Bone microarchitecture and bone turnover in hepatic cirrhosis.
Aged
Biomarkers
/ blood
Bone Density
Bone Remodeling
/ physiology
Cancellous Bone
/ diagnostic imaging
Case-Control Studies
Cortical Bone
/ diagnostic imaging
Female
Humans
Liver Cirrhosis
/ diagnostic imaging
Liver Cirrhosis, Alcoholic
/ diagnostic imaging
Male
Middle Aged
Porosity
Radius
/ diagnostic imaging
Tibia
/ diagnostic imaging
Tomography, X-Ray Computed
/ methods
Weight-Bearing
/ physiology
Alcoholic liver disease
Cortical bone
Hepatic cirrhosis
Trabecular microarchitecture
Journal
Osteoporosis international : a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA
ISSN: 1433-2965
Titre abrégé: Osteoporos Int
Pays: England
ID NLM: 9100105
Informations de publication
Date de publication:
Jun 2019
Jun 2019
Historique:
received:
06
06
2018
accepted:
21
01
2019
pubmed:
23
2
2019
medline:
7
1
2020
entrez:
22
2
2019
Statut:
ppublish
Résumé
Liver cirrhosis leads to bone loss. To date, information on bone quality (three-dimensional microarchitecture) and, thus, bone strength is scarce. We observed decreased bone quality at both assessed sites, independent of disease severity. Therefore, all patients should undergo early-stage screening for osteoporosis. Recent studies found low bone mineral density in cirrhosis, but data on bone microstructure are scarce. This study assessed weight-bearing and non-weight-bearing bones in patients with cirrhosis and healthy controls. The primary objective was to evaluate trabecular and cortical microarchitecture. This was a single-center study in patients with recently diagnosed hepatic cirrhosis. Thirty-two patients and 32 controls participated in this study. After determining the type of cirrhosis, the parameters of bone microarchitecture were assessed by high-resolution peripheral quantitative computed tomography. Both cortical and trabecular microarchitectures showed significant alterations. At the radius, trabecular bone volume fraction was 17% lower (corrected p = 0.028), and, at the tibia, differences were slightly more pronounced. Trabecular bone volume fraction was 19% lower (p = 0.024), cortical bone mineral density 7% (p = 0.007), and cortical thickness 28% (p = 0.001), while cortical porosity was 32% higher (p = 0.023), compared to controls. Areal bone mineral density was lower (lumbar spine - 13%, total hip - 11%, total body - 9%, radius - 17%, and calcaneus - 26%). There was no correlation between disease severity and microarchitecture. Areal bone mineral density (aBMD) measured by dual-energy X-ray absorptiometry (DXA) correlated well with parameters of cortical and trabecular microarchitecture. Hepatic cirrhosis deteriorates both trabecular and cortical microarchitecture, regardless of disease severity. Areal bone mineral density is diminished at all sites as a sign of generalized affection. In patients with hepatic cirrhosis, regardless of its origin or disease severity, aBMD measurements are an appropriate tool for osteologic screening.
