Introduction
Materials and methods
Study participants and variables
Measurements
Subgroup categorization
Statistical analysis
Results
Characteristics of the study participants
Variable | eGFR ≥ 90 (normal) | eGFR < 90 (decreased renal function) | ||||
---|---|---|---|---|---|---|
Diabetes | Non-diabetes | p | Diabetes | Non-diabetes | p | |
Anemia | ||||||
N (%) | 43 (3.4) | 1217 (96.6) | 66 (16.8) | 327 (83.2) | ||
Age (years) | 58.7 (10.8) | 50.8 (11.0) | < 0.001 | 67.5 (8.8) | 62.3 (11.4) | < 0.001 |
Body mass index (kg/m2) | 26.0 (5.6) | 22.8 (3.3) | 0.001 | 26.3 (4.7) | 23.8 (3.4) | < 0.001 |
Hemoglobin (g/dL) | 11.0 (1.1) | 10.8 (1.2) | 0.192 | 11.2 (0.7) | 11.1 (0.9) | 0.565 |
Anemia level, n (%) | 0.383 | 0.764 | ||||
Mild | 29 (67.4) | 694 (57.0) | 47 (71.2) | 224 (68.5) | ||
Moderate | 13 (30.2) | 472 (38.8) | 19 (28.8) | 101 (30.9) | ||
Severe | 1 (2.3) | 51 (4.2) | 0 | 2 (0.6) | ||
Hypertension, n (%) | 19 (44.2) | 101 (8.3) | < 0.001 | 46 (69.7) | 104 (31.8) | < 0.001 |
Hyperlipidemia, n (%) | 8 (18.6) | 30 (2.5) | < 0.001 | 24 (36.4) | 22 (6.7) | < 0.001 |
Chronic kidney disease, n (%) | 0 (0.0) | 5 (0.4) | > 0.999 | 9 (13.6) | 25 (7.6) | 0.114 |
Systolic blood pressure (mmHg) | 131.2 (18.3) | 119.5 (19.7) | < 0.001 | 135.4 (22.6) | 126.3 (21.6) | 0.002 |
Low-density lipoprotein cholesterol (mg/dL) | 93.2 (25.2) | 104.8 (27.1) | 0.005 | 88.4 (26.5) | 111.3 (29.2) | < 0.001 |
Fasting blood glucose (mg/dL) | 148.4 (44.5) | 96.7 (11.7) | < 0.001 | 139.8 (40.1) | 99.0 (10.6) | < 0.001 |
eGFR (mL/min/1.73m2) | 118.3 (26.5) | 120.3 (22.0) | 0.558 | 60.7 (20.4) | 72.2 (18.4) | < 0.001 |
Alkaline phosphatase (IU/L) | 70.4 (19.5) | 65.0 (28.4) | 0.215 | 68.4 (21.2) | 71.3 (24.4) | 0.367 |
Osteoporosis, n (%) | 13 (30.2) | 223 (18.3) | 0.049 | 27 (40.9) | 136 (41.6) | 0.918 |
Non-anemia | ||||||
N (%) | 522 (6.4) | 7663 (93.6) | 207 (10.2) | 1827 (89.8) | ||
Age (years) | 62.0 (8.2) | 55.5 (10.5) | < 0.001 | 65.3 (7.9) | 61.6 (9.6) | < 0.001 |
Body mass index (kg/m2) | 25.2 (4.0) | 23.4 (3.4) | < 0.001 | 25.4 (3.4) | 24.4 (3.6) | < 0.001 |
Hemoglobin (g/dL) | 13.6 (0.9) | 13.5 (0.8) | 0.002 | 13.3 (0.9) | 13.4 (0.9) | 0.018 |
Hypertension, n (%) | 236 (45.2) | 1110 (14.5) | < 0.001 | 114 (55.1) | 532 (29.1) | < 0.001 |
Hyperlipidemia, n (%) | 144 (27.6) | 392 (5.1) | < 0.001 | 78 (37.7) | 148 (8.1) | < 0.001 |
Chronic kidney disease, n (%) | 4 (0.8) | 39 (0.5) | 0.351 | 7 (3.4) | 29 (1.6) | 0.086 |
Systolic blood pressure (mmHg) | 131.3 (19.3) | 124.1 (20.5) | < 0.001 | 131.2 (19.5) | 129.9 (21.5) | 0.371 |
Low-density lipoprotein cholesterol (mg/dL) | 105.6 (30.7) | 119.6 (30.9) | < 0.001 | 99.0 (30.3) | 123.9 (31.7) | < 0.001 |
Fasting blood glucose (mg/dL) | 150.0 (43.1) | 100.7 (15.3) | < 0.001 | 149.8 (43.7) | 102.3 (15.1) | < 0.001 |
eGFR (mL/min/1.73m2) | 116.6 (20.8) | 116.8 (19.4) | 0.795 | 75.2 (11.9) | 79.6 (9.0) | < 0.001 |
Alkaline phosphatase (IU/L) | 76.4 (22.8) | 77.1 (42.3) | 0.730 | 74.8 (22.5) | 77.9 (23.1) | 0.073 |
Osteoporosis, n (%) | 146 (28.0) | 2097 (27.4) | 0.765 | 58 (28.0) | 612 (33.5) | 0.112 |
Variable | eGFR ≥ 90 (normal) | eGFR < 90 (decreased renal function) | ||||
