Archives of Medical Research
Volume 40, Issue 6 , Pages 486-492 , August 2009

Innovation in Cervical Cancer Prevention and Control in Mexico

  • Eduardo Lazcano-Ponce

      Affiliations

    • Center for Population Health Research, National Institute of Public Health, Mexico, D.F., Mexico
  • ,
  • Betania Allen-Leigh

      Affiliations

    • Reproductive Health Division, Center for Population Health Research, National Institute of Public Health, Mexico, D.F., Mexico
    • Corresponding Author InformationAddress reprint requests to: Dr. Betania Allen-Leigh, PhD, Reproductive Health Division, Center for Population Health Research, National Institute of Public Health, 7a Cerrada de Fray Pedro de Gante # 50, Colonia Seccion XVI, Delegacion Tlalpan, Mexico, D.F., Mexico, 14000; Phone: (+52) (55) 5487-1041; FAX: (+52) (55) 5573-0009.

Received 29 June 2009 ,Accepted 8 July 2009.

References 

  1. Newmann SJ, Garner EO. Social inequities along the cervical cancer continuum: a structured review. Cancer Causes Control. 2005;16:63–70
  2. Chu KC, Miller BA, Springfield SA. Measures of racial/ethnic health disparities in cancer mortality rates and the influence of socioeconomic status. J Natl Med Assoc. 2007;99:1092–11001102-1104
  3. Yabroff KR, Lawrence WF, King JC, et al. Geographic disparities in cervical cancer mortality: what are the roles of risk factor prevalence, screening, and use of recommended treatment?. J Rural Health. 2005;21:149–157
  4. Ward E, Jemal A, Cokkinides V, et al. Cancer disparities by race/ethnicity and socioeconomic status. CA Cancer J Clin. 2004;54:78–93
  5. Dietsch E, Gibb H, Francis K. Abnormal Pap test results and the rurality factor. Aust J Rural Health. 2003;11:50–56
  6. Friedell GH, Tucker TC, McManmon E, et al. Incidence of dysplasia and carcinoma of the uterine cervix in an Appalachian population. J Natl Cancer Inst. 1992;84:1030–1032
  7. Doescher MP, Jackson JE. Trends in cervical and breast cancer screening practices among women in rural and urban areas of the United States. J Public Health Manag Pract. 2009;15:200–209
  8. Binns PL, Condon JR. Participation in cervical screening by indigenous women in the Northern Territory: a longitudinal study. Med J Aust. 2006;185:490–494
  9. Wain G, Morrell S, Taylor R, et al. Variation in cervical cancer screening by region, socio-economic, migrant and indigenous status in women in New South Wales. Aust NZ J Obstet Gynaecol. 2001;41:320–325
  10. Coory MD, Fagan PS, Muller JM, et al. Participation in cervical cancer screening by women in rural and remote Aboriginal and Torres Strait Islander communities in Queensland. Med J Aust. 2002;177:544–547
  11. Palacio-Mejía LS, Rangel-Gómez G, Hernández-Avila M, et al. Cervical cancer, a disease of poverty: mortality differences between urban and rural areas in Mexico. Salud Publica Mex. 2003;45(suppl 3):S315–S325
  12. Bray F, Loos AH, McCarron P, et al. Trends in cervical squamous cell carcinoma incidence in 13 European countries: changing risk and the effects of screening. Cancer Epidemiol Biomarkers Prev. 2005;14:677–686
  13. Hristova L, Hakama M. Effect of screening for cancer in the Nordic countries on deaths, cost and quality of life up to the year 2017. Acta Oncol. 1997;36(suppl 9):1–60
  14. Peto J, Gilham C, Fletcher O, et al. The cervical cancer epidemic that screening has prevented in the UK. Lancet. 2004;364:249–456
  15. Sankaranarayanan R, Budukh AM, Rajkumar R. Effective screening programmes for cervical cancer in low- and middle-income developing countries. Bull World Health Organ. 2001;79:954–962
  16. Cuzick J, Arbyn M, Sankaranarayanan R, et al. Overview of human papillomavirus-based and other novel options for cervical cancer screening in developed and developing countries. Vaccine. 2008;26(suppl 10):K29–K41
  17. Gravitt PE, Coutlée F, Iftner T, et al. New technologies in cervical cancer screening. Vaccine. 2008;26(suppl 10):K42–K52
  18. Parkin DM, Almonte M, Bruni L, et al. Burden and trends of type-specific human papillomavirus infections and related diseases in the Latin American and Caribbean region. Vaccine. 2008;26(suppl 11):L1–L15
