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Cancer Epidemiology, Biomarkers & Prevention

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Research Articles

Human Papillomavirus Genotype Distribution in Low-Grade Cervical Lesions: Comparison by Geographic Region and with Cervical Cancer

Gary M. Clifford, Rashida K. Rana, Silvia Franceschi, Jennifer S. Smith, Gerald Gough and Jeanne M. Pimenta
Gary M. Clifford
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Rashida K. Rana
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Silvia Franceschi
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Jennifer S. Smith
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Gerald Gough
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Jeanne M. Pimenta
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DOI: 10.1158/1055-9965.EPI-04-0812 Published May 2005
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    Figure 1.

    Prevalence of the 15 most common HPV genotypes in 5,910 HPV-positive LSILs by region. *, Denominators of HPV-positive LSIL vary by HPV type, from 2,516 to 5,910 for all regions, from 268 to 2,746 for Europe, from 1,640 to 1,943 for North America, from 466 to 874 for South/Central America, from 62 to 178 for Africa, and from 160 to 169 for Asia. †, In Asia, upper 95% CI for HPV16 is 39.6%, and HPV53 is not shown because the denominator was 33 cases only.

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    Figure 2.

    ORs and corresponding 95% FCIs for infection with HPV16 and HPV18 in HPV-positive LSILs by region.

Tables

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  • Table 1.

    Regional distribution and overall HPV prevalence among 8,308 LSILs

    RegionStudies, nCountries representedLSIL cases, nHPV positive, n (%)
    Europe21Belgium, Croatia, Czech Republic, France, Germany, Greece, Holland, Italy, Portugal, Sweden, United Kingdom4,0512,746 (67.8)
    North America13Canada, United States2,4251,943 (80.1)
    South/Central America13Argentina, Brazil, Colombia, Costa Rica, Honduras, Jamaica, Mexico, Paraguay1,279874 (68.3)
    Africa4Ivory Coast, Kenya, Nigeria, Senegal301178 (59.1)
    Asia4China, Korea, Thailand252169 (67.1)
    Total558,3085,910 (71.1)
  • Table 2.

    Prevalence of 15 most common HPV genotypes in HPV-positive LSILs and comparison with that in SCC

    HPV genotypeHPV-positive LSIL*
    SCC†,‡
    SCC/LSIL
    Tested, nHPV positive, %Tested, nHPV positive, %Prevalence ratio (95% CI)
    HPV165,91026.68,59454.32.06 (2.02-2.11)
    HPV185,9108.68,50212.61.47 (1.39-1.54)
    HPV453,5454.95,1744.20.85 (0.77-0.94)
    HPV335,7447.68,4494.30.58 (0.54-0.62)
    HPV315,80111.77,2044.20.36 (0.34-0.39)
    HPV583,3808.55,6463.00.36 (0.32-0.39)
    HPV523,2628.85,3042.50.28 (0.25-0.31)
    HPV354,7545.96,2231.00.17 (0.15-0.20)
    HPV593,2326.04,4880.80.13 (0.11-0.16)
    HPV63,6388.16,5690.60.08 (0.06-0.09)
    HPV563,3489.74,4930.70.07 (0.06-0.09)
    HPV513,56610.94,5800.60.06 (0.05-0.07)
    HPV393,2517.83,8990.40.05 (0.04-0.07)
    HPV663,1328.54,7990.20.02 (0.02-0.04)
    HPV532,51610.13,0530.10.01 (0.01-0.02)
    • ↵* Regional distribution of included cases: Europe 46.5%, North America 32.9%, South/Central America 14.8%, Africa 3.0%, and Asia 2.9%.

    • ↵† Data from Clifford et al. (32).

    • ↵‡ Regional distribution of included cases: Europe 32.0%, North America 13.0%, South/Central America 16.5%, Africa 6.9%, and Asia 31.7%.

