- Email: [email protected]
Bone Mineral Density in Premenopausal Arab Women With Type 2 Diabetes Mellitus
Journal of Clinical Densitometry: Assessment of Skeletal Health, vol. 12, no. 1, 54e57, 2009 Ó Copyright 2009 by The International Society for Clinical Densitometry 1094-6950/09/12:54e57/$36.00 DOI: 10.1016/j.jocd.2008.09.003
Original Article
Bone Mineral Density in Premenopausal Arab Women With Type 2 Diabetes Mellitus Renu Gupta,*,1,2 Ahmed M. Mohammed,3,4 Olusegun A. Mojiminiyi,5,6 Eman K. Alenizi,7 and Nabila A. Abdulla8,9 1
Department of Radiology, Faculty of Medicine, Kuwait University, Kuwait; 2Department of Radiology, Mubarak Al-Kabeer Hospital, Kuwait; 3Department of Nuclear Medicine, Faculty of Medicine, Kuwait University, Kuwait; 4Department of Nuclear Medicine, Farwania Hospital, Kuwait; 5Department of Pathology, Faculty of Medicine, Kuwait University, Kuwait; 6Department of Pathology, Mubarak Al-Kabeer Hospital, Kuwait; 7Department of Nuclear Medicine, Mubarak Al-Kabeer Hospital, Kuwait; 8Department of Medicine, Faculty of Medicine, Kuwait University, Kuwait; and 9Department of Medicine, Mubarak Al-Kabeer Hospital, Kuwait
Abstract Introduction: This study compares an ethnically uniform group of premenopausal type 2 diabetic (T2DM) Arab women with a matched control group of nondiabetic subjects, in terms of their bone mineral density (BMD) and anthropometric measurements. Methods: The study included 252 premenopausal Arab women. Their age ranged from 26 to 50 yr with a mean SD of 43.65 8.97 yr. One hundred and twenty-two women were T2DM patients and 130 women were nondiabetic controls. The controls matched the subjects in gender, age, and body mass index (BMI). BMD was measured at total lumbar spine (L1eL4) and total left hip, using dual-energy X-ray absorptiometry (DXA; HOLOGIC, QRS SERIES, Europe, Belgium). Difference in BMD and its relationship to the anthropometric measurements in T2DM and control groups were assessed. Results: Significant difference was found between T2DM patients and nondiabetic patients in their mean hip BMD (0.92 0.16 vs. 0.87 0.14, p ! 0.05) and spine BMD (0.93 0.15 vs. 0.88 0.14, p ! 0.01). No significant difference was found in age, height, weight, and BMI ( p O 0.05). The increase in hip BMD in T2DM patients normalized and the increase in spine BMD persisted after controlling for the confounding effect of age and anthropometric measurements. Conclusion: Premenopausal Arab women with T2DM have higher BMD at the spine than women without T2DM. The underlying mechanism causing this increase does not seem to be related to ethnicity, gender, hormonal status, or anthropometric measurements. Key Words: Bone mineral density; premenopausal women; type 2 diabetes mellitus.
be 14.8% (14.7% in men, 14.8% in women), ranging from 5.7% in the age group 20e39 yr to 18.3% in the age group 40e59 yr (1). The reported effects of T2DM on bone metabolism and bone mineral density (BMD) are controversial. The early, small studies reported either unchanged or decreased (3e5) BMD. Those studies that reported decreased BMD described diabetic osteopenia as one of the chronic complications associated with diabetes mellitus (DM). All recent, large epidemiological studies show, in general, an increase in bone mass at both the lumbar spine (6e9) and the hip
Introduction Type 2 diabetes mellitus (T2DM) is a major clinical and public health problem in Kuwait (1,2), an Arab country. The overall prevalence of T2DM in Kuwait was reported to Received 08/02/08; Revised 09/08/08; Accepted 09/19/08. *Address correspondence to: R. Gupta, MD, Department of Radiology, Faculty of Medicine, Kuwait University, PO Box 24923, Safat 13110, Kuwait. E-mail: [email protected]
54
BMD in Premenopausal Arab Diabetic Women (4e7,10e12). In some of the studies, the increase in BMD was partly accounted for by increased body weight among T2DM patients (13e15). In others, the increase persisted after correction for body weight or body composition (16). BMD shows significant differences among different ethnic groups (17), and is affected by gender and the menopausal status in women. Hence, this study was aimed to compare an ethnically uniform group of premenopausal T2DM Arab women to a matched control group of nondiabetic patients in terms of their BMD and anthropometric measurements.
