Abstract
Summary
We report that compared with normoglycaemia, post-menopausal women (non-obese and obese) with diabetes had higher lumbar spine bone mineral density (LSBMD). Femoral neck bone mineral density (FNBMD) was higher in obese post-menopausal women with diabetes. Only non-obese post-menopausal women with impaired fasting glucose (IFG) had a higher LSBMD than normoglycaemia. No other associations with IFG were observed.
Introduction
Individuals with diabetes have a higher or normal bone mineral density (BMD) compared with those without diabetes. However, paradoxically, they also have a higher fracture risk. It is not clear whether those with IFG also have altered BMD. This study aimed to determine whether individuals with IFG have elevated or normal BMD.
Methods
Women (n = 858) and men (n = 970) (aged 20–80 years) from the Geelong Osteoporosis Study were included. IFG was defined as fasting plasma glucose (FPG) 5.5–6.9 mmol/L and diabetes as FPG ≥ 7.0 mmol/L, use of antihyperglycaemic medication and/or self-report. Using multivariable linear regression, the relationships between glycaemia and BMD at the femoral neck and lumbar spine were examined, and adjusted for age, body mass index (BMI), and other variables. In women, two interaction terms were identified: menopause × glycaemia and BMI × glycaemia, and thus, the analyses were stratified by menopause and obesity status (BMI cut point ≥ 30 kg/m2).
Results
There were no associations between glycaemic status and BMD for pre-menopausal women. For non-obese post-menopausal women, there was no association between FNBMD and glycaemic status, but women with IFG or diabetes had higher LSBMD than those with normoglycaemia (7.1% and 9.7%, respectively, both p < 0.01). Obese post-menopausal women with diabetes had a higher FNBMD (8.8%, p = 0.008) and LSBMD (12.2%, p < 0.001), but those with IFG were not different from the normoglycaemia group. There were no associations detected between glycaemic status and BMD in men.
Conclusions
In this study, we report that compared with normoglycaemia, post-menopausal women (non-obese and obese) with diabetes had higher LSBMD. FNBMD was higher in obese post-menopausal women with diabetes. Only non-obese post-menopausal women with IFG had a higher LSBMD than normoglycaemia. No other associations with IFG were observed.
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References
Compston J (2017) Type 2 diabetes mellitus and bone. J Intern Med 283:140–153. https://doi.org/10.1111/joim.12725
Ferrari S (2017) Diabetes and bone. Calcif Tissue Int 100:107–108. https://doi.org/10.1007/s00223-017-0234-y
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.2014.12.008
Poiana C, Capatina C (2017) Fracture risk assessment in patients with diabetes mellitus. J Clin Densitom 20:432–443. https://doi.org/10.1016/j.jocd.2017.06.011
Sealand R, Razavi C, Adler RA (2013) Diabetes mellitus and osteoporosis. Curr Diab Rep 13:411–418
Shibuya N, Humphers JM, Fluhman BL, Jupiter DC (2013) Factors associated with nonunion, delayed union, and malunion in foot and ankle surgery in diabetic patients. J Foot Ankle Surg 52:207–211
Gehling DJ, Lecka-Czernik B, Ebraheim NA (2016) Orthopedic complications in diabetes. Bone 82:79–92. https://doi.org/10.1016/j.bone.2015.07.029
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 27:301–308
Danaei G, Finucane MM, Lu Y, Singh GM, Cowan MJ, Paciorek CJ, Lin JK, Farzadfar F, Khang YH, Stevens GA, Rao M, Ali MK, Riley LM, Robinson CA, Ezzati M (2011) National, regional, and global trends in fasting plasma glucose and diabetes prevalence since 1980: systematic analysis of health examination surveys and epidemiological studies with 370 country-years and 2·7 million participants. Lancet 378:31–40. https://doi.org/10.1016/S0140-6736(11)60679-X
de Abreu L, Holloway KL, Kotowicz MA, Pasco JA (2015) Dysglycaemia and other predictors for progression or regression from impaired fasting glucose to diabetes or normoglycaemia. J Diabetes Res. https://doi.org/10.1155/2015/373762
