Visceral obesity exacerbates perioperative muscle loss and impairs survival in colorectal cancer

Table 1 Patient baseline characteristics, mean ± SD/n (%)/median (interquartile range)

Feature	All patients (n = 389)
Gender
Male	229 (58.87)
Female	160 (41.13)
Age%
≤ 65	202 (51.93)
> 65	187 (48.07)
BMI (kg/m2)	22.80 ± 3.17
Cardiovascular disease
None	281 (72.24)
Present	108 (27.76)
Respiratory disease
None	313 (80.46)
Present	76 (19.54)
Diabetes
None	320 (82.26)
Present	69 (17.74)
VFA (cm2)	116.36 ± 62.98
Visceral obesity, VFA ≥ 100 cm2
Yes	214 (55.01)
No	175 (44.99)
VSR (%, cm2/m2)	2.64 ± 1.36
Preoperative SMI (cm2/m2)	43.92 ± 7.89
Preoperative sarcopenia
Yes	147 (37.79)
No	242 (62.21)
Postoperative SMI	44.23 ± 8.56
Change value (SMI%)	0.011 ± 0.116
SML% (ΔSMI ≥ -5%)
No	272 (69.92)
Yes	117 (30.08)
Serum total protein(g/L)	69.67 ± 7.33
Preoperative albumin(g/L)	41.24 ± 5.20
Globulin level (g/L)	28.41 ± 5.26
Hemoglobin (g/L)	120.60 ± 26.52
Platelets (× 109/L)	226.77 ± 91.14
Neutrophil count (× 109/L)	4.869 ± 2.34
Lymphocyte count (× 109/L)	1.436 ± 0.534
Tumor location
Sigmoid colon	43 (11.05)
Colon	95 (24.42)
Rectum	251 (64.52)
Differentiation degree
Low	90 (23.14)
Moderate	270 (69.41)
High	29 (7.46)
ASA classification
< III	203 (52.19)
≥ III	186 (47.81)
Vascular nerve invasion
None	238 (61.18)
Present	151 (38.82)
pTMN stage
Stage I	46 (11.83)
Stage II	188 (48.33)
Stage III	155 (39.85)
Postoperative adjuvant chemotherapy
None	208 (53.47)
Present	181 (46.53)
Surgical approach
Open	190 (48.84)
Laparoscopic	199 (51.16)
Intraoperative blood loss (mL)	109.82 ± 105.65
Operation time (minutes)	215.21 ± 75.81
Prophylactic ileostomy status
None	322 (82.78)
Present	67(17.22)
LOS (days)	15.00 (13.00-19.00)
Number of lymph nodes dissected (n)	10.43 ± 10.00
FPT (time to flatus, days)	3.00 (2.00-3.00)
Complications
None	286 (73.52)
Present	103 (26.48)
Postoperative infectious complications
No	298 (76.61)
Yes	91 (23.39)
Postoperative non-infectious complications
No	360 (92.54)
Yes	29 (7.46)

BMI: Body mass index; VFA: Visceral fat area; VSR: Visceral-to-skeletal muscle ratio; SMI: Skeletal muscle index; SML: Skeletal muscle loss; ASA: American Society of Anesthesiologist; pTMN: Pathologic tumor-node-metastasis; LOS: Length of hospital stay; FPT: Flatus passage time.

Table 2 The relationship between skeletal muscle loss, visceral fat area, and clinical characteristics, mean ± SD/n (%)/median (interquartile range)

