Osteoporos Int DOI 10.1007/s00198-016-3527-5
ORIGINAL ARTICLE
Association of bone mineral density and diabetic retinopathy in diabetic subjects: the 2008–2011 Korea National Health and Nutrition Examination Survey Y. Lim 1 & S. Chun 2 & J. H. Lee 3 & K. H. Baek 1 & W. K. Lee 3 & H.-W. Yim 2 & M.-I. Kang 1
Received: 30 September 2015 / Accepted: 4 February 2016 # International Osteoporosis Foundation and National Osteoporosis Foundation 2016
Abstract Summary Because diabetic retinopathy increases fracture risk, we studied the association between bone mineral density (BMD) and diabetic retinopathy in a nationally representative sample. A significant association between the presence of diabetic retinopathy and low BMD was observed. Therefore, diabetic retinopathy might be considered as a marker of low BMD. Introduction Several diabetic complications, including nephropathy, retinopathy, and peripheral neuropathy, are associated with a higher fracture risk in diabetic subjects. However, in contrast to diabetic nephropathy and peripheral neuropathy, which are associated with low bone mineral density (BMD), little is known about the association between BMD and diabetic retinopathy. The aim of the present study was to determine whether the prevalence of diabetic retinopathy is associated with BMD. Methods This cross-sectional study included a nationally representative sample consisting of 4357 men aged 50 years and
older and 4392 postmenopausal women who participated in the Korea National Health and Nutritional Examination Survey (KNHANES) from 2008 to 2011 and underwent BMD measurement by dual-energy X-ray absorptiometry (DXA) and diabetic retinopathy assessments using seven standard gradable photographs. Results The diabetic women with retinopathy had lower mean BMD at all measured sites than those without retinopathy, although the BMD difference between the two groups was small (3–5 %). In addition, the diabetic women with retinopathy were 2.27 times more likely to have osteoporosis following adjustments for all clinically relevant covariates. However, the prevalence of diabetes mellitus (DM) or diabetic retinopathy was not associated with the prevalence of osteoporosis in men. Conclusions This study has shown that the presence of diabetic retinopathy is significantly associated with a reduced BMD and increased prevalence of osteoporosis in diabetic women.
Yejee Lim is the first author.
Keywords Angiogenesis factor . Bone mineral density . Diabetes mellitus . DXA scan . Retinopathy
* M.-I. Kang [email protected]
1
Division of Endocrinology and Metabolism, Department of Internal Medicine, Seoul St. Mary’s Hospital, College of Medicine, The Catholic University of Korea, 222 Banpo-daero, Seocho-gu 137-701, Seoul, Korea
2
Department of Preventive Medicine, College of Medicine, The Catholic University of Korea, 222 Banpo-daero, Seocho-gu, Seoul 137-701, Republic of Korea
3
Department of Ophthalmology, College of Medicine, The Catholic University of Korea, 222 Banpo-daero, Seocho-gu, Seoul 137-701, Republic of Korea
Introduction Diabetic retinopathy is the most common microvascular complication of diabetes mellitus (DM), affecting approximately 30 % of people with DM [1], a third of whom have vision-threatening retinopathy, defined as severe retinopathy or macular edema [2]. It has been estimated that approximately 18.6 % of diabetic patients have retinopathy in South Korea [3]. This condition is the most frequent cause of preventable blindness in working-age adults (20–74 years) [4]. Hyperglycemia, hypertension, hypercholesterolemia, and a
Osteoporos Int
longer duration of DM are well-known risk factors for diabetic retinopathy [5]. A significantly increased risk of fractures associated with visual impairment due to diabetic retinopathy has been reported in many studies [6, 7]. There is a substantial body of literature on the association between type 2 DM and fracture risk. An increased fracture risk in type 2 DM patients has been reported [8, 9] although bone mineral density (BMD) is typically normal or higher than in non-diabetic controls [10]. A longer disease duration, the presence of diabetic complications, and inadequate glycemic control all have been reported to increase the fracture risk in diabetic patients [11]. Diabetic neuropathy, retinopathy, peripheral neuropathy, vestibular dysfunction, cognitive impairment, and muscle weakness of the lower limbs are common complications of DM. All of these complications have been shown to increase the risk of fracture in diabetic patients by promoting falls [12]. Several studies have reported that the presence of chronic complications is associated with low BMD. Patients with neuropathy [13, 14], and even those with early-stage diabetic kidney disease with microalbuminuria, exhibited decreased BMD [15]. However, little is known regarding the association between BMD and diabetic retinopathy in diabetic patients. To the best of our knowledge, this is the first study that shows the association between diabetic retinopathy and BMD in type 2 DM subjects. We hypothesized that diabetic subjects with retinopathy may have lower BMD because of the long disease duration and poor disease control statuses which are considered to be the risk factors of fracture. The aim of this study was to evaluate the relationship between the prevalence of diabetic retinopathy and osteoporosis in diabetic subjects who participated in the Korea National Health and Nutritional Examination Surveys (KNHANES).
