Skip to main content
Erschienen in: Osteoporosis International 7/2017

12.04.2017 | Original Article

Reduced bone mass and preserved marrow adipose tissue in patients with inflammatory bowel diseases in long-term remission

verfasst von: C. M. Bastos, I. M. Araújo, M. H. Nogueira-Barbosa, C. E. G. Salmon, F. J. A. de Paula, L. E. A. Troncon

Erschienen in: Osteoporosis International | Ausgabe 7/2017

Einloggen, um Zugang zu erhalten

Abstract

Summary

Bone marrow adipose tissue has not been studied in patients with inactive inflammatory bowel disease. We found that these patients have preserved marrow adiposity even with low bone mass. Factors involved in bone loss in active disease may have long-lasting effects but do not seem to affect bone marrow adiposity.

Introduction

Reduced bone mass is known to occur at varying prevalence in patients with inflammatory bowel diseases (IBD) because of inflammation, malnutrition, and steroid therapy. Osteoporosis may develop in these patients as the result of an imbalanced relationship between osteoblasts and adipocytes in bone marrow. This study aimed to evaluate for the first time bone mass and bone marrow adipose tissue (BMAT) in a particular subgroup of IBD patients characterized by long-term, steroid-free remission.

Methods

Patients with Crohn’s disease (CD; N = 21) and ulcerative colitis (UC; N = 15) and controls (C; N = 65) underwent dual X-ray energy absorptiometry and nuclear magnetic resonance spectroscopy of the L3 lumbar vertebra for BMAT assessment.

Results

Both the CD and UC subgroups showed significantly higher proportions of patients than controls with Z-score ≤−2.0 at L1–L4 (C 1.54%; CD 19.05%; UC 20%; p = 0.02), but not at other sites. The proportions of CD patients with a T-score ˂−1.0 at the femoral neck (C 18.46%; CD 47.62%; p = 0.02) and total hip (C 16.92%; CD 42.86%; p = 0.03) were significantly higher than among controls. There were no statistically significant differences between IBD patients and controls regarding BMAT at L3 (C 28.62 ± 8.15%; CD 29.81 ± 6.90%; UC 27.35 ± 9.80%; p = 0.67).

