Effect of intramuscular adipose tissue in the skeletal muscle of thigh on glucose metabolism in male patients with obesity

doi:10.3969/j.issn.1674-8115.2023.09.011

Abstract

Abstract:

Objective ·To investigate the correlation between intramuscular adipose tissue (IMAT) content and glucose metabolism in male patients with obesity. Methods ·Eighty male patients with obesity were recruited from the Endocrinology Department of Renji Hospital, Shanghai Jiao Tong University School of Medicine from December 2019 to December 2020. According to the results of oral glucose tolerance test (OGTT), they were divided into normal glucose tolerance (NGT) group and impaired glucose regulation (IGR) group. General data and laboratory test indicators of the two groups were collected and compared. mDixon-Quant technique was used to measure the IMAT content in each skeletal muscle of the thigh in the two groups, and the proton density fat fractions (PDFF) of skeletal muscle in the two groups were compared. The multivariate Logistic regression model was used to analyze the independent influencing factors of IGR occurrence. Results ·Compared with the NGT group, patients in the IGR group had a larger waist circumference (P=0.017), higher glutamic-pyruvic transaminase level, glutamic-oxaloacetic transaminase level, γ-glutamyl transferase (GGT) level, triacylglycerol (TAG) level, nonestesterified fatty acid (NEFA) level and sartorius PDFF (all P<0.05). After adjusting for confounding factors such as age, body mass index, GGT, TAG and NEFA, the results of multivariate Logistic regression analysis showed that PDFF of vastus lateralis, semitendinosus and sartorius were the risk factors for IGR (all P<0.05). Conclusion ·Higher levels of IMAT content in vastus lateralis, semitendinosus and sartorius will increase the risk of IGR in male patients with obesity.

Key words: obesity, intramuscular adipose, glucose metabolism, skeletal muscle, magnetic resonance imaging (MRI)

CLC Number:

R589.1

LU Xiaobing, YUE Jiang, HE Shengyun, DONG Ying, LU Qing, MA Jing. Effect of intramuscular adipose tissue in the skeletal muscle of thigh on glucose metabolism in male patients with obesity[J]. Journal of Shanghai Jiao Tong University (Medical Science), 2023, 43(9): 1169-1174.

