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23-12-2022 | Computed Tomography | Original Article

Peripheral quantitative computed tomography-derived bone parameters in men with impaired fasting glucose and diabetes

Authors: Kara L. Holloway-Kew, Kara B. Anderson, Monica C. Tembo, Sophia X. Sui, Jacob W. Harland, Natalie K. Hyde, Mark A. Kotowicz, Julie A. Pasco

Published in: Journal of Bone and Mineral Metabolism | Issue 1/2023

Abstract

Introduction

Individuals with type 2 diabetes mellitus (T2DM) are at higher risk of fracture, but paradoxically do not have reduced bone mineral density. We investigated associations between peripheral quantitative computed tomography (pQCT) and glycaemia status.

Materials and methods

Participants were men (n = 354, age 33–92 year) from the Geelong Osteoporosis Study. Diabetes was defined by fasting plasma glucose (FPG) ≥ 7.0 mmol/L, self-report of diabetes and/or antihyperglycaemic medication use and impaired fasting glucose (IFG) as FPG 5.6–6.9 mmol/L. Bone measures were derived using pQCT (XCT2000) at 4% and 66% radial and tibial sites. Linear regression was used, adjusting for age, body mass index and socio-economic status.

Results

At the 4% site, men with T2DM had lower adjusted bone total area, trabecular area and cortical area at the radius (all − 6.2%) and tibia (all − 6.4%) compared to normoglycaemia. Cortical density was higher for T2DM at the radius (+ 5.8%) and tibia (+ 8.0%), as well as adjusted total bone density at the tibial site (+ 6.1%). At the 66% site, adjusted total bone area and polar stress strain index were lower for T2DM at the radius (− 4.3% and − 8.0%). Total density was also higher for T2DM (+ 1.2%).

Only cortical density at the 4% tibial site was different between IFG and normoglycaemia in adjusted analyses (+ 4.5%).

Conclusion

Men with T2DM had lower total bone area, trabecular area, cortical area and polar stress strain index than the other two groups; however, total density and cortical density were higher. Only one difference was observed between IFG and normoglycaemia; increased tibial cortical density.

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de Liefde II, van der Klift M, de Laet CEDH, van Daele PLA, Hofman A, Pols HAP (2005) Bone mineral density and fracture risk in type-2 diabetes mellitus: the Rotterdam study. Osteoporos Int 16:1713–1720. https://doi.org/10.1007/s00198-005-1909-1CrossRef

Napoli N, Strotmeyer ES, Ensrud KE, Sellmeyer DE, Bauer DC, Hoffman AR, Dam TT, Barrett-Connor E, Palermo L, Orwoll ES, Cummings SR, Black DM, Schwartz AV (2014) Fracture risk in diabetic elderly men: the MrOS study. Diabetologia 57:2057–2065. https://doi.org/10.1007/s00125-014-3289-6CrossRef

de Abreu LLF, Holloway-Kew KL, Mohebbi M, Sajjad MA, Kotowicz MA, Pasco JA (2019) Fracture risk in women with dysglycaemia: assessing effects of baseline and time-varying risk factors. Calcif Tissue Int 104:262–272. https://doi.org/10.1007/s00223-018-0498-xCrossRef

Looker AC, Eberhardt MS, Saydah SH (2016) Diabetes and fracture risk in older U.S. adults. Bone 82:9–15. https://doi.org/10.1016/j.bone.2014.12.008CrossRef

Botella Martinez S, Varo Cenarruzabeitia N, Escalada San Martin J, Calleja Canelas A (2016) The diabetic paradox: bone mineral density and fracture in type 2 diabetes. Endocrinol Nutr 63:495–501. https://doi.org/10.1016/j.endonu.2016.06.004CrossRef

Christensen JO, Svendsen OL (1999) Bone mineral in pre- and postmenopausal women with insulin-dependent and non-insulin-dependent diabetes mellitus. Osteoporos Int 10:307–311. https://doi.org/10.1007/s001980050232CrossRef

