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Published in: Osteoporosis International 8/2019

01-08-2019 | Biomarkers | Original Article

Dietary inflammatory index® and cortical bone outcomes in healthy adolescent children

Authors: L. M. Coheley, N. Shivappa, J. R. Hebert, R. D. Lewis

Published in: Osteoporosis International | Issue 8/2019

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Abstract

Summary

Diet is thought to modulate inflammation. This study shows no relationships between the dietary inflammatory index (DII) and biomarkers of inflammation or bone after adjusting for covariates. Monocyte chemoattractant protein-1 was inversely associated with peripheral tibia cortical thickness and prospective childhood studies should be conducted to better understand this relationship and to determine if there are long-term consequences in adulthood.

Introduction

Examine the relationships between the DII-scores and bone and biomarkers of inflammation in 290 adolescents, ages 9–13 years.

Methods

DII-scores were calculated from 3-day diet records and categorized into tertiles, low (< − 1.34), medium (− 1.34 to 1.41), and high (> 1.41) inflammation. Radius and tibia bone were assessed via peripheral quantitative computed tomography (Stratec XCT 2000) at the 66% site relative to the distal growth plate. Fasting serum was measured for tumor necrosis factor alpha (TNF-α), interleukin-6 (IL-6), vascular endothelial growth factor (VEGF), and monocyte chemoattractant protein-1 (MCP-1). The relationships between DII-scores and bone and biomarkers of inflammation were assessed using bivariate and partial correlations adjusting for sexual maturation, sex, race, muscle cross-sectional area, and height. ANOVA/ANCOVA models were used to compare DII-tertiles with dependent variables.

Results

DII-scores were negatively associated with tibia trabecular area (TtAr; r = − .141, P = .019), periosteal perimeter (PsPM; r = − .145, P = .016), endosteal perimeter (r = − .145, P = .016), strength strain index (SSI; r = − .129, P = .032), and radius TtAr (r = − .140, P = .020), PsPM (r = −.138, P = .027) and SSI (r = −.131, P = .036) but nullified when adjusting for covariates. Tibia PsPM was higher in the low DII group compared to the medium (P = .050) and high (P = .046) groups but nullified after controlling for covariates. DII-scores were not associated with TNF-α, VEGF, or IL-6, but were associated with MCP-1 only in the unadjusted model (r = .125, P = .042). In the adjusted model, MCP-1 was inversely associated with tibia cortical thickness (r = −.150 P = .030).

