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Increased inflammatory potential of diet is associated with bone mineral density among postmenopausal women in Iran

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Abstract

Purpose

Diet has been shown to be associated with bone mineral density (BMD); however, the inflammatory potential of diet in modulating BMD has not yet been studied.

Methods

We examined the association between a newly developed dietary inflammatory index (DII) and BMD in a sample of postmenopausal Iranian women. In this cross-sectional study, 160 postmenopausal women aged 50–85 years were studied and their femoral neck and lumbar spine BMDs were measured by dual-energy X-ray absorptiometry. The DII was computed based on dietary intake assessed using a previously validated, 168-item semiquantitative food frequency questionnaire. Logistic and linear regression models were fit to derive beta estimates and odds ratios (ORs), with DII fit as continuous and as a dichotomous variable.

Results

After adjusting for potential confounders, women with higher DII scores were more likely to have BMD below the median in the lumbar spine with the DII being used as both a continuous variable [ORcontinuous 1.64, 95 % confidence interval (CI) 1.11–2.43, p value = 0.01; one-unit increase corresponding to ≈17 % of its range in the current study] and a categorical variable (ORDII>−0.06/≤ 2.30, 95 % CI 1.05–5.07, p value = 0.04). Similar associations were observed when lumbar spine BMD was used as a continuous outcome. No significant association was observed with BMD in femoral neck, although the direction was along expected lines.

Conclusion

These data suggest a pro-inflammatory diet, as indicated by increasing DII score, may be a risk factor for lower BMD in lumbar spine in postmenopausal Iranian women.

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References

  1. Holroyd C, Cooper C, Dennison E (2008) Epidemiology of osteoporosis. Best Pract Res Clin Endocrinol Metabol 22(5):671–685. doi:10.1016/j.beem.2008.06.001

    Article  Google Scholar 

  2. Jamshidian Tehrani M, Kalantari N, Azadbakht L, Rajaie A, Hooshiar-rad A, Golestan B, Kamali Z (2003) The prevalence of osteoporosis among women aged 40–60 in Tehran. Iran J Endocrinol Metabol 5(4):271–276

    Google Scholar 

  3. Abolhassani F, Mohammadi M, Soltani A (2004) Burden of osteoporosis in Iran. Iran J Public Health, 18–28

  4. Irani AD, Poorolajal J, Khalilian A, Esmailnasab N, Cheraghi Z (2013) Prevalence of osteoporosis in Iran: a meta-analysis. J Res Med Sci Off J Isfahan Univ Med Sci 18(9):759–766

    Google Scholar 

  5. Cooper C, Campion G, Melton LJ III (1992) Hip fractures in the elderly: a world-wide projection. Osteoporos Int 2(6):285–289. doi:10.1007/BF01623184

    Article  CAS  Google Scholar 

  6. McGuigan FEA, Murray L, Gallagher A, Davey-Smith G, Neville CE, Van’t Hof R, Boreham C, Ralston SH (2002) Genetic and environmental determinants of peak bone mass in young men and women. J Bone Miner Res 17(7):1273–1279. doi:10.1359/jbmr.2002.17.7.1273

    Article  CAS  Google Scholar 

  7. Nih Consensus Development Panel on Osteoporosis Prevention D, Therapy (2001) Osteoporosis prevention, diagnosis, and therapy. JAMA 285(6):785–795

    Article  Google Scholar 

  8. Apalset EM, Gjesdal CG, Ueland PM, Midttun Ø, Ulvik A, Eide GE, Meyer K, Tell GS (2014) Interferon (IFN)-γ-mediated inflammation and the kynurenine pathway in relation to bone mineral density: the Hordaland Health Study. Clin Exp Immunol 176(3):452–460. doi:10.1111/cei.12288

    Article  CAS  Google Scholar 

  9. 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 

  10. 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 

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

    Article  CAS  Google Scholar 

  12. Philip M, Rowley DA, Schreiber H (2004) Inflammation as a tumor promoter in cancer induction. Semin Cancer Biol 14(6):433–439

    Article  CAS  Google Scholar 

  13. Utsal L, Tillmann V, Zilmer M, Mäestu J, Purge P, Saar M, Lätt E, Jürimäe T, Maasalu K, Jürimäe J (2014) Serum interferon gamma concentration is associated with bone mineral density in overweight boys. J Endocrinol Invest 37(2):175–180. doi:10.1007/s40618-013-0029-6

