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Association between inflammatory potential of diet and mortality in the Iowa Women’s Health study

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Abstract

Purpose

Chronic diseases such as cancer and cardiovascular disease (CVD) are well-established causes of disability and premature deaths. Dietary components that are known to affect chronic inflammation have been implicated in the etiology and prognosis of these chronic diseases. We examined the ability of the dietary inflammatory index (DII) to predict overall, cancer and CVD mortality in the Iowa Women’s Health study.

Methods

The DII was computed from baseline dietary intake assessed in this cohort of 37,525 women, who were aged 55–69 years when enrolled starting in 1986. During the follow-up period, through December 31, 2010, in a total of 17,793 deaths, 5044 cancer- and 6528 CVD-related deaths were identified through mortality record linkage. Cox proportional hazards regression was used to estimate hazard ratios (HR) with DII expressed both as a continuous variable and as quartiles.

Results

Comparing subjects in DII Quartile 4 versus Quartile 1, modest positive associations were noted for all-cause mortality (HRQ4vsQ1 1.07; 95 % CI 1.01–1.13; p-trend = 0.006), digestive cancer mortality (HRQ4vsQ1 1.19; 95 % CI 1.00–1.43; p-trend = 0.05), CVD mortality (HRQ4vsQ1 1.09; 95 % CI 1.01–1.18; p-trend = 0.08), non-cancer/non-CVD/non-acute mortality (HRQ4vsQ1 1.09; 95 % CI 1.00–1.19; p-trend = 0.19), coronary heart disease (CHD) mortality (HRQ4vsQ1 1.17; 95 % CI 1.05–1.30; p-trend = 0.001) and chronic obstructive pulmonary disease (COPD) mortality (HRQ4vsQ1 1.43; 95 % CI 1.18–1.75; p-trend = 0.0006). No substantial associations were observed for mortality from stroke, Alzheimer’s disease or unspecified dementia.

Conclusion

These results indicate that a pro-inflammatory diet, as evidenced by higher DII scores, may be associated with total mortality as well as mortality from digestive cancer, CVD, CHD and COPD.

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References

  1. Keibel A, Singh V, Sharma MC (2009) Inflammation, microenvironment, and the immune system in cancer progression. Curr Pharm Des 15(17):1949–1955

    Article  CAS  Google Scholar 

  2. Pan MH, Lai CS, Dushenkov S, Ho CT (2009) Modulation of inflammatory genes by natural dietary bioactive compounds. J Agric Food Chem 57(11):4467–4477

    Article  CAS  Google Scholar 

  3. Thun MJ, Henley SJ, Gansler T (2004) Inflammation and cancer: an epidemiological perspective. Novartis Found Symp 256:6-21; discussion 22-28, 49-52, 266-269

  4. Warnberg J, Gomez-Martinez S, Romeo J, Diaz LE, Marcos A (2009) Nutrition, inflammation, and cognitive function. Ann N Y Acad Sci 1153:164–175

    Article  CAS  Google Scholar 

  5. Erlinger TP, Muntner P, Helzlsouer KJ (2004) WBC count and the risk of cancer mortality in a national sample of U.S. adults: results from the second national health and nutrition examination survey mortality study. Cancer Epidemiol Biomarkers Prev 13(6):1052–1056

    Google Scholar 

  6. Balkwill F, Mantovani A (2001) Inflammation and cancer: back to Virchow?[see comment]. Lancet 357(9255):539–545

    Article  CAS  Google Scholar 

  7. Coussens LM, Werb Z (2002) Inflammation and cancer. Nature 420(6917):860–867

    Article  CAS  Google Scholar 

  8. Balkwill F (2009) Tumour necrosis factor and cancer. Nat Rev Cancer 9(5):361–371

    Article  CAS  Google Scholar 

  9. Pearson TA, Mensah GA, Alexander RW, Anderson JL, Cannon RO 3rd, Criqui M, Fadl YY, Fortmann SP, Hong Y, Myers GL, Rifai N, Smith SC Jr, Taubert K, Tracy RP, Vinicor F (2003) Markers of inflammation and cardiovascular disease: application to clinical and public health practice: A statement for healthcare professionals from the centers for disease control and prevention and the american heart association. Circulation 107(3):499–511

