Cervical cancer in resource-limited settings: preventable but not yet prevented

References

• Ferlay J, Bray F, Pisani P, Parkin DM; GLOBOCAN 2002 (Eds). Cancer incidence, mortality and prevalence worldwide. Version 2.0 IARC Cancer Base No. 5. International Agency for Research on Cancer Press, Lyon, France (2004).
   Google Scholar
• Parkin DM. The global health burden of infection-associated cancers in the year 2002. Int. J. Cancer118, 3030–3044 (2006).
   PubMed Web of Science ®Google Scholar
• Parkin DM, Whelan SL, Ferlay J, Teppo L, Thomas DB (Eds). Cancer incidence in five continents. VIII IARC Scientific Publication No.155. International Agency for Research on Cancer Press, Lyon, France (2002).
   Google Scholar
• Walboomers JM, Jacobs MV, Manos MM et al. Human papilloma virus is a necessary cause of invasive cervical cancer worldwide. J. Pathol.189, 12–19 (1999).
   PubMed Web of Science ®Google Scholar
• Munoz N, Bosch FX, de Sanajose S et al. Epidemiological classification of human papilloma virus types associated with cervical cancer. N. Engl. J. Med.348, 518–527 (2003).
   PubMed Web of Science ®Google Scholar
• Clifford GM, Smith JS, Plummer M, Munoz N, Franceschi S. Human papilloma virus types in invasive cervical cancer worldwide: meta-analysis. Br. J. Cancer88, 63–73 (2003).
   PubMed Web of Science ®Google Scholar
• Speck LM, Tyring SK. Vaccine for the prevention of HPV infection. Skin Therapy Lett.11, 1–3 (2006).
   PubMedGoogle Scholar
• Stanley M. Prophylactic HPV vaccines. J. Clin. Pathol. (2007) DOI: 10.1136/jcp.2006.040568 (Epub ahead of print).
   PubMed Web of Science ®Google Scholar
• Arbyn M, Dillner J. Review of current knowledge on HPV vaccination: an appendix to the European Guidelines for Quality Assurance in cervical cancer screening. J. Clin. Virol.38, 189–197 (2007).
   PubMed Web of Science ®Google Scholar
• Bradley J, Barone M, Mahe C, Lewis R, Luciani S. Delivering cervical cancer prevention services in low resource settings. Int. J. Gynecol. Obstet.89, S21–S29 (2005).
   PubMed Web of Science ®Google Scholar
• Wiwanitkit V. Screening for cervical cancer: results from Thailand. Asian Pac. J. Cancer Prev.7, 329–330 (2006).
   PubMedGoogle Scholar
• Ponten J, Adami HO, Bergstrom R et al. Strategies for global control of cervical cancer. Int. J. Cancer60, 1–26 (1995).
   PubMed Web of Science ®Google Scholar
• Denny L. The prevention of cervical cancer in developing countries. Br. J. Obstet. Gynaecol.112, 1204–1212 (2005).
   Google Scholar
• Braun V, Gavey N. Exploring the possibility of sexual–behavioral primary prevention interventions for cervical cancer. Aust. NZ J. Public Health22(3 Suppl.), 353–359 (1998).
   PubMed Web of Science ®Google Scholar
• Agurto I, Sandoval J, De La Rosa M, Guardado ME. Improving cervical cancer prevention in a developing country. Int. J. Qual. Health Care18, 81–86 (2006).
   PubMed Web of Science ®Google Scholar
• Frazer H. Chapter 8: HPV vaccines. Int. J. Gynecol. Obstet.94(Suppl. 1), S81–S88 (2006).
   Google Scholar
• Stanley M, Lowy DR, Frazer I. Chapter 12: prophylactic vaccines: underlying mechanisms. Vaccine24(Suppl. 3), S106–S113 (2006).
   PubMed Web of Science ®Google Scholar
• Goldie SJ, Kohli M, Grima D et al. Projected clinical benefits and cost–effectiveness of a human papillomavirus 16/18 vaccine. J. Natl Cancer Inst.96, 604–615 (2004).
   PubMed Web of Science ®Google Scholar
• Mahdavi A, Monk BJ. Vaccines against human papillomavirus and cervical cancer: promises and challenges. Oncologist10, 528–538 (2005).
