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

C-reactive Protein and Future Risk of Clinical and Molecular Subtypes of Colorectal Cancer

Stina Bodén, Robin Myte, Justin Harbs, Anneli Sundkvist, Carl Zingmark, Anna Löfgren Burström, Richard Palmqvist, Sophia Harlid and Bethany Van Guelpen
Stina Bodén
1Department of Radiation Sciences, Oncology, Umeå University, Umeå, Sweden.
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  • ORCID record for Stina Bodén
  • For correspondence: stina.boden@umu.se
Robin Myte
1Department of Radiation Sciences, Oncology, Umeå University, Umeå, Sweden.
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Justin Harbs
1Department of Radiation Sciences, Oncology, Umeå University, Umeå, Sweden.
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Anneli Sundkvist
1Department of Radiation Sciences, Oncology, Umeå University, Umeå, Sweden.
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Carl Zingmark
2Department of Medical Biosciences, Pathology, Umeå University, Umeå, Sweden.
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Anna Löfgren Burström
2Department of Medical Biosciences, Pathology, Umeå University, Umeå, Sweden.
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Richard Palmqvist
2Department of Medical Biosciences, Pathology, Umeå University, Umeå, Sweden.
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Sophia Harlid
1Department of Radiation Sciences, Oncology, Umeå University, Umeå, Sweden.
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Bethany Van Guelpen
1Department of Radiation Sciences, Oncology, Umeå University, Umeå, Sweden.
3Wallenberg Centre for Molecular Medicine, Umeå University, Umeå, Sweden.
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DOI: 10.1158/1055-9965.EPI-19-1339 Published July 2020
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    Figure 1.

    Summary of the study design, including inclusions and exclusions of study participants.

  • Figure 2.
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    Figure 2.

    Estimated average intraindividual changes in ln plasma CRP concentrations over time in colorectal cancer cases and matched controls. Linear mixed models were used to estimate marginal effects of time and 95% CIs in 259 cases and 259 matched controls with matched repeated measurements prior to case diagnosis. A, The crude model included participants and matched case–control pairs as random factors, and time between sample collection and case diagnosis, case–control status, and an interaction term between time and case–control status as fixed factors. B, The adjusted model was additionally adjusted for smoking status, recreational physical activity, alcohol intake, diabetes, and BMI, which were included as fixed factors.

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  • Table 1.

    Baseline characteristics of participants, N (%)a or median (IQR).

    AllCRP <1 mg/LCRP 1–3 mg/LCRP >3 mg/LPbMissingc
    All participants2,020793 (39.3)716 (35.4)511 (25.3)—0
    CRC status0.164
     Cases1,010 (50)385 (48.5)351 (49.0)274 (53.6)0
     Controls1,010 (50)408 (51.5)365 (51.0)237 (46.4)0
    Sex0.249
     Male1,050 (52.0)427 (53.8)372 (52.0)251 (49.1)0
     Female970 (48.0)366 (46.2)344 (48.0)260 (50.9)
    Age at baseline56.3 (49.9–60.0)50.3 (49.8–60.0)59.3 (50.0–60.0)59.8 (50.0–60.1)<0.0010
    Age at diagnosis of cases66.4 (60.5–72.6)65.3 (57.4–71.2)67.6 (61.7–73.6)66.8 (61.9–73.0)<0.0010
    Follow-up time of casesd12.3 (7.5–16.6)12.3 (7.7–16.5)12.7 (7.9–17.9)11.7 (6.4–15.6)0.0350
    BMI, kg/m225.7 (23.5–28.4)24.4 (22.6–26.4)26.2 (24.0–28.5)27.6 (24.9–30.5)<0.00120 (1.0)
    Recreational physical activity0.109161 (8.0)
     No physical activity793 (42.7)298 (41.2)277 (41.8)218 (46.1)
     Low472 (25.4)181 (25.0)183 (27.6)108 (22.8)
     Moderate504 (27.1)217 (30.0)167 (25.2)120 (25.4)
     High90 (4.8)28 (3.9)35 (5.3)27 (5.7)
    Alcohol intake groups, gram/day0.589298 (14.8)
     Zero142 (8.2)49 (7.5)48 (7.7)45 (10.1)
     Below mediane725 (42.1)279 (42.7)263 (42.1)183 (41.1)
     Above mediane855 (49.7)325 (49.8)313 (50.2)217 (48.8)
    Smoking status0.00143 (2.1)
     Nonsmoker832 (42.1)358 (46.0)300 (43.2)174 (34.5)
     Ex-smoker680 (34.4)255 (32.7)237 (34.1)188 (37.3)
     Current smoker465 (23.5)166 (21.3)157 (22.6)142 (28.2)
    Diabetesf122 (6.0)27 (3.4)47 (6.6)48 (9.4)<0.0010
    Education level<0.00143 (2.1)
     No secondary1,327 (67.1)478 (61.2)498 (71.3)351 (70.5)
     Secondary314 (15.9)144 (18.4)99 (14.2)71 (14.3)
     Post-secondary336 (17.0)159 (20.4)101 (14.5)76 (15.3)
    • Abbreviation: CRC, colorectal cancer.

