Skip to main content
Top
Published in: Calcified Tissue International 2/2018

01-08-2018 | Original Research

Marrow Adipose Tissue in Older Men: Association with Visceral and Subcutaneous Fat, Bone Volume, Metabolism, and Inflammation

Authors: Ebrahim Bani Hassan, Oddom Demontiero, Sara Vogrin, Alvin Ng, Gustavo Duque

Published in: Calcified Tissue International | Issue 2/2018

Login to get access

Abstract

Marrow (MAT) and subcutaneous (SAT) adipose tissues display different metabolic profiles and varying associations with aging, bone density, and fracture risk. Using a non-invasive imaging methodology, we aimed to investigate the associations between MAT, SAT, and visceral fat (VAT) with bone volume, bone remodeling markers, insulin resistance, and circulating inflammatory mediators in a population of older men. In this cross-sectional study, 96 healthy men (mean age 67 ± 5.5) were assessed for anthropometric parameters, body composition, serum biochemistry, and inflammatory panel. Using single-energy computed tomography images, MAT (in L2 and L3 and both hips), VAT, and SAT (at the level of L2–L3 and L4–L5) were measured employing Slice-O-Matic software (Tomovision), which enables specific tissue demarcation applying previously reported Hounsfield unit thresholds. MAT volume was similar in all anatomical sites and independent of BMI. In all femoral regions of interest (ROIs) there was a strong negative association between bone and MAT volumes (r = − 0.840 to − 0.972, p < 0.001), with location-dependent variations in the lumbar spine. Unlike VAT and SAT, no associations between MAT and serum glucose, inflammatory markers or insulin resistance indicators were found. Bone decline occurred without red marrow expansion; thus lost bone was mainly (if not exclusively) replaced by MAT. In conclusion, strong inverse correlations between MAT and bone mass, which have been previously observed in women, were also confirmed in older men. However, MAT volume in all ROIs was interrelated and unlike women, mainly independent of VAT or SAT. The lack of strong association between MAT vs VAT/SAT, and its discordant associations with metabolic and inflammatory mediators provide further evidence on MAT’s distinct attributes in older men.
Literature
1.
go back to reference Devlin MJ, Rosen CJ (2015) The bone-fat interface: basic and clinical implications of marrow adiposity. Lancet Diabetes Endocrinol 3:141–147CrossRefPubMed Devlin MJ, Rosen CJ (2015) The bone-fat interface: basic and clinical implications of marrow adiposity. Lancet Diabetes Endocrinol 3:141–147CrossRefPubMed
2.
go back to reference Gasparrini M, Rivas D, Elbaz A, Duque G (2009) Differential expression of cytokines in subcutaneous and marrow fat of aging C57BL/6J mice. Exp Gerontol 44:613–618CrossRefPubMed Gasparrini M, Rivas D, Elbaz A, Duque G (2009) Differential expression of cytokines in subcutaneous and marrow fat of aging C57BL/6J mice. Exp Gerontol 44:613–618CrossRefPubMed
4.
go back to reference Baum T, Yap SP, Karampinos DC, Nardo L, Kuo D, Burghardt AJ, Masharani UB, Schwartz AV, Li X, Link TM (2012) Does vertebral bone marrow fat content correlate with abdominal adipose tissue, lumbar spine BMD and blood biomarkers in women with type 2 diabetes mellitus? J Magn Reson Imaging 35:117–124CrossRefPubMed Baum T, Yap SP, Karampinos DC, Nardo L, Kuo D, Burghardt AJ, Masharani UB, Schwartz AV, Li X, Link TM (2012) Does vertebral bone marrow fat content correlate with abdominal adipose tissue, lumbar spine BMD and blood biomarkers in women with type 2 diabetes mellitus? J Magn Reson Imaging 35:117–124CrossRefPubMed
5.
go back to reference Bredella MA, Torriani M, Ghomi RH, Thomas BJ, Brick DJ, Gerweck AV, Rosen CJ, Klibanski A, Miller KK (2011) Vertebral bone marrow fat is positively associated with visceral fat and inversely associated with IGF-1 in obese women. Obesity 19:49–53CrossRefPubMed Bredella MA, Torriani M, Ghomi RH, Thomas BJ, Brick DJ, Gerweck AV, Rosen CJ, Klibanski A, Miller KK (2011) Vertebral bone marrow fat is positively associated with visceral fat and inversely associated with IGF-1 in obese women. Obesity 19:49–53CrossRefPubMed
