Abstract
Osteoporosis has become an increasingly recognized complication among patients with chronic liver disease (CLD). The aim of the present study was to assess the prevalence and risk factors of osteoporosis in patients with CLD (primary biliary cirrhosis and chronic viral hepatitis B or C patients) in comparison with a group of age- and sex-matched controls. Sixty-four patients with CLD (mean age 51.66 ± 11.54 years), 48 females and 16 males were included. Age- and sex-matched individuals from the general population served as controls. Osteoporosis was evaluated by dual energy X-ray absorptiometry (bone mineral density below −2.5 T score) at the lumbar spine (LS) and total hip (TH). Vertebral fractures were established by densitometric morphometry (vertebral fracture assessment). Bone turnover was assessed by intact parathyroid hormone, osteocalcin and C-telopeptides of type I collagen in the serum. Prevalence of osteoporosis in either the LS or the TH was 45.3%, twice as high as in the controls (19.6%) (RR 2.31, 95% CI 1.42–3.75, P < 0.001). Age, menopausal status, cirrhosis and advanced histological stage are not determinant factors for developing osteoporosis in patients with CLD. However, female sex, cholestasis, lower weight and height but not body mass index seem to play predominant role. Three (5.3%) patients had dorsal and LS fractures. It was concluded that osteoporosis is effectively a complication of CLD. Cholestasis in addition to female sex and lower weight and height are risk factors of osteoporosis in CLD.
Similar content being viewed by others
References
AGA Clinical Practice Committee (2003) AGA technical review on osteoporosis in hepatic disorders. Gastroenterology 125:941–966. doi:10.1016/S0016-5085(03)01062-X
Rouillard S, Lane NE (2001) Hepatic osteodystrophy. Hepatology 33(1):301–306. doi:10.1053/jhep.2001.20533
Ormarsdottir S, Ljunggren O, Mallmin H, Brahm H, Loof L (1999) Low body mass index and use of corticosteroids, but not cholestasis, are risk factors for osteoporosis in patients with chronic liver disease. J Hepatol 31:84–90. doi:10.1016/S0168-8278(99)80167-6
Hodgson SF, Dickson ER, Heinz WW, Johnson KA, Mann KG, Riggs BL (1985) Bone loss and reduced osteoblast function in primary biliary cirrhosis. Ann Intern Med 103:855–860
Diamond TH, Stiel D, Lunzer M, Mc Dowall D, Eckstein RP, Posen S (1989) Hepatic osteodystrophy. Static and dynamic bone histomorphometry and bone Gla-protein in 80 patients with chronic liver disease. Gastroenterology 96:213–221
El Maghraoui A, Guerboub AA, Achemlal L, Mounach A, Nouijai A, Ghazi M, Bezza A, Tazi MA (2006) Bone mineral density of the spine and femur in healthy Moroccan women. J Clin Densitom 9(4):454–460. doi:10.1016/j.jocd.2006.07.001
Ludwig J (1987) New concepts in biliary cirrhosis. Semin Liver Dis 7:293–301. doi:10.1055/s-2008-1040584
El Maghraoui A, Do Santos Zounon AA, Jroundi I, Nouijai A, Ghazi M, Achemlal L, Bezza A, Tazi MA, Abouqual R (2005) Reproducibility of bone mineral density measurements using dual X-ray absorptiometry in daily clinical practice. Osteoporos Int 16(12):1742–1748. doi:10.1007/s00198-005-1916-2
El Maghraoui A, Achemlal L, Bezza A (2006) Monitoring of dual energy X-ray absorptiometry measurement in clinical practice. J Clin Densitom 9(3):281–286. doi:10.1016/j.jocd.2006.03.014
El Maghraoui A, Guerboub AA, Mounach A, Ghozlani I, Nouijai A, Ghazi M, Achemlal L, Bezza A, Tazi MA (2007) Body mass index and gynecological factors as determinants of bone mass in healthy Moroccan postmenopausal women. Maturitas 56(4):375–382. doi:10.1016/j.maturitas.2006.10.004
World Health Organization Study Group (1994) Assessment of fracture risk and its application to screening for postmenopausal osteoporosis. World Health Organisation Technical Report Series, Geneva, 843 p
Duboeuf F, Bauer DC, Chapurlat RD, Dinten JMP, Delmas P (2005) Assessment of vertebral fracture using densitometric morphometry. J Clin Densitom 8(3):362–368. doi:10.1385/JCD:8:3:362
Vokes T, Bachman D, Baim S et al (2006) Vertebral fracture assessment: The 2005 ISCD Official Positions. J Clin Densitom 9(1):37–46. doi:10.1016/j.jocd.2006.05.006
Genant HK, Van Kuijk C, Nevitt M (1993) Vertebral fracture assessment using a semi-quantitative technique. J Bone Miner Res 8:1137–1148
Collier J (2007) Bone disorders in chronic liver disease. Hepatology 46:1271–1278. doi:10.1002/hep.21852
Diamond T, Stiel D, Lunzer M, Wilkinson M, Roche J, Posen S (1980) Osteoporosis and skeletal fractures in chronic liver disease. Gut 31:82–87. doi:10.1136/gut.31.1.82
Guanabens N, Pares A, Ros I, Caballeria L, Pons F, Vidal S et al (2005) Severity of cholestasis and advanced histological stage but not menopausal status are the major risk factors for osteoporosis in primary biliary cirrhosis. J Hepatol 42:573–577. doi:10.1016/j.jhep.2004.11.035
