Dietary factors may influence colorectal cancer (CRC) survival through effects on inflammation. We examined the association between post-CRC diagnosis inflammatory potential of diet and all-cause and cancer-specific mortality in the Women’s Health Initiative.
The study included 463 postmenopausal women who developed CRC during follow-up and completed a food frequency questionnaire (FFQ), on average 1.7 years after diagnosis. Women were followed from CRC diagnosis until death, censoring, or the end of follow-up in October 2014. Energy-adjusted dietary inflammatory index (E-DII)® scores were calculated from the FFQ and dietary supplement inventory. Cox proportional hazards models were fitted to estimate multivariable-adjusted HRs and 95% confidence intervals (CIs) for all-cause, total cancer, and CRC-specific mortality with the most pro-inflammatory E-DII scores (tertile 3) as referent.
After a median 11.6 years of follow-up, 162 deaths occurred, including 77 from CRC. Lowest tertile (i.e., most anti-inflammatory) E-DII scores from diet plus supplements were associated with significantly lower all-cause mortality (HRT1vsT3 = 0.49; 95% CI 0.31–0.79) compared to the most pro-inflammatory E-DII tertile. Modest associations with total cancer mortality or CRC-specific mortality were observed, though 95% CIs included 1.
Consuming a dietary pattern and supplements with more anti-inflammatory potential after CRC diagnosis may improve overall survival among postmenopausal women.
This is a preview of subscription content, log in to check access.
Buy single article
Instant access to the full article PDF.
Price includes VAT for USA
Subscribe to journal
Immediate online access to all issues from 2019. Subscription will auto renew annually.
This is the net price. Taxes to be calculated in checkout.
Siegel RL, Miller KD, Jemal A (2018) Cancer statistics, 2018. CA Cancer J Clin 68(1):7–30. https://doi.org/10.3322/caac.21442
American Cancer Society. Cancer treatment & survivorship facts & figures, 2016–2017
Denlinger CS, Engstrom PF (2011) Colorectal cancer survivorship: movement matters. Cancer Prev Res (Phila) 4(4):502–511. https://doi.org/10.1158/1940-6207.capr-11-0098
Vrieling A, Kampman E (2010) The role of body mass index, physical activity, and diet in colorectal cancer recurrence and survival: a review of the literature. Am J Clin Nutr 92(3):471–490
Ratjen I, Schafmayer C, di Giuseppe R, Waniek S, Plachta-Danielzik S, Koch M, Nöthlings U, Hampe J, Schlesinger S, Lieb W (2017) Postdiagnostic Mediterranean and healthy nordic dietary patterns are inversely associated with all-cause mortality in long-term colorectal cancer survivors. J Nutr 147(4):636–644
World Cancer Research Fund/American Institute for Cancer Research (2018) Diet, nutrition, physical activity, and cancer: a global perspective. Third expert report. AICR, Washington, DC
Schoenberg MH (2016) Physical activity and nutrition in primary and tertiary prevention of colorectal cancer. Visc Med 32(3):199–204
Krebs-Smith SM, Subar AF, Reedy J (2015) Examining dietary patterns in relation to chronic disease: matching measures and methods to questions of interest. Circulation 132(9):790–793. https://doi.org/10.1161/circulationaha.115.018010
Meyerhardt JA, Niedzwiecki D, Hollis D, Saltz LB, Hu FB, Mayer RJ, Nelson H, Whittom R, Hantel A, Thomas J (2007) Association of dietary patterns with cancer recurrence and survival in patients with stage III colon cancer. JAMA 298(7):754–764
Fung TT, Kashambwa R, Sato K, Chiuve SE, Fuchs CS, Wu K, Giovannucci E, Ogino S, Hu FB, Meyerhardt JA (2014) Post diagnosis diet quality and colorectal cancer survival in women. PLoS One 9(12):e115377