6.
go back to reference Meunier P, Aaron J, Edouard C, Vignon G (1971) Osteoporosis and the replacement of cell populations of the marrow by adipose tissue. A quantitative study of 84 iliac bone biopsies. Clin Orthop Relat Res 80:147–154CrossRefPubMed Meunier P, Aaron J, Edouard C, Vignon G (1971) Osteoporosis and the replacement of cell populations of the marrow by adipose tissue. A quantitative study of 84 iliac bone biopsies. Clin Orthop Relat Res 80:147–154CrossRefPubMed
7.
go back to reference Rosen CJ, Ackert-Bicknell C, Rodriguez JP, Pino AM (2009) Marrow fat and the bone microenvironment: developmental, functional, and pathological implications. Crit Rev Eukaryot Gene Expr 19:109–124CrossRefPubMedPubMedCentral Rosen CJ, Ackert-Bicknell C, Rodriguez JP, Pino AM (2009) Marrow fat and the bone microenvironment: developmental, functional, and pathological implications. Crit Rev Eukaryot Gene Expr 19:109–124CrossRefPubMedPubMedCentral
9.
go back to reference Schwartz RS, Shuman WP, Bradbury VL, Cain KC, Fellingham GW, Beard JC, Kahn SE, Stratton JR, Cerqueira MD, Abrass IB (1990) Body fat distribution in healthy young and older men. J Gerontol 45:M181–M185CrossRef Schwartz RS, Shuman WP, Bradbury VL, Cain KC, Fellingham GW, Beard JC, Kahn SE, Stratton JR, Cerqueira MD, Abrass IB (1990) Body fat distribution in healthy young and older men. J Gerontol 45:M181–M185CrossRef
10.
go back to reference Chowdhury B, Sjöström L, Alpsten M, Kostanty J, Kvist H, Löfgren R (1994) A multicompartment body composition technique based on computerized tomography. Int J Obes Relat Metab Disord 18:219–234PubMed Chowdhury B, Sjöström L, Alpsten M, Kostanty J, Kvist H, Löfgren R (1994) A multicompartment body composition technique based on computerized tomography. Int J Obes Relat Metab Disord 18:219–234PubMed
11.
go back to reference Demerath EW, Ritter KJ, Couch WA, Rogers NL, Moreno GM, Choh A, Lee M, Remsberg K, Czerwinski SA, Chumlea WC, Siervogel RM, Towne B (2007) Validity of a new automated software program for visceral adipose tissue estimation. Int J Obes 31:285–291CrossRef Demerath EW, Ritter KJ, Couch WA, Rogers NL, Moreno GM, Choh A, Lee M, Remsberg K, Czerwinski SA, Chumlea WC, Siervogel RM, Towne B (2007) Validity of a new automated software program for visceral adipose tissue estimation. Int J Obes 31:285–291CrossRef
12.
go back to reference Demontiero O, Li W, Thembani E, Duque G (2011) Validation of noninvasive quantification of bone marrow fat volume with microCT in aging rats. Exp Gerontol 46:435–440CrossRefPubMed Demontiero O, Li W, Thembani E, Duque G (2011) Validation of noninvasive quantification of bone marrow fat volume with microCT in aging rats. Exp Gerontol 46:435–440CrossRefPubMed
14.
go back to reference White DR, Woodard HQ, Hammond SM (1987) Average soft-tissue and bone models for use in radiation dosimetry. Br J Radiol 60:907–913CrossRefPubMed White DR, Woodard HQ, Hammond SM (1987) Average soft-tissue and bone models for use in radiation dosimetry. Br J Radiol 60:907–913CrossRefPubMed
15.
go back to reference Schneider W, Bortfeld T, Schlegel W (2000) Correlation between CT numbers and tissue parameters needed for Monte Carlo simulations of clinical dose distributions. Phys Med Biol 45:459–478CrossRefPubMed Schneider W, Bortfeld T, Schlegel W (2000) Correlation between CT numbers and tissue parameters needed for Monte Carlo simulations of clinical dose distributions. Phys Med Biol 45:459–478CrossRefPubMed
16.
go back to reference Despres JP (1993) Abdominal obesity as important component of insulin-resistance syndrome. Nutrition 9:452–459PubMed Despres JP (1993) Abdominal obesity as important component of insulin-resistance syndrome. Nutrition 9:452–459PubMed
17.
go back to reference Verma S, Rajaratnam JH, Denton J, Hoyland JA, Byers RJ (2002) Adipocytic proportion of bone marrow is inversely related to bone formation in osteoporosis. J Clin Pathol 55:693–698CrossRefPubMedPubMedCentral Verma S, Rajaratnam JH, Denton J, Hoyland JA, Byers RJ (2002) Adipocytic proportion of bone marrow is inversely related to bone formation in osteoporosis. J Clin Pathol 55:693–698CrossRefPubMedPubMedCentral