  19. Villa LL, Costa RL, Petta CA, et al. Prophylactic quadrivalent human papillomavirus (types 6, 11, 16 and 18) L1 virus-like particle vaccine in young women: a randomised double-blind placebo-controlled multicentre phase 11 efficacy trial. Lancet Oncol. 2005;6:271–278
  20. Harper D, Franco E, Wheeler C, et al. Efficacy of a bivalent L1 virus-like particle in prevention of infection with human papillomavirus types 16 and 18 in young women: a randomised controlled trial. Lancet. 2004;364:1757–1765
  21. Palacio-Mejía LS, Lazcano-Ponce E, Allen-Leigh B, et al. Diferencias regionales en la mortalidad por cáncer de mama y cérvix en México entre 1979 y 2006. Salud Publica Mex. 2009;51(suppl 2):S208–S219
  22. Lazcano-Ponce E, Palacio-Mejia LS, Allen-Leigh B, et al. Decreasing cervical cancer mortality in Mexico: effect of Papanicolaou coverage, birthrate, and the importance of diagnostic validity of cytology. Cancer Epidemiol Biomarkers Prev. 2008;17:2808–2817
  23. Salmerón J, Lazcano-Ponce E, Lorincz 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
  24. Eltoum IA, Roberson J. Impact of HPV testing, HPV vaccine development, and changing screening frequency on national Pap test volume: projections from the National Health Interview Survey (NHIS). Cancer. 2007;111:34–40
  25. Sherman ME, Lorincz AT, Scott DR, et al. Baseline cytology, human papillomavirus testing, and risk for cervical neoplasia: a 10 year cohort analysis. J Natl Cancer Inst. 2003;95:46–52
  26. Moriarty AT, Schwartz MR, Eversole G, et al. Human papillomavirus testing and reporting rates: practices of participants in the College of American Pathologists Interlaboratory Comparison Program in Gynecologic Cytology in 2006. Arch Pathol Lab Med. 2008;132:1290–1244
  27. Villa LL, Denny L. Methods for detection of HPV infection and its clinical utility. Int J Gyn Obstet. 2006;94(suppl 1):S71–S80
  28. Adams M, Jasani B, Fiander A. Human papilloma virus (HPV) prophylactic vaccination: challenges for public health and implications for screening. Vaccine. 2007;25:3007–3013
  29. Herrero R, Ferreccio C, Salmerón J, et al. New approaches to cervical cancer screening in Latin America and the Caribbean. Vaccine. 2008;26(suppl 11):L49–L58
  30. Ogilvie GS, Patrick DM, Schulzer M, et al. Diagnostic accuracy of self collected vaginal specimens for human papillomavirus compared to clinician collected human papillomavirus specimens: a meta-analysis. Sex Transm Infect. 2005;81:207–212
  31. Anhang R, Nelson JA, Telerant R, et al. Acceptability of self-collection of specimens for HPV DNA testing in an urban population. J Womens Health (Larchmt). 2005;14:721–728
  32. Dzuba IG, Díaz EY, Allen B, et al. The acceptability of self-collected samples for HPV testing vs. the pap test as alternatives in cervical cancer screening. J Womens Health Gend Based Med. 2002;11:265–275
  33. Waller J, McCaffery K, Forrest S, et al. Acceptability of unsupervised HPV self-sampling using written instructions. J Med Screen. 2006;13:208–213
  34. Barata PC, Mai V, Howlett R, et al. Discussions about self-obtained samples for HPV testing as an alternative for cervical cancer prevention. J Psychosom Obstet Gynaecol. 2008;29:251–257
  35. Wikström I, Stenvall H, Wilander E. Attitudes to self-sampling of vaginal smear for human papilloma virus analysis among women not attending organized cytological screening. Acta Obstet Gynecol Scand. 2007;86:720–725
  36. Lazcano-Ponce EC, Moss S, Alonso de Ruíz P, et al. Cervical cancer screening in developing countries: why is it ineffective? The case of Mexico. Arch Med Res. 1999;30:240–250
  37. Lazcano-Ponce EC, Alonso de Ruíz P, López-Carrillo L, et al. Validity and reproducibility of cytologic diagnosis in a sample of cervical cancer screening centers in Mexico. Acta Cytol. 1997;41:277–284
  38. Lazcano-Ponce EC, de Ruiz PA, Lopez-Carrillo L, et al. Quality control study on negative gynecological cytology in Mexico. Diagn Cytopathol. 1994;10:10–14
  39. Krieger P, Naryshkin S. Random rescreening of cytologic smears: a practical and effective component of quality assurance programs in both large and small cytology laboratories. Acta Cytol. 1994;38:291–298