Figures/Tables 3

TrendMD

References 24

1	YAMAZAKI H, TAUCHI S, MACHANN J, et al. Fat distribution patterns and future type 2 diabetes[J]. Diabetes, 2022, 71(9): 1937-1945.
2	PICHÉ M E, TCHERNOF A, DESPRÉS J P. Obesity phenotypes, diabetes, and cardiovascular diseases[J]. Circ Res, 2020, 126(11): 1477-1500.
3	NEELAND I J, ROSS R, DESPRÉS J P, et al. Visceral and ectopic fat, atherosclerosis, and cardiometabolic disease: a position statement[J]. Lancet Diabetes Endocrinol, 2019, 7(9): 715-725.
4	SACHS S, ZARINI S, KAHN D E, et al. Intermuscular adipose tissue directly modulates skeletal muscle insulin sensitivity in humans[J]. Am J Physiol Endocrinol Metab, 2019, 316(5): E866-E879.
5	YU F Y, FAN Y P, SUN H, et al. Intermuscular adipose tissue in type 2 diabetes mellitus: non-invasive quantitative imaging and clinical implications[J]. Diabetes Res Clin Pract, 2022, 187: 109881.
6	PARK S S, SEO Y K. Excess accumulation of lipid impairs insulin sensitivity in skeletal muscle[J]. Int J Mol Sci, 2020, 21(6): E1949.
7	KAHN D, MACIAS E, ZARINI S, et al. Quantifying the inflammatory secretome of human intermuscular adipose tissue[J]. Physiol Rep, 2022, 10(16): e15424.
8	WU H Z, BALLANTYNE C M. Skeletal muscle inflammation and insulin resistance in obesity[J]. J Clin Invest, 2017, 127(1): 43-54.
9	YARIBEYGI H, FARROKHI F R, BUTLER A E, et al. Insulin resistance: review of the underlying molecular mechanisms[J]. J Cell Physiol, 2019, 234(6): 8152-8161.
10	TUBBS E, CHANON S, ROBERT M, et al. Disruption of mitochondria-associated endoplasmic reticulum membrane (MAM) integrity contributes to muscle insulin resistance in mice and humans[J]. Diabetes, 2018, 67(4): 636-650.
11	GOODPASTER B H, THAETE F L, KELLEY D E. Thigh adipose tissue distribution is associated with insulin resistance in obesity and in type 2 diabetes mellitus[J]. Am J Clin Nutr, 2000, 71(4): 885-892.
12	GOODPASTER B H, KRISHNASWAMI S, RESNICK H, et al. Association between regional adipose tissue distribution and both type 2 diabetes and impaired glucose tolerance in elderly men and women[J]. Diabetes Care, 2003, 26(2): 372-379.
13	KIM J E, DUNVILLE K, LI J J, et al. Intermuscular adipose tissue content and intramyocellular lipid fatty acid saturation are associated with glucose homeostasis in middle-aged and older adults[J]. Endocrinol Metab (Seoul), 2017, 32(2): 257-264.
14	GOSS A M, GOWER B A. Insulin sensitivity is associated with thigh adipose tissue distribution in healthy postmenopausal women[J]. Metabolism, 2012, 61(12): 1817-1823.
15	MILJKOVIC-GACIC I, GORDON C L, GOODPASTER B H, et al. Adipose tissue infiltration in skeletal muscle: age patterns and association with diabetes among men of African ancestry[J]. Am J Clin Nutr, 2008, 87(6): 1590-1595.
16	THOMAS E L, FITZPATRICK J A, MALIK S J, et al. Whole body fat: content and distribution[J]. Prog Nucl Magn Reson Spectrosc, 2013, 73: 56-80.
17	NOUREDDIN M, LAM J, PETERSON M R, et al. Utility of magnetic resonance imaging versus histology for quantifying changes in liver fat in nonalcoholic fatty liver disease trials[J]. Hepatology, 2013, 58(6): 1930-1940.
18	中国营养学会肥胖防控分会, 中国营养学会临床营养分会, 中华预防医学会行为健康分会, 等. 中国居民肥胖防治专家共识[J]. 中华流行病学杂志, 2022, 43(5): 609-626.
	Chinese Nutrition Society Obesity Prevention and Control Section, Chinese Nutrition Society Clinical Nutrition Section, Chinese Preventive Medicine Association Behavioral Health Section, et al. Expert Consensus on Obesity Prevention and Treatment in China[J]. Chinese Journal of Epidemiology, 2022, 43(5): 609-626.
19	ELSAYED N A, ALEPPO G, ARODA V R, et al. 2. classification and diagnosis of diabetes: standards of care in diabetes-2023[J]. Diabetes Care, 2023, 46(Suppl 1): S19-S40.
20	GARRETT W E Jr, CALIFF J C, BASSETT F H 3rd. Histochemical correlates of hamstring injuries[J]. Am J Sports Med, 1984, 12(2): 98-103.
21	YU F Y, HE B, CHEN L, et al. Intermuscular fat content in young Chinese men with newly diagnosed type 2 diabetes: based on MR mDIXON-quant quantitative technique[J]. Front Endocrinol (Lausanne), 2021, 12: 536018.
22	GRANADOS A, GEBREMARIAM A, GIDDING S S, et al. Association of abdominal muscle composition with prediabetes and diabetes: the CARDIA study[J]. Diabetes Obes Metab, 2019, 21(2): 267-275.
23	KIEFER L S, FABIAN J, ROSPLESZCZ S, et al. Assessment of the degree of abdominal myosteatosis by magnetic resonance imaging in subjects with diabetes, prediabetes and healthy controls from the general population[J]. Eur J Radiol, 2018, 105: 261-268.
24	KIEFER L S, FABIAN J, ROSPLESZCZ S, et al. Distribution patterns of intramyocellular and extramyocellular fat by magnetic resonance imaging in subjects with diabetes, prediabetes and normoglycaemic controls[J]. Diabetes Obes Metab, 2021, 23(8): 1868-1878.