18.
go back to reference de Luca C, Olefsky JM (2008) Inflammation and Insulin Resistance. Fed Eur Biochem Soc Lett 582:97–105CrossRef de Luca C, Olefsky JM (2008) Inflammation and Insulin Resistance. Fed Eur Biochem Soc Lett 582:97–105CrossRef
19.
go back to reference Jung UJ, Choi M-S (2014) Obesity and its metabolic complications: the role of adipokines and the relationship between obesity, inflammation, insulin resistance, dyslipidemia and nonalcoholic fatty liver disease. Int J Mol Sci 15:6184–6223CrossRefPubMedPubMedCentral Jung UJ, Choi M-S (2014) Obesity and its metabolic complications: the role of adipokines and the relationship between obesity, inflammation, insulin resistance, dyslipidemia and nonalcoholic fatty liver disease. Int J Mol Sci 15:6184–6223CrossRefPubMedPubMedCentral
20.
go back to reference McArdle MA, Finucane OM, Connaughton RM, McMorrow AM, Roche HM (2013) Mechanisms of obesity-induced inflammation and insulin resistance: insights into the emerging role of nutritional strategies. Front Endocrinol 4:52CrossRef McArdle MA, Finucane OM, Connaughton RM, McMorrow AM, Roche HM (2013) Mechanisms of obesity-induced inflammation and insulin resistance: insights into the emerging role of nutritional strategies. Front Endocrinol 4:52CrossRef
21.
go back to reference Malkov S, Cawthon PM, Peters KW, Cauley JA, Murphy RA, Visser M, Wilson JP, Harris T, Satterfield S, Cummings S, Shepherd JA, for the Health ABCS (2015) Hip fractures risk in older men and women associated with DXA-derived measures of thigh subcutaneous fat thickness, cross-sectional muscle area, and muscle density. J Bone Miner Res 30:1414–1421CrossRefPubMedPubMedCentral Malkov S, Cawthon PM, Peters KW, Cauley JA, Murphy RA, Visser M, Wilson JP, Harris T, Satterfield S, Cummings S, Shepherd JA, for the Health ABCS (2015) Hip fractures risk in older men and women associated with DXA-derived measures of thigh subcutaneous fat thickness, cross-sectional muscle area, and muscle density. J Bone Miner Res 30:1414–1421CrossRefPubMedPubMedCentral
22.
go back to reference Guo W, Pirtskhalava T, Tchkonia T, Xie W, Thomou T, Han J, Wang T, Wong S, Cartwright A, Hegardt FG, Corkey BE, Kirkland JL (2007) Aging results in paradoxical susceptibility of fat cell progenitors to lipotoxicity. Am J Physiol Endocrinol Metab 292:E1041-1051CrossRef Guo W, Pirtskhalava T, Tchkonia T, Xie W, Thomou T, Han J, Wang T, Wong S, Cartwright A, Hegardt FG, Corkey BE, Kirkland JL (2007) Aging results in paradoxical susceptibility of fat cell progenitors to lipotoxicity. Am J Physiol Endocrinol Metab 292:E1041-1051CrossRef
23.
go back to reference Kirkland JL, Tchkonia T, Pirtskhalava T, Han J, Karagiannides I (2002) Adipogenesis and aging: does aging make fat go MAD? Exp. Gerontol 37:757–767 Kirkland JL, Tchkonia T, Pirtskhalava T, Han J, Karagiannides I (2002) Adipogenesis and aging: does aging make fat go MAD? Exp. Gerontol 37:757–767
24.
go back to reference Zamboni M, Mazzali G, Zoico E, Harris TB, Meigs JB, Di Francesco V, Fantin F, Bissoli L, Bosello O (2005) Health consequences of obesity in the elderly: a review of four unresolved questions. Int J Obes 29:1011–1029CrossRef Zamboni M, Mazzali G, Zoico E, Harris TB, Meigs JB, Di Francesco V, Fantin F, Bissoli L, Bosello O (2005) Health consequences of obesity in the elderly: a review of four unresolved questions. Int J Obes 29:1011–1029CrossRef
25.
go back to reference Elbaz A, Wu X, Rivas D, Gimble JM, Duque G (2010) Inhibition of fatty acid biosynthesis prevents adipocyte lipotoxicity on human osteoblasts in vitro. J Cell Mol Med 14:982–991CrossRefPubMed Elbaz A, Wu X, Rivas D, Gimble JM, Duque G (2010) Inhibition of fatty acid biosynthesis prevents adipocyte lipotoxicity on human osteoblasts in vitro. J Cell Mol Med 14:982–991CrossRefPubMed
26.