Feature	SML			VFA
	No (n = 272)	Yes (n = 117)	P value	Low (n = 175)	High (n = 214)	P value
Gender			0.801			0.062
Male	159 (58.46)	70 (59.83)		94 (53.71)	135 (63.08)
Female	113 (41.54)	47 (40.17)		81 (46.29)	79 (36.92)
Age			0.542			0.023
≤ 65	144 (52.94)	58 (49.57)		102 (58.29)	100 (46.73)
> 65	128 (47.06)	59 (50.43)		73 (41.71)	114 (53.27)
BMI (kg/m2)	22.74 ± 3.11	22.92 ± 3.30	0.623	21.34 ± 2.90	24.00 ± 2.87	0.000
Cardiovascular disease			0.905			0.001
None	196 (72.06)	85 (72.65)		141 (80.57)	140 (65.42)
Yes	76 (27.94)	32 (27.35)		34 (19.43)	74 (34.58)
Respiratory disease			0.811			0.835
None	218 (80.15)	95 (81.20)		140 (80.00)	173 (80.84)
Yes	54 (19.85)	22 (18.80)		35 (20.00)	41 (19.16)
Diabetes			0.943			0.000
None	224 (82.35)	96 (82.05)		158 (90.29)	162 (75.70)
Yes	48 (17.65)	21 (17.95)		17 (9.71)	52 (24.30)
VFA (cm2)	99.45 (66.08-143.54)	134.0 (81.30-174.40)	0.001	66.27 (44.26-85.52)	148.965 (126.16-181.58)	0.000
Preoperative SMI (cm2/m2)	42.79 (37.7-47.2)	45.09 (40.7-51.3)	0.004	40.56 (36.11-45.60)	45.035 (41.47-50.27)	0.000
Preoperative Sarcopenia			0.026			0.006
Yes	179 (65.81)	63 (53.85)		122 (69.71)	120 (56.08)
No	93 (34.19)	54 (46.15)		53 (30.29)	94 (43.93)
Postoperative SMI (cm2/m2)	45.41 (40.4-50.1)	39.92 (35.0-45.4)	0.000	42.45 (37.21-47.66)	45.20 (40.06-49.65)	0.001
ΔSMI (%)	0.04 (0.00-0.11)	-0.10 (-0.15 to -0.08)	0.000	0.03 (-0.04 to 0.10)	-0.01 (-0.09 to 0.06)	0.001
VSR (%, cm2/m2)	2.524 ± 1.295	2.898 ± 1.465	0.012	1.53 (1.02-1.95)	3.25 (2.77-4.04)	0.000
Preoperative albumin (g/L)	41.60 (37.4-44.7)	42.70 (38.7-45.7)	0.047	42.30 (37.70-45.10)	41.50 (37.38-44.83)	0.308
Serum total protein (g/L)	69.38 ± 7.62	70.34 ± 6.58	0.236	70.40 (65.40-75.40)	69.95 (64.325-74.70)	0.476
Globulin level (g/L)	28.250 (24.8-31.5)	28.30 (25.6-31.2)	0.798	28.40 (24.80-31.00)	28.20 (25.08-31.70)	0.875
Hemoglobin (g/L)	126.50 (105.0-140.0)	130.00 (105.0-142.0)	0.565	126.00 (105.00-140.00)	128.50 (104.75-140.00)	0.962
Platelet (× 109/L)	216.50 (167.3-278.8)	204.00 (151.5-251.5)	0.065	215.00 (168.00-277.00)	210.00 (159.25-262.25)	0.59
Neutrophil count (× 109/L)	4.43 (3.3-5.9)	4.20 (3.2-5.6)	0.234	4.40 (3.370-5.40)	4.35 (3.192-5.92)	0.687
Lymphocyte count (× 109/L)	1.380 (1.0-1.8)	1.40 (1.0-1.8)	0.686	1.34 (1.00-1.75)	1.42 (1.07-1.79)	0.161
Tumor site			0.923			0.818
Sigmoid colon	30 (11.03)	13 (11.11)		18 (10.29)	25 (11.68)
Rectum	67 (24.63)	28 (23.93)		45 (25.71)	50 (23.36)
Colon	175 (64.34)	76 (64.96)		112 (64.00)	139 (64.95)
Differentiation degree			0.24			0.84
Low	59 (21.69)	31 (26.50)		39 (22.29)	51 (23.83)
Medium	191 (70.22)	79 (67.52)		124 (70.86)	146 (68.22)
High	22 (8.09)	7 (5.98)		12 (6.86)	17 (7.94)
Vascular nerve invasion			0.206			0.091
None	172 (63.24)	66 (56.41)		99 (56.57)	139 (64.95)