Methods The study included 252 premenopausal Arab women who had a menstrual period during the last 3 mo. Their age ranged from 26 to 50 yr with a mean SD of 43.65 8.97 yr. One hundred and twenty-two women were T2DM patients (mean SD age: 44.19 8.83 yr) who were referred for assessment of BMD to the Department of Radiology at Mubarak Al-Kabeer Teaching Hospital, Kuwait, from several polyclinics, primary, secondary, and tertiary health centers, and diabetic clinics of outpatient departments. One hundred and thirty women were nondiabetic controls (mean SD age: 42.96 9.29 yr) whose data were retrieved from the department database. The controls matched the subjects in gender, age, and body mass index (BMI). Diabetes was defined as a self-report of diabetes previously diagnosed by a physician, use of hypoglycemic medications, or fasting glucose 126 mg/dL (7.0 mmol/L). Patients who had rheumatic bone disease, rickets or osteomalacia, kidney diseases, and history of corticosteroid therapy for more than 6 mo were excluded from the study. Informed consent was obtained and the study protocol was in conformity with ethical guidelines of the Faculty of Medicine, Kuwait University, Kuwait, and according to Helsinki’s declaration. BMD was measured at total lumbar spine (L1eL4) and total left hip, using dual energy X-ray absorptiometry (DXA; HOLOGIC, QRS SERIES, Europe, Belgium). Data were analyzed using SPSS, version 15 (SPSS Inc., Chicago, IL). When appropriate, frequency distribution and descriptive statistics were obtained and the values were expressed as number of cases, percentage of cases, and mean standard deviation (SD). The difference in BMD and the anthropometric measurements (height, weight, and BMI) between T2DM patients and the control group was assessed using the t-test for parametric data and Mann-Whitney test for nonparametric data. Multivariate linear regression models examined independent effect of T2DM on BMD while adjusting for relevant covariates. The relationship between BMD and anthropometric measurements was assessed using Pearson correlation. p Value ! 0.05 was considered significant.
Results Significant difference was found between T2DM patients and nondiabetic patients in their mean hip BMD Journal of Clinical Densitometry: Assessment of Skeletal Health
55 (0.92 0.16 vs. 0.87 0.14, p ! 0.05) and spine BMD (0.93 0.15 vs. 0.88 0.14, p ! 0.01). No significant difference was found in age, height, weight, and BMI between the 2 groups ( p O 0.05) (Table 1). Hip BMD was found to have a significant negative correlation with age in nondiabetic patients, and a positive correlation with height, weight, and BMI in both diabetic and nondiabetic patients (Table 2). Spine BMD was found to have a negative correlation with age and a positive correlation with weight in both diabetic and nondiabetic patients, a positive correlation with height in diabetic patients and with BMI in nondiabetic patients. The increase in hip BMD in T2DM patients, compared with nondiabetic patients, was normalized after controlling for the confounding effect of age and the anthropometric measurements using a multivariate linear regression model. Although not statistically significant, hip BMD remained higher in T2DM than in nondiabetic patients by 0.046 g/ cm2 (95% confidence interval [CI]: 0.018 to 0.110). Age was the only factor that had a significant effect (15.2%) on hip BMD. The increase in spine BMD remained significantly higher in T2DM patients by 0.091 g/cm2 (95% CI: 0.019e0.163; p ! 0.05). None of the examined factors had a significant confounding effect on spine BMD.
