Bone microarchitecture in patients with autoimmune hepatitis.
AUTOIMMUNE HEPATITIS
AUTOIMMUNE LIVER DISEASE
BONE MICROARCHITECTURE
HR-pQCT
OSTEOPOROSIS
Journal
Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research
ISSN: 1523-4681
Titre abrégé: J Bone Miner Res
Pays: United States
ID NLM: 8610640
Informations de publication
Date de publication:
07 2021
07 2021
Historique:
revised:
22
02
2021
received:
21
11
2020
accepted:
11
03
2021
pubmed:
17
3
2021
medline:
10
8
2021
entrez:
16
3
2021
Statut:
ppublish
Résumé
In patients with autoimmune hepatitis (AIH), osteoporosis represents a common extrahepatic complication, which we recently showed by an assessment of areal bone mineral density (aBMD) via dual-energy x-ray absorptiometry (DXA). However, it is well established that bone quality and fracture risk does not solely depend on aBMD, but also on bone microarchitecture. It is currently not known whether AIH patients exhibit a site-specific or compartment-specific deterioration in the skeletal microarchitecture. In order to assess potential geometric, volumetric, and microarchitectural changes, high-resolution peripheral quantitative computed tomography (HR-pQCT) measurements were performed at the distal radius and distal tibia in female patients with AIH (n = 51) and compared to age-matched female healthy controls (n = 32) as well as to female patients with AIH/primary biliary cholangitis (PBC) overlap syndrome (n = 25) and female patients with PBC alone (PBC, n = 36). DXA at the lumbar spine and hip, clinical characteristics, transient elastography (FibroScan) and laboratory analyses were also included in this analysis. AIH patients showed a predominant reduction of cortical thickness (Ct.Th) in the distal radius and tibia compared to healthy controls (p < .0001 and p = .003, respectively). In contrast, trabecular parameters such as bone volume fraction (BV/TV) did not differ significantly at the distal radius (p = .453) or tibia (p = .508). Linear regression models revealed significant negative associations between age and Ct.Th (95% confidence interval [CI], -14 to -5 μm/year, p < .0001), but not between liver stiffness, cumulative prednisolone dose (even after an adjustment for age), or disease duration with bone microarchitecture. The duration of high-dose prednisolone (≥7.5 mg) was negatively associated with trabecular thickness (Tb.Th) at the distal radius. No differences in bone microarchitecture parameters between AIH, AIH/PBC, and PBC could be detected. In conclusion, AIH patients showed a severe age-dependent deterioration of the cortical bone microarchitecture, which is most likely the major contribution to the observed increased fracture risk in these patients. © 2021 The Authors. Journal of Bone and Mineral Research published by Wiley Periodicals LLC on behalf of American Society for Bone and Mineral Research (ASBMR).
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1316-1325Informations de copyright
© 2021 The Authors. Journal of Bone and Mineral Research published by Wiley Periodicals LLC on behalf of American Society for Bone and Mineral Research (ASBMR).
Références
Lamers MM, van Oijen MG, Pronk M, Drenth JP. Treatment options for autoimmune hepatitis: a systematic review of randomized controlled trials. J Hepatol. 2010;53(1):191-198.
Gronbaek L, Vilstrup H, Jepsen P. Autoimmune hepatitis in Denmark: incidence, prevalence, prognosis, and causes of death. A nationwide registry-based cohort study. J Hepatol. 2014;60(3):612-617.
Krawitt EL. Autoimmune hepatitis. N Engl J Med. 2006;354(1):54-66.
Manns MP, Lohse AW, Vergani D. Autoimmune hepatitis-update 2015. J Hepatol. 2015;62(1 Suppl):S100-S111.
Trivedi PJ, Hubscher SG, Heneghan M, Gleeson D, Hirschfield GM. Grand round: autoimmune hepatitis. J Hepatol. 2019;70(4):773-784.
Heneghan MA, Yeoman AD, Verma S, Smith AD, Longhi MS. Autoimmune hepatitis. Lancet. 2013;382(9902):1433-1144.
Johnson PJ, McFarlane IG. Meeting report: International Autoimmune Hepatitis Group. Hepatology. 1993;18(4):998-1005.
Trivedi PJ, Hirschfield GM. Treatment of autoimmune liver disease: current and future therapeutic options. Ther Adv Chronic Dis. 2013;4(3):119-141.