---|---|---|---|---|---|---|
Diabetes | Non-diabetes | p | Diabetes | Non-diabetes | p | |
Anemia | ||||||
N (%) | 43 (3.4) | 1217 (96.6) | 66 (16.8) | 327 (83.2) | ||
Lumbar spine BMD (g/cm2) | 0.935 (0.182) | 0.929 (0.156) | 0.814 | 0.870 (0.163) | 0.854 (0.174) | 0.493 |
Lumbar spine T-score | −0.6 (1.6) | −0.7 (1.4) | 0.853 | −1.1 (1.4) | −1.3 (1.5) | 0.431 |
Right hip femoral neck BMD (g/cm2) | 0.667 (0.149) | 0.678 (0.123) | 0.569 | 0.613 (0.134) | 0.610 (0.125) | 0.864 |
Right hip femoral neck T-score | −1.3 (1.3) | −1.2 (1.1) | 0.428 | −1.8 (1.3) | −1.8 (1.2) | 0.783 |
Right hip total BMD (g/cm2) | 0.827 (0.139) | 0.812 (0.127) | 0.459 | 0.786 (0.137) | 0.763 (0.136) | 0.220 |
Right hip total T-score | −0.2 (1.2) | −0.3 (1.1) | 0.426 | −0.5 (1.2) | −0.7 (1.2) | 0.226 |
Left hip neck femoral BMD (g/cm2) | 0.671 (0.144) | 0.686 (0.125) | 0.430 | 0.627 (0.135) | 0.618 (0.125) | 0.624 |
Left hip neck femoral T-score | −1.3 (1.4) | −1.1 (1.2) | 0.433 | −1.7 (1.3) | −1.7 (1.2) | 0.661 |
Left hip total BMD (g/cm2) | 0.785 (0.143) | 0.781 (0.130) | 0.842 | 0.753 (0.137) | 0.732 (0.137) | 0.247 |
Left hip total T-score | −0.6 (1.2) | −0.6 (1.1) | 0.772 | −0.8 (1.2) | −1.0 (1.2) | 0.258 |
Non-anemia | ||||||
N (%) | 522 (6.4) | 7663 (93.6) | 207 (10.2) | 1827 (89.8) | ||
Lumbar spine BMD (g/cm2) | 0.876 (0.147) | 0.881 (0.153) | 0.431 | 0.894 (0.138) | 0.856 (0.149) | < 0.001 |
Lumbar spine T-score | −1.1 (1.3) | −1.1 (1.3) | 0.593 | −0.9 (1.2) | −1.3 (1.3) | < 0.001 |
Right hip femoral neck BMD (g/cm2) | 0.646 (0.119) | 0.645 (0.112) | 0.888 | 0.639 (0.110) | 0.622 (0.110) | 0.035 |
Right hip femoral neck T-score | −1.5 (1.1) | −1.5 (1.1) | 0.799 | −1.6 (1.0) | −1.7 (1.0) | 0.051 |
Right hip total BMD (g/cm2) | 0.795 (0.135) | 0.782 (0.122) | 0.039 | 0.801 (0.120) | 0.778 (0.121) | 0.010 |
Right hip total T-score | −0.5 (1.1) | −0.6 (1.1) | 0.007 | −0.4 (1.0) | −0.6 (1.0) | 0.015 |
Left hip femoral neck BMD (g/cm2) | 0.653 (0.117) | 0.654 (0.112) | 0.766 | 0.649 (0.109) | 0.631 (0.112) | 0.030 |
Left hip femoral neck T-score | −1.4 (1.1) | −1.4 (1.1) | 0.894 | −1.4 (1.1) | −1.6 (1.1) | 0.021 |
Left hip total BMD (g/cm2) | 0.776 (0.133) | 0.760 (0.123) | 0.007 | 0.785 (0.114) | 0.754 (0.123) | 0.001 |
Left hip total T-score | −0.6 (1.1) | −0.8 (1.1) | 0.001 | −0.6 (1.0) | −0.8 (1.1) | < 0.001 |
Univariate logistic regression analysis of osteoporosis
Variable | Odds ratios (95% confidence interval) | p |
---|---|---|
Age (/10 years) | 2.74 (2.60‒2.89) | < 0.001 |
Body mass index (kg/m2) | 0.89 (0.88‒0.90) | < 0.001 |
Hemoglobin (g/dL) | 1.05 (1.02‒1.09) | 0.002 |
Anemia | 0.76 (0.67‒0.86) | < 0.001 |
Hypertension | 1.59 (1.43‒1.77) | < 0.001 |
Hyperlipidemia | 1.36 (1.14‒1.62) | 0.001 |
Chronic kidney disease | 1.38 (0.91‒2.10) | 0.128 |
Systolic blood pressure (/10 mmHg) | 1.09 (1.07‒1.11) | < 0.001 |
Low-density lipoprotein cholesterol(/10 mg/dL) | 1.02 (1.01‒1.04) | 0.001 |
Fasting blood glucose (/10 mg/dL) | 1.04 (1.01‒1.07) | 0.005 |
eGFR (/10 mL/min/1.73m2) | 0.92 (0.90‒0.93) | < 0.001 |
Alkaline phosphatase (/10 mg/dL) | 1.22 (1.19‒1.24) | < 0.001 |
Variable | Odds ratios (95% confidence interval) | p |