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, Expert Committee on the Diagnosis and Classification of Diabetes Mellitus (2003) Follow-up report on the diagnosis of diabetes mellitus. Diabetes Care 26:3160–3167
Pasco JA, Nicholson GC, Kotowicz MA (2012) Cohort profile: Geelong Osteoporosis Study. Int J Epidemiol 41:1565–1575
Sanders KM, Pasco JA, Ugoni AM, Nicholson GC, Seeman E, Martin TJ, Skoric B, Panahi S, Kotowicz MA (1998) The exclusion of high trauma fractures may underestimate the prevalence of bone fragility fractures in the community: the Geelong Osteoporosis Study. J Bone Miner Res 13:1337–1342
World Health Organization (2018) WHO | Obesity and overweight. http://www.who.int/dietphysicalactivity/pa/en/. Accessed 20 Aug 2018
Kunst A, Draeger B, Ziegenhorn J (1984) UV-methods with hexokinase and glucose-6-phosphate dehydrogenase. In: Bergmeyer HU (ed) Methods of enzymatic analysis, 3rd edn. Verlag Chemie, Weinheim, pp 163–172
Giles GG, Ireland PD (1996) Dietary questionnaire for epidemiological studies (version 2). Melbourne, Cancer Counc Victoria
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/s001980050232
Zakeri Z, Azizi Z, Mehrabifar H, Hashemi M (2011) Evaluation of bone mineral density in premenopausal women with type-2 diabetes mellitus in Zahedan, southeast Iran. J Pak Med Assoc 61:443–445
Gupta R, Mohammed AM, Mojiminiyi OA, Alenizi EK, Abdulla NA (2009) Bone mineral density in premenopausal Arab women with type 2 diabetes mellitus. J Clin Densitom 12:54–57. https://doi.org/10.1016/j.jocd.2008.09.003
Mitchell A, Fall T, Melhus H, Wolk A, Michaëlsson K, Byberg L (2018) Type 2 diabetes in relation to hip bone density, area, and bone turnover in Swedish men and women: a cross-sectional study. Calcif Tissue Int 103:501–511. https://doi.org/10.1007/s00223-018-0446-9
Napoli N, Strotmeyer ES, Ensrud KE, Sellmeyer DE, Bauer DC, Hoffman AR, Dam TTL, 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/s00125-014-3289-6
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/s00198-014-2714-5
Moseley KF, Chia CW, Simonsick EM, Egan JM, Ferrucci L, Sellmeyer DE (2015) Sex-specific differences in progressive glucose intolerance and hip geometry: the Baltimore longitudinal study of aging. Osteoporos Int 26:1555–1562. https://doi.org/10.1007/s00198-015-3027-z
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/s00198-005-1909-1
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-x
Gagnon C, Magliano DJ, Ebeling PR, Dunstan DW, Zimmet PZ, Shaw JE, Daly RM (2010) Association between hyperglycaemia and fracture risk in non-diabetic middle-aged and older Australians: a national, population-based prospective study (AusDiab). Osteoporos Int 21:2067–2074. https://doi.org/10.1007/s00198-009-1164-y
Strotmeyer ES, Cauley JA, Schwartz AV, Nevitt MC, Resnick HE, Bauer DC, Tylavsky FA, de Rekeneire N, Harris TB, Newman AB (2005) Nontraumatic fracture risk with diabetes mellitus and impaired fasting glucose in older white and black adults: the health, aging, and body composition study. Arch Intern Med 165:1612–1617. https://doi.org/10.1001/archinte.165.14.1612
Evans AL, Paggiosi MA, Eastell R, Walsh JS (2015) Bone density, microstructure and strength in obese and normal weight men and women in younger and older adulthood. J Bone Miner Res 30:920–928. https://doi.org/10.1002/jbmr.2407
Beck TJ, Petit MA, Wu G, LeBoff MS, Cauley JA, Chen Z (2009) Does obesity really make the femur stronger? BMD, geometry, and fracture incidence in the women’s health initiative-observational study. J Bone Miner Res 24:1369–1379
Compston JE, Watts NB, Chapurlat R, Cooper C, Boonen S, Greenspan S, Pfeilschifter J, Silverman S, Díez-Pérez A, Lindsay R, Saag KG, Netelenbos JC, Gehlbach S, Hooven FH, Flahive J, Adachi JD, Rossini M, Lacroix AZ, Roux C, Sambrook PN, Siris ES, Glow Investigators (2011) Obesity is not protective against fracture in postmenopausal women: GLOW. Am J Med 124:1043–1050
