The Paradoxical Impact of Diabetes Mellitus on Osteoporosis and Sarcopenia: The ParaDOS Study

The Paradoxical Impact of Diabetes Mellitus on Osteoporosis and Sarcopenia: The ParaDOS Study | Research Square window.SnipcartSettings = { analytics: { enabled: false } }; (function() { var accessVector = localStorage.getItem('access_vector') || ''; window.dataLayer = window.dataLayer || []; if (accessVector) { window.dataLayer.push({ user: { profile: { profileInfo: { snid: accessVector } } } }); } })(); (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0],j=d.createElement(s),dl=l!='dataLayer'?'&l='+l:'';j.async=true;j.src='https://www.googletagmanager.com/gtm.js?id='+i+dl;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-K279D39R'); Browse Preprints In Review Journals COVID-19 Preprints AJE Video Bytes Research Tools Research Promotion AJE Professional Editing AJE Rubriq About Preprint Platform In Review Editorial Policies Our Team Advisory Board Help Center Sign In Submit a Preprint Cite Share Download PDF Research Article The Paradoxical Impact of Diabetes Mellitus on Osteoporosis and Sarcopenia: The ParaDOS Study Tülay Tiftik, Murat Kara, Cevriye Mülkoğlu, İrem Çiftçi, Ömer Faruk Çiftçi, and 6 more This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-3091225/v1 This work is licensed under a CC BY 4.0 License Status: Posted Version 1 posted You are reading this latest preprint version Abstract Purpose Type 2 diabetes mellitus (T2DM), osteoporosis (OP) and sarcopenia are major public health problems related with higher fall/fracture risks, morbidity and mortality. Due to the lack of a comprehensive analysis among T2DM, OP and sarcopenia; we aimed to explore the impact of T2DM on OP and sarcopenia in postmenopausal women. Methods This cross-sectional study included postmenopausal women who admitted to the departments of physical & rehabilitation medicine, and endocrinology and metabolism. Demographic data, nutrition/cognition status and frailty scores were recorded. Sarcopenia-related parameters including SARC-F, anterior thigh muscle thickness, handgrip strength, chair stand test, gait speed, and one-leg stand test for balance were measured. ISarcoPRM algorithm was used for the diagnosis of sarcopenia. Results A total of 444 postmenopausal women were consecutively enrolled. T2DM patients (N = 158, 35.6%) had higher frequency of sarcopenia, but lower frequency of OP than controls (both p < 0.05). As regards regression analyses; T2DM - either under the treatment of oral antidiabetic drugs or insulin - had a negative association with presence of OP (about 2 to 3 times lower, respectively). The duration of T2DM had a positive association with sarcopenia and a negative association with balance (all p < 0.05). Conclusion T2DM has paradoxical effects on bone, muscle and balance. Although insulin treatment might have anabolic effects on bone (protecting OP), the disease (duration) itself has negative effects on sarcopenia/balance. Hyperglycemia insulin muscle bone balance quadriceps INTRODUCTION Diabetes mellitus (DM) is a global health problem which affects patients’ physical performance and function, and quality of life, leading to significant morbidity and mortality [ 1 ]. In 2021, there were about 537 million estimated DM patients worldwide, and more than 90% of them were type 2 DM (T2DM) [ 2 ]. Besides its well-known complications on the cardiovascular and renal systems; body composition (bone, muscle and fat tissues), balance and physical performance/function are also impaired in these patients due to not only microvascular complications, but also decline in skeletal muscle dysfunction and physical performance [ 3 ]. Aging and age-related decrease of sex hormones usually leads to chronic conditions such as metabolic syndrome and cardiovascular diseases, loss of skeletal muscle mass and function (i.e. sarcopenia), increased adipose tissue and decreased bone mineral density (BMD) - especially in the postmenopausal period [ 4 ]. In addition to T2DM, both osteoporosis (OP) and sarcopenia are also major public health problems related with higher fall risks, fractures, morbidity, and even premature death [ 4 , 5 ]. It has been shown that abdominal obesity, BMD and sarcopenia are related with hyperinsulinism and insulin resistance, which is typical for T2DM [ 6 – 8 ]. Of note, although BMD is found normal or higher, the fracture risk has increased by 40–70% in T2DM patients [ 9 ] whereby clinical factors such as increased risk of falls, obesity, sarcopenia, and certain anti-diabetic drugs have been considered responsible [ 10 , 11 ]. Although the relationship between sarcopenia and OP has been investigated in postmenopausal women with T2DM in a few studies, the results are conflicting [ 12 – 16 ]. Further, sarcopenia was evaluated by measuring the skeletal muscle loss in several regions e.g. psoas major [ 12 ], gluteus maximus [ 14 ] and quadriceps [ 15 ] muscles in those studies. On the other hand, it is well known that prompt detection of age-related muscle loss can be done by measurement of the quadriceps (i.e. anterior midthigh) muscle [ 4 , 17 ]. To this end, due to the lack of a comprehensive analysis as regards the relationship among T2DM, OP and sarcopenia; in the present study, we aimed to explore the impact of T2DM on the two aforementioned conditions as well as balance of postmenopausal women. METHODS Subjects This cross-sectional study included postmenopausal women who admitted to the departments of physical & rehabilitation medicine, and endocrinology and metabolism at Ankara Education and Research Hospital between July 2022 and December 2022. Women who had any organ (hearth, liver or renal) failure, neuromuscular or rheumatic disease, history of any major orthopedic surgery, and hyperthyroidism and hyperparathyroidism were excluded. All subjects were informed of the study procedure and they were enrolled after they gave written informed consent. The study protocol was approved by the local Ethics Committee (number no: E-93471371-514.99, decision no: E-22-1119). The study was conducted in accordance with the principles of the Declaration of Helsinki. General evaluation Demographic data including age, weight, height, body mass index (BMI), waist and hip circumferences, age at menopause, education level, exercise and smoking statuses and accompanying comorbidities (e.g., hypertension and hypothyroidism) were recorded. Nutrition status was evaluated by Mini Nutritional Assessment short form (MNA-SF) [ 18 ]. Cognitive status was assessed by the Mini‐Mental State Examination (MMSE) [ 19 ]. Frailty was scored according to the Fried’s frailty phenotype whereby score 0 was recorded as “robust”; 1–2 as prefrail and ≥ 3 as “frail” [ 20 ]. To measure the functional balance, one-leg standing time (OLST) up to a maximum of 60 seconds with eyes open was performed on each leg [ 21 ]. Osteoporosis evaluation The BMD measurements were performed from lumbar vertebrae (L1-L4), femoral neck and femoral total regions using dual energy X-ray absorptiometry (DXA) (Hologic Explorer, Hologic Inc. scanner, Bedford, USA). The OP was diagnosed as a BMD T-score of ≤ -2.5 SD at any of the lumbar vertebrae, femoral neck or femoral total regions [ 22 ]. While calculating the mean L1-L4 vertebral T-scores; any abnormal T-score i.e. more than one standard deviation (SD) difference between the T-scores of consecutive vertebrae were excluded, and the mean value of the other three (or at least two) vertebrae was used for the analyses [ 23 ]. Ten-year probability of hip and major osteoporotic fracture risk (by using FRAX tool) was also calculated using the clinical risk factors and femoral neck BMD values [ 24 ]. Ultrasonographic measurements Anterior midthigh (i.e. quadriceps) muscle thickness (MT) (between the anterior superior iliac spine and the superior border of the patella), and rectus abdominus MT and subcutaneous abdominal fat thickness (just 2–3 cm lateral and distal to the umbilicus level) were measured by using a 6–11 MHz linear probe (Nemio XH, Toshiba, Japan) from the dominant hand side [ 25 , 26 ]. The same physiatrist (TT) - who had more than 10 years of experience in the musculoskeletal ultrasound - performed all the measurements. Sarcopenia evaluation The SARC-F (Strength, Assistance with walking, Rise from a chair, Climb stairs and Falls) - a simple questionnaire for screening probable sarcopenic patients - consists of five components. The scores range from 0 to 2 points for each component, and a score of ≥ 4 is predictive of sarcopenia and poor outcomes [ 27 ]. Handgrip strength measurement was performed from the dominant side using a Jamar hydraulic hand dynamometer (Baseline Hydraulic Hand dynamometer Irvington, NY, USA). Physical performance was assessed by chair stand test (CST) and gait speed. After three measurements were obtained, the maximum value for the handgrip strength and the mean values for the performance tests (i.e. CST and gait speed) were used for the analyses. The ISarcoPRM algorithm was used for the diagnosis of sarcopenia [ 4 , 17 ]. Statistical analysis Statistical analyses were performed using SPSS statistical software, version 21.0. Numerical variables are given as mean ± SD or median and first and third quarters in parenthesis (Q1-Q3), and categorical variables are given as frequency and percentage in parenthesis (%). Normal distribution was tested by Kolmogorov-Smirnov test. Comparisons for numerical variables were performed by Student’s t- or Mann-Whitney U test, where appropriate. For comparing the balance tests between the right and left sides within DM patients, paired t-test was used. Categorical variables were compared by Chi-square test. While investigating the possible associations among DM, OP, sarcopenia and clinical parameters (i.e. age, weight, height, menopause duration, education level, smoking and exercise statuses, and presences of hypertension and hypothyroidism, and MMSE and MNA-SF scores); binary logistic regression analyses with backward elimination method were performed. For