Discussion Kuwait is an Arab country, which has high incidence of DM (1,2). Healthy women in Kuwait in all age groups tend to have lower spine BMD and more spine osteoporosis than their US counterparts (18). Women with DM are less likely to receive screening services for osteoporosis than women without DM (19). Therefore, it is important to study BMD in diabetic women in Kuwait and give any recommendations regarding patient care and management. Unlike the previous reports of diabetic osteopenia in patients with T2DM (3e5), this study shows that T2DM patients have a significantly higher spine and hip BMD than Table 1 A Comparison of Mean Age, Height, Weight, BMI, and Hip and Spine BMD Between T2DM and Nondiabetic Patients T2DM
Nondiabetics
Age (yr) 48.50 8.18 48.20 8.36 Height (cm) 156.26 6.25 155.76 6.89 Weight (kg) 79.71 17.39 76.74 16.56 BMI (kg/m2) 33.47 6.87 32.04 6.95 Left hip BMD (g/cm2) 0.92 0.16* 0.87 0.14 Lumbar spine BMD (g/cm2) 0.93 0.15** 0.88 0.14 *p ! 0.05 for T2DM vs. nondiabetic patients. **p ! 0.01 for T2DM vs. nondiabetic patients. Abbrev: T2DM, type 2 diabetes mellitus; BMI, body mass index; BMD, bone mineral density. Volume 12, 2009
56
Gupta et al. Table 2 Pearson Correlation Coefficients of the Relationship Between Age, Height, Weight, and BMI, and Hip and Spine BMD in T2DM and Nondiabetic Patients Hip BMD T2DM
Age Height Weight BMI
0.086 0.292** 0.411** 0.332**
Nondiabetics 0.169* 0.280** 0.507* 0.387**
Spine BMD T2DM 0.252** 0.365** 0.243** 0.119
Nondiabetics 0.187* 0.157 0.413** 0.351**
*p ! 0.05. **p ! 0.01. Abbrev: T2DM, type 2 diabetes mellitus; BMI, body mass index; BMD, bone mineral density.
nondiabetic patients. Multivariate linear regression analysis, which was used to control for the possible confounding effect of age and the anthropometric measurements, revealed that the increase in hip BMD may have been accounted for by the negative effect of age on BMD. However, the increase in spine BMD was not affected by any of the examined factors, suggesting that T2DM was a significant independent correlate of higher spine BMD. Having increased BMD at the spine that is not affected by age or the anthropometric measurements suggests a T2DMrelated mechanism, which affects BMD at the spine more than at the hip. Different mechanisms have been suggested as possible underlying causes for increased BMD in DM patients. Lower levels of serum parathyroid hormone and lower bone turnover (20), lower recruitment of osteoblasts, and a diminished mineral apposition rate (21,22), and altered leptin or osteoprotegerin (23,24) are some of the reported mechanisms. Whatever the underlying mechanism is, the present data indicate that T2DM is a strong protective factor that can change BMD values from lowerdin case of healthy Arab womendto higher, and that the mechanism is not related to differences in ethnicity, gender, or hormonal status. The included subjects were women all in their premenopausal stage. Increased spine BMD and unchanged hip BMD among T2DM patients suggest that the reported increased rate and risk of fracture among the diabetic patients (25) may not be related to reduced BMD but to other factors, which may include increased susceptibility to fall due to visual impairment and peripheral neuropathy, as well as foot problems (26,27) and impaired cognitive capabilities (28).
Conclusion Premenopausal Arab women with T2DM have higher BMD at the spine than women without T2DM. The underlying mechanism causing this increase does not seem to be related to ethnicity, gender, hormonal status, or anthropometric measurements. Journal of Clinical Densitometry: Assessment of Skeletal Health