Conclusions

IBD patients in long-term, steroid-free remission may have a low bone mass in spite of preserved BMAT. These findings confirm the heterogeneity of bone disorders in IBD and may indicate that factors involved in bone loss in active disease may have long-lasting effects on these patients.
Literatur
2.
Zurück zum Zitat Ghosh S, Cowen S, Hannan WJ et al (1994) Low bone mineral density in Crohn’s disease, but not in ulcerative colitis, at diagnosis. Gastroenterology 107:1031–1039CrossRefPubMed Ghosh S, Cowen S, Hannan WJ et al (1994) Low bone mineral density in Crohn’s disease, but not in ulcerative colitis, at diagnosis. Gastroenterology 107:1031–1039CrossRefPubMed
3.
Zurück zum Zitat Tilg H, Moschen AR, Kaser A et al (2008) Gut, inflammation and osteoporosis: basic and clinical concepts. Gut 57:684–694CrossRefPubMed Tilg H, Moschen AR, Kaser A et al (2008) Gut, inflammation and osteoporosis: basic and clinical concepts. Gut 57:684–694CrossRefPubMed
4.
Zurück zum Zitat Jahnsen J, Falch JA, Aadland E et al (1997) Bone mineral density is reduced in patients with Crohn’s disease but not in patients with ulcerative colitis: a population based study. Gut 40:313–319CrossRefPubMedPubMedCentral Jahnsen J, Falch JA, Aadland E et al (1997) Bone mineral density is reduced in patients with Crohn’s disease but not in patients with ulcerative colitis: a population based study. Gut 40:313–319CrossRefPubMedPubMedCentral
5.
Zurück zum Zitat Ardizzone S, Bollani S, Bettica P et al (2000) Altered bone metabolism in inflammatory bowel disease: there is a difference between Crohn’s disease and ulcerative colitis. J Intern Med 247:63–70CrossRefPubMed Ardizzone S, Bollani S, Bettica P et al (2000) Altered bone metabolism in inflammatory bowel disease: there is a difference between Crohn’s disease and ulcerative colitis. J Intern Med 247:63–70CrossRefPubMed
6.
Zurück zum Zitat Silvennoinen A, Karttunen TJ, Niemelã SE et al (1995) A controlled study of bone mineral density in patients with inflammatory bowel disease. Gut 37:71–76CrossRefPubMedPubMedCentral Silvennoinen A, Karttunen TJ, Niemelã SE et al (1995) A controlled study of bone mineral density in patients with inflammatory bowel disease. Gut 37:71–76CrossRefPubMedPubMedCentral
7.
Zurück zum Zitat Kanis JA (1994) Assessment of fracture risk and its application to screening for postmenopausal osteoporosis: synopsis of a WHO report. WHO Study Group. Osteoporos Int 4:368–381CrossRefPubMed Kanis JA (1994) Assessment of fracture risk and its application to screening for postmenopausal osteoporosis: synopsis of a WHO report. WHO Study Group. Osteoporos Int 4:368–381CrossRefPubMed
8.
Zurück zum Zitat Pigot F, Roux C, Chaussade S et al (1992) Low bone mineral density in patients with inflammatory bowel disease. Dig Dis Sci 37:1396–1403CrossRefPubMed Pigot F, Roux C, Chaussade S et al (1992) Low bone mineral density in patients with inflammatory bowel disease. Dig Dis Sci 37:1396–1403CrossRefPubMed
9.
Zurück zum Zitat Roux C, Abitbol V, Chaussade S et al (1995) Bone loss in patients with inflammatory bowel disease: a prospective study. Osteoporos Int 5:156–160CrossRefPubMed Roux C, Abitbol V, Chaussade S et al (1995) Bone loss in patients with inflammatory bowel disease: a prospective study. Osteoporos Int 5:156–160CrossRefPubMed
10.
Zurück zum Zitat Targownik LE, Bernstein CN, Leslie WD (2014) Risk factors and management of osteoporosis in inflammatory bowel disease. Curr Opin Gastroenterol 30:168–174CrossRefPubMed Targownik LE, Bernstein CN, Leslie WD (2014) Risk factors and management of osteoporosis in inflammatory bowel disease. Curr Opin Gastroenterol 30:168–174CrossRefPubMed
11.
Zurück zum Zitat Pietschmann P, Resch H, Woloszczuk W et al (1990) A circadian rhythm of serum osteocalcin levels in postmenopausal osteoporosis. Eur J Clin Investig 20:310–312CrossRef Pietschmann P, Resch H, Woloszczuk W et al (1990) A circadian rhythm of serum osteocalcin levels in postmenopausal osteoporosis. Eur J Clin Investig 20:310–312CrossRef
