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Research ArticleOriginal Research

Fecal Immunochemical Test (FIT) for Colon Cancer Screening: Variable Performance with Ambient Temperature

Chyke A. Doubeni, Christopher D. Jensen, Stacey A. Fedewa, Virginia P. Quinn, Ann G. Zauber, Joanne E. Schottinger, Douglas A. Corley and Theodore R. Levin
The Journal of the American Board of Family Medicine November 2016, 29 (6) 672-681; DOI: https://doi.org/10.3122/jabfm.2016.06.160060
Chyke A. Doubeni
From the University of Pennsylvania (CAD); Division of Research, Kaiser Permanente, Oakland, CA (CDJ, DAC, TRL); American Cancer Society, Atlanta, GA (SAF); Research and Evaluation, Kaiser Permanente, Pasadena, CA (VPQ, JES); Memorial Sloan Kettering Cancer Center, New York, NY (AGZ).
MD, MPH
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Christopher D. Jensen
From the University of Pennsylvania (CAD); Division of Research, Kaiser Permanente, Oakland, CA (CDJ, DAC, TRL); American Cancer Society, Atlanta, GA (SAF); Research and Evaluation, Kaiser Permanente, Pasadena, CA (VPQ, JES); Memorial Sloan Kettering Cancer Center, New York, NY (AGZ).
PhD
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Stacey A. Fedewa
From the University of Pennsylvania (CAD); Division of Research, Kaiser Permanente, Oakland, CA (CDJ, DAC, TRL); American Cancer Society, Atlanta, GA (SAF); Research and Evaluation, Kaiser Permanente, Pasadena, CA (VPQ, JES); Memorial Sloan Kettering Cancer Center, New York, NY (AGZ).
MPH, PhD
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Virginia P. Quinn
From the University of Pennsylvania (CAD); Division of Research, Kaiser Permanente, Oakland, CA (CDJ, DAC, TRL); American Cancer Society, Atlanta, GA (SAF); Research and Evaluation, Kaiser Permanente, Pasadena, CA (VPQ, JES); Memorial Sloan Kettering Cancer Center, New York, NY (AGZ).
PhD
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Ann G. Zauber
From the University of Pennsylvania (CAD); Division of Research, Kaiser Permanente, Oakland, CA (CDJ, DAC, TRL); American Cancer Society, Atlanta, GA (SAF); Research and Evaluation, Kaiser Permanente, Pasadena, CA (VPQ, JES); Memorial Sloan Kettering Cancer Center, New York, NY (AGZ).
PhD
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Joanne E. Schottinger
From the University of Pennsylvania (CAD); Division of Research, Kaiser Permanente, Oakland, CA (CDJ, DAC, TRL); American Cancer Society, Atlanta, GA (SAF); Research and Evaluation, Kaiser Permanente, Pasadena, CA (VPQ, JES); Memorial Sloan Kettering Cancer Center, New York, NY (AGZ).
MD
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Douglas A. Corley
From the University of Pennsylvania (CAD); Division of Research, Kaiser Permanente, Oakland, CA (CDJ, DAC, TRL); American Cancer Society, Atlanta, GA (SAF); Research and Evaluation, Kaiser Permanente, Pasadena, CA (VPQ, JES); Memorial Sloan Kettering Cancer Center, New York, NY (AGZ).
MD, PhD
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Theodore R. Levin
From the University of Pennsylvania (CAD); Division of Research, Kaiser Permanente, Oakland, CA (CDJ, DAC, TRL); American Cancer Society, Atlanta, GA (SAF); Research and Evaluation, Kaiser Permanente, Pasadena, CA (VPQ, JES); Memorial Sloan Kettering Cancer Center, New York, NY (AGZ).
MD
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Article Figures & Data

Figures

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  • Figure 1.
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    Figure 1.

    Distribution of temperatures across the regions over the study period, Kaiser Permanente–Northern California (KPNC) 2007 to 2013. Note: The horizontal reference line is for the model probability of a positive test (0.045). The temperature distribution in Celsius used the average of the daily minimum and maximums of the entire regions and study period; the average for the 4 temperature categories is: 1, 9.6°C; 2, 11.7°C; 3, 14.3°C; 4, 17.5°C; and 5, 18.7°C.

  • Figure 2.
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    Figure 2.

    Seasonal variation in the positivity rate of fecal immunochemical test, Kaiser Permanente–Northern California (KPNC) 2007 to 2013. Note: The figure was generated using time series analysis methods for the minimum and maximum air temperatures (min–max temperatures, °C) and the positivity rates aggregated according to week over the study years. The positivity rate ranged from 2.6% to 8.0%). The false-positive rates paralleled the positivity rate such that the higher the positivity rate, the higher the false-positivity rate.

  • Figure 3.
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    Figure 3.

