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Crossing the quality chasm: a requirement for successful cervical cancer prevention in developing countries

      Cervical cancer is the leading cause of cancer-related death among women in many developing countries, where over 80% of new cases of cervical cancer occur [
      • Pisani P.
      • Bray F.
      • Parkin D.M.
      Estimates of the world-wide prevalence of cancer for 25 sites in the adult population.
      ]. Because global cancer rates could increase 50% by the year 2020 [
      ], the impact of this disease is likely to increase over time. Introduction of conventional Papanicolaou cytologic (Pap) screening services to populations naïve to screening reduces cervical cancer rates by 60% to 90% within 3 years of implementation; these reductions of incidence and mortality are consistent and dramatic across populations [

      Agency for Healthcare Research and Quality. Screening for cervical cancer. Systematic evidence review number 25. January 2002. Available at: http://www.ahrq.gov/clinic/prev/crvcainv.htm. Accessed March 1, 2004.

      ]. On a global scale, cervical cancer is therefore the most preventable form of cancer-related death among women. Although progress is optional in all settings, Pap screening services are feasible anywhere in the world where cervical screening is appropriate and should be implemented in high-risk communities with access to curative treatment services [
      • Suba E.J.
      • Raab S.S.
      The Viet/American Cervical Cancer Prevention Project. Papanicolaou screening in developing countries: an idea whose time has come.
      ]. Past failures of cervical screening in developing countries are attributable to failures in programmatic quality, rather than to technological limitations of the screening test [
      • Miller A.B.
      Quality assurance in screening strategies. Review.
      ]. A shift in paradigmatic focus from technology to quality is therefore mandatory in developing countries [
      • Suba E.J.
      • Raab S.S.
      The Viet/American Cervical Cancer Prevention Project. Papanicolaou screening in developing countries: an idea whose time has come.
      ,
      • Committee on Quality of Health Care in America
      Crossing the quality chasm: a new health system for the 21st century.
      ].
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      References

        • Pisani P.
        • Bray F.
        • Parkin D.M.
        Estimates of the world-wide prevalence of cancer for 25 sites in the adult population.
        Int J Cancer. 2002; 97: 72-81
      1. Stewart B.W. Kleihues P. Global cancer report. World Health Organization, Geneva (Switzerland)2003
      2. Agency for Healthcare Research and Quality. Screening for cervical cancer. Systematic evidence review number 25. January 2002. Available at: http://www.ahrq.gov/clinic/prev/crvcainv.htm. Accessed March 1, 2004.

