Association Between Hemoglobin Levels and Osteoporosis in Chinese Patients with Type 2 Diabetes Mellitus: A Cross-Sectional Study

Figures & data

Figure 1 Flow diagram of the subjects selection process.

Table 1 Characteristics of the Study Population Stratified by the Prevalence of Osteoporosis

	All (n=495)	NOP (n=330)	OP (n=165)	P
Age (years)	60.37±11.41	58.28±11.09	64.26±11.00	<0.001
Gender				<0.001
Male	299 (60.40%)	228 (69.09%)	71 (43.03%)	–
Female	196 (39.60%)	102 (30.91%)	94 (56.97%)	–
BMI (kg/m^2)	24.39 (22.59, 26.63)	24.76 (22.86, 27.34)	23.68 (22.05, 25.90)	<0.001
Diabetic duration (years)	6.00 (0.50, 12.00)	6.00 (0.75, 12.00)	5.00 (0.50, 13.00)	0.889
Smoking (%)	106 (21.41%)	83 (25.15%)	23 (13.94%)	0.004
Drinking (%)	195 (39.39%)	144 (43.64%)	51 (30.91%)	0.006
FBG (mmol/L)	6.84 (5.58, 8.96)	6.88 (5.58, 9.12)	6.77 (5.57, 8.68)	0.536
HbA1c (%)	8.50 (7.20, 10.60)	8.70 (7.20, 10.60)	8.30 (7.20, 10.60)	0.545
RBC (10^12/L)	4.67 (4.29, 5.10)	4.72 (4.34, 5.14)	4.53 (4.20, 4.95)	<0.001
HGB (g/L)	134.70 (124.35, 145.30)	137.25 (126.00, 147.00)	131.6 (120.00, 140.00)	<0.001
PLT (10^9/L)	243.00 (199.00, 275.05)	232.35 (198.00, 272.00)	240 (200.00, 286.90)	0.122
ALB (g/L)	39.30 (36.90, 41.90)	38.45 (37.30, 42.10)	39.00 (36.20, 41.10)	0.009
25(OH)D (nmol/L)	46.51 (39.60, 56.25)	47.60 (41.63, 56.20)	44.98 (38.01, 56.65)	0.051
eGFR (mL/min/1.73m^2)	94.43 (78.58, 103.36)	94.81 (78.51, 104.36)	91.44 (78.64, 101.35)	0.327
FN BMD (g/cm^2)	0.70 (0.61, 0.80)	0.76 (0.69, 0.83)	0.58 (0.54, 0.65)	<0.001
TH BMD (g/cm^2)	0.84±0.14	0.90±0.11	0.72±0.11	<0.001
LS BMD (g/cm^2)	0.90±0.16	0.97±0.12	0.77±0.13	<0.001

Abbreviations: OP, osteoporosis; BMI, body mass index; FBG, fast blood glucose; HbA1c, glycated hemoglobin A1c; RBC, red blood cell; HGB, hemoglobin; PLT, platelets; ALB, albumin; eGFR, estimated glomerular filtration rate; FN, femoral neck; TH, total hip; LS, lumbar spine; BMD, bone mineral density.

Table 2 The Prevalence of Osteoporosis and BMD Grouped by Hemoglobin Levels

	Hemoglobin Levels
	Q1(n=56)	Q2 (n=194)	Q3 (n=245)	P
OP (%)	22 (39.29%)	70 (36.08%)	73 (29.80%)	0.231
FN BMD (g/cm^2)	0.69 (0.58, 0.78)	0.67 (0.58, 0.78)	0.72 (0.63, 0.82)^ab	0.002
TH BMD (g/cm^2)	0.80±0.14	0.82±0.14^a	0.86±0.13^ab	0.001
LS BMD (g/cm^2)	0.88±0.15	0.90±0.16	0.90±0.15	0.585

Notes: ^aCompared to Q1, P<0.05; ^bCompared to Q2, P<0.05.

Abbreviations: OP, osteoporosis; FN, femoral neck; TH, total hip; LS, lumbar spine; BMD, bone mineral density.