  40. Lazcano-Ponce EC, Buiatti E, Nájera-Aguilar P, Alonso-de-Ruiz P, et al. Evaluation model of the Mexican national program for early cervical cancer detection and proposals for a new approach. Cancer Causes Control. 1998;9:241–251
  41. Madrigal de la Campa Mde L, Lazcano Ponce EC, Infante Castañeda C. Overuse of colposcopy service in Mexico. Ginecol Obstet Mex. 2005;73:637–647
  42. Deizell JE, Pereira SL, Ruplinger J. Colposcopy 101: a didactic curriculum to complement the clinical experience. Fam Med. 2001;33:658–660
  43. Caruthers BS, Sheets KJ. Development of a curriculum in colposcopy. J Fam Pract. 1991;32:590–597
  44. Spitzer M, Apgar BS, Brotzman GL, et al. Residency training in colposcopy: a survey of program directors in obstetrics and gynecology and family practice. Am J Obstet Gynecol. 2001;185:507–513
  45. Brotzman GL, Apgar BS. Assessing colposcopic skills: the instructor's handbook. Fam Med. 1998;30:350–355
  46. Pagliusi SR, Dillner J, Pawlita M, et al. Chapter 23: International Standard reagents for harmonization of HPV serology and DNA assays–an update. Vaccine. 2006;24(suppl 3):193–200
  47. Lowy DR, Solomon D, Hildesheim A, et al. Human papillomavirus infection and the primary and secondary prevention of cervical cancer. Cancer. 2008;113(7 suppl):1980–1993
  48. Kotaniemi-Talonen L, Malila N, Nieminen P, et al. Test positivity cutoff level of a high risk human papillomavirus test could be increased in routine cervical cancer screening. Int J Cancer. 2008;123:2902–2906
  49. Jhala D, Eltoum I. Barriers to adoption of recent technology in cervical screening. Cytojournal. 2007;4:16
  50. Zapka JG, Puleo E, Taplin S, et al. Breast and cervical cancer screening: clinicians' views on health plan guidelines and implementation efforts. J Natl Cancer Inst Monogr. 2005;35:46–54
  51. Goins KV, Zapka JG, Geiger AM, et al. Implementation of systems strategies for breast and cervical cancer screening services in health maintenance organizations. Am J Manag Care. 2003;9:745–755
  52. Dabash R, Vajpayee J, Jacob M, et al. A strategic assessment of cervical cancer prevention and treatment services in 3 districts of Uttar Pradesh. India. Reprod Health. 2005;2:11
  53. Arillo-Santillan E, Nigenda G, Sanchez-Prado VM, et al. Mexico City physicians' awareness about cervical cancer prevention: implications for cancer screening. J Cancer Educ. 2001;16:75–79
  54. Gany F, Trinh-Shevrin C, Aragones A. Cancer screening and Haitian immigrants: the primary care provider factor. J Immigr Minor Health. 2008;10:255–261
  55. Shell R, Tudiver F. Barriers to cancer screening by rural Appalachian primary care providers. J Rural Health. 2004;20:368–373
  56. Ka'ano'i ME, Braun KL, Gotay CC. Primary care physicians' knowledge, attitudes and practices related to cancer screening and cancer prevention clinical trials. Pac Health Dialog. 2004;11:160–165
  57. Holland-Barkis P, Forjuoh SN, Couchman GR, et al. Primary care physicians' awareness and adherence to cervical cancer screening guidelines in Texas. Prev Med. 2006;42:140–145
  58. Goldzweig CL, Parkerton PH, Washington DL, et al. Primary care practice and facility quality orientation: influence on breast and cervical cancer screening rates. Am J Manag Care. 2004;10:265–272
  59. Ahmad F, Stewart DE, Cameron JI, et al. Rural physicians' perspectives on cervical and breast cancer screening: a gender-based analysis. J Womens Health Gend Based Med. 2001;10:201–208
  60. Cochran CR, Gorospe EC. Physician satisfaction in a cancer prevention program for low-income women in Nevada. Sci World J. 2007;7:177–186
  61. Gorospe EC, Cochran CR, Cabb EE. Factors for satisfaction among providers of ancillary health services in a community-based cancer prevention program: a pilot study in Nevada. Sci World J. 2006;6:727–733
  62. Laurant M, Reeves D, Hermens R, et al. Substitution of doctors by nurses in primary care. Cochrane Database Syst Rev. 2005;CD001271
  63. Dierick-van Daele AT, Metsemakers JF, Derckx EW, et al. Nurse practitioners substituting for general practitioners: randomized controlled trial. J Adv Nurs. 2009;65:391–401
