Skip to main content
Top
Published in: European Journal of Nutrition 2/2016

01-03-2016 | Original Contribution

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

Authors: Nitin Shivappa, James R. Hébert, Mohsen Karamati, Seyedeh-Elaheh Shariati-Bafghi, Bahram Rashidkhani

Published in: European Journal of Nutrition | Issue 2/2016

Login to get access

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.
Appendix
Available only for authorised users
Literature
2.
go back to reference 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 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
3.
go back to reference Abolhassani F, Mohammadi M, Soltani A (2004) Burden of osteoporosis in Iran. Iran J Public Health, 18–28 Abolhassani F, Mohammadi M, Soltani A (2004) Burden of osteoporosis in Iran. Iran J Public Health, 18–28
4.
go back to reference 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 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
6.
go back to reference 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 CrossRef 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 CrossRef
7.
go back to reference Nih Consensus Development Panel on Osteoporosis Prevention D, Therapy (2001) Osteoporosis prevention, diagnosis, and therapy. JAMA 285(6):785–795CrossRef Nih Consensus Development Panel on Osteoporosis Prevention D, Therapy (2001) Osteoporosis prevention, diagnosis, and therapy. JAMA 285(6):785–795CrossRef
8.
go back to reference 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 CrossRef 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 CrossRef
9.
go back to reference Keibel A, Singh V, Sharma MC (2009) Inflammation, microenvironment, and the immune system in cancer progression. Curr Pharm Des 15(17):1949–1955CrossRef Keibel A, Singh V, Sharma MC (2009) Inflammation, microenvironment, and the immune system in cancer progression. Curr Pharm Des 15(17):1949–1955CrossRef
10.
go back to reference 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 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
11.
go back to reference Coussens LM, Werb Z (2002) Inflammation and cancer. Nature 420(6917):860–867CrossRef Coussens LM, Werb Z (2002) Inflammation and cancer. Nature 420(6917):860–867CrossRef
12.
go back to reference Philip M, Rowley DA, Schreiber H (2004) Inflammation as a tumor promoter in cancer induction. Semin Cancer Biol 14(6):433–439CrossRef Philip M, Rowley DA, Schreiber H (2004) Inflammation as a tumor promoter in cancer induction. Semin Cancer Biol 14(6):433–439CrossRef
13.
go back to reference 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 CrossRef 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 CrossRef
14.
go back to reference 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 CrossRef 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 CrossRef
15.
go back to reference 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 17:1689–1696CrossRef 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 17:1689–1696CrossRef
16.
go back to reference 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 17:1825–1833CrossRef 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 17:1825–1833CrossRef
17.
go back to reference 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 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
18.
go back to reference 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):177–183CrossRef 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):177–183CrossRef
19.
go back to reference 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 CrossRef 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/​S000711451400395​X CrossRef
20.
go back to reference 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 CrossRef 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 CrossRef
21.
go back to reference 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 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
22.
23.
go back to reference 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):2383–2392CrossRef 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):2383–2392CrossRef
24.
go back to reference 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 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
25.
go back to reference 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 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
26.
go back to reference 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 CrossRef 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/​S000711451400357​2 CrossRef
27.
go back to reference 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 CrossRef 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/​S000711451400362​6 CrossRef
28.
go back to reference 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 CrossRef 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 CrossRef
29.
go back to reference 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):150–158CrossRef 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):150–158CrossRef
30.
go back to reference 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 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
31.
go back to reference 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 CrossRef 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 CrossRef
32.
go back to reference 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 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
33.
go back to reference 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 CrossRef 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 CrossRef
34.
go back to reference 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 CrossRef 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/​S136898001200331​X CrossRef
36.
go back to reference 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 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
38.
go back to reference 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):389–398CrossRef 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):389–398CrossRef
39.
go back to reference 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):1046–1055CrossRef 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):1046–1055CrossRef
40.
go back to reference 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):577–586CrossRef 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):577–586CrossRef
Metadata
Title
Increased inflammatory potential of diet is associated with bone mineral density among postmenopausal women in Iran
Authors
Nitin Shivappa
James R. Hébert
Mohsen Karamati
Seyedeh-Elaheh Shariati-Bafghi
Bahram Rashidkhani
Publication date
01-03-2016
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Nutrition / Issue 2/2016
Print ISSN: 1436-6207
Electronic ISSN: 1436-6215
DOI
https://doi.org/10.1007/s00394-015-0875-4

Other articles of this Issue 2/2016

European Journal of Nutrition 2/2016 Go to the issue