the relationship between insulin treatment and balance in DM patients, multivariate linear logistic regression analysis (with backward elimination method) was performed. The most parsimonious but statistically significant models were given as the final models. Statistical significance was set at p < 0.05. RESULTS A total of 444 postmenopausal women (aged between 45 to 92 years) were consecutively enrolled in this study. Comparisons of the clinical data of women between T2DM patients (N = 158) and without DM subjects (N = 286) are given in Table 1 . There were no significant differences between the groups regarding age, weight, height, BMI, menopause duration, hip circumference, frequency of smoking, and MMSE and MNA-SF scores (all p > 0.05). Diabetic patients had lower education levels and higher waist circumferences, and higher frequencies of hypertension, hypothyroidism and sarcopenia, but lower frequencies of doing exercise and OP (all p < 0.05). In addition, DM patients had lower OLST (bilateral), subcutaneous abdominal fat thickness, rectus abdominus and anterior thigh MTs as well as worse grip strength, CST, gait speed values and SARC-F and frailty scores when compared to those of the non-diabetic controls (all p < 0.05). Further, DM patients had lower 10-year probabilities of hip and major osteoporotic fracture risks according to FRAX tool (both p < 0.05). Table 1 Comparison of the demographic and clinical characteristics of the subjects (n = 444) Characteristic DM (n = 158) Control (n = 286) p Age (year) 62.1 ± 7.9 61.2 ± 7.4 0.319 Weight (kg) 74.6 ± 11.6 72.8 ± 12.2 0.072 Height (cm) 156.4 ± 5.6 157.1 ± 5.9 0.256 BMI (kg/m 2 ) 30.2 ± 4.4 29.8 ± 4.8 0.136 Menopause duration (year) 14.8 ± 9.3 14.3 ± 9.5 0.496 Education (year) 8 (5–8) 8 (8–8) 0.001 Exercise 0.019 Absent 99 (62.7) 153 (53.5) Mild 25 (15.8) 79 (27.6) Moderate 34 (21.5) 54 (18.9) Smoking 22 (13.9) 46 (16.1) 0.545 Circumference (cm) Waist 98.1 ± 10.3 94.7 ± 10.3 0.001 Hip 111.0 ± 10.7 111.8 ± 13.0 0.110 Comorbidities , n (%) Hypertension 118 (74.7) 117 (40.9) < 0.001 Hypothyroidism 49 (31.0) 60 (21.0) 0.019 BMD , g/cm 2 L1-L4 0.857 ± 0.1331 0.805 ± 0.127 < 0.001 Femoral neck 0.754 ± 0.131 0.714 ± 0.112 0.001 Femoral total 0.814 ± 0.141 0.772 ± 0.119 0.005 Osteoporosis 53 (33.5) 145 (50.7) < 0.001 MMSE 26.7 ± 3.6 26.6 ± 3.9 0.833 MNA-SF 12.3 ± 2.1 12.4 ± 2.0 0.536 Outcome measurements OLST, right 6.9 ± 3.2 8.4 ± 2.7 < 0.001 OLST, left 7.0 ± 3.1 8.3 ± 2.7 < 0.001 Abdominal fat thickness (mm) 40.4 ± 11.4 43.2 ± 12.0 0.017 RA MT (mm) 6.9 ± 1.6 7.3 ± 1.5 0.014 Anterior thigh MT (mm) 32.0 ± 6.3 33.6 ± 6.6 0.017 Grip strength (kg) 21.1 ± 4.2 22.0 ± 4.3 0.046 CST (sec) 11.1 ± 3.3 10.1 ± 2.5 0.007 Gait speed (m/sec) 1.00 ± 0.24 1.05 ± 0.21 0.023 SARC-F 4 (3–7) 4 (2–5) < 0.001 Frailty score 3 (2–3) 3 (1–3) 0.011 Sarcopenia 33 (20.9) 37 (12.9) 0.028 FRAX score Hip fx risk 0.4 (0.2–1.1) 0.6 (0.3–1.7) 0.005 Major osteoporotic fx risk 4.1 (3.3–6.3) 4.7 (3.6–7.1) 0.016 Data are given as mean ± standard deviation, median first and third quarters (Q1-Q3) or number and percentage (%). BMI; body mass index, BMD; bone mineral density, MMSE; mini-mental state examination test, MNA-SF; mini-nutritional assessment short-form, OLST; one-leg standing time test, RA; rectus abdominus, MT; muscle thickness, CST; chair stand test, fx; fracture Among 52 patients with T2DM using insulin treatment, 13 of them (25.5%) had lowest frequency of OP than patients using oral antidiabetic drugs (OAD) (N = 40; 37.7%) or non-diabetic controls (N = 145; 50.7%) (p = 0.001). In addition, T2DM patients using insulin treatment had higher frequency of sarcopenia (N = 15; 28.8%) than patients using OAD (N = 18; 17.0%) or non-diabetic controls (N = 37; 12.9%) (p = 0.014). As regards binary logistic regression analyses (Table 2 ); menopause duration was positively related with the presence of OP, but weight and presence of DM under the treatment of OAD and insulin were negatively associated with the OP (all p < 0.05). On the other hand; age, body weight and duration of DM were positively related with the presence of sarcopenia (all p < 0.05). Table 2 Binary logistic regression model for predicting osteoporosis (n = 444) Parameter OR 95% CI p Menopause duration 1.054 1.030–1.078 < 0.001 Weight 0.957 0.940–0.975 0.001 DM using OAD* 0.588 0.362–0.956 0.032 DM using insulin* 0.296 0.146–0.620 0.001 OR; odds ratio, CI; confidence interval, DM; diabetes mellitus, OAD; oral antidiabetic drug. Statistically significant variables are shown as bold. *According to the non-diabetic controls. As the right and left sides’ OLST results were found to be similar in all 444 participants (p > 0.05), the right sides’ values were chosen for the multivariate linear regression analysis (Table 3 ). Age (β=-0.321), duration of DM (β=-0.192), use of insulin (β=-130) and body weight (β=-0.113) were negatively related with OLST values, whereas height was positively (β = 0.115) related with OLST values (all p < 0.05). Table 3 Binary logistic regression model for predicting sarcopenia (n = 444) Parameter OR 95% CI P Age 1.081 1.042–1.122 < 0.001 Weight 1.055 1.030–1.081 < 0.001 Height 0.950 0.901–1.003 0.062 Duration of DM 1.039 1.009–1.071 0.012 OR; odds ratio, CI; confidence interval, DM; diabetes mellitus Statistically significant variables are shown as bold. DISCUSSION In this study, when compared to healthy controls; T2DM - either under the treatment of OAD or insulin - was found to have negative associations with the presence of OP (about 2 to 3 times lower, respectively). Additionally, the duration of T2DM had a positive association with the presence of sarcopenia and a negative association with balance. A recent meta-analysis has shown that sarcopenia was frequent in T2DM patients with a pooled prevalence of 18% [ 28 ]. In our study, we also found a similar frequency (20.9%) in our DM population. The meta-analysis reported that different diagnostic criteria and tests, definition of sarcopenia and the population (e.g. postmenopausal women as in our study) may affect the prevalence of sarcopenia. Similar to the relevant literature [ 29 , 30 ], we found that all sarcopenia-related parameters (i.e., SARC-F, anterior thigh MT, handgrip strength, CST and gait speed values) were worse in diabetic patients than non-diabetic subjects. Other than older age, and increased weight and duration of DM had positive and independent impact concerning the presence of sarcopenia. Recently, it has been shown that the presence of DM was negatively related with handgrip strength values [ 17 ]. Moreover, a longitudinal study has also reported that chronic conditions such as cardiovascular disease, hypertension and DM were associated with a rapid decline of handgrip strength [ 31 ]. Although hyperinsulinemia might have an anabolic effect in the skeletal system, uncontrolled or progressive T2DM might negatively affect the skeletal muscle mass and physical function. Herein, possible mechanisms of sarcopenia and balance problems in T2DM comprise increased levels of reactive oxygen radc, loss of alpha motor neurons, central, peripheral and autonomic neuropathies, hyperglycemia, insulin resistance, chronic inflammation, and declines in the number of radicals, neuromuscular junctions, and hormonal changes (i.e., estrogen, insulin, and adrenocorticotropic hormone) [ 28 ]. Needless to say, the deleterious effects of DM on the peripheral nervous system are well-known - although not assessed in our study. Osteoporosis (OP) can develop with aging, especially after menopause. The pertinent risk factors include - but not confined to - older age, low body weight, physical inactivity, and smoking [ 32 ]. On the other hand, while overweight and obesity are positively correlated with BMD (i.e. protective against the OP); together with hyperinsulinemia, they are also risk factors for T2DM [ 33 ]. A study including 313 postmenopausal women has found that DM patients had higher BMD values than non-diabetic women [ 12 ]. A meta-analysis has also shown that T2DM patients had higher BMD levels (about 25–50% SD) than non-diabetic subjects - independent of the age, gender, BMI, skeletal site measurement or medication use [ 9 ]. It is noteworthy that higher BMD in DM patients - probably independent of increased skeletal loading - can be caused by hormonal changes such as hyperinsulinemia, adipokines, leptin, and drug use (thiazide, exogenous statin, insulin, etc.) [ 9 ]. Moreover, higher weight or BMI, hyperinsulinemia, performing less exercise or physical inactivity, smoking and use of diuretics and statins are more common in diabetic patients, and they might influence the bone metabolism (9). In our study, DM patients had similar age, body weight and BMI, and lower frequency of OP, whereas they had higher waist circumferences, and higher frequency of sarcopenia and lower balance test values when compared to non-diabetics. Although BMD increases in T2DM patients even after adjustment for BMI in numerous cohort studies [ 9 ], paradoxical increase in the risk of fracture (independent of BMD values) has been demonstrated in T2DM [ 34 , 35 ]. In some studies, this increased fracture risk has been attributed to the deterioration of bone quality in T2DM [ 11 , 36 ]. Notably, despite the preserved BMD in T2DM, sarcopenia and balance problems can - for sure - increase the risk of falls and fractures [ 30 ]. The mechanism is multifactorial, including bone fragility and extra-skeletal factors such as peripheral neuropathy, retinopathy and microvascular complications of diabetes, and usage of other medications (e.g. insulin and diuretics), and presence of comorbidities (e.g. obesity, sarcopenia and frailty) [ 30 ]. According to our results, presence of T2DM under the treatment of insulin was found to be at least three times protective against the OP, but increased duration of DM was related with sarcopenia and negatively impacted the balance. Therefore, the increased fracture risk might stem from the presence of sarcopenia and balance problems in T2DM. While the abdominal subcutaneous