    • ↵aPercent of participants calculated within CRP categories, except for “all participants.”

    • ↵bχ2 tests for differences between CRP groups (% of participants with existing data) for categorical variables, Kruskal–Wallis tests for differences between CRP groups for continuous variables.

    • ↵cN and % of participants in total (N = 2,020). Missing category not included in the statistical comparisons.

    • ↵dFollow-up time from baseline sample collection to CRC diagnosis.

    • ↵eSex-specific median.

    • ↵fObtained from self-reported question (yes/no) or from fasting plasma glucose levels or from 2-hour oral glucose tolerance test levels, according to WHO diagnostic criteria for diabetes mellitus.

  • Table 2.

    Baseline and follow-up characteristics of participants with repeated measures.

    BaselineRepeatMissing
    (n = 518)(n = 518)PaBaselineRepeat
    CRC status—
     Cases259 (50)259 (50)
     Controls259 (50)259 (50)
    Sex—
     Male292 (56.4)292 (56.4)
     Female226 (43.6)226 (43.6)
    Follow-up timeb, years15.6 (12.9–19.0)5.83 (2.9–9.1)00
    Age at sampling, years50.0 (40.5–50.2)59.9 (51.0–60.1)<0.00100
    CRP mg/L
     Cases1.26 (0.52–2.69)1.90 (0.95–4.06)<0.00100
     Controls1.14 (0.51–2.21)1.48 (0.78–3.21)<0.00100
    BMI, kg/m2
     Cases25.3 (23.4–27.6)26.4 (24.3–29.1)<0.0015 (1.9)0
     Controls24.6 (22.8–27.0)26.0 (23.4–28.4)<0.0012 (0.8)0
    Recreational physical activity
     Cases0.24442 (16.2)27 (10.4)
      No physical activity104 (40.2)108 (41.7)
      Low47 (18.1)52 (20.1)
      Moderate61 (23.6)58 (22.4)
      High5 (1.9)14 (5.4)
     Controls0.79147 (18.1)31 (12.0)
      No physical activity98 (37.8)106 (40.9)
      Low56 (21.6)52 (20.1)
      Moderate49 (18.9)60 (23.2)
      High9 (3.5)10 (3.9)
    Alcohol intake groups, grams/day
     Cases0.33144 (17.0)2 (0.3)
      Zero6 (2.8)10 (3.9)
      Below medianc95 (44.2)97 (37.7)
      Above medianc114 (53.0)150 (58.4)
     Controls0.74041 (15.8)0
      Zero13 (6.0)17 (6.6)
      Below medianc87 (39.9)111 (42.9)
      Above medianc118 (54.1)131 (50.6)
    Smoking status
     Cases0.0016 (2.3)5 (1.9)
      Nonsmoker97 (37.5)112 (43.2)
      Ex-smoker82 (31.7)103 (39.8)
      Current smoker74 (28.6)39 (15.1)
     Controls0.0036 (2.3)8 (3.1)
      Nonsmoker110 (42.5)114 (44.0)
      Ex-smoker80 (30.9)103 (39.8)
      Current smoker63 (24.3)34 (13.1)
    Diabetesd
     Cases7 (2.7)16 (6.2)0.05500
     Controls2 (0.8)8 (3.1)0.05500
    • Note: N (%) or median (IQR).

    • Abbreviation: CRC, colorectal cancer.

    • ↵aPaired Wilcoxon signed rank test within the matched case sets for continuous variables, χ2 tests for categorical variables. Cells showing missing data were not included in the statistical comparisons.

    • ↵bFollow-up time from sample collection to CRC diagnosis.

    • ↵cSex-specific median.

    • ↵dObtained from self-reported question (yes/no) and/or from fasting plasma glucose levels and/or from 2-hour oral glucose tolerance test levels, according to WHO diagnostic criteria for diabetes mellitus.