  • First authorReferenceCountryHPV DNA sourcePCR primersCases nLSIL/CIN1HPV prevalence (% of all LSILs tested)
    Any16315153565266586183933593545
    Africa
        de Vuyst HSex Transm Dis (2002)KenyaCellsSPF10300/3060.013.33.33.310.03.313.33.36.70.06.70.00.00.023.33.3
        La Ruche GInt J Cancer (1998)Ivory CoastCellsMY09/11151151/068.210.65.30.0—2.62.6—3.33.36.02.05.31.31.32.0
        Thomas JOBr J Cancer (2003)NigeriaCellsGP5+/6+3434/038.25.92.92.9—2.92.90.05.92.92.90.00.00.00.00.0
        Xi LFInt J Cancer (2003)SenegalCellsMY09/118686/051.28.11.21.23.51.23.51.29.32.34.70.02.32.32.30.0
        Africa subtotal301271/3059.19.63.61.05.22.34.01.35.62.75.31.03.31.33.71.3
    Asia
        Bhattarakosol PJ Med Assoc Thai (2002)ThailandBiopsiesMY09/11270/2733.30.0——————0.03.7—0.0———
        Chan PKSJ Med Virol (1999)ChinaCellsMY09/11510/5164.721.67.80.00.02.05.90.015.72.09.80.02.00.00.00.0
        Chan PKSJ Med Virol (1999)ChinaCellsMY09/11510/5164.721.67.80.00.02.05.90.015.72.09.80.02.00.00.00.0
        Cho NHAm J Obstet Gynecol (2003)KoreaCellsGP5+/6+150150/073.326.71.35.3—6.02.70.710.00.77.34.00.70.02.01.3
        Hwang TSGynecol Oncol (2003)KoreaCellsGP5+/6+240/2470.816.70.04.2—4.24.24.20.00.016.78.40.00.04.20.0
        Asia subtotal252150/10267.121.82.74.00.04.93.62.210.20.87.13.60.80.01.80.9
    Europe
        Astori GVirus Res (1997)ItalyCellsMY09/11111111/077.524.35.40.07.20.90.00.07.210.85.40.90.00.91.80.0
        Baay MFDEur J Gynaecol Oncol (2001)BelgiumBiopsiesGP5+/6+580/5869.024.11.73.4—5.21.71.70.00.019.00.00.00.00.05.2
        Cuschieri KSJ Clin Pathol (2004)United KingdomCellsGP5+/6+243243/090.928.012.817.3—9.912.311.95.00.09.59.17.48.62.15.3
        Cuzick JBr J Cancer (1999)United KingdomCellsMY09/11500/5042.012.00.02.0—4.012.0—2.0—10.0—2.0—0.0—
        Giannoudis AInt J Cancer (1999)United KingdomBiopsiesGP5+/6+118118/0100.012.75.17.6—5.9—11.97.615.37.60.80.82.514.42.5
        Grce MEur J Epidemiol (1997)CroatiaCellsMY09/11183183/035.56.08.7———————2.2—1.6———
        Grce MAnticancer Res (2001)CroatiaCellsMY09/111,0281,028/054.511.65.8———————2.9—3.1———
        Humbey OEur J Obstet Gynecol Reprod Biol (2002)FranceCellsMY09/114040/060.030.0—5.0——5.0—7.52.510.0—7.5—2.52.5
        Kalantari MHum Pathol (1997)SwedenCellsMY09/111410/14170.917.75.7———————12.1—5.0———
        Labropoulou VSex Transm Dis (1997)GreeceBiopsies/cellsMY09/11510/5190.211.89.80.02.0——2.0—11.811.8—9.8———
        Laconi SPathologica (2000)ItalyBiopsiesGP5+/6+200/2095.030.00.020.0—0.00.0—0.010.00.00.00.0—0.0—
        Medeiros RInt Meet Gynecol Oncol (1997)PortugalBiopsiesMY09/11310/3174.235.5————————3.2—0.0———
        Meyer TInt J Gynecol Cancer (2001)GermanyBiopsies/cellsMY09/11130130/069.213.113.13.12.30.83.13.85.43.12.31.55.40.03.10.8