fat tissue was found thinner in DM patients, the waist circumference was wider than the controls. These findings might imply that DM affects intraabdominal (rather than subcutaneous) fat deposition in postmenopausal women with aging [ 12 ]. Patients with T2DM are more prone to sarcopenia and frailty than non-diabetics, and they have decreased extremity muscle strength, balance and aerobic endurance [ 29 ]. Interestingly, we found that frailty scores were found higher in DM patients, while their nutritional and cognition statuses were found similar to non-diabetic subjects. These may actually indicate that T2DM affects skeletal muscle mass and function, and physical performance (including balance, endurance, and gait speed) which accelerates sarcopenia, frailty and balance problems in DM - eventually increasing falls and fractures [ 29 ]. Likewise, poor walking speed and CST performance were shown to be related with higher risk of falls and fractures [ 37 ]. The CST evaluates muscle power and strength, and balance and endurance of the lower extremity muscles, which are closely associated with power required daily life activities such as speed walking, standing from a chair and climbing stairs [ 4 , 17 ]. Studies have shown that the risk of hip fracture is increased in T2DM patients [ 38 ], which may be due to increased falls caused by age- and chronic disease related loss of skeletal muscle mass (i.e., sarcopenia) and deterioration in balance [ 5 , 8 , 25 ]. In addition, poor glycemic control and/or longer duration of DM can increase fracture risk due to microstructural changes of the bone in DM patients with microvascular complications [ 39 ]. It has been shown that the fracture risk is not increased within the first five years of T2DM [ 40 ], and that high risk of fracture is observed only in patients with at least 10 years of DM [ 41 ]. In our study, we found that the duration of DM was positively related with the presence of sarcopenia and negatively related with balance, which may increase the risk of falls and fractures. On the other hand, we found that DM patients had lower 10-year probability of fracture risk calculated with FRAX tool, which could be perceived as a limitation or underestimation of the FRAX. Of note, it was found that the fracture risk in T2DM calculated with FRAX is equal to adding 10 years of age or decreasing the BMD T-score by 0.5 SD [ 42 ]. There are a few limitations of this study. The frequency of sarcopenia (15.8%) was found lower than the frequency of OP (44.6%) in our relatively young postmenopausal population. Therefore, the association of DM was found to be more prominent on OP than on sarcopenia. Although the age range of our subjects (around 61.5 years) was compatible with OP, sarcopenia, falls and fractures, and balance problems are more likely to ensue in older (geriatric) postmenopausal DM patients. Additionally, the lack of electrophysiological studies for peripheral neuropathy or the absence of any history taking for microvascular complications related to T2DM would be other limitations of this study. Lastly, our study design was cross-sectional and further larger and longitudinal studies are indisputably needed to examine the effects of DM and other medications on the risk of sarcopenia, OP, balance, and falls and fractures. CONCLUSIONS The T2DM has different paradoxical effects on bone, skeletal muscle mass and function, and balance. Although insulin treatment might have anabolic effects on bone, the disease itself and its duration have negative effects on the skeletal and neuromuscular system (causing decreased bone quality, sarcopenia and balance problems), possibly explaining the increased fall and fracture risks. Future longitudinal studies are warranted to uncover the riddle of DM, OP and sarcopenia in different (patient) populations. Declarations Author Contributions: Conceptualization, T.T. and M.K.; methodology, T.T., M.K. and B.K.; software, M.K.; validation, M.K. and C.M; formal analysis, B.K. and L.Ö; investigation, M.K. and T.T.; resources, T.T., İ.Ç., Ö.F.Ç and M.K.; data curation, T.T., M.K., C.M., M.E.D., Ö.K., H.G., İ.Ç., Ş.M.K. and Ö.F.Ç.; writing—original draft preparation, T.T., M.K., B.K. and L.Ö.; writing—review and editing, T.T., M.K., B.K., L.Ö.; visualization, M.K., B.K. and T.T.; supervision, T.T., M.K., L.Ö., H.G.; project administration, T.T., M.K., C.M.,L.Ö. All authors have read and agreed to the published version of the manuscript. Conflicts of Interest: The authors declare no conflicts of interest. Funding: None References R. Ramtahal, C. Khan, K. Maharaj-Khan et al., Prevalence of self-reported sleep duration and sleep habits in type 2 diabetes patients in South Trinidad. J. Epidemiol. Glob Health. 5 , 35–43 (2015) H. Sun, P. Saeedi, S. 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Osteoporos. 15 , 173 (2020) S.L. Ferrari, B. Abrahamsen, N. Napoli et al., Diagnosis and management of bone fragility in diabetes: an emerging challenge. Osteoporos. Int. 29 , 2585–2596 (2018) J.A. Kanis, Assessment of osteoporosis at the primary health care level. World Health Organization Scientific Group (University of Sheffield, WHO Collaborating Centre for Metabolic Bone Diseases, 2008) R.Q. Ivers, R.G. Cumming, P. Mitchell et al., Diabetes and risk of fracture: The Blue Mountains Eye Study. Diabetes Care. 24 , 1198–1203 (2001) V.V. Shanbhogue, S. Hansen, M. Frost et al., Compromised cortical bone compartment in type 2 diabetes mellitus patients with microvascular disease. Eur. J. Endocrinol. 174 , 115–124 (2016) A.V. Schwartz, E. Vittinghoff, D.C. Bauer et al., Association of BMD and FRAX score with risk of fracture in older adults with type 2 diabetes. 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Tiftik","email":"data:image/png;base64,iVBORw0KGgoAAAANSUhEUgAAAZAAAAAyAQMAAABI0h/eAAAABlBMVEX///8AAABVwtN+AAAACXBIWXMAAA7EAAAOxAGVKw4bAAAA10lEQVRIiWNgGAWjYDCCA0CcYMPAI8HeAGQZWBCjhZmxISHNgEeCB6TZQIJILQxpBgwSEgkgLhFa+G6fP/7gQcIfGcmZz69u+FEgwcDf3p2AV4vkuWSgwxIMeKSlc8pu9gAdJnHm7Aa8WgzOAB2W+MOAR046J+0GD1CLgUQuEVpAtshJnkm7+YckLdIS7MduE2WL5BlmwxkJCcY8kj05bLdlDCR4CPqF7wzjg48/EuTsJY4ff3bzzR8bOf72XvxakACPAZgkVjkIsD8gRfUoGAWjYBSMIAAAQNVEzJ8LWj4AAAAASUVORK5CYII=","orcid":"https://orcid.org/0000-0001-8748-1561","institution":"Ankara Training and Research Hospital: Saglik Bakanligi Ankara Egitim ve Arastirma Hastanesi","correspondingAuthor":true,"submittingAuthor":false,"prefix":"","firstName":"Tülay","middleName":"","lastName":"Tiftik","suffix":""},{"id":215047865,"identity":"a2169fe6-7821-4b96-9dbb-8f8f235249d7","order_by":1,"name":"Murat Kara","email":"","orcid":"","institution":"Hacettepe Universitesi Tip 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Hastanesi","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Mahmut","middleName":"Esad","lastName":"Durmuş","suffix":""},{"id":215047870,"identity":"a4359ee7-4bd1-4d6e-be20-d078bd618f22","order_by":6,"name":"Özgür Kara","email":"","orcid":"","institution":"Dr Abdurrahman Yurtaslan Onkoloji Eğitim ve Araştırma Hastanesi: Ankara Dr Abdurrahman Yurtaslan Onkoloji Egitim ve Arastirma Hastanesi","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Özgür","middleName":"","lastName":"Kara","suffix":""},{"id":215047871,"identity":"e95ec8ce-b1bd-47a0-b51c-303335d1af27","order_by":7,"name":"Şerife Mehlika Kuşkonmaz","email":"","orcid":"","institution":"Sağlık Bakanlığı Ankara Eğitim ve Araştırma Hastanesi: Saglik Bakanligi Ankara Egitim ve Arastirma Hastanesi","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Şerife","middleName":"Mehlika","lastName":"Kuşkonmaz","suffix":""},{"id":215047872,"identity":"3b68aabc-06bb-478a-a2b2-4807fa76d66b","order_by":8,"name":"Hakan Genç","email":"","orcid":"","institution":"Sağlık Bakanlığı Ankara Eğitim ve Araştırma Hastanesi: Saglik Bakanligi Ankara Egitim ve Arastirma Hastanesi","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Hakan","middleName":"","lastName":"Genç","suffix":""},{"id":215047873,"identity":"236d5e8b-f0d7-4fd9-b4ab-cd1f3e5003e8","order_by":9,"name":"Bayram Kaymak","email":"","orcid":"","institution":"Hacettepe Universitesi Tip Fakultesi","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Bayram","middleName":"","lastName":"Kaymak","suffix":""},{"id":215047874,"identity":"3150eef9-6dd8-4042-b8a0-10cc31f52674","order_by":10,"name":"Levent Özçakar","email":"","orcid":"","institution":"Hacettepe Universitesi Tip Fakultesi","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Levent","middleName":"","lastName":"Özçakar","suffix":""}],"badges":[],"createdAt":"2023-06-21 09:15:01","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-3091225/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-3091225/v1","draftVersion":[],"editorialEvents":[],"editorialNote":"","failedWorkflow":false,"files":[{"id":42218327,"identity":"177165b6-3a3c-49a5-b349-7c2bfb2200f8","added_by":"auto","created_at":"2023-08-28 06:51:29","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":426135,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-3091225/v1/63b43caf-d087-46e4-b7bf-df7cb4b24e74.pdf"}],"financialInterests":"","formattedTitle":"The Paradoxical Impact of Diabetes Mellitus on Osteoporosis and Sarcopenia:\nThe ParaDOS Study","fulltext":[{"header":"INTRODUCTION","content":"\u003cp\u003eDiabetes mellitus (DM) is a global health problem which affects patients\u0026rsquo; physical performance and function, and quality of life, leading to significant morbidity and mortality [\u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e1\u003c/span\u003e]. In 2021, there were about 537\u0026nbsp;million estimated DM patients worldwide, and more than 90% of them were type 2 DM (T2DM) [\u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2\u003c/span\u003e]. Besides its well-known complications on the cardiovascular and renal systems; body composition (bone, muscle and fat tissues), balance and physical performance/function are also impaired in these patients due to not only microvascular complications, but also decline in skeletal muscle dysfunction and physical performance [\u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e3\u003c/span\u003e].