    Article  Google Scholar 

  10. 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 Biomarkers Prev 15:15

    Google Scholar 

  11. Jacobs DR, Gross MD, Tapsell LC (2009) Food synergy: an operational concept for understanding nutrition. Am J Clin Nutr 89(5):1543S–1548S. doi:10.3945/ajcn.2009.26736B

    Article  CAS  Google Scholar 

  12. Jacobs DR, Steffen LM (2003) Nutrients, foods, and dietary patterns as exposures in research: a framework for food synergy. Am J Clin Nutr 78(3):508S–513S

    CAS  Google Scholar 

  13. Hebert JR, Wirth M, Davis L, Davis B, Harmon BE, Hurley TG, Drayton R, Angela Murphy E, Shivappa N, Wilcox S, Adams SA, Brandt HM, Blake CE, Armstead CA, Steck SE, Blair SN (2013) C-reactive protein levels in African Americans: a diet and lifestyle randomized community trial. Am J Prev Med 45(4):430–440. doi:10.1016/j.amepre.2013.05.011

    Article  Google Scholar 

  14. Imayama I, Ulrich CM, Alfano CM, Wang C, Xiao L, Wener MH, Campbell KL, Duggan C, Foster-Schubert KE, Kong A, Mason CE, Wang CY, Blackburn GL, Bain CE, Thompson HJ, McTiernan A (2012) Effects of a caloric restriction weight loss diet and exercise on inflammatory biomarkers in overweight/obese postmenopausal women: a randomized controlled trial. Cancer Res 72(9):2314–2326. doi:10.1158/0008-5472.CAN-11-3092

    Article  CAS  Google Scholar 

  15. Shivappa N, Prizment AE, Blair CK, Jacobs DR Jr, Steck SE, Hebert JR (2014) Dietary inflammatory index and risk of colorectal cancer in the Iowa women’s health study. Cancer Epidemiol Biomarkers Prev 23(11):2383–2392. doi:10.1158/1055-9965.EPI-14-0537

    Article  CAS  Google Scholar 

  16. Bobe G, Sansbury LB, Albert PS, Cross AJ, Kahle L, Ashby J, Slattery ML, Caan B, Paskett E, Iber F, Kikendall JW, Lance P, Daston C, Marshall JR, Schatzkin A, Lanza E (2008) Dietary flavonoids and colorectal adenoma recurrence in the polyp prevention trial. Cancer Epidemiol Biomarkers Prev 17(6):1344–1353. doi:10.1158/1055-9965.EPI-07-0747

    Article  CAS  Google Scholar 

  17. Cai H, Shu XO, Gao YT, Li H, Yang G, Zheng W (2007) A prospective study of dietary patterns and mortality in Chinese women. Epidemiology 18(3):393–401

    Article  Google Scholar 

  18. Zazpe I, Sanchez-Tainta A, Toledo E, Sanchez-Villegas A, Martinez-Gonzalez MA (2013) Dietary patterns and total mortality in a mediterranean cohort: the SUN project. J Acad Nutr Diet 1(13):01180–01185

    Google Scholar 

  19. Mitrou PN, Kipnis V, Thiébaut AM et al (2007) Mediterranean dietary pattern and prediction of all-cause mortality in a US population: results from the NIH-AARP diet and health study. Arch Intern Med 167(22):2461–2468. doi:10.1001/archinte.167.22.2461

    Article  Google Scholar 

  20. Huijbregts P, Feskens E, Räsänen L, Fidanza F, Nissinen A, Menotti A, Kromhout D (1997) Dietary pattern and 20 year mortality in elderly men in Finland, Italy, and the Netherlands: longitudinal cohort study. BMJ 315(7099):13–17. doi:10.1136/bmj.315.7099.13

    Article  CAS  Google Scholar 

  21. Mursu J, Steffen LM, Meyer KA, Duprez D, Jacobs DR Jr (2013) Diet quality indexes and mortality in postmenopausal women: the Iowa women’s health study. Am J Clin Nutr 98(2):444–453

    Article  CAS  Google Scholar 

  22. Shivappa N, Bosetti C, Zucchetto A, Montella M, Serraino D, LaVecchia C, Hebert JR (2014) Association between dietary inflammatory index and prostate cancer among Italian men. Br J Nutr 17:1–6