Conclusion

The DII-scores were not related to biomarkers of inflammation or bone; however, the biomarker of inflammation, MCP-1 was negatively associated with tibia CtTh. Future prospective pediatric studies should be conducted to better understand this relationship and determine if there are long-term implications in adulthood.
Literature
1.
2.
go back to reference Martinez BK, White CM (2018) The emerging role of inflammation in cardiovascular disease. Ann Pharmacother 1060028018765939 Martinez BK, White CM (2018) The emerging role of inflammation in cardiovascular disease. Ann Pharmacother 1060028018765939
3.
go back to reference Donath MY, Shoelson SE (2011) Type 2 diabetes as an inflammatory disease. Nat Rev Immunol 11:98–107CrossRefPubMed Donath MY, Shoelson SE (2011) Type 2 diabetes as an inflammatory disease. Nat Rev Immunol 11:98–107CrossRefPubMed
4.
go back to reference Skalicky J, Muzakova V, Kandar R, Meloun M, Rousar T, Palicka V (2008) Evaluation of oxidative stress and inflammation in obese adults with metabolic syndrome. Clin Chem Lab Med 46:499–505CrossRefPubMed Skalicky J, Muzakova V, Kandar R, Meloun M, Rousar T, Palicka V (2008) Evaluation of oxidative stress and inflammation in obese adults with metabolic syndrome. Clin Chem Lab Med 46:499–505CrossRefPubMed
6.
go back to reference Ganesan K, Teklehaimanot S, Tran TH, Asuncion M, Norris K (2005) Relationship of C-reactive protein and bone mineral density in community-dwelling elderly females. J Natl Med Assoc 97:329–333PubMedPubMedCentral Ganesan K, Teklehaimanot S, Tran TH, Asuncion M, Norris K (2005) Relationship of C-reactive protein and bone mineral density in community-dwelling elderly females. J Natl Med Assoc 97:329–333PubMedPubMedCentral
7.
go back to reference Go AS, Mozaffarian D, Roger VL, Benjamin EJ, Berry JD, Blaha MJ, Dai S, Ford ES, Fox CS, Franco S, Fullerton HJ, Gillespie C, Hailpern SM, Heit JA, Howard VJ, Huffman MD, Judd SE, Kissela BM, Kittner SJ, Lackland DT, Lichtman JH, Lisabeth LD, Mackey RH, Magid DJ, Marcus GM, Marelli A, Matchar DB, McGuire D, Mohler ER 3rd, Moy CS, Mussolino ME, Neumar RW, Nichol G, Pandey DK, Paynter NP, Reeves MJ, Sorlie PD, Stein J, Towfighi A, Turan TN, Virani SS, Wong ND, Woo D, Turner MB, American Heart Association Statistics Committee and Stroke Statistics Subcommittee (2014) Heart disease and stroke statistics--2014 update: a report from the American Heart Association. Circulation 129:e28–e292CrossRefPubMed Go AS, Mozaffarian D, Roger VL, Benjamin EJ, Berry JD, Blaha MJ, Dai S, Ford ES, Fox CS, Franco S, Fullerton HJ, Gillespie C, Hailpern SM, Heit JA, Howard VJ, Huffman MD, Judd SE, Kissela BM, Kittner SJ, Lackland DT, Lichtman JH, Lisabeth LD, Mackey RH, Magid DJ, Marcus GM, Marelli A, Matchar DB, McGuire D, Mohler ER 3rd, Moy CS, Mussolino ME, Neumar RW, Nichol G, Pandey DK, Paynter NP, Reeves MJ, Sorlie PD, Stein J, Towfighi A, Turan TN, Virani SS, Wong ND, Woo D, Turner MB, American Heart Association Statistics Committee and Stroke Statistics Subcommittee (2014) Heart disease and stroke statistics--2014 update: a report from the American Heart Association. Circulation 129:e28–e292CrossRefPubMed
8.
go back to reference Weiss R, Dziura J, Burgert TS, Tamborlane WV, Taksali SE, Yeckel CW, Allen K, Lopes M, Savoye M, Morrison J, Sherwin RS, Caprio S (2004) Obesity and the metabolic syndrome in children and adolescents. N Engl J Med 350:2362–2374CrossRefPubMed Weiss R, Dziura J, Burgert TS, Tamborlane WV, Taksali SE, Yeckel CW, Allen K, Lopes M, Savoye M, Morrison J, Sherwin RS, Caprio S (2004) Obesity and the metabolic syndrome in children and adolescents. N Engl J Med 350:2362–2374CrossRefPubMed
