Physical Activity and Stool Metabolite Relationships Among Adults at High Risk for Colorectal Cancer

in Journal of Physical Activity and Health
Restricted access

Purchase article

USD  $24.95

Student 1 year online subscription

USD  $119.00

1 year online subscription

USD  $159.00

Student 2 year online subscription

USD  $227.00

2 year online subscription

USD  $302.00

Background: Adenomatous polyps are associated with an increased risk of developing colorectal cancer. Physical activity (PA) and spending less time sedentary may reduce risk of polyp recurrence and cancer incidence. This study examined associations between PA, sedentary time, and stool metabolites in adults at high risk for developing colorectal cancer. Methods: Participants were ≥18 years old with ≥1 adenomatous polyps removed in the previous 3 years. PA and sedentary time were assessed using an activPAL accelerometer. Stool samples were analyzed for short-chain fatty acids, and primary/secondary bile acid metabolites by mass spectrometry. Linear regression models examined associations between PA, sedentary time, and stool parameters, with dietary fiber as a covariate. Results: Participants (N = 21) were 59 (9) years old and had a body mass index of 28.1 (3.35 kg/m2). Light-intensity PA was associated with butyrate (β = 1.88; 95% confidence interval [CI], 0.477 to 3.291) and propionate (β = 1.79; 95% CI, 0.862 to 2.724). Moderate to vigorous PA was associated with deoxycholic acid (β = −6.13; 95% CI, −12.14 to −0.11) and ursodeoxycholic acid (β = −0.45; 95% CI, −0.80 to −0.12) abundance. Conclusions: Both light and moderate to vigorous PA were associated with gut microbial metabolite production. These findings suggest the importance of examining PA intensity alongside stool metabolites for colorectal cancer prevention.

Beale and Leach are with the Department of Health and Exercise Science, Colorado State University, Fort Collins, CO, USA. Leach is also with the Department of Community and Behavioral Health, Colorado School of Public Health, Aurora, CO, USA. Baxter and Ryan are with the Department of Environmental and Radiological Health Sciences, Colorado State University, Fort Collins, CO, USA. Beale is also with the PA Program, MEDEX Northwest, University of Washington, Seattle, WA, USA. Smith and Ryan are with the Department of Occupational and Environmental Health, Colorado School of Public Health, Fort Collins, CO, USA. Lyden is with the Department of Kinesiology, University of Massachusetts Amherst, Amherst, MA, USA.

Ryan (E.P.Ryan@colostate.edu) is corresponding author.

Supplementary Materials

    • Supplementary Table S1 (PDF 175 KB)
  • 1.

    Levin B, Lieberman D, McFarland B, et al. Screening and surveillance for the early detection of colorectal cancer and adenomatous polyps, 2008: a joint guideline from the American Cancer Society, the US Multi-Society Task Force on Colorectal Cancer, and the American College of Radiology. CA Cancer J Clin. 2008;58(3):130160. PubMed ID: 18322143 doi:10.3322/CA.2007.0018

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2.

    Siegel RL, Miller KD, Goding Sauer A, et al. Colorectal cancer statistics, 2020. CA Cancer J Clin. 2020;70(3):145164. PubMed ID: 32133645 doi:10.3322/caac.21601

  • 3.

    Wolf AMD, Fontham ETH, Church TR, et al. Colorectal cancer screening for average-risk adults: 2018 guideline update from the American Cancer Society. CA Cancer J Clin. 2018;68(4):250281. PubMed ID: 29846947 doi:10.3322/caac.21457

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4.

    Haggar FA, Boushey RP. Colorectal cancer epidemiology: incidence, mortality, survival, and risk factors. Clin Colon Rectal Surg. 2009;22(4):191197. PubMed ID: 21037809 doi:10.1055/s-0029-1242458

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5.

    World Cancer Research Fund/American Institute for Cancer Research. Food, Nutrition, Physical Activity, and the Prevention of Cancer: A Global Perspective. Washington, DC: AICR; 2007.

    • Search Google Scholar
    • Export Citation
  • 6.

    Moore SC, Lee IM, Weiderpass E, et al. Association of leisure-time physical activity with risk of 26 types of cancer in 1.44 million adults. JAMA Intern Med. 2016;176(6):816825. PubMed ID: 27183032 doi:10.1001/jamainternmed.2016.1548

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7.

    Wolin KY, Yan Y, Colditz GA. Physical activity and risk of colon adenoma: a meta-analysis. Br J Cancer. 2011;104(5):882885. PubMed ID: 21304525 doi:10.1038/sj.bjc.6606045

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8.

    Patel AV, Friedenreich CM, Moore SC, et al. American College of Sports Medicine Roundtable Report on physical activity, sedentary behavior, and cancer prevention and control. Med Sci Sports Exerc. 2019;51(11):23912402. PubMed ID: 31626056 doi:10.1249/MSS.0000000000002117

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9.