Crozier JE, McKee RF, McArdle CS, Angerson WJ, Anderson JH, Horgan PG, McMillan DC (2006) The presence of a systemic inflammatory response predicts poorer survival in patients receiving adjuvant 5-FU chemotherapy following potentially curative resection for colorectal cancer. Br J Cancer 94(12):1833–1836. https://doi.org/10.1038/sj.bjc.6603185
Cooney RV, Chai W, Franke AA, Wilkens LR, Kolonel LN, Le Marchand L (2013) C-reactive protein, lipid-soluble micronutrients, and survival in colorectal cancer patients. Cancer Epidemiol Biomark Prev 22(7):1278–1288. https://doi.org/10.1158/1055-9965.epi-13-0199
Tabung FK, Steck SE, Ma Y, Liese AD, Zhang J, Caan B, Hou L, Johnson KC, Mossavar-Rahmani Y, Shivappa N, Wactawski-Wende J, Ockene JK, Hebert JR (2015) The association between dietary inflammatory index and risk of colorectal cancer among postmenopausal women: results from the Women’s Health Initiative. Cancer Causes Control 26(3):399–408. https://doi.org/10.1007/s10552-014-0515-y
Steck SE, Guinter M, Zheng J, Thomson CA (2015) Index-based dietary patterns and colorectal cancer risk: a systematic review. Adv Nutr 6(6):763–773. https://doi.org/10.3945/an.115.009746
Shivappa N, Prizment AE, Blair CK, Jacobs DR, Steck SE, Hébert JR (2014) Dietary inflammatory index and risk of colorectal cancer in the Iowa Women’s Health Study. Cancer Epidemiol Biomark Prev 23(11):2383–2392. https://doi.org/10.1158/1055-9965.epi-14-0537
Wirth MD, Shivappa N, Steck SE, Hurley TG, Hebert JR (2015) The dietary inflammatory index is associated with colorectal cancer in the National Institutes of Health-American Association of Retired Persons Diet and Health Study. Br J Nutr 113(11):1819–1827. https://doi.org/10.1017/s000711451500104x
Harmon BE, Wirth MD, Boushey CJ, Wilkens LR, Draluck E, Shivappa N, Steck SE, Hofseth L, Haiman CA, Le Marchand L, Hébert JR (2017) The dietary inflammatory index is associated with colorectal cancer risk in the multiethnic Cohort 1–3. J Nutr 147(3):430–438. https://doi.org/10.3945/jn.116.242529
Shivappa N, Hebert JR, Steck SE, Hofseth LJ, Shehadah I, Bani-Hani KE, Al-Jaberi T, Al-Nusairr M, Heath D, Tayyem R (2017) Dietary inflammatory index and odds of colorectal cancer in a case-control study from Jordan. Appl Physiol Nutr Metab 42(7):744–749. https://doi.org/10.1139/apnm-2017-0035
Tabung FK, Steck SE, Ma Y, Liese AD, Zhang J, Lane DS, Ho GYF, Hou L, Snetselaar L, Ockene JK, Hebert JR (2017) Changes in the inflammatory potential of diet over time and risk of colorectal cancer in postmenopausal women. Am J Epidemiol 186(5):514–523. https://doi.org/10.1093/aje/kwx115
Ratjen I, Shivappa N, Schafmayer C, Burmeister G, Nothlings U, Hampe J, Hebert JR, Lieb W, Schlesinger S (2019) Association between the dietary inflammatory index and all-cause mortality in colorectal cancer long-term survivors. Int J Cancer 144(6):1292–1301. https://doi.org/10.1002/ijc.31919
Guinter MA, McCullough ML, Gapstur SM, Campbell PT (2018) Associations of pre- and postdiagnosis diet quality with risk of mortality among men and women with colorectal cancer. J Clin Oncol. https://doi.org/10.1200/jco.18.00714
Study TWsHI (1998) Design of the Women’s Health Initiative clinical trial and observational study. Control Clin Trials 19(1):61–109
Hays J, Hunt JR, Hubbell FA, Anderson GL, Limacher M, Allen C, Rossouw JE (2003) The Women’s Health Initiative recruitment methods and results. Ann Epidemiol 13(9 Suppl):S18–S77
Langer RD, White E, Lewis CE, Kotchen JM, Hendrix SL, Trevisan M (2003) The Women’s Health Initiative Observational Study: baseline characteristics of participants and reliability of baseline measures. Ann Epidemiol 13(9 Suppl):S107–S121
