Osteoporosis occurs in every third individual after simultaneous pancreas kidney transplantation (SPKT). Currently used bone measures insufficiently predict their fracture risk. Lumbar spine Trabecular bone score (TBS) and distal radius areal and volumetric bone mineral density (BMD) were monitored for the first time in patients with type 1 diabetes and chronic renal failure after SPKT with steroid-sparing protocol. In 33 subjects (mean age 43.4 ± 9.8 years), dual-energy X-ray absorptiometry and peripheral quantitative computed tomography were performed just after SPKT (baseline) and one and three years later. While TBS Z-scores increased (-1.1 ± 1.2 and -0.3 ± 1.0; p˂0.001, at baseline and year three, respectively), trabecular volumetric BMD Z-scores at distal radius metaphysis did not change during the study (-1.3 ± 1.3 and -1.3 ± 1.0; p = 0.38). Similarly, areal BMD Z-scores increased at lumbar spine, total hip and femoral neck (all p < 0.01), but not at the distal radius. SPKT induced bone measures' improvement at lumbar spine and hip but not at distal radius. Before suggesting changes in current clinical care, predictive value of individual bone measures or its combination for fracture risk assessment remains to be elucidated.

Department of Pediatrics 2nd Faculty of Medicine Charles University and Motol University Hospital Prague Czech Republic

Department of Probability and Mathematical Statistics Faculty of Mathematics and Physics Charles University Prague Czech Republic

Diabetes Centre Institute for Clinical and Experimental Medicine Prague Czech Republic

Zobrazit více v PubMed

Anastasilakis A.D., Tsourdi E., Makras P., Polyzos S.A., Meier C., McCloskey E.V., Pepe J., Zillikens M.C. Bone disease following solid organ transplantation: a narrative review and recommendations for management from the European calcified tissue society. Bone. 2019;127:401–418. PubMed

Anderson K.B., Holloway-Kew K.L., Hans D., Kotowicz M.A., Hyde N.K., Pasco J.A. Reference ranges for trabecular bone score in Australian men and women: a cross-sectional study. JBMR Plus. 2019;3 PubMed PMC

Arlot M.E., Sornay-Rendu E., Garnero P., Vey-Marty B., Delmas P.D. Apparent pre- and postmenopausal bone loss evaluated by DXA at different skeletal sites in women: the OFELY cohort. J. Bone Miner. Res. 1997;12:683–690. PubMed

(1994) Assessment of fracture risk and its application to screening for postmenopausal osteoporosis. Report of a WHO Study Group. World Health Organ Tech Rep Ser 843:1–129. PubMed

Binkley N., Bilezikian J.P., Kendler D.L., Leib E.S., Lewiecki E.M., Petak S.M., International Society for Clinical D Official positions of the International Society for Clinical Densitometry and Executive Summary of the 2005 position development conference. J. Clin. Densitom. 2006;9:4–14. PubMed

Collaborators G.B.D.F. Global, regional, and national burden of bone fractures in 204 countries and territories, 1990-2019: a systematic analysis from the global burden of disease study 2019. Lancet Healthy Longev. 2021;2:e580–e592. PubMed PMC

Dempster D.W., Muller R., Zhou H., Kohler T., Shane E., Parisien M., Silverberg S.J., Bilezikian J.P. Preserved three-dimensional cancellous bone structure in mild primary hyperparathyroidism. Bone. 2007;41:19–24. PubMed PMC

Ebeling P.R. Approach to the patient with transplantation-related bone loss. J. Clin. Endocrinol. Metab. 2009;94:1483–1490. PubMed

Girman P., Saudek F. The IKEM pancreas and islet transplant program as part of healthcare for type 1 diabetes patients: retrospective analysis of outcome from 1983 to 2010. Rev. Diabet. Stud. 2011;8:35–43. PubMed PMC

Girman P., Lipar K., Kocik M., Voska L., Koznarova R., Marada T., Lanska V., Saudek F. Results of a long-term prospective randomized study; Am J Transplant: 2019. Sirolimus vs mycophenolate mofetil (MMF) in primary combined pancreas and kidney transplantation. PubMed

