The Japanese guideline for cervical cancer screening

Japanese Journal of Clinical Oncology

Volumn 40, Issue 6, 2010, Pages 485-502

  Hamashima, Chisato ^a   Aoki, Daisuke ^b   Miyagi, Etsuko ^c   Saito, Eiko ^d   Nakayama, Tomio ^e   Sagawa, Motoyasu ^f   Saito, Hiroshi ^a   Sobue, Tomotaka ^a  

^a NATIONAL CANCER CENTER   (Japan)

^b KEIO UNIVERSITY   (Japan)

^c YOKOHAMA CITY UNIVERSITY HOSPITAL   (Japan)

^d TOKYO ELECTRIC POWER COMPANY   (Japan)

^e OSAKA MEDICAL CENTER FOR CANCER AND CARDIOVASCULAR DISEASES   (Japan)

^f KANAZAWA MEDICAL UNIVERSITY   (Japan)

Author keywords

Cancer screening; Cervical cancer; Conventional cytology; Guideline; HPV testing; Liquid based cytology; Recommendation

Indexed keywords

CANCER SCREENING; COLPOSCOPY; GYNECOLOGIC SURGERY; HPV TESTING; HUMAN; JAPANESE; LIQUID BASED CYTOLOGY; LOOP ELECTROSURGICAL EXCISION PROCEDURE; PRACTICE GUIDELINE; REVIEW; SYSTEMATIC REVIEW; UTERINE CERVIX CANCER; UTERINE CERVIX CYTOLOGY; VIRUS DETECTION; CYTODIAGNOSIS; FEMALE; ISOLATION AND PURIFICATION; PAPILLOMA VIRUS; PAPILLOMAVIRUS INFECTION; SENSITIVITY AND SPECIFICITY; UTERINE CERVIX CARCINOMA IN SITU; UTERINE CERVIX TUMOR; VIROLOGY;

CERVICAL INTRAEPITHELIAL NEOPLASIA; CYTODIAGNOSIS; FEMALE; HUMANS; PAPILLOMAVIRIDAE; PAPILLOMAVIRUS INFECTIONS; SENSITIVITY AND SPECIFICITY; UTERINE CERVICAL NEOPLASMS;

EID: 77953425536     PISSN: 03682811     EISSN: 14653621     Source Type: Journal    
DOI: 10.1093/jjco/hyq036     Document Type: Review

References (95)