        • Suba E.J.
        • Raab S.S.
        The Viet/American Cervical Cancer Prevention Project. Papanicolaou screening in developing countries: an idea whose time has come.
        Am J Clin Pathol. 2004; 121: 315-320
        • Miller A.B.
        Quality assurance in screening strategies. Review.
        Virus Res. 2002; 89: 295-299
        • Committee on Quality of Health Care in America
        Crossing the quality chasm: a new health system for the 21st century.
        National Academy Press, Washington, DC2001
      3. Institute of Medicine.
        in: Lohr K.N. Medicare: a strategy for quality assurance. National Academy Press, Washington, DC1990
        • Brown R.W.
        Why is quality assurance so difficult? A review of issues in quality assurance over the last decade.
        Intern Med J. 2002; 32: 331-337
        • Iezzoni L.I.
        Monitoring quality of care: what do we need to know?.
        Inq. 1993; 30: 112-114
        • Renshaw A.A.
        Rescreening in cervical cytology for quality control. When bad data is worse than no data or what works, what doesn't, and why.
        Clin Lab Med. 2003; 23: 695-708
        • Suba E.J.
        • Raab S.S.
        The Viet/American Cervical Cancer Prevention Project. De novo establishment and cost-effectiveness of Papanicolaou cytology screening services in the Socialist Republic of Vietnam.
        Cancer. 2002; 94 ([author reply]): 2314-2316
        • Donabedian A.
        Evaluating the quality of medical care.
        Milbank Mem Fund Q. 1966; 44: 166-203
        • Arrossi S.
        • Sankaranarayanan R.
        • Parkin D.M.
        Incidence and mortality of cervical cancer in Latin America.
        Salud Publica Mex. 2003; 45: S306-S314
        • Parkin D.M.
        • Bray F.I.
        • Devesa S.S.
        Cancer burden in the year 2000. The global picture.
        Eur J Cancer. 2001; 37: s4-s66
        • Parkin D.M.
        The epidemiological basis for evaluating screening policies.
        in: Franco E. Monsonego J. New developments in cervical cancer screening and prevention. Blackwell Sciences, Oxford (U.K.)1997: 51-69
        • Robles S.C.
        • White F.
        • Peruga A.
        Trends in cervical cancer mortality in the Americas.
        Bull Pan Am Health Organ. 2002; 30: 290-301
        • Institute of Medicine
        Measuring the quality of health care.
        in: Donaldson M.S. National Academy Press, Washington, DC1999
        • Flisser A.
        • Garcia-Malo F.
        • Canepa Mde L.
        • Doncel S.
        • Espinoza R.
        • Moreno R.
        • et al.
        Implementation and evaluation of a national external quality control program for cervical cytology in Mexico.
        Salud Publica Mex. 2002; 44: 431-436
        • Garcia F.
        • Mendez de Galaz E.
        • Baldwin S.
        • Papenfuss M.
        • Giuliano A.R.
        • Hatch K.
        • et al.
        Factors that affect the quality of cytologic cervical cancer screening along the Mexico–United States border.
        Am J Obstet Gynecol. 2003; 189: 467-472
        • Ponten J.
        • Adami H.O.
        • Bergstrom R.
        • Dillner J.
        • Friberg L.G.
        • Gustafsson L.
        • et al.
        Strategies for global control of cervical cancer.
        Int J Cancer. 1995; 60: 1-26
        • Marrett L.D.
        • Robles S.
        • Ashbury F.D.
        • Green B.
        • Goel V.
        • Luciani S.
        A proposal for cervical screening information systems in developing countries.
        Int J Cancer. 2002; 102: 293-299
        • Miller A.B.
        Cervical cancer screening programmes: technical guidelines.
        World Health Organization, Geneva (Switzerland)1988
        • Stjernsward J.
        • Eddy D.
        • Luthra U.
        • Stanley K.
        Plotting a new course for cervical cancer screening in developing countries.
        World Health Forum. 1987; 8: 42-45
        • Pickle L.W.
        • Gillum R.G.
        Geographic variation in cardiovascular disease mortality in US blacks and whites.
        J Natl Med Assoc. 1999; 91: 545-556
        • Hoang Anh P.T.
        • Parkin D.M.
        • Hanh N.T.
        • Duc N.B.
        Cancer in the population of Hanoi, Vietnam, 1988–1990.
        Br J Cancer. 1993; 68: 1236-1242
        • Quoc N.M.
        • Hung N.C.
        • Parkin D.M.
        Cancer incidence in Ho Chi Minh City, Vietnam, 1995–1996.
        Int J Cancer. 1998; 76: 472-479
        • Anh P.T.H.
        • Hieu N.T.
        • Herrero R.
        • Vaccarella S.
        • Smith J.S.
        • Thuy N.T.
        • et al.
        Human papillomavirus infection among women in South and North Vietnam.
        Int J Cancer. 2003; 104: 213-220
        • Huynh M.L.D.
        • Raab S.S.
        • Suba E.J.
        Association between war and cervical cancer among Vietnamese women.
        Int J Cancer. 2004; (in press)
        • Suba E.J.
        • Hung N.C.
        • Duc N.B.
        • Raab S.S.
        Viet/American Cervical Cancer Prevention Project. De novo establishment and cost-effectiveness of Papanicolaou cytology screening services in the Socialist Republic of Vietnam.
        Cancer. 2001; 91: 928-939
        • Miller A.B.
        Cervical cancer screening programmes: managerial guidelines.
        World Health Organization, Geneva (Switzerland)1992
      4. Australian Institute of Health and Welfare. Cervical screening in Australia, 1998–1999. Available at: http://www.aihw.gov.au/publications/can/csa98-99/index.html. Accessed March 1, 2004.