   PubMed Web of Science ®Google Scholar
• Miller AB, Chamberlain J, Day NE et al. Report on a workshop of the UICC project on evaluation of screening for cancer. Int. J. Cancer46, 761–769 (1990).
   PubMed Web of Science ®Google Scholar
• US Preventive Services Task Force. Guide to Clinical Preventive Services (Second Edition). US Department of Health and Human Services, DC, USA (1996).
   Google Scholar
• Fahey MT, Irwig L, Macaskill P. Meta-analysis of Pap test accuracy. Am. J. Epidemiol.141, 680–689 (1995).
   PubMed Web of Science ®Google Scholar
• Mitchell MF, Schottenfeld D, Tortolera-Luna G, Cantor SB, Richard-Kortum R. Colposcopy for the diagnosis of squamous intra-epithelial lesions – a meta-analysis. Obstet. Gynecol.91, 616–631 (1998).
   Google Scholar
• Nanda K, McCrory DC, Myers ER, Bastian LA et al. Accuracy of the Papanicolaou test in screening for and follow up of cervical cytologic abnormalities: a systematic review. Ann. Intern. Med.132, 810–819 (2000).
   PubMed Web of Science ®Google Scholar
• Hakama M, Miller AB, Day NE (Eds). Screening for cancer of uterine cervix. IARC Scientific Publication No.76. International Agency for Research on Cancer, Lyon, France 47–60 (1986).
   Google Scholar
• Das DK, Murthy NS, Bhatnagar P et al. Efficacy of a hospital based cytology screening program. Neoplasma39, 381–384 (1992).
   PubMedGoogle Scholar
• WHO. National Cancer Control Programs: policies and managerial guidelines (Second Edition). WHO, Geneva, Switzerland (2002).
   Google Scholar
• Gupta S, Sodhani P, Halder K, Chachra KL, Sardana S, Singh V. Spectrum of epithelial cell abnormalities of uterine cervix in a cervical cancer screening program: implications for resource limited settings. Eur. J. Obstet. Gynecol. Reprod. Biol. (2006) DOI: 10.1016/j.ejogrb.2006.07.022 (Epub ahead of print).
   Google Scholar
• University of Zimbabwe/JHPIEGO Cervical Cancer Project. Visual inspection with acetic acid for cervical cancer screening: test qualities in primary care settings. Lancet353, 869–873 (1999).
   PubMed Web of Science ®Google Scholar
• Denny L, Kuhn L, Pollack A, Wainwright H, Wright T. Evaluation of alternative methods of cervical cancer screening in resource poor settings. Cancer89, 826–833 (2000).
   PubMed Web of Science ®Google Scholar
• Wright Jr TC, Denny L, Kuhn L, Pollack A, Lorincz A. HPV DNA testing of self-collected vaginal samples compared with cytologic screening to detect cervical cancer. JAMA283, 81–86 (2000).
   PubMed Web of Science ®Google Scholar
• Denny L, Kuhn L, Pollack A, Wright Jr TC. Direct visual inspection for cervical cancer screening: an analysis of factors influencing test performance. Cancer94, 1699–1707 (2002).
   PubMed Web of Science ®Google Scholar
• Cronje HS, Parham GP, Cooreman BF, de Beer A, Divall P, Bam RH. A comparison of four screening methods for cervical neoplasia in a developing country. Am. J. Obstet. Gynecol.188, 395–400 (2003).
   PubMed Web of Science ®Google Scholar
• Sankaranarayanan R, Thara S, Anjali S et al. Accuracy of conventional cytology: results from a multicentre screening study in India. J. Med. Screen.11, 77–84 (2004).
   PubMed Web of Science ®Google Scholar
• Shastri S, Dinshaw K, Amin G et al. Concurrent evaluation of visual, cytological and HPV testing screening methods in the early detection of cervical neoplasia in Mumbai, India. Bull. World Health Organ.83, 186–194 (2005).
   PubMed Web of Science ®Google Scholar
• Sodhani P, Gupta S, Sharma JK et al. Test characteristics of various screening modalities for cervical cancer: a feasibility study to develop an alternative strategy for resource limited settings. Cytopathology17, 348–352 (2006).
   PubMed Web of Science ®Google Scholar
• Koliopoulos G, Arbyn M, Martin-Hirsch P, Kyrgion M, Prendivill W, Paraskevaidis E. Diagnostic accuracy of human papilloma virus testing in primary cervical screening: a systematic review and meta-analysis of non-randomized studies. Gynecol. Oncol.104, 232–246 (2007).
