Skip to main content
Log in

Primary biliary cirrhosis and osteoporosis: a case-control study

  • Original Article
  • Published:
Journal of Bone and Mineral Metabolism Aims and scope Submit manuscript

Abstract

Osteoporosis is a common complication of chronic liver disease, from cholestatic disorders to autoimmune, alcoholic, and posthepatitic cirrhosis. Osteoporosis appears more striking in patients with primary biliary cirrhosis (PBC) because the disease usually affects elderly women, who are naturally prone to osteoporosis. Our aims were (1) to compare the prevalence of osteoporosis (T-score ≤2.5 SD) between PBC patients and a group of age-and sex-matched controls consisting of healthy subjects from the general population; and (2) to identify the main risk factors for the development of bone loss. Thirty-three women with PBC (mean age, 47.3 ± 10.4 years) and 66 healthy subjects were enrolled in the study. Bone mineral density (BMD) was assessed at the lumbar spine by dual-photon X-ray absorptiometry. Bone metabolism was evaluated by measuring serum calcium corrected for serum albumin, 25-hydroxyvitamin D (25-OH vit D), parathyroid hormone, and osteocalcin. Vertebral fractures were analyzed using vertebral fracture assessment (VFA). The mean T-score was lower in the PBC group compared to healthy controls, with a significant statistical difference (−2.39 ± 0.93 and −1.47 ± 0.99 in lumbar spine and total hip, respectively, in the PBC group versus −0.99 ± 0.51 and −0.56 ± 1.14 in healthy controls (P < 0.001). The prevalence of osteoporosis was 51.5% in the PBC group versus 22.7% in healthy controls with a statistically significant difference (P = 0.004). BMD of the PBC group was significantly correlated positively with body mass index (BMI) and 25-OH vit D, and negatively with menopausal status, duration of disease, and parathyroid hormone (PTH) levels. Vertebral fractures were present in 9% of the patients. We found that osteoporosis is more prevalent in women with PBC than in the general population. BMI, menopausal status, duration of the disease, and vitamin D deficiency are the main risk factors for osteoporosis in this liver disease.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Eastell R, Dickson ER, Hodgson SF, Wiesner RH, Porayko MK, Wahner HW, Cedel SL, Riggs BL, Krom RA (1991) Rates of vertebral bone loss before and after liver transplantation in patients with primary biliary cirrhosis. Hepatology 14:296–300

    PubMed  CAS  Google Scholar 

  2. Lindor KD (1993) Management of osteopenia of liver disease with special emphasis on primary biliary cirrhosis. Semin Liver Dis 13:367–373

    PubMed  CAS  Google Scholar 

  3. Hay JE (1995) Bone disease in cholestatic liver disease. Gastroenterology 108:276–283

    Article  PubMed  CAS  Google Scholar 

  4. Guañabens N, Parés A, Mariñoso L, Brancós MA, Piera C, Serrano S, Rivera F, Rodés J (1990) Factors influencing the development of metabolic bone disease in primary biliary cirrhosis. Am J Gastroenterol 85:1356–1362

    PubMed  Google Scholar 

  5. Solerio E, Isaia G, Innarella R, Di Stefano M, Farina M, Borghesio E, Framarin L, Rizzetto M, Rosina F (2003) Osteoporosis: still a typical complication of primary biliary cirrhosis? Dig Liver Dis 35:339–346

    Article  PubMed  CAS  Google Scholar 

  6. AGA Technical Review on Osteoporosis in Hepatic Disorders (2003) Gastroenterology 125:941–966

    Article  Google Scholar 

  7. Hodgson SF, Dickson ER, Eastell R, Eriksen EF, Bryant SC, Riggs BL (1993) Rates of cancellous bone remodelling and turnover in osteopenia associated with primary biliary cirrhosis. Bone (NY) 14:819–827

    CAS  Google Scholar 

  8. Hodgson SF, Dickson ER, Wahner HW, Johnson KA, Mann KG, Riggs BL (1985) Bone loss and reduced osteoblast function in primary biliary cirrhosis. Ann Intern Med 103:855–860