    Howard RA, Freedman DM, Park Y, Hollenbeck A, Schatzkin A, Leitzmann MF. Physical activity, sedentary behavior, and the risk of colon and rectal cancer in the NIH-AARP Diet and Health Study. Cancer Causes Control. 2008;19(9):939953. PubMed ID: 18437512 doi:10.1007/s10552-008-9159-0

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10.

    Park J, Kim JH, Lee HJ, et al. The effects of physical activity and body fat mass on colorectal polyp recurrence in patients with previous colorectal cancer. Cancer Prev Res. 2017;10(8):478484. doi:10.1158/1940-6207.CAPR-17-0065

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11.

    Holloszy J, Booth F. Biochemical adaptations to endurance exercise in muscle. Annu Rev Physiol. 1976;38(1):273291. doi:10.1146/annurev.ph.38.030176.001421

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12.

    Leon A, Conrad J, Hunninghake D, Serfass R. Effects of a vigorous walking program on body composition, and carbohydrate and lipid metabolism of obese young men. Am J Clin Nutr. 1979;32(9):17761787. PubMed ID: 474467 doi:10.1093/ajcn/32.9.1776

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13.

    Kruijsen-Jaarsma M, Révész D, Bierings M, Buffart L, Takken T. Effects of exercise on immune function in patients with cancer: a systematic review. Exerc Immunol Rev. 2013;19:120143.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14.

    Gleeson M, Bishop NC, Stensel DJ, Lindley MR, Mastana SS, Nimmo MA. The anti-inflammatory effects of exercise: mechanisms and implications for the prevention and treatment of disease. Nat Rev Immunol. 2011;11(9):607615. PubMed ID: 21818123 doi:10.1038/nri3041

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15.

    Ahn J, Sinha R, Pei Z, et al. Human gut microbiome and risk for colorectal cancer. J Natl Cancer Inst. 2013;105(24):19071911. PubMed ID: 24316595 doi:10.1093/jnci/djt300

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16.

    Bull MJ, Plummer NT. Part 1: the human gut microbiome in health and disease. Integrative Med. 2014;13(6):1722.

  • 17.

    Wertheim BC, Martinez ME, Ashbeck EL, et al. Physical activity as a determinant of fecal bile acid levels. Cancer Epidemiol Biomarkers Prev. 2009;18(5):15911598. PubMed ID: 19383885 doi:10.1158/1055-9965.EPI-08-1187

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18.

    Allen JM, Mailing LJ, Niemiro GM, et al. Exercise alters gut microbiota composition and function in lean and obese humans. Med Sci Sports Exerc. 2018;50(4):747757. PubMed ID: 29166320 doi:10.1249/MSS.0000000000001495

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19.

    Zeng H, Umar S, Rust B, Lazarova D, Bordonaro M. Secondary bile acids and short chain fatty acids in the colon: a focus on colonic microbiome, cell proliferation, inflammation, and cancer. Int J Mol Sci. 2019;20(5):1214. doi:10.3390/ijms20051214

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20.

    Hu J, Lin S, Zheng B, Cheung P. Short-chain fatty acids in control of energy metabolism. Crit Rev Food Sci Nutr. 2018;58(8):12431249. doi:10.1080/10408398.2016.1245650

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21.

    Williams EA, Coxhead JM, Mathers JC. Anti-cancer effects of butyrate: use of micro-array technology to investigate mechanisms. Proc Nutr Soc. 2003;62(1):107115. doi:10.1079/PNS2002230

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22.

    Koh A, De Vadder F, Kovatcheva-Datchary P, Backhed F. From dietary fiber to host physiology: short-chain fatty acids as key bacterial metabolites. Cell. 2016;165(6):13321345. PubMed ID: 27259147 doi:10.1016/j.cell.2016.05.041

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23.

    Gentile CL, Weir TL. The gut microbiota at the intersection of diet and human health. Science. 2018;362(6416):776780. doi:10.1126/science.aau5812

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 24.

    Quadrilatero J, Hoffman-Goetz L. Physical activity and colon cancer. J Sports Med Phys Fitness. 2003;43:121138.

  • 25.

    Ridlon JM, Kang DJ, Hylemon PB, Bajaj JS. Bile acids and the gut microbiome. Curr Opin Gastroenterol. 2014;30(3):332338. PubMed ID: 24625896 doi:10.1097/MOG.0000000000000057

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26.

    Turnbaugh PJ, Gordon JI. The core gut microbiome, energy balance and obesity. J Physiol. 2009;587(17):41534158. PubMed ID: 19491241 doi:10.1113/jphysiol.2009.174136

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27.

    Chiang JY. Regulation of bile acid synthesis: pathways, nuclear receptors, and mechanisms. J Hepatol. 2004;40(3):539551. PubMed ID: 15123373 doi:10.1016/j.jhep.2003.11.006

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28.