1. Center for Cancer Control and Information Services, National Cancer Center [Internet], Japan. http://ganjoho.ncc.go.jp/professional/statistics/index.html (cited 20 July 2008).
2. Hisamichi S, editor. Guidelines for Cancer Screening Programs. Tokyo: Japan Public Health Association 2001 (in Japanese).
3. Hamashima C, Saito H, Nakayama T, Nakayama T, Sobue T. The standardized development method of the Japanese guidelines for cancer screening. Jpn J Clinical Oncol 2008;38:288-95.
4. International Agency for Research on Cancer. IARC Handbooks of Cancer Prevention. Lyon, France: IARC Press 2005.
5. Berget A. Influence of population screening on morbidity and mortality of cancer of the uterine cervix in Maribo Amt. Danish Med Bull 1979;26:91-100.
6. Aklimunnessa K, Mori M, Khan MMH, Sakauchi F, Kubo T, Fujino Y, et al. Effectiveness of cervical cancer screening over cervical cancer mortality among Japanese women. Jpn J Clin Oncol 2006;36:511-8.
7. Ronco G, Pilutti S, Patriarca S, Montanari G, Ghiringhello B, Volante R, et al., Turin Cervical Screening Working Group. Impact of the introduction of organized screening for cervical cancer in Turin, Italy: cancer incidence by screening history 1992-98. Br J Cancer 2005;93:376-8.
8. Macgregor JE, Campbell MK, Mann EM, Swanson KY. Screening for cervical intraepithelial neoplasia in north east Scotland shows fall in incidence and mortality from invasive cancer with concomitant rise in preinvasive disease. Br Med J 1994;308:1407-11.
9. Sobue T, Suzuki T, Hashimoto S, Yokoi N, Fujimoto I. A case-control study of the effectiveness of cervical cancer screening in Osaka, Japan. Jpn J Cancer Res 1988;79:1269-75.
10. Macgregor JE, Moss SM, Parkin DM, Day NE. A case-control study of cervical cancer screening in north east Scotland. Br Med J (Clin Res Ed) 1985;290:1543-6.
11. Yang B, Morrell S, Zuo Y, Roder D, Tracey E, Jelfs P. A case-control study of the protective benefit of cervical screening against invasive cervical cancer in NSW women. Cancer Causes Control 2008;19: 569-76.
12. Hernández-Avila M, Lazcano-Ponce EC, de Ruíz PA, Romieu I. Evaluation of the cervical cancer screening programme in Mexico: a population-based case-control study. Int J Epidemiol 1998;27:370-6.
13. Sato S, Makino H, Yajima A, Fukao A. Cervical cancer screening in Japan. A case-control study. Acta Cytol 1997;41:1103-6.
14. Jiménez-Prez M, Thomas DB. Has the use of pap smears reduced the risk of invasive cervical cancer in Guadalajara, Mexico? Int J Cancer 1999;82:804-9.
15. Palli D, Carli S, Cecchini S, Venturini A, Piazzesi G, Buiatti E. A centralized cytology screening programme for cervical cancer in Florence. J Epidemiol Commun Health 1990;44:47-51.
16. Herrero R, Brinton LA, Reeves WC, Brenes MM, de Britton RC, Gaitan E, et al. Screening for cervical cancer in Latin America: a case-control study. Int J Epidemiol 1992;21:1050-6.
17. Celentano DD, Klassen AC, Weisman CS, Rosenshein NB. Duration of relative protection of screening for cervical cancer. Prev Med 1989;18:411-22.
18. Makino H, Sato S, Yajima A, Komatsu S, Fukao A. Evaluation of the effectiveness of cervical cancer screening: a case-control study in Miyagi, Japan. Tohoku J Exp Med 1995;175:171-8.
19. Magnus K, Langmark F, Andersen A. Mass screening for cervical cancer in Ostfold county of Norway 1959-77. Int J Cancer 1987;39:311-6.
20. Hakama M, Joutsenlahti U, Virtanen A, Räsänen-Virtanen U. Mass screenings for cervical cancer in Finland 1963-71. Organization, extent, and epidemiological implications. Ann Clin Res 1975;7:101-11.
21. Miller AB, Lindsay J, Hill GB. Mortality from cancer of the uterus in Canada and its relationship to screening for cancer of the cervix. Int J Cancer 1976;17:602-12.
22. Aareleid T, Pukkala E, Thomson H, Hakama M. Cervical cancer incidence and mortality trends in Finland and Estonia: a screened vs. an unscreened population. Eur J Cancer 1993;29A:745-9.