Materials and methods Study design and participants This study was based on data acquired from the KNHANES, which has been periodically conducted by the Division of Health and Nutritional Survey in the Korean Centers for Disease Control and Prevention (KCDCP) since 1998. It is an ongoing, population-based, cross-sectional, and nationally representative survey, and it provides the largest publicly available database in South Korea. Participants were chosen from candidates using proportional-allocation, systematic sampling with multistage stratification (by age, gender, and region). Twenty-three households from 200 randomly selected sampling units were chosen in 2008 and 2009, whereas 20 households from 192 sampling units were chosen in 2010 and 2011. The KNHANES consists of three different components: a health interview, a nutrition survey, and a health
examination. Data were collected by household interviews and direct standardized physical examinations conducted at mobile examination centers. During the period from July 2008 to May 2011, the KNHANES interview and examination were completed for 26,775 individuals. Of the 10,366 participants who were aged ≥50 years, 617 were excluded according to the following exclusion criteria: current or previous usage of anti-osteoporotic medication or estrogen therapy, severe chronic kidney disease (CKD), and pre-menopausal female or suspicion of type 1 DM (Fig. 1). The institutional review board of the Catholic University of Korea approved this study (no. KC15RISI0608). Written informed consent was obtained from all participants. Health examination survey and laboratory tests Various factors were examined. After the height and weight were measured using standardized techniques and equipment, body mass index (BMI) was calculated by dividing body weight by height squared (kg/m2). Blood pressure (BP) was measured by standard methods using a sphygmomanometer with the patient in a sitting position. Information regarding demographic and social factors was obtained using a standardized questionnaire during the health interview. Heavy alcohol drinking was categorized as drinking four or more times per week and 3 units of alcohol per time. Current smoker was defined as currently smoking with a smoking history of ≥100 cigarettes in a lifetime. In addition, a urinary cotinine level of above 164 ng/mL was used to determine inaccurate reporting of current tobacco use [16]. After fasting for at least 8 h, blood samples were collected in the morning and analyzed at a central, certified laboratory. Severe CKD was defined as glomerular filtration rate (GFR) of less than 30 mL/ min/1.73 m2, as calculated using the Cockcroft-Gault formula. The following definitions were obtained from the Division of Health and Nutritional Survey under the KCDCP. Hypertension was defined by either a self-reported history of hypertension diagnosis and current usage of antihypertensive drugs or a systolic BP of ≥140 mm Hg or a diastolic BP of ≥90 mm Hg. Hypercholesterolemia was defined as a total cholesterol concentration of ≥240 mg/dL or prescription of anti-cholesterol medication. The results of urine dipstick tests were recorded as (−), trace, (1+), (2+), or (3+), and proteinuria was defined as ≥(1+) proteinuria by dipstick. Assessment of BMD and definition of osteoporosis Osteoporosis examinations began in July 2008 and ended in May 2011. The subjects were ≥19 years of age from July 2008 to June 2009 and ≥10 years of age from July 2009 to May 2011. The BMD of the lumbar spine, left total hip, and left femoral neck was measured by dual-energy X-ray absorptiometry (DXA; Discovery-W; Hologic Inc., Waltham, MA,