Patterson RE, Kristal AR, Tinker LF, Carter RA, Bolton MP, Agurs-Collins T (1999) Measurement characteristics of the Women’s Health Initiative food frequency questionnaire. Ann Epidemiol 9(3):178–187
Schakel S, Sievert Y, Buzzard I (1988) Sources of data for developing and maintaining a nutrient database. J Am Diet Assoc 88(10):1268–1271
Patterson RE, Kristal A, Rodabough R, Caan B, Lillington L, Mossavar-Rahmani Y, Simon MS, Snetselaar L, van Horn L (2003) Changes in food sources of dietary fat in response to an intensive low-fat dietary intervention: early results from the Women’s Health Initiative. J Am Diet Assoc 103(4):454–460
Shivappa N, Steck SE, Hurley TG, Hussey JR, Hebert JR (2014) Designing and developing a literature-derived, population-based dietary inflammatory index. Public Health Nutr 17(8):1689–1696. https://doi.org/10.1017/s1368980013002115
Shivappa N, Steck SE, Hurley TG, Hussey JR, Ma Y, Ockene IS, Tabung F, Hébert JR (2014) A population-based dietary inflammatory index predicts levels of C-reactive protein in the Seasonal Variation of Blood Cholesterol Study (SEASONS). Public Health Nutr 17(08):1825–1833
Tabung FK, Steck SE, Zhang J, Ma Y, Liese AD, Agalliu I, Hingle M, Hou L, Hurley TG, Jiao L (2015) Construct validation of the dietary inflammatory index among postmenopausal women. Ann Epidemiol 25(6):398–405
Shivappa N, Hébert JR, Rietzschel ER, De Buyzere ML, Langlois M, Debruyne E, Marcos A, Huybrechts I (2015) Associations between dietary inflammatory index and inflammatory markers in the Asklepios Study. Br J Nutr 113(04):665–671
George SM, Ballard-Barbash R, Shikany JM, Caan BJ, Freudenheim JL, Kroenke CH, Vitolins MZ, Beresford SA, Neuhouser ML (2014) Better postdiagnosis diet quality is associated with reduced risk of death among postmenopausal women with invasive breast cancer in the Women’s Health Initiative. Cancer Epidemiol Biomark Prev 23(4):575–583
Irwin ML, McTiernan A, Manson JE, Thomson CA, Sternfeld B, Stefanick ML, Wactawski-Wende J, Craft L, Lane D, Martin LW, Chlebowski R (2011) Physical activity and survival in postmenopausal women with breast cancer: results from the Women’s Health Initiative. Cancer Prev Res (Philadelphia, Pa) 4(4):522–529. https://doi.org/10.1158/1940-6207.capr-10-0295
Seidell JC, Flegal KM (1997) Assessing obesity: classification and epidemiology. Br Med Bull 53(2):238–252
Curb JD, McTiernan A, Heckbert SR, Kooperberg C, Stanford J, Nevitt M, Johnson KC, Proulx-Burns L, Pastore L, Criqui M, Daugherty S (2003) Outcomes ascertainment and adjudication methods in the Women’s Health Initiative. Ann Epidemiol 13(9 Suppl):S122–S128
Fritz A, Ries L (1998) The SEER Program code manual. National Cancer Institute, Bethesda (United States Cancer Statistics: 2004 incidence and mortality)
Coghill AE, Phipps AI, Bavry AA, Wactawski-Wende J, Lane DS, LaCroix A, Newcomb PA (2012) The association between NSAID use and colorectal cancer mortality: results from the Women’s Health Initiative. Cancer Epidemiol Biomark Prev 21(11):1966–1973. https://doi.org/10.1158/1055-9965.epi-12-0672
Zheng J, Tabung FK, Zhang J, Liese AD, Shivappa N, Ockene JK, Caan B, Kroenke CH, Hebert JR, Steck SE (2018) Association between post-cancer diagnosis dietary inflammatory potential and mortality among invasive breast cancer survivors in the Women’s Health Initiative. Cancer Epidemiol Biomark Prev 27(4):454–463. https://doi.org/10.1158/1055-9965.epi-17-0569
Schoenfeld D (1980) Chi squared goodness-of-fit tests for the proportional hazards regression model. Biometrika 67(1):145–153
Hess KR (1994) Assessing time-by-covariate interactions in proportional hazards regression models using cubic spline functions. Stat Med 13(10):1045–1062