\u003c/p\u003e \u003cp\u003eAging and age-related decrease of sex hormones usually leads to chronic conditions such as metabolic syndrome and cardiovascular diseases, loss of skeletal muscle mass and function (i.e. sarcopenia), increased adipose tissue and decreased bone mineral density (BMD) - especially in the postmenopausal period [\u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e4\u003c/span\u003e]. In addition to T2DM, both osteoporosis (OP) and sarcopenia are also major public health problems related with higher fall risks, fractures, morbidity, and even premature death [\u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e4\u003c/span\u003e, \u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e5\u003c/span\u003e]. It has been shown that abdominal obesity, BMD and sarcopenia are related with hyperinsulinism and insulin resistance, which is typical for T2DM [\u003cspan additionalcitationids=\"CR7\" citationid=\"CR6\" class=\"CitationRef\"\u003e6\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e8\u003c/span\u003e]. Of note, although BMD is found normal or higher, the fracture risk has increased by 40\u0026ndash;70% in T2DM patients [\u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e9\u003c/span\u003e] whereby clinical factors such as increased risk of falls, obesity, sarcopenia, and certain anti-diabetic drugs have been considered responsible [\u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e10\u003c/span\u003e, \u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e11\u003c/span\u003e].\u003c/p\u003e \u003cp\u003eAlthough the relationship between sarcopenia and OP has been investigated in postmenopausal women with T2DM in a few studies, the results are conflicting [\u003cspan additionalcitationids=\"CR13 CR14 CR15\" citationid=\"CR12\" class=\"CitationRef\"\u003e12\u003c/span\u003e\u0026ndash;\u003cspan citationid=\"CR16\" class=\"CitationRef\"\u003e16\u003c/span\u003e]. Further, sarcopenia was evaluated by measuring the skeletal muscle loss in several regions e.g. psoas major [\u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e12\u003c/span\u003e], gluteus maximus [\u003cspan citationid=\"CR14\" class=\"CitationRef\"\u003e14\u003c/span\u003e] and quadriceps [\u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e15\u003c/span\u003e] muscles in those studies. On the other hand, it is well known that prompt detection of age-related muscle loss can be done by measurement of the quadriceps (i.e. anterior midthigh) muscle [\u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e4\u003c/span\u003e, \u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e17\u003c/span\u003e].\u003c/p\u003e \u003cp\u003eTo this end, due to the lack of a comprehensive analysis as regards the relationship among T2DM, OP and sarcopenia; in the present study, we aimed to explore the impact of T2DM on the two aforementioned conditions as well as balance of postmenopausal women.\u003c/p\u003e"},{"header":"METHODS","content":"\u003cdiv id=\"Sec3\" class=\"Section2\"\u003e \u003ch2\u003eSubjects\u003c/h2\u003e \u003cp\u003eThis cross-sectional study included postmenopausal women who admitted to the departments of physical \u0026amp; rehabilitation medicine, and endocrinology and metabolism at Ankara Education and Research Hospital between July 2022 and December 2022. Women who had any organ (hearth, liver or renal) failure, neuromuscular or rheumatic disease, history of any major orthopedic surgery, and hyperthyroidism and hyperparathyroidism were excluded. All subjects were informed of the study procedure and they were enrolled after they gave written informed consent. The study protocol was approved by the local Ethics Committee (number no: E-93471371-514.99, decision no: E-22-1119). The study was conducted in accordance with the principles of the Declaration of Helsinki.\u003c/p\u003e \u003cdiv id=\"Sec4\" class=\"Section3\"\u003e \u003ch2\u003eGeneral evaluation\u003c/h2\u003e \u003cp\u003eDemographic data including age, weight, height, body mass index (BMI), waist and hip circumferences, age at menopause, education level, exercise and smoking statuses and accompanying comorbidities (e.g., hypertension and hypothyroidism) were recorded. Nutrition status was evaluated by Mini Nutritional Assessment short form (MNA-SF) [\u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e18\u003c/span\u003e]. Cognitive status was assessed by the Mini‐Mental State Examination (MMSE) [\u003cspan citationid=\"CR19\" class=\"CitationRef\"\u003e19\u003c/span\u003e]. Frailty was scored according to the Fried\u0026rsquo;s frailty phenotype whereby score 0 was recorded as \u0026ldquo;robust\u0026rdquo;; 1\u0026ndash;2 as prefrail and \u0026ge;\u0026thinsp;3 as \u0026ldquo;frail\u0026rdquo; [\u003cspan citationid=\"CR20\" class=\"CitationRef\"\u003e20\u003c/span\u003e]. To measure the functional balance, one-leg standing time (OLST) up to a maximum of 60 seconds with eyes open was performed on each leg [\u003cspan citationid=\"CR21\" class=\"CitationRef\"\u003e21\u003c/span\u003e].\u003c/p\u003e \u003c/div\u003e \u003c/div\u003e \u003cdiv id=\"Sec5\" class=\"Section2\"\u003e \u003ch2\u003eOsteoporosis evaluation\u003c/h2\u003e \u003cp\u003eThe BMD measurements were performed from lumbar vertebrae (L1-L4), femoral neck and femoral total regions using dual energy X-ray absorptiometry (DXA) (Hologic Explorer, Hologic Inc. scanner, Bedford, USA). The OP was diagnosed as a BMD T-score of \u0026le; -2.5 SD at any of the lumbar vertebrae, femoral neck or femoral total regions [\u003cspan citationid=\"CR22\" class=\"CitationRef\"\u003e22\u003c/span\u003e]. While calculating the mean L1-L4 vertebral T-scores; any abnormal T-score i.e. more than one standard deviation (SD) difference between the T-scores of consecutive vertebrae were excluded, and the mean value of the other three (or at least two) vertebrae was used for the analyses [\u003cspan citationid=\"CR23\" class=\"CitationRef\"\u003e23\u003c/span\u003e]. Ten-year probability of hip and major osteoporotic fracture risk (by using FRAX tool) was also calculated using the clinical risk factors and femoral neck BMD values [\u003cspan citationid=\"CR24\" class=\"CitationRef\"\u003e24\u003c/span\u003e].\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec6\" class=\"Section2\"\u003e \u003ch2\u003eUltrasonographic measurements\u003c/h2\u003e \u003cp\u003eAnterior midthigh (i.e. quadriceps) muscle thickness (MT) (between the anterior superior iliac spine and the superior border of the patella), and rectus abdominus MT and subcutaneous abdominal fat thickness (just 2\u0026ndash;3 cm lateral and distal to the umbilicus level) were measured by using a 6\u0026ndash;11 MHz linear probe (Nemio XH, Toshiba, Japan) from the dominant hand side [\u003cspan citationid=\"CR25\" class=\"CitationRef\"\u003e25\u003c/span\u003e, \u003cspan citationid=\"CR26\" class=\"CitationRef\"\u003e26\u003c/span\u003e]. The same physiatrist (TT) - who had more than 10 years of experience in the musculoskeletal ultrasound - performed all the measurements.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec7\" class=\"Section2\"\u003e \u003ch2\u003eSarcopenia evaluation\u003c/h2\u003e \u003cp\u003eThe SARC-F (Strength, Assistance with walking, Rise from a chair, Climb stairs and Falls) - a simple questionnaire for screening probable sarcopenic patients - consists of five components. The scores range from 0 to 2 points for each component, and a score of \u0026ge;\u0026thinsp;4 is predictive of sarcopenia and poor outcomes [\u003cspan citationid=\"CR27\" class=\"CitationRef\"\u003e27\u003c/span\u003e]. Handgrip strength measurement was performed from the dominant side using a Jamar hydraulic hand dynamometer (Baseline Hydraulic Hand dynamometer Irvington, NY, USA). Physical performance was assessed by chair stand test (CST) and gait speed. After three measurements were obtained, the maximum value for the handgrip strength and the mean values for the performance tests (i.e. CST and gait speed) were used for the analyses. The ISarcoPRM algorithm was used for the diagnosis of sarcopenia [\u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e4\u003c/span\u003e, \u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e17\u003c/span\u003e].\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec8\" class=\"Section2\"\u003e \u003ch2\u003eStatistical analysis\u003c/h2\u003e \u003cp\u003eStatistical analyses were performed using SPSS statistical software, version 21.0. Numerical variables are given as mean\u0026thinsp;\u0026plusmn;\u0026thinsp;SD or median and first and third quarters in parenthesis (Q1-Q3), and categorical variables are given as frequency and percentage in parenthesis (%). Normal distribution was tested by Kolmogorov-Smirnov test. Comparisons for numerical variables were performed by Student\u0026rsquo;s t- or Mann-Whitney U test, where appropriate. For comparing the balance tests between the right and left sides within DM patients, paired t-test was used. Categorical variables were compared by Chi-square test.\u003c/p\u003e \u003cp\u003eWhile investigating the possible associations among DM, OP, sarcopenia and clinical parameters (i.e. age, weight, height, menopause duration, education level, smoking and exercise statuses, and presences of hypertension and hypothyroidism, and MMSE and MNA-SF scores); binary logistic regression analyses with backward elimination method were performed. For the relationship between insulin treatment and balance in DM patients, multivariate linear logistic regression analysis (with backward elimination method) was performed. The most parsimonious but statistically significant models were given as the final models. Statistical significance was set at p\u0026thinsp;\u0026lt;\u0026thinsp;0.05.