9.
go back to reference Rubin DA, McMurray RG, Harrell JS, Hackney AC, Thorpe DE, Haqq AM (2008) The association between insulin resistance and cytokines in adolescents: the role of weight status and exercise. Metabolism 57:683–690CrossRefPubMedPubMedCentral Rubin DA, McMurray RG, Harrell JS, Hackney AC, Thorpe DE, Haqq AM (2008) The association between insulin resistance and cytokines in adolescents: the role of weight status and exercise. Metabolism 57:683–690CrossRefPubMedPubMedCentral
10.
go back to reference Pirkola J, Vaarasmaki M, Ala-Korpela M et al (2010) Low-grade, systemic inflammation in adolescents: association with early-life factors, gender, and lifestyle. Am J Epidemiol 171:72–82CrossRefPubMed Pirkola J, Vaarasmaki M, Ala-Korpela M et al (2010) Low-grade, systemic inflammation in adolescents: association with early-life factors, gender, and lifestyle. Am J Epidemiol 171:72–82CrossRefPubMed
11.
go back to reference Calder PC, Ahluwalia N, Albers R, Bosco N, Bourdet-Sicard R, Haller D, Holgate ST, Jönsson LS, Latulippe ME, Marcos A, Moreines J, M'Rini C, Müller M, Pawelec G, van Neerven RJJ, Watzl B, Zhao J (2013) A consideration of biomarkers to be used for evaluation of inflammation in human nutritional studies. Br J Nutr 109(Suppl 1):S1–S34CrossRefPubMed Calder PC, Ahluwalia N, Albers R, Bosco N, Bourdet-Sicard R, Haller D, Holgate ST, Jönsson LS, Latulippe ME, Marcos A, Moreines J, M'Rini C, Müller M, Pawelec G, van Neerven RJJ, Watzl B, Zhao J (2013) A consideration of biomarkers to be used for evaluation of inflammation in human nutritional studies. Br J Nutr 109(Suppl 1):S1–S34CrossRefPubMed
12.
go back to reference Minihane AM, Vinoy S, Russell WR, Baka A, Roche HM, Tuohy KM, Teeling JL, Blaak EE, Fenech M, Vauzour D, McArdle HJ, Kremer BHA, Sterkman L, Vafeiadou K, Benedetti MM, Williams CM, Calder PC (2015) Low-grade inflammation, diet composition and health: current research evidence and its translation. Br J Nutr 114:999–1012CrossRefPubMedPubMedCentral Minihane AM, Vinoy S, Russell WR, Baka A, Roche HM, Tuohy KM, Teeling JL, Blaak EE, Fenech M, Vauzour D, McArdle HJ, Kremer BHA, Sterkman L, Vafeiadou K, Benedetti MM, Williams CM, Calder PC (2015) Low-grade inflammation, diet composition and health: current research evidence and its translation. Br J Nutr 114:999–1012CrossRefPubMedPubMedCentral
13.
go back to reference Sears B, Ricordi C (2011) Anti-inflammatory nutrition as a pharmacological approach to treat obesity. J Obes 2011:1–14CrossRef Sears B, Ricordi C (2011) Anti-inflammatory nutrition as a pharmacological approach to treat obesity. J Obes 2011:1–14CrossRef
14.
go back to reference Nicklas TA, Baranowski T, Cullen KW, Berenson G (2001) Eating patterns, dietary quality and obesity. J Am Coll Nutr 20:599–608CrossRefPubMed Nicklas TA, Baranowski T, Cullen KW, Berenson G (2001) Eating patterns, dietary quality and obesity. J Am Coll Nutr 20:599–608CrossRefPubMed
15.
go back to reference Cavicchia PP, Steck SE, Hurley TG, Hussey JR, Ma Y, Ockene IS, Hebert JR (2009) A new dietary inflammatory index predicts interval changes in serum high-sensitivity C-reactive protein. J Nutr 139:2365–2372CrossRefPubMedPubMedCentral Cavicchia PP, Steck SE, Hurley TG, Hussey JR, Ma Y, Ockene IS, Hebert JR (2009) A new dietary inflammatory index predicts interval changes in serum high-sensitivity C-reactive protein. J Nutr 139:2365–2372CrossRefPubMedPubMedCentral
16.
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 17:1689–1696CrossRefPubMed 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 17:1689–1696CrossRefPubMed