Therneau TM, Grambsch PM (2000) Modeling survival data: extending the Cox model. Springer Science & Business Media, Berlin
Desquilbet L, Mariotti F (2010) Dose-response analyses using restricted cubic spline functions in public health research. Stat Med 29(9):1037–1057. https://doi.org/10.1002/sim.3841
Kerr J, Anderson C, Lippman SM (2017) Physical activity, sedentary behaviour, diet, and cancer: an update and emerging new evidence. Lancet Oncol 18(8):e457–e471. https://doi.org/10.1016/s1470-2045(17)30411-4
Galas A, Kulig J (2014) Low-grade dietary-related inflammation and survival after colorectal cancer surgery. J Cancer Res Clin Oncol 140(9):1517–1525. https://doi.org/10.1007/s00432-014-1711-6
Meyerhardt JA (2011) Beyond standard adjuvant therapy for colon cancer: role of nonstandard interventions. Semin Oncol 38(4):533–541. https://doi.org/10.1053/j.seminoncol.2011.05.007
Wirth MD, Hébert JR, Shivappa N, Hand GA, Hurley TG, Drenowatz C, McMahon D, Shook RP, Blair SN (2016) Anti-inflammatory Dietary Inflammatory Index scores are associated with healthier scores on other dietary indices. Nutr Res 36(3):214–219
Meyerhardt JA, Sato K, Niedzwiecki D, Ye C, Saltz LB, Mayer RJ, Mowat RB, Whittom R, Hantel A, Benson A, Wigler DS, Venook A, Fuchs CS (2012) Dietary glycemic load and cancer recurrence and survival in patients with stage III colon cancer: findings from CALGB 89803. J Natl Cancer Inst 104(22):1702–1711. https://doi.org/10.1093/jnci/djs399
Yuan C, Bao Y, Sato K, Nimptsch K, Song M, Brand-Miller JC, Morales-Oyarvide V, Zoltick ES, Keum N, Wolpin BM, Meyerhardt JA, Chan AT, Willett WC, Stampfer MJ, Wu K, Giovannucci EL, Fuchs CS, Ng K (2017) Influence of dietary insulin scores on survival in colorectal cancer patients. Br J Cancer 117(7):1079–1087. https://doi.org/10.1038/bjc.2017.272
Macpherson H, Pipingas A, Pase MP (2013) Multivitamin-multimineral supplementation and mortality: a meta-analysis of randomized controlled trials. Am J Clin Nutr 97(2):437–444. https://doi.org/10.3945/ajcn.112.049304
Schwingshackl L, Boeing H, Stelmach-Mardas M, Gottschald M, Dietrich S, Hoffmann G, Chaimani A (2017) Dietary supplements and risk of cause-specific death, cardiovascular disease, and cancer: a systematic review and meta-analysis of primary prevention trials. Adv Nutr 8(1):27–39. https://doi.org/10.3945/an.116.013516
Gaziano JM, Sesso HD, Christen WG, Bubes V, Smith JP, MacFadyen J, Schvartz M, Manson JE, Glynn RJ, Buring JE (2012) Multivitamins in the prevention of cancer in men: the Physicians’ Health Study II randomized controlled trial. JAMA 308(18):1871–1880. https://doi.org/10.1001/jama.2012.14641
Wassertheil-Smoller S, McGinn AP, Budrys N, Chlebowski R, Ho GY, Johnson KC, Lane DS, Li W, Neuhouser ML, Saquib J, Shikany JM, Song Y, Thomson C (2013) Multivitamin and mineral use and breast cancer mortality in older women with invasive breast cancer in the Women’s Health Initiative. Breast Cancer Res Treat 141(3):495–505. https://doi.org/10.1007/s10549-013-2712-x
Kwan ML, Greenlee H, Lee VS, Castillo A, Gunderson EP, Habel LA, Kushi LH, Sweeney C, Tam EK, Caan BJ (2011) Multivitamin use and breast cancer outcomes in women with early-stage breast cancer: the Life After Cancer Epidemiology study. Breast Cancer Res Treat 130(1):195–205. https://doi.org/10.1007/s10549-011-1557-4
Neuhouser ML, Wassertheil-Smoller S, Thomson C, Aragaki A, Anderson GL, Manson JE, Patterson RE, Rohan TE, van Horn L, Shikany JM, Thomas A, LaCroix A, Prentice RL (2009) Multivitamin use and risk of cancer and cardiovascular disease in the Women’s Health Initiative cohorts. Arch Intern Med 169(3):294–304. https://doi.org/10.1001/archinternmed.2008.540