        • Renshaw A.A.
        Measuring sensitivity in gynecologic cytology: a review.
        Cancer. 2002; 96: 210-217
        • Davey D.D.
        • McGoogan E.
        • Somrak T.M.
        • Allen K.A.
        • Beccati D.
        • Cramer S.F.
        • et al.
        Competency assessment and proficiency testing.
        Acta Cytol. 2000; 44: 939-943
      5. United States Congress. Clinical laboratory improvement amendments of 1988 (CLIA). Washington, DC; 1988. House Report 100–899.

        • Hindman W.M.
        An approach to the problem of false negatives in gynecologic cytologic screening.
        Acta Cytol. 1989; 33: 814-818
        • Brooke D.
        • Dudding N.
        • Sutton J.
        Rapid (partial) prescreening of cervical smears: the quality control method of choice?.
        Cytopathology. 2002; 13: 191-199
        • Renshaw A.A.
        • Bellerose B.
        • DiNisco S.A.
        • Minter L.J.
        • Lee K.R.
        False negative rate of cervical cytologic smear screening as determined by rapid rescreening.
        Acta Cytol. 1999; 43: 344-350
        • Arbyn M.
        • Schenck U.
        • Ellison E.
        • Hanselaar A.
        Metaanalysis of the accuracy of rapid prescreening relative to full screening of pap smears.
        Cancer. 2003; 99: 9-16
        • Johnson E.J.
        National Co-ordinator of the NHS Cervical Screening Programme (NHSCSP). Achievable standards, benchmarks for reporting, and criteria for evaluating cervical cytopathology. 2nd edition including revised performance indicators.
        Cytopathology. 2000; 11: 212-241
        • Krieger P.A.
        • McGoogan E.
        • Vooijs G.P.
        • Amma N.S.
        • Cochand-Priollet B.
        • Colgan T.J.
        • et al.
        Quality assurance/control issues. International Academy of Cytology Task Force summary. Diagnostic Cytology Towards the 21st Century: An International Expert Conference and Tutorial.
        Acta Cytol. 1998; 42: 133-140
        • Jones B.A.
        • Davey D.D.
        Quality management in gynecologic cytology using interlaboratory comparison.
        Arch Pathol Lab Med. 2000; 124: 672-681
        • Xuan L.V.
        • Man P.D.
        • Truc N.Q.
        • Quoc N.M.
        • Trung N.S.
        • Vu V.V.
        • et al.
        Establishment and cost-effectiveness of Pap smear screening services in a developing country.
        Mod Pathol. 1999; 12 ([abstract]): 189A
        • Gupta D.K.
        • Komaromy-Hiller G.
        • Raab S.S.
        • Nath M.E.
        Interobserver and intraobserver variability in the cytologic diagnosis of normal and abnormal metaplastic squamous cells in pap smears.
        Acta Cytol. 2001; 45: 697-703
        • Berwick D.M.
        Quality of health care. Part 5: payment by capitation and the quality of care.
        N Engl J Med. 1996; 335: 1227-1231
        • Chassin M.R.
        • Hannan E.L.
        • DeBuono B.A.
        Benefits and hazards of reporting medical outcomes publicly.
        N Engl J Med. 1996; 334: 394-398
      6. United States Veterans Administration National Center for Patient Safety. Root cause analysis. Available at: http://www.patientsafety.gov/tools.html.