        Nindl IJ Clin Pathol (1999)GermanyCellsGP5+/6+490/4953.112.22.04.1—4.10.02.08.2—0.02.06.10.00.04.1
        Reesink-Peters NEur J Obstet Gynecol Reprod Biol (2001)NetherlandsCellsSPF10350/3597.128.631.4——11.4————31.4—17.1———
        Southern SHum Pathol (2001)United KingdomBiopsiesGP5+/6+490/49100.010.22.04.1—2.06.16.110.224.58.24.12.00.00.00.0
        Tachezy RJ Med Virol (1999)Czech RepublicCellsMY09/118787/052.934.52.31.12.30.01.10.05.7—4.60.02.30.02.31.1
        Venturoli SJ Clin Virol (2002)ItalyCellsMY09/114040/047.57.510.0——————5.02.5—2.5——0.0
        Voglino GPathologica (2000)ItalyBiopsiesMY09/111,4990/1,49973.024.715.9———————4.2—8.9—4.3—
        Zehbe IVirchows Arch (1996)SwedenBiopsiesGP5+/6+450/4593.340.011.1——6.72.2—6.76.76.7—2.2—2.20.0
        Zerbini MJ Clin Pathol (2001)ItalyCellsMY09/114343/053.514.04.7——————9.30.0—9.3——2.3
        Europe subtotal4,0512,023/2,02867.819.410.46.93.74.85.46.05.76.85.13.45.73.03.82.5
    North America
        Adam EAm J Obstet Gynecol (2000)United StatesCellsMY09/111610/16172.745.33.1———————23.6—6.2—17.4—
        ASCUS-LSIL Triage Study GroupAm J Obstet Gynecol (2003)United StatesCellsPGMY09/111,2421,242/092.421.59.016.111.112.811.710.97.66.810.511.04.410.07.06.0
        Brown DRSex Transm Dis (2002)United StatesCellsMY09/112525/088.040.012.04.04.020.012.024.04.04.00.08.04.08.012.00.0
        Evans MFMod Pathol (2002)United StatesBiopsiesGP5+/6+260/28100.07.17.110.70.03.67.110.70.07.13.610.73.610.73.63.6
        Jarboe EAHum Pathol (2004)United StatesCellsPGMY09/11950/9555.87.43.24.28.43.29.55.32.12.13.21.10.010.52.15.3
        Kulasingam SJAMA (2002)United StatesCellsMY09/11166166/079.015.73.615.011.47.28.49.05.410.23.67.83.03.64.22.4
        Liaw KJ Natl Cancer Inst (1999)United StatesCellsMY09/11173173/042.27.54.06.44.64.61.71.23.5—1.72.91.70.01.71.2
        Richardson HCancer Epidemiol Biomarkers Prev (2003)CanadaCellsMY09/114444/088.618.22.318.218.220.54.59.16.80.09.16.80.02.32.30.0
        Schiff MAm J Epidemiol (2000)United StatesCellsMY09/111900/19058.45.88.94.210.57.44.76.810.54.24.77.44.26.31.14.7
        Sellors JWCMAJ (2000)CanadaCellsMY09/112222/090.950.04.50.00.04.50.0—0.04.54.54.50.00.00.00.0
        Sellors JWCMAJ (2000)CanadaCellsMY09/112424/095.837.512.50.00.00.00.0—4.24.225.00.04.20.00.00.0
        Tortolero-LunaCad Saude Publica (1998)United StatesCellsMY09/11175175/064.612.66.9———————8.0———4.09.1
        Tran-Thanh DAm J Obstet Gynecol (2003)CanadaBiopsiesMY09/11800/8083.815.08.83.88.815.08.08.86.36.38.87.55.03.80.01.3
        North America subtotal2,4251,872/55480.219.47.412.610.110.79.39.36.86.39.28.83.97.65.85.0
    South/Central America