References 1. Abdella N, Al Arouj M, Al Nakhi A, et al. 1998 Non-insulindependent diabetes in Kuwait: prevalence rates and associated risk factors. Diabetes Res Clin Pract 42(3):187e196. 2. Shaltout AA, Moussa MA, Qabazard M, et al. 2002 Kuwait Diabetes Study further evidence for the rising incidence of childhood type 1 diabetes in Kuwait. Diabet Med 19(6):522e525. 3. Isaia G, Bodrato L, Carlevatto V, et al. 1987 Osteoporosis in type II diabetes. Acta Diabetol Lat 24:305e310. 4. McNair P, Christensen MS, Madsbad S, et al. 1981 Hyperparathyroidism in diabetes mellitus. Acta Endocrinol 96:81e86. 5. Gregorio F, Cristallini S, Santeusanio F, et al. 1994 Osteopenia associated with non-insulin-dependent diabetes mellitus: what are the causes? Diabetes Res Clin Pract 23:43e54. 6. Liefde De II, Van der Klift M, De Laet CEDH, et al. 2005 Bone mineral density and fracture risk in type-2 diabetes mellitus: the Rotterdam Study. Osteoporos Int 16:1713e1720. 7. Lunt M, Masaryk P, Scheidt-Nave C, et al. 2001 The effects of lifestyle, dietary dairy intake and diabetes on bone density and vertebral deformity prevalence: the EVOS Study. Osteoporos Int 12:688e698. 8. Dennison EM, Syddall HE, Aihie Sayer A, et al. 2004 Type 2 diabetes mellitus is associated with increased axial bone density in men and women from the Hertfordshire Cohort Study: evidence for an indirect effect of insulin resistance? Diabetologia 47:1963e1968. 9. Barrett-Connor E, Holbrook TL. 1992 Sex differences in osteoporosis in older adults with non-insulin dependent diabetes mellitus. JAMA 268:3333e3337. 10. Gerdhem P, Isaksson A, Akesson K, Obrant KJ. 2005 Increased bone density and decreased bone turnover, but no evident alteration of fracture susceptibility in elderly women with diabetes mellitus. Osteoporos Int 16:1506e1512. 11. Schwartz AV, Sellmeyer DE, Ensrud KE, , et al.Study of Osteoporotic Features Research Group. 2005 Older women with diabetes have an increased risk of fracture: a prospective study. J Clin Endocrinol Metab 86:32e38. 12. Schwartz AV, Sellmeyer DE, Strotmeyer ES, , et al.Health ABC Study. 2005 Diabetes and bone loss at the hip in older black and white adults. J Bone Miner Res 20:596e603. 13. Christensen JO, Svendsen OL. 1999 Bone mineral in pre- and postmenopausal women with insulin-dependent and non-insulin dependent diabetes mellitus. Osteoporos Int 10:307e311. 14. van Daele PL, Stolk RP, Burger H, et al. 1995 Bone density in non-insulin-dependent diabetes mellitus: the Rotterdam Study. Ann Intern Med 122:409e414. 15. Weinstock RS, Goland RS, Shane E, et al. 1989 Bone mineral density in women with type II diabetes mellitus. J Bone Miner Res 4:97e101. 16. Strotmeyer ES, Cauley JA, Schwartz AV, , et al.Health ABC Study. 2004 Diabetes is associated independently of body composition with BMD and bone volume in older white and black men and women: the health, aging, and body composition study. J Bone Miner Res 19:1084e1091. 17. Finkelstein J, Lee M, Sowers M, et al. 2002 Ethnic variation in bone density in premenopausal and early perimenopausal women: effects of anthropometric and lifestyle factors. J Clin Endocrinol Metab 87(7):3057e3067. 18. World Health Organization (WHO). 1994 Assessment of fracture risk and its application to screening for postmenopausal osteoporosis. Geneva. 19. Mcbean M, Yu X. 2007 The underuse of screening services among elderly women with diabetes. Diabetes Care 30: 1466e1472.
Volume 12, 2009
BMD in Premenopausal Arab Diabetic Women 20. Dobnig H, Piswanger-So¨lkner JC, Roth M, et al. 2006 Type 2 diabetes mellitus in nursing home patients: effects on bone turnover, bone mass, and fracture risk. J Clin Endocrinol Metab 91(9):3355e3363. 21. Bouillon R. 1991 Diabetic bone disease. Calcif Tissue Int 49: 155e160. 22. Collin P, Kaukinen K, Valimaki M, Salmi J. 2002 Endocrinological disorders and celiac disease. Endocr Rev 23:464e483. 23. Reid IR, Cornish J, Baldock PA. 2006 Nutrition-related peptides and bone homeostasis. J Bone Miner Res 21:495e500. 24. Knudsen ST, Foss CH, Poulsen PL, et al. 2003 Increased plasma concentrations of osteoprotegerin in type 2 diabetic patients with microvascular complications. Eur J Endocrinol 149:39e42.