Identifiants
pubmed: 30788527
doi: 10.1007/s00198-019-04870-6
pii: 10.1007/s00198-019-04870-6
pmc: PMC6546655
doi:
Substances chimiques
Biomarkers
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1195-1204Références
Guarino M, Loperto I, Camera S, Cossiga V, di Somma C, Colao A, Caporaso N, Morisco F (2016) Osteoporosis across chronic liver disease. Osteoporos Int 27:1967–1977. https://doi.org/10.1007/s00198-016-3512-z
doi: 10.1007/s00198-016-3512-z
pubmed: 26846777
Santos LAA, Lima TB, Augusti L, Franzoni LC, Yamashiro FS, Bolfi F, Nunes VS, Dorna MS, de Oliveira CV, Caramori CA, Silva GF, Romeiro FG (2016) Handgrip strength as a predictor of bone mineral density in outpatients with cirrhosis. J Gastroenterol Hepatol 31:229–234. https://doi.org/10.1111/jgh.13062
doi: 10.1111/jgh.13062
pubmed: 26212461
Lupoli R, Di Minno A, Spadarella G et al (2016) The risk of osteoporosis in patients with liver cirrhosis: a meta-analysis of literature studies. Clin Endocrinol 84:30–38. https://doi.org/10.1111/cen.12780
doi: 10.1111/cen.12780
Culafić D, Djonic D, Culafic-Vojinovic V, Ignjatovic S, Soldatovic I, Vasic J, Beck TJ, Djuric M (2015) Evidence of degraded BMD and geometry at the proximal femora in male patients with alcoholic liver cirrhosis. Osteoporos Int 26:253–259. https://doi.org/10.1007/s00198-014-2849-4
doi: 10.1007/s00198-014-2849-4
pubmed: 25172381
Burghardt AJ, Issever AS, Schwartz AV, Davis KA, Masharani U, Majumdar S, Link TM (2010) High-resolution peripheral quantitative computed tomographic imaging of cortical and trabecular bone microarchitecture in patients with type 2 diabetes mellitus. J Clin Endocrinol Metab 95:5045–5055. https://doi.org/10.1210/jc.2010-0226
doi: 10.1210/jc.2010-0226
pubmed: 20719835
pmcid: 2968722
Guichelaar MMJ, Malinchoc M, Sibonga J et al (2002) Bone metabolism in advanced cholestatic liver disease: analysis by bone histomorphometry. Hepatology 36:895–903. https://doi.org/10.1053/jhep.2002.36357
doi: 10.1053/jhep.2002.36357
pubmed: 12297836
Jorge-Hernandez JA, Gonzalez-Reimers CE, Torres-Ramirez A, Santolaria-Fernandez F, Gonzalez-Garcia C, Batista-Lopez JN, Pestana-Pestana M, Hernandez-Nieto L (1988) Bone changes in alcoholic liver cirrhosis—a histomorphometrical analysis of 52 cases. Dig Dis Sci 33:1089–1095. https://doi.org/10.1007/BF01535783
doi: 10.1007/BF01535783
pubmed: 3044713
Cohen A, Dempster DW, Müller R, Guo XE, Nickolas TL, Liu XS, Zhang XH, Wirth AJ, van Lenthe GH, Kohler T, McMahon DJ, Zhou H, Rubin MR, Bilezikian JP, Lappe JM, Recker RR, Shane E (2010) Assessment of trabecular and cortical architecture and mechanical competence of bone by high-resolution peripheral computed tomography: comparison with transiliac bone biopsy. Osteoporos Int 21:263–273. https://doi.org/10.1007/s00198-009-0945-7
doi: 10.1007/s00198-009-0945-7
pubmed: 19455271
Boutroy S, Bouxsein ML, Munoz F, Delmas PD (2005) In vivo assessment of trabecular bone microarchitecture by high-resolution peripheral quantitative computed tomography. J Clin Endocrinol Metab 90:6508–6515. https://doi.org/10.1210/jc.2005-1258
doi: 10.1210/jc.2005-1258
pubmed: 16189253
Kroker A, Plett R, Nishiyama KK, McErlain DD, Sandino C, Boyd SK (2017) Distal skeletal tibia assessed by HR-pQCT is highly correlated with femoral and lumbar vertebra failure loads. J Biomech 59:43–49. https://doi.org/10.1016/j.jbiomech.2017.05.011
doi: 10.1016/j.jbiomech.2017.05.011
pubmed: 28558915
O’Shea RS, Dasarathy S, McCullough AJ et al (2010) Alcoholic liver disease. Hepatology 51:307–328. https://doi.org/10.1002/hep.23258
doi: 10.1002/hep.23258