Verma S, Gunuwan B, Mendler M, Govindrajan S, Redeker A. Factors predicting relapse and poor outcome in type I autoimmune hepatitis: role of cirrhosis development, patterns of transaminases during remission and plasma cell activity in the liver biopsy. Am J Gastroenterol. 2004;99(8):1510-1516.
Boberg KM, Chapman RW, Hirschfield GM, et al. Overlap syndromes: the International Autoimmune Hepatitis Group (IAIHG) position statement on a controversial issue. J Hepatol. 2011;54(2):374-385.
Menon KV, Angulo P, Weston S, Dickson ER, Lindor KD. Bone disease in primary biliary cirrhosis: independent indicators and rate of progression. J Hepatol. 2001;35(3):316-323.
Schmidt T, Schwinge D, Rolvien T, et al. Th17 cell frequency is associated with low bone mass in primary sclerosing cholangitis. J Hepatol. 2019;70(5):941-953.
Wariaghli G, Allali F, El Maghraoui A, Hajjaj-Hassouni N. Osteoporosis in patients with primary biliary cirrhosis. Eur J Gastroenterol Hepatol. 2010;22(12):1397-1401.
van den Brand FF, van der Veen KS, Lissenberg-Witte BI, et al. Adverse events related to low dose corticosteroids in autoimmune hepatitis. Aliment Pharmacol Ther. 2019;50(10):1120-1126.
Schmidt T, Schmidt C, Strahl A, et al. A system to determine risk of osteoporosis in patients with autoimmune hepatitis. Clin Gastroenterol Hepatol. 2020;18(1):226-233.e3.
Rand T, Seidl G, Kainberger F, et al. Impact of spinal degenerative changes on the evaluation of bone mineral density with dual energy X-ray absorptiometry (DXA). Calcif Tissue Int. 1997;60(5):430-433.
Boutroy S, Khosla S, Sornay-Rendu E, et al. Microarchitecture and peripheral BMD are impaired in postmenopausal white women with fracture independently of total hip T-score: an international multicenter study. J Bone Miner Res. 2016;31(6):1158-1166.
Nishiyama KK, Shane E. Clinical imaging of bone microarchitecture with HR-pQCT. Curr Osteoporos Rep. 2013;11(2):147-155.
Sornay-Rendu E, Boutroy S, Munoz F, Delmas PD. Alterations of cortical and trabecular architecture are associated with fractures in postmenopausal women, partially independent of decreased BMD measured by DXA: the OFELY study. J Bone Miner Res. 2007;22(3):425-433.
Stone KL, Seeley DG, Lui LY, et al. BMD at multiple sites and risk of fracture of multiple types: long-term results from the Study of Osteoporotic Fractures. J Bone Miner Res. 2003;18(11):1947-1954.
Schmidt T, Schmidt C, Schmidt FN, et al. Disease duration and stage influence bone microstructure in patients with primary biliary cholangitis. J Bone Miner Res. 2018;33(6):1011-1019.
European Association for the Study of the Liver. EASL Clinical Practice Guidelines: autoimmune hepatitis. J Hepatol. 2015;63(4):971-1004.
Hartl J, Denzer U, Ehlken H, et al. Transient elastography in autoimmune hepatitis: timing determines the impact of inflammation and fibrosis. J Hepatol. 2016;65(4):769-775.
Milovanovic P, Adamu U, Simon MJ, et al. Age- and sex-specific bone structure patterns portend bone fragility in radii and tibiae in relation to osteodensitometry: a high-resolution peripheral quantitative computed tomography study in 385 individuals. J Gerontol A Biol Sci Med Sci. 2015;70(10):1269-1275.
Pialat JB, Burghardt AJ, Sode M, Link TM, Majumdar S. Visual grading of motion induced image degradation in high resolution peripheral computed tomography: impact of image quality on measures of bone density and micro-architecture. Bone. 2012;50(1):111-118.
Whittier DE, Boyd SK, Burghardt AJ, et al. Guidelines for the assessment of bone density and microarchitecture in vivo using high-resolution peripheral quantitative computed tomography. Osteoporos Int. 2020;31(9):1607-1627.
Burt LA, Liang Z, Sajobi TT, Hanley DA, Boyd SK. Sex- and site-specific normative data curves for HR-pQCT. J Bone Miner Res. 2016;31(11):2041-2047.
Bala Y, Zebaze R, Seeman E. Role of cortical bone in bone fragility. Curr Opin Rheumatol. 2015;27(4):406-413.
