Skip to main content
Log in

Pro-inflammatory dietary pattern is associated with fractures in women: an eight-year longitudinal cohort study

  • Original Article
  • Published:
Osteoporosis International Aims and scope Submit manuscript

Abstract

Summary

In this study, during 8 years of follow-up, we reported that higher dietary inflammatory index values were associated with a higher risk of incident fractures in women, but not in men, after adjusting for potential confounders.

Introduction

Inflammation is a key risk factor for many adverse outcomes in older people. While diet is a potential source of inflammation, little is known about the impact of inflammatory diet on fractures. Thus, we investigated whether higher Dietary Inflammatory Index (DII)™ ® scores are associated with fractures in a cohort of North American people.

Methods

This longitudinal study with a follow-up of 8 years included 3648 participants (1577 males and 2071 females; mean age = 60.6 years) with/at risk of knee osteoarthritis participating with in the Osteoarthritis Initiative. DII scores were calculated using the validated Block Brief 2000 Food Frequency Questionnaire, categorized into sex-specific quintiles. Information on fractures was obtained through self-reported history of fractures at hip, spine, and forearm. The relationship between baseline DII score and incident fracture was assessed through a Cox’s regression analysis, adjusted for potential baseline confounders, and reported as hazard ratios (HRs).

Results

During 8 years of follow-up, 560 individuals developed fractures (15.4%). Adjusting for 10 potential confounders, women in the highest DII score quintile (i.e., most pro-inflammatory diet) had a significantly higher risk for fractures (HR = 1.46; 95% CI = 1.02–2.11) compared to women in the lowest quintile. An increase in one standard deviation of DII scores significantly predicted fracture onset in women (adjusted HR = 1.14; 95% CI = 1.02–1.27). The association between DII score and fractures was not significant among men or in the sample as whole.

Conclusion

Pro-inflammatory diet is associated with a higher incidence of fractures in women but not men.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  1. Johnell O, Kanis JA (2006) An estimate of the worldwide prevalence and disability associated with osteoporotic fractures. Osteoporosis Int 17:1726–1733

    Article  CAS  Google Scholar 

  2. Veronese N, Stubbs B, Crepaldi G, et al (2017) Relationship between low bone mineral density and fractures with incident cardiovascular disease: a systematic review and meta-analysis. J Bone Miner Res 32:1126–1135

  3. Iqbal MM (2000) Osteoporosis: epidemiology, diagnosis, and treatment. South Med J 93:2–18

    CAS  PubMed  Google Scholar 

  4. Lips P, van Schoor NM (2005) Quality of life in patients with osteoporosis. Osteoporosis Int 16:447–455

    Article  Google Scholar 

  5. Organization WH (1994) Assessment of fracture risk and its application to screening for postmenopausal osteoporosis. Report of a WHO Study Group. World Health Organ Tech Rep Ser 843:1–129

    Google Scholar 

  6. Nguyen TV, Sambrook PN, Eisman JA (1998) Bone loss, physical activity, and weight change in elderly women: the Dubbo Osteoporosis Epidemiology Study. J Bone Miner Res 13:1458–1467

    Article  CAS  PubMed  Google Scholar 

  7. Cawthon PM (2011) Gender differences in osteoporosis and fractures. Clin Orthop Relat Res 469:1900–1905

    Article  PubMed  PubMed Central  Google Scholar 

  8. Kanis JA, Johnell O, Oden A et al (2005) Smoking and fracture risk: a meta-analysis. Osteoporosis Int 16:155–162

    Article  CAS  Google Scholar 

  9. Kanis JA, Johansson H, Johnell O, Oden A, De Laet C, Eisman JA, Pols H, Tenenhouse A (2005) Alcohol intake as a risk factor for fracture. Osteoporosis Int 16:737–742

    Article  Google Scholar 

  10. De Laet C, Kanis JA, Oden A et al (2005) Body mass index as a predictor of fracture risk: a meta-analysis. Osteoporosis Int 16:1330–1338

    Article  Google Scholar 

  11. Solmi M, Veronese N, Correll CU, Favaro A, Santonastaso P, Caregaro L, Vancampfort D, Luchini C, De Hert M, Stubbs B (2016) Bone mineral density, osteoporosis, and fractures among people with eating disorders: a systematic review and meta-analysis. Acta psychiatrica Scandinavica 133:341–51

  12. Rizzoli R, Cooper C, Reginster JY et al (2012) Antidepressant medications and osteoporosis. Bone 51:606–613

    Article  CAS  PubMed  Google Scholar 

  13. Vestergaard P, Rejnmark L, Mosekilde L (2006) Anxiolytics, sedatives, antidepressants, neuroleptics and the risk of fracture. Osteoporosis Int 17:807–816

