Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress 2023 EHA Congress 2023 ASCO Annual Meeting
Clinical Collections
Advances in Alzheimer’s

Keynote webinar | Spotlight on sleep in brain health

LIVE: Thursday 2nd May 2024, 18:00-19:30 (CEST)

Quality sleep is essential for health. But what happens to our brains when sleep patterns are disturbed? Join our experts to explore the interplay between sleep disruption and neurological diseases, and the questions that you need to be asking your patients to help you prevent the harmful effects of sleep deprivation.
ADVANCED SEARCH
Log in
Top
European Journal of Nutrition
Published in: European Journal of Nutrition 2/2017

01-03-2017 | Original Contribution

Inflammatory potential of diet and all-cause, cardiovascular, and cancer mortality in National Health and Nutrition Examination Survey III Study

Authors: Nitin Shivappa, Susan E. Steck, James R. Hussey, Yunsheng Ma, James R. Hebert

Published in: European Journal of Nutrition | Issue 2/2017

Login to get access

Abstract

Background

Various dietary components have been studied in relation to overall mortality; however, little is known about the relationship between the inflammatory potential of overall diet and mortality.

Materials and methods

We examined the association between the dietary inflammatory index (DII) and mortality in the National Health and Nutrition Examination Survey III follow-up study. The DII was computed from baseline dietary intake assessed using 24-h dietary recalls (1988–1994). Mortality was determined from the National Death Index records through 2006. Cox proportional hazards regression was used to estimate hazard ratios (HRs) and 95 % confidence interval (95 % CI). During the follow-up, 2795 deaths were identified, including 1233 due to cardiovascular disease (CVD), and 615 due to cancer, 158 of which were due to digestive-tract cancers.

Results

Multivariate Cox proportional hazards regression analyses, adjusting for age, race, diabetes status, hypertension, physical activity, body mass index, poverty index, and smoking, revealed positive associations between higher DII scores and mortality. Comparing subjects in DII tertile 3 versus tertile 1, significant associations were noted for all-cause mortality (HRTertile3vs1 1.34; 95 % CI 1.19–1.51, P trend < 0.0001), CVD mortality (HRTertile3vs1 1.46; 95 % CI 1.18–1.81, P trend = 0.0006), cancer mortality (HRTertile3vs1 1.46; 95 % CI 1.10–1.96, P trend = 0.01), and digestive-tract cancer mortality (HRTertile3vs1 2.10; 95 % CI 1.15–3.84, P trend = 0.03).