Item	NGT group (n=41)	IGR group (n=39)	P value
General data
Age/year	32.00 (28.50, 42.00)	35.00 (31.00, 41.00)	0.338
BMI/(kg·m^-2)	34.34 (30.80, 38.55)	34.56 (31.95, 37.65)	0.605
WC/cm	114.31±11.55	124.25±18.26	0.017
HC/cm	115.00 (107.00, 122.00)	117.50 (110.25, 126.25)	0.101
WHR	0.99±0.06	1.01±0.06	0.095
Laboratory test indicators
FBG/(mmol·L^-1)	5.10 (4.63, 5.43)	5.99 (5.33, 7.54)	0.000
PBG-0.5h/(mmol·L^-1)	8.61 (7.56, 9.92)	9.24 (8.32, 11.41)	0.043
PBG-1h/(mmol·L^-1)	9.18 (6.97, 9.97)	12.39 (9.87, 13.99)	0.000
PBG-2h/(mmol·L^-1)	6.41 (5.78, 7.03)	10.35 (8.88, 12.86)	0.000
PBG-3h/(mmol·L^-1)	4.18 (3.78, 4.81)	6.60 (5.71, 8.81)	0.000
FINS/(μIU·mL^-1)	15.12 (10.15, 20.69)	21.20 (12.02, 28.63)	0.064
INS-0.5h/(μIU·mL^-1)	107.18 (80.63, 162.12)	79.47 (25.74, 116.61)	0.025
INS-1h/(μIU·mL^-1)	127.05 (83.54, 171.24)	113.44 (52.24, 175.94)	0.307
INS-2h/(μIU·mL^-1)	70.69 (45.45, 117.95)	98.84 (53.35, 205.92)	0.028
INS-3h/(μIU·mL^-1)	20.75 (11.08, 28.14)	48.82 (33.61, 106.97)	0.000
FCP/(ng·mL^-1)	3.95 (3.33, 4.85)	4.67 (3.80, 5.73)	0.037
CP-0.5h/(ng·mL^-1)	11.83 (8.13, 13.76)	7.96 (6.41, 12.01)	0.015
CP-1h/(ng·mL^-1)	13.22 (10.83, 16.94)	10.77 (8.43, 16.27)	0.115
CP-2h/(ng·mL^-1)	11.43 (9.17, 14.97)	13.68 (10.87, 18.24)	0.051
CP-3h/(ng·mL^-1)	6.01 (4.43, 7.84)	10.29 (8.03, 12.70)	0.000
HbA1c/%	5.50 (5.20, 5.70)	6.45 (5.70, 7.95)	0.000
HOMA-IR	3.31 (2.14, 4.56)	6.24 (3.45, 8.17)	0.002
GPT/(U·L^-1)	40.00 (20.00, 69.00)	67.00 (38.00, 87.00)	0.013
GOT/(U·L^-1)	22.00 (16.00, 35.75)	36.00 (25.00, 54.00)	0.001
GGT/(U·L^-1)	40.50 (26.00, 55.00)	52.00 (41.00, 77.00)	0.002
BUN/(mmol·L^-1)	4.83±1.08	4.60±0.99	0.324
Cre/(μmol·L^-1)	79.97±12.98	74.28±13.37	0.060
UA/(mmol·L^-1)	487.82±122.65	479.23±104.40	0.740
TAG/(mmol·L^-1)	1.63 (1.25, 2.71)	2.36 (1.83, 3.41)	0.010
TC/(mmol·L^-1)	5.01±1.09	5.44±0.99	0.068
HDL-C/(mmol·L^-1)	1.09±0.24	1.06±0.20	0.531
LDL-C/(mmol·L^-1)	3.07±0.84	3.34±0.86	0.164
NEFA/(mmol·L^-1)	0.53 (0.47, 0.64)	0.69 (0.57, 0.78)	0.004