    Article  CAS  Google Scholar 

  14. Chung HY, Cesari M, Anton S, Marzetti E, Giovannini S, Seo AY, Carter C, BP Y, Leeuwenburgh C (2009) Molecular inflammation: underpinnings of aging and age-related diseases. Ageing Res Rev 8:18–30

    Article  CAS  PubMed  Google Scholar 

  15. Barbour KE, Lui LY, Ensrud KE, Hillier TA, LeBlanc ES, Ing SW, Hochberg MC, Cauley JA (2014) Inflammatory markers and risk of hip fracture in older white women: the study of osteoporotic fractures. J Bone Miner Res 29:2057–2064

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Eriksson AL, Movérare-Skrtic S, Ljunggren Ö, Karlsson M, Mellström D, Ohlsson C (2014) High-sensitivity CRP is an independent risk factor for all fractures and vertebral fractures in elderly men: The MrOS Sweden Study. J Bone Miner Res 29:418–423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Ishii S, Cauley JA, Greendale GA, Crandall CJ, Danielson ME, Ouchi Y, Karlamangla AS (2013) C-reactive protein, bone strength, and nine-year fracture risk: data from the Study of Women’s Health Across the Nation (SWAN)J Bone Miner Res 28:1688–1698

  18. Cauley JA, Barbour KE, Harrison SL, Cloonan YK, Danielson ME, Ensrud KE, Fink HA, Orwoll ES, Boudreau R (2016) Inflammatory markers and the risk of hip and vertebral fractures in men: the osteoporotic fractures in men (MrOS). J Bone Miner Res 31:2129–2138

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Ing SW, Orchard TS, Lu B, LaMonte MJ, Barbour KE, Cauley JA, Jackson RD (2015) TNF receptors predict hip fracture risk in the WHI study and fatty acid intake does not modify this association. J Clin Endocrinol Metab 100:3380–3387

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Barbour KE, Boudreau R, Danielson ME et al (2012) Inflammatory markers and the risk of hip fracture: the Women’s Health Initiative. J Bone Miner Res 27:1167–1176

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. 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 17:1689–1696

    Article  PubMed  Google Scholar 

  22. Tabung FK, Steck SE, Zhang J et al (2015) Construct validation of the dietary inflammatory index among postmenopausal women. Ann Epidemiol 25:398–405

    Article  PubMed  PubMed Central  Google Scholar 

  23. Orchard T, Yildiz V, Steck SE, et al (2016) Dietary Inflammatory Index, bone mineral density, and risk of fracture in postmenopausal women: results from the Women’s Health Initiative. J Bone Miner Res 32:1136–1146

  24. Zhang ZQ, Cao WT, Shivappa N, Hebert JR, Li BL, He J, Tang XY, Liang YY, Chen YM (2017) Association between diet inflammatory index and osteoporotic hip fracture in elderly Chinese population. J Am Med Dir Assoc 18:671–677

    Article  PubMed  Google Scholar 

  25. Eby GA, Eby KL (2006) Rapid recovery from major depression using magnesium treatment. Med Hypotheses 67:362–370

    Article  CAS  PubMed  Google Scholar 

  26. Block G, Hartman AM, Naughton D (1990) A reduced dietary questionnaire: development and validation. Epidemiology (Cambridge, Mass) 1:58–64

    Article  CAS  Google Scholar 

  27. 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 17:1825–1833

    Article  PubMed  Google Scholar 

  28. Wirth MD, Shivappa N, Davis L et al (2016) Construct validation of the Dietary Inflammatory Index among African Americans. J Nutr Health Aging:1–5

  29. Wirth MD, Burch J, Shivappa N et al (2014) Association of a Dietary Inflammatory Index with inflammatory indices and metabolic syndrome among police officers. J Occup Environ Med 56:986–989

    Article  PubMed  PubMed Central  Google Scholar 

  30. Ramallal R, Toledo E, Martinez-Gonzalez MA, Hernandez-Hernandez A, Garcia-Arellano A, Shivappa N, Hebert JR, Ruiz-Canela M (2015) Dietary Inflammatory Index and incidence of cardiovascular disease in the SUN cohort. PLoS One 10

  31. 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 113:665–671

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Willett WC, Howe GR, Kushi LH (1997) Adjustment for total energy intake in epidemiologic studies. Am J Clin Nutr 65:1220S–1228S discussion 1229S-1231S

    Article  CAS  PubMed  Google Scholar 

  33. Veronese N, Stubbs B, Solmi M, Noale M, Vaona A, Demurtas J, Maggi S (2017) Dietary magnesium intake and fracture risk: data from a large prospective study. Br J Nutr 117:1570–1576

