Osteoporosis and type 2 diabetes mellitus: what do we know, and what we can do?

Figures & data

Table 1 Osteoporosis in type 2 diabetes mellitus

Country	Sample size/ sex (F/M)^*	Age (years)	Duration (years)	Method of BMD measurement/ study design	Control	Major finding
						Site	HbA1c	Duration	Complication	BMD
Canada^Citation78	n, 63 F nc, 99	78 77	8–40	Roentgenographic	Age-matched control	Radius	NR	NR	NR	↑
USA^Citation79	n, 79 POM nc, 59	50–70	8.6 ± 7.2	Photon absorptiometry	Age-matched control	Radius	↓	↑	NR	↑
Japan^Citation76	n, 168 (84/84)* nc, 78 (27/51)*	30–80	1–31	X-ray film/ microdensitometer	Age-matched control	Metacarpal bone	↔	↔	NR	↓ ON 38.1%
Italy^Citation74	n, 40 F nc, 35	42–83	NR	DPA	Age-matched control	LS	↔	↔	↔	↓
Italy^Citation82	n, 53 (26/27)* DM1 n, 47 (29/18)* DM2 nc, 500 (300/200)	40.9 ± 2.3 DM1 56.7 ± 2.0 DM2	15.8 ± 1.3 DM1 14.7 ± 1.1 DM2	SPA CS	Age-matched control	Forearm/ DR	↔	↔	NR	↔
USA^Citation73	n, 28 F nc, 207	26–84, mean, 59.2 ± 2.9	8.9 ± 1.2	DPA NR	Age- and WT- matched control	LS	↔	↔	NR	↔
USA^Citation75	n, 80 (39/41)* nc, 381 (242/139)*	72 (55–88)	1–5	SPA/DXA CS	IGT and NGT	Wrist, midradius/ LS, FN	NR	NR	NR	↑ in F ↔ in M
Japan^Citation28	n, 78 (40/38)*	62/63	12	DXA NR	Age- and sex- matched control	LV	↔	↑ (−ve R with BMD)	NR	↔
Italy^Citation33	n, 110 DM2 [60(35/25)¶ 50 (26/24) μ] nc, 50	60–75	>5–15	DPA CS	Age-, sex-, and BMI-matched control	BMC	↑	NR	NR	↓
Netherlands^Citation89	n, 578 (335/243)* nc, 5353 (3115/2238)*	≥55	NR	DXA CS/PS population-based study	Age-matched control	LS PF	NR	NR	NR	↑ ↓ nonvertebral fractures
Norway^Citation149	n, 36 (15 POM/21)	40–65	3–15	DXA/US CS	Age- and sex- matched control	BMC, FN/calcaneus	NR	NR	NR	↑ in M only
Spain^Citation84	n, 47 F nc, 252	61.3 ± 7	NR	DXA/QCT CS	Age-matched control	LV, FN, trochanter, intertrochanter, WT	NR	NR	NR	Normal
Korea^Citation91	n, 185 F	35–74	0–≥16	DXA CS	Age-matched control	LV Hip	NR	↑ (−ve R)	NR	↑ ↓ by 10% in >15 y duration of DM ↓ after 55 y age ↓ at YSM
Italy^Citation81	n, 66 F (POM) nc, 70	63.2 ± 7.4	≥2	DXA CS	Age-matched control	LS FN	NR	NR	NR	↑ at FN
Egypt^Citation150	n, (40 POM/20)* nc, 40/20	52.9 ± 6.16	NR	QCT CS	Age-matched control	LS	NR	NR	NR	↑ in F
Denmark^Citation48	n, (31/22)^† DM1 n, (11/21)^† DM2	(39.6/64.5)^† DM1 (44.1/63.4)^† DM2	(15.3/27.8)^† DM1 (3/7)^† DM2	DXA CS	Sex- and menopausal status-matched control	LS PF Total body	NR	NR	NR	↓ in POM – T1DM ↑ in POM – DM2
Finland^Citation83	n, 56 (27/29)* DM1 n, 68 (34/34)* DM2 nc, 498	(61.7 ± 6.3) DM1 (64.4 ± 4.8) DM2	dx after 30 y	DXA CS	Age-matched control	PF	NR	NR/DM2 ↑ in DM1	NR	Normal in DM2 ↓ FN BMD DM1 (6.8% in women; 7.6% lower in men)
Japan^Citation44	n, 104 M nc, 108	54.0 ± 1.0	5.6 ± 0.6	CXD NR	Age-matched control	Metacarpal	NR	↔	↑ RP	↓
Turkey^Citation151	n, 161 F (POM)	POM	≥2	DXA NR	Age-matched control	LS FN	NR	NR	NR	↑
USA^Citation88	n, 80 (38/42)*	(64/61)* 39–81	At least 3	DXA/QCT NR	Z-score	LS DR Total hip FM	NR	NR	NR	↓ in F
USA^Citation46	n, 600 (34 families) n, 153 (98/55)* nc, 447 (285/162)*	54.8 ± 12.5 F 54.3 ± 13.3 M	New dx and older	DXA CS population-based family study	Age-matched control	LS Hip FN	↔	↔	NR	↑ by 3.7% FN in F
Turkey^Citation152	n, 277 (176/101)* nc, 262	30–60	6.5 ± 5.3	DXA PS/CS	Age-matched control	LS FN Trochanter WT	↔	↔	↔	↑ FN in F/M (51–60 y) ↓ LS in M ↔ at WT/tronchanter