Journal of Clinical Densitometry: Assessment of Skeletal Health
57 25. Lorraine L, Lipscombe, SophieJamal A, et al. 2007 The risk of hip fractures in older individuals with diabetes. Diabetes Care 30:835e841. 26. Wallace C, Reiber GE, LeMaster J, et al. 2002 Incidence of falls, risk factors for falls, and fall-related fractures in individuals with diabetes and a prior foot ulcer. Diabetes Care 25:1983e1986. 27. Keegan TH, Kelsey JL, Sidney S, Quesenberry CP Jr. 2002 Foot problems as risk factors of fractures. Am J Epidemiol 155: 926e931. 28. Gregg EW, Yaffe K, Cauley JA, et al. 2000 Is diabetes associated with cognitive impairment and cognitive decline among older women? Study of Osteoporotic Fractures Research Group. Arch Intern Med 160:174e180.
Volume 12, 2009
Original Article
Bone Mineral Density in Premenopausal Arab Women With Type 2 Diabetes Mellitus Renu Gupta,*,1,2 Ahmed M. Mohammed,3,4 Olusegun A. Mojiminiyi,5,6 Eman K. Alenizi,7 and Nabila A. Abdulla8,9 1
Department of Radiology, Faculty of Medicine, Kuwait University, Kuwait; 2Department of Radiology, Mubarak Al-Kabeer Hospital, Kuwait; 3Department of Nuclear Medicine, Faculty of Medicine, Kuwait University, Kuwait; 4Department of Nuclear Medicine, Farwania Hospital, Kuwait; 5Department of Pathology, Faculty of Medicine, Kuwait University, Kuwait; 6Department of Pathology, Mubarak Al-Kabeer Hospital, Kuwait; 7Department of Nuclear Medicine, Mubarak Al-Kabeer Hospital, Kuwait; 8Department of Medicine, Faculty of Medicine, Kuwait University, Kuwait; and 9Department of Medicine, Mubarak Al-Kabeer Hospital, Kuwait
Abstract Introduction: This study compares an ethnically uniform group of premenopausal type 2 diabetic (T2DM) Arab women with a matched control group of nondiabetic subjects, in terms of their bone mineral density (BMD) and anthropometric measurements. Methods: The study included 252 premenopausal Arab women. Their age ranged from 26 to 50 yr with a mean SD of 43.65 8.97 yr. One hundred and twenty-two women were T2DM patients and 130 women were nondiabetic controls. The controls matched the subjects in gender, age, and body mass index (BMI). BMD was measured at total lumbar spine (L1eL4) and total left hip, using dual-energy X-ray absorptiometry (DXA; HOLOGIC, QRS SERIES, Europe, Belgium). Difference in BMD and its relationship to the anthropometric measurements in T2DM and control groups were assessed. Results: Significant difference was found between T2DM patients and nondiabetic patients in their mean hip BMD (0.92 0.16 vs. 0.87 0.14, p ! 0.05) and spine BMD (0.93 0.15 vs. 0.88 0.14, p ! 0.01). No significant difference was found in age, height, weight, and BMI ( p O 0.05). The increase in hip BMD in T2DM patients normalized and the increase in spine BMD persisted after controlling for the confounding effect of age and anthropometric measurements. Conclusion: Premenopausal Arab women with T2DM have higher BMD at the spine than women without T2DM. The underlying mechanism causing this increase does not seem to be related to ethnicity, gender, hormonal status, or anthropometric measurements. Key Words: Bone mineral density; premenopausal women; type 2 diabetes mellitus.
be 14.8% (14.7% in men, 14.8% in women), ranging from 5.7% in the age group 20e39 yr to 18.3% in the age group 40e59 yr (1). The reported effects of T2DM on bone metabolism and bone mineral density (BMD) are controversial. The early, small studies reported either unchanged or decreased (3e5) BMD. Those studies that reported decreased BMD described diabetic osteopenia as one of the chronic complications associated with diabetes mellitus (DM). All recent, large epidemiological studies show, in general, an increase in bone mass at both the lumbar spine (6e9) and the hip
Introduction Type 2 diabetes mellitus (T2DM) is a major clinical and public health problem in Kuwait (1,2), an Arab country. The overall prevalence of T2DM in Kuwait was reported to Received 08/02/08; Revised 09/08/08; Accepted 09/19/08. *Address correspondence to: R. Gupta, MD, Department of Radiology, Faculty of Medicine, Kuwait University, PO Box 24923, Safat 13110, Kuwait. E-mail: [email protected]
54
BMD in Premenopausal Arab Diabetic Women (4e7,10e12). In some of the studies, the increase in BMD was partly accounted for by increased body weight among T2DM patients (13e15). In others, the increase persisted after correction for body weight or body composition (16). BMD shows significant differences among different ethnic groups (17), and is affected by gender and the menopausal status in women. Hence, this study was aimed to compare an ethnically uniform group of premenopausal T2DM Arab women to a matched control group of nondiabetic patients in terms of their BMD and anthropometric measurements.