Osteoporos Int Fig. 1 Flow diagram for identification of the study population. A total of 9749 subjects were finally included. KNHANES, Korea National Health and Nutrition Examination Survey; GFR, glomerular filtration rate
USA). For the lumbar spine BMD, the mean value of L1 to L4 was chosen for analysis following the recommendation of the International Society for Clinical Densitometry (ISCD) in 2007 [17]. When the BMD of the left femur could not be measured (e.g., postoperative state, fracture, deformity, or malformation), the BMD of the right femur was used. The technicians who performed the BMD measurements were tested for precision based on duplicate measurements of 30 participants or triplicate measurement of 15 participants. Precision error was calculated as a percentage coefficient of variation (CV%). The allowed precision errors for the total hip, femur neck, and total lumbar spine were 1.8, 2.5, and 1.9 %, respectively. According to the criteria established by the World Health Organization (WHO), osteoporosis was diagnosed in subjects with a T-score of less than or equal to −2.5, and osteopenia was diagnosed in subjects with a T-score of between −2.5 and −1.0, and subjects with a T-score of −1.0 or higher were considered normal [18]. Assessments and definitions of DM and diabetic retinopathy DM was defined as a previous diagnosis of DM made by a physician, the use of insulin or oral hypoglycemic agents, and/ or a fasting blood glucose level of 126 mg/dL or higher. The participants were considered to have type 1 DM if they were younger than 30 of age when diagnosed with DM and were receiving insulin therapy. Non-mydriatic digital fundus photographs (TRC-NW6S; Topcon, Tokyo, Japan) were taken of all the participants ≥19 years old. Next, seven gradable
standard photographs were obtained from both eyes after pharmacologic pupil dilatation for diabetic retinopathy assessment. It was performed for participants with a history of DM, a random blood glucose level of >200 mg/dL, or a suspicious diabetic retinopathy finding in digital fundus photographs. Each image was graded for retinopathy according to the Early Treatment for Diabetic Retinopathy Study (ETDRS) severity level and was dichotomized as having retinopathy (level 15 and above) or not having retinopathy (≤14) [19]. Because the level of retinopathy was determined based on the worse eye, diabetic retinopathy was defined as the presence of diabetic retinopathy, in either eye. The quality of the survey was verified by the Epidemiologic Survey Committee of the Korean Ophthalmologic Society. Statistical analysis Participants in the KNHANES were selected for participation based on a stratified, multi-stage probability sampling design. The weights for each respondent, representing the inverse of their sampling probabilities, were provided by the Korean Center for Disease Control and have been used in many analyses to obtain estimates that are representative of the non-institutionalized South Korean civilian population. All continuous data were presented as the mean ± standard error (SE). All categorical data were presented as numbers and percentages. To compare the principal characteristics of the study subjects between the two groups, Student’s t test for continuous variables and the χ2 test for categorical variables were used. The multiple linear regression analyses were used to
Osteoporos Int
determine whether the BMD at each measured site differed according to the prevalence of DM or diabetic retinopathy. Univariable and multivariable logistic regression models were used to estimate the odds ratio (OR) of osteoporosis in each group. All analyses were two-tailed and were carried out using SAS version 9.3 (SAS Institute, Cary, NC, USA). Results with a p value of less than 0.05 were considered statistically significant.