    PubMed  CAS  Google Scholar 

  9. Janes CH, Dickson ER, Okazaki R, Bonde S, McDonagh AF, Riggs BL (1995) Role of hyperbilirubinemia in the impairment of osteoblast proliferation associated with cholestatic jaundice. J Clin Invest 95:2581–2586

    Article  PubMed  CAS  Google Scholar 

  10. Parés A, Guañabens N, Alvarez L, De Osaba MJ, Oriola J, Pons F, Caballería L, Monegal A, Salvador G, Jo J, Peris P, Rivera F, Ballesta AM, Rodés J (2001) Collagen type I a1 and vitamin D receptor gene polymorphisms and bone mass in primary biliary cirrhosis. Hepatology 33:554–560

    Article  PubMed  Google Scholar 

  11. Springer JE, Cole DE, Rubin LA, Cauch-Dudek K, Harewood L, Evrovski J, Peltekova VD, Heathcote EJ (2000) Vitamin Dreceptor genotypes as independent genetic predictors of decreased bone mineral density in primary biliary cirrhosis. Gastroenterology 118:145–151

    Article  PubMed  CAS  Google Scholar 

  12. 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

    Article  PubMed  Google Scholar 

  13. 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

    Article  PubMed  Google Scholar 

  14. 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

    Article  PubMed  Google Scholar 

  15. 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

    Article  PubMed  Google Scholar 

  16. Ludwig J, Dickson ER, McDonald GSA (1978) Staging of chronic non-suppurative destructive cholangitis (syndrome of primary biliary cirrhosis). Virchows Arch A Pathol Anat Histol 379:103–110

    Article  PubMed  CAS  Google Scholar 

  17. Hay JE, Lindor KD, Wiesner RH (1991) The metabolic bone disease of primary sclerosing cholangitis. Hepatology 14:257–261

    PubMed  CAS  Google Scholar 

  18. Lindor KD, Janes CH, Crippin JS, Jorgensen RA, Dickson ER (1995) Bone disease in primary biliary cirrhosis: does ursodeoxycholic acid make a difference? Hepatology 21:389–392

    PubMed  CAS  Google Scholar 

  19. Diamond TH, Stiel D, Lunzer M, McDowall 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

    PubMed  CAS  Google Scholar 

  20. Diamond-Hodgson SF, Dickson ER, Wahner HW, Johnson KA, Mann KG, Riggs BL (1985) Bone loss and reduced osteoblast function in primary biliary cirrhosis. Ann Intern Med 103:855–860

    Google Scholar 

  21. Trautwein C, Possienke P, Schlitt H, Klaus H, Roland H, Rudolph R, et al. (2000) Bone density and metabolism in patients with viral hepatitis and cholestatic liver diseases before and after liver transplantation. Am J Gastroenterol 95:2343–2351

    Article  PubMed  CAS  Google Scholar 

  22. Rosen H (1996) Primary biliary cirrhosis and bone disease. Hepatology 21:253–255

    Article  Google Scholar 

  23. Crosbie OM, Freaney R, McKenna MJ, Hegarty JE (1999) Bone density, Vitamin D status, and disordered bone remodeling in endstage chronic liver disease. Calcif Tissue Int 64:295–300

    Article  PubMed  CAS  Google Scholar 

  24. Guichelaar M, Hay J, Egan K, Therneau T (2000) Incidence and pretransplant risk factors for posttransplant fractures in patients with chronic cholestatic liver disease. J Hepatol 32:49

    Article  Google Scholar 

  25. Menon K, Angulo P, Weston S, Dickson E, Lindor K (2001) Bone disease in primary biliary cirrhosis: independent indicators and rate of progression. J Hepatol 35:316–323

    Article  PubMed  CAS  Google Scholar 

  26. Pares A, Guanabens N, Ros I, Caballeria L, Pons F, Vidal S, Monegal A, Peris P, Rodes J (2002) Duration and severity of the disease but not menopausal status are the main risk factors for osteoporosis in primary biliary cirrhosis. J Hepatol 36:154–155