    Article  CAS  Google Scholar 

  14. Öztürk ZA, Yesil Y, Kuyumcu ME, Bilici M, Öztürk N, Yeşil NK, Özkaya M, Kısacık B, Kepekçi Y, Arıoğul S (2013) Inverse relationship between neutrophil lymphocyte ratio (NLR) and bone mineral density (BMD) in elderly people. Arch Gerontol Geriatr 57(1):81–85. doi:10.1016/j.archger.2013.02.005

    Article  Google Scholar 

  15. 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  Google Scholar 

  16. 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  Google Scholar 

  17. 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 

  18. Wood L, 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

    Article  Google Scholar 

  19. Shivappa N, Hebert JR, Rietzschel ER, De Buyzere ML, Langlois M, Debruyne E, Huybrecht I (2015) Associations between dietary inflammatory index and inflammatory markers in Asklepios study. Br J Nutr 113:665–671. doi:10.1017/S000711451400395X

    Article  CAS  Google Scholar 

  20. 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 34(12):1058–1065. doi:10.1016/j.nutres.2014.07.017

    Article  Google Scholar 

  21. 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 27:1–12

    Google Scholar 

  22. Wirth MD, Burch J, Shivappa N, Steck SE, Hurley TG, Vena JE, Hebert JR (2014) Dietary inflammatory index scores differ by shift work status: NHANES 2005 to 2010. J Occup Environ Med 56(2):145–148. doi:10.1097/JOM.0000000000000088

    Article  Google Scholar 

  23. Shivappa N, Prizment AE, Blair CK, Jacobs DR Jr, Steck SE, Hebert JR (2014) Dietary inflammatory index (DII) and risk of colorectal cancer in Iowa Women’s Health Study. Cancer Epidemiol Biomarkers Prev 23(11):2383–2392

    Article  CAS  Google Scholar 

  24. Zamora-Ros R, Shivappa N, Steck S, Canzian F, Landi S, Alonso MH, Hébert J, Moreno V (2014) 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):1–9. doi:10.1007/s12263-014-0447-x

    Google Scholar 

  25. Tabung F, Steck S, Ma Y, Liese A, Zhang J, Caan B, Hou L, Johnson K, Mossavar-Rahmani Y, Shivappa N, Wactawski-Wende J, Ockene J, Hebert J (2014) The association between dietary inflammatory index and risk of colorectal cancer among postmenopausal women: results from the Women’s Health Initiative. Cancer Causes Control  26:399–408. doi:10.1007/s10552-014-0515-y

    Google Scholar 

  26. Shivappa N, Bosetti C, Zucchetto A, Montella M, Serraino D, LaVecchia C, Hebert JR (2015) Association between dietary inflammatory index and prostate cancer among Italian men. Br J Nutr 113:278–283. doi:10.1017/S0007114514003572

    Article  CAS  Google Scholar 

  27. Shivappa N, Bosetti C, Zucchetto A, Serraino D, LaVecchia C, Hebert JR (2014) Dietary inflammatory index and risk of pancreatic cancer in an Italian case–control study. Br J Nutr 113:292–298. doi:10.1017/S0007114514003626

    Article  Google Scholar 

  28. Karamati M, Jessri M, Shariati-Bafghi S-E, Rashidkhani B (2012) Dietary patterns in relation to bone mineral density among menopausal Iranian women. Calcif Tissue Int 91(1):40–49. doi:10.1007/s00223-012-9608-3

    Article  CAS  Google Scholar 

  29. Esfahani FH, Asghari G, Mirmiran P, Azizi F (2010) Reproducibility and relative validity of food group intake in a food frequency questionnaire developed for the Tehran Lipid and Glucose Study. J Epidemiol 20(2):150–158

    Article  Google Scholar 

  30. 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):2365–2372

    Article  CAS  Google Scholar 

  31. Karamati M, Yousefian-Sanni M, Shariati-Bafghi S-E, Rashidkhani B (2014) Major nutrient patterns and bone mineral density among postmenopausal Iranian women. Calcif Tissue Int 94(6):648–658. doi:10.1007/s00223-014-9848-5

