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Cancer Epidemiology, Biomarkers & Prevention
Cancer Epidemiology, Biomarkers & Prevention
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Research Articles

Oral Alpha, Beta, and Gamma HPV Types and Risk of Incident Esophageal Cancer

Ilir Agalliu, Zigui Chen, Tao Wang, Richard B. Hayes, Neal D. Freedman, Susan M. Gapstur and Robert D. Burk
Ilir Agalliu
1Department of Epidemiology and Population Health, Albert Einstein College of Medicine, Bronx, New York.
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  • For correspondence: ilir.agalliu@einstein.yu.edu robert.burk@einstein.yu.edu
Zigui Chen
2Department of Pediatrics (Genetics), Albert Einstein College of Medicine, Bronx, New York.
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Tao Wang
1Department of Epidemiology and Population Health, Albert Einstein College of Medicine, Bronx, New York.
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Richard B. Hayes
3Department of Population Health and Environmental Medicine, New York University, New York, New York.
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  • ORCID record for Richard B. Hayes
Neal D. Freedman
4Division of Cancer Epidemiology and Genetics, National Cancer Institute, National Institutes of Health, Bethesda, Maryland.
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Susan M. Gapstur
5American Cancer Society, Atlanta, Georgia.
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Robert D. Burk
1Department of Epidemiology and Population Health, Albert Einstein College of Medicine, Bronx, New York.
2Department of Pediatrics (Genetics), Albert Einstein College of Medicine, Bronx, New York.
6Departments of Microbiology and Immunology; and Obstetrics, Gynecology and Women's Health, Albert Einstein College of Medicine, Bronx, New York.
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  • For correspondence: ilir.agalliu@einstein.yu.edu robert.burk@einstein.yu.edu
DOI: 10.1158/1055-9965.EPI-18-0287 Published October 2018
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Article Figures & Data

Tables

  • Table 1.

    Selected characteristics of incident cases of esophageal cancer and their matched controls in each cohort study

    ACS CPS-II NC CohortPLCO Cohort
    CharacteristicsCasesControlsCasesControls
    Matching variablesN = 51N = 153PN = 74N = 219P
     Age at mouthwash collection; mean (SD)71.4 (6.1)71.4 (6.0)0.9765.2 (5.6)65.3 (5.5)0.82
     Months from mouthwash collection to diagnosis (cases) or riskset (controls); mean (SD)35.3 (24.5)35.3 (24.3)1.0052.6 (30.1)53.3 (29.9)0.85
     Gender; n %1.000.97
      Female8 (15.7)24 (15.7)15 (20.3)44 (20.1)
      Male43 (84.3)129 (84.3)59 (79.7)175 (79.9)
     Race/ethnicity; n %1.000.99
      Caucasian50 (98.0)150 (98.0)67 (90.5)198 (90.4)
      African American/other1 (2.0)3 (2.0)7 (9.5)21 (9.6)
    Unmatched variables
     BMI group (kg/m2); n (%)0.380.89
      <2522 (43.1)50 (32.7)18 (24.3)55 (25.1)
      25–29.918 (35.3)63 (41.2)37 (50.0)113 (51.6)
      ≥305 (9.8)26 (17.0)17 (23.0)48 (21.9)
      Missing6 (11.8)14 (9.1)2 (2.7)3 (1.4)
     Smoking status; n (%)0.010.01
      Never11 (21.6)60 (39.2)20 (27.0)99 (45.2)
      Former32 (62.7)86 (56.2)44 (59.5)108 (49.3)
      Current8 (15.7)7 (4.6)10 (13.5)12 (5.5)
     Pack-years, former and current smokers; mean (SD)31.5 (26.7)31.9 (31.9)0.9454.0 (30.4)36.2 (28.3)0.0002
     Alcohol consumption; n (%)
      None16 (31.4)55 (35.9)0.5523 (31.1)73 (33.3)0.72
      Drinker35 (68.6)98 (64.1)51 (68.9)146 (66.7)
       Drinks/week; median (IQR)5.7 (2.1–18.1)3.4 (1.0–9.1)0.105.8 (1.1–14.6)2.4 (1.1–7.0)0.13
     Education; n %0.940.41
      <12 grade3 (5.9)12 (7.8)2 (2.7)17 (7.8)
      High school/vocational15 (29.4)39 (25.5)30 (40.5)77 (35.2)
      Some college10 (19.6)33 (21.5)10 (13.5)38 (17.4)
      College graduate10 (19.6)29 (19.0)13 (17.6)39 (17.8)
      Graduate degree12 (23.5)39 (25.5)18 (24.3)48 (21.9)
      Missing1 (2.0)1 (0.7)1 (1.4)—
     Marital status; n %0.480.85
      Married40 (78.4)113 (73.9)60 (81.1)175 (79.9)
      Separated/divorced—2 (1.3)7 (9.5)20 (9.1)
      Widowed2 (3.9)12 (7.8)4 (5.4)18 (8.2)
      Never married——2 (2.7)6 (2.7)
      Missing9 (17.6)26 (17.0)1 (1.4)—
     Tumor histology; n (%)
      Adenocarcinoma31 (60.8)N/A49 (66.2)N/A
      Squamous cell carcinoma12 (23.5)N/A16 (21.6)N/A
      Other8 (15.7)N/A9 (12.2)N/A
    • Abbreviations: IQR: interquartile range; SD: standard deviation.