Conclusion

These results indicate that a pro-inflammatory diet, as indicated by higher DII scores, was associated with higher risk of all-cause, CVD, and cancer mortality.
Literature
1.
Keibel A, Singh V, Sharma MC (2009) Inflammation, microenvironment, and the immune system in cancer progression. Curr Pharm Des 15(17):1949–1955CrossRef
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):4467–4477CrossRef
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) CrossRef
4.
Warnberg J, Gomez-Martinez S, Romeo J, Diaz LE, Marcos A (2009) Nutrition, inflammation, and cognitive function. Ann N Y Acad Sci 1153:164–175CrossRef
5.
Chung Y-C, Chang Y-F (2003) Serum interleukin-6 levels reflect the disease status of colorectal cancer. J Surg Oncol 83(4):222–226CrossRef
6.
Terzic J, Grivennikov S, Karin E, Karin M (2010) Inflammation and colon cancer. Gastroenterology 138(6):2101–2114CrossRef
7.
Toriola AT, Cheng TY, Neuhouser ML, Wener MH, Zheng Y, Brown E, Miller JW, Song X, Beresford SA, Gunter MJ, Caudill MA, Ulrich CM (2013) Biomarkers of inflammation are associated with colorectal cancer risk in women but are not suitable as early detection markers. Int J Cancer 132(11):2648–2658. doi:10.​1002/​ijc.​27942 CrossRef
8.
World Health Organization (2008) The global burden of disease: 2004 update. WHO, Geneva
9.
Calabro P, Golia E, Yeh ET (2009) CRP and the risk of atherosclerotic events. Semin Immunopathol 31(1):79–94CrossRef
10.
Lloyd-Jones D, Adams R, Carnethon M, De Simone G, Ferguson TB, Flegal K, Ford E, Furie K, Go A, Greenlund K, Haase N, Hailpern S, Ho M, Howard V, Kissela B, Kittner S, Lackland D, Lisabeth L, Marelli A, McDermott M, Meigs J, Mozaffarian D, Nichol G, O’Donnell C, Roger V, Rosamond W, Sacco R, Sorlie P, Stafford R, Steinberger J, Thom T, Wasserthiel-Smoller S, Wong N, Wylie-Rosett J, Hong Y (2009) Heart disease and stroke statistics–2009 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation 119(3):480–486CrossRef
11.
de Mello VD, Schwab U, Kolehmainen M, Koenig W, Siloaho M, Poutanen K, Mykkanen H, Uusitupa M (2011) A diet high in fatty fish, bilberries and wholegrain products improves markers of endothelial function and inflammation in individuals with impaired glucose metabolism in a randomised controlled trial: the Sysdimet study. Diabetologia 54(11):2755–2767CrossRef
12.
Khoo J, Piantadosi C, Duncan R, Worthley SG, Jenkins A, Noakes M, Worthley MI, Lange K, Wittert GA (2011) Comparing effects of a low-energy diet and a high-protein low-fat diet on sexual and endothelial function, urinary tract symptoms, and inflammation in obese diabetic men. J Sex Med 8(10):2868–2875CrossRef
13.
Luciano M, Mottus R, Starr JM, McNeill G, Jia X, Craig LC, Deary IJ (2012) Depressive symptoms and diet: their effects on prospective inflammation levels in the elderly. Brain Behav Immun 26(5):717–720CrossRef
14.
Chang AR, Lazo M, Appel LJ, Gutierrez OM, Grams ME (2014) High dietary phosphorus intake is associated with all-cause mortality: results from NHANES III. Am J Clin Nutr 99(2):320–327. doi:10.​3945/​ajcn.​113.​073148 CrossRef
15.
16.
Cohen HW, Hailpern SM, Alderman MH (2008) Sodium intake and mortality follow-up in the Third National Health and Nutrition Examination Survey (NHANES III). J Gen Intern Med 23(9):1297–1302. doi:10.​1007/​s11606-008-0645-6 CrossRef
17.
Deng X, Song Y, Manson JE, Signorello LB, Zhang SM, Shrubsole MJ, Ness RM, Seidner DL, Dai Q (2013) Magnesium, vitamin D status and mortality: results from US National Health and Nutrition Examination Survey (NHANES) 2001 to 2006 and NHANES III. BMC Med 11:187. doi:10.​1186/​1741-7015-11-187 CrossRef
18.
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. doi:10.​1017/​S136898001300211​5 CrossRef
19.
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/​S136898001300256​5 CrossRef
20.
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):986–989CrossRef
21.
Wood L, Shivappa N, Berthon BS, Gibson PG, Hebert JR (2014) Dietary inflammatory index is related to asthma risk, lung function and systemic inflammation in asthma. Clin Exp Allergy. doi:10.​1111/​cea.​12323
22.
Shivappa N, Hebert JR, Rietzschel ER, De Buyzere ML, Langlois M, Debruyne E et al (2015) Associations between dietary inflammatory index and inflammatory markers in the Asklepios Study. Br J Nutr 113(4):665–671. PubMed PMID: 25639781. Pubmed Central PMCID: 4355619
23.
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 25(6):398–405. doi:10.​1016/​j.​annepidem.​2015.​03.​009 CrossRef
24.
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
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/​S000711451400395​X CrossRef
26.
27.
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 CrossRef
28.
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 CrossRef
29.
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 CrossRef
30.
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 FirstView. doi:10.​1017/​S000711451500104​X
31.
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/​S000711451400357​2
32.
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/​S000711451400362​6
33.
Shivappa N, Hebert JR, Polesel J, Zucchetto A, Crispo A, Montella M, Franceschi S, Rossi M, La Vecchia C, Serraino D (2015) Inflammatory potential of diet and risk for hepatocellular cancer in a case-control study from Italy. Br J Nutr. doi:10.​1017/​S000711451500441​9
34.
Shivappa N, Hébert JR, Zucchetto A, Montella M, Serraino D, La Vecchia C, Rossi M (2015) Dietary inflammatory index and endometrial cancer risk in an Italian case–control study. Br J Nutr FirstView. doi:10.​1017/​S000711451500417​1
35.
Shivappa N, Zucchetto A, Serraino D, Rossi M, La Vecchia C, Hebert JR (2015) Dietary inflammatory index and risk of esophageal squamous cell cancer in a case-control study from Italy. Cancer Causes Control CCC 26(10):1439–1447. doi:10.​1007/​s10552-015-0636-y CrossRef
36.
Shivappa N, Blair C, Prizment A, Jacobs D Jr, Steck S, Hébert J (2015) Association between inflammatory potential of diet and mortality in the Iowa Women’s Health study. Eur J Nutr. doi:10.​1007/​s00394-015-0967-1
37.