    Makki K, Deehan EC, Walter J, Backhed F. The impact of dietary fiber on gut microbiota in host health and disease. Cell Host Microbe. 2018;23(6):705715. PubMed ID: 29902436 doi:10.1016/j.chom.2018.05.012

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29.

    Rock CL, Thomson C, Gansler T, et al. American Cancer Society guideline for diet and physical activity for cancer prevention. CA Cancer J Clin. 2020;70(4):245271. PubMed ID: 32515498 doi:10.3322/caac.21591

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30.

    Kujala UM, Makinen VP, Heinonen I, et al. Long-term leisure-time physical activity and serum metabolome. Circulation. 2013;127(3):340348. doi:10.1161/CIRCULATIONAHA.112.105551

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31.

    Xiao Q, Moore SC, Keadle SK, et al. Objectively measured physical activity and plasma metabolomics in the Shanghai physical activity study. Int J Epidemiol. 2016;45(5):14331444. PubMed ID: 27073263 doi:10.1093/ije/dyw033

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32.

    Leach HJ, Baxter BA, Beale MN, et al. Feasibility of beans/bran enriching nutritional eating for intestinal health & cancer including activity for longevity: a pilot trial to improve healthy lifestyles among individuals at high risk for colorectal cancer. Integr Cancer Ther. 2020;19:1534735420967101. doi:10.1177/1534735420967101.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33.

    George SM, Alfano CM, Groves J, et al. Objectively measured sedentary time is related to quality of life among cancer survivors. PLoS One. 2014;9(2):e87937. PubMed ID: 24505335 doi:10.1371/journal.pone.0087937

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34.

    Grant PM, Ryan CG, Tigbe WW, Granat MH. The validation of a novel activity monitor in the measurement of posture and motion during everyday activities. Br J Sports Med. 2006;40(12):992997. PubMed ID: 16980531 doi:10.1136/bjsm.2006.030262

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35.

    Lyden K, Keadle SK, Staudenmayer J, Freedson PS. The activPAL accurately classifies activity intensity categories in healthy adults. Med Sci Sports Exerc. 2017;49(5):10221028. PubMed ID: 28410327 doi:10.1249/MSS.0000000000001177

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36.

    Paltechnologies. Activpal Operating Guide. 2010. http://www.paltechnologies.com/. Accessed May 20, 2019.

  • 37.

    Lyden K, Staudenmayer J. Activpal processing: process activPAL Events Files. 2016. http://CRAN.R-project.org/package=activpalProcessing. Accessed May 20, 2019.

    • Search Google Scholar
    • Export Citation
  • 38.

    Ainsworth BE, Haskell WL. Compendium of physical activities: a second update of codes and MET values. Med Sci Sports Exerc. 2011;43(8):15751581. PubMed ID: 21681120 doi:10.1249/MSS.0b013e31821ece12

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39.

    Yang YJ, Kim MK, Hwang SH, Ahn Y, Shim JE, Kim DH. Relative validities of 3-day food records and the food frequency questionnaire. Nutr Res Pract. 2010;4(2):142148. PubMed ID: 20461203 doi:10.4162/nrp.2010.4.2.142

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40.

    Lenth R. Java applets for power and sample size [Computer software]. 2006. http://www.divms.uiowa.edu/∼rlenth/Power/. Accessed May 20, 2019.

    • Search Google Scholar
    • Export Citation
  • 41.

    Piercy KL, Troiano RP, Ballard RM, et al. The physical activity guidelines for Americans. JAMA. 2018;320(19):20202028. PubMed ID: 30418471 doi:10.1001/jama.2018.14854

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 42.

    Matsumoto M, Inoue R, Tsukahara T, et al. Voluntary running exercise alters microbiota composition and increases n-butyrate concentration in the rat cecum. Biosci Biotechnol Biochem. 2008;72(2):572576. PubMed ID: 18256465 doi:10.1271/bbb.70474

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 43.

    Louis P, Hold GL, Flint HJ. The gut microbiota, bacterial metabolites and colorectal cancer. Nat Rev Microbiol. 2014;12(10):661672. PubMed ID: 25198138 doi:10.1038/nrmicro3344

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 44.

    Huang WK, Hsu HC, Liu JR, et al. The association of ursodeoxycholic acid use with colorectal cancer risk: a Nationwide Cohort Study. Medicine. 2016;95(11):e2980. doi:10.1097/MD.0000000000002980.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 45.

    Ajouz H, Mukherhi D, Shamseddine A. Secondary bile acids: an underrecognized cause of colon cancer. J Surg Oncol. 2014;12(164):14.

  • 46.

    Colley RC, Butler G, Garriguet D, Prince SA. Comparison of self-reported and accelerometer-measured physical activity in Canadian adults. Health Rep. 2018;29(12):315. PubMed ID: 30566204

    • PubMed
    • Search Google Scholar
    • Export Citation
All Time Past Year Past 30 Days
Abstract Views 1738 1738 147
Full Text Views 24 24 3
PDF Downloads 25 25 3