---|---|---|
Age (/10 years) | 2.57 (2.07‒3.20) | < 0.001 |
Body mass index (kg/m2) | 0.86 (0.82‒0.90) | < 0.001 |
Hemoglobin (g/dL) | 0.83 (0.73‒0.93) | 0.002 |
Anemia | 1.49 (0.98‒2.28) | 0.063 |
Hypertension | 0.98 (0.73‒1.32) | 0.899 |
Hyperlipidemia | 1.03 (0.75‒1.42) | 0.863 |
Chronic kidney disease | 1.64 (0.66‒4.07) | 0.283 |
Systolic blood pressure (/10 mmHg) | 0.98 (0.91‒1.06) | 0.688 |
Low-density lipoprotein cholesterol (/10 mg/dL) | 0.99 (0.94‒1.04) | 0.655 |
Fasting blood glucose (/10 mg/dL) | 0.98 (0.95‒1.02) | 0.309 |
eGFR (/10 mL/min/1.73m2) | 0.96 (0.91‒1.01) | 0.117 |
Alkaline phosphatase (/10 mg/dL) | 1.13 (1.06‒1.21) | < 0.001 |
Disease status | n | odds ratios (95% confidence interval) | p | ||
---|---|---|---|---|---|
Diabetes | Anemia | Renal function | |||
non-diabetes | anemia | normal | 1217 | 1.14 (1.02‒1.27) | 0.023 |
non-diabetes | anemia | decreased | 327 | 1.12 (0.91‒1.38) | 0.285 |
non-diabetes | non-anemia | normal | 7663 | 1.04 (1.01‒1.07) | 0.015 |
non-diabetes | non-anemia | decreased | 1827 | 0.94 (0.88‒1.01) | 0.084 |
Diabetes | anemia | normal | 43 | 0.87 (0.72‒1.05) | 0.136 |
diabetes | anemia | decreased | 66 | 1.25 (1.05‒1.47) | 0.010 |
diabetes | non-anemia | normal | 522 | 0.97 (0.92‒1.02) | 0.180 |
diabetes | non-anemia | decreased | 207 | 0.98 (0.91‒1.05) | 0.579 |
Multiple logistic regression analysis of osteoporosis and fasting blood glucose
Disease status | n | odds ratios (95% confidence interval) | p | ||
---|---|---|---|---|---|
Diabetes | Anemia | Renal function | |||
non-diabetes | anemia | normal | 1217 | 1.01 (0.88‒1.17) | 0.847 |
non-diabetes | anemia | decreased | 327 | 0.91 (0.67‒1.22) | 0.513 |
non-diabetes | non-anemia | normal | 7663 | 0.98 (0.94‒1.02) | 0.289 |
non-diabetes | non-anemia | decreased | 1827 | 0.93 (0.86‒1.02) | 0.114 |
diabetes | anemia | normal | 43 | 0.92 (0.62‒1.35) | 0.656 |
diabetes | anemia | decreased | 66 | 1.57 (1.16‒2.14) | 0.004 |
diabetes | non-anemia | normal | 522 | 0.95 (0.89‒1.00) | 0.070 |
diabetes | non-anemia | decreased | 207 | 0.97 (0.90‒1.05) | 0.508 |
Discussion
Osteoporosis, bone mineral density, and fasting blood glucose
Predictor | Outcome variable | Association | Study population | Definition of outcome variable | Reference |
---|---|---|---|---|---|
Diabetes | bone quality | − | [1] | ||
Diabetes | fracture | + | |||
Diabetes | bone mineral density | + | review, 26 articles | comprehensive review of 47 studies | [20] |
Diabetes | bone mineral density | NS | review, 8 articles | ||
Diabetes | bone mineral density | − | review, 13 articles | ||
Diabetes | body mass index | + | [21] | ||
Diabetes | osteoporosis | + | n = 3331, Taiwan retrospective cohort study, ≥ 40 years from the 2002 TwSHHH linked to the NHIRD, over a median follow-up duration of 13.6 years | incident osteoporosis based on ICD9-CM codes or the use of anti-osteoporotic agents | [10] |
Diabetes | osteoporosis | − | n = 96,626, Korean cohort study, over 55 years received health check-up in 2009 linked to NHIS, average follow-up period 4.14 person-years | incident osteoporosis basis of ICD-code with newly registered | [26] |