\u003c/p\u003e \u003c/div\u003e"},{"header":"RESULTS","content":"\u003cp\u003eA total of 444 postmenopausal women (aged between 45 to 92 years) were consecutively enrolled in this study. Comparisons of the clinical data of women between T2DM patients (N\u0026thinsp;=\u0026thinsp;158) and without DM subjects (N\u0026thinsp;=\u0026thinsp;286) are given in Table\u0026nbsp;\u003cspan refid=\"Tab1\" class=\"InternalRef\"\u003e1\u003c/span\u003e. There were no significant differences between the groups regarding age, weight, height, BMI, menopause duration, hip circumference, frequency of smoking, and MMSE and MNA-SF scores (all p\u0026thinsp;\u0026gt;\u0026thinsp;0.05). Diabetic patients had lower education levels and higher waist circumferences, and higher frequencies of hypertension, hypothyroidism and sarcopenia, but lower frequencies of doing exercise and OP (all p\u0026thinsp;\u0026lt;\u0026thinsp;0.05). In addition, DM patients had lower OLST (bilateral), subcutaneous abdominal fat thickness, rectus abdominus and anterior thigh MTs as well as worse grip strength, CST, gait speed values and SARC-F and frailty scores when compared to those of the non-diabetic controls (all p\u0026thinsp;\u0026lt;\u0026thinsp;0.05). Further, DM patients had lower 10-year probabilities of hip and major osteoporotic fracture risks according to FRAX tool (both p\u0026thinsp;\u0026lt;\u0026thinsp;0.05).\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab1\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 1\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003e\u003cb\u003eComparison of the demographic and clinical characteristics of the subjects (n\u0026thinsp;=\u0026thinsp;444)\u003c/b\u003e\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"4\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c4\" colnum=\"4\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\"\u003e \u003cp\u003eCharacteristic\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c2\"\u003e \u003cp\u003eDM (n\u0026thinsp;=\u0026thinsp;158)\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c3\"\u003e \u003cp\u003eControl (n\u0026thinsp;=\u0026thinsp;286)\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c4\"\u003e \u003cp\u003ep\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003eAge\u003c/b\u003e (year)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e62.1\u0026thinsp;\u0026plusmn;\u0026thinsp;7.9\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e61.2\u0026thinsp;\u0026plusmn;\u0026thinsp;7.4\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e0.319\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003eWeight\u003c/b\u003e (kg)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e74.6\u0026thinsp;\u0026plusmn;\u0026thinsp;11.6\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e72.8\u0026thinsp;\u0026plusmn;\u0026thinsp;12.2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e0.072\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003eHeight\u003c/b\u003e (cm)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e156.4\u0026thinsp;\u0026plusmn;\u0026thinsp;5.6\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e157.1\u0026thinsp;\u0026plusmn;\u0026thinsp;5.9\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e0.256\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003eBMI\u003c/b\u003e (kg/m\u003csup\u003e2\u003c/sup\u003e)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e30.2\u0026thinsp;\u0026plusmn;\u0026thinsp;4.4\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e29.8\u0026thinsp;\u0026plusmn;\u0026thinsp;4.8\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e0.136\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003eMenopause duration\u003c/b\u003e (year)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e14.8\u0026thinsp;\u0026plusmn;\u0026thinsp;9.3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e14.3\u0026thinsp;\u0026plusmn;\u0026thinsp;9.5\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e0.496\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003eEducation\u003c/b\u003e (year)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e8 (5\u0026ndash;8)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e8 (8\u0026ndash;8)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e\u003cb\u003e0.001\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003eExercise\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e\u003cb\u003e0.019\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eAbsent\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e99 (62.7)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e153 (53.5)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eMild\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e25 (15.8)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e79 (27.6)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eModerate\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e34 (21.5)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e54 (18.9)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003eSmoking\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e22 (13.9)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e46 (16.1)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e0.545\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003eCircumference\u003c/b\u003e (cm)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eWaist\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e98.1\u0026thinsp;\u0026plusmn;\u0026thinsp;10.3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e94.7\u0026thinsp;\u0026plusmn;\u0026thinsp;10.3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e\u003cb\u003e0.001\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eHip\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e111.0\u0026thinsp;\u0026plusmn;\u0026thinsp;10.7\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e111.8\u0026thinsp;\u0026plusmn;\u0026thinsp;13.0\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e0.110\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003eComorbidities\u003c/b\u003e, n (%)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eHypertension\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e118 (74.7)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e117 (40.9)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e\u003cb\u003e\u0026lt;\u0026thinsp;0.001\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eHypothyroidism\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e49 (31.0)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e60 (21.0)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e\u003cb\u003e0.019\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003eBMD\u003c/b\u003e, g/cm\u003csup\u003e2\u003c/sup\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eL1-L4\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e0.857\u0026thinsp;\u0026plusmn;\u0026thinsp;0.1331\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e0.805\u0026thinsp;\u0026plusmn;\u0026thinsp;0.127\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e\u003cb\u003e\u0026lt;\u0026thinsp;0.001\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eFemoral neck\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e0.754\u0026thinsp;\u0026plusmn;\u0026thinsp;0.131\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e0.714\u0026thinsp;\u0026plusmn;\u0026thinsp;0.112\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e\u003cb\u003e0.001\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003eFemoral total\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e0.814\u0026thinsp;\u0026plusmn;\u0026thinsp;0.141\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e0.772\u0026thinsp;\u0026plusmn;\u0026thinsp;0.119\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e\u003cb\u003e0.005\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003eOsteoporosis\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e53 (33.5)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e145 (50.7)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e\u003cb\u003e\u0026lt;\u0026thinsp;0.001\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eMMSE\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e26.7\u0026thinsp;\u0026plusmn;\u0026thinsp;3.6\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e26.6\u0026thinsp;\u0026plusmn;\u0026thinsp;3.9\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e0.833\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eMNA-SF\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e12.3\u0026thinsp;\u0026plusmn;\u0026thinsp;2.1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e12.4\u0026thinsp;\u0026plusmn;\u0026thinsp;2.0\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e0.536\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003eOutcome measurements\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eOLST, right\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e6.9\u0026thinsp;\u0026plusmn;\u0026thinsp;3.2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e8.4\u0026thinsp;\u0026plusmn;\u0026thinsp;2.7\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e\u003cb\u003e\u0026lt;\u0026thinsp;0.001\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eOLST, left\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e7.0\u0026thinsp;\u0026plusmn;\u0026thinsp;3.1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e8.3\u0026thinsp;\u0026plusmn;\u0026thinsp;2.7\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e\u003cb\u003e\u0026lt;\u0026thinsp;0.001\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eAbdominal fat thickness (mm)\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e40.4\u0026thinsp;\u0026plusmn;\u0026thinsp;11.4\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e43.2\u0026thinsp;\u0026plusmn;\u0026thinsp;12.0\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e\u003cb\u003e0.017\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eRA MT (mm)\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e6.9\u0026thinsp;\u0026plusmn;\u0026thinsp;1.6\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e7.3\u0026thinsp;\u0026plusmn;\u0026thinsp;1.5\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e\u003cb\u003e0.014\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eAnterior