12.
Zurück zum Zitat Yavropoulou MP, Tomos K, Tsekmekidou X et al (2011) Response of biochemical markers of bone turnover to oral glucose load in diseases that affect bone metabolism. Eur J Endocrinol 164:1035–1041CrossRefPubMed Yavropoulou MP, Tomos K, Tsekmekidou X et al (2011) Response of biochemical markers of bone turnover to oral glucose load in diseases that affect bone metabolism. Eur J Endocrinol 164:1035–1041CrossRefPubMed
13.
Zurück zum Zitat Sanchez Cano D, Ruiz-Villaverde R, Olvera Porcel MC et al (2011) Evaluation of bone mineral density, bone turnover markers, the OPG/RANKL system and sTNF-RI in Crohn’s disease. Gastroenterol Hepatol 34:3–9CrossRefPubMed Sanchez Cano D, Ruiz-Villaverde R, Olvera Porcel MC et al (2011) Evaluation of bone mineral density, bone turnover markers, the OPG/RANKL system and sTNF-RI in Crohn’s disease. Gastroenterol Hepatol 34:3–9CrossRefPubMed
15.
Zurück zum Zitat Bianco P, Riminucci M, Gronthos S et al (2001) Bone marrow stromal stem cells: nature, biology, and potential applications. Stem Cells 19:180–192CrossRefPubMed Bianco P, Riminucci M, Gronthos S et al (2001) Bone marrow stromal stem cells: nature, biology, and potential applications. Stem Cells 19:180–192CrossRefPubMed
16.
Zurück zum Zitat Li X, Kuo D, Schafer AL et al (2011) Quantification of vertebral bone marrow fat content using 3 tesla MR spectroscopy: reproducibility, vertebral variation, and applications in osteoporosis. J Magn Reson Imaging 33:974–979CrossRefPubMedPubMedCentral Li X, Kuo D, Schafer AL et al (2011) Quantification of vertebral bone marrow fat content using 3 tesla MR spectroscopy: reproducibility, vertebral variation, and applications in osteoporosis. J Magn Reson Imaging 33:974–979CrossRefPubMedPubMedCentral
18.
Zurück zum Zitat Liu Y, Tang GY, Tang RB et al (2010) Assessment of bone marrow changes in postmenopausal women with varying bone densities: magnetic resonance spectroscopy and diffusion magnetic resonance imaging. Chin Med J 123:1524–1527PubMed Liu Y, Tang GY, Tang RB et al (2010) Assessment of bone marrow changes in postmenopausal women with varying bone densities: magnetic resonance spectroscopy and diffusion magnetic resonance imaging. Chin Med J 123:1524–1527PubMed
19.
Zurück zum Zitat Tang GY, Lv ZW, Tang RB et al (2010) Evaluation of MR spectroscopy and diffusion-weighted MRI in detecting bone marrow changes in postmenopausal women with osteoporosis. Clin Radiol 65:377–381CrossRefPubMed Tang GY, Lv ZW, Tang RB et al (2010) Evaluation of MR spectroscopy and diffusion-weighted MRI in detecting bone marrow changes in postmenopausal women with osteoporosis. Clin Radiol 65:377–381CrossRefPubMed
20.
Zurück zum Zitat Silverberg MS, Satsangi J, Ahmad T et al (2005) Toward an integrated clinical, molecular and serological classification of inflammatory bowel disease: report of a Working Party of the 2005 Montreal World Congress of Gastroenterology. Can J Gastroenterol 19(Suppl A):5a–36aCrossRefPubMed Silverberg MS, Satsangi J, Ahmad T et al (2005) Toward an integrated clinical, molecular and serological classification of inflammatory bowel disease: report of a Working Party of the 2005 Montreal World Congress of Gastroenterology. Can J Gastroenterol 19(Suppl A):5a–36aCrossRefPubMed
21.
Zurück zum Zitat Best WR, Becktel JM, Singleton JW et al (1976) Development of a Crohn’s disease activity index. National Cooperative Crohn’s Disease Study. Gastroenterology 70:439–444PubMed Best WR, Becktel JM, Singleton JW et al (1976) Development of a Crohn’s disease activity index. National Cooperative Crohn’s Disease Study. Gastroenterology 70:439–444PubMed
22.
Zurück zum Zitat Schousboe JT, Shepherd JA, Bilezikian JP et al (2013) Executive summary of the 2013 ISCD position development conference on bone densitometry. J Clin Densitom 16:455–467CrossRefPubMed Schousboe JT, Shepherd JA, Bilezikian JP et al (2013) Executive summary of the 2013 ISCD position development conference on bone densitometry. J Clin Densitom 16:455–467CrossRefPubMed
23.
