Full Length ArticleImpact microindentation in men with impaired fasting glucose and type 2 diabetes
Introduction
It has been reported in many studies that individuals with type 2 diabetes (T2DM) are at an increased risk of fracture [[1], [2], [3], [4], [5], [6], [7]]. This is despite individuals with T2DM having increased bone mineral density (BMD) compared to those without T2DM, which is counter-intuitive to the observed increase in fracture risk [1,6,[8], [9], [10], [11]].
Other measures have been useful in detecting differences in bone that occur in patients with T2DM that might render the bone more susceptible to fracture. One such example is trabecular bone score (TBS), which provides an indication of trabecular microarchitecture [12]. Two recent studies have reported that TBS is lower in postmenopausal women with T2DM compared to those without T2DM [13,14]. Another study has reported that TBS values are also lower women in a wider age range (aged 30–90 years) with T2DM [15]. Lower TBS values have also been reported for men with T2DM. Two studies, one from Korea and another from Australia, showed lower TBS values in men, as well as women, with T2DM compared to those without T2DM [16,17]. However, one study including both older men and women has reported no differences in TBS between those with and without T2DM [18]. One possible reason for this differing observation could be that only individuals with T2DM <5 years duration and not taking insulin were included in the study, and there may have been insufficient time for T2DM-related bone changes to develop. One other Korean study involving postmenopausal women with T2DM has reported that TBS is also useful for differentiating between those with and without vertebral fractures [19]. That study showed women with T2DM and vertebral fractures had a lower TBS than women with T2DM and no vertebral fractures.
Impact microindentation (IMI) measurement is another possible technique for assessing bone fragility in individuals with T2DM. These measurements are performed using the OsteoProbe [20], and involve indenting the bone surface of the tibial plateau, and measuring the depth the probe tip penetrates into the bone. The device measures the indentation distance from the starting position (resting on the surface of the bone at 10 N) to the maximum depth upon an impact load (~40 N). The indentation distance is standardised by comparison to a plastic reference material (poly methyl methacrylate) and expressed as bone material strength index, or BMSi.
To date, three studies have reported lower BMSi values for those with T2DM compared to controls [[21], [22], [23]]. All studies included women only and two had small sample sizes. Another study examined differences in BMSi values between participants with recently diagnosed T2DM (<5 years), prediabetes and controls [18]. The authors reported that there were no differences in BMSi values for white individuals across the glycaemia groups, however, there were differences observed between black individuals with T2DM and normoglycaemia. Further studies with larger sample sizes are needed to confirm these observations. Another recent study also showed no differences in BMSi between men and women with and without T2DM [24]. Additionally, only one of the studies [18] examined whether BMSi values differed between individuals with moderately elevated fasting glucose levels; i.e. prediabetes or impaired fasting glucose (IFG). The reasons for the differing results observed in these previous studies could be related to the inclusion/exclusion criteria employed. One of the studies that showed no differences in BMSi [18] excluded participants with T2DM duration ≥5 years and those that used insulin. Additionally, the two studies that showed no differences in BMSi both included pooled data from men and women [18,24], while the other studies included postmenopausal women only. These studies detected no differences in BMSi values between men and women and thus analysed the two sexes together, but the impact of T2DM on BMSi values may differ between men and women. Several differences between men and women have been noted, in particular, men are considered to have a higher risk of developing T2DM and are diagnosed at a younger age and lower level of obesity [25]. In addition, it has been reported that the increased risk of T2DM-related cardiovascular complications is greater in women than men [26].
Therefore, the aim of this study was to determine the association between BMSi and glycaemia status in a sample of men. A secondary aim was to compare these results with those obtained from dual energy X-ray absorptiometry (DXA; BMD and TBS).
Section snippets
Participants
This study included male participants of the Geelong Osteoporosis Study (GOS), a population-based cohort study of participants residing in the Barwon Statistical Division, located in south-eastern Australia [27]. Participants were randomly selected from Australian electoral rolls and since voting is compulsory in Australia, the electoral roll captures almost all adults in the region. Baseline assessment occurred during 2001–2006 and included 1540 men, aged 20–92 years. The data for this study
Results
Of 625 men who were eligible for inclusion, 471 provided sufficient information to determine glycaemia status. Of these, two had type 1 diabetes and were excluded from the analyses. Of the remaining 469 participants, 340 (72.5%) had the IMI measurement completed. Reasons for non-participation included excessive soft tissues around the mid-tibia (n = 82, two related to oedema), existing skin conditions (n = 19), needle phobia (n = 6), discomfort following first indentation (n = 5) and no reason
Discussion
This study reports that T2DM was associated with a lower BMSi and TBS, however no differences were observed for FNBMD or LSBMD. No differences were detected for the bone measures between men with IFG and normoglycaemia.