thigh MT (mm)\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e32.0\u0026thinsp;\u0026plusmn;\u0026thinsp;6.3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e33.6\u0026thinsp;\u0026plusmn;\u0026thinsp;6.6\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e\u003cb\u003e0.017\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eGrip strength (kg)\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e21.1\u0026thinsp;\u0026plusmn;\u0026thinsp;4.2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e22.0\u0026thinsp;\u0026plusmn;\u0026thinsp;4.3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e\u003cb\u003e0.046\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eCST (sec)\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e11.1\u0026thinsp;\u0026plusmn;\u0026thinsp;3.3\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e10.1\u0026thinsp;\u0026plusmn;\u0026thinsp;2.5\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e\u003cb\u003e0.007\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eGait speed (m/sec)\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e1.00\u0026thinsp;\u0026plusmn;\u0026thinsp;0.24\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e1.05\u0026thinsp;\u0026plusmn;\u0026thinsp;0.21\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e\u003cb\u003e0.023\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eSARC-F\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e4 (3\u0026ndash;7)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e4 (2\u0026ndash;5)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e\u003cb\u003e\u0026lt;\u0026thinsp;0.001\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eFrailty score\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e3 (2\u0026ndash;3)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e3 (1\u0026ndash;3)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e\u003cb\u003e0.011\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eSarcopenia\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e33 (20.9)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e37 (12.9)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e\u003cb\u003e0.028\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eFRAX score\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e\u0026nbsp;\u003c/td\u003e \u003ctd align=\"left\" colname=\"c4\"\u003e\u0026nbsp;\u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eHip fx risk\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e0.4 (0.2\u0026ndash;1.1)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e0.6 (0.3\u0026ndash;1.7)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e\u003cb\u003e0.005\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cem\u003eMajor osteoporotic fx risk\u003c/em\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e4.1 (3.3\u0026ndash;6.3)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c3\"\u003e \u003cp\u003e4.7 (3.6\u0026ndash;7.1)\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e\u003cb\u003e0.016\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003ctfoot\u003e \u003ctr\u003e\u003ctd colspan=\"4\"\u003eData are given as mean\u0026thinsp;\u0026plusmn;\u0026thinsp;standard deviation, median first and third quarters (Q1-Q3) or number and percentage (%).\u003c/td\u003e\u003c/tr\u003e \u003ctr\u003e\u003ctd colspan=\"4\"\u003eBMI; body mass index, BMD; bone mineral density, MMSE; mini-mental state examination test, MNA-SF; mini-nutritional assessment short-form, OLST; one-leg standing time test, RA; rectus abdominus, MT; muscle thickness, CST; chair stand test, fx; fracture\u003c/td\u003e\u003c/tr\u003e \u003c/tfoot\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003cp\u003eAmong 52 patients with T2DM using insulin treatment, 13 of them (25.5%) had lowest frequency of OP than patients using oral antidiabetic drugs (OAD) (N\u0026thinsp;=\u0026thinsp;40; 37.7%) or non-diabetic controls (N\u0026thinsp;=\u0026thinsp;145; 50.7%) (p\u0026thinsp;=\u0026thinsp;0.001). In addition, T2DM patients using insulin treatment had higher frequency of sarcopenia (N\u0026thinsp;=\u0026thinsp;15; 28.8%) than patients using OAD (N\u0026thinsp;=\u0026thinsp;18; 17.0%) or non-diabetic controls (N\u0026thinsp;=\u0026thinsp;37; 12.9%) (p\u0026thinsp;=\u0026thinsp;0.014).\u003c/p\u003e \u003cp\u003eAs regards binary logistic regression analyses (Table\u0026nbsp;\u003cspan refid=\"Tab2\" class=\"InternalRef\"\u003e2\u003c/span\u003e); menopause duration was positively related with the presence of OP, but weight and presence of DM under the treatment of OAD and insulin were negatively associated with the OP (all p\u0026thinsp;\u0026lt;\u0026thinsp;0.05). On the other hand; age, body weight and duration of DM were positively related with the presence of sarcopenia (all p\u0026thinsp;\u0026lt;\u0026thinsp;0.05).\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab2\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 2\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eBinary logistic regression model for predicting osteoporosis (n\u0026thinsp;=\u0026thinsp;444)\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"4\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c4\" colnum=\"4\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\"\u003e \u003cp\u003eParameter\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c2\"\u003e \u003cp\u003eOR\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c3\"\u003e \u003cp\u003e95% CI\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c4\"\u003e \u003cp\u003ep\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003eMenopause duration\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e1.054\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c3\"\u003e \u003cp\u003e1.030\u0026ndash;1.078\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e\u003cb\u003e\u0026lt;\u0026thinsp;0.001\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003eWeight\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e0.957\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c3\"\u003e \u003cp\u003e0.940\u0026ndash;0.975\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e\u003cb\u003e0.001\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003eDM using OAD*\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e0.588\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c3\"\u003e \u003cp\u003e0.362\u0026ndash;0.956\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e\u003cb\u003e0.032\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003eDM using insulin*\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e0.296\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c3\"\u003e \u003cp\u003e0.146\u0026ndash;0.620\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e\u003cb\u003e0.001\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003ctfoot\u003e \u003ctr\u003e\u003ctd colspan=\"4\"\u003eOR; odds ratio, CI; confidence interval, DM; diabetes mellitus, OAD; oral antidiabetic drug.\u003c/td\u003e\u003c/tr\u003e \u003ctr\u003e\u003ctd colspan=\"4\"\u003eStatistically significant variables are shown as bold.\u003c/td\u003e\u003c/tr\u003e \u003ctr\u003e\u003ctd colspan=\"4\"\u003e*According to the non-diabetic controls.\u003c/td\u003e\u003c/tr\u003e \u003c/tfoot\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003cp\u003eAs the right and left sides\u0026rsquo; OLST results were found to be similar in all 444 participants (p\u0026thinsp;\u0026gt;\u0026thinsp;0.05), the right sides\u0026rsquo; values were chosen for the multivariate linear regression analysis (Table\u0026nbsp;\u003cspan refid=\"Tab3\" class=\"InternalRef\"\u003e3\u003c/span\u003e). Age (β=-0.321), duration of DM (β=-0.192), use of insulin (β=-130) and body weight (β=-0.113) were negatively related with OLST values, whereas height was positively (β\u0026thinsp;=\u0026thinsp;0.115) related with OLST values (all p\u0026thinsp;\u0026lt;\u0026thinsp;0.05).\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab3\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 3\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eBinary logistic regression model for predicting sarcopenia (n\u0026thinsp;=\u0026thinsp;444)\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"4\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\".\" class=\"colspec\" colname=\"c4\" colnum=\"4\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\"\u003e \u003cp\u003eParameter\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c2\"\u003e \u003cp\u003eOR\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c3\"\u003e \u003cp\u003e95% CI\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c4\"\u003e \u003cp\u003eP\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003eAge\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e1.081\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c3\"\u003e \u003cp\u003e1.042\u0026ndash;1.122\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e\u003cb\u003e\u0026lt;\u0026thinsp;0.001\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003eWeight\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e1.055\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c3\"\u003e \u003cp\u003e1.030\u0026ndash;1.081\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e\u003cb\u003e\u0026lt;\u0026thinsp;0.001\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003eHeight\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e0.950\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c3\"\u003e \u003cp\u003e0.901\u0026ndash;1.003\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e0.062\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\"\u003e \u003cp\u003e\u003cb\u003eDuration of DM\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c2\"\u003e \u003cp\u003e1.039\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c3\"\u003e \u003cp\u003e1.009\u0026ndash;1.071\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\".