   PubMed Web of Science ®Google Scholar
• Klinkamer PJ, Meerdung WJ, Rosier PF, Hanselaar R. Liquid based cervical cytology. Cancer99, 263–271 (2003).
   PubMed Web of Science ®Google Scholar
• Hutchinson ML, Zahniser DJ, Sherman ME et al. Utility of liquid based cytology for cervical carcinoma screening. Results of a population-based study conducted in a region of Costa Rica with a high incidence of cervical carcinoma. Cancer87, 48–55 (1999).
   PubMed Web of Science ®Google Scholar
• Suba EJ, Raab SS. Viet/American cervical cancer prevention project. Papanicolaou screening in developing countries: an idea whose time has come. Am. J. Clin. Pathol.121, 315–320 (2004).
   PubMed Web of Science ®Google Scholar
• Suba EJ, Murphy SK, Donnely AD, Furia LM, Huynh MLD, Raab SS. Systems analysis of real world obstacles to successful cervical cancer prevention in developing countries. Am. J. Public Health96, 480–487 (2006).
   PubMed Web of Science ®Google Scholar
• Sankaranarayanan R, Shyamalakumary B, Wesley R et al. Visual inspection as a screening test for cervical cancer control in developing countries. In: New Developments in Cervical Cancer Screening and Prevention. Franco E, Monosonego J (Eds). Blackwell Science, Oxford, UK 411–421 (1997).
   Google Scholar
• Ottaviano M, La Torre P. Examination of the cervix with the naked eye using acetic acid test. Am. J. Obstet. Gynecol.143, 139–142 (1982).
   PubMed Web of Science ®Google Scholar
• Cecchini S, Bonardi R, Mazzotta A, Grazzini G, Iossa A, Ciatto S. Testing cervicography and cervicoscopy as a screening test for cervical cancer. Tumori79, 22–25 (1993).
   PubMed Web of Science ®Google Scholar
• Megevand E, Denny L, Dehaeck K, Soeters R, Bloch B. Acetic acid visualization of the cervix: an alternative to cytologic screening. Obstet. Gynecol.88, 383–386 (1996).
   PubMed Web of Science ®Google Scholar
• Sankaranarayanan R, Wesley R, Somanathan T et al. Visual inspection of uterine cervix after application of acetic acid in the detection of cervical carcinoma and its precursors. Cancer83, 2150–2156 (1998).
   PubMed Web of Science ®Google Scholar
• Sankaranarayanan R, Shyamalakumary B, Wesley R, Sreedevi Amma N, Parkin DM, Nair MK. Visual inspection with acetic acid in the early detection of cervical cancer and precursors. Int. J. Cancer80, 161–163 (1999).
   PubMed Web of Science ®Google Scholar
• Belinson JL, Pretorius RG, Zhang WH, Wu LY, Qiao YL, Elson P. Cervical cancer screening by simple visual inspection after acetic acid. Obstet. Gynecol.98, 441–444 (2001).
   PubMed Web of Science ®Google Scholar
• Sankaranarayanan R, Rajkumar R, Theresa R et al. Initial results from a randomized trial of cervical visual screening in rural South India. Int. J. Cancer109, 461–467 (2004).
   PubMed Web of Science ®Google Scholar
• Sankaranarayanan R, Basu P, Wesley R et al. Accuracy of visual screening for cervical neoplasia: results from an IARC multicentric study in India and Africa. Int. J. Cancer110, 907–913 (2004).
   PubMed Web of Science ®Google Scholar
• Londhe M, George SS, Seshadri L. Detection of CIN by naked eye visualization after application of acetic acid. Indian J. Cancer34, 88–91 (1997).
   PubMedGoogle Scholar
• Sankaranarayanan R, Wesley R, Somanathan T et al. Performance of visual inspection after acetic acid application (VIA) in detection of cervical cancer precursors. Cancer83, 2150–2156 (1998).
   PubMed Web of Science ®Google Scholar
• Sarian LO, Derchain SF, Nand P et al. Evaluation of VIA, Lugol’s iodine (VILI), cervical cytology and HPV testing as cervical screening tools in Latin America. J. Med. Screen.12, 142–149 (2005).