pubmed: 20034030
Chalasani N, Younossi Z, Lavine JE, Diehl AM, Brunt EM, Cusi K, Charlton M, Sanyal AJ (2012) The diagnosis and management of non-alcoholic fatty liver disease: practice guideline by the American Association for the Study of Liver Diseases, American College of Gastroenterology, and the American Gastroenterological Association. Hepatology 55:2005–2023. https://doi.org/10.1002/hep.25762
doi: 10.1002/hep.25762
pubmed: 22488764
Hind K, Oldroyd B, Truscott JG (2010) In vivo precision of the GE Lunar iDXA densitometer for the measurement of total-body, lumbar spine, and femoral bone mineral density in adults. J Clin Densitom 13:413–417. https://doi.org/10.1016/j.jocd.2010.06.002
doi: 10.1016/j.jocd.2010.06.002
pubmed: 20705494
Thorpe JA, Steel SA (2006) The DXL Calscan heel densitometer: evaluation and diagnostic thresholds. Br J Radiol 79:336–341. https://doi.org/10.1259/bjr/22191429
doi: 10.1259/bjr/22191429
pubmed: 16585728
Stellon AJ, Webb A, Compston J, Williams R (1987) Low bone turnover state in primary biliary cirrhosis. Hepatology 7:137–142. https://doi.org/10.1002/hep.1840070127
doi: 10.1002/hep.1840070127
pubmed: 3804193
Diamond TH, Stiel D, Lunzer M, McDowall D, Eckstein RP, Posen S (1989) Hepatic osteodystrophy. Static and dynamic bone histomorphometry and serum bone Gla-protein in 80 patients with chronic liver disease. Gastroenterology 96:213–221
doi: 10.1016/0016-5085(89)90783-X
pubmed: 2783312
Sornay-Rendu E, Boutroy S, Munoz F, Delmas PD (2007) 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 22:425–433. https://doi.org/10.1359/JBMR.061206
doi: 10.1359/jbmr.061206
pubmed: 17181395
Nickolas TL, Stein E, Cohen A, Thomas V, Staron RB, McMahon DJ, Leonard MB, Shane E (2010) Bone mass and microarchitecture in CKD patients with fracture. J Am Soc Nephrol 21:1371–1380. https://doi.org/10.1681/ASN.2009121208
doi: 10.1681/ASN.2009121208
pubmed: 20395370
pmcid: 2938588
Patsch JM, Burghardt AJ, Yap SP, Baum T, Schwartz AV, Joseph GB, Link TM (2013) Increased cortical porosity in type 2 diabetic postmenopausal women with fragility fractures. J Bone Miner Res 28:313–324. https://doi.org/10.1002/jbmr.1763
doi: 10.1002/jbmr.1763
pubmed: 22991256
pmcid: 3534818
Mansueto P, Carroccio A, Seidita A, di Fede G, Craxì A (2013) Osteodystrophy in chronic liver diseases. Intern Emerg Med 8:377–388. https://doi.org/10.1007/s11739-012-0753-5
doi: 10.1007/s11739-012-0753-5
pubmed: 22241574
Wibaux C, Legroux-Gerot I, Dharancy S, Boleslawski E, Declerck N, Canva V, Mathurin P, Pruvot FR, Cortet B (2011) Assessing bone status in patients awaiting liver transplantation. Joint Bone Spine 78:387–391. https://doi.org/10.1016/j.jbspin.2011.03.001
doi: 10.1016/j.jbspin.2011.03.001
pubmed: 21565541
Diamond T, Stiel D, Lunzer M, Wilkinson M, Roche J, Posen S (1990) Osteoporosis and skeletal fractures in chronic liver disease. Gut 31:82–87. https://doi.org/10.1136/gut.31.1.82
doi: 10.1136/gut.31.1.82
pubmed: 2318434
pmcid: 1378345
Muschitz C, Kocijan R, Haschka J, Pahr D, Kaider A, Pietschmann P, Hans D, Muschitz GK, Fahrleitner-Pammer A, Resch H (2015) TBS reflects trabecular microarchitecture in premenopausal women and men with idiopathic osteoporosis and low-traumatic fractures. Bone 79:259–266. https://doi.org/10.1016/j.bone.2015.06.007
doi: 10.1016/j.bone.2015.06.007
pubmed: 26092650
Kocijan R, Muschitz C, Haschka J, Hans D, Nia A, Geroldinger A, Ardelt M, Wakolbinger R, Resch H (2015) Bone structure assessed by HR-pQCT, TBS and DXL in adult patients with different types of osteogenesis imperfecta. Osteoporos Int 26:2431–2440. https://doi.org/10.1007/s00198-015-3156-4