\" colname=\"c4\"\u003e \u003cp\u003e\u003cb\u003e0.012\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003ctfoot\u003e \u003ctr\u003e\u003ctd colspan=\"4\"\u003eOR; odds ratio, CI; confidence interval, DM; diabetes mellitus\u003c/td\u003e\u003c/tr\u003e \u003ctr\u003e\u003ctd colspan=\"4\"\u003eStatistically significant variables are shown as bold.\u003c/td\u003e\u003c/tr\u003e \u003c/tfoot\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e"},{"header":"DISCUSSION","content":"\u003cp\u003eIn this study, when compared to healthy controls; T2DM - either under the treatment of OAD or insulin - was found to have negative associations with the presence of OP (about 2 to 3 times lower, respectively). Additionally, the duration of T2DM had a positive association with the presence of sarcopenia and a negative association with balance.\u003c/p\u003e \u003cp\u003eA recent meta-analysis has shown that sarcopenia was frequent in T2DM patients with a pooled prevalence of 18% [\u003cspan citationid=\"CR28\" class=\"CitationRef\"\u003e28\u003c/span\u003e]. In our study, we also found a similar frequency (20.9%) in our DM population. The meta-analysis reported that different diagnostic criteria and tests, definition of sarcopenia and the population (e.g. postmenopausal women as in our study) may affect the prevalence of sarcopenia. Similar to the relevant literature [\u003cspan citationid=\"CR29\" class=\"CitationRef\"\u003e29\u003c/span\u003e, \u003cspan citationid=\"CR30\" class=\"CitationRef\"\u003e30\u003c/span\u003e], we found that all sarcopenia-related parameters (i.e., SARC-F, anterior thigh MT, handgrip strength, CST and gait speed values) were worse in diabetic patients than non-diabetic subjects. Other than older age, and increased weight and duration of DM had positive and independent impact concerning the presence of sarcopenia. Recently, it has been shown that the presence of DM was negatively related with handgrip strength values [\u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e17\u003c/span\u003e]. Moreover, a longitudinal study has also reported that chronic conditions such as cardiovascular disease, hypertension and DM were associated with a rapid decline of handgrip strength [\u003cspan citationid=\"CR31\" class=\"CitationRef\"\u003e31\u003c/span\u003e]. Although hyperinsulinemia might have an anabolic effect in the skeletal system, uncontrolled or progressive T2DM might negatively affect the skeletal muscle mass and physical function. Herein, possible mechanisms of sarcopenia and balance problems in T2DM comprise increased levels of reactive oxygen radc, loss of alpha motor neurons, central, peripheral and autonomic neuropathies, hyperglycemia, insulin resistance, chronic inflammation, and declines in the number of radicals, neuromuscular junctions, and hormonal changes (i.e., estrogen, insulin, and adrenocorticotropic hormone) [\u003cspan citationid=\"CR28\" class=\"CitationRef\"\u003e28\u003c/span\u003e]. Needless to say, the deleterious effects of DM on the peripheral nervous system are well-known - although not assessed in our study.\u003c/p\u003e \u003cp\u003eOsteoporosis (OP) can develop with aging, especially after menopause. The pertinent risk factors include - but not confined to - older age, low body weight, physical inactivity, and smoking [\u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e32\u003c/span\u003e]. On the other hand, while overweight and obesity are positively correlated with BMD (i.e. protective against the OP); together with hyperinsulinemia, they are also risk factors for T2DM [\u003cspan citationid=\"CR33\" class=\"CitationRef\"\u003e33\u003c/span\u003e]. A study including 313 postmenopausal women has found that DM patients had higher BMD values than non-diabetic women [\u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e12\u003c/span\u003e]. A meta-analysis has also shown that T2DM patients had higher BMD levels (about 25\u0026ndash;50% SD) than non-diabetic subjects - independent of the age, gender, BMI, skeletal site measurement or medication use [\u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e9\u003c/span\u003e]. It is noteworthy that higher BMD in DM patients - probably independent of increased skeletal loading - can be caused by hormonal changes such as hyperinsulinemia, adipokines, leptin, and drug use (thiazide, exogenous statin, insulin, etc.) [\u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e9\u003c/span\u003e]. Moreover, higher weight or BMI, hyperinsulinemia, performing less exercise or physical inactivity, smoking and use of diuretics and statins are more common in diabetic patients, and they might influence the bone metabolism (9). In our study, DM patients had similar age, body weight and BMI, and lower frequency of OP, whereas they had higher waist circumferences, and higher frequency of sarcopenia and lower balance test values when compared to non-diabetics.\u003c/p\u003e \u003cp\u003eAlthough BMD increases in T2DM patients even after adjustment for BMI in numerous cohort studies [\u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e9\u003c/span\u003e], paradoxical increase in the risk of fracture (independent of BMD values) has been demonstrated in T2DM [\u003cspan citationid=\"CR34\" class=\"CitationRef\"\u003e34\u003c/span\u003e, \u003cspan citationid=\"CR35\" class=\"CitationRef\"\u003e35\u003c/span\u003e]. In some studies, this increased fracture risk has been attributed to the deterioration of bone quality in T2DM [\u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e11\u003c/span\u003e, \u003cspan citationid=\"CR36\" class=\"CitationRef\"\u003e36\u003c/span\u003e]. Notably, despite the preserved BMD in T2DM, sarcopenia and balance problems can - for sure - increase the risk of falls and fractures [\u003cspan citationid=\"CR30\" class=\"CitationRef\"\u003e30\u003c/span\u003e]. The mechanism is multifactorial, including bone fragility and extra-skeletal factors such as peripheral neuropathy, retinopathy and microvascular complications of diabetes, and usage of other medications (e.g. insulin and diuretics), and presence of comorbidities (e.g. obesity, sarcopenia and frailty) [\u003cspan citationid=\"CR30\" class=\"CitationRef\"\u003e30\u003c/span\u003e]. According to our results, presence of T2DM under the treatment of insulin was found to be at least three times protective against the OP, but increased duration of DM was related with sarcopenia and negatively impacted the balance. Therefore, the increased fracture risk might stem from the presence of sarcopenia and balance problems in T2DM.\u003c/p\u003e \u003cp\u003eWhile the abdominal subcutaneous fat tissue was found thinner in DM patients, the waist circumference was wider than the controls. These findings might imply that DM affects intraabdominal (rather than subcutaneous) fat deposition in postmenopausal women with aging [\u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e12\u003c/span\u003e]. Patients with T2DM are more prone to sarcopenia and frailty than non-diabetics, and they have decreased extremity muscle strength, balance and aerobic endurance [\u003cspan citationid=\"CR29\" class=\"CitationRef\"\u003e29\u003c/span\u003e]. Interestingly, we found that frailty scores were found higher in DM patients, while their nutritional and cognition statuses were found similar to non-diabetic subjects. These may actually indicate that T2DM affects skeletal muscle mass and function, and physical performance (including balance, endurance, and gait speed) which accelerates sarcopenia, frailty and balance problems in DM - eventually increasing falls and fractures [\u003cspan citationid=\"CR29\" class=\"CitationRef\"\u003e29\u003c/span\u003e]. Likewise, poor walking speed and CST performance were shown to be related with higher risk of falls and fractures [\u003cspan citationid=\"CR37\" class=\"CitationRef\"\u003e37\u003c/span\u003e]. The CST evaluates muscle power and strength, and balance and endurance of the lower extremity muscles, which are closely associated with power required daily life activities such as speed walking, standing from a chair and climbing stairs [\u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e4\u003c/span\u003e, \u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e17\u003c/span\u003e].\u003c/p\u003e \u003cp\u003eStudies have shown that the risk of hip fracture is increased in T2DM patients [\u003cspan citationid=\"CR38\" class=\"CitationRef\"\u003e38\u003c/span\u003e], which may be due to increased falls caused by age- and chronic disease related loss of skeletal muscle mass (i.e., sarcopenia) and deterioration in balance [\u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e5\u003c/span\u003e, \u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e8\u003c/span\u003e, \u003cspan citationid=\"CR25\" class=\"CitationRef\"\u003e25\u003c/span\u003e]. In addition, poor glycemic control and/or longer duration of DM can increase fracture risk due to microstructural changes of the bone in DM patients with microvascular complications [\u003cspan citationid=\"CR39\" class=\"CitationRef\"\u003e39\u003c/span\u003e]. It has been shown that the fracture risk is not increased within the first five years of T2DM [\u003cspan citationid=\"CR40\" class=\"CitationRef\"\u003e40\u003c/span\u003e], and that high risk of fracture is observed only in patients with at least 10 years of DM [\u003cspan citationid=\"CR41\" class=\"CitationRef\"\u003e41\u003c/span\u003e]. In our study, we found that the duration of DM was positively related with the presence of sarcopenia and negatively related with balance, which may increase the risk of falls and fractures. On the other hand, we found that DM patients had lower 10-year probability of fracture risk calculated with FRAX tool, which could be perceived as a limitation or underestimation of the FRAX. Of note, it was found that the fracture risk in T2DM calculated with FRAX is equal to adding 10 years of age or decreasing the BMD T-score by 0.5 SD [\u003cspan citationid=\"CR42\" class=\"CitationRef\"\u003e42\u003c/span\u003e].