23. Johannesson G, Geirsson G, Day N. The effect of mass screening in Iceland, 1965-74, on the incidence and mortality of cervical carcinoma. Int J Cancer 1978;21:418-25.
24. Anderson GH, Boyes DA, Benedet JL, Le Riche JC, Matisic JP, Suen KC, et al. Organization and results of the cervical cytology screening programme in British Columbia, 1955-85. Br Med J (Clin Res Ed) 1988;296:975-8.
25. Pettersson F, Björkholm E, Näslund I. Evaluation of screening for cervical cancer in Sweden: trends in incidence and mortality 1958-1980. Int J Epidemiol 1985;14:521-7.
26. Duguid HL, Duncan ID, Currie J. Screening for cervical intraepithelial neoplasia in Dundee and Angus 1962-81 and its relation with invasive cervical cancer. Lancet 1985;2:1053-6.
27. Lǎǎrǎ E, Day NE, Hakama M. Trends in mortality from cervical cancer in the Nordic countries: association with organized screening programmes. Lancet 1987;1:1247-9.
28. Free K, Roberts S, Bourne R, Dickie G, Ward B, Wright G,et al. Cancer of the cervix-old and young, now and then. Gynecol Oncol 1991;43:129-36.
29. Gao CM, Kuroishi T, Hirose K, Tajima K, Tominaga S. An epidemiological evaluation of the efficacy of mass screening for uterine cancer in Japan. The relationship between coverage rate of mass screening and reduction in death rate from uterine cancer. Jpn J Public Health 1992;39:784-8 (in Japanese).
30. Levi F, La Vecchia C, Randimbison L, Te VC. Incidence, mortality and survival from invasive cervical cancer in Vaud, Switzerland, 1974-1991. Ann Oncol 1994;5:747-52.
31. Sato S, Matsunaga G, Konno R, Yajima A. Mass screening for cancer of the uterine cervix in Miyagi Prefecture, Japan. Effects and problems. Acta Cytol 1998;42:299-304.
32. Anttila A, Pukkala E, Söderman B, Kallio M, Nieminen P, Hakama M. Effect of organized screening on cervical cancer incidence and mortality in Finland, 1963-1995: recent increase in cervical cancer incidence. Int J Cancer 1999;83:59-65.
33. Vutuc C, Haidinger G, Waldhoer T, Ahmad F, Breitenecker G. Prevalence of self-reported cervical cancer screening and impact on cervical cancer mortality in Austria. Wien Klin Wochenschr 1999;111:354-9.
34. Bulk S, Visser O, Rozendaal L, Verheijen RH, Meijer CJ. Incidence and survival rate of women with cervical cancer in the Greater Amsterdam area. Br J Cancer 2003;89:834-9.
35. Comber H, Gavin A. Recent trends in cervical cancer mortality in Britain and Ireland: the case for population-based cervical cancer screening. Br J Cancer 2004;91:1902-4.
36. Sigurdsson K, Sigvaldason H. Effectiveness of cervical cancer screening in Iceland, 1964-2002: a study on trends in incidence and mortality and the effect of risk factors. Acta Obstet Gynecol Scand 2006;85:343-9.
37. van der Aa MA, Pukkala E, Coebergh JW, Anttila A, Siesling S. Mass screening programmes and trends in cervical cancer in Finland and the Netherlands. Int J Cancer 2008;122:1854-8.
38. Yoshida Y, Sato S, Okamura C, Nishino Y, Yajima A. Evaluating the accuracy of uterine cancer screening with the regional cancer registration system. Acta Cytol 2001;45:157-62.
39. Taylor S, Kuhn L, Dupree W, Denny L, De Souza M, Wright TC, Jr. Direct comparison of liquid-based and conventional cytology in a South African screening trial. Int J Cancer 2006;118:957-62.
40. Cochand-Priollet B, Cartier I, de Cremoux P, Le Galès C, Ziol M, Molinié V, et al. Cost-effectiveness of liquid-based cytology with or without hybrid-capture II HPV test compared with conventional Pap smears: a study by the French Society of Clinical Cytology. Diagn Cytopathol 2005;33:338-43.
41. Cecchini S, Piazzesi G, Carli S. Sensitivity of the screening program for cervical cancer in the Florence District. Gynecol Oncol 1989;33:182-4.
42. Mayrand MH, Duarte-Franco E, Rodrigues I, Walter SD, Hanley J, Ferenczy A, et al., Canadian Cervical Cancer Screening Trial Study Group. Human papillomavirus DNA versus Papanicolaou screening tests for cervical cancer. N Engl J Med 2007;357:1579-88.