Results Baseline characteristics of the subjects according to the presence of diabetes mellitus Among the total participants who were 50 years of age and older from the KNHANES 2008–2011, 655 (15.0 %) men and 703 (13.0 %) women were diagnosed as having diabetes. The baseline characteristics of diabetic subjects and non-diabetic controls are shown in Table 1. The diabetic women were older than non-diabetic women (mean age 66.35 vs. 63.18 years), although the mean age of diabetic men did not differ from that of non-diabetic men (62.03 vs. 61.41 years). Both the male and female diabetic subjects were more likely to be Table 1
overweight or obese, and to have higher fasting glucose, and HbA1c levels, proteinuria, hypertension, and hypercholesterolemia (p < 0.05). The subjects with or without DM did not differ in terms of BMD according to the WHO criteria. Association between prevalence of diabetes and osteoporosis The BMDs at various measured sites were compared in the diabetic subjects and non-diabetic controls. The diabetic men had higher lumbar spine and total hip BMDs than non-diabetic men in crude analysis. However, this association was diminished after further adjustments for all clinically relevant covariates (age, BMI, current smoking status, heavy alcohol intake, proteinuria, hypertension, and hypercholesterolemia). The BMDs at all measured sites of women did not differ in terms of diabetic status prior to adjustments for confounders. However, the diabetic women had higher BMDs at the lumbar spine and total hip than non-diabetic women following adjustments for age and BMI with or without the other confounders (Table 2). Further logistic regression analyses of osteoporosis according to the prevalence of DM are shown in Fig. 2. The prevalence of osteoporosis did not differ according to the diabetic status in men regardless of the adjustment model
Weighted baseline characteristics of study participants from the KNHANES (2008–2011) Men (n = 4,357)
Women (n = 4,392)
DM (−) n = 3702 (N = 5,841,433)
DM (+) n = 655 (N = 1,006,815)
p value
DM (−) n = 4689 (N = 6,429,843)
DM (+) n = 703 (N = 911,792)
p value
Age (years)
61.41 ± 0.23
62.03 ± 0.41
0.145
63.18 ± 0.21
66.35 ± 0.46
ORIGINAL ARTICLE
Association of bone mineral density and diabetic retinopathy in diabetic subjects: the 2008–2011 Korea National Health and Nutrition Examination Survey Y. Lim 1 & S. Chun 2 & J. H. Lee 3 & K. H. Baek 1 & W. K. Lee 3 & H.-W. Yim 2 & M.-I. Kang 1
Received: 30 September 2015 / Accepted: 4 February 2016 # International Osteoporosis Foundation and National Osteoporosis Foundation 2016
Abstract Summary Because diabetic retinopathy increases fracture risk, we studied the association between bone mineral density (BMD) and diabetic retinopathy in a nationally representative sample. A significant association between the presence of diabetic retinopathy and low BMD was observed. Therefore, diabetic retinopathy might be considered as a marker of low BMD. Introduction Several diabetic complications, including nephropathy, retinopathy, and peripheral neuropathy, are associated with a higher fracture risk in diabetic subjects. However, in contrast to diabetic nephropathy and peripheral neuropathy, which are associated with low bone mineral density (BMD), little is known about the association between BMD and diabetic retinopathy. The aim of the present study was to determine whether the prevalence of diabetic retinopathy is associated with BMD. Methods This cross-sectional study included a nationally representative sample consisting of 4357 men aged 50 years and
older and 4392 postmenopausal women who participated in the Korea National Health and Nutritional Examination Survey (KNHANES) from 2008 to 2011 and underwent BMD measurement by dual-energy X-ray absorptiometry (DXA) and diabetic retinopathy assessments using seven standard gradable photographs. Results The diabetic women with retinopathy had lower mean BMD at all measured sites than those without retinopathy, although the BMD difference between the two groups was small (3–5 %). In addition, the diabetic women with retinopathy were 2.27 times more likely to have osteoporosis following adjustments for all clinically relevant covariates. However, the prevalence of diabetes mellitus (DM) or diabetic retinopathy was not associated with the prevalence of osteoporosis in men. Conclusions This study has shown that the presence of diabetic retinopathy is significantly associated with a reduced BMD and increased prevalence of osteoporosis in diabetic women.