Giustina A., Adler R.A., Binkley N., Bouillon R., Ebeling P.R., Lazaretti-Castro M., Marcocci C., Rizzoli R., Sempos C.T., Bilezikian J.P. Controversies in vitamin D: summary Statement from an international conference. J. Clin. Endocrinol. Metab. 2019;104:234–240. PubMed

Hart N.H., Newton R.U., Tan J., Rantalainen T., Chivers P., Siafarikas A., Nimphius S. Biological basis of bone strength: anatomy, physiology and measurement. J. Musculoskelet. Neuronal Interact. 2020;20:347–371. PubMed PMC

Hygum K., Starup-Linde J., Langdahl B.L. Diabetes and bone. Osteoporos Sarcopenia. 2019;5:29–37. PubMed PMC

International Federation of Clinical C, Laboratory Medicine ISD, Mosca A., et al. Global standardization of glycated hemoglobin measurement: the position of the IFCC working group. Clin. Chem. Lab. Med. 2007;45:1077–1080. PubMed

Iseri K., Carrero J.J., Evans M., Fellander-Tsai L., Berg H.E., Runesson B., Stenvinkel P., Lindholm B., Qureshi A.R. Fractures after kidney transplantation: incidence, predictors, and association with mortality. Bone. 2020;140 PubMed

Iyer S.P., Nikkel L.E., Nishiyama K.K., et al. Kidney transplantation with early corticosteroid withdrawal: paradoxical effects at the central and peripheral skeleton. J. Am. Soc. Nephrol. 2014;25:1331–1341. PubMed PMC

Jorgensen N.R., Mollehave L.T., Hansen Y.B.L., Quardon N., Lylloff L., Linneberg A. Comparison of two automated assays of BTM (CTX and P1NP) and reference intervals in a Danish population. Osteoporos. Int. 2017;28:2103–2113. PubMed

Kanis J.A. Diagnosis of osteoporosis and assessment of fracture risk. Lancet. 2002;359:1929–1936. PubMed

Kanis J.A., Johnell O., Oden A., Dawson A., De Laet C., Jonsson B. Ten year probabilities of osteoporotic fractures according to BMD and diagnostic thresholds. Osteoporos. Int. 2001;12:989–995. PubMed

Kratochvilova S., Brunova J., Wohl P., Lanska V., Saudek F. Retrospective analysis of bone metabolism in patients on waiting list for simultaneous pancreas-kidney transplantation. J. Diabetes Res. 2019;2019 PubMed PMC

Krohn K., Schwartz E.N., Chung Y.S., Lewiecki E.M. Dual-energy X-ray absorptiometry monitoring with trabecular bone score: 2019 ISCD official position. J. Clin. Densitom. 2019;22:501–505. PubMed

Kukla A., Ventura-Aguiar P., Cooper M., et al. Transplant options for patients with diabetes and advanced kidney disease: a review. Am. J. Kidney Dis. 2021;78:418–428. PubMed PMC

Lan G.B., Xie X.B., Peng L.K., Liu L., Song L., Dai H.L. Current status of research on osteoporosis after solid organ transplantation: pathogenesis and management. Biomed. Res. Int. 2015;2015 PubMed PMC

Lauria M.W., Ribeiro-Oliveira A., Jr. Diabetes and other endocrine-metabolic abnormalities in the long-term follow-up of pancreas transplantation. Clin Diabetes Endocrinol. 2016;2:14. PubMed PMC

Levey A.S., Coresh J., Greene T., Marsh J., Stevens L.A., Kusek J.W., Van Lente F., Chronic Kidney Disease Epidemiology C Expressing the modification of diet in renal disease study equation for estimating glomerular filtration rate with standardized serum creatinine values. Clin. Chem. 2007;53:766–772. PubMed

Malluche H.H., Monier-Faugere M.C., Herberth J. Bone disease after renal transplantation. Nat. Rev. Nephrol. 2010;6:32–40. PubMed PMC