43. Naucler P, Ryd W, Tornberg S, Strand A, Wadell G, Elfgren K, et al. Efficacy of HPV DNA testing with cytology triage and/or repeat HPV DNA testing in primary cervical cancer screening. J Natl Cancer Inst 2009;101:88-99.
44. Abulafia O, Pezzullo JC, Sherer DM. Performance of ThinPrep liquid-based cervical cytology in comparison with conventionally prepared Papanicolaou smears: a quantitative survey. Gynecol Oncol 2003;90:137-44.
45. Cuzick J, Clavel C, Petry KU, Meijer CJ, Hoyer H, Ratnam S, et al. Overview of the European and North American studies on HPV testing in primary cervical cancer screening. Int J Cancer 2006;119:1095-101.
46. Ioka A, Tsukuma H, Ajiki W, Oshima A. Influence of age on cervical cancer survival in Japan. Jpn J Clin Oncol 2005;35:464-9.
47. Strander B, Andersson-Ellström A, Milsom I, Rådberg T, Ryd W. Liquid-based cytology versus conventional Papanicolaou smear in an organized screening program: a prospective randomized study. Cancer 2007;111:285-91.
48. Belinson JL, Pan QJ, Biscotti C, Wu LY, Pretorius RG, Li L, et al. Primary screening with liquid-based cytology in an unscreened population in rural China, with an emphasis on reprocessing unsatisfactory samples. Acta Cytol 2002;46:470-4.
49. Ronco G, Giorgi-Rossi P, Carozzi F, Confortini M, Dalla Palma P, Del Mistro A, et al., New Technologies for Cervical Cancer Screening Working Group. Results at recruitment from a randomized controlled trial comparing human papillomavirus testing alone with conventional cytology as the primary cervical cancer screening test. J Natl Cancer Inst 2008;100:492-501.
50. Naucler P, Ryd W, Törnberg S, Strand A, Wadell G, Elfgren K, et al. Human papillomavirus and Papanicolaou tests to screen for cervical cancer. N Engl J Med 2007;357:1589-97.
51. Ronco G, Segnan N, Giorgi-Rossi P, Zappa M, Casadei GP, Carozzi F, et al., New Technologies for Cervical Cancer Working Group. Human papillomavirus testing and liquid-based cytology: results at recruitment from the new technologies for cervical cancer randomized controlled trial. J Natl Cancer Inst 2006;98:765-74.
52. Kotaniemi-Talonen L, Anttila A, Malila N, Tarkkanen J, Laurila P, Hakama M, et al. Screening with a primary human papillomavirus test does not increase detection of cervical cancer and intraepithelial neoplasia 3. Eur J Cancer 2008;44:565-71.
53. Guillaud M, Benedet JL, Cantor SB, Staerkel G, Follen M, MacAulay C. DNA ploidy compared with human papilloma virus testing (Hybrid Capture II) and conventional cervical cytology as a primary screening test for cervical high-grade lesions and cancer in 1555 patients with biopsy confirmation. Cancer 2006;107:309-18.
54. Bulk S, Bulkmans NW, Berkhof J, Rozendaal L, Boeke AJ, Verheijen RH, et al. Risk of high-grade cervical intra-epithelial neoplasia based on cytology and high-risk HPV testing at baseline and at 6-months. Int J Cancer 2007;121:361-7.
55. Schneider A, Hoyer H, Lotz B, Leistritza S, Kühne-Heid R, Nindl I, et al. Screening for high-grade cervical intra-epithelial neoplasia and cancer by testing for high-risk HPV, routine cytology or colposcopy. Int J Cancer 2000;89:529-34.
56. Sankaranarayanan R, Chatterji R, Shastri SS, Wesley RS, Basu P, Mahe C, et al. Accuracy of human papillomavirus testing in primary screening of cervical neoplasia: results from a multicenter study in India. Int J Cancer 2004;112:341-7.
57. Cuzick J, Szarewski A, Mesher D, Cadman L, Austin J, Perryman K, et al. Long-term follow-up of cervical abnormalities among women screened by HPV testing and cytology-Results from the Hammersmith study. Int J Cancer 2008;122:2294-300.
58. Bulkmans NW, Berkhof J, Rozendaal L, van Kemenade FJ, Boeke AJ, Bulk S, et al. Human papillomavirus DNA testing for the detection of cervical intraepithelial neoplasia grade 3 and cancer: 5-year follow-up of a randomized controlled implementation trial. Lancet 2007; 370:1764-72.