  • Table 3.

    ORsa and 95% CI of colorectal cancer and colorectal cancer subtypes per 1 unit increase in ln plasma CRP concentrationsb.

    CRC subgroupn complete cases/controlscOR (95% CI)Pheterogeneityd
    All CRC835/8171.03 (0.97–1.09)
    Sex
     Male437/4281.03 (0.95–1.12)0.824
     Female398/3891.02 (0.94–1.11)
    BRAF/KRAS mutation status
     BRAF mutated123/1161.11 (0.96–1.27)0.354
     KRAS mutated137/1381.05 (0.91–1.20)
     BRAF/KRAS wild-type320/3140.99 (0.91–1.08)
    MSI status
     MSI78/701.05 (0.87–1.27)0.833
     MSS504/4981.03 (0.96–1.09)
    Tumor location
     Right colon258/2451.02 (0.91–1.13)0.426
     Left colon247/2481.09 (0.98–1.22)
     Rectum324/3180.99 (0.90–1.09)
    Disease stage
     Stage I–II395/3851.01 (0.93–1.10)0.641
     Stage III–IV390/3831.04 (0.96–1.14)
    Lag time
     <5 years134/1341.13 (0.96–1.32)0.583
     5–10 years202/1980.98 (0.85–1.12)
     10–15 years251/2451.01 (0.90–1.13)
     >15 years248/2401.03 (0.93–1.14)
    Disease stage/lag time
     Stage III–IV/lag time <5 years64/611.32 (1.01–1.73)0.288
     Stage III–IV/lag time 5–10 years90/880.96 (0.77–1.19)
     Stage III–IV/lag time 10–15 years124/1221.01 (0.87–1.18)
     Stage III–IV/lag time >15 years112/1121.02 (0.88–1.18)
    BMIe, kg/m2
     <25317/3540.99 (0.97–1.02)0.129
     25–30384/3431.03 (1.00–1.06)
     >30134/1201.02 (0.98–1.06)
    • Abbreviation: CRC, colorectal cancer.

    • ↵aMultivariable ORs adjusted for age, sex, cohort, sample year and fasting status, smoking status, recreational physical activity, alcohol intake, diabetes mellitus, and BMI (model 3). For estimates from model 1 and 2, see Supplementary Table S1.

    • ↵bFrom multiple imputation data.

    • ↵cNumbers (n) per subgroup represent complete cases and controls with complete covariate data, molecular data for the remaining cases were imputed. Complete estimates for all adjusted models for imputed and complete case data are presented in Supplementary Table S1 for comparison.

    • ↵dPheterogeneity between subtypes was tested with Wald test comparing the observed overall log OR and subtype-specific log ORs from the final multivariable model (model 3).

    • ↵eORs from unconditional logistic regression model (model 2) adjusted for all covariates listed above, except BMI.

Additional Files

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  • Supplementary Data

    • Supplementary Table 1, Supplementary Table 2, Supplementary Figure 1 - Supplementary Table 1 shows the ORs and 95% CI for increase in CRP concentrations in complete CRC and CRC subtype cases and in multiple imputation analysis. Supplementary Table 2 shows the clinical characteristics in CRC cases by BRAF/KRAS mutation status. Supplementary Figure 1 shows mean CRP concentration (mg/L) for BMI categories (&lt;25, 25-30, and &gt;30).
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Cancer Epidemiology Biomarkers & Prevention: 29 (7)
July 2020
Volume 29, Issue 7
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C-reactive Protein and Future Risk of Clinical and Molecular Subtypes of Colorectal Cancer
Stina Bodén, Robin Myte, Justin Harbs, Anneli Sundkvist, Carl Zingmark, Anna Löfgren Burström, Richard Palmqvist, Sophia Harlid and Bethany Van Guelpen
Cancer Epidemiol Biomarkers Prev July 1 2020 (29) (7) 1482-1491; DOI: 10.1158/1055-9965.EPI-19-1339

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C-reactive Protein and Future Risk of Clinical and Molecular Subtypes of Colorectal Cancer
Stina Bodén, Robin Myte, Justin Harbs, Anneli Sundkvist, Carl Zingmark, Anna Löfgren Burström, Richard Palmqvist, Sophia Harlid and Bethany Van Guelpen
Cancer Epidemiol Biomarkers Prev July 1 2020 (29) (7) 1482-1491; DOI: 10.1158/1055-9965.EPI-19-1339
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