Holmes RS, Zheng Y, Baron JA, Li L, McKeown-Eyssen G, Newcomb PA, Stern MC, Haile RW, Grady WM, Potter JD, Le Marchand L, Campbell PT, Figueiredo JC, Limburg PJ, Jenkins MA, Hopper JL, Ulrich CM, Colon Cancer Family R (2010) Use of folic acid-containing supplements after a diagnosis of colorectal cancer in the Colon Cancer Family Registry. Cancer Epidemiol Biomark Prev 19(8):2023–2034. https://doi.org/10.1158/1055-9965.EPI-09-1097
Lewis CM, Wolf WA, Xun P, Sandler RS, He K (2016) Racial differences in dietary changes and quality of life after a colorectal cancer diagnosis: a follow-up of the Study of Outcomes in Colorectal Cancer Survivors cohort. Am J Clin Nutr 103(6):1523–1530. https://doi.org/10.3945/ajcn.115.126276
Edwards BK, Noone AM, Mariotto AB, Simard EP, Boscoe FP, Henley SJ, Jemal A, Cho H, Anderson RN, Kohler BA, Eheman CR, Ward EM (2014) Annual Report to the Nation on the status of cancer, 1975–2010, featuring prevalence of comorbidity and impact on survival among persons with lung, colorectal, breast, or prostate cancer. Cancer 120(9):1290–1314. https://doi.org/10.1002/cncr.28509
Erreni M, Mantovani A, Allavena P (2011) Tumor-associated macrophages (TAM) and inflammation in colorectal cancer. Cancer Microenviron 4(2):141–154. https://doi.org/10.1007/s12307-010-0052-5
Wang S, Liu Z, Wang L, Zhang X (2009) NF-κB signaling pathway, inflammation and colorectal cancer. Cell Mol Immunol 6(5):327
Richmond A (2002) Nf-kappa B, chemokine gene transcription and tumour growth. Nat Rev Immunol 2(9):664–674. https://doi.org/10.1038/nri887
Ogino S, Kirkner GJ, Nosho K, Irahara N, Kure S, Shima K, Hazra A, Chan AT, Dehari R, Giovannucci EL, Fuchs CS (2008) Cyclooxygenase-2 expression is an independent predictor of poor prognosis in colon cancer. Clin Cancer Res 14(24):8221–8227. https://doi.org/10.1158/1078-0432.ccr-08-1841
Proctor MJ, McMillan DC, Horgan PG, Fletcher CD, Talwar D, Morrison DS (2015) Systemic inflammation predicts all-cause mortality: a glasgow inflammation outcome study. PLoS One 10(3):e0116206
McMillan DC (2013) The systemic inflammation-based Glasgow Prognostic Score: a decade of experience in patients with cancer. Cancer Treat Rev 39(5):534–540
Leung EY, Crozier JE, Talwar D, O’Reilly DS, McKee RF, Horgan PG, McMillan DC (2008) Vitamin antioxidants, lipid peroxidation, tumour stage, the systemic inflammatory response and survival in patients with colorectal cancer. Int J Cancer 123(10):2460–2464. https://doi.org/10.1002/ijc.23811
Tabung FK, Steck SE, Zhang J, Ma Y, Liese AD, Tylavsky FA, Vitolins MZ, Ockene JK, Hebert JR (2016) Longitudinal changes in the dietary inflammatory index: an assessment of the inflammatory potential of diet over time in postmenopausal women. Eur J Clin Nutr 70(12):1374–1380. https://doi.org/10.1038/ejcn.2016.116
Neuhouser ML, Tinker L, Shaw PA, Schoeller D, Bingham SA, Horn LV, Beresford SA, Caan B, Thomson C, Satterfield S, Kuller L, Heiss G, Smit E, Sarto G, Ockene J, Stefanick ML, Assaf A, Runswick S, Prentice RL (2008) Use of recovery biomarkers to calibrate nutrient consumption self-reports in the Women’s Health Initiative. Am J Epidemiol 167(10):1247–1259. https://doi.org/10.1093/aje/kwn026
Tabung FK, Steck SE, Liese AD, Zhang J, Ma Y, Caan B, Chlebowski RT, Freudenheim JL, Hou L, Mossavar-Rahmani Y, Shivappa N, Vitolins MZ, Wactawski-Wende J, Ockene JK, Hebert JR (2016) Association between dietary inflammatory potential and breast cancer incidence and death: results from the Women’s Health Initiative. Br J Cancer 114(11):1277–1285. https://doi.org/10.1038/bjc.2016.98