59. Ronco G, Giorgi-Rossi P, Carozzi F, Dalla Palma P, Del Mistro A, De Marco L, et al., New Technologies for Cervical Cancer screening Working Group. Human papillomavirus testing and liquid-based cytology in primary screening of women younger than 35 years: results at recruitment for a randomized controlled trial. Lancet Oncol 2006;7:547-55.
60. Holowaty P, Miller AB, Rohan T, To T. Natural history of dysplasia of the uterine cervix. J Natl Cancer Inst 1999;91:252-8.
61. Bruinsma F, Lumley J, Tan J, Quinn M. Precancerous changes in the cervix and risk of subsequent preterm birth. BJOG 2007;114:70-80.
62. El-Bastawissi AY, Becker TM, Daling JR. Effect of cervical carcinoma in situ and its management on pregnancy outcome. Obstet Gynecol 1999;93:207-12.
63. Jakobsson M, Gissler M, Sainio S, Paavonen J, Tapper AM. Preterm delivery after surgical treatment for cervical intraepithelial neoplasia. Obstet Gynecol 2007;109:309-13.
64. Kyrgiou M, Koliopoulos G, Martin-Hirsch P, Arbyn M, Prendiville W, Paraskevaidis E. Obstetric outcomes after conservative treatment for intraepithelial or early invasive cervical lesions: systematic review and meta-analysis. Lancet 2006;367:489-98.
65. Sjøborg KD, Vistad I, Myhr SS, Svenningsen R, Herzog C, Kloster-Jensen A, et al. Pregnancy outcome after cervical cone excision: a case-control study. Acta Obstet Gynecol Scand 2007;86:423-8.
66. Nøhr B, Tabor A, Frederiksen K, Kjaer SK. Loop electrosurgical excision of the cervix and the subsequent risk of preterm delivery. Acta Obstet Gynecol Scand 2007;86:596-603.
67. Sankaranarayanan 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.
68. Sankaranarayanan R, Nene BM, Dinshaw KA, Mahe C, Jayant K, Shastri SS, et al., Osmanabad District Cervical Screening Study Group. A cluster randomized controlled trial of visual, cytology and human papillomavirus screening for cancer of the cervix in rural India. Int J Cancer 2005;116:617-23.
69. Kitchener HC, Almonte M, Thomson C, Wheeler P, Sargent A, et al. HPV testing in combination with liquid-based cytology in primary cervical screening (ARTISTIC): a randomised controlled trial. Lancet Oncol 2009;10:672-82.
70. Ministry of Health, Labour and Welfare. Report from the National Screening Committee: Revision of the Programs for Breast and Cervical Cancer Screening based on the Law for the Health Law for the Aged. Tokyo, March 2004 (in Japanese).
71. Statistics and Information Department, Ministry of Health, Labour, and Welfare. National Reports on Cancer Screening Programs 2006. Tokyo: Health and Welfare Statistics Association 2008.
72. Arbyn M, Anttila A, Jordan J, Ronco G, Scheneck U, Seganan N, et al. European guidelines for quality assurance in cervical cancer screening. Luxembourg, International Agency for Research on Cancer 2008.
73. United States Preventive Services Task Force. Screening for cervical cancer: recommendations and rationale. AHRQ Pub.no.03-515A.2003.
74. ACOG Committee on Practice Bulletins. ACOG Practice Bulletin: clinical management guidelines for obstetrician-gynecologists. Number 45, August 2003. Cervical cytology screening. Obstet Gynecol 2003;102:417-27.
75. Wright TC, Jr, Schiffman M, Solomon D, Cox JT, Garcia F, Goldie S, et al. Interim guidance for the use of human papillomavirus DNA testing as an adjunct to cervical cytology for screening. Obstet Gynecol 2004;103:304-9.
76. Wright TC, Jr, Massad LS, Dunton CJ, Spitzer M, Wilkinson EJ, Solomon D, 2006 American Society for Colposcopy, Cervical Pathology-sponsored Consensus Conference. 2006 consensus guidelines for the management of women with abnormal cervical cancer screening tests. Am J Obstet Gynecol 2007;197:346-55.
77. Saslow D, Runowicz CD, Solomon D, Moscicki AB, Smith RA, Eyre HJ, et al. American Cancer Society guideline for the early detection of cervical neoplasia and cancer. CA Cancer J Clin 2002;52:342-62.