   PubMed Web of Science ®Google Scholar
• Sankaranarayanan R, Nene BM, Dinshaw K et al. Early detection of cervical cancer by visual inspection methods: a summary of completed and ongoing studies in India. Salud. Publica. Mex.45, S274–S282 (2003).
   Google Scholar
• Sankaranarayanan R, Nene BM, Dinshaw K et al. A cluster randomized controlled trial of visual, cytology and HPV screening for the cervix in rural India. Int. J. Cancer116, 617–623 (2005).
   PubMed Web of Science ®Google Scholar
• Sankaranarayanan R, Shastri SS, Basu P et al. The role of low-level magnification in visual inspection with acetic acid for early detection of cervical neoplasia. Cancer Detect. Prev.28, 345–351 (2004).
   PubMedGoogle Scholar
• Bluementhal PD, Lauterbach M, Sellors JW, Sankaranarayan R. Training for cervical cancer prevention programs in low resource settings: focus on visual inspection with acetic acid. Int. J. Gynecol. Obstet.89, S30–S37 (2005).
   Google Scholar
• Vernon SD, Unger ER, Williams D. Comparison of HPV detection and typing by cell sequencing, line blotting and hybrid capture. J. Clin. Microbiol.38, 651–655 (2000).
   PubMed Web of Science ®Google Scholar
• Davies P, Kornegay J, Iftner T. Current methods of testing for human papilloma virus. Best Pract. Res. Clin. Obstet. Gynecol.15, 677–700 (2001).
   PubMed Web of Science ®Google Scholar
• van den Brule AJ, Pol R, Fransen-Daalmeijer N, Schoulsw LM, Meijer CJ, Snijders PJ. GP 5+ 6- PCR followed by reverse line blot analyses rapid and high throughput identification of HPV genotypes. J. Clin. Microbiol.40, 779–787 (2002).
   PubMed Web of Science ®Google Scholar
• Womack SD, Chirenje IM, Blumenthal PD et al. Evaluation of human papilloma virus assay in cervical screening in Zimbabwe. Br. J. Obstet. Gynecol.107, 33–38 (2000).
   Google Scholar
• Franco EL. Primary screening of cervical cancer with human papilloma virus tests. J. Natl Cancer Inst. Monographs31, 89–96 (2000).
   Google Scholar
• Sankaranarayanan R, Chatterji R, Shastri SS et al. Accuracy of human papilloma virus testing in the primary screening of cervical neoplasia. Results from a multicentric study in India. Int. J. Cancer112, 341–347 (2004).
   PubMed Web of Science ®Google Scholar
• Belinson J, Qiao Y, Pretorius R et al. Prevalence of cervical cancer and feasibility of screening in rural China: a pilot study for the Shanzi province cervical cancer screening study. Int. J. Gyn. Cancer9, 411–417 (1999).
   PubMed Web of Science ®Google Scholar
• Van Ham MA, Bakkers JM, Harbers GK, Quint WG, Masuger LF, Melchers WJ. Comparison of two commercial assays for detection of human papillomavirus (HPV) in cervical scrape specimens: validation of the Roche AMPLICOR HPV test as a means to screen for HPV genotypes associated with a higher risk of cervical disorders. J. Clin. Microbiol.43, 2662–2667 (2005).
   PubMed Web of Science ®Google Scholar
• Molijn A, Kleter B, Quint WG, van Doorn LJ. Molecular diagnosis of human papillomavirus infections. J. Clin. Virol.32 (Suppl. 1), S43–S51 (2005).
   Web of Science ®Google Scholar
• Castle PE, Solomon D, Schiffman M, Wheeler CM. HPV type 16 infections and 2 year absolute risk of cervical precancer in women with equivocal or mild cytologic abnormalities. J. Natl Cancer Inst.97, 1066–1071 (2005).
   PubMed Web of Science ®Google Scholar
• Oh Y, Bae SM, Kim YW et al. Polymerase chain reaction-based fluorescent Luminex assay to detect the presence of human papillomavirus types. Cancer Sci.98, 549–554 (2007).
   PubMed Web of Science ®Google Scholar
• van Hamont D, Van Ham MAPC, Bakkers JMJE, Massuger LFAG, Melchers WJG. Evaluation of the SPF10 INNO LiPA human papillomavirus (HPV) genotyping test and the Roche Linear Array HPV genotyping test. J. Clin. Microbiol.44, 3122–3129 (2006).