Yejee Lim is the first author.
Keywords Angiogenesis factor . Bone mineral density . Diabetes mellitus . DXA scan . Retinopathy
* M.-I. Kang [email protected]
1
Division of Endocrinology and Metabolism, Department of Internal Medicine, Seoul St. Mary’s Hospital, College of Medicine, The Catholic University of Korea, 222 Banpo-daero, Seocho-gu 137-701, Seoul, Korea
2
Department of Preventive Medicine, College of Medicine, The Catholic University of Korea, 222 Banpo-daero, Seocho-gu, Seoul 137-701, Republic of Korea
3
Department of Ophthalmology, College of Medicine, The Catholic University of Korea, 222 Banpo-daero, Seocho-gu, Seoul 137-701, Republic of Korea
Introduction Diabetic retinopathy is the most common microvascular complication of diabetes mellitus (DM), affecting approximately 30 % of people with DM [1], a third of whom have vision-threatening retinopathy, defined as severe retinopathy or macular edema [2]. It has been estimated that approximately 18.6 % of diabetic patients have retinopathy in South Korea [3]. This condition is the most frequent cause of preventable blindness in working-age adults (20–74 years) [4]. Hyperglycemia, hypertension, hypercholesterolemia, and a
Osteoporos Int
longer duration of DM are well-known risk factors for diabetic retinopathy [5]. A significantly increased risk of fractures associated with visual impairment due to diabetic retinopathy has been reported in many studies [6, 7]. There is a substantial body of literature on the association between type 2 DM and fracture risk. An increased fracture risk in type 2 DM patients has been reported [8, 9] although bone mineral density (BMD) is typically normal or higher than in non-diabetic controls [10]. A longer disease duration, the presence of diabetic complications, and inadequate glycemic control all have been reported to increase the fracture risk in diabetic patients [11]. Diabetic neuropathy, retinopathy, peripheral neuropathy, vestibular dysfunction, cognitive impairment, and muscle weakness of the lower limbs are common complications of DM. All of these complications have been shown to increase the risk of fracture in diabetic patients by promoting falls [12]. Several studies have reported that the presence of chronic complications is associated with low BMD. Patients with neuropathy [13, 14], and even those with early-stage diabetic kidney disease with microalbuminuria, exhibited decreased BMD [15]. However, little is known regarding the association between BMD and diabetic retinopathy in diabetic patients. To the best of our knowledge, this is the first study that shows the association between diabetic retinopathy and BMD in type 2 DM subjects. We hypothesized that diabetic subjects with retinopathy may have lower BMD because of the long disease duration and poor disease control statuses which are considered to be the risk factors of fracture. The aim of this study was to evaluate the relationship between the prevalence of diabetic retinopathy and osteoporosis in diabetic subjects who participated in the Korea National Health and Nutritional Examination Surveys (KNHANES).