Zurück zum Zitat de Paula FJA, de Araújo IM, Carvalho AL et al (2015) The relationship of fat distribution and insulin resistance with lumbar spine bone mass in women. PLoS One 10:e0129764CrossRefPubMedPubMedCentral de Paula FJA, de Araújo IM, Carvalho AL et al (2015) The relationship of fat distribution and insulin resistance with lumbar spine bone mass in women. PLoS One 10:e0129764CrossRefPubMedPubMedCentral
25.
Zurück zum Zitat Rosen CJ, Bouxsein ML (2006) Mechanisms of disease: is osteoporosis the obesity of bone? Nat Clin Pract Rheumatol 2:35–43CrossRefPubMed Rosen CJ, Bouxsein ML (2006) Mechanisms of disease: is osteoporosis the obesity of bone? Nat Clin Pract Rheumatol 2:35–43CrossRefPubMed
26.
27.
Zurück zum Zitat van Hogezand RA, Hamdy NA (2006) Skeletal morbidity in inflammatory bowel disease. Scand J Gastroenterol Suppl 243:59–64CrossRef van Hogezand RA, Hamdy NA (2006) Skeletal morbidity in inflammatory bowel disease. Scand J Gastroenterol Suppl 243:59–64CrossRef
28.
Zurück zum Zitat Bernstein CN, Leslie WD, Leboff MS (2003) AGA technical review on osteoporosis in gastrointestinal diseases. Gastroenterology 124:795–841CrossRefPubMed Bernstein CN, Leslie WD, Leboff MS (2003) AGA technical review on osteoporosis in gastrointestinal diseases. Gastroenterology 124:795–841CrossRefPubMed
29.
Zurück zum Zitat Compston J, Reid DM, Boisdron J et al (2008) Recommendations for the registration of agents for prevention and treatment of glucocorticoid-induced osteoporosis: an update from the Group for the Respect of Ethics and Excellence in Science. Osteoporos Int 19:1247–1250CrossRefPubMed Compston J, Reid DM, Boisdron J et al (2008) Recommendations for the registration of agents for prevention and treatment of glucocorticoid-induced osteoporosis: an update from the Group for the Respect of Ethics and Excellence in Science. Osteoporos Int 19:1247–1250CrossRefPubMed
30.
Zurück zum Zitat Seguro LP, Rosario C, Shoenfeld Y (2013) Long-term complications of past glucocorticoid use. Autoimmun Rev 12:629–632CrossRefPubMed Seguro LP, Rosario C, Shoenfeld Y (2013) Long-term complications of past glucocorticoid use. Autoimmun Rev 12:629–632CrossRefPubMed
31.
Zurück zum Zitat Cohen A, Shen W, Dempster DW et al (2015) Marrow adiposity assessed on transiliac crest biopsy samples correlates with noninvasive measurement of marrow adiposity by proton magnetic resonance spectroscopy (1H-MRS) at the spine but not the femur. Osteoporos Int 26:2471–2478CrossRefPubMedPubMedCentral Cohen A, Shen W, Dempster DW et al (2015) Marrow adiposity assessed on transiliac crest biopsy samples correlates with noninvasive measurement of marrow adiposity by proton magnetic resonance spectroscopy (1H-MRS) at the spine but not the femur. Osteoporos Int 26:2471–2478CrossRefPubMedPubMedCentral
32.
Zurück zum Zitat Bredella MA, Daley SM, Kalra MK et al (2015) Marrow adipose tissue quantification of the lumbar spine by using dual-energy CT and single-voxel 1H MR spectroscopy: a feasibility study. Radiology 277:230–235CrossRefPubMedPubMedCentral Bredella MA, Daley SM, Kalra MK et al (2015) Marrow adipose tissue quantification of the lumbar spine by using dual-energy CT and single-voxel 1H MR spectroscopy: a feasibility study. Radiology 277:230–235CrossRefPubMedPubMedCentral
34.
Zurück zum Zitat Blebea JS, Houseni M, Torigian DA et al (2007) Structural and functional imaging of normal bone marrow and evaluation of its age-related changes. Semin Nucl Med 37:185–194CrossRefPubMed Blebea JS, Houseni M, Torigian DA et al (2007) Structural and functional imaging of normal bone marrow and evaluation of its age-related changes. Semin Nucl Med 37:185–194CrossRefPubMed
35.
Zurück zum Zitat Liney GP, Bernard CP, Manton DJ et al (2007) Age, gender, and skeletal variation in bone marrow composition: a preliminary study at 3.0 tesla. J Magn Reson Imaging 26:787–793CrossRefPubMed Liney GP, Bernard CP, Manton DJ et al (2007) Age, gender, and skeletal variation in bone marrow composition: a preliminary study at 3.0 tesla. J Magn Reson Imaging 26:787–793CrossRefPubMed