17.
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 17:1825–1833CrossRefPubMed 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 17:1825–1833CrossRefPubMed
18.
go back to reference 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 25:398–405CrossRefPubMedPubMedCentral 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 25:398–405CrossRefPubMedPubMedCentral
19.
go back to reference Shivappa N, Hebert JR, Marcos A et al (2017) Association between dietary inflammatory index and inflammatory markers in the HELENA study. Mol Nutr Food Res 61 Shivappa N, Hebert JR, Marcos A et al (2017) Association between dietary inflammatory index and inflammatory markers in the HELENA study. Mol Nutr Food Res 61
20.
go back to reference Cauley JA, Danielson ME, Boudreau RM, Forrest KY, Zmuda JM, Pahor M, Tylavsky FA, Cummings SR, Harris TB, Newman AB, Health ABC Study (2007) Inflammatory markers and incident fracture risk in older men and women: the Health Aging and Body Composition Study. J Bone Miner Res 22:1088–1095CrossRefPubMed Cauley JA, Danielson ME, Boudreau RM, Forrest KY, Zmuda JM, Pahor M, Tylavsky FA, Cummings SR, Harris TB, Newman AB, Health ABC Study (2007) Inflammatory markers and incident fracture risk in older men and women: the Health Aging and Body Composition Study. J Bone Miner Res 22:1088–1095CrossRefPubMed
21.
22.
go back to reference Lien G, Selvaag AM, Flato B, Haugen M, Vinje O, Sorskaar D, Dale K, Egeland T, Forre O (2005) A two-year prospective controlled study of bone mass and bone turnover in children with early juvenile idiopathic arthritis. Arthritis Rheum 52:833–840CrossRefPubMed Lien G, Selvaag AM, Flato B, Haugen M, Vinje O, Sorskaar D, Dale K, Egeland T, Forre O (2005) A two-year prospective controlled study of bone mass and bone turnover in children with early juvenile idiopathic arthritis. Arthritis Rheum 52:833–840CrossRefPubMed
24.
go back to reference Roth J, Palm C, Scheunemann I, Ranke MB, Schweizer R, Dannecker GE (2004) Musculoskeletal abnormalities of the forearm in patients with juvenile idiopathic arthritis relate mainly to bone geometry. Arthritis Rheum 50:1277–1285CrossRefPubMed Roth J, Palm C, Scheunemann I, Ranke MB, Schweizer R, Dannecker GE (2004) Musculoskeletal abnormalities of the forearm in patients with juvenile idiopathic arthritis relate mainly to bone geometry. Arthritis Rheum 50:1277–1285CrossRefPubMed
25.
go back to reference Haring B, Crandall CJ, Wu C, LeBlanc ES, Shikany JM, Carbone L, Orchard T, Thomas F, Wactawaski-Wende J, Li W, Cauley JA, Wassertheil-Smoller S (2016) Dietary patterns and fractures in postmenopausal women: results from the Women’s Health Initiative. JAMA Intern Med 176:645–652CrossRefPubMedPubMedCentral Haring B, Crandall CJ, Wu C, LeBlanc ES, Shikany JM, Carbone L, Orchard T, Thomas F, Wactawaski-Wende J, Li W, Cauley JA, Wassertheil-Smoller S (2016) Dietary patterns and fractures in postmenopausal women: results from the Women’s Health Initiative. JAMA Intern Med 176:645–652CrossRefPubMedPubMedCentral
26.
go back to reference Shivappa N, Hebert JR, Karamati M, Shariati-Bafghi SE, Rashidkhani B (2016) Increased inflammatory potential of diet is associated with bone mineral density among postmenopausal women in Iran. Eur J Nutr 55:561–568CrossRefPubMed Shivappa N, Hebert JR, Karamati M, Shariati-Bafghi SE, Rashidkhani B (2016) Increased inflammatory potential of diet is associated with bone mineral density among postmenopausal women in Iran. Eur J Nutr 55:561–568CrossRefPubMed
27.
