mechanisms of human papillomavirus-induced carcinogenesis. Public Health Genomics 2009;12:268-80.
51Insinga RP, Dasbach EJ, Elbasha EH. Epidemiologic natural history and clinical management of Human Papillomavirus (HPV) Disease: A critical and systematic review of the literature in the development of an HPV dynamic transmission model. BMC Infect Dis 2009;9:119.
52Nunes EM, Sudenga SL, Gheit T, Tommasino M, Baggio ML, Ferreira S, et al. Diversity of beta-papillomavirus at anogenital and oral anatomic sites of men: The HIM Study. Virology 2016;495:33-41.
53Schmitt M, Bravo IG, Snijders PJ, Gissmann L, Pawlita M, Waterboer T. Bead-based multiplex genotyping of human papillomaviruses. J Clin Microbiol 2006;44:504-12.
54Gheit T, Billoud G, de Koning MN, Gemignani F, Forslund O, Sylla BS, et al. Development of a sensitive and specific multiplex PCR method combined with DNA microarray primer extension to detect Betapapillomavirus types. J Clin Microbiol 2007;45:2537-44.
55ICO Information Centre on HPV and Cancer. Human Papillomavirus and Related Diseases in India (Summary Report 2014). ICO Information Centre on HPV and Cancer; 2014. p. 8-22.
56Sreedevi A, Javed R, Dinesh A. Epidemiology of cervical cancer with special focus on India. Int J Womens Health 2015;7:405-14.
57Dhananjaya S. Current status of cancer burden: Global and Indian scenario. Biomed Res J 2014;1:1-5.
58IARC Working Group on the Evaluation of Carcinogenic Risk to Humans. Biological Agents. IARC Monographs on the Evaluation of Carcinogenic Riskto Humans, No. 100B. Lyon: IARC; 2012.
59Walboomers JM, Jacobs MV, Manos MM, Bosch FX, Kummer JA, Shah KV, et al. Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J Pathol 1999;189:12-9.
60Ferenczy A, Franco E. Persistent human papillomavirus infection and cervical neoplasia. Lancet Oncol 2002;3:11-6.
61Sherman SM, Nailer E. Attitudes towards and knowledge about Human Papillomavirus (HPV) and the HPV vaccination in parents of teenage boys in the UK. PLoS One 2018;13:e0195801.
62Yarbro CH. Cancer Nursing: Principles and Practice. 7th ed. Jones & Bartlett Learning. Burlington, MA: Jones & Bartlett Publishers; 2010.
63Frazer IH. Prevention of cervical cancer through papillomavirus vaccination. Nat Rev Immunol 2004;4:46-54.
64Aggarwal R, Gupta S, Nijhawan R, Suri V, Kaur A, Bhasin V, et al. Prevalence of high--risk human papillomavirus infections in women with benign cervical cytology: A hospital based study from North India. Indian J Cancer 2006;43:110-6.
65Miller D, Okolo CA, Mirabal Y, Guillaud M, Arulogun OS, Oladepo O, et al. Knowledge dissemination and evaluation in a cervical cancer screening implementation program in Nigeria. Gynecol Oncol 2007;107:S196-207.
66Arbyn M, Sasieni P, Meijer CJ, Clavel C, Koliopoulos G, Dillner J. Chapter 9: Clinical applications of HPV testing: A summary of meta-analyses. Vaccine 2006;24 Suppl 3:S3/78-89.
67Bang RA, Bang AT, Baitule M, Choudhary Y, Sarmukaddam S, Tale O. High prevalence of gynaecological diseases in rural Indian women. Lancet 1989;1:85-8.
68Basu PS, Sankaranarayanan R, Mandal R, Roy C, Das P, Choudhury D, et al. Visual inspection with acetic acid and cytology in the early detection of cervical neoplasia in Kolkata, India. Int J Gynecol Cancer 2003;13:626-32.
69Human papillomavirus vaccines: WHO position paper, October 2014. Wkly Epidemiol Rec 2014;89:465-91.
70Schensul SL, Mekki-Berrada A, Nastasi BK, Singh R, Burleson JA, Bojko M. Men's extramarital sex, marital relationships and sexual risk in urban poor communities in India. J Urban Health 2006;83:614-24.
71Sellors J, Sankaranarayanan R. Colposcopy and Treatment of Cervical Intraepithelial Neoplasia: A Beginners' Manual. Lyon: IARC Press; 2003.
