Association between sarcopenic obesity and higher risk of type 2 diabetes in adults: A systematic review and meta-analysis

Table 1 Studies included in the systematic review

Study	Design	Definition of SO	Body composition	Gender	Sample	Mean age	Mean BMI	Prevalence Sarcopenic Obesity	Prevalence of Diabetes
Sénéchal et al[35], 2012	Cross sectional	Dynapenic obesity, defined as low leg muscle strength, combined with abdominal obesity	Kin- Com dynamometer	M-F	T = 1963	Non DO: 65.5 ± 9.6; DO: 65.4 ± 9.9	Non DO: 30.8 ± 4.5; DO: 29.9 ± 4.6	DO: n = 566/1963 (Did not distinguish in gender)	T2D: Non DO: n = 196; DO: n = 130
Lu et al[18], 2013	Cross sectional	Defined by combination of total skeletal muscle mass/wt. (100) and BMI ≥ 25 kg/m2	BIA	M-F	T = 180; M = 60; F = 120	Non SO: 69.9 ± 7.3; SO: 61.1 ± 9.9	Non SO: 26.8 ± 1.6; SO: 27.8 ± 2.6	n = 35/60 in males; n = 80/120 in females	T2D: Non SO: n = 12/65; SO: n = 17/115
Poggiogalle et al[36], 2015	Cross sectional	Defined by ASMM/h2 or ASMM/wt. < 2SD of sex specific mean combined with assessment of FM and FFM	DXA	M-F	T = 727; M = 141; F = 586	46.49 ± 13.73; 46.99 ± 13.76	38.85 ± 5.88; 38.84 ± 5.79	SO: n = 68/141 in males; n = 350/586 in females	Pre-diabetes or T2D: Non-SO: n = 69; SO: n = 155
Ma et al[37], 2016	Retrospective; Cross sectional	SO: BMI > 30 kg/m2 and 24 h- UC < median	Sex-specific 24-h urinary creatinine excretion	M-F	T = 310; M = 144; F = 166	71.8 ± 7.6	34.1 ± 4.0	SO: n = 44/144 in males; n = 52/166 in females	T2D: Non SO: n = 51; SO: n = 40
Xiao et al[38], 2017	Retrospective	FMI/FFMI ratio > 95 percentile of sex, BMI and ethnicity specific population-representative references	BIA	M-F	T = 144; M = 45; F = 99	Non SO: 56.6 ± 12.7; SO: 54.6 ± 10.1	Non SO: 44.0 ± 7.6; SO: 49.1 ± 8.3	SO: 73/144 in total; (Did not distinguish in gender)	T2D: Non SO: n = 36/71; SO: n = 34/71
Kang et al[39], 2017	Cross sectional	ASM/Wt < 1 SD the mean of the reference group, and BMI ≥ 25 kg/m2	DXA	F	T = 1555	Non SO: 61.05 ± 0.44; SO: 62.91 ± 0.44	Non SO: 26.80 ± 0.07; SO: 27.93 ± 0.11	SO: n = 855/1555 (All females)	T2D: Non SO: n = 105/700; SO: n = 165/855
Aubertin-Leheudre et al[40], 2017	Cross sectional	Dynapenic obesity, defined as low handgrip strength (≤ 19.9 in females; ≤ 31.9 in males), combined with BMI ≥ 30 kg/m2	Jamar Handheld Dynamometer	M-F	T = 670; M = 213; F = 457	Non SO: 76.3 ± 4.7; SO: 78.0 ± 4.6	Non SO: 35.6 ± 4.8; SO: 34.9 ± 4.8	SO: n = 77/213 in males; n = 179/457 in females	T2D: Non SO: n = 133/414; SO: n = 81/256
Park et al[41], 2018	Cross sectional	SO defined by combination of SMI < 2 SD and WC ≥ 90 cm for men and ≥ 85 cm women	BIA	M-F	T = 53818; M = 38820; F = 14998	Non SO: 40.5 ± 9.2; SO: 40.0 ± 11.3	Non SO: 26.9 ± 2.2; SO: 30.7 ± 3.4	n = 6513; M = 3341; F = 3172	T2D; Non-SO: n = 2176; SO: n = 391
Kreidieh et al[42], 2018	Cross sectional	ALM/BMI < 0.512	BIA	F	T = 154	33.26 ± 14.65	31.42 ± 4.94	n = 31	T2D: Non SO: n = 3/123; SO: n = 4/31
Khazem et al[43], 2018	Cross sectional	ALM/BMI < 0.789, (ALM/Wt.) × 100% < 25.72, and (ALM/Wt.) × 100% < 29.60	BIA	M	T = 72	32.79 ± 13.65	33.69 ± 5.85	23.9%-69.4%	T2D: Non SO: n = 1/22; SO: n = 3/50
Scott et al[46], 2018	Cross sectional (includes a longitudinal part)	ALM/height < 7.26 kg/m2 combined with handgrip strength < 30 kg and/or low gait speed ≤ 0.8 m/s. Obesity was defined as body fat percentage ≥ 30%	DXA Handgrip strength Gait speed	M	T = 525	Non SO: 75.9 ± 4.7; SO: 80.3 ± 6.5	Non SO: 30.7 ± 3.4; SO: 27.2 ± 2.3	n = 80	High fasting glucose or diabetes medications: Non SO: n = 177/445; SO: n = 29/80

SO: Sarcopenic obesity; DO: Dynapenic obesity; BMI: Body mass index; M: Male; F: Female; BIA: Bioelectric impedance analysis; T2D: Type 2 diabetes; DXA: Dual-energy X-ray absorptiometry.

Table 2 Quality assessment of the included studies

Author	Sénéchal et al[35], 2012	Lu et al[18], 2013	Poggiogalle et al[36], 2016	Ma et al[37], 2016	Xiao et al[38], 2017	Kang et al[39], 2017	Aubertin- Leheudre et al[40], 2017	Park et al[41], 2018	Scott et al[46], 2018	Kreidieh et al[42], 2018	Khazem et al[43], 2018
Selection
Represents cases with independent validation	1	1	1	1	1	1	1	1	1	1	1
Cases are consecutive or obviously representative	1	1	1	1	1	1	1	1	1	1	1
Controls from the community	1	1	1	1	1	1	1	1	1	1	1
Controls have no history of sarcopenic obesity	1	1	1	1	1	1	1	1	1	1	1
Comparability
Controls are comparable for the most important factors	1	1	1	1	1	1	1	1	1	1	1
Control for any additional factor	0	0	1	0	0	1	0	1	0	0	0
Ascertainment of exposure
Secured record or structured interview where blind to/control status	1	1	1	1	0	1	1	1	1	1	1
Same method of ascertainment for cases and controls	1	1	1	1	1	1	1	1	1	1	1
Cases and controls have completed follow up	0	0	0	1	0	0	0	0	1	0	0
Total score	7	7	8	8	6	8	7	8	8	7	7

Newcastle-Ottawa Scale (NOS) for longitudinal and cross-sectional studies. Yes = 1, No (not reported, not available) = 0; Studies with scores of 0-3, 4-6, 7-9 were considered as low, moderate and high quality, respectively.