go back to reference Mazidi M, Shivappa N, Wirth MD, Hebert JR, Vatanparast H, Kengne AP (2017) The association between dietary inflammatory properties and bone mineral density and risk of fracture in US adults. Eur J Clin Nutr 71:1273–1277CrossRefPubMed Mazidi M, Shivappa N, Wirth MD, Hebert JR, Vatanparast H, Kengne AP (2017) The association between dietary inflammatory properties and bone mineral density and risk of fracture in US adults. Eur J Clin Nutr 71:1273–1277CrossRefPubMed
28.
go back to reference Gordon CM, Zemel BS, Wren TA, Leonard MB, Bachrach LK, Rauch F, Gilsanz V, Rosen CJ, Winer KK (2017) The determinants of peak bone mass. J Pediatr 180:261–269CrossRefPubMed Gordon CM, Zemel BS, Wren TA, Leonard MB, Bachrach LK, Rauch F, Gilsanz V, Rosen CJ, Winer KK (2017) The determinants of peak bone mass. J Pediatr 180:261–269CrossRefPubMed
29.
go back to reference Lewis RD, Laing EM, Hill Gallant KM, Hall DB, McCabe GP, Hausman DB, Martin BR, Warden SJ, Peacock M, Weaver CM (2013) A randomized trial of vitamin D(3) supplementation in children: dose-response effects on vitamin D metabolites and calcium absorption. J Clin Endocrinol Metab 98:4816–4825CrossRefPubMedPubMedCentral Lewis RD, Laing EM, Hill Gallant KM, Hall DB, McCabe GP, Hausman DB, Martin BR, Warden SJ, Peacock M, Weaver CM (2013) A randomized trial of vitamin D(3) supplementation in children: dose-response effects on vitamin D metabolites and calcium absorption. J Clin Endocrinol Metab 98:4816–4825CrossRefPubMedPubMedCentral
30.
go back to reference Tanner JM (1975) The measurement of maturity. Trans Eur Orthod Soc, pp 45–60 Tanner JM (1975) The measurement of maturity. Trans Eur Orthod Soc, pp 45–60
31.
go back to reference Crawford PB, Obarzanek E, Morrison J, Sabry ZI (1994) Comparative advantage of 3-day food records over 24-hour recall and 5-day food frequency validated by observation of 9- and 10-year-old girls. J Am Diet Assoc 94:626–630CrossRefPubMed Crawford PB, Obarzanek E, Morrison J, Sabry ZI (1994) Comparative advantage of 3-day food records over 24-hour recall and 5-day food frequency validated by observation of 9- and 10-year-old girls. J Am Diet Assoc 94:626–630CrossRefPubMed
32.
go back to reference Bergman EA, Boyungs JC, Erickson ML (1990) Comparison of a food frequency questionnaire and a 3-day diet record. J Am Diet Assoc 90:1431–1433PubMed Bergman EA, Boyungs JC, Erickson ML (1990) Comparison of a food frequency questionnaire and a 3-day diet record. J Am Diet Assoc 90:1431–1433PubMed
33.
go back to reference Kuczmarski RJ, Ogden CL, Grummer-Strawn LM, Flegal KM, Guo SS, Wei R, Mei Z, Curtin LR, Roche AF, Johnson CL (2000) CDC growth charts: United States. Adv Data 1–27 Kuczmarski RJ, Ogden CL, Grummer-Strawn LM, Flegal KM, Guo SS, Wei R, Mei Z, Curtin LR, Roche AF, Johnson CL (2000) CDC growth charts: United States. Adv Data 1–27
34.
go back to reference Warden SJ, Hill KM, Ferira AJ, Laing EM, Martin BR, Hausman DB, Weaver CM, Peacock M, Lewis RD (2013) Racial differences in cortical bone and their relationship to biochemical variables in Black and White children in the early stages of puberty. Osteoporos Int 24:1869–1879CrossRefPubMed Warden SJ, Hill KM, Ferira AJ, Laing EM, Martin BR, Hausman DB, Weaver CM, Peacock M, Lewis RD (2013) Racial differences in cortical bone and their relationship to biochemical variables in Black and White children in the early stages of puberty. Osteoporos Int 24:1869–1879CrossRefPubMed
35.