    Article  CAS  PubMed  Google Scholar 

  34. Katz JN, Chang LC, Sangha O, Fossel AH, Bates DW (1996) Can comorbidity be measured by questionnaire rather than medical record review? Med Care 34:73–84

    Article  CAS  PubMed  Google Scholar 

  35. Washburn RA, McAuley E, Katula J, Mihalko SL, Boileau RA (1999) The physical activity scale for the elderly (PASE): evidence for validity. J Clin Epidemiol 52:643–651

    Article  CAS  PubMed  Google Scholar 

  36. Jonckheere AR (1954) A distribution-free k-sample test against ordered alternatives. Biometrika 41:133–145

    Article  Google Scholar 

  37. Miles J (2009) Tolerance and variance inflation factor. Statistics Reference Online, Wiley StatsRef

    Google Scholar 

  38. Fairweather D (2014) Sex differences in inflammation during atherosclerosis. Clinical medicine insights. Cardiology 8:49–59

    PubMed  Google Scholar 

  39. Dahl K, Ahmed LA, Joakimsen RM, Jorgensen L, Eggen AE, Eriksen EF, Bjornerem A (2015) High-sensitivity C-reactive protein is an independent risk factor for non-vertebral fractures in women and men: the Tromso Study. Bone 72:65–70

    Article  CAS  PubMed  Google Scholar 

  40. Pasco JA, Kotowicz MA, Henry MJ et al (2006) High-sensitivity C-reactive protein and fracture risk in elderly women. JAMA 296:1349–1355

    Article  Google Scholar 

  41. Ginaldi L, Di Benedetto MC, De Martinis M (2005) Osteoporosis, inflammation and ageing. Immun Ageing 2:14–14

    Article  PubMed  PubMed Central  Google Scholar 

  42. Manolagas SC, Jilka RL (1995) Bone marrow, cytokines, and bone remodeling. Emerging insights into the pathophysiology of osteoporosis. N Engl J Med 332:305–311

    Article  CAS  PubMed  Google Scholar 

  43. Hu FB (2002) Dietary pattern analysis: a new direction in nutritional epidemiology. Curr Opin Lipidol 13:3–9

  44. Fung TT, Feskanich D (2015) Dietary patterns and risk of hip fractures in postmenopausal women and men over 50 years. Osteoporos Int 26:1825–1830

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Haring B, Crandall CJ, Wu C et al (2016) Dietary patterns and fractures in postmenopausal women. In: JAMA internal medicine

    Google Scholar 

  46. Feart C, Lorrain S, Coupez VG, Samieri C, Letenneur L, Paineau D, Barberger-Gateau P (2013) Adherence to a Mediterranean diet and risk of fractures in French older persons. Osteoporos Int 24:3031–3041

    Article  CAS  PubMed  Google Scholar 

  47. Romero Pérez A, Rivas Velasco A (2014) Adherence to Mediterranean diet and bone health. Nutr Hosp 29:989–996

  48. Steven R (1995) Report assessing vertebral fractures. J Bone Miner Res 10:518–523

    Google Scholar 

Download references

Funding

The OAI is a public-private partnership comprised of five contracts (N01-AR-2-2258; N01-AR-2-2259; N01-AR-2-2260; N01-AR-2-2261; N01-AR-2-2262) funded by the National Institutes of Health, a branch of the Department of Health and Human Services, and conducted by the OAI Study Investigators. Private funding partners include Merck Research Laboratories; Novartis Pharmaceuticals Corporation, GlaxoSmithKline; and Pfizer, Inc. Private sector funding for the OAI is managed by the Foundation for the National Institutes of Health. This manuscript was prepared using an OAI public use data set and does not necessarily reflect the opinions or views of the OAI investigators, the NIH, or the private funding partners. NS and JRH were supported by the US National Institute for Diabetes, Digestive and Kidney Diseases (grant no. R44DK103377). The sponsors had no role in the design, methods, subject recruitment, data collection, analysis or preparation of this paper.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to N. Veronese.

Ethics declarations

Conflicts of interest

Dr. JRH 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. NS is an employee of CHI. Prof. Reginster received consulting fees or paid advisory boards from IBSA-GENEVRIER, MYLAN, Radius Health, PIERRE FABRE; lecture fees when speaking at the invitation of sponsor: IBSA-GENEVRIER, MYLAN, CNIEL, Dairy Research Council (DRC), and grant supports from IBSA-GENEVRIER, MYLAN, CNIEL, Radius Health.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Veronese, N., Stubbs, B., Koyanagi, A. et al. Pro-inflammatory dietary pattern is associated with fractures in women: an eight-year longitudinal cohort study. Osteoporos Int 29, 143–151 (2018). https://doi.org/10.1007/s00198-017-4251-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00198-017-4251-5

Keywords

Navigation