Methods The study included 252 premenopausal Arab women who had a menstrual period during the last 3 mo. Their age ranged from 26 to 50 yr with a mean SD of 43.65 8.97 yr. One hundred and twenty-two women were T2DM patients (mean SD age: 44.19 8.83 yr) who were referred for assessment of BMD to the Department of Radiology at Mubarak Al-Kabeer Teaching Hospital, Kuwait, from several polyclinics, primary, secondary, and tertiary health centers, and diabetic clinics of outpatient departments. One hundred and thirty women were nondiabetic controls (mean SD age: 42.96 9.29 yr) whose data were retrieved from the department database. The controls matched the subjects in gender, age, and body mass index (BMI). Diabetes was defined as a self-report of diabetes previously diagnosed by a physician, use of hypoglycemic medications, or fasting glucose 126 mg/dL (7.0 mmol/L). Patients who had rheumatic bone disease, rickets or osteomalacia, kidney diseases, and history of corticosteroid therapy for more than 6 mo were excluded from the study. Informed consent was obtained and the study protocol was in conformity with ethical guidelines of the Faculty of Medicine, Kuwait University, Kuwait, and according to Helsinki’s declaration. BMD was measured at total lumbar spine (L1eL4) and total left hip, using dual energy X-ray absorptiometry (DXA; HOLOGIC, QRS SERIES, Europe, Belgium). Data were analyzed using SPSS, version 15 (SPSS Inc., Chicago, IL). When appropriate, frequency distribution and descriptive statistics were obtained and the values were expressed as number of cases, percentage of cases, and mean standard deviation (SD). The difference in BMD and the anthropometric measurements (height, weight, and BMI) between T2DM patients and the control group was assessed using the t-test for parametric data and Mann-Whitney test for nonparametric data. Multivariate linear regression models examined independent effect of T2DM on BMD while adjusting for relevant covariates. The relationship between BMD and anthropometric measurements was assessed using Pearson correlation. p Value ! 0.05 was considered significant.
Results Significant difference was found between T2DM patients and nondiabetic patients in their mean hip BMD Journal of Clinical Densitometry: Assessment of Skeletal Health
55 (0.92 0.16 vs. 0.87 0.14, p ! 0.05) and spine BMD (0.93 0.15 vs. 0.88 0.14, p ! 0.01). No significant difference was found in age, height, weight, and BMI between the 2 groups ( p O 0.05) (Table 1). Hip BMD was found to have a significant negative correlation with age in nondiabetic patients, and a positive correlation with height, weight, and BMI in both diabetic and nondiabetic patients (Table 2). Spine BMD was found to have a negative correlation with age and a positive correlation with weight in both diabetic and nondiabetic patients, a positive correlation with height in diabetic patients and with BMI in nondiabetic patients. The increase in hip BMD in T2DM patients, compared with nondiabetic patients, was normalized after controlling for the confounding effect of age and the anthropometric measurements using a multivariate linear regression model. Although not statistically significant, hip BMD remained higher in T2DM than in nondiabetic patients by 0.046 g/ cm2 (95% confidence interval [CI]: 0.018 to 0.110). Age was the only factor that had a significant effect (15.2%) on hip BMD. The increase in spine BMD remained significantly higher in T2DM patients by 0.091 g/cm2 (95% CI: 0.019e0.163; p ! 0.05). None of the examined factors had a significant confounding effect on spine BMD.