  64. Horrocks S, Anderson E, Salisbury C. Systematic review of whether nurse practitioners working in primary care can provide equivalent care to doctors. BMJ. 2002;324:819–823
  65. Tsu VD, Levin CE. Making the case for cervical cancer prevention: what about equity?. Reprod Health Matters. 2008;16:104–112
  66. Goldie SJ, O'Shea M, Diaz M, et al. Benefits, cost requirements and cost-effectiveness of the HPV16, 18 vaccine for cervical cancer prevention in developing countries: policy implications. Reprod Health Matters. 2008;16:86–96
  67. Perez G, Lazcano-Ponce E, Hernandez-Avila M, et al. Safety, immunogenicity, and efficacy of quadrivalent human papillomavirus (types 6, 11, 16, 18) L1 virus-like-particle vaccine in Latin American women. Int J Cancer. 2008;122:1311–1318
  68. Joura EA, Leodolter S, Hernandez-Avila M, et al. Efficacy of a quadrivalent prophylactic human papillomavirus (types 6, 11, 16, and 18) L1 virus-like-particle vaccine against high-grade vulval and vaginal lesions: a combined analysis of three randomised clinical trials. Lancet. 2007;369:1693–1702
  69. Paavonen J, Jenkins D, Bosch FX, et al. Efficacy of a prophylactic adjuvanted bivalent L1 virus-like-particle vaccine against infection with human papillomavirus types 16 and 18 in young women: an interim analysis of a phase III double-blind, randomised controlled trial. Lancet. 2007;369:2161–2170
  70. Hildesheim A, Herrero R, Wacholder S, et al. Effect of human papillomavirus 16/18 L1 viruslike particle vaccine among young women with preexisting infection: a randomized trial. JAMA. 2007;298:743–753
  71. Giuliano AR, Lazcano-Ponce E, Villa L, et al. Impact of baseline covariates on the immunogenicity of a quadrivalent (types 6, 11, 16, and 18) human papillomavirus virus-like-particle vaccine. J Infect Dis. 2007;196:1153–1162
  72. Reisinger KS, Block SL, Lazcano-Ponce E, et al. Safety and persistent immunogenicity of a quadrivalent human papillomavirus types 6, 11, 16, 18 L1 virus-like particle vaccine in preadolescents and adolescents: a randomized controlled trial. Pediatr Infect Dis J. 2007;26:201–209
  73. Schiller JT, Castellsagué X, Villa LL, et al. An update of prophylactic human papillomavirus L1 virus-like particle vaccine clinical trial results. Vaccine. 2008;26(suppl 10):K53–K61
  74. Kovács K, Varnai AD, Bollmann M, et al. Prevalence and genotype distribution of multiple human papillomavirus infection in the uterine cervix: a 7.5 year longitudinal study in a routine cytology-based screening population in West Germany. J Med Virol. 2008;80:1814–1823
  75. Sigurdsson K, Sigvaldason H, Gudmundsdottir T, et al. The efficacy of HPV 16/18 vaccines on sexually active 18–23 year old women and the impact of HPV vaccination on organized cervical cancer screening. Acta Obstet Gynecol Scand. 2008;88:27–35
  76. Rambout L, Hopkins L, Hutton B, et al. Prophylactic vaccination against human papillomavirus infection and disease in women: a systematic review of randomized controlled trials. CMAJ. 2007;177:469–479
  77. Dessy FJ, Giannini SL, Bougelet CA, et al. Correlation between direct ELISA, single epitope-based inhibition ELISA and pseudovirion-based neutralization assay for measuring anti-HPV-16 and anti-HPV-18 antibody response after vaccination with the AS04-adjuvanted HPV-16/18 cervical cancer vaccine. Hum Vaccine. 2008;4:425–434
  78. Chesson HW, Forhan SE, Gottlieb SL, et al. The potential health and economic benefits of preventing recurrent respiratory papillomatosis through quadrivalent human papillomavirus vaccination. Vaccine. 2008;26:4513–4518
  79. Andrews E, Seaman WT, Webster-Cyriaque J. Oropharyngeal carcinoma in non-smokers and non-drinkers: a role for HPV. Oral Oncol. 2009;45:486–491
  80. Feltkamp MC, de Koning MN, Bavinck JN, et al. Betapapillomaviruses: innocent bystanders or causes of skin cancer. J Clin Virol. 2008;43:353–360
  81. Paavonen J. Future II Study Group. Baseline demographic characteristics of subjects enrolled in international quadrivalent HPV (types 6/11/16/18) vaccine clinical trials. Curr Med Res Opin. 2008;24:1623–1634

PII: S0188-4409(09)00133-7

doi: 10.1016/j.arcmed.2009.07.007

Archives of Medical Research
Volume 40, Issue 6 , Pages 486-492 , August 2009