    Article  Google Scholar 

  27. Mitchison HC, Malcolm AJ, Bassendine MF, James OF (1988) Metabolic bone disease in primary biliary cirrhosis at presentation. Gastroenterology 94:463–470

    PubMed  CAS  Google Scholar 

  28. Cuthbert JA, Pak CY, Zerwekh JE, Glass KD, Combes B (1984) Bone disease in primary biliary cirrhosis: increased bone resorption and turnover in the absence of osteoporosis or osteomalacia. Hepatology 4(1–8):1091–1095

    Google Scholar 

  29. 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

    Article  PubMed  CAS  Google Scholar 

  30. Allali F, El Aichaoui S, Benyahya B, Khazani H, Saoud B, Abouqal R, Hajjaj-Hassouni H (2006) Hypovitaminosis D in a sunny country: relation to lifestyle, bone markers and bone mineral density. Ann Rheum Dis 65(suppl 2):412

    Google Scholar 

  31. Pereira SP, Bray GP, Pitt PI, Li FM, Moniz C, Williams R (1999) Noninvasive assessment of bone density in primary biliary cirrhosis. Eur J Gastroenterol Hepatol 11:323–328

    Article  PubMed  CAS  Google Scholar 

  32. Shih MS, Anderson C (1987) Does “hepatic osteodystrophy” differ from peri-and postmenopausal osteoporosis? A histomorphometric study. Calcif Tissue Int 41:187–191

    Article  PubMed  CAS  Google Scholar 

  33. Hay JE, Lindor KD, Wiesner RH, Dickson ER, Krom RA, LaRusso NF (1991) The metabolic bone disease of primary sclerosing cholangitis. Hepatology 14:257–261

    Article  PubMed  CAS  Google Scholar 

  34. Floreani A, Fries W, Luisetto G, Burra P, Fagiuoli S, Boccagni P, Della Rovere GR, Plebani M, Piccoli A, Naccarato R (1998) Bone metabolism in orthotopic liver transplantation: a prospective study. Liver Transpl Surg 4:311–319

    Article  PubMed  CAS  Google Scholar 

  35. 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

    Article  PubMed  CAS  Google Scholar 

  36. Linderthal B, Leuschner MS, Ackerman H, Happ J, Leuschner UF (2000) Is primary biliary cirrhosis (PBC) in itself a risk factor for osteoporosis? Hepatology 32:168A

    Google Scholar 

  37. Floreani A, Mega A, Camozzi V, Baldo V, Plebani M, Burra P, Luisetto G (2005) Is osteoporosis a peculiar association with primary biliary cirrhosis? World J Gastroenterol 11(34):5347–5350

    PubMed  Google Scholar 

  38. Le Gars L, Grandpierre C, Chazouilleres O, Berenbaum F, Poupon R (2002) Bone loss in primary biliary cirrhhosis: absence of association with severity of liver disease. Joint Bone Spine 69:195–200

    Article  PubMed  Google Scholar 

  39. Olsson R, Johansson C, Lindstedt G, Mellstrom D (1994) Risk factors for bone loss in chronic active hepatitis and primary biliary cirrhosis. Scand J Gastroenterol 29:753–756

    Article  PubMed  CAS  Google Scholar 

  40. 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

    Article  PubMed  CAS  Google Scholar 

  41. Guanabens N, Pares A, Navasa M, Martinez de Osaba MJ, Hernandez ME, Munoz J, Rodes J (1994) Cyclosporin A increases the biochemical markers of bone remodeling in primary biliary cirrhosis. J Hepatol 21:24–28

    Article  PubMed  CAS  Google Scholar 

  42. Lindor KD, Jorgensen RA, Tiegs RD, Khosla S, Dickson ER (2000) Etidronate for osteoporosis in primary biliary cirrhosis: a randomized trial. J Hepatol 33:878–882

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Aziza Mounach.

About this article

Cite this article

Mounach, A., Ouzzif, Z., Wariaghli, G. et al. Primary biliary cirrhosis and osteoporosis: a case-control study. J Bone Miner Metab 26, 379–384 (2008). https://doi.org/10.1007/s00774-007-0833-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00774-007-0833-1

Key words

Navigation