doi: 10.1007/s00198-015-3156-4
pubmed: 25956285
Pérez-Sáez MJ, Herrera S, Prieto-Alhambra D, Vilaplana L, Nogués X, Vera M, Redondo-Pachón D, Mir M, Güerri R, Crespo M, Díez-Pérez A, Pascual J (2017) Bone density, microarchitecture, and material strength in chronic kidney disease patients at the time of kidney transplantation. Osteoporos Int 28:2723–2727. https://doi.org/10.1007/s00198-017-4065-5
doi: 10.1007/s00198-017-4065-5
pubmed: 28497224
Kim JH, Choi HJ, Ku EJ, Kim KM, Kim SW, Cho NH, Shin CS (2015) Trabecular bone score as an indicator for skeletal deterioration in diabetes. J Clin Endocrinol Metab 100:475–482. https://doi.org/10.1210/jc.2014-2047
doi: 10.1210/jc.2014-2047
pubmed: 25368976
Sens C, Altrock E, Rau K, Klemis V, von Au A, Pettera S, Uebel S, Damm T, Tiwari S, Moser M, Nakchbandi IA (2017) An O-glycosylation of fibronectin mediates hepatic osteodystrophy through α4β1 integrin. J Bone Miner Res 32:70–81. https://doi.org/10.1002/jbmr.2916
doi: 10.1002/jbmr.2916
pubmed: 27427791
Nakchbandi IA, van der Merwe SW (2009) Current understanding of osteoporosis associated with liver disease. Nat Rev Gastroenterol Hepatol 6:660–670. https://doi.org/10.1038/nrgastro.2009.166
doi: 10.1038/nrgastro.2009.166
pubmed: 19881518
Hodgson SF, Dickson ER, Eastell R, Eriksen EF, Bryant SC, Riggs BL (1993) Rates of cancellous bone remodeling and turnover in osteopenia associated with primary biliary cirrhosis. Bone 14:819–827. https://doi.org/10.1016/8756-3282(93)90310-7
doi: 10.1016/8756-3282(93)90310-7
pubmed: 8155404
Foresta C, Schipilliti M, Ciarleglio FA, Lenzi A, D’Amico D (2008) Male hypogonadism in cirrhosis and after liver transplantation. J Endocrinol Investig 31:470–478. https://doi.org/10.1007/BF03346393
doi: 10.1007/BF03346393
Guichelaar MMJ, Kendall R, Malinchoc M, Hay JE (2006) Bone mineral density before and after OLT: long-term follow-up and predictive factors. Liver Transpl 12:1390–1402. https://doi.org/10.1002/lt.20874
doi: 10.1002/lt.20874
pubmed: 16933236
Campos-Obando N, Koek WNH, Hooker ER, van der Eerden BCJ, Pols HA, Hofman A, van Leeuwen JPTM, Uitterlinden AG, Nielson CM, Zillikens MC (2017) Serum phosphate is associated with fracture risk: the Rotterdam Study and MrOS. J Bone Miner Res 32:1182–1193. https://doi.org/10.1002/jbmr.3094
doi: 10.1002/jbmr.3094
pubmed: 28177140
pmcid: 5466477
European Food Safety Authority (2013) Assessment of one published review on health risks associated with phosphate additives in food. EFSA J 11:3444. https://doi.org/10.2903/j.efsa.2013.3444
doi: 10.2903/j.efsa.2013.3444
Monegal A, Navasa M, Peris P, Alvarez L, Pons F, Rodés J, Guañabens N (2007) Serum osteoprotegerin and its ligand in cirrhotic patients referred for orthotopic liver transplantation: relationship with metabolic bone disease. Liver Int 27:492–497. https://doi.org/10.1111/j.1478-3231.2007.01448.x
doi: 10.1111/j.1478-3231.2007.01448.x
pubmed: 17403189
Wariaghli G, Allali F, El Maghraoui A, Hajjaj-Hassouni N (2010) Osteoporosis in patients with primary biliary cirrhosis. Eur J Gastroenterol Hepatol 22:1397–1401. https://doi.org/10.1097/MEG.0b013e3283405939
doi: 10.1097/MEG.0b013e3283405939
pubmed: 20926953
Schmidt T, Schmidt C, Schmidt FN, Butscheidt S, Mussawy H, Hubert J, Hawellek T, Oehler N, Barvencik F, Lohse AW, Schinke T, Schramm C, Amling M, Rolvien T (2018) Disease duration and stage influence bone microstructure in patients with primary biliary cholangitis. J Bone Miner Res 33:1011–1019. https://doi.org/10.1002/jbmr.3410
doi: 10.1002/jbmr.3410
pubmed: 29470841