Saudi Arabia^Citation109	n, 104 POM nc, 101	55–70	6–30	DXA PS	Age-matched control	LS FN	NR	↔	NR	↓ (more in LS than FN) ON 43.68% OP 46.8% 14% low vit D
USA^Citation153	n, 566 (243/323)* nc, 2413 (1280/1133)*	70–79 (73/74)*	11 F/10 M (<5–>20)	DXA/spine QCT CS/PS cohort	Age-matched control	LS Hip TBD	↔	↓	NR	↑ 4%–5% regardless of sex and race
Spain^Citation154	n, 92 (56/36)* nc, 92 (56/36)*	40–81 (63/65)*	1–40 (10 ± 8 y)	DXA NR	Age-matched control	Calcaneus	↔	NR	NR	↑ 8% in F
UK^Citation155	n, 32/33 DM2 n, 134/83 IGT	59–71 (66.4/64.8)*	New dx	DXA CS	Age-matched control	FN LS	↔	↔	↔	↑ in F
Iran^Citation156	n, 146 (20 PRM/ 124 POM) nc, 372 (57 PRM/ 315 POM)	40–81		DXA historical cohort study	Age- and BMI- matched control	LS PF	NR	NR	NR	↔ in PRM ↑ LS in POM
Netherlands^Citation157	n, 792 (483/309)* nc, 5863	73.8 ± 9.2	dx > 30	DXA PS	Age- and gender- matched control	LS FN	NR	NR	NR	↑ ↑ fracture risk by 1.69-fold
Japan^Citation117	n, 145 (81/64)* nc, 95 (54/41)*	(67/63)*	>2 y	DXA CS	Age-matched control	LS FN DR	↑ (−ve R)	NR	NR	↓ DR ↔ LS ↔ FN
Sweden^Citation158	n, 67 F nc, 961	75	9.8 (0.04–61)	DXA/US NR	Age- and gender- matched control	LS FN Calcaneus	NR	↔	↓ NP	↑ FN BMD 11% ↑ LS BMD 8% ↔ at calcaneus
Greece^Citation3	n, 40 D-EMPDM2 nc, 60 EMP n, 60 D-NMP	58.7 ± 5	13.9 ± 3.9	DXA NR	Age- and BMI- matched control	LV FN	↑ (+ve R)	↔	NR	↑ LV BMD in D-EMP ↔ FN
UK^Citation104	n, 35 DM1 M n, 90 DM2 M nc, 50	49.3 DM1 62.8 DM2 38.5 control	19.7 DM1 10.1 DM2	DXA CS/controlled study	Age-matched control	DR	↔	↔	↔	↔
Iran^Citation159	n, 40 MW nc, 40	POM		DXA Case-control study	Age-, BMI-, and MPL- matched control	LS FN Forearm	↑	NR	NR	↑ FN ↓ LS with ↑ HbA1c
Saudi Arabia^Citation85	n, 154 M n, 57 DM2 n, 34 IFG nc, 63	50–76	NR	DXA NR	Age-matched control	LS Hip	↔	NR	NR	Normal
Turkey^Citation120	n, 52 (37/15)* nc, 48 (34/14)*	41–64	0–20	DXA CS	Age-, sex-, and BMI- matched control	Forearm FN LS	NR	NR	NR	↑ FN
China^Citation103	n, 131 M	73.12 ± 5.54	5.28 ± 3.56	DXA NR	NR	FN LS FT	↑	↔	NR	↓ OP 31.3%/ON 29% LS OP 30%/ON 31.3% FN OP 29%/ ON 33.6% FT
Iran^Citation160	n, 146 F nc, 372	59.3/48.3^†	6.18/10.68^†	DXA CS	Age- and BMI- matched control	LS FN	NR	NR	NR	↑
Japan^Citation102	n, 151 M nc, 48	55.4 ± 1.2	5.8 ± 1.2	CXD NR	Age-matched control	Metacarpal	NR	NR	NR	↓
USA^Citation161	n, 4929 (2505/2424)* nc, 3967 (1993/1974)*	50–79	NR	DXA CS	Age-matched control	Trochanter FN Hip	↔	NR	NR	↑
Kuwait^Citation162	n, 210 F nc, 655	59	11.99 ± 8.6	DXA CS	Age-matched control	LS FN	NR	−ve R	NR	↔
Iran^Citation108	n, 242 POM nc, 221	53.6 ± 10.59	5.9 ± 3.7	DXA NR	Age- and BMI- matched control	LV FN	↔	NR	↔	↓ FN OP/ON 78.5% LS OP/ON 54.1%
Croatia^Citation163	n, 130 POM nc, 166	67 (45–80)	NR	DXA CS	Age-matched control	LS FN Radius	↔	NR	NR	↑
Japan^Citation164	n, 196 POM	69.7 ± 7.1	14.6 ± 10.7	QUS CS	Age-matched control	Calcaneus	↔	↔	↓ with NP	↑
Kuwait^Citation165	n, 122 PRM DM2 nc, 130	26–50	NR	DXA NR	Age-, gender-, and BMI-matched control	LS Total hip	NR	NR	NR	↑ LS
China^Citation166	n, 1042 POM nc, 919	62.2 ± 7.15	6.6 ± 6.09	DXA NR	Age-matched control	LS/FN WT Trochanter Total hip	NR	NR	NR	↑ LS ↔ hip
Turkey^Citation110	n, 206 POM nc, 61	44–88	10.3 ± 8.2	DXA NR	Age-matched control	LS FN Radius	↔	↑ (−ve R) with ↓ BMD	↔	↔
China^Citation167	n, 890 (432/458)§ POM nc, 689 (318/371)§	(58.5/56.1)§	NR	DXA CS	Age- and BMI- matched control	LS FN Hip	↑ (−ve R)	↔	NR	↓ in non-obese DM2