    Article  CAS  Google Scholar 

  32. Kwon YM, Kim GW, Yim HW, Paek YJ, Lee KS (2014) Association between dietary fat intake and bone mineral density in Korean adults: data from Korea National Health and Nutrition Examination Survey IV (2008–2009). Osteoporos Int. doi:10.1007/s00198-014-2977-x

    Google Scholar 

  33. Shin S, Hong K, Kang SW, Joung H (2013) A milk and cereal dietary pattern is associated with a reduced likelihood of having a low bone mineral density of the lumbar spine in Korean adolescents. Nutr Res 33(1):59–66. doi:10.1016/j.nutres.2012.11.003

    Article  CAS  Google Scholar 

  34. Sommer I, Erkkila AT, Jarvinen R, Mursu J, Sirola J, Jurvelin JS, Kroger H, Tuppurainen M (2013) Alcohol consumption and bone mineral density in elderly women. Public Health Nutr 16(4):704–712. doi:10.1017/S136898001200331X

    Article  Google Scholar 

  35. Takayanagi H (2007) Osteoimmunology: shared mechanisms and crosstalk between the immune and bone systems. Nat Rev Immunol 7(4):292–304. http://www.nature.com/nri/journal/v7/n4/suppinfo/nri2062_S1.html

  36. 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 

  37. Lorenzo J, Horowitz M, Choi Y (2008) Osteoimmunology: interactions of the bone and immune system. Endocr Rev 29(4):403–440. doi:10.1210/er.2007-0038

    Article  CAS  Google Scholar 

  38. Hebert JR, Clemow L, Pbert L, Ockene IS, Ockene JK (1995) Social desirability bias in dietary self-report may compromise the validity of dietary intake measures. Int J Epidemiol 24(2):389–398

    Article  CAS  Google Scholar 

  39. Hebert JR, Ma Y, Clemow L, Ockene IS, Saperia G, Stanek EJ 3rd, Merriam PA, Ockene JK (1997) Gender differences in social desirability and social approval bias in dietary self-report. Am J Epidemiol 146(12):1046–1055

    Article  CAS  Google Scholar 

  40. Hebert JR, Ebbeling CB, Matthews CE, Hurley TG, Ma Y, Druker S, Clemow L (2002) Systematic errors in middle-aged women’s estimates of energy intake: comparing three self-report measures to total energy expenditure from doubly labeled water. Ann Epidemiol 12(8):577–586

    Article  Google Scholar 

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Acknowledgments

We are grateful to all field investigators, staffs, and participants of the present study. This study was supported by a grant from National Nutrition and Food Technology Research Institute, Shahid Beheshti University of Medical Sciences, Tehran, Iran. Dr. Hébert was supported by an Established Investigator Award in Cancer Prevention and Control from the Cancer Training Branch of the National Cancer Institute (K05 CA136975). 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 DII from the University of South Carolina in order to develop computer and smart phone applications for patient counselling and dietary intervention in clinical settings. Dr Nitin Shivappa is an employee of CHI. The subject matter of this paper will not have any direct bearing on the work of CHI, nor has that activity exerted any influence on this project.

Conflict of interest

The authors declare no conflict of interest.

Author information

Authors and Affiliations

  1. Cancer Prevention and Control Program, University of South Carolina, Columbia, SC, 29208, USA

    Nitin Shivappa & James R. Hébert

  2. Department of Epidemiology and Biostatistics, Arnold School of Public Health, University of South Carolina, Columbia, SC, 29208, USA

    Nitin Shivappa & James R. Hébert

  3. Department of Nutrition Sciences, Varastegan Institute for Medical Sciences, Mashhad, Iran

    Mohsen Karamati & Seyedeh-Elaheh Shariati-Bafghi

  4. Community Nutrition Department, Faculty of Nutrition Sciences and Food Technology, National Nutrition and Food Technology Research Institute (WHO Collaborating Center), Shahid Beheshti University of Medical Sciences, Tehran, Iran

    Bahram Rashidkhani

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  1. Nitin Shivappa
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Correspondence to Bahram Rashidkhani.

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Shivappa, N., Hébert, J.R., Karamati, M. et al. Increased inflammatory potential of diet is associated with bone mineral density among postmenopausal women in Iran. Eur J Nutr 55, 561–568 (2016). https://doi.org/10.1007/s00394-015-0875-4

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  • DOI: https://doi.org/10.1007/s00394-015-0875-4

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