Our results are consistent with previous reports in the literature for BMD; that individuals with T2DM have a higher, or normal BMD compared to those without T2DM, despite their increased risk of fracture [1,6,[9], [10], [11],13,34]. Similar to our study, TBS values have been
Conclusion
Men with T2DM had lower BMSi and TBS compared to those without T2DM (normoglycaemia and IFG combined), however there were no differences observed for FNBMD or LSBMD. Bone measures for men with IFG were not different to those with normoglycaemia. Measurements of BMSi and TBS may be better than BMD for detecting bone fragility in individuals with T2DM.
CRediT authorship contribution statement
Kara L. Holloway-Kew: Conceptualisation, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Supervision, Writing - original draft, Writing - review & editing. Amelia Betson: Data curation, Formal analysis, Writing - original draft, Writing - review & editing. Pamela G. Rufus-Membere: Data curation, Investigation, Methodology, Writing - review & editing. James Gaston: Formal analysis, Methodology, Writing - review & editing. Adolfo Diez-Perez: Methodology,
Acknowledgements
The Geelong Osteoporosis Study was supported by grants from the National Health and Medical Research Council (NHMRC; projects 299831, 628582), Amgen-GSK OA-ANZBMS and Amgen Australia, but they played no role in the collection or interpretation of data.
PGR was supported by Deakin University Postgraduate Industry Research Scholarship. KLH-K was supported by an Alfred Deakin Postdoctoral Research Fellowship. AD-P owns shares of Active Life Scientific, Inc., the manufacturer of the reference point
References (50)
- et al.
The diabetic paradox: bone mineral density and fracture in type 2 diabetes
Endocrinol. Nutr.
(2016) - et al.
Bone mineral density in premenopausal Arab women with type 2 diabetes mellitus
J. Clin. Densitom.
(2009) - et al.
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.
(2011) - et al.
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.
(2016) - et al.
Technical note: recommendations for a standard procedure to assess cortical bone at the tissue-level in vivo using impact microindentation
Bone Rep.
(2016) - et al.
Research electronic data capture (REDCap)—a metadata-driven methodology and workflow process for providing translational research informatics support
J. Biomed. Inform.
(2009) - et al.
Lower bone turnover markers in metabolic syndrome and diabetes: the population-based Study of Health in Pomerania
Nutr. Metab. Cardiovasc. Dis.
(2015) - et al.
Fracture risk assessment in patients with diabetes mellitus
J. Clin. Densitom.
(2017) - et al.
Bone mineral density and fracture risk in type-2 diabetes mellitus: the Rotterdam Study
Osteoporos. Int.
(2005) - et al.
Fracture risk in diabetic elderly men: the MrOS study
Diabetologia
(2014)
The association between hyperglycemia and fracture risk in middle age. A prospective, population-based study of 22,444 men and 10,902 women
J. Clin. Endocrinol. Metab.
Association between hyperglycaemia and fracture risk in non-diabetic middle-aged and older Australians: a national, population-based prospective study (AusDiab)
Osteoporos. Int.
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.
High bone mineral density and fracture risk in type 2 diabetes as skeletal complications of inadequate glucose control
Diabetes Care
Fracture risk in women with dysglycaemia: assessing effects of baseline and time-varying risk factors
Calcif. Tissue Int.
Evaluation of bone mineral density in premenopausal women with type-2 diabetes mellitus in Zahedan, Southeast Iran
J. Pak. Med. Assoc.
Bone mineral density in diabetes and impaired fasting glucose
Osteoporos. Int.
Assessment of bone quality with trabecular bone score in type 2 diabetes mellitus: a study from the FRISBEE cohort
Int. J. Clin. Pract.
Comparison of trabecular bone score and hip structural analysis with FRAX(R) in postmenopausal women with type 2 diabetes mellitus
Aging Clin. Exp. Res.
Bone quality assessment in type 2 diabetes mellitus
Osteoporos. Int.
Trabecular bone score as an indicator for skeletal deterioration in diabetes
J. Clin. Endocrinol. Metab.
Trabecular bone score in men and women with impaired fasting glucose and diabetes
Calcif. Tissue Int.
Bone material strength in normoglycemic and hyperglycemic black and white older adults
Osteoporos. Int.
A new device for performing reference point indentation without a reference probe
Rev. Sci. Instrum.
Advanced glycation endproducts and bone material strength in type 2 diabetes
J. Clin. Endocrinol. Metab.
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2022, BoneCitation Excerpt :There are multiple diabetes-related changes to bone that possibly portend a loss of fracture resistance. For example, five different groups reported that the ability of the tibia mid-diaphysis to resist impact micro-indentation using an instrument called the OsteoProbe was lower in adults with type 2 diabetes than those without T2D [102–106]. While the determinants of Bone Material Strength Index (BMSi), the primary measurement of the OsteoProbe, are debatable [107,108], Samakkarnthai et al. [109] observed negative correlations between BMSi and skin AGEs (via autofluorescence) in 171 subjects with T2D (r = −0.30, p < 0.0001) and 108 age-matched subjects without diabetes (r = −0.23, p = 0.020).
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