    Association of positivity rate by season, month, and temperature levels, Kaiser Permanente–Northern California (KPNC) 2007 to 2013. *, Each set of estimates (by levels, by month, and by season of the year) was generated, separately, using predictive margins from the logistic regression adjusted for age, race/ethnicity, and sex using the generalized estimating equations approach with exchangeable covariance matrix.

Tables

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    Table 1.

    Characteristics of the Cohort, Kaiser Permanente–Northern California (KPNC) 2006 to 2013

    Characteristics, %N (472,541)%
    Age, years
        50 to 54204,01943.2
        55 to 59111,75623.7
        60 to 6472,07615.3
        65 to 6952,14911.0
        70 to 7432,5416.9
    Females254,63253.9
    Race-ethnicity
        Non-Hispanic White269,63957.1
        Non-Hispanic Black34,3697.3
        Hispanics/Latinos57,72912.2
        Asian/Pacific Islanders68,68314.5
        Native Americans2,1970.5
        Multiple race18,9594.0
        Unknown20,9654.4
    Geographical region
        Alameda80,22517.0
        San Francisco/Peninsula/South Bay158,87733.6
        North Bay46,5509.9
        Walnut Creek/Diablo47,0019.9
        Central Valley26,8405.7
        Sacramento105,78322.4
        Fresno7,2651.5
    Percentage of households below federal poverty level, quintiles
        1100,49821.3
        298,42820.9
        396,15020.4
        492,07219.5
        584,79818.0
    Charlson Comorbidity Index
        0370,54478.4
        185,73018.1
        212,7642.7
        3+3,5030.7
    Enrollment in health plan, years
        2.0 to 4.9972,67515.4
        5.0 to 9.99114,06524.1
        10.0+285,80160.5
    • View popup
    Table 2.

    Temperature Ranges and Positivity Rates and Adjusted Rate Ratios for Associations of Daily Ambient Temperatures with Fecal Immunochemical Test Positivity Rate, Kaiser Permanente–Northern California (KPNC) 2007 to 2013

    Temperature CategoriesAverage of the Minimum–Maximum, °C, mean (range)Positive %Positivity Rate Ratio (95% Confidence Interval)
    Temperature levels
        1 (lowest)9.6 (8.0 to 11.1)5.51.00
        211.7 (10.3 to 12.9)4.40.82 (0.78 to 0.86)
        314.3 (12.7 to 15.8)4.40.82 (0.77 to 0.86)
        417.5 (15.5 to 19.4)4.20.78 (0.75 to 0.82)
        5 (highest)18.7 (16.7 to 20.7)4.30.81 (0.76 to 0.86)
    Seasons
        Winter10.9 (9.5 to 12.4)4.51.00
        Spring14.8 (12.6 to 16.5)4.10.92 (0.90 to 0.96)
        Summer18.3 (16.1 to 20.1)4.20.93 (0.90 to 0.96)
        Autumn15.4 (13.1 to 17.9)5.11.13 (1.09 to 1.17)
    Test result month (individually)
        January10.0 (8.5 to 11.7)4.80.83 (0.77 to 0.90)
        February11.0 (9.8 to 12.4)4.30.74 (0.69 to 0.79)
        March11.8 (10.4 to 13.0)4.30.75 (0.70 to 0.80)
        April13.5 (11.8 to 14.9)4.20.73 (0.68 to 0.77)
        May15.2 (13.5 to 16.5)4.10.72 (0.67 to 0.77)
        June17.3 (15.3 to 19.0)4.10.72 (0.67 to 0.77)
        July18.1 (16.1 to 19.8)3.90.69 (0.64 to 0.74)
        August18.5 (16.2 to 20.5)4.20.74 (0.69 to 0.79)
        September18.9 (16.7 to 20.9)4.40.77 (0.71 to 0.82)
        October17.2 (15.4 to 18.6)4.90.85 (0.79 to 0.91)
        November13.7 (11.8 to 15.5)5.20.91 (0.84 to 0.98)
        December9.9 (8.4 to 11.5)5.81.00
    Test result month (grouped in pairs)
        December/January10.0 (8.4 to 11.7)5.21.00
        February/March11.4 (10.2 to 12.7)4.30.84 (0.80 to 0.88)
        April/November13.6 (11.8 to 15.1)4.50.87 (0.83 to 0.91)
        May/October15.9 (14.1 to 17.4)4.40.86 (0.82 to 0.90)
        June/July17.7 (15.7 to 19.4)4.00.79 (0.76 to 0.83)
        August/September18.6 (16.4 to 20.6)4.30.84 (0.80 to 0.88)
    • Ambient temperature levels were defined using the mean and 1.25 times the standard deviation (SD) of maximum temperatures by year aggregated over weekly intervals, >mean + 1.25 SD, >mean, >means-1.25 SD, and <means + 1.25 SD (reference), in that order. Thus, the highest and lowest temperature levels were 1.25 times the level above or below the mean, respectively.