        Abba MCRev Argent Microbiol (2003)ArgentinaCellsMY09/11279279/080.326.52.50.7—————22.92.5—5.4———
        Ferrera AInt J Cancer (1999)HondurasCellsMY09/11440/4447.711.411.40.04.50.00.00.02.30.06.80.00.00.00.02.3
        Franco EPan Am J Public Health (1999)BrazilCellsMY09/112727/081.526.011.014.814.83.711.10.011.10.00.03.73.73.73.70.0
        Giuliano ACancer Epidemiol Biomarkers Prev (2001)Mexico (some United States)CellsPGMY09/114040/062.515.00.07.52.55.07.55.05.02.52.510.00.07.52.52.5
        Gonzalez-Losa MdRJ Clin Virol (2004)MexicoBiopsiesMY09/11104104/028.85.82.91.92.91.01.91.96.73.83.81.01.01.90.01.0
        Herrero RJ Natl Cancer Inst (2000)Costa RicaCellsMY09/11181181/073.012.27.29.96.18.87.24.48.86.14.46.61.11.72.23.9
        Illades-Aguiar BInt Papillomarivus Conf Proc (2001)MexicoBiopsiesMY09/111480/14886.512.82.00.00.70.00.70.03.42.00.70.036.50.00.74.1
        Lorenzato FInt J Gynecol Cancer (2000)BrazilCellsMY09/11620/6267.719.422.6———0.0—6.50.03.2—11.3—4.80.0
        Molano JBr J Cancer (2002)ColombiaCellsGP5+/6+7070/055.710.04.34.3—4.37.11.45.72.97.14.38.60.02.94.3
        Rattray CJ Infect Dis (1996)JamaicaCellsMY09/116262/080.69.78.1——————4.84.8—12.9—8.116.1
        Strickler HJ Med Virol (1999)JamaicaCellsMY09/11186186/054.34.31.61.62.71.62.72.22.22.22.71.61.60.52.20.5
        Tonon SAInfect Dis Obstet Gynecol (1999)Argentina/ParaguayCellsGP5+/6+5555/096.474.5———————5.512.7—————
        Torroella-Kouri MGynecol Oncol (1998)MexicoBiopsies/cellsMY09/112121/033.34.80.04.80.04.80.00.00.00.00.00.00.00.00.04.8
        South/Central America subtotal1,2791,025/25468.316.74.83.33.63.33.62.15.27.43.62.97.91.22.23.3
    Total 8,308 5,341/2,967 71.218.78.28.07.67.26.76.56.36.26.15.85.34.64.33.7
    • * HPV prevalence represents that at study enrollment and not at LSIL diagnosis.

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Cancer Epidemiology Biomarkers & Prevention: 14 (5)
May 2005
Volume 14, Issue 5
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Human Papillomavirus Genotype Distribution in Low-Grade Cervical Lesions: Comparison by Geographic Region and with Cervical Cancer
Gary M. Clifford, Rashida K. Rana, Silvia Franceschi, Jennifer S. Smith, Gerald Gough and Jeanne M. Pimenta
Cancer Epidemiol Biomarkers Prev May 1 2005 (14) (5) 1157-1164; DOI: 10.1158/1055-9965.EPI-04-0812

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Human Papillomavirus Genotype Distribution in Low-Grade Cervical Lesions: Comparison by Geographic Region and with Cervical Cancer
Gary M. Clifford, Rashida K. Rana, Silvia Franceschi, Jennifer S. Smith, Gerald Gough and Jeanne M. Pimenta
Cancer Epidemiol Biomarkers Prev May 1 2005 (14) (5) 1157-1164; DOI: 10.1158/1055-9965.EPI-04-0812
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