Gnudi S, Sitta E, Lisi L (2009) Relationship of body mass index with main limb fragility fractures in postmenopausal women. J Bone Miner Metab 27:479–484
Johansson H, Kanis JA, Odén A et al (2013) A meta-analysis of the association of fracture risk and body mass index in women. J Bone Miner Res 29:223–233
Nielson CM, Marshall LM, Adams AL, LeBlanc ES, Cawthon PM, Ensrud K, Stefanick ML, Barrett-Connor E, Orwoll ES, for the Osteoporotic Fractures in Men Study (MrOS) Research Group (2011) BMI and fracture risk in older men: the osteoporotic fractures in men study (MrOS). J Bone Miner Res 26:496–502
Andersen S, Frederiksen KD, Hansen S, Brixen K, Gram J, Støving RK (2014) Bone structure and estimated bone strength in obese patients evaluated by high-resolution peripheral quantitative computed tomography. Calcif Tissue Int 95:19–28. https://doi.org/10.1007/s00223-014-9857-4
Sornay-Rendu E, Boutroy S, Vilayphiou N, Claustrat B, Chapurlat RD (2013) In obese postmenopausal women, bone microarchitecture and strength are not commensurate to greater body weight: the Os des Femmes de Lyon (OFELY) study. J Bone Miner Res 28:1679–1687. https://doi.org/10.1002/jbmr.1880
Holloway KL, De Abreu LLF, Hans D et al (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-z
Baleanu F, Bergmann P, Hambye AS, Dekelver C, Iconaru L, Cappelle SI, Moreau M, Paesmans M, Karmali R, Body JJ (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.13347
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/s40520-016-0634-2
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.2016.04.001
Dhaliwal R, Cibula D, Ghosh C, Weinstock RS, Moses AM (2014) Bone quality assessment in type 2 diabetes mellitus. Osteoporos Int 25:1969–1973. https://doi.org/10.1007/s00198-014-2704-7
Leslie WD, Aubry-Rozier B, Lamy O, Hans D (2013) TBS (trabecular bone score) and diabetes-related fracture risk. J Clin Endocrinol Metab 98:602–609. https://doi.org/10.1210/jc.2012-3118
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/s00198-018-4678-3
Samelson EJ, Demissie S, Cupples LA, Zhang X, Xu H, Liu CT, 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.3240
Farr JN, Drake MT, Amin S, Melton LJ III, McCready LK, Khosla S (2014) In vivo assessment of bone quality in postmenopausal women with type 2 diabetes. J Bone Miner Res 29:787–795
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/s00198-014-2676-7
Holloway-Kew KL, De Abreu LLF, Kotowicz MA et al (2019) Bone turnover markers in men and women with impaired fasting glucose and diabetes. Calcif Tissue Int 104:599–604. https://doi.org/10.1007/s00223-019-00527-y
Rubin MR, Patsch JM (2016) Assessment of bone turnover and bone quality in type 2 diabetic bone disease: current concepts and future directions. Bone Res 4:16001. https://doi.org/10.1038/boneres.2016.1
Choi YJ, Ock SY, Jin Y, Lee JS, Kim SH, Chung YS (2018) Urinary Pentosidine levels negatively associates with trabecular bone scores in patients with type 2 diabetes mellitus. Osteoporos Int 29:907–915. https://doi.org/10.1007/s00198-017-4359-7
Funding
The study was supported by the Victorian Health Promotion Foundation, National Health and Medical Research Council (NHMRC), Australia (Projects 251638 and 628582), and the Geelong Regional Medical Foundation. KLH-K is supported by an Alfred Deakin Postdoctoral Research Fellowship, Deakin University. LLFA is supported by a Deakin University Postgraduate Award. MAS is supported by a Deakin University stipend via the IMPACT Strategic Research Centre.
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Holloway-Kew, K., Marijanovic, N., De Abreu, L. et al. Bone mineral density in diabetes and impaired fasting glucose. Osteoporos Int 30, 1799–1806 (2019). https://doi.org/10.1007/s00198-019-05108-1
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DOI: https://doi.org/10.1007/s00198-019-05108-1