    • Each set of estimates (by level, month, and by season of the year) was generated individually using generalized estimating equations with logit link and exchangeable covariance matrix, adjusted for age, sex, and medical region. The estimates are relative ratios from the predictive margins.

    • View popup
    Table 3.

    Fecal Immunochemical Test Sensitivity for All Cases According to Regions, Seasons, Months and Temperature Levels and by Location of Tumors, Kaiser Permanente–Northern California (KPNC) 2007 to 2013

    All CasesRight-Sided CancersLeft-Sided Cancers
    Tests, nCasesPositiveAdjusted sensitivity, %*CasesPositiveAdjusted sensitivity, %*CasesPositiveAdjusted sensitivity, %*
    Overall1,141,1621837142575.8 (73.8 to 77.8)70052572.6 (69.2 to 75.9)112489378.3 (75.9 to 80.7)
    Temperature levels
        1 (Lowest)60,19713110379.6 (77.8 to 81.4)392976.9 (73.8 to 80.0)917481.6 (79.4 to 83.8)
        2322,86446536176.2 (74.3 to 78.2)18613573.0 (70.0 to 76.4)27522378.4 (76.0 to 81.0)
        3160,51626020376.0 (74.0 to 78.0)1078372.8 (69.5 to 76.2)15011978.2 (76.0 to 80.7)
        4528,12984565775.2 (73.2 to 77.2)33025172.0 (68.6 to 75.4)51040377.5 (75.0 to 80.0)
        5 (Highest)69,45613610175.7 (73.6 to 77.8)382772.6 (69.2 to 76.1)987477.9 (75.4 to 80.4)
    Seasons
        Winter239,87334826976.4 (74.4 to 78.3)†1329573.2 (69.9 to 76.5)21517378.6 (76.2 to 81.0)
        Spring393,11955442774.9 (73.0 to 77.0)23517671.6 (68.2 to 75.0)31524977.3 (75.8 to 79.8)
        Summer340,99859346075.0 (73.0 to 77.0)21015971.8 (68.3 to 75.2)37929977.3 (74.8 to 80.0)
        Autumn167,17234226978.6 (76.8 to 80.5)1239575.7 (72.6 to 78.9)21517280.6 (78.5 to 83.0)
    Test result month
        December/January87,82516112779.0 (77.0 to 80.7)†543875.9 (72.8 to 79.1)1068980.9 (78.7 to 83.1)
        February/March220,79229422975.7 (73.7 to 77.7)1188672.4 (69.0 to 75.8)17414178.0 (75.5 to 80.4)
        April/November175,19528321876.4 (74.4 to 78.3)1078173.2 (70.0 to 76.5)17313578.6 (76.2 to 81.0)
        May/October204,81433325976.2 (74.3 to 78.2)14811773.3 (70.0 to 76.6)18214178.5 (76.1 to 81.0)
        June/July249,65638029974.5 (72.5 to 76.6)13810671.1 (67.8 to 74.7)23919176.9 (74.3 to 79.4)
        August/September202,88038629375.6 (73.6 to 77.6)1359772.4 (69.0 to 75.8)25019678.0 (75.5 to 80.3)
    • Ambient temperature levels were defined using the mean and 1.25 times the standard deviation (SD) of maximum temperatures by year aggregated over weekly intervals, >mean + 1.25 SD, >0.25mean, >means-0.25 SD, >means-1.25 SD and <means-1.25 SD (reference), in that order. Thus, the highest and lowest temperature levels were 1.25 times the level above or below the mean, respectively.

    • ↵* The P-values for the differences in sensitivities in pair-wise comparison using Bonferonni correction were all < .01 relative to this group.

    • ↵† This model was adjusted for age, race/ethnicity, and sex. All models included a variable on colorectal cancer diagnosis and the sensitivity was derived using a predictive margins conditioned on cancer diagnosis.

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Fecal Immunochemical Test (FIT) for Colon Cancer Screening: Variable Performance with Ambient Temperature
Chyke A. Doubeni, Christopher D. Jensen, Stacey A. Fedewa, Virginia P. Quinn, Ann G. Zauber, Joanne E. Schottinger, Douglas A. Corley, Theodore R. Levin
The Journal of the American Board of Family Medicine Nov 2016, 29 (6) 672-681; DOI: 10.3122/jabfm.2016.06.160060

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Fecal Immunochemical Test (FIT) for Colon Cancer Screening: Variable Performance with Ambient Temperature
Chyke A. Doubeni, Christopher D. Jensen, Stacey A. Fedewa, Virginia P. Quinn, Ann G. Zauber, Joanne E. Schottinger, Douglas A. Corley, Theodore R. Levin
The Journal of the American Board of Family Medicine Nov 2016, 29 (6) 672-681; DOI: 10.3122/jabfm.2016.06.160060
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