36.
Zurück zum Zitat Schwartz AV (2015) Marrow fat and bone: review of clinical findings. Front Endocrinol 6:1–6CrossRef Schwartz AV (2015) Marrow fat and bone: review of clinical findings. Front Endocrinol 6:1–6CrossRef
37.
Zurück zum Zitat Devlin MJ, Cloutier AM, Thomas NA et al (2010) Caloric restriction leads to high marrow adiposity and low bone mass in growing mice. J Bone Miner Res 25:2078–2088CrossRefPubMedPubMedCentral Devlin MJ, Cloutier AM, Thomas NA et al (2010) Caloric restriction leads to high marrow adiposity and low bone mass in growing mice. J Bone Miner Res 25:2078–2088CrossRefPubMedPubMedCentral
38.
Zurück zum Zitat Fazeli PK, Bredella MA, Freedman L et al (2012) Marrow fat and preadipocyte factor-1 levels decrease with recovery in women with anorexia nervosa. J Bone Miner Res 27:1864–1871CrossRefPubMedPubMedCentral Fazeli PK, Bredella MA, Freedman L et al (2012) Marrow fat and preadipocyte factor-1 levels decrease with recovery in women with anorexia nervosa. J Bone Miner Res 27:1864–1871CrossRefPubMedPubMedCentral
39.
Zurück zum Zitat de Araújo IM, Salmon CE, Nahas AK et al (2017) Marrow adipose tissue spectrum in obesity and type 2 diabetes mellitus. Eur J Endocrinol 176:21–30CrossRefPubMed de Araújo IM, Salmon CE, Nahas AK et al (2017) Marrow adipose tissue spectrum in obesity and type 2 diabetes mellitus. Eur J Endocrinol 176:21–30CrossRefPubMed
40.
Zurück zum Zitat Schett G, Kiechl S, Redlich K et al (2004) Soluble RANKL and risk of nontraumatic fracture. JAMA 291:1108–1113CrossRefPubMed Schett G, Kiechl S, Redlich K et al (2004) Soluble RANKL and risk of nontraumatic fracture. JAMA 291:1108–1113CrossRefPubMed
41.
Zurück zum Zitat Vega D, Maalouf NM, Sakhaee K (2007) CLINICAL review #: the role of receptor activator of nuclear factor-kappaB (RANK)/RANK ligand/osteoprotegerin: clinical implications. J Clin Endocrinol Metab 92:4514–4521CrossRefPubMed Vega D, Maalouf NM, Sakhaee K (2007) CLINICAL review #: the role of receptor activator of nuclear factor-kappaB (RANK)/RANK ligand/osteoprotegerin: clinical implications. J Clin Endocrinol Metab 92:4514–4521CrossRefPubMed
42.
Zurück zum Zitat Cawthorn WP, Scheller EL, Leaman BS et al (2014) Bone marrow adipose tissue is an endocrine organ that contributes to increased circulating adiponectin during caloric restriction. Cell Metab 20:368–375CrossRefPubMedPubMedCentral Cawthorn WP, Scheller EL, Leaman BS et al (2014) Bone marrow adipose tissue is an endocrine organ that contributes to increased circulating adiponectin during caloric restriction. Cell Metab 20:368–375CrossRefPubMedPubMedCentral
43.
Zurück zum Zitat Pironi L, Callegari C, Cornia GL et al (1988) Lactose malabsorption in adult patients with Crohn’s disease. Am J Gastroenterol 83:1267–1271PubMed Pironi L, Callegari C, Cornia GL et al (1988) Lactose malabsorption in adult patients with Crohn’s disease. Am J Gastroenterol 83:1267–1271PubMed
44.
Zurück zum Zitat Dinca M, Fries W, Luisetto G et al (1999) Evolution of osteopenia in inflammatory bowel disease. Am J Gastroenterol 94:1292–1297CrossRefPubMed Dinca M, Fries W, Luisetto G et al (1999) Evolution of osteopenia in inflammatory bowel disease. Am J Gastroenterol 94:1292–1297CrossRefPubMed
45.
Zurück zum Zitat Arj A, Razavi Zade M, Yavari M et al (2016) Proton pump inhibitors use and change in bone mineral density. Int J Rheum Dis 19:864–868CrossRefPubMed Arj A, Razavi Zade M, Yavari M et al (2016) Proton pump inhibitors use and change in bone mineral density. Int J Rheum Dis 19:864–868CrossRefPubMed
Metadaten
Titel
Reduced bone mass and preserved marrow adipose tissue in patients with inflammatory bowel diseases in long-term remission
verfasst von
C. M. Bastos
I. M. Araújo
M. H. Nogueira-Barbosa
C. E. G. Salmon
F. J. A. de Paula
L. E. A. Troncon
Publikationsdatum
12.04.2017
Verlag
Springer London
Erschienen in
Osteoporosis International / Ausgabe 7/2017
Print ISSN: 0937-941X
Elektronische ISSN: 1433-2965
DOI
https://doi.org/10.1007/s00198-017-4014-3