   PubMed Web of Science ®Google Scholar
• Karwalajtys T, Howard M, Sellors JW, Kaczorowski J. Vaginal self-sampling virus physician cervical sampling for HPV among younger and older women. Sex. Infect.82, 337–339 (2006).
   PubMed Web of Science ®Google Scholar
• Sellors JW, Lorincz AT, Mahony B et al. Comparison of self-collected vaginal, vulvar and urine samples with physician-collected cervical samples for HPV testing to detect HSIL. Can. Med. Assoc. J.163, 513–518 (2000).
   PubMed Web of Science ®Google Scholar
• Gupta A, Arora R, Gupta S et al. HPV DNA in urine samples of women with or without cervical cancer and their male partners compared with simultaneously collected cervical/penile smear or biopsy specimens. J. Clin. Virol.37, 190–194 (2006).
   PubMed Web of Science ®Google Scholar
• Geddy PM, Wells M, Lacey CJ. Lack of detection of HPV DNA in male urine samples. Genitourin. Med.69, 276–279 (1993).
   PubMedGoogle Scholar
• Denny L, Kuhn L, Risi L et al. Two stage cervical cancer screening: an alternative for resource poor settings. Am. J. Obstet. Gynecol.183, 383–388 (2000).
   PubMed Web of Science ®Google Scholar
• Wright TC, Schiffman M, Solomon D et al. Interim guidance for the use of HPV DNA testing as an adjunct to cervical cytology for screening. Obstet. Gynecol.103, 304–309 (2004).
   PubMed Web of Science ®Google Scholar
• Rebello G, Hallam N, Smart G, Farquharson D, McCafferty J. Human papilloma virus testing and the management of women with mildly abnormal cervical smears: an observational study. Br. Med. J.322, 893–894 (2001).
   PubMedGoogle Scholar
• Cuzic J, Szarewski A, Cubie HD et al. Management of women who test positive for high-risk types of human papilloma virus: the HART study. Lancet362, 1871–1876 (2003).
   PubMed Web of Science ®Google Scholar
• Bulkmans NW, Rozendaal L, Snijders PJ et al. POBASCAM, a population based randomized control trial for implementation of high-risk HPV testing in cervical screening: design, methods and baseline data of 44102 women. Int. J. Cancer110, 94–101 (2004).
   PubMed Web of Science ®Google Scholar
• Mitchell MF, Totolero-Luna G, Cook E, Whitaker L, Rhodes-Morris H, Silva E. A randomized clinical trial of cryotherapy, laser vaporization and loop electrosurgical excision for treatment of squamous intraepithelial lesions of the cervix. Obstet. Gynecol.92, 737–744 (1998).
   PubMed Web of Science ®Google Scholar
• Gaffikin L, Blumenthal PD, Emerson M, Limpaphayom K. Safety, acceptability and feasibility of a single visit approach to cervical cancer prevention in rural Thailand: a demonstration project. Lancet361, 814–820 (2003).
   PubMed Web of Science ®Google Scholar
• Goldie SJ, Kuhn L, Denny L, Pollack A, Wright TC. Policy analysis of cervical cancer screening strategies in low resource settings: clinical benefits and cost–effectiveness. JAMA285, 3107–3115 (2001).
   PubMed Web of Science ®Google Scholar
• Denny L, Kuhn L, DeSouza M, Pollack A, Dupree W, Wright TC Jr. Screen-and-treat approaches for cervical cancer prevention in low-resource settings: a randomized controlled trial. JAMA294, 2173–2181 (2005).
   PubMed Web of Science ®Google Scholar
• Goldie SJ, Gaffikin L, Goldhaber-Fiebert JD et al. Cost–effectiveness of cervical cancer screening in five developing countries. N. Engl. J. Med.350, 2158–2168 (2005).
   Google Scholar
• Mandelblatt JS, Lawrence WF, Gaffikin L et al. Cost and benefits of different strategies to screen for cervical cancer in less developed countries. J. Natl Cancer Inst.94, 1469–1483 (2002).
   PubMedGoogle Scholar
• Legood R, Gray AM, Mahe C 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. Cancer117, 981–982 (2005).
   PubMed Web of Science ®Google Scholar
• Tsu VD, Pollack AE. Preventing cervical cancer in low resource settings. How far have we come and what does future hold? Int. J. Gynecol. Obstet.89, 555–559 (2005).
   Google Scholar