Shivappa N, Harris H, Wolk A, Hebert JR (2015) Association between inflammatory potential of diet and mortality among women in the Swedish Mammography Cohort. Eur J Nutr. doi:10.​1007/​s00394-015-1005-z
38.
Plan and operation of the Third National Health and Nutrition Examination Survey, 1988–94. Series 1: programs and collection procedures (1994). Vital Health Stat 1(32):1–407
39.
Erlinger TP, Platz EA, Rifai N, Helzlsouer KJ (2004) C-reactive protein and the risk of incident colorectal cancer.[see comment]. JAMA 291(5):585–590CrossRef
40.
Gunter MJ, Stolzenberg-Solomon R, Cross AJ, Leitzmann MF, Weinstein S, Wood RJ, Virtamo J, Taylor PR, Albanes D, Sinha R (2006) A prospective study of serum C-reactive protein and colorectal cancer risk in men. Cancer Res 66(4):2483–2487CrossRef
41.
Otani T, Iwasaki M, Sasazuki S, Inoue M, Tsugane S, Japan Public Health Center-Based Prospective Study G (2006) Plasma C-reactive protein and risk of colorectal cancer in a nested case-control study: Japan Public Health Center-based prospective study. Cancer Epidemiol Biomarkers Prev 15(4):690–695CrossRef
42.
Nikiteas NI, Tzanakis N, Gazouli M, Rallis G, Daniilidis K, Theodoropoulos G, Kostakis A, Peros G (2005) Serum IL-6, TNFalpha and CRP levels in Greek colorectal cancer patients: prognostic implications. World J Gastroenterol 11(11):1639–1643CrossRef
43.
Kennedy ET, Ohls J, Carlson S, Fleming K (1995) The healthy eating index: design and applications. J Am Diet Assoc 95(10):1103–1108CrossRef
44.
Miller PE, Lazarus P, Lesko SM, Muscat JE, Harper G, Cross AJ, Sinha R, Ryczak K, Escobar G, Mauger DT, Hartman TJ (2010) Diet index-based and empirically derived dietary patterns are associated with colorectal cancer risk. J Nutr 140(7):1267–1273. doi:10.​3945/​jn.​110.​121780 CrossRef
45.
Panagiotakos DB, Pitsavos C, Stefanadis C (2006) Dietary patterns: a Mediterranean diet score and its relation to clinical and biological markers of cardiovascular disease risk. Nutr Metab Cardiovasc Dis 16(8):559–568CrossRef
46.
Mitrou PN, Kipnis V, Thiebaut AC, Reedy J, Subar AF, Wirfalt E, Flood A, Mouw T, Hollenbeck AR, Leitzmann MF, Schatzkin A (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 CrossRef
47.
48.
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 CrossRef
49.
Reedy J, Krebs-Smith SM, Miller PE, Liese AD, Kahle LL, Park Y, Subar AF (2014) Higher diet quality is associated with decreased risk of all-cause, cardiovascular disease, and cancer mortality among older adults. J Nutr. doi:10.​3945/​jn.​113.​189407
50.
51.
Li K, Kaaks R, Linseisen J, Rohrmann S (2011) Dietary calcium and magnesium intake in relation to cancer incidence and mortality in a German prospective cohort (EPIC-Heidelberg). Cancer Causes Control 22(10):1375–1382CrossRef
52.
Pocobelli G, Peters U, Kristal AR, White E (2009) Use of supplements of multivitamins, vitamin C, and vitamin E in relation to mortality. Am J Epidemiol 170(4):472–483CrossRef
53.
Cavicchia PP, Steck SE, Hurley TG, Hussey JR, Ma Y, Ockene IS, Hébert JR (2009) A new dietary inflammatory index predicts interval changes in high-sensitivity c-reactive protein. J Nutr 139(12):2365–2372CrossRef
54.
Shivappa N, Steck SE, Hurley TG, Hussey JR, Ma Y, Ockene IS, Tabung F, Hebert JR (2013) A population-based dietary inflammatory index predicts levels of C-reactive protein in the Seasonal Variation of Blood Cholesterol Study (SEASONS). Public Health Nutr 10:1–9
55.
Hebert JR (1985) Relationship of vegetarianism to child growth in South India. Am J Clin Nutr 42(6):1246–1254
56.
Hebert JR (1985) Effects of water quality and water quantity on nutritional status: findings from a south Indian community. Bull World Health Organ 63(1):145–155
57.
Hebert JR (1984) Water quality and water quantity and wasting in south India. Trop Geogr Med 36(4):375–381
58.
Hebert JR, Toporoff E (1989) Dietary exposures and other factors of possible prognostic-significance in relation to tumor size and nodal involvement in early-stage breast-cancer. Int J Epidemiol 18(3):518–526. doi:10.​1093/​Ije/​18.​3.​518 CrossRef
59.
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
60.
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 CrossRef
61.
62.
Bruce WR, Giacca A, Medline A (2000) Possible mechanisms relating diet and risk of colon cancer. Cancer Epidemiol Biomarkers Prev 9(12):1271–1279
63.
64.
65.
66.
Hebert JR, Gupta PC, Mehta H, Ebbeling CB, Bhonsle RR, Varghese F (2000) Sources of variability in dietary intake in two distinct regions of rural India: implications for nutrition study design and interpretation. Eur J Clin Nutr 54(6):479–486CrossRef
67.
Hebert JR, Hurley TG, Steck SE, Miller DR, Tabung FK, Peterson KE, Kushi LH, Frongillo EA (2014) Considering the value of dietary assessment data in informing nutrition-related health policy. Adv Nutr 5(4):447–455. doi:10.​3945/​an.​114.​006189 CrossRef
68.
Copeland KT, Checkoway H, McMichael AJ, Holbrook RH (1977) Bias due to misclassification in the estimation of relative risk. Am J Epidemiol 105(5):488–495CrossRef
69.
Freedman LS, Schatzkin A, Midthune D, Kipnis V (2011) Dealing with dietary measurement error in nutritional cohort studies. J Natl Cancer Inst 103(14):1086–1092CrossRef
70.
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):422–429CrossRef
71.
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):281–290CrossRef
72.
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):135–149CrossRef
73.
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):444–453CrossRef
74.
Sijtsma FP, Meyer KA, Steffen LM, Shikany JM, Van Horn L, Harnack L, Kromhout D, Jacobs DR Jr (2012) Longitudinal trends in diet and effects of sex, race, and education on dietary quality score change: the Coronary Artery Risk Development in Young Adults study. Am J Clin Nutr 95(3):580–586CrossRef
75.
Metadata
Title
Inflammatory potential of diet and all-cause, cardiovascular, and cancer mortality in National Health and Nutrition Examination Survey III Study
Authors
Nitin Shivappa
Susan E. Steck
James R. Hussey
Yunsheng Ma
James R. Hebert
Publication date
01-03-2017
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Nutrition / Issue 2/2017
Print ISSN: 1436-6207
Electronic ISSN: 1436-6215
DOI
https://doi.org/10.1007/s00394-015-1112-x