We thank the Women’s Health Initiative Investigators: Program Office (National Heart, Lung, and Blood Institute, Bethesda, Maryland): Jacques Rossouw, Shari Ludlam, Joan McGowan, Leslie Ford, and Nancy Geller. Clinical Coordinating Center (Fred Hutchinson Cancer Research Center, Seattle, WA): Garnet Anderson, Ross Prentice, Andrea LaCroix, and Charles Kooperberg. Investigators and Academic Centers (Brigham and Women’s Hospital, Harvard Medical School, Boston, MA): JoAnn E. Manson (MedStar Health Research Institute/Howard University, Washington, DC); Barbara V. Howard (Stanford Prevention Research Center, Stanford, CA); Marcia L. Stefanick (The Ohio State University, Columbus, OH); Rebecca Jackson (University of Arizona, Tucson/Phoenix, AZ); Cynthia A. Thomson (University at Buffalo, Buffalo, NY); Jean Wactawski-Wende (University of Florida, Gainesville/Jacksonville, FL); Marian Limacher (University of Iowa, Iowa City/Davenport, IA); Jennifer Robinson (University of Pittsburgh, Pittsburgh, PA); Lewis Kuller (Wake Forest University School of Medicine, Winston-Salem, NC); Sally Shumaker (University of Nevada, Reno, NV); Robert Brunner (University of Minnesota, Minneapolis, MN); Karen L. Margolis. Women’s Health Initiative Memory Study (Wake Forest University School of Medicine, Winston-Salem, NC): Mark Espeland. Additional Information: a full list of all the investigators who have contributed to Women’s Health Initiative science appears at https://www.whi.org/researchers/Documents%20%20Write%20a%20Paper/WHI%20Investigator%20Long%20List.pdf. We also thank the Women’s Health Initiative staff and the trial participants for their outstanding dedication and commitment.
J Zheng, FK Tabung, J Zhang, JK Ockene, JR Hébert, and SE Steck were supported by Grant #318258 from the American Institute for Cancer Research. J Zheng was supported by Cancer Prevention & Research Institute of Texas Grant PR170259. FK Tabung was supported by National Cancer Institute grant # K99CA207736. N Shivappa and JR Hébert were supported by Grant number R44 DK103377 from the National Institute of Diabetes and Digestive and Kidney Diseases. The WHI program is funded by the National Heart, Lung, and Blood Institute, National Institutes of Health, U.S. Department of Health and Human Services through Contracts HHSN268201600018C, HHSN268201600001C, HHSN268201600002C, HHSN268201600003C, and HHSN268201600004C.
Conflict of interest
Dr. Hébert owns controlling interest in Connecting Health Innovations, LLC (CHI), a company planning to license the right to his invention of the dietary inflammatory index (DII®) from the University of South Carolina to develop computer and smart phone applications for patient counseling and dietary intervention in clinical settings. Dr. Nitin Shivappa is an employee of CHI.
The WHI protocol was approved by the Institutional Review Boards at the Clinical Coordinating Center (CCC) at the Fred Hutchinson Cancer Research Center (Seattle, WA) and at each of the participating Clinical Centers, and has, therefore, been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments. All participants provided written informed consent in accordance with the US Common Rule. This study was also approved as exempt category from the Institutional Review Boards at the University of South Carolina where the study was conducted.
Electronic supplementary material
Below is the link to the electronic supplementary material.
About this article
Cite this article
Zheng, J., Tabung, F.K., Zhang, J. et al. Post-cancer diagnosis dietary inflammatory potential is associated with survival among women diagnosed with colorectal cancer in the Women’s Health Initiative. Eur J Nutr 59, 965–977 (2020). https://doi.org/10.1007/s00394-019-01956-z
- Post-cancer diagnosis
- Dietary pattern
- Colorectal cancer survival
- Cohort study
- Postmenopausal women