Materials and methods Study design and participants This study was based on data acquired from the KNHANES, which has been periodically conducted by the Division of Health and Nutritional Survey in the Korean Centers for Disease Control and Prevention (KCDCP) since 1998. It is an ongoing, population-based, cross-sectional, and nationally representative survey, and it provides the largest publicly available database in South Korea. Participants were chosen from candidates using proportional-allocation, systematic sampling with multistage stratification (by age, gender, and region). Twenty-three households from 200 randomly selected sampling units were chosen in 2008 and 2009, whereas 20 households from 192 sampling units were chosen in 2010 and 2011. The KNHANES consists of three different components: a health interview, a nutrition survey, and a health
examination. Data were collected by household interviews and direct standardized physical examinations conducted at mobile examination centers. During the period from July 2008 to May 2011, the KNHANES interview and examination were completed for 26,775 individuals. Of the 10,366 participants who were aged ≥50 years, 617 were excluded according to the following exclusion criteria: current or previous usage of anti-osteoporotic medication or estrogen therapy, severe chronic kidney disease (CKD), and pre-menopausal female or suspicion of type 1 DM (Fig. 1). The institutional review board of the Catholic University of Korea approved this study (no. KC15RISI0608). Written informed consent was obtained from all participants. Health examination survey and laboratory tests Various factors were examined. After the height and weight were measured using standardized techniques and equipment, body mass index (BMI) was calculated by dividing body weight by height squared (kg/m2). Blood pressure (BP) was measured by standard methods using a sphygmomanometer with the patient in a sitting position. Information regarding demographic and social factors was obtained using a standardized questionnaire during the health interview. Heavy alcohol drinking was categorized as drinking four or more times per week and 3 units of alcohol per time. Current smoker was defined as currently smoking with a smoking history of ≥100 cigarettes in a lifetime. In addition, a urinary cotinine level of above 164 ng/mL was used to determine inaccurate reporting of current tobacco use [16]. After fasting for at least 8 h, blood samples were collected in the morning and analyzed at a central, certified laboratory. Severe CKD was defined as glomerular filtration rate (GFR) of less than 30 mL/ min/1.73 m2, as calculated using the Cockcroft-Gault formula. The following definitions were obtained from the Division of Health and Nutritional Survey under the KCDCP. Hypertension was defined by either a self-reported history of hypertension diagnosis and current usage of antihypertensive drugs or a systolic BP of ≥140 mm Hg or a diastolic BP of ≥90 mm Hg. Hypercholesterolemia was defined as a total cholesterol concentration of ≥240 mg/dL or prescription of anti-cholesterol medication. The results of urine dipstick tests were recorded as (−), trace, (1+), (2+), or (3+), and proteinuria was defined as ≥(1+) proteinuria by dipstick. Assessment of BMD and definition of osteoporosis Osteoporosis examinations began in July 2008 and ended in May 2011. The subjects were ≥19 years of age from July 2008 to June 2009 and ≥10 years of age from July 2009 to May 2011. The BMD of the lumbar spine, left total hip, and left femoral neck was measured by dual-energy X-ray absorptiometry (DXA; Discovery-W; Hologic Inc., Waltham, MA,
Osteoporos Int Fig. 1 Flow diagram for identification of the study population. A total of 9749 subjects were finally included. KNHANES, Korea National Health and Nutrition Examination Survey; GFR, glomerular filtration rate
USA). For the lumbar spine BMD, the mean value of L1 to L4 was chosen for analysis following the recommendation of the International Society for Clinical Densitometry (ISCD) in 2007 [17]. When the BMD of the left femur could not be measured (e.g., postoperative state, fracture, deformity, or malformation), the BMD of the right femur was used. The technicians who performed the BMD measurements were tested for precision based on duplicate measurements of 30 participants or triplicate measurement of 15 participants. Precision error was calculated as a percentage coefficient of variation (CV%). The allowed precision errors for the total hip, femur neck, and total lumbar spine were 1.8, 2.5, and 1.9 %, respectively. According to the criteria established by the World Health Organization (WHO), osteoporosis was diagnosed in subjects with a T-score of less than or equal to −2.5, and osteopenia was diagnosed in subjects with a T-score of between −2.5 and −1.0, and subjects with a T-score of −1.0 or higher were considered normal [18]. Assessments and definitions of DM and diabetic retinopathy DM was defined as a previous diagnosis of DM made by a physician, the use of insulin or oral hypoglycemic agents, and/ or a fasting blood glucose level of 126 mg/dL or higher. The participants were considered to have type 1 DM if they were younger than 30 of age when diagnosed with DM and were receiving insulin therapy. Non-mydriatic digital fundus photographs (TRC-NW6S; Topcon, Tokyo, Japan) were taken of all the participants ≥19 years old. Next, seven gradable