    Google Scholar 

  23. Shivappa N, Steck SE, Hurley TG, Hussey JR, Ma Y, Ockene IS, Tabung F, Hebert 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(8):1825–1833. doi:10.1017/S1368980013002565

    Article  Google Scholar 

  24. Wirth MD, Burch J, Shivappa N, Violanti JM, Burchfiel CM, Fekedulegn D, Andrew ME, Hartley TA, Miller DB, Mnatsakanova A, Charles LE, Steck SE, Hurley TG, Vena JE, Hebert JR (2014) Association of a dietary inflammatory index with inflammatory indices and metabolic syndrome among police officers. J Occup Environ Med 56(9):986–989. doi:10.1097/JOM.0000000000000213

    Article  Google Scholar 

  25. Shivappa N, Hebert 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(4):665–671. doi:10.1017/S000711451400395X

    Article  CAS  Google Scholar 

  26. Tabung FK, Steck SE, Zhang J, Ma Y, Liese AD, Agalliu I, Hingle M, Hou L, Hurley TG, Jiao L, Martin LW, Millen AE, Park HL, Rosal MC, Shikany JM, Shivappa N, Ockene JK, Hebert JR (2015) Construct validation of the dietary inflammatory index among postmenopausal women. Ann Epidemiol. doi:10.1016/j.annepidem.2015.03.009

    Google Scholar 

  27. Wood LG, Shivappa N, Berthon BS, Gibson PG, Hebert JR (2015) Dietary inflammatory index is related to asthma risk, lung function and systemic inflammation in asthma. Clin Exp Allergy 45(1):177–183. doi:10.1111/cea.12323

    Article  CAS  Google Scholar 

  28. Aa Alkerwi, Shivappa N, Crichton G, Hébert JR (2014) No significant independent relationships with cardiometabolic biomarkers were detected in the observation of cardiovascular risk factors in luxembourg study population. Nutr Res. doi:10.1016/j.nutres.2014.07.017

    Google Scholar 

  29. Wirth MD, Burch J, Shivappa N, Violanti JM, Burchfiel CM, Fekedulegn D, Andrew ME, Hartley TA, Miller DB, Mnatsakanova A, Charles LE, Steck SE, Hurley TG, Vena JE, Hebert JR (2014) Association of a dietary inflammatory index with inflammatory indices and metabolic syndrome among police officers. J Occup Environ Med 56(9):986–989

    Article  Google Scholar 

  30. Ruiz-Canela M, Zazpe I, Shivappa N, Hebert JR, Sanchez-Tainta A, Corella D, Salas-Salvado J, Fito M, Lamuela-Raventos RM, Rekondo J, Fernandez-Crehuet J, Fiol M, Santos-Lozano JM, Serra-Majem L, Pinto X, Martinez JA, Ros E, Estruch R, Martinez-Gonzalez MA (2015) Dietary inflammatory index and anthropometric measures of obesity in a population sample at high cardiovascular risk from the PREDIMED (PREvencion con DIeta MEDiterranea) trial. Br J Nutr. doi:10.1017/S0007114514004401

    Google Scholar 

  31. Maisonneuve P, Shivappa N, Hébert J, Bellomi M, Rampinelli C, Bertolotti R, Spaggiari L, Palli D, Veronesi G, Gnagnarella P (2015) Dietary inflammatory index and risk of lung cancer and other respiratory conditions among heavy smokers in the COSMOS screening study. Eur J Nutr. doi:10.1007/s00394-015-0920-3

    Google Scholar 

  32. Shivappa N, Hebert JR, Karamati M, Shariati-Bafghi SE, Rashidkhani B (2015) Increased inflammatory potential of diet is associated with bone mineral density among postmenopausal women in Iran. Eur J Nutr. doi:10.1007/s00394-015-0875-4

    Google Scholar 

  33. Zamora-Ros R, Shivappa N, Steck SE, Canzian F, Landi S, Alonso MH, Hebert JR, Moreno V (2015) Dietary inflammatory index and inflammatory gene interactions in relation to colorectal cancer risk in the Bellvitge colorectal cancer case–control study. Genes Nutr 10(1):447. doi:10.1007/s12263-014-0447-x