Baleanu F, Bergmann P, Hambye AS, Dekelver C, Iconaru L, Cappelle SI, Moreau M, Paesmans M, Karmali R, Body J-J (2019) Assessment of bone quality with trabecular bone score in type 2 diabetes mellitus: a study from the FRISBEE cohort. Int J Clin Pract 73:e13347. https://doi.org/10.1111/ijcp.13347CrossRef

Holloway-Kew KL, Marijanovic N, De Abreu LLF, Sajjad MA, Pasco JA, Kotowicz MA (2019) Bone mineral density in diabetes and impaired fasting glucose. Osteoporos Int 30:1799–1806. https://doi.org/10.1007/s00198-019-05108-1CrossRef

Giangregorio LM, Leslie WD, Lix LM, Johansson H, Oden A, McCloskey E, Kanis JA (2012) FRAX underestimates fracture risk in patients with diabetes. J Bone Miner Res 27:301–308CrossRef

10.

Choi YJ, Ock SY, Chung YS (2016) Trabecular bone score (TBS) and TBS-adjusted fracture risk assessment tool are potential supplementary tools for the discrimination of morphometric vertebral fractures in postmenopausal women with type 2 diabetes. J Clin Densitom 19:507–514. https://doi.org/10.1016/j.jocd.2016.04.001CrossRef

11.

Leslie WD, Johansson H, McCloskey EV, Harvey NC, Kanis JA, Hans D (2018) Comparison of methods for improving fracture risk assessment in diabetes: the Manitoba BMD registry. J Bone Miner Res 33:1923–1930. https://doi.org/10.1002/jbmr.3538CrossRef

12.

Hans D, Barthe N, Boutroy S, Pothuaud L, Winzenrieth R, Krieg MA (2011) Correlations between trabecular bone score, measured using anteroposterior dual-energy X-ray absorptiometry acquisition, and 3-dimensional parameters of bone microarchitecture: an experimental study on human cadaver vertebrae. J Clin Densitom 14:302–312. https://doi.org/10.1016/j.jocd.2011.05.005CrossRef

13.

Bonaccorsi G, Fila E, Messina C, Maietti E, Ulivieri FM, Caudarella R, Greco P, Guglielmi G (2016) Comparison of trabecular bone score and hip structural analysis with FRAX(R) in postmenopausal women with type 2 diabetes mellitus. Aging Clin Exp Res 29:951–957. https://doi.org/10.1007/s40520-016-0634-2CrossRef

14.

Ho-Pham LT, Nguyen TV (2019) Association between trabecular bone score and type 2 diabetes: a quantitative update of evidence. Osteoporos Int 30:2079–2085. https://doi.org/10.1007/s00198-019-05053-zCrossRef

15.

Ho-Pham LT, Tran B, Do AT, Nguyen TV (2019) Association between pre-diabetes, type 2 diabetes and trabecular bone score: the Vietnam osteoporosis study. Diabetes Res Clin Pract. https://doi.org/10.1016/j.diabres.2019.107790CrossRef

16.

Holloway KL, De Abreu LLF, Hans D, Kotowicz MA, Sajjad MA, Hyde NK, Pasco JA (2018) Trabecular bone score in men and women with impaired fasting glucose and diabetes. Calcif Tissue Int 102:32–40. https://doi.org/10.1007/s00223-017-0330-zCrossRef

17.

Dawson-Hughes B, Bouxsein M, Shea K (2019) Bone material strength in normoglycemic and hyperglycemic black and white older adults. Osteoporos Int 30:2429–2435CrossRef

18.

Farr JN, Drake MT, Amin S, Joseph Melton III L, McCready LK, Khosla S (2014) In vivo assessment of bone quality in postmenopausal women with type 2 diabetes. J Bone Miner Res 29:787–795CrossRef

19.

Furst JR, Bandeira LC, Fan WW, Agarwal S, Nishiyama KK, McMahon DJ, Dworakowski E, Jiang H, Silverberg SJ, Rubin MR (2016) Advanced glycation endproducts and bone material strength in type 2 diabetes. J Clin Endocrinol Metab 101:2502–2510. https://doi.org/10.1210/jc.2016-1437CrossRef

20.