78. Smith RA, Cokkinides V, Brawley OW. Cancer screening in the United States, 2009: a review of current American Cancer Society guidelines and issues in cancer screening. CA Cancer J Clin 2009;59:27-41.
79. ACOG Committee on Practice Bulletins. ACOG Practice Bulletin: clinical management guidelines for obstetrician-gynecologists. Number 300, December 2009. Cervical cytology screening. Obstet Gynecol 2009;114:1409-20.
80. Sasieni P, Castanon A, Cuzick J. Effectiveness of cervical screening with age: population based case-control study of prospectively recorded data. Br Med J 2009;339:b2968.
81. National Institute for Clinical Excellence (NICE). Guidance on the Use of Liquid-based Cytology for Cervical Screening. Technology appraisal no. 69, London, UK 2003.
82. International Collaboration of Epidemiological Studies of Cervical Cancer. Comparison of risk factors for invasive squamous cell carcinoma and adenocarcinoma of the cervix: collaborative reanalysis of individual data on 8,097 women with squamous cell carcinoma and 1,374 women with adenocarcinoma from 12 epidemiological studies. Int J Cancer 2007;120:885-991.
83. Onuki M, Matsumoto K, Satoh T, Oki A, Okada S, et al. Human papillomavirus infections among Japanese women: age-related prevalence and type-specific risk for cervical cancer. Cancer Sci 2009;100:1312-6.
84. Olsson SE, Villa LL, Costa RL, Petta CA, Andrade RP, Malm C, et al. Induction of immune memory following administration of a prophylactic quadrivalent human papillomavirus (HPV) types 6/11/16/18L1 virus-like particle (VLP) vaccine. Vaccine 2007;25:4931-9.
85. Schwarz TF, Leo O. Immune response to human papillomavirus after prophylactic vaccination with AS04-adjuvanted HPV-16/18 vaccine: improving upon nature. Gynecol Oncol 2008;110:S1-10.
86. Koulova A, Tsui J, Irwin K, Van Damme P, Biellik R, Aguado MT. Country recommendation on the inclusion of HPV vaccines in national immunization programmes among high-income countries. June 2006-January 2008. Vaccine 2008;26:6529-41.
87. Garland SM, Brotherton JML, Skinner SR, Pitts M, Saville M, Mola G, et al. Human papillomavirus and cervical cancer in Australia and Oceania: risk-factors, epidemiology and prevention. Vaccine 2008;26S:M80-8.
88. HPV Project Team Population Health Directorate Ministry of Health, NZ. The HPV (Human Papillomavirus) Immunization Programme. National Implementation Strategic Overview 2008.
89. Shefer A, Markowittz L, Deeks S, Tam T, Irwin K, Garland SM, et al. Early experience with human papillomavirus vaccine introduction in the United States, Canada and Australia. Vaccine 2008;26S: K68-75.
90. de Kok IM, Habbema JD, Mourits MJ, Coebergh JW, van Leeuwen FE. Insufficient basis for the inclusion of human papillomavirus vaccination in the National Immunization Programme in the Netherlands. Ned Tijdschr Geneeskd 2008;152:2001-4.
91. Howlett RI, Miller AB, Pasut G, Mai V. Defining a strategy to evaluate cervical cancer prevention and early detection in the era of HPV vaccination. Prev Med 2009;48:432-7.
92. European Centre for Disease Prevention and Control. Guidance for the Introduction of HPV Vaccines in EU Countries. Stockholm, Sweden, 2008.
93. Akamatsu S, Himeji Y, Ikuta N, Shimagaki N, Maruoka H, Kodama S. The propriety of the gynecological mass screening: comparison of the liquid-based method and the conventional method. J Jpn Soc Clin Cytol 2008;47:420-4 (in Japanese).
94. Anttila A, Hakama M, Kotaniemi-Talonen L, Nieminen P. Alternative technologies in cervical cancer screening: a randomized evaluation trial. BMC Public Health 2006;6:252.
95. Davies P, Arbyn M, Dillner J, Kitchener HC, Meijer CJ, Ronco G, et al. A report on the current status of European research on the use of human papillomavirus testing for primary cervical cancer screening. Int J Cancer 2006;118:791-6.