Gallejo-Rojo FJ, Gonzalez-Calvin JL, Munoz-Torres M, Mundi JL, Fernandez-Perez R, Rodrigo-Moneno D (1998) Bone mineral density, serum insulin like growth factor I and bone turnover markers in viral cirrhosis. Hepatology 28:695–699. doi:10.1002/hep.510280315
Guichelaar MMJ, Kendall R, Schmoll J, Malinchoc M, Hay JE (2006) Bone mineral density before and after OLT; long-term follow-up and predictive factors. Liver Transpl 12:1390–1402. doi:10.1002/lt.20874
Hay JE (1995) Bone disease in cholestatic liver disease. Gastroenterology 108:276–283. doi:10.1016/0016-5085(95)90033-0
Guichelaar M, Schmoll J, Malinchoc M, Hay EJ (2007) Fractures and avascular necrosis before and after orthotopic liver transplantation: long-term follow-up and predictive factors. Hepatology 46(4):1198–1207. doi:10.1002/hep.21805
Solaymani-Dodaran M, Card TR, Aithal GP, West J (2006) Fracture risk in people with primary biliary cirrhosis: a population-based cohort study. Gastroenterology 131:1752–1757. doi:10.1053/j.gastro.2006.09.012
Chen CC, Wang SS, Jeng FS, Lee SD (1996) Metabolic bone disease of liver cirrhosis: is it parallel to the clinical severity of the cirrhosis? J Gastroenterol Hepatol 11:417–421. doi:10.1111/j.1440-1746.1996.tb00284.x
Allali F, El Aichaoui S, Benyahya B, Khazani H, Saoud B, Abouqal R, Hajjaj-Hassouni N (2006) Hypovitaminosis D in a sunny country: relation to lifestyle, bone markers and bone mineral density. Ann Rheum Dis 65(Suppl 2):412
Kaymakoglu S, Okten A, Cakalogu Y, Boztas G, Besisik F, Tascioglu C et al (1995) Hypogonadism is not related to the etiology of liver cirrhosis. J Gastroenterol 30:745–750. doi:10.1007/BF02349641
Menon KVN, Angulo P, Weston S, Dickson ER, Lindor KD (2001) Bone disease in primary biliary cirrhosis: independent indicators and rate of progression. J Hepatol 35:316–323. doi:10.1016/S0168-8278(01)00144-1
Michaelsson K (1996) Screening for osteopenia and osteoporosis—selection by body composition. Osteoporos Int 6:120–126. doi:10.1007/BF01623934
Gabuzda GJ, Shear L (1970) Metabolism of dietary protein in hepatic cirrhosis. Nutritional and clinical considerations. Am J Clin Nutr 23:479–487
Bagur A, Mautalen C, Findor J, Sorda J, Somoza J (1998) Risk factors for the development of vertebral and total skeleton osteoporosis in patients with primary biliary cirrhosis. Calcif Tissue Int 63:385–390. doi:10.1007/s002239900545
Guanabens N, Pares A, Marinoso L et al (1990) Factors influencing the development of metabolic bone disease in primary biliary cirrhosis. Am J Gastroenterol 85:1356–1362
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. doi:10.1136/gut.31.1.82
Bonkovsky HL, Hawkins M, Steinberg K, Hersch T, Galambos JT, Henderson JM et al (1990) Prevalence and prediction of osteopenia in chronic liver disease. Hepatology 12:273–280. doi:10.1002/hep.1840120214
Mc Caughan GW, Feller RB (1994) Osteoporosis in chronic liver disease: pathogenesis, risk factors, and management. Dig Dis 12:223–231. doi:10.1159/000171456
Guañabens N, Parés A, Alvarez L et al (1998) Collagen-related markers of bone turnover reflect the severity of liver fibrosis in patients with primary biliary cirrhosis. J Bone Miner Res 13:731–738. doi:10.1359/jbmr.1998.13.4.731
Pares A, Guanabenes N, Rhodes J (2005) Gene polymorphisms as predictors of decreased bone mineral density and osteoporosis in primary biliary cirrhosis. Eur J Gastroenterol Hepatol 17:331–335
Parés A, Guañabens N, Alvarez L et al (2001) Collagen type I and vitamin D receptor gene polymorphisms and bone mass in primary biliary cirrhosis. Hepatology 33:554–560. doi:10.1053/jhep.2001.22758
Moschen AR, Kaser A, Stadlmann S, Millonig G, Kaser S, Muhlleschner P et al (2005) The RANKL/OPG system and bone mineral density in patients with chronic liver disease. J Hepatol 43:973–983. doi:10.1016/j.jhep.2005.05.034
Szalay F, Hegedus D, Lakatos PL et al (2003) High serum osteoprotegerin and low RANKL in primary biliary cirrhosis. J Hepatol 38:395–400. doi:10.1016/S0168-8278(02)00435-X
Janes CH, Dickson ER, Okazaki R, Bonde S, McDonagh AF, Riggs LB (1995) Role of hyperbilirubinemia in the impairment of osteoblast proliferation associated with cholestatic jaundice. J Clin Invest 95:2581–2586. doi:10.1172/JCI117959
Möller S, Becker U (1992) Insulin-like growth factor 1 and growth hormone in chronic liver disease. Dig Dis 10:239–248. doi:10.1159/000171362
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Wariaghli, G., Mounach, A., Achemlal, L. et al. Osteoporosis in chronic liver disease: a case–control study. Rheumatol Int 30, 893–899 (2010). https://doi.org/10.1007/s00296-009-1071-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00296-009-1071-8