Discussion Kuwait is an Arab country, which has high incidence of DM (1,2). Healthy women in Kuwait in all age groups tend to have lower spine BMD and more spine osteoporosis than their US counterparts (18). Women with DM are less likely to receive screening services for osteoporosis than women without DM (19). Therefore, it is important to study BMD in diabetic women in Kuwait and give any recommendations regarding patient care and management. Unlike the previous reports of diabetic osteopenia in patients with T2DM (3e5), this study shows that T2DM patients have a significantly higher spine and hip BMD than Table 1 A Comparison of Mean Age, Height, Weight, BMI, and Hip and Spine BMD Between T2DM and Nondiabetic Patients T2DM
Nondiabetics
Age (yr) 48.50 8.18 48.20 8.36 Height (cm) 156.26 6.25 155.76 6.89 Weight (kg) 79.71 17.39 76.74 16.56 BMI (kg/m2) 33.47 6.87 32.04 6.95 Left hip BMD (g/cm2) 0.92 0.16* 0.87 0.14 Lumbar spine BMD (g/cm2) 0.93 0.15** 0.88 0.14 *p ! 0.05 for T2DM vs. nondiabetic patients. **p ! 0.01 for T2DM vs. nondiabetic patients. Abbrev: T2DM, type 2 diabetes mellitus; BMI, body mass index; BMD, bone mineral density. Volume 12, 2009
56
Gupta et al. Table 2 Pearson Correlation Coefficients of the Relationship Between Age, Height, Weight, and BMI, and Hip and Spine BMD in T2DM and Nondiabetic Patients Hip BMD T2DM
Age Height Weight BMI
0.086 0.292** 0.411** 0.332**
Nondiabetics 0.169* 0.280** 0.507* 0.387**
Spine BMD T2DM 0.252** 0.365** 0.243** 0.119
Nondiabetics 0.187* 0.157 0.413** 0.351**
*p ! 0.05. **p ! 0.01. Abbrev: T2DM, type 2 diabetes mellitus; BMI, body mass index; BMD, bone mineral density.
nondiabetic patients. Multivariate linear regression analysis, which was used to control for the possible confounding effect of age and the anthropometric measurements, revealed that the increase in hip BMD may have been accounted for by the negative effect of age on BMD. However, the increase in spine BMD was not affected by any of the examined factors, suggesting that T2DM was a significant independent correlate of higher spine BMD. Having increased BMD at the spine that is not affected by age or the anthropometric measurements suggests a T2DMrelated mechanism, which affects BMD at the spine more than at the hip. Different mechanisms have been suggested as possible underlying causes for increased BMD in DM patients. Lower levels of serum parathyroid hormone and lower bone turnover (20), lower recruitment of osteoblasts, and a diminished mineral apposition rate (21,22), and altered leptin or osteoprotegerin (23,24) are some of the reported mechanisms. Whatever the underlying mechanism is, the present data indicate that T2DM is a strong protective factor that can change BMD values from lowerdin case of healthy Arab womendto higher, and that the mechanism is not related to differences in ethnicity, gender, or hormonal status. The included subjects were women all in their premenopausal stage. Increased spine BMD and unchanged hip BMD among T2DM patients suggest that the reported increased rate and risk of fracture among the diabetic patients (25) may not be related to reduced BMD but to other factors, which may include increased susceptibility to fall due to visual impairment and peripheral neuropathy, as well as foot problems (26,27) and impaired cognitive capabilities (28).