Abbreviations: BMC, body mineral content; BMD, bone mass density; BMI, body mass index; CS, cross-sectional study; CXD, computed X-ray densitometry; DM1, diabetes mellitus type 1; DM2, diabetes mellitus type 2; D-EMP, diabetic women with premature menopause; D-NMP, diabetic women with normal menopause; DXA, dual X-ray absorptiometry; DR, distal radius; dx, diagnosis; DPA, dual photon absorptiometry; EMP, prematurely menopausal women; ; FM, fat mass; FN, femoral neck; FT, femoral trochanter; (F/M)*, female/male; F, female; IFG, impared fasting glucose; IGT, impaired glucose tolerance; LS, lumbar spine; LV, lumbar vertebrae; M, male; MW, menopausal women; MPL, menopausal period length; nc, control healthy people; NGT, normal glucose tolerance; NGL, normal glucose level; NR, not reported; NP, nephropathy; OP, osteoporosis; ON, osteopenia; PRM, premenopausal women; POM, postmenopausal women; PS, prospective study; PF, proximal femoral; QCT, quantitative computed tomography; RP, retinopathy; SPA, single photon absorptiometry; TBD, total bone density; WT, weight; US, ultrasound; y, years; YSM, years since menopause; vit, vitamin; +ve R, positive relation with BMD; ¶ good glycemic control (HbA_1c, < 8.5%); μ, poor glycemic control (HbA_1c > 10%); ^†(PRM/POM), premenopausal women/postmenopausal women; §, diabetic patient with BMI ≥ 25 kg/m²/<25 kg/m²; −ve R, negative relation with BMD; ↔, no association.

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