    Article  Google Scholar 

  34. Shivappa N, Zucchetto A, Montella M, Serraino D, Steck SE, La Vecchia C, Hebert JR (2015) Inflammatory potential of diet and risk of colorectal cancer: a case–control study from Italy. Br J Nutr 1–7. doi:10.1017/S0007114515001828

  35. 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: CCC 26(3):399–408. doi:10.1007/s10552-014-0515-y

    Article  Google Scholar 

  36. Wirth MD, Shivappa N, Steck SE, Hurley TG, Hébert 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. doi:10.1017/S000711451500104X

    Google Scholar 

  37. Shivappa N, Bosetti C, Zucchetto A, Serraino D, La Vecchia C, Hebert JR (2014) Dietary inflammatory index and risk of pancreatic cancer in an Italian case–control study. Br J Nutr. doi:10.1017/S0007114514003626

    Google Scholar 

  38. Shivappa N, Bosetti C, Zucchetto A, Montella M, Serraino D, La Vecchia C, Hebert JR (2014) Association between dietary inflammatory index and prostate cancer among Italian men. Br J Nutr. doi:10.1017/S0007114514003572

    Google Scholar 

  39. Folsom AR, Kaye SA, Prineas RJ, Potter JD, Gapstur SM, Wallace RB (1990) Increased incidence of carcinoma of the breast associated with abdominal adiposity in postmenopausal women. Am J Epidemiol 131(5):794–803

    CAS  Google Scholar 

  40. Willett WC, Sampson L, Browne ML, Stampfer MJ, Rosner B, Hennekens CH, Speizer FE (1988) The use of a self-administered questionnaire to assess diet four years in the past. Am J Epidemiol 127(1):188–199

    CAS  Google Scholar 

  41. Park K, Harnack L, Jacobs DR Jr (2009) Trends in dietary supplement use in a cohort of postmenopausal women from Iowa. Am J Epidemiol 169(7):887–892

    Article  Google Scholar 

  42. Hoevenaar-Blom MP, Nooyens AC, Kromhout D, Spijkerman AM, Beulens JW, van der Schouw YT, Bueno-de-Mesquita B, Verschuren WM (2012) Mediterranean style diet and 12-year incidence of cardiovascular diseases: the EPIC-NL cohort study. PLoS One 7(9):e45458. doi:10.1371/journal.pone.0045458

    Article  CAS  Google Scholar 

  43. Akbaraly TN, Ferrie JE, Berr C, Brunner EJ, Head J, Marmot MG, Singh-Manoux A, Ritchie K, Shipley MJ, Kivimaki M (2011) Alternative healthy eating index and mortality over 18 y of follow-up: results from the Whitehall II cohort. Am J Clin Nutr 94(1):247–253. doi:10.3945/ajcn.111.013128

    Article  CAS  Google Scholar 

  44. Kappeler R, Eichholzer M, Rohrmann S (2013) Meat consumption and diet quality and mortality in NHANES III. Eur J Clin Nutr 67(6):598–606. doi:10.1038/ejcn.2013.59

    Article  CAS  Google Scholar 

  45. McCullough ML, Gapstur SM, Shah R, Jacobs EJ, Campbell PT (2013) Association between red and processed meat intake and mortality among colorectal cancer survivors. J Clin Oncol 31(22):2773–2782. doi:10.1200/JCO.2013.49.1126

    Article  Google Scholar 

  46. Orlich MJ, Singh PN, Sabate J, Jaceldo-Siegl K, Fan J, Knutsen S, Beeson WL, Fraser GE (2013) Vegetarian dietary patterns and mortality in adventist health study 2. JAMA Intern Med 173(13):1230–1238. doi:10.1001/jamainternmed.2013.6473

    Article  CAS  Google Scholar 

  47. Folsom AR, Parker ED, Harnack LJ (2007) Degree of concordance with DASH diet guidelines and incidence of hypertension and fatal cardiovascular disease*. Am J Hypertens 20(3):225–232. doi:10.1016/j.amjhyper.2006.09.003

    Article  Google Scholar 

  48. 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 Biomarkers Prev 23(11):2383–2392. doi:10.1158/1055-9965.epi-14-0537

    Article  CAS  Google Scholar 

  49. Esmaillzadeh A, Kimiagar M, Mehrabi Y, Azadbakht L, Hu FB, Willett WC (2007) Dietary patterns and markers of systemic inflammation among Iranian women. J Nutr 137(4):992–998