        • Condel J.L.
        • Sharbaugh D.T.
        • Raab S.S.
        Error-free pathology: applying lean production methods to anatomic pathology.
        Clin Lab Med. 2004; (in press)
        • Schneider V.
        • Henry M.R.
        • Jiminez-Ayala M.
        • Turnbull L.S.
        • Wright T.C.
        Cervical cancer screening, screening errors, and reporting.
        Acta Cytol. 2001; 45: 493-498
        • Lazcano-Ponce E.
        • Alonso P.
        • Ruiz-Moreno J.A.
        • Hernandez-Avila M.
        Recommendations for cervical cancer screening programs in developing countries. The need for equity and technological development.
        Salud Publica Mex. 2003; 45: S449-S462
        • Wright Jr., T.C.
        • Cox J.T.
        • Massad L.S.
        • Twiggs L.B.
        • Wilkinson E.J.
        ASCCP-Sponsored Consensus Conference. 2001 consensus guidelines for the management of women with cervical cytological abnormalities.
        JAMA. 2002; 287: 2120-2129
        • Richart R.M.
        • Sankaranarayanan R.
        • Robles S.
        • Wright Jr., T.C.
        Cervical cancer screening strategies for developing countries.
        Contemp Ob/Gyn. 2001; 71-79: 100-127
        • Denny L.
        • Kuhn L.
        • Pollack A.
        • Wainwright H.
        • Wright Jr., T.C.
        Evaluation of alternative methods of cervical cancer screening for resource-poor settings.
        Cancer. 2000; 89: 826-833
        • Wang L.
        Developing countries put cervical cancer tests to the test.
        J Natl Cancer Inst. 2002; 94: 245-247
        • Robyr R.
        • Nazeer S.
        • Vassilakos P.
        • Matute J.C.
        • Sando Z.
        • Halle G.
        • et al.
        Feasibility of cytology-based cervical cancer screening in rural Cameroon.
        Acta Cytol. 2002; 46: 1110-1116
        • Belinson J.L.
        • Qiao Y.
        • Pretorius R.
        • Zhang W.
        • Keaton K.
        • Elson P.
        • et al.
        Prevalence of cervical cancer and feasibility of screening in rural China: a pilot study for the Shanxi Province Cervical Cancer Screening Study.
        Int J Gynecol Cancer. 1999; 9: 411-417
        • Belinson J.
        • Qiao Y.L.
        • Pretorius R.
        • Zhang W.H.
        • Elson P.
        • Li L.
        • et al.
        Shanxi Province Cervical Cancer Screening Study: a cross-sectional comparative trial of multiple techniques to detect cervical neoplasia.
        Gynecol Oncol. 2001; 83: 439-444
        • Pan Q.
        • Belinson J.L.
        • Li L.
        • Pretorius R.G.
        • Qiao Y.L.
        • Zhang W.H.
        • et al.
        A thin-layer, liquid-based pap test for mass screening in an area of China with a high incidence of cervical carcinoma. A cross-sectional, comparative study.
        Acta Cytol. 2003; 47: 45-50
        • Schiffman M.
        • Herrero R.
        • Hildesheim A.
        • Sherman M.E.
        • Bratti M.
        • Wacholder S.
        • et al.
        HPV DNA testing in cervical cancer screening: results from women in a high-risk province of Costa Rica.
        JAMA. 2000; 283: 87-93
        • Wright Jr., T.C.
        • Denny L.
        • Kuhn L.
        • Pollack A.
        • Lorincz A.
        HPV DNA testing of self-collected vaginal samples compared with cytologic screening to detect cervical cancer.
        JAMA. 2000; 283: 81-86
        • University of Zimbabwe/JHPIEGO Cervical Cancer Project
        Visual inspection with acetic acid for cervical cancer screening: test qualities in a primary care setting.
        Lancet. 1999; 353: 869-873
        • Geisinger K.R.
        Obstacles to reducing cervical cancer in Vietnam.
        Am J Clin Pathol. 2004; 121: 313-314
      7. World Medical Association. Declaration of Helsinki: ethical principles for medical research involving human subjects. Available at: http://www.wma.net/e/policy/pdf/17c.pdf. Accessed March 1, 2004.