Other articles of this Issue 2/2017

European Journal of Nutrition 2/2017 Go to the issue

Original Contribution

Effect of olive oil phenolic compounds on the expression of blood pressure-related genes in healthy individuals

Original Contribution

Effects of proanthocyanidin on oxidative stress biomarkers and adipokines in army cadets: a placebo-controlled, double-blind study

Original Contribution

The effect of three different ad libitum diets for weight loss maintenance: a randomized 18-month trial

Original Contribution

Taurine supplementation regulates Iκ-Bα protein expression in adipose tissue and serum IL-4 and TNF-α concentrations in MSG obesity

Original Contribution

Intakes of whole grain in an Italian sample of children, adolescents and adults

Original Contribution

The synergistic effect between the Mediterranean diet and GSTP1 or NAT2 SNPs decreases breast cancer risk in Greek-Cypriot women

ACC 2024 Congress Coverage

Cardiology Video

Highlights from the ACC 2024 Congress

Watch now

Watch official videos from the ACC congress summarizing key highlights from the last year in heart failure, cardiomyopathies, valvular disease, pulmonary vascular disease, and pediatric cardiology.

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

16-04-2024 Type 2 Diabetes News

Incentivised to exercise

11-04-2024 Lifestyle Modifications News

New intervention for STEMI-related cardiogenic shock

10-04-2024 Myocardial Infarction News

» View more highlights on the ACC 2024 congress hub page

Image Credits