Diabetes | anemia | + | [12] | ||
Diabetes (older males) | osteoporosis | − | n = 553, Iran cross-sectional study, ≥ 60 years from Amirkola health and ageing project in 2011–2012 | osteoporosis based on T-score ≤ − 2.5 at either lumbar spine or femoral neck, bone mineral density by DXA | [68] |
anemia | − | ||||
Iron deficiency anemia | osteoporosis | + | Iron deficiency anemia (n = 35,751) and no iron deficiency anemia (n = 178,755) sampled individuals from the 1998–2012 Taiwan NHIRD, cross-sectional study | osteoporosis based on ICD-9-CM code T score < 2.5 by DXA | [43] |
Hemoglobin | osteoporosis | − | n = 139,520, osteoporosis and control 1:1 matched, Korean cross-sectional study, ≥ 40 years from NHIS Health Screening Cohort data, 2002–2013 | osteoporosis based on ICD-10 codes | [14] |
Hemoglobin & diabetes | osteoporosis (older men) | − | n = 573, China cross-sectional study, ≥ 60 years from Xuanwu Hospital, 2016/07–2018/05 | osteoporosis based on T-score ≤ − 2.5 at any of lumbar spine, femoral neck and hip sites, bone mineral density by DXA | [72] |
Fasting blood glucose + non-diabetes (women) | bone mineral density | + | n = 2367, China cross-sectional study, > 65 years, three medical examination centers, 2019/01–2020/12, | osteoporosis based on T-score ≤ − 2.5 at any of lumbar spine, femoral neck and hip sites, bone mineral density by DXA | [78] |
osteoporosis | − | ||||
Fasting blood glucose | osteoporosis | + | n = 101, Vietnam type-2 diabetic patients, cross-sectional study, ≥ 30 years, admitted to 175 Military Hospital for treatment, 2018/04–2019/03 | DXA | [24] |
Fasting blood glucose or diabetes | bone mineral density | + | T2DM n = 1719, non-diabetes n = 6401, Taiwan cross-sectional study, 50–90 years from Health Examination Database of a hospital, 2010/01–2015/12 | osteoporosis based on T-score ≤ − 2.5 at lumbar spine or femoral neck, bone mineral density by DXA | [21] |
osteoporosis | − | ||||
Fasting blood glucose | osteoporosis, diabetes with high-increasing fasting blood glucose in men | + | n = 18,313, China, cohort study, physical examinations at a center during 2008–2018, more than 4-year follow-up period | incidence of osteoporosis based on T-score ≤ − 2.5 at lumbar spine, bone mineral density by DXA | [25] |
osteoporosis, non-diabetes with elevated-increasing fasting blood glucose in women | − | ||||
Fasting blood glucose | vBMD | NS | n = 10,309, China health check-up cohort, 2018–2019 | vBMD, lumbar spine by QCT | [88] |
aBMD (men) | + | aBMD, lumbar spine, by DXA | |||
Insulin resistance (HOMA-IR) + diabetes | osteoporosis (women) | + | n = 234, China, cross-sectional study, department of Endocrinology and Metabolism at a hospital, 2016/02–2018/08 | osteoporosis based on T-score ≤ − 2.5 at lumbar spine, bone mineral density by DXA | [31] |
Insulin resistance (HOMA-IR) + non-diabetes, postmenopausal women | aBMD | NS | n = 146, Study of Women’s Health Across the Nation, cross-sectional study | aBMD at lumbar spine and total hip by DXA | [89] |
vBMD and trabecular and cortical thickness | + | vBMD and bone microarchitecture by HR-pQCT, 2008/09–2011/04 |