  • Table 2.

    Associations of HPV16, high-risk (HR) oncogenic HPV, and other α HPV types with risks of esophageal cancer and histologic type

    Cases (n = 125)Controls (n = 371)aAdjusted modelb
    All esophageal cancersα HPV typeN (%)N (%)ORa (95% CI)PPermutated Pd
    HPV161 (0.8)6 (1.6)0.54 (0.10–4.84)0.58>0.999
    HR-HPVsc excluding HPV168 (6.4)18 (4.9)1.21 (0.49–2.99)0.68>0.999
    NonHR HPV types16 (12.8)36 (9.7)1.47 (0.77–2.81)0.240.801
    Any α HPV23 (18.4)53 (14.3)1.39 (0.78–2.48)0.260.823
    ESCC
    α HPV typeCases (n = 28)Controls (n = 83)ORa (95% CI)PPermutated Pd
    HPV160 (0)1 (1.2)——>0.999
    HR-HPVsc excluding HPV163 (10.7)1 (1.2)10.52 (1.01–108.5)0.0480.236
    Non-HR HPV types4 (14.3)11 (13.3)1.68 (0.41–6.91)0.48>0.999
    Any α HPV6 (21.4)13 (15.7)2.21 (0.61–8.05)0.230.772
    Esophageal cancer: adenocarcinoma
    α HPV typeCases (n = 80)Controls (n = 238)ORa (95% CI)PPermutated Pd
    HPV161 (1.3)5 (2.1)0.60 (0.10–5.85)0.66>0.999
    HR-HPVsc excluding HPV163 (3.8)14 (5.9)0.52 (0.14–1.96)0.33>0.999
    NonHR HPV types8 (10.0)21 (8.8)1.21 (0.51–2.86)0.66>0.999
    Any α HPV12 (15.0)35 (14.6)0.98 (0.46–2.08)0.96>0.999
    • ↵aOne control had missing α HPV exposure and thus was excluded from these analyses.

    • ↵bOR and 95% CI were estimated from CLR models adjusted for smoking, alcohol consumption, and study cohort.

    • ↵cHigh-risk (HR) oncogenic HPVs include HPV16, 18, 31, 33, 35, 39, 45, 51, 52, 56, 58, and 59.

    • ↵dPermutated P values were calculated to account for multiple comparisons (see Material and Methods).

  • Table 3.