Holloway-Kew KL, Betson A, Rufus-Membere PG, Gaston J, Diez-Perez A, Kotowicz MA, Pasco JA (2021) Impact microindentation in men with impaired fasting glucose and type 2 diabetes. Bone 142:115685. https://doi.org/10.1016/j.bone.2020.115685CrossRef

21.

Nilsson AG, Sundh D, Johansson L, Nilsson M, Mellstrom D, Rudang R, Zoulakis M, Wallander M, Darelid A, Lorentzon M (2017) Type 2 diabetes mellitus is associated with better bone microarchitecture but lower bone material strength and poorer physical function in elderly women: a population-based study. J Bone Miner Res 32:1062–1071. https://doi.org/10.1002/jbmr.3057CrossRef

22.

Dumitru N, Carsote M, Cocolos A, Petrova E, Olaru M, Caragheorgheopol A, Dumitrache C, Ghemigian A (2018) Metabolic and bone profile in postmenopausal women with and without type 2 diabetes: a cross-sectional study. Rom J Intern Med. https://doi.org/10.2478/rjim-2018-0036CrossRef

23.

Lerchbaum E, Schwetz V, Nauck M, Volzke H, Wallaschofski H, Hannemann A (2015) Lower bone turnover markers in metabolic syndrome and diabetes: the population-based study of health in Pomerania. Nutr Metab Cardiovasc Dis 25:458–463. https://doi.org/10.1016/j.numecd.2015.02.002CrossRef

24.

Reyes-García R, Rozas-Moreno P, López-Gallardo G, García-Martín A, Varsavsky M, Avilés-Perez MD, Muñoz-Torres M (2013) Serum levels of bone resorption markers are decreased in patients with type 2 diabetes. Acta Diabetol 50:47–52. https://doi.org/10.1007/s00592-011-0347-0CrossRef

25.

Starup-Linde J, Eriksen SA, Lykkeboe S, Handberg A, Vestergaard P (2014) Biochemical markers of bone turnover in diabetes patients—a meta-analysis, and a methodological study on the effects of glucose on bone markers. Osteoporos Int 25:1697–1708. https://doi.org/10.1007/s00198-014-2676-7CrossRef

26.

Holloway-Kew KL, De Abreu LLF, Kotowicz MA, Sajjad MA, Pasco JA (2019) Bone turnover markers in men and momen with impaired fasting glucose and diabetes. Calcif Tissue Int 104:599–604. https://doi.org/10.1007/s00223-019-00527-yCrossRef

27.

Pawlowska M, Bilezikian JP (2016) Beyond DXA: advances in clinical applications of new bone imaging technology. Endocr Pr 22:990–998. https://doi.org/10.4158/ep151019.raCrossRef

28.

Ho-Pham LT, Chau PMN, Do AT, Nguyen HC, Nguyen TV (2018) Type 2 diabetes is associated with higher trabecular bone density but lower cortical bone density: the Vietnam osteoporosis study. Osteoporos Int 29:2059–2067. https://doi.org/10.1007/s00198-018-4579-5CrossRef

29.

Petit MA, Paudel ML, Taylor BC, Hughes JM, Strotmeyer ES, Schwartz AV, Cauley JA, Zmuda JM, Hoffman AR, Ensrud KE (2010) Bone mass and strength in older men with type 2 diabetes: the osteoporotic fractures in men study. J Bone Miner Res 25:285–291. https://doi.org/10.1359/jbmr.090725CrossRef

30.

Dennison EM, Jameson KA, Edwards MH, Denison HJ, Aihie Sayer A, Cooper C (2014) Peripheral quantitative computed tomography measures are associated with adult fracture risk: the Hertfordshire cohort study. Bone 64:13–17. https://doi.org/10.1016/j.bone.2014.03.040CrossRef

31.

Sheu Y, Zmuda JM, Boudreau RM, Petit MA, Ensrud KE, Bauer DC, Gordon CL, Orwoll ES, Cauley JA, Group for the OF in M (MrOS) R (2011) Bone strength measured by peripheral quantitative computed tomography and the risk of Nonvertebral fractures: The osteoporotic fractures in men (MrOS) study. J Bone Miner Res 26:63–71. https://doi.org/10.1002/jbmr.172CrossRef

32.