Conclusion Premenopausal Arab women with T2DM have higher BMD at the spine than women without T2DM. The underlying mechanism causing this increase does not seem to be related to ethnicity, gender, hormonal status, or anthropometric measurements. Journal of Clinical Densitometry: Assessment of Skeletal Health
References 1. Abdella N, Al Arouj M, Al Nakhi A, et al. 1998 Non-insulindependent diabetes in Kuwait: prevalence rates and associated risk factors. Diabetes Res Clin Pract 42(3):187e196. 2. Shaltout AA, Moussa MA, Qabazard M, et al. 2002 Kuwait Diabetes Study further evidence for the rising incidence of childhood type 1 diabetes in Kuwait. Diabet Med 19(6):522e525. 3. Isaia G, Bodrato L, Carlevatto V, et al. 1987 Osteoporosis in type II diabetes. Acta Diabetol Lat 24:305e310. 4. McNair P, Christensen MS, Madsbad S, et al. 1981 Hyperparathyroidism in diabetes mellitus. Acta Endocrinol 96:81e86. 5. Gregorio F, Cristallini S, Santeusanio F, et al. 1994 Osteopenia associated with non-insulin-dependent diabetes mellitus: what are the causes? Diabetes Res Clin Pract 23:43e54. 6. Liefde De II, Van der Klift M, De Laet CEDH, et al. 2005 Bone mineral density and fracture risk in type-2 diabetes mellitus: the Rotterdam Study. Osteoporos Int 16:1713e1720. 7. Lunt M, Masaryk P, Scheidt-Nave C, et al. 2001 The effects of lifestyle, dietary dairy intake and diabetes on bone density and vertebral deformity prevalence: the EVOS Study. Osteoporos Int 12:688e698. 8. Dennison EM, Syddall HE, Aihie Sayer A, et al. 2004 Type 2 diabetes mellitus is associated with increased axial bone density in men and women from the Hertfordshire Cohort Study: evidence for an indirect effect of insulin resistance? Diabetologia 47:1963e1968. 9. Barrett-Connor E, Holbrook TL. 1992 Sex differences in osteoporosis in older adults with non-insulin dependent diabetes mellitus. JAMA 268:3333e3337. 10. Gerdhem P, Isaksson A, Akesson K, Obrant KJ. 2005 Increased bone density and decreased bone turnover, but no evident alteration of fracture susceptibility in elderly women with diabetes mellitus. Osteoporos Int 16:1506e1512. 11. Schwartz AV, Sellmeyer DE, Ensrud KE, , et al.Study of Osteoporotic Features Research Group. 2005 Older women with diabetes have an increased risk of fracture: a prospective study. J Clin Endocrinol Metab 86:32e38. 12. Schwartz AV, Sellmeyer DE, Strotmeyer ES, , et al.Health ABC Study. 2005 Diabetes and bone loss at the hip in older black and white adults. J Bone Miner Res 20:596e603. 13. Christensen JO, Svendsen OL. 1999 Bone mineral in pre- and postmenopausal women with insulin-dependent and non-insulin dependent diabetes mellitus. Osteoporos Int 10:307e311. 14. van Daele PL, Stolk RP, Burger H, et al. 1995 Bone density in non-insulin-dependent diabetes mellitus: the Rotterdam Study. Ann Intern Med 122:409e414. 15. Weinstock RS, Goland RS, Shane E, et al. 1989 Bone mineral density in women with type II diabetes mellitus. J Bone Miner Res 4:97e101. 16. Strotmeyer ES, Cauley JA, Schwartz AV, , et al.Health ABC Study. 2004 Diabetes is associated independently of body composition with BMD and bone volume in older white and black men and women: the health, aging, and body composition study. J Bone Miner Res 19:1084e1091. 17. Finkelstein J, Lee M, Sowers M, et al. 2002 Ethnic variation in bone density in premenopausal and early perimenopausal women: effects of anthropometric and lifestyle factors. J Clin Endocrinol Metab 87(7):3057e3067. 18. World Health Organization (WHO). 1994 Assessment of fracture risk and its application to screening for postmenopausal osteoporosis. Geneva. 19. Mcbean M, Yu X. 2007 The underuse of screening services among elderly women with diabetes. Diabetes Care 30: 1466e1472.
Volume 12, 2009
BMD in Premenopausal Arab Diabetic Women 20. Dobnig H, Piswanger-So¨lkner JC, Roth M, et al. 2006 Type 2 diabetes mellitus in nursing home patients: effects on bone turnover, bone mass, and fracture risk. J Clin Endocrinol Metab 91(9):3355e3363. 21. Bouillon R. 1991 Diabetic bone disease. Calcif Tissue Int 49: 155e160. 22. Collin P, Kaukinen K, Valimaki M, Salmi J. 2002 Endocrinological disorders and celiac disease. Endocr Rev 23:464e483. 23. Reid IR, Cornish J, Baldock PA. 2006 Nutrition-related peptides and bone homeostasis. J Bone Miner Res 21:495e500. 24. Knudsen ST, Foss CH, Poulsen PL, et al. 2003 Increased plasma concentrations of osteoprotegerin in type 2 diabetic patients with microvascular complications. Eur J Endocrinol 149:39e42.
Journal of Clinical Densitometry: Assessment of Skeletal Health
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Volume 12, 2009