    Associations of β and γ HPV species and types with risk of esophageal cancer

    Cases (n = 125)Controls (n = 372)Adjusted modela
    β HPV SpeciesbN (%)N (%)ORa (95% CI)PPermutated Pc
    Any β HPV81 (64.8)205 (55.1)1.57 (1.00–2.47)0.0480.538
    Any β 1 HPV59 (47.2)146 (39.3)1.49 (0.96–2.31)0.080.716
    Any β 2 HPV64 (51.2)160 (43.0)1.34 (0.88–2.05)0.170.951
    Any β 3 HPV24 (19.2)60 (16.1)1.26 (0.73–2.18)0.41>0.999
    Specific β HPV typesb
     β 1 HPV522 (17.6)42 (11.3)1.75 (0.97–3.16)0.070.655
     β 1 HPV1211 (8.8)27 (7.3)1.24 (0.58–2.65)0.58>0.999
     β 1 HPV2022 (17.6)46 (12.4)1.53 (0.87–2.70)0.140.908
     β 1 HPV3615 (12.0)33 (8.9)1.20 (0.61–2.35)0.60>0.999
     Clade of β 1 HPVs 5, 36, 47, & 14326 (20.8)59 (15.9)1.34 (0.79–2.27)0.280.995
     β 1 HPV10514 (11.2)29 (7.8)1.31 (0.65–2.63)0.45>0.999
     β 1 HPV12410 (8.0)28 (7.5)1.01 (0.46–2.21)0.99>0.999
     β 2 HPV2312 (9.6)26 (7.0)1.34 (0.64–2.81)0.44>0.999
     β 2 HPV378 (6.4)28 (7.5)0.97 (0.42–2.27)0.95>0.999
     β 2 HPV3824 (19.2)57 (15.3)1.28 (0.75–2.18)0.37>0.999
     β 2 HPV10717 (13.6)29 (7.8)1.85 (0.94–3.62)0.080.703
    γHPV Speciesb
     Any γ HPV53 (42.4)125 (33.6)1.38 (0.89–2.13)0.150.924
     Any γ 7 HPV20 (16.0)49 (13.2)1.11 (0.62–2.01)0.72>0.999
     Any γ 8 HPV13 (10.4)38 (10.2)1.02 (0.52–2.01)0.95>0.999
     Any γ 10 HPV13 (10.4)28 (7.5)1.33 (0.66–2.71)0.42>0.999
     Any γ 12 HPV8 (6.4)19 (5.1)1.34 (0.56–3.20)0.51>0.999
     Any γ 15 HPV13 (10.4)28 (7.5)1.39 (0.66–2.89)0.39>0.999
    • ↵aOR and 95% CI were estimated from CLR models adjusted for smoking, alcohol consumption, and study cohort.

    • ↵bβ and γ HPV species and types presented have a prevalence of 5% or higher either in cases or controls.

    • ↵cPermutated P values were calculated to account for multiple comparisons (see methods).

  • Table 4.

    Associations of β and γ HPVs species and types with risk of histologic type of esophageal cancer