        • Denny L.
        • Kuhn L.
        • Pollack A.
        • Wright Jr., T.C.
        Direct visual inspection for cervical cancer screening.
        Cancer. 2002; 94: 1699-1707
        • Wright Jr., T.C.
        • Menton M.
        • Myrtle J.F.
        • Chow C.
        • Singer A.
        Visualization techniques (colposcopy, direct visual inspection, and spectroscopic and other visual methods). Summary of task force 7.
        Acta Cytol. 2002; 46: 793-800
        • Goldie S.J.
        • Kuhn L.
        • Denny L.
        • Pollack A.
        • Wright T.C.
        Policy analysis of cervical cancer screening strategies in low-resource settings: clinical benefits and cost-effectiveness.
        JAMA. 2001; 285: 3107-3115
        • Mandelblatt J.S.
        • Lawrence W.F.
        • Gaffikin L.
        • Limpahayom K.K.
        • Lumbiganon P.
        • Warakamin S.
        • et al.
        Costs and benefits of different strategies to screen for cervical cancer in less-developed countries.
        J Natl Cancer Inst. 2002; 94: 1469-1483
        • Brook R.H.
        • Lohr K.N.
        Efficacy, effectiveness, variations, and quality: boundary crossing research.
        Med Care. 1985; 23: 710-722
        • Sasieni P.
        • Cuzick J.
        • Boyle P.
        • Craddock P.
        • Hince T.
        • Kitchener H.
        • et al.
        Routine audit is an ethical requirement of screening.
        Br Med J. 2001; 322: 1179
        • Goldie S.J.
        • Kuhn L.
        • Denny L.
        • Pollack A.
        • Wright Jr., T.C.
        Cervical cancer screening in developing countries.
        JAMA. 2001; 286 ([letter]): 3079-3081
        • Belinson J.L.
        • Pretorius R.G.
        Cervical cancer screening by simple visual inspection after acetic acid.
        Obstet Gynecol. 2002; 99 ([letter]): 518
        • Suba E.J.
        • Raab S.S.
        Direct visual inspection for cervical cancer screening.
        Cancer. 2004; (in press)
        • Kuhn L.
        • Denny L.
        • Pollack A.
        • Lorincz A.
        • Richart R.M.
        • Wright T.C.
        Human papillomavirus DNA testing for cervical cancer screening in low-resource settings.
        J Natl Cancer Inst. 2000; 92: 818-825
        • Cuzick J.
        • Szarewski A.
        • Cubie H.
        • Hulman G.
        • Kitchener H.
        • Luesley D.
        • et al.
        Management of women who test positive for high-risk types of human papillomavirus: the HART study.
        Lancet. 2003; 362: 1871-1876
        • Coste J.
        • Cochand-Priollet B.
        • de Cremoux P.
        • Le Gales C.
        • Cartier I.
        • Molinie V.
        • et al.
        Cross-sectional study of conventional cervical smear, monolayer cytology, and human papillomavirus DNA testing for cervical cancer screening.
        BMJ. 2003; 326: 733-737
        • Kulasingam S.L.
        • Hughes J.P.
        • Kiviat N.B.
        • Mao C.
        • Weiss N.S.
        • Kuypers J.M.
        • et al.
        Evaluation of human papillomavirus testing in primary screening for cervical abnormalities: comparison of sensitivity, specificity, and frequency of referral.
        JAMA. 2002; 288: 1749-1757
        • Davidoff F.
        • DeAngelis C.D.
        • Drazen J.M.
        • Hoey J.
        • Hojgaard L.
        • Horton R.
        • et al.
        Sponsorship, authorship, and accountability.
        JAMA. 2001; 286: 1232-1234
        • Bekelman J.E.
        • Li Y.
        • Gross C.P.
        Scope and impact of financial conflicts of interest in biomedical research: a systematic review.
        JAMA. 2003; 289: 454-465
        • Belinson J.L.
        • Qiao Y.L.
        • Pretorius R.G.
        • Zhang W.H.
        • Rong S.D.
        • Huang M.N.
        • et al.
        Shanxi Province cervical cancer screening study II: self-sampling for high-risk human papillomavirus compared to direct sampling for human papillomavirus and liquid based cervical cytology.
        Int J Gynecol Cancer. 2003; 13: 819-826
        • Salmeron J.
        • Lazcano-Ponce E.
        • Lorincz A.
        • Hernandez M.
        • Hernandez P.
        • Leyva A.
        • et al.
        Comparison of HPV-based assays with Papanicolaou smears for cervical cancer screening in Morelos State, Mexico.
        Cancer Causes Control. 2003; 14: 505-512
        • The Appalachia Leadership Initiative on Cancer
        Sowing seeds in the mountains: community-based coalitions for cancer prevention and control.
        National Cancer Institute, Bethesda (MD)1994 (Publication #NIH 94–3779. p. 1)
        • Hutchinson M.L.
        • Zahniser D.J.
        • Sherman M.E.
        • Herrero R.
        • Alfaro M.
        • Bratti M.C.
        • 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.
        Cancer. 1999; 87: 48-55
        • Womack S.D.
        • Chirenje Z.M.
        • Blumenthal P.D.
        • Gaffikin L.
        • McGrath J.A.
        • Chipato T.
        • et al.
        Evaluation of a human papillomavirus assay in cervical screening in Zimbabwe.
        BJOG. 2000; 107: 33-38