    CAS  Google Scholar 

  50. Festa A, D’Agostino R, Howard G, Mykkänen L, Tracy RP, Haffner SM (2000) Chronic subclinical inflammation as part of the insulin resistance syndrome: the Insulin Resistance Atherosclerosis Study (IRAS). Circulation 102(1):42–47. doi:10.1161/01.cir.102.1.42

    Article  CAS  Google Scholar 

  51. Djiogue S, Nwabo Kamdje AH, Vecchio L, Kipanyula MJ, Farahna M, Aldebasi Y, Seke Etet PF (2013) Insulin resistance and cancer: the role of insulin and IGFs. Endocr Relat Cancer 20(1):R1–R17. doi:10.1530/erc-12-0324

    Article  CAS  Google Scholar 

  52. Pihlajamäki J, Gylling H, Miettinen TA, Laakso M (2004) Insulin resistance is associated with increased cholesterol synthesis and decreased cholesterol absorption in normoglycemic men. J Lipid Res 45(3):507–512. doi:10.1194/jlr.M300368-JLR200

    Article  Google Scholar 

  53. Bruce WR, Wolever TM, Giacca A (2000) Mechanisms linking diet and colorectal cancer: the possible role of insulin resistance. Nutr Cancer 37(1):19–26. doi:10.1207/S15327914NC3701_2

    Article  CAS  Google Scholar 

  54. Bruce WR, Giacca A, Medline A (2000) Possible mechanisms relating diet and risk of colon cancer. Cancer Epidemiol Biomarkers Prev 9(12):1271–1279

    CAS  Google Scholar 

  55. Bruce WR, Giacca A, Medline A (2000) Possible mechanisms relating diet and risk of colon cancer. Cancer Epidemiol Biomark Prev 9(12):1271–1279

    CAS  Google Scholar 

  56. De Caterina R, Zampolli A, Del Turco S, Madonna R, Massaro M (2006) Nutritional mechanisms that influence cardiovascular disease. Am J Clin Nutr 83(2):421S–426S

    Google Scholar 

  57. Thompson FE, Metzner HL, Lamphiear DE, Hawthorne VM (1990) Characteristics of individuals and long term reproducibility of dietary reports: the Tecumseh Diet Methodology Study. J Clin Epidemiol 43(11):1169–1178. doi:10.1016/0895-4356(90)90018-K

    Article  CAS  Google Scholar 

  58. Jensen OM, Wahrendorf J, Rosenqvist A, Geser A (1984) The reliability of questionnaire-derived historical dietary information and temporal stability of food habits in individuals. Am J Epidemiol 120(2):281–290

    CAS  Google Scholar 

  59. Lindsted KD, Kuzma JW (1989) Long-term (24-year) recall reliability in cancer cases and controls using a 21-item food frequency questionnaire. Nutr Cancer 12(2):135–149

    Article  CAS  Google Scholar 

  60. Jain M, Howe GR, Harrison L, Miller AB (1989) A study of repeatability of dietary data over a seven-year period. Am J Epidemiol 129(2):422–429

    CAS  Google Scholar 

  61. Thompson FE, Metzner HL, Lamphiear DE, Hawthorne VM (1990) Characteristics of individuals and long term reproducibility of dietary reports: the Tecumseh Diet Methodology Study. J Clin Epidemiol 43:1169–1178

    Article  CAS  Google Scholar 

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Acknowledgments

This study was supported by National Cancer Institute Grant R01 CA39742. Drs. N. Shivappa and J.R. Hebert were supported by Grant Number R44DK103377 from the United States National Institute of Diabetes and Digestive and Kidney Diseases. A.E. Prizment was supported by the National Center for Advancing Translational Sciences of the National Institutes of Health Award Number UL1TR000114. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

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Correspondence to Nitin Shivappa.

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Dr. James R. 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 in order to develop computer and smart phone applications for patient counseling and dietary intervention in clinical settings. Dr Nitin Shivappa is an employee of CHI.

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Shivappa, N., Blair, C.K., Prizment, A.E. et al. Association between inflammatory potential of diet and mortality in the Iowa Women’s Health study. Eur J Nutr 55, 1491–1502 (2016). https://doi.org/10.1007/s00394-015-0967-1

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