Pasco JA, Nicholson GC, Kotowicz MA (2012) Cohort profile: geelong osteoporosis study. Int J Epidemiol 41:1565–1575CrossRef

33.

Henry MJ, Pasco JA, Nicholson GC, Seeman E, Kotowicz MA (2000) Prevalence of osteoporosis in Australian women: Geelong osteoporosis study. J Clin Densitom 3:261–268CrossRef

34.

Genuth S, Alberti KG, Bennett P, Buse J, Defronzo R, Kahn R, Kitzmiller J, Knowler WC, Lebovitz H, Lernmark A, Nathan D, Palmer J, Rizza R, Saudek C, Shaw J, Steffes M, Stern M, Tuomilehto J, Zimmet P (2003) Follow-up report on the diagnosis of diabetes mellitus. Diabetes Care 26:3160–3167CrossRef

35.

Blew RM, Lee VR, Farr JN, Schiferl DJ, Going SB (2014) Standardizing evaluation of pQCT image quality in the presence of subject movement: qualitative versus quantitative assessment. Calcif Tissue Int 94:202–211. https://doi.org/10.1007/s00223-013-9803-xCrossRef

36.

Wong AK (2016) A comparison of peripheral imaging technologies for bone and muscle quantification: a technical review of image acquisition. J Musculoskelet Neuronal Interact 16:265–282

37.

Giles GG, Ireland PD (1996) Dietary Questionnaire for Epidemiological Studies (Version 2). Melbourne, Cancer Counc Victoria

38.

Harris PA, Taylor R, Thielke R, Payne J, Gonzalez N, Conde JG (2009) Research electronic data capture (REDCap)—A metadata-driven methodology and workflow process for providing translational research informatics support. J Biomed Inform 42:377–381. https://doi.org/10.1016/j.jbi.2008.08.010CrossRef

39.

Zhukouskaya VV, Eller-Vainicher C, Gaudio A, Privitera F, Cairoli E, Ulivieri FM, Palmieri S, Morelli V, Grancini V, Orsi E, Masserini B, Spada AM, Fiore CE, Chiodini I (2016) The utility of lumbar spine trabecular bone score and femoral neck bone mineral density for identifying asymptomatic vertebral fractures in well-compensated type 2 diabetic patients. Osteoporos Int 27:49–56. https://doi.org/10.1007/s00198-015-3212-0CrossRef

40.

Patel S, Hyer S, Tweed K, Kerry S, Allan K, Rodin A, Barron J (2008) Risk factors for fractures and falls in older women with type 2 diabetes mellitus. Calcif Tissue Int 82:87–91CrossRef

41.

Oei L, Zillikens MC, Dehghan A, Buitendijk GHS, Castaño-Betancourt MC, Estrada K, Stolk L, Oei EHG, van Meurs JBJ, Janssen JAMJL, Hofman A, van Leeuwen JPTM, Witteman JCM, Pols HAP, Uitterlinden AG, Klaver CCW, Franco OH, Rivadeneira F (2013) High bone mineral density and fracture risk in type 2 diabetes as skeletal complications of inadequate glucose control. Diabetes Care 36:1619–1628. https://doi.org/10.2337/dc12-1188CrossRef

42.

Anderson KB, Tembo MC, Sui SX, Hyde NK, Rufus PG, Pasco JA, Kotowicz MA, Holloway-Kew KL (2021) Normative data for peripheral quantitative computed tomography (pQCT) bone parameters in Australian men. Bone Reports 15:101107. https://doi.org/10.1016/j.bonr.2021.101107CrossRef

43.

Paul J, Devarapalli V, Johnson JT, Cherian KE, Jebasingh FK, Asha HS, Kapoor N, Thomas N, Paul TV (2021) Do proximal hip geometry, trabecular microarchitecture, and prevalent vertebral fractures differ in postmenopausal women with type 2 diabetes mellitus? A cross-sectional study from a teaching hospital in southern India. Osteoporos Int 32:1585–1593. https://doi.org/10.1007/s00198-021-05855-0CrossRef

44.