go back to reference Ferira AJ, Laing EM, Hausman DB, Hall DB, McCabe GP, Martin BR, Hill Gallant KM, Warden SJ, Weaver CM, Peacock M, Lewis RD (2016) Vitamin D supplementation does not impact insulin resistance in Black and White children. J Clin Endocrinol Metab 101:1710–1718CrossRefPubMedPubMedCentral Ferira AJ, Laing EM, Hausman DB, Hall DB, McCabe GP, Martin BR, Hill Gallant KM, Warden SJ, Weaver CM, Peacock M, Lewis RD (2016) Vitamin D supplementation does not impact insulin resistance in Black and White children. J Clin Endocrinol Metab 101:1710–1718CrossRefPubMedPubMedCentral
36.
go back to reference Kontulainen SA, Johnston JD, Liu D, Leung C, Oxland TR, McKay HA (2008) Strength indices from pQCT imaging predict up to 85% of variance in bone failure properties at tibial epiphysis and diaphysis. J Musculoskelet Neuronal Interact 8:401–409PubMed Kontulainen SA, Johnston JD, Liu D, Leung C, Oxland TR, McKay HA (2008) Strength indices from pQCT imaging predict up to 85% of variance in bone failure properties at tibial epiphysis and diaphysis. J Musculoskelet Neuronal Interact 8:401–409PubMed
37.
go back to reference Pollock NK, Laing EM, Baile CA, Hamrick MW, Hall DB, Lewis RD (2007) Is adiposity advantageous for bone strength? A peripheral quantitative computed tomography study in late adolescent females. Am J Clin Nutr 86:1530–1538CrossRefPubMed Pollock NK, Laing EM, Baile CA, Hamrick MW, Hall DB, Lewis RD (2007) Is adiposity advantageous for bone strength? A peripheral quantitative computed tomography study in late adolescent females. Am J Clin Nutr 86:1530–1538CrossRefPubMed
38.
go back to reference Swinford RR, Warden SJ (2010) Factors affecting short-term precision of musculoskeletal measures using peripheral quantitative computed tomography (pQCT). Osteoporos Int 21:1863–1870CrossRefPubMed Swinford RR, Warden SJ (2010) Factors affecting short-term precision of musculoskeletal measures using peripheral quantitative computed tomography (pQCT). Osteoporos Int 21:1863–1870CrossRefPubMed
39.
go back to reference Berger PK, Pollock NK, Laing EM, Warden SJ, Hill Gallant KM, Hausman DB, Tripp RA, McCabe LD, McCabe GP, Weaver CM, Peacock M, Lewis RD (2014) Association of adenovirus 36 infection with adiposity and inflammatory-related markers in children. J Clin Endocrinol Metab 99:3240–3246CrossRefPubMedPubMedCentral Berger PK, Pollock NK, Laing EM, Warden SJ, Hill Gallant KM, Hausman DB, Tripp RA, McCabe LD, McCabe GP, Weaver CM, Peacock M, Lewis RD (2014) Association of adenovirus 36 infection with adiposity and inflammatory-related markers in children. J Clin Endocrinol Metab 99:3240–3246CrossRefPubMedPubMedCentral
40.
go back to reference Binkovitz LA, Henwood MJ (2007) Pediatric DXA: technique and interpretation. Pediatr Radiol 37:21–31CrossRefPubMed Binkovitz LA, Henwood MJ (2007) Pediatric DXA: technique and interpretation. Pediatr Radiol 37:21–31CrossRefPubMed
41.
go back to reference Wetzsteon RJ, Zemel BS, Shults J, Howard KM, Kibe LW, Leonard MB (2011) Mechanical loads and cortical bone geometry in healthy children and young adults. Bone 48:1103–1108CrossRefPubMedPubMedCentral Wetzsteon RJ, Zemel BS, Shults J, Howard KM, Kibe LW, Leonard MB (2011) Mechanical loads and cortical bone geometry in healthy children and young adults. Bone 48:1103–1108CrossRefPubMedPubMedCentral
42.
go back to reference Cole ZA, Harvey NC, Kim M, Ntani G, Robinson SM, Inskip HM, Godfrey KM, Cooper C, Dennison EM, Southampton Women’s Survey Study G (2012) Increased fat mass is associated with increased bone size but reduced volumetric density in pre pubertal children. Bone 50:562–567CrossRefPubMed Cole ZA, Harvey NC, Kim M, Ntani G, Robinson SM, Inskip HM, Godfrey KM, Cooper C, Dennison EM, Southampton Women’s Survey Study G (2012) Increased fat mass is associated with increased bone size but reduced volumetric density in pre pubertal children. Bone 50:562–567CrossRefPubMed