Mussawy H, Ferrari G, Schmidt FN, et al. Changes in cortical microarchitecture are independent of areal bone mineral density in patients with fragility fractures. Injury. 2017;48(11):2461-2465.
Nicks KM, Amin S, Atkinson EJ, Riggs BL, Melton LJ 3rd, Khosla S. Relationship of age to bone microstructure independent of areal bone mineral density. J Bone Miner Res. 2012;27(3):637-644.
Zebaze RM, Ghasem-Zadeh A, Bohte A, et al. Intracortical remodelling and porosity in the distal radius and post-mortem femurs of women: a cross-sectional study. Lancet. 2010;375(9727):1729-1736.
Kendler DL, Roux C, Benhamou CL, et al. Effects of denosumab on bone mineral density and bone turnover in postmenopausal women transitioning from alendronate therapy. J Bone Miner Res. 2010;25(1):72-81.
Arase Y, Tsuruya K, Hirose S, et al. Efficacy and safety of 3-year denosumab therapy for osteoporosis in patients with autoimmune liver diseases. Hepatology. 2020;71(2):757-759.
Kocijan R, Finzel S, Englbrecht M, Engelke K, Rech J, Schett G. Decreased quantity and quality of the periarticular and nonperiarticular bone in patients with rheumatoid arthritis: a cross-sectional HR-pQCT study. J Bone Miner Res. 2014;29(4):1005-1014.
Maggiore G, De Benedetti F, Massa M, Pignatti P, Martini A. Circulating levels of interleukin-6, interleukin-8, and tumor necrosis factor-alpha in children with autoimmune hepatitis. J Pediatr Gastroenterol Nutr. 1995;20(1):23-27.
Thomas-Dupont P, Remes-Troche JM, Izaguirre-Hernandez IY, et al. Elevated circulating levels of IL-21 and IL-22 define a cytokine signature profile in type 2 autoimmune hepatitis patients. Ann Hepatol. 2016;15(4):550-558.
Okamoto K, Nakashima T, Shinohara M, et al. Osteoimmunology: the conceptual framework unifying the immune and skeletal systems. Physiol Rev. 2017;97(4):1295-1349.
Takayanagi H. Osteoimmunology: shared mechanisms and crosstalk between the immune and bone systems. Nat Rev Immunol. 2007;7(4):292-304.
Gravallese EM, Schett G. Effects of the IL-23-IL-17 pathway on bone in spondyloarthritis. Nat Rev Rheumatol. 2018;14(11):631-640.
Zhao L, Tang Y, You Z, et al. Interleukin-17 contributes to the pathogenesis of autoimmune hepatitis through inducing hepatic interleukin-6 expression. PLoS One. 2011;6(4):e18909.
Alvarez F, Berg PA, Bianchi FB, et al. International Autoimmune Hepatitis Group Report: review of criteria for diagnosis of autoimmune hepatitis. J Hepatol. 1999;31(5):929-938.
Canalis E, Delany AM. Mechanisms of glucocorticoid action in bone. Ann N Y Acad Sci. 2002;966:73-81.
Frenkel B, White W, Tuckermann J. Glucocorticoid-induced osteoporosis. Adv Exp Med Biol. 2015;872:179-215.
Sutter S, Nishiyama KK, Kepley A, et al. Abnormalities in cortical bone, trabecular plates, and stiffness in postmenopausal women treated with glucocorticoids. J Clin Endocrinol Metab. 2014;99(11):4231-4240.
Poordad F. Diagnosis, treatment, and monitoring of patients with primary biliary cholangitis. Gastroenterol Hepatol (N Y). 2016;12(9):561-564.
Xi L, Song Y, Wu W, et al. Investigation of bone matrix composition, architecture and mechanical properties reflect structure-function relationship of cortical bone in glucocorticoid induced osteoporosis. Bone. 2020;136:115334.
Chiba K, Okazaki N, Kurogi A, et al. Precision of second-generation high-resolution peripheral quantitative computed tomography: intra- and intertester reproducibilities and factors involved in the reproducibility of cortical porosity. J Clin Densitom. 2018;21(2):295-302.
Tjong W, Kazakia GJ, Burghardt AJ, Majumdar S. The effect of voxel size on high-resolution peripheral computed tomography measurements of trabecular and cortical bone microstructure. Med Phys. 2012;39(4):1893-1903.