\u003c/p\u003e \u003cp\u003eThere are a few limitations of this study. The frequency of sarcopenia (15.8%) was found lower than the frequency of OP (44.6%) in our relatively young postmenopausal population. Therefore, the association of DM was found to be more prominent on OP than on sarcopenia. Although the age range of our subjects (around 61.5 years) was compatible with OP, sarcopenia, falls and fractures, and balance problems are more likely to ensue in older (geriatric) postmenopausal DM patients. Additionally, the lack of electrophysiological studies for peripheral neuropathy or the absence of any history taking for microvascular complications related to T2DM would be other limitations of this study. Lastly, our study design was cross-sectional and further larger and longitudinal studies are indisputably needed to examine the effects of DM and other medications on the risk of sarcopenia, OP, balance, and falls and fractures.\u003c/p\u003e"},{"header":"CONCLUSIONS","content":"\u003cp\u003eThe T2DM has different paradoxical effects on bone, skeletal muscle mass and function, and balance. Although insulin treatment might have anabolic effects on bone, the disease itself and its duration have negative effects on the skeletal and neuromuscular system (causing decreased bone quality, sarcopenia and balance problems), possibly explaining the increased fall and fracture risks. Future longitudinal studies are warranted to uncover the riddle of DM, OP and sarcopenia in different (patient) populations.\u003c/p\u003e"},{"header":"Declarations","content":"\u003cp\u003e\u003cstrong\u003eAuthor Contributions:\u003c/strong\u003e Conceptualization, T.T. and M.K.; methodology, T.T., M.K. and B.K.; software, M.K.; validation, M.K. and C.M; formal analysis, B.K. and L.\u0026Ouml;; investigation, M.K. and T.T.; resources, T.T., İ.\u0026Ccedil;., \u0026Ouml;.F.\u0026Ccedil; and M.K.; data curation, T.T., M.K., C.M., M.E.D., \u0026Ouml;.K., H.G., İ.\u0026Ccedil;., Ş.M.K. and \u0026Ouml;.F.\u0026Ccedil;.; writing\u0026mdash;original draft preparation, T.T., M.K., B.K. and L.\u0026Ouml;.; writing\u0026mdash;review and editing, T.T., M.K., B.K., L.\u0026Ouml;.; visualization, M.K., B.K. and T.T.; supervision, T.T., M.K., L.\u0026Ouml;., H.G.; project administration, T.T., M.K., C.M.,L.\u0026Ouml;. All authors have read and agreed to the published version of the manuscript.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eConflicts of Interest:\u003c/strong\u003e The authors declare no conflicts of interest.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eFunding:\u0026nbsp;\u003c/strong\u003eNone\u003cstrong\u003e\u003cbr\u003e\u0026nbsp;\u003c/strong\u003e\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\u003cli\u003e\u003cspan\u003eR. Ramtahal, C. Khan, K. Maharaj-Khan et al., Prevalence of self-reported sleep duration and sleep habits in type 2 diabetes patients in South Trinidad. J. Epidemiol. Glob Health. \u003cb\u003e5\u003c/b\u003e, 35\u0026ndash;43 (2015)\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eH. Sun, P. Saeedi, S. Karuranga et al., IDF Diabetes Atlas: Global, regional and country-level diabetes prevalence estimates for 2021 and projections for 2045. Diabetes Res. Clin. 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Hsu et al., Beyond Sarcopenia: Older adults with type II diabetes mellitus tend to experience an elevated risk of poor dynamic balance-a case-control study. BMC Geriatr. \u003cb\u003e22\u003c/b\u003e, 138 (2022)\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eC. Sarodnik, S.P.G. Bours, N.C. Schaper et al., The risks of sarcopenia, falls and fractures in patients with type 2 diabetes mellitus. Maturitas. \u003cb\u003e109\u003c/b\u003e, 70\u0026ndash;77 (2018)\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eS. Stenholm, K. Tiainen, T. Rantanen et al., Long-term determinants of muscle strength decline: prospective evidence from the 22-year mini-Finland follow-up survey. J. Am. Geriatr. Soc. \u003cb\u003e60\u003c/b\u003e, 77\u0026ndash;85 (2012)\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eT. Tiftik, M. Kara, E.G. Koyuncu et al., The relationship between sarcopenia-related measurements and osteoporosis: The SARCOP study. Osteoporos. Int. \u003cb\u003e34\u003c/b\u003e, 53\u0026ndash;58 (2023)\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eD.E. Bonds, J.C. Larson, A.V. Schwartz et al., Risk of fracture in women with type 2 diabetes: the Women's Health Initiative Observational Study. J. Clin. Endocrinol. Metab. \u003cb\u003e91\u003c/b\u003e, 3404\u0026ndash;3410 (2006)\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eA.V. Schwartz, D.E. Sellmeyer, K.E. Ensrud et al., Older women with diabetes have an increased risk of fracture: a prospective study. J. Clin. Endocrinol. Metab. \u003cb\u003e86\u003c/b\u003e, 32\u0026ndash;38 (2001)\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eE.S. Strotmeyer, J.A. Cauley, A.V. Schwartz et al., 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. \u003cb\u003e165\u003c/b\u003e, 1612\u0026ndash;1617 (2005)\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eC. Eller-Vainicher, E. Cairoli, G. Grassi et al., Pathophysiology and management of type 2 diabetes mellitus bone fragility. J Diabetes Res. 2020, 7608964 (2020)\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eD. Dai, F. Xu, R. Sun et al., Decreased lower-extremity muscle performance is associated with decreased hip bone mineral density and increased estimated fracture risk in community-dwelling postmenopausal women. Arch. Osteoporos. \u003cb\u003e15\u003c/b\u003e, 173 (2020)\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eS.L. Ferrari, B. Abrahamsen, N. Napoli et al., Diagnosis and management of bone fragility in diabetes: an emerging challenge. Osteoporos. Int. \u003cb\u003e29\u003c/b\u003e, 2585\u0026ndash;2596 (2018)\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eJ.A. Kanis, \u003cem\u003eAssessment of osteoporosis at the primary health care level. World Health Organization Scientific Group\u003c/em\u003e (University of Sheffield, WHO Collaborating Centre for Metabolic Bone Diseases, 2008)\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eR.Q. Ivers, R.G. Cumming, P. Mitchell et al., Diabetes and risk of fracture: The Blue Mountains Eye Study. Diabetes Care. \u003cb\u003e24\u003c/b\u003e, 1198\u0026ndash;1203 (2001)\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eV.V. Shanbhogue, S. Hansen, M. Frost et al., Compromised cortical bone compartment in type 2 diabetes mellitus patients with microvascular disease. Eur. J. Endocrinol. \u003cb\u003e174\u003c/b\u003e, 115\u0026ndash;124 (2016)\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eA.V. Schwartz, E. Vittinghoff, D.C. Bauer et al., Association of BMD and FRAX score with risk of fracture in older adults with type 2 diabetes. JAMA \u003cb\u003e305\u003c/b\u003e, 2184\u0026ndash;2192 (2011)\u003c/span\u003e\u003c/li\u003e\u003c/ol\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":true,"highlight":"","institution":"","isAcceptedByJournal":false,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true},"keywords":"Hyperglycemia, insulin, muscle, bone, balance, quadriceps","lastPublishedDoi":"10.21203/rs.3.rs-3091225/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-3091225/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003ch2\u003ePurpose\u003c/h2\u003e \u003cp\u003eType 2 diabetes mellitus (T2DM), osteoporosis (OP) and sarcopenia are major public health problems related with higher fall/fracture risks, morbidity and mortality. Due to the lack of a comprehensive analysis among T2DM, OP and sarcopenia; we aimed to explore the impact of T2DM on OP and sarcopenia in postmenopausal women.\u003c/p\u003e\u003ch2\u003eMethods\u003c/h2\u003e \u003cp\u003eThis cross-sectional study included postmenopausal women who admitted to the departments of physical \u0026amp; rehabilitation medicine, and endocrinology and metabolism. Demographic data, nutrition/cognition status and frailty scores were recorded. Sarcopenia-related parameters including SARC-F, anterior thigh muscle thickness, handgrip strength, chair stand test, gait speed, and one-leg stand test for balance were measured. ISarcoPRM algorithm was used for the diagnosis of sarcopenia.\u003c/p\u003e\u003ch2\u003eResults\u003c/h2\u003e \u003cp\u003eA total of 444 postmenopausal women were consecutively enrolled. T2DM patients (N\u0026thinsp;=\u0026thinsp;158, 35.6%) had higher frequency of sarcopenia, but lower frequency of OP than controls (both p\u0026thinsp;\u0026lt;\u0026thinsp;0.05). As regards regression analyses; T2DM - either under the treatment of oral antidiabetic drugs or insulin - had a negative association with presence of OP (about 2 to 3 times lower, respectively). The duration of T2DM had a positive association with sarcopenia and a negative association with balance (all p\u0026thinsp;\u0026lt;\u0026thinsp;0.05).\u003c/p\u003e\u003ch2\u003eConclusion\u003c/h2\u003e \u003cp\u003eT2DM has paradoxical effects on bone, muscle and balance. Although insulin treatment might have anabolic effects on bone (protecting OP), the disease (duration) itself has negative effects on sarcopenia/balance.\u003c/p\u003e","manuscriptTitle":"The Paradoxical Impact of Diabetes Mellitus on Osteoporosis and Sarcopenia:\nThe ParaDOS Study","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2023-07-06 19:39:54","doi":"10.21203/rs.3.rs-3091225/v1","editorialEvents":[{"type":"communityComments","content":0}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true}}],"origin":"","ownerIdentity":"868b674c-123e-442d-a10d-fc6c59d53c9f","owner":[],"postedDate":"July 6th, 2023","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"posted","subjectAreas":[],"tags":[],"updatedAt":"2023-08-28T06:43:22+00:00","versionOfRecord":[],"versionCreatedAt":"2023-07-06 19:39:54","video":"","vorDoi":"","vorDoiUrl":"","workflowStages":[]},"version":"v1","identity":"rs-3091225","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-3091225","identity":"rs-3091225","version":["v1"]},"buildId":"WrCJVZZCHTDjtuVLN7oU0","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}