standard photographs were obtained from both eyes after pharmacologic pupil dilatation for diabetic retinopathy assessment. It was performed for participants with a history of DM, a random blood glucose level of >200 mg/dL, or a suspicious diabetic retinopathy finding in digital fundus photographs. Each image was graded for retinopathy according to the Early Treatment for Diabetic Retinopathy Study (ETDRS) severity level and was dichotomized as having retinopathy (level 15 and above) or not having retinopathy (≤14) [19]. Because the level of retinopathy was determined based on the worse eye, diabetic retinopathy was defined as the presence of diabetic retinopathy, in either eye. The quality of the survey was verified by the Epidemiologic Survey Committee of the Korean Ophthalmologic Society. Statistical analysis Participants in the KNHANES were selected for participation based on a stratified, multi-stage probability sampling design. The weights for each respondent, representing the inverse of their sampling probabilities, were provided by the Korean Center for Disease Control and have been used in many analyses to obtain estimates that are representative of the non-institutionalized South Korean civilian population. All continuous data were presented as the mean ± standard error (SE). All categorical data were presented as numbers and percentages. To compare the principal characteristics of the study subjects between the two groups, Student’s t test for continuous variables and the χ2 test for categorical variables were used. The multiple linear regression analyses were used to
Osteoporos Int
determine whether the BMD at each measured site differed according to the prevalence of DM or diabetic retinopathy. Univariable and multivariable logistic regression models were used to estimate the odds ratio (OR) of osteoporosis in each group. All analyses were two-tailed and were carried out using SAS version 9.3 (SAS Institute, Cary, NC, USA). Results with a p value of less than 0.05 were considered statistically significant.
Results Baseline characteristics of the subjects according to the presence of diabetes mellitus Among the total participants who were 50 years of age and older from the KNHANES 2008–2011, 655 (15.0 %) men and 703 (13.0 %) women were diagnosed as having diabetes. The baseline characteristics of diabetic subjects and non-diabetic controls are shown in Table 1. The diabetic women were older than non-diabetic women (mean age 66.35 vs. 63.18 years), although the mean age of diabetic men did not differ from that of non-diabetic men (62.03 vs. 61.41 years). Both the male and female diabetic subjects were more likely to be Table 1
overweight or obese, and to have higher fasting glucose, and HbA1c levels, proteinuria, hypertension, and hypercholesterolemia (p < 0.05). The subjects with or without DM did not differ in terms of BMD according to the WHO criteria. Association between prevalence of diabetes and osteoporosis The BMDs at various measured sites were compared in the diabetic subjects and non-diabetic controls. The diabetic men had higher lumbar spine and total hip BMDs than non-diabetic men in crude analysis. However, this association was diminished after further adjustments for all clinically relevant covariates (age, BMI, current smoking status, heavy alcohol intake, proteinuria, hypertension, and hypercholesterolemia). The BMDs at all measured sites of women did not differ in terms of diabetic status prior to adjustments for confounders. However, the diabetic women had higher BMDs at the lumbar spine and total hip than non-diabetic women following adjustments for age and BMI with or without the other confounders (Table 2). Further logistic regression analyses of osteoporosis according to the prevalence of DM are shown in Fig. 2. The prevalence of osteoporosis did not differ according to the diabetic status in men regardless of the adjustment model
Weighted baseline characteristics of study participants from the KNHANES (2008–2011) Men (n = 4,357)
Women (n = 4,392)
DM (−) n = 3702 (N = 5,841,433)
DM (+) n = 655 (N = 1,006,815)
p value
DM (−) n = 4689 (N = 6,429,843)
DM (+) n = 703 (N = 911,792)
p value
Age (years)
61.41 ± 0.23
62.03 ± 0.41
0.145
63.18 ± 0.21
66.35 ± 0.46