    A. ESCC
    Cases (n = 28)Controls (n = 83)Adjusted modela
    N (%)N (%)ORa (95% CI)PPermutated Pc
    β HPV speciesb
     Any β HPV14 (50.0)41 (49.4)1.05 (0.37–2.97)0.93>0.999
     Any β 1 HPV10 (35.7)27 (32.5)1.19 (0.42–3.35)0.75>0.999
     Any β 2 HPV11 (39.3)33 (39.8)0.99 (0.36–2.72)0.99>0.999
     Any β 3 HPV3 (10.7)19 (22.9)0.35 (0.1–1.48)0.150.792
    Specific β HPV typesb
     β 1 HPV55 (17.9)10 (12.1)1.56 (0.44–5.53)0.49>0.999
     β 1 HPV123 (10.7)9 (10.8)1.24 (0.26–5.79)0.79>0.999
     β 1 HPV203 (10.7)8 (9.6)1.10 (0.25–4.81)0.89>0.999
     β 1 HPV364 (14.3)6 (7.2)1.72 (0.36–8.14)0.50>0.999
     Clade of β 1 HPVs 5, 36, 47, & 1436 (21.4)12 (14.5)1.31 (0.39–4.39)0.66>0.999
     β 2 HPV232 (7.1)6 (7.2)1.31 (0.20–8.38)0.78>0.999
     β 2 HPV384 (14.3)16 (19.3)0.62 (0.18–2.11)0.45>0.999
    γ HPV speciesb
     Any γ HPV12 (42.9)26 (31.3)1.31 (0.51–3.31)0.57>0.999
     Any γ 7 HPV3 (10.7)6 (7.2)0.81 (0.15–4.48)0.81>0.999
     Any γ 8 HPV3 (10.7)9 (10.8)0.61 (0.12–3.11)0.55>0.999
     Any γ 10 HPV4 (14.3)8 (9.6)1.46 (0.37–5.82)0.59>0.999
     Any γ 15 HPV3 (10.7)8 (9.6)1.22 (0.29–5.14)0.79>0.999
    B. Esophageal adenocarcinoma
    Cases (n = 80)Controls (n = 239)Adjusted modela
    N (%)N (%)ORa (95% CI)PPermutated Pc
    β HPV Speciesb
     Any β HPV56 (70.0)134 (56.1)1.84 (1.05–3.23)0.040.199
     Any β 1 HPV41 (51.3)94 (39.3)1.74 (1.00–3.04)0.050.296
     Any β 2 HPV42 (52.5)105 (43.9)1.34 (0.80–2.25)0.27>0.999
     Any β 3 HPV18 (22.5)34 (14.2)1.86 (0.95–3.63)0.070.363
    Specific β HPV typesb
     β 1 HPV514 (17.5)27 (11.3)1.78 (0.85–3.72)0.130.605
     β 1 HPV126 (7.5)16 (6.7)1.11 (0.42–2.93)0.83>0.999
     β 1 HPV2014 (17.5)31 (13.0)1.42 (0.70–2.91)0.33>0.999
     β 1 HPV3610 (12.5)23 (9.6)1.13 (0.50–2.55)0.77>0.999
     Clade of β 1 HPVs 5, 36, 47, & 14317 (21.3)39 (16.3)1.36 (0.71–2.58)0.35>0.999
     β 1 HPV10511 (13.8)20 (8.4)1.62 (0.72–3.63)0.24>0.999
     β 1 HPV1247 (8.8)20 (8.4)1.06 (0.42–2.67)0.90>0.999
     β 2 HPV239 (11.3)17 (7.1)1.67 (0.70–3.97)0.24>0.999
     β 2 HPV378 (10.0)21 (8.8)1.21 (0.49–2.97)0.68>0.999
     β 2 HPV3815 (18.8)34 (14.2)1.48 (0.75–2.92)0.26>0.999
     β 2 HPV10710 (12.5)19 (8.0)1.69 (0.72–3.98)0.23>0.999
    γ HPV speciesb
     Any γ HPV32 (40.0)77 (32.2)1.53 (0.86–2.70)0.150.668
     Any γ 7 HPV13 (16.3)34 (14.2)1.12 (0.54–2.34)0.76>0.999
     Any γ 8 HPV4 (5.0)21 (8.8)0.43 (0.14–1.36)0.15>0.999
     Any γ 10 HPV7 (8.8)17 (7.1)1.38 (0.52–3.66)0.52>0.999
     Any γ 12 HPV7 (8.8)13 (5.4)1.92 (0.72–5.14)0.19>0.999
     Any γ 15 HPV8 (10.0)14 (5.9)1.93 (0.69–5.42)0.21>0.999
    • ↵aOR and 95% CI were estimated from CLR models adjusted for smoking, alcohol consumption, and study cohort.

    • ↵bβ and γ HPV species and types presented have a prevalence of 5% or higher either in cases or controls.

    • ↵cPermutated P values were calculated to account for multiple comparisons (see methods).

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Cancer Epidemiology Biomarkers & Prevention: 27 (10)
October 2018
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Oral Alpha, Beta, and Gamma HPV Types and Risk of Incident Esophageal Cancer
Ilir Agalliu, Zigui Chen, Tao Wang, Richard B. Hayes, Neal D. Freedman, Susan M. Gapstur and Robert D. Burk
Cancer Epidemiol Biomarkers Prev October 1 2018 (27) (10) 1168-1175; DOI: 10.1158/1055-9965.EPI-18-0287

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Oral Alpha, Beta, and Gamma HPV Types and Risk of Incident Esophageal Cancer
Ilir Agalliu, Zigui Chen, Tao Wang, Richard B. Hayes, Neal D. Freedman, Susan M. Gapstur and Robert D. Burk
Cancer Epidemiol Biomarkers Prev October 1 2018 (27) (10) 1168-1175; DOI: 10.1158/1055-9965.EPI-18-0287
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