Item	NGT group (n=41)	IGR group (n=39)	P value
General data
Age/year	32.00 (28.50, 42.00)	35.00 (31.00, 41.00)	0.338
BMI/(kg·m^-2)	34.34 (30.80, 38.55)	34.56 (31.95, 37.65)	0.605
WC/cm	114.31±11.55	124.25±18.26	0.017
HC/cm	115.00 (107.00, 122.00)	117.50 (110.25, 126.25)	0.101
WHR	0.99±0.06	1.01±0.06	0.095
Laboratory test indicators
FBG/(mmol·L^-1)	5.10 (4.63, 5.43)	5.99 (5.33, 7.54)	0.000
PBG-0.5h/(mmol·L^-1)	8.61 (7.56, 9.92)	9.24 (8.32, 11.41)	0.043
PBG-1h/(mmol·L^-1)	9.18 (6.97, 9.97)	12.39 (9.87, 13.99)	0.000
PBG-2h/(mmol·L^-1)	6.41 (5.78, 7.03)	10.35 (8.88, 12.86)	0.000
PBG-3h/(mmol·L^-1)	4.18 (3.78, 4.81)	6.60 (5.71, 8.81)	0.000
FINS/(μIU·mL^-1)	15.12 (10.15, 20.69)	21.20 (12.02, 28.63)	0.064
INS-0.5h/(μIU·mL^-1)	107.18 (80.63, 162.12)	79.47 (25.74, 116.61)	0.025
INS-1h/(μIU·mL^-1)	127.05 (83.54, 171.24)	113.44 (52.24, 175.94)	0.307
INS-2h/(μIU·mL^-1)	70.69 (45.45, 117.95)	98.84 (53.35, 205.92)	0.028
INS-3h/(μIU·mL^-1)	20.75 (11.08, 28.14)	48.82 (33.61, 106.97)	0.000
FCP/(ng·mL^-1)	3.95 (3.33, 4.85)	4.67 (3.80, 5.73)	0.037
CP-0.5h/(ng·mL^-1)	11.83 (8.13, 13.76)	7.96 (6.41, 12.01)	0.015
CP-1h/(ng·mL^-1)	13.22 (10.83, 16.94)	10.77 (8.43, 16.27)	0.115
CP-2h/(ng·mL^-1)	11.43 (9.17, 14.97)	13.68 (10.87, 18.24)	0.051
CP-3h/(ng·mL^-1)	6.01 (4.43, 7.84)	10.29 (8.03, 12.70)	0.000
HbA1c/%	5.50 (5.20, 5.70)	6.45 (5.70, 7.95)	0.000
HOMA-IR	3.31 (2.14, 4.56)	6.24 (3.45, 8.17)	0.002
GPT/(U·L^-1)	40.00 (20.00, 69.00)	67.00 (38.00, 87.00)	0.013
GOT/(U·L^-1)	22.00 (16.00, 35.75)	36.00 (25.00, 54.00)	0.001
GGT/(U·L^-1)	40.50 (26.00, 55.00)	52.00 (41.00, 77.00)	0.002
BUN/(mmol·L^-1)	4.83±1.08	4.60±0.99	0.324
Cre/(μmol·L^-1)	79.97±12.98	74.28±13.37	0.060
UA/(mmol·L^-1)	487.82±122.65	479.23±104.40	0.740
TAG/(mmol·L^-1)	1.63 (1.25, 2.71)	2.36 (1.83, 3.41)	0.010
TC/(mmol·L^-1)	5.01±1.09	5.44±0.99	0.068
HDL-C/(mmol·L^-1)	1.09±0.24	1.06±0.20	0.531
LDL-C/(mmol·L^-1)	3.07±0.84	3.34±0.86	0.164
NEFA/(mmol·L^-1)	0.53 (0.47, 0.64)	0.69 (0.57, 0.78)	0.004

Skeletal muscle PDFF	NGT group (n=41)	IGR group (n=39)	P value
Vastus lateralis	6.49±1.87	7.36±2.48	0.080
Rectus femoris	6.08±2.00	6.44±2.02	0.431
Vastus medialis	4.85 (4.07, 5.85)	5.04 (3.97, 6.90)	0.353
Vastus internus	5.41 (4.44, 6.24)	5.30 (4.47, 6.64)	0.878
Biceps femoris	10.22±3.28	11.37±3.53	0.136
Semitendinosus	10.01 (6.98, 11.69)	10.83 (7.87, 14.90)	0.088
Semimembranosus	9.94 (7.56, 14.61)	11.07 (8.99, 12.73)	0.607
Adductor magnus	4.81 (4.18, 5.71)	5.29 (4.46, 6.50)	0.103
Gracilis	10.03 (8.48, 14.57)	12.24 (9.43, 16.20)	0.172
Sartorius	10.92 (8.94, 16.30)	15.09 (11.92, 18.82)	0.006

Skeletal muscle PDFF	NGT group (n=41)	IGR group (n=39)	P value
Vastus lateralis	6.49±1.87	7.36±2.48	0.080
Rectus femoris	6.08±2.00	6.44±2.02	0.431
Vastus medialis	4.85 (4.07, 5.85)	5.04 (3.97, 6.90)	0.353
Vastus internus	5.41 (4.44, 6.24)	5.30 (4.47, 6.64)	0.878
Biceps femoris	10.22±3.28	11.37±3.53	0.136
Semitendinosus	10.01 (6.98, 11.69)	10.83 (7.87, 14.90)	0.088
Semimembranosus	9.94 (7.56, 14.61)	11.07 (8.99, 12.73)	0.607
Adductor magnus	4.81 (4.18, 5.71)	5.29 (4.46, 6.50)	0.103
Gracilis	10.03 (8.48, 14.57)	12.24 (9.43, 16.20)	0.172
Sartorius	10.92 (8.94, 16.30)	15.09 (11.92, 18.82)	0.006

Model	Vastus lateralis		Semitendinosus		Sartorius
Model	OR (95% CI)	P value	OR (95% CI)	P value	OR (95% CI)	P value
Model 1	1.204 (0.975‒1.488)	0.085	1.128 (1.010‒1.260)	0.088	1.125 (1.021‒1.239)	0.006
Model 2	1.199 (0.959‒1.499)	0.112	1.134 (1.008‒1.277)	0.036	1.128 (1.020‒1.248)	0.019
Model 3	1.402 (1.037‒1.895)	0.028	1.253 (1.051‒1.493)	0.012	1.149 (1.016‒1.300)	0.027