72Sen A. The Delivery of Primary Health Services. A Study in West Bengal and Jharkhand. The Pratichi Health Report Number 1. TLM Books with Pratichi (India) Trust; 2005.
73Shanta V. Perspectives in Cervical Cancer prevention in India. The International Network for Cancer Treatment and Research; 2003.
74Shastri SS, Dinshaw K, Amin G, Goswami S, Patil S, Chinoy R, et al. Concurrent evaluation of visual, cytological and HPV testing as screening methods for the early detection of cervical neoplasia in Mumbai, India. Bull World Health Organ 2005;83:186-94.
75Sankaranarayanan R, Budukh AM, Rajkumar R. Effective screening programmes for cervical cancer in low-and middle-income developing countries. Bull World Health Organ 2001;79:954-62.
76Sankaranarayanan R, Nene BM, Shastri SS, Jayant K, Muwonge R, Budukh AM, et al. HPV screening for cervical cancer in rural India. N Engl J Med 2009;360:1385-94.
77Sankaranarayanan R, Esmy PO, Rajkumar R, Muwonge R, Swaminathan R, Shanthakumari S, et al. Effect of visual screening on cervical cancer incidence and mortality in Tamil Nadu, India: A cluster-randomised trial. Lancet 2007;370:398-406.
78Plotkin M, Besana GV, Yuma S, Kim YM, Kulindwa Y, Kabole F, et al. Integrating HIV testing into cervical cancer screening in Tanzania: An analysis of routine service delivery statistics. BMC Womens Health 2014;14:120.
79Finocchario-Kessler S, Wexler C, Maloba M, Mabachi N, Ndikum-Moffor F, Bukusi E. Cervical cancer prevention and treatment research in Africa: A systematic review from a public health perspective. BMC Womens Health 2016;16:29.
80Abotchie PN, Shokar NK. Cervical cancer screening among college students in Ghana: Knowledge and health beliefs. Int J Gynecol Cancer 2009;19:412-6.
81Maree JE, Lu XM, Wright SC. Combining breast and cervical screening in an attempt to increase cervical screening uptake. An intervention study in a South African context. Eur J Cancer Care (Engl) 2012;21:78-86.
82Mingo AM, Panozzo CA, DiAngi YT, Smith JS, Steenhoff AP, Ramogola-Masire D, et al. Cervical cancer awareness and screening in Botswana. Int J Gynecol Cancer 2012;22:638-44.
83Mupepi SC, Sampselle CM, Johnson TR. Knowledge, attitudes, and demographic factors influencing cervical cancer screening behavior of Zimbabwean women. J Womens Health (Larchmt) 2011;20:943-52.
84Tebeu PM, Major AL, Rapiti E, Petignat P, Bouchardy C, Sando Z, et al. The attitude and knowledge of cervical cancer by Cameroonian women; a clinical survey conducted in Maroua, the capital of Far North province of Cameroon. Int J Gynecol Cancer 2008;18:761-5.
85Lăără E, Day NE, Hakama M. Trends in mortality from cervical cancer in the Nordic countries: Association with organised screening programmes. Lancet 1987;1:1247-9.
86Laikangbam P, Sengupta S, Bhattacharya P, Duttagupta C, Dhabali Singh T, Verma Y, et al. A comparative profile of the prevalence and age distribution of human papillomavirus type 16/18 infections among three states of India with focus on northeast India. Int J Gynecol Cancer 2007;17:107-17.
87Legood R, Gray AM, Mahé C, Wolstenholme J, Jayant K, Nene BM, et al. Screening for cervical cancer in India: How much will it cost? A trial based analysis of the cost per case detected. Int J Cancer 2005;117:981-7.
88Londhe M, George SS, Seshadri L. Detection of CIN by naked eye visualization after application of acetic acid. Indian J Cancer 1997;34:88-91.
89Current Trends in Biotechnology and Pharmacy Mandal R, Mittal S, Basu P. 8:4; October, ISSN 0973-8916 (Print), 2230-7303 (Online).
90Ezechi OC, Gab-Okafor CV, Ostergren PO, Odberg Pettersson K. Willingness and acceptability of cervical cancer screening among HIV positive Nigerian women. BMC Public Health 2013;13:46.
91Rosser JI, Njoroge B, Huchko MJ. Cervical cancer screening knowledge and behavior among women attending an Urban HIV clinic in Western Kenya. J Cancer Educ 2015;30:567-72.