McCloskey E.V., Oden A., Harvey N.C., et al. A Meta-analysis of trabecular bone score in fracture risk prediction and its relationship to FRAX. J. Bone Miner. Res. 2016;31:940–948. PubMed

Nickolas T.L., Stein E.M., Dworakowski E., et al. Rapid cortical bone loss in patients with chronic kidney disease. J. Bone Miner. Res. 2013;28:1811–1820. PubMed PMC

Pereira S., Pedroso S., Martins L., et al. Bone mineral density after simultaneous kidney-pancreas transplantation: four years follow-up of 57 recipients. Transplant. Proc. 2010;42:555–557. PubMed

Pinheiro J., Bates D., DebRoy S., Sarkar D., R Core Team nlme: linear and nonlinear mixed effects Models_. R package version 3.1-137. 2018. https://CRAN.R-project.org/package=nlme

R Core Team . R Foundation for Statistical Computing; Vienna, Austria: 2018. R: A Language and Environment for Statistical Computing.https://www.R-project.org/

Rauch F., Schoenau E. Peripheral quantitative computed tomography of the distal radius in young subjects - new reference data and interpretation of results. J. Musculoskelet. Neuronal Interact. 2005;5:119–126. PubMed

Rauch F, Schoenau E (2008) Peripheral quantitative computed tomography of the proximal radius in young subjects--new reference data and interpretation of results. J. Musculoskelet. Neuronal Interact. 8:217–226. PubMed

Rocha A., Martins L.S., Malheiro J., Dores J., Santos C., Henriques C. Changes in bone mineral density following long-term simultaneous pancreas-kidney transplantation. J. Bone Miner. Metab. 2016;34:209–215. PubMed

Samelson E.J., Broe K.E., Xu H., et al. Cortical and trabecular bone microarchitecture as an independent predictor of incident fracture risk in older women and men in the bone microarchitecture international consortium (BoMIC): a prospective study. Lancet Diabetes Endocrinol. 2019;7:34–43. PubMed PMC

Silva B.C., Broy S.B., Boutroy S., Schousboe J.T., Shepherd J.A., Leslie W.D. Fracture risk prediction by non-BMD DXA measures: the 2015 ISCD official positions part 2: trabecular bone score. J. Clin. Densitom. 2015;18:309–330. PubMed

Smets Y.F., van der Pijl J.W., de Fijter J.W., Ringers J., Lemkes H.H., Hamdy N.A. Low bone mass and high incidence of fractures after successful simultaneous pancreas-kidney transplantation. Nephrol. Dial. Transplant. 1998;13:1250–1255. PubMed

Smets Y.F., de Fijter J.W., Ringers J., Lemkes H.H., Hamdy N.A. Long-term follow-up study on bone mineral density and fractures after simultaneous pancreas-kidney transplantation. Kidney Int. 2004;66:2070–2076. PubMed

Soucek O., Lebl J., Snajderova M., Kolouskova S., Rocek M., Hlavka Z., Cinek O., Rittweger J., Sumnik Z. Bone geometry and volumetric bone mineral density in girls with turner syndrome of different pubertal stages. Clin. Endocrinol. (Oxf) 2011;74:445–452. PubMed

Soucek O., Schonau E., Lebl J., Willnecker J., Hlavka Z., Sumnik Z. A 6-year follow-up of fracture incidence and volumetric bone mineral density development in girls with turner syndrome. J. Clin. Endocrinol. Metab. 2018;103:1188–1197. PubMed

Torregrosa J.V., Sanchez-Escuredo A., Fuster D., et al. DXA variations and fractures after simultaneous pancreas-renal transplantation: results of a long-term follow-up. Clin. Nucl. Med. 2015;40:e232–e235. PubMed

Vangala C., Pan J., Cotton R.T., Ramanathan V. Mineral and bone disorders after kidney transplantation. Front Med (Lausanne) 2018;5:211. PubMed PMC

Wolf M., Weir M.R., Kopyt N., Mannon R.B., Von Visger J., Deng H., Yue S., Vincenti F. A prospective cohort study of mineral metabolism after kidney transplantation. Transplantation. 2016;100:184–193. PubMed PMC