Weitere Artikel der Ausgabe 7/2017

Osteoporosis International 7/2017 Zur Ausgabe

Arthropedia

Grundlagenwissen der Arthroskopie und Gelenkchirurgie. Erweitert durch Fallbeispiele, Videos und Abbildungen. 
» Jetzt entdecken

Notfall-TEP der Hüfte ist auch bei 90-Jährigen machbar

26.04.2024 Hüft-TEP Nachrichten

Ob bei einer Notfalloperation nach Schenkelhalsfraktur eine Hemiarthroplastik oder eine totale Endoprothese (TEP) eingebaut wird, sollte nicht allein vom Alter der Patientinnen und Patienten abhängen. Auch über 90-Jährige können von der TEP profitieren.

Arthroskopie kann Knieprothese nicht hinauszögern

25.04.2024 Gonarthrose Nachrichten

Ein arthroskopischer Eingriff bei Kniearthrose macht im Hinblick darauf, ob und wann ein Gelenkersatz fällig wird, offenbar keinen Unterschied.

Therapiestart mit Blutdrucksenkern erhöht Frakturrisiko

25.04.2024 Hypertonie Nachrichten

Beginnen ältere Männer im Pflegeheim eine Antihypertensiva-Therapie, dann ist die Frakturrate in den folgenden 30 Tagen mehr als verdoppelt. Besonders häufig stürzen Demenzkranke und Männer, die erstmals Blutdrucksenker nehmen. Dafür spricht eine Analyse unter US-Veteranen.

Ärztliche Empathie hilft gegen Rückenschmerzen

23.04.2024 Leitsymptom Rückenschmerzen Nachrichten

Personen mit chronischen Rückenschmerzen, die von einfühlsamen Ärzten und Ärztinnen betreut werden, berichten über weniger Beschwerden und eine bessere Lebensqualität.

Update Orthopädie und Unfallchirurgie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.