Table 3 Spearman Correlation Analysis on Associations of Risk Factors with BMD and Osteoporosis

	OP	FN BMD	TH BMD	LS BMD
Age (years)	0.247**	−0.317**	−0.325**	−0.128**
Gender	0.251**	−0.389**	−0.414**	−0.352**
BMI (kg/m^2)	−0.211*	0.267**	0.299**	0.304**
Diabetic duration (years)	0.006	−0.105*	−0.054	0.030
Smoking (%)	−0.106*	0.198**	0.219**	0.131**
Drinking (%)	−0.123**	0.269**	0.244**	0.136**
FBG (mmol/L)	−0.028	0.023	−0.017	0.020
HbA1c (%)	−0.027	0.069	0.047	0.074
RBC (10^12/L)	−0.170**	0.219**	0.227**	0.133**
HGB (g/L)	−0.204**	0.309**	0.308**	0.184**
PLT (10^9/L)	0.070	−0.044	−0.027	−0.080
ALB (g/L)	−0.118**	0.105*	0.072	0.033
25(OH)D (nmol/L)	−0.088	0.105*	0.089*	0.129**
eGFR (mL/min/1.73m^2)	−0.044	0.130**	0.123**	−0.066

Notes: *P<0.05. **P<0.01.

Abbreviations: OP, osteoporosis; BMI, body mass index; FBG, fast blood glucose; HbA1c, glycated hemoglobin A1c; RBC, red blood cell; HGB, hemoglobin; PLT, platelets; ALB, albumin; eGFR, estimated glomerular filtration rate; FN, femoral neck; TH, total hip; LS, lumbar spine; BMD, bone mineral density.

Table 4 Logistic Regression Analysis of Osteoporosis Risk Factors in Patients with T2DM

	P	OR (95% CI)
Age (years)	<0.001	1.046 (1.028–1.065)
Gender	<0.001	2.959 (2.010–4.356)
BMI (kg/m^2)	<0.001	0.856 (0.805–0.910)
Diabetes duration (years)	0.452	1.010 (0.985–1.035)
Smoking (%)	0.005	0.482 (0.291–0.799)
Drinking (%)	0.007	0.578 (0.389–0.858)
FBG (mmol/L)	0.985	1.001 (0.943–1.062)
HbA1c (%)	0.727	0.986 (0.911–1.067)
RBC (10^12/L)	0.004	0.678 (0.520–0.884)
HGB (g/L)	<0.001	0.974 (0.963–0.985)
PLT (10^9/L)	0.063	1.003 (1.000–1.006)
ALB (g/L)	0.012	0.944 (0.903–0.987)
25(OH)D (nmol/L)	0.115	0.989 (0.975–1.003)
eGFR (mL/min/1.73m^2)	0.533	0.997 (0.988–1.006)

Abbreviations: OP, osteoporosis; BMI, body mass index; FBG, fast blood glucose; HbA1c, glycated hemoglobin A1c; RBC, red blood cell; HGB, hemoglobin; PLT, platelets; ALB, albumin; eGFR, estimated glomerular filtration rate.

Table 5 Logistic Regression Models for the Association Between Hemoglobin Levels and Osteoporosis Stratified by Gender and Age

Model	P	OR (95% CI)
Model 1
Male	0.015	0.976 (0.956–0.995)
Female	0.712	0.996 (0.973–1.019)
Model 2
Male	0.016	0.976 (0.956–0.995)
Female	0.733	0.996 (0.973–1.019)
Model 3
Male
<50	0.574	0.978 (0.906–1.056)
≥50	0.030	0.978 (0.958–0.998)

Notes: Model 1: adjusted for age, BMI, diabetic duration and eGFR; Model 2: further adjusted for smoking and drinking based on Model 1; Model 3: adjusted for BMI, diabetic duration, eGFR, smoking and drinking.

Table 6 The Association Between Hemoglobin at Three Levels and Osteoporosis Stratified by Gender

Model	Q1		Q2
	P	OR (95% CI)	P	OR (95% CI)
Model 1
Male	0.030	2.954 (1.113–7.837)	0.249	1.457 (0.768–2.766)
Female	0.476	0.683 (0.239–1.951)	0.397	0.752 (0.389–1.454)
Model 2
Male	0.032	2.943 (1.095–7.907)	0.221	1.494 (0.785–2.842)
Female	0.444	0.661 (0.230–1.905)	0.372	0.740 (0.382–1.434)

Notes: Model 1: adjusted for age, BMI, diabetic duration and eGFR; Model 2: further adjusted for smoking and drinking based on Model 1.