43.
go back to reference Correa-Rodriguez M, Rueda-Medina B, Gonzalez-Jimenez E, Correa-Bautista JE, Ramirez-Velez R, Schmidt-RioValle J (2018) Dietary inflammatory index, bone health and body composition in a population of young adults: a cross-sectional study. Int J Food Sci Nutr 1–7 Correa-Rodriguez M, Rueda-Medina B, Gonzalez-Jimenez E, Correa-Bautista JE, Ramirez-Velez R, Schmidt-RioValle J (2018) Dietary inflammatory index, bone health and body composition in a population of young adults: a cross-sectional study. Int J Food Sci Nutr 1–7
44.
go back to reference Berteus Forslund H, Torgerson JS, Sjostrom L, Lindroos AK (2005) Snacking frequency in relation to energy intake and food choices in obese men and women compared to a reference population. Int J Obes 29:711–719CrossRef Berteus Forslund H, Torgerson JS, Sjostrom L, Lindroos AK (2005) Snacking frequency in relation to energy intake and food choices in obese men and women compared to a reference population. Int J Obes 29:711–719CrossRef
45.
go back to reference Sjoberg A, Hallberg L, Hoglund D, Hulthen L (2003) Meal pattern, food choice, nutrient intake and lifestyle factors in The Goteborg Adolescence Study. Eur J Clin Nutr 57:1569–1578CrossRefPubMed Sjoberg A, Hallberg L, Hoglund D, Hulthen L (2003) Meal pattern, food choice, nutrient intake and lifestyle factors in The Goteborg Adolescence Study. Eur J Clin Nutr 57:1569–1578CrossRefPubMed
47.
go back to reference Deo R, Khera A, McGuire DK, Murphy SA, Meo Neto Jde P, Morrow DA, de Lemos JA (2004) Association among plasma levels of monocyte chemoattractant protein-1, traditional cardiovascular risk factors, and subclinical atherosclerosis. J Am Coll Cardiol 44:1812–1818CrossRefPubMed Deo R, Khera A, McGuire DK, Murphy SA, Meo Neto Jde P, Morrow DA, de Lemos JA (2004) Association among plasma levels of monocyte chemoattractant protein-1, traditional cardiovascular risk factors, and subclinical atherosclerosis. J Am Coll Cardiol 44:1812–1818CrossRefPubMed
48.
go back to reference Palozza P, Parrone N, Catalano A, Simone R (2010) Tomato lycopene and inflammatory cascade: basic interactions and clinical implications. Curr Med Chem 17:2547–2563CrossRefPubMed Palozza P, Parrone N, Catalano A, Simone R (2010) Tomato lycopene and inflammatory cascade: basic interactions and clinical implications. Curr Med Chem 17:2547–2563CrossRefPubMed
49.
go back to reference Chung RWS, Leanderson P, Lundberg AK, Jonasson L (2017) Lutein exerts anti-inflammatory effects in patients with coronary artery disease. Atherosclerosis 262:87–93CrossRefPubMed Chung RWS, Leanderson P, Lundberg AK, Jonasson L (2017) Lutein exerts anti-inflammatory effects in patients with coronary artery disease. Atherosclerosis 262:87–93CrossRefPubMed
50.
go back to reference Birch L, Savage JS, Ventura A (2007) Influences on the development of children’s eating behaviours: from infancy to adolescence. Can J Diet Pract Res 68:s1–s56PubMedPubMedCentral Birch L, Savage JS, Ventura A (2007) Influences on the development of children’s eating behaviours: from infancy to adolescence. Can J Diet Pract Res 68:s1–s56PubMedPubMedCentral
51.
Metadata
Title
Dietary inflammatory index® and cortical bone outcomes in healthy adolescent children
Authors
L. M. Coheley
N. Shivappa
J. R. Hebert
R. D. Lewis
Publication date
01-08-2019
Publisher
Springer London
Keyword
Biomarkers
Published in
Osteoporosis International / Issue 8/2019
Print ISSN: 0937-941X
Electronic ISSN: 1433-2965
DOI
https://doi.org/10.1007/s00198-019-04946-3

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