Jiajue R, Jiang Y, Wang O, Li M, Xing X, Cui L, Yin J, Xu L, Xia W (2014) Suppressed bone turnover was associated with increased osteoporotic fracture risks in non-obese postmenopausal Chinese women with type 2 diabetes mellitus. Osteoporos Int 25:1999–2005. https://doi.org/10.1007/s00198-014-2714-5CrossRef

45.

Zhang L, Liu Y, Wang D, Zhao X, Qiu Z, Ji H, Rong H (2009) Bone biomechanical and histomorphometrical investment in type 2 diabetic Goto-Kakizaki rats. Acta Diabetol 46:119–126. https://doi.org/10.1007/s00592-008-0068-1CrossRef

46.

Manavalan JS, Cremers S, Dempster DW, Zhou H, Dworakowski E, Kode A, Kousteni S, Rubin MR (2012) Circulating osteogenic precursor cells in type 2 diabetes mellitus. J Clin Endocrinol Metab 97:3240–3250. https://doi.org/10.1210/jc.2012-1546CrossRef

47.

Ferron M, Wei J, Yoshizawa T, Del Fattore A, DePinho RA, Teti A, Ducy P, Karsenty G (2010) Insulin signaling in osteoblasts integrates bone remodeling and energy metabolism. Cell 142:296–308. https://doi.org/10.1016/j.cell.2010.06.003CrossRef

48.

Malekzadeh B, Tengvall P, Ohrnell L-O, Wennerberg A, Westerlund A (2013) Effects of locally administered insulin on bone formation in non-diabetic rats. J Biomed Mater Res A 101:132–137. https://doi.org/10.1002/jbm.a.34313CrossRef

49.

de Waard EAC, de Jong JJA, Koster A, Savelberg HHCM, van Geel TA, Houben AJHM, Schram MT, Dagnelie PC, van der Kallen CJ, Sep SJS, Stehouwer CDA, Schaper NC, Berendschot TTJM, Schouten JSAG, Geusens PPMM, van den Bergh JPW (2018) The association between diabetes status, HbA1c, diabetes duration, microvascular disease, and bone quality of the distal radius and tibia as measured with high-resolution peripheral quantitative computed tomography—the Maastricht study. Osteoporos Int 29:2725–2738. https://doi.org/10.1007/s00198-018-4678-3CrossRef

50.

Samelson EJ, Demissie S, Cupples LA, Zhang X, Xu H, Liu C-T, Boyd SK, McLean RR, Broe KE, Kiel DP, Bouxsein ML (2018) Diabetes and deficits in cortical bone density, microarchitecture, and bone size: Framingham HR-pQCT study. J Bone Miner Res 33:54–62. https://doi.org/10.1002/jbmr.3240CrossRef

51.

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.1763CrossRef

52.

Patsch JM, Burghardt AJ, Kazakia G, Majumdar S (2011) Noninvasive imaging of bone microarchitecture. Ann N Y Acad Sci 1240:77–87. https://doi.org/10.1111/j.1749-6632.2011.06282.xCrossRef

53.

Heilmeier U, Cheng K, Pasco C, Parrish R, Nirody J, Patsch JM, Zhang CA, Joseph GB, Burghardt AJ, Schwartz AV, Link TM, Kazakia G (2016) Cortical bone laminar analysis reveals increased midcortical and periosteal porosity in type 2 diabetic postmenopausal women with history of fragility fractures compared to fracture-free diabetics. Osteoporos Int 27:2791–2802. https://doi.org/10.1007/s00198-016-3614-7CrossRef

Title: Peripheral quantitative computed tomography-derived bone parameters in men with impaired fasting glucose and diabetes
Authors: Kara L. Holloway-Kew
Kara B. Anderson
Monica C. Tembo
Sophia X. Sui
Jacob W. Harland
Natalie K. Hyde
Mark A. Kotowicz
Julie A. Pasco
Publication date: 23-12-2022
Publisher: Springer Nature Singapore
Keywords: Computed Tomography
Computed Tomography
Type 2 Diabetes
Published in: Journal of Bone and Mineral Metabolism / Issue 1/2023
Print ISSN: 0914-8779
Electronic ISSN: 1435-5604
DOI: https://doi.org/10.1007/s00774-022-01389-5

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Abstract

Introduction

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