go back to reference Gunaratnam K, Vidal C, Gimble JM, Duque G (2014) Mechanisms of palmitate-induced lipotoxicity in human osteoblasts. Endocrinology 155:108–116CrossRefPubMed Gunaratnam K, Vidal C, Gimble JM, Duque G (2014) Mechanisms of palmitate-induced lipotoxicity in human osteoblasts. Endocrinology 155:108–116CrossRefPubMed
27.
go back to reference Martin RB, Chow BD, Lucas PA (1990) Bone marrow fat content in relation to bone remodeling and serum chemistry in intact and ovariectomized dogs. Calcif Tissue Int 46:189–194CrossRefPubMed Martin RB, Chow BD, Lucas PA (1990) Bone marrow fat content in relation to bone remodeling and serum chemistry in intact and ovariectomized dogs. Calcif Tissue Int 46:189–194CrossRefPubMed
28.
29.
go back to reference Wronski T, Smith J, Jee W (1981) Variations in mineral apposition rate of trabecular bone within the beagle skeleton. Calcif Tissue Int 33:583CrossRefPubMed Wronski T, Smith J, Jee W (1981) Variations in mineral apposition rate of trabecular bone within the beagle skeleton. Calcif Tissue Int 33:583CrossRefPubMed
30.
go back to reference Schwartz AV, Sigurdsson S, Hue TF, Lang TF, Harris TB, Rosen CJ, Vittinghoff E, Siggeirsdottir K, Sigurdsson G, Oskarsdottir D, Shet K, Palermo L, Gudnason V, Li X (2013) Vertebral bone marrow fat associated with lower trabecular BMD and prevalent vertebral fracture in older adults. J Clin Endocrinol Metab 98:2294–2300CrossRefPubMedPubMedCentral Schwartz AV, Sigurdsson S, Hue TF, Lang TF, Harris TB, Rosen CJ, Vittinghoff E, Siggeirsdottir K, Sigurdsson G, Oskarsdottir D, Shet K, Palermo L, Gudnason V, Li X (2013) Vertebral bone marrow fat associated with lower trabecular BMD and prevalent vertebral fracture in older adults. J Clin Endocrinol Metab 98:2294–2300CrossRefPubMedPubMedCentral
31.
go back to reference Griffith JF, Yeung DK, Antonio GE, Lee FK, Hong AW, Wong SY, Lau EM, Leung PC (2005) Vertebral bone mineral density, marrow perfusion, and fat content in healthy men and men with osteoporosis: dynamic contrast-enhanced MR imaging and MR spectroscopy. Radiology 236:945–951CrossRefPubMed Griffith JF, Yeung DK, Antonio GE, Lee FK, Hong AW, Wong SY, Lau EM, Leung PC (2005) Vertebral bone mineral density, marrow perfusion, and fat content in healthy men and men with osteoporosis: dynamic contrast-enhanced MR imaging and MR spectroscopy. Radiology 236:945–951CrossRefPubMed
32.
go back to reference Gillet C, Spruyt D, Rigutto S, Dalla Valle A, Berlier J, Louis C, Debier C, Gaspard N, Malaisse WJ, Gangji V, Rasschaert J (2015) Oleate abrogates palmitate-induced lipotoxicity and proinflammatory response in human bone marrow-derived mesenchymal stem cells and osteoblastic cells. Endocrinology 156:4081–4093CrossRefPubMed Gillet C, Spruyt D, Rigutto S, Dalla Valle A, Berlier J, Louis C, Debier C, Gaspard N, Malaisse WJ, Gangji V, Rasschaert J (2015) Oleate abrogates palmitate-induced lipotoxicity and proinflammatory response in human bone marrow-derived mesenchymal stem cells and osteoblastic cells. Endocrinology 156:4081–4093CrossRefPubMed
33.
go back to reference Kuiper JW, van Kuijk C, Grashuis JL, Ederveen AG, Schutte HE (1996) Accuracy and the influence of marrow fat on quantitative CT and dual-energy X-ray absorptiometry measurements of the femoral neck in vitro. Osteoporos Int 6:25–30CrossRefPubMed Kuiper JW, van Kuijk C, Grashuis JL, Ederveen AG, Schutte HE (1996) Accuracy and the influence of marrow fat on quantitative CT and dual-energy X-ray absorptiometry measurements of the femoral neck in vitro. Osteoporos Int 6:25–30CrossRefPubMed
Metadata
Title
Marrow Adipose Tissue in Older Men: Association with Visceral and Subcutaneous Fat, Bone Volume, Metabolism, and Inflammation
Authors
Ebrahim Bani Hassan
Oddom Demontiero
Sara Vogrin
Alvin Ng
Gustavo Duque
Publication date
01-08-2018
Publisher
Springer US
Published in
Calcified Tissue International / Issue 2/2018
Print ISSN: 0171-967X
Electronic ISSN: 1432-0827
DOI
https://doi.org/10.1007/s00223-018-0412-6

Other articles of this Issue 2/2018

Calcified Tissue International 2/2018 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.