Yes	100 (36.76)	51 (43.59)		76 (43.43)	75 (35.05)
Pathological grade (pTNM)			0.096			0.063
Stage I	33 (12.13)	13 (11.11)		19 (10.86)	27 (12.62)
Stage II	139 (51.10)	49 (41.88)		96 (54.86)	92 (42.99)
Stage III	100 (36.76)	55 (47.01)		60 (34.29)	95 (44.39)
Postoperative adjuvant chemotherapy			0.589			0.003
None	100 (36.76)	55 (47.01)		79 (45.14)	129 (60.28)
Yes	129 (47.43)	52 (44.44)		96 (54.86)	85 (39.72)
Surgical approach			0.36			0.260
Open	137 (50.37)	53 (45.30)		91 (52.00)	99 (46.26)
Laparoscopic	135 (49.63)	64 (54.70)		84 (48.00)	115 (53.74)
Prophylactic ileostomy status			0.047			0.598
None	231 (85.24)	90 (76.92)		142 (81.61)	179 (83.65)
Yes	40 (14.76)	27 (23.08)		32 (18.39)	35 (16.36)
Intraoperative blood loss (mL)	100.00 (50.00-100.00)	100.00 (50.00-100.00)	0.569			0.947
Operation time (minutes)	200.00 (165.00-240.00)	205.00 (165.00-257.50)	0.735	91 (52.00)	112 (52.34)
ASA classification			0.815	84 (48.00)	102 (47.66)
< III	143 (52.57)	60 (51.28)		80.0 (50.0-100.0)	100.0 (50.0-150.00)	0.001
≥ III	129 (47.43)	57 (48.72)		200 (165.0-245.0)	204. (165.00-245.25)	0.452
LOS (days)	15.00 (13.00-19.00)	15.00 (13.00-20.00)	0.356	14.0 (13.0-18.0)	16.0 (13.0-20.0)	0.001
Number of lymph nodes dissected (n)	10.00 (5.00-14.00)	10.00 (6.00-13.00)	0.677	10.00 (6.0-14.0)	10.00 (5.0-14.0)	0.495
FPT (days)	3.00 (2.00-3.00)	3.00 (2.00-3.00)	0.782	3.00 (2.00-4.00)	3.00 (2.00-3.00)	0.199
Complications			0.613			0.757
None	202 (74.26)	84 (71.79)		130 (74.29)	156 (72.90)
Yes	70 (25.74)	33 (28.21)		45 (25.71)	58 (27.10)
Postoperative infectious complications			0.721			0.427
No	207 (76.10)	91 (77.78)		164 (93.71)	196 (91.59)
Yes	65 (23.90)	26 (22.22)		11 (6.29)	18 (8.41)
Postoperative non-infectious complications			0.338			0.798
No	254 (93.38)	106 (90.60)		133 (76.00)	165 (77.10)
Yes	18 (6.62)	11 (9.40)		42 (24.00)	49 (22.90)

This table illustrates the association between skeletal muscle loss and visceral fat area groupings and the preoperative clinical indicators as well as short-term outcomes in patients with colorectal cancer. BMI: Body mass index; VFA: Visceral fat area; VSR: Visceral-to-skeletal muscle ratio; SMI: Skeletal muscle index; SML: Skeletal muscle loss; ASA: American Society of Anesthesiologist; pTMN: Pathologic tumor-node-metastasis; LOS: Length of hospital stay; FPT: Flatus passage time.

Table 3 Factors associated with skeletal muscle loss

	SML
	Single factor OR (95%CI)	P value	Multivariate OR (95%CI)	P value
Age
≤ 65	Reference
> 65	1.144 (0.742-1.766)	0.542
Gender
Female	Reference
Male	0.945 (0.608-1.469)	0.801
BMI	1.017 (0.95-1.089)	0.622	0.846 (0.757-0.946)	0.003
VFA
Low VFA	Reference
High VFA	2.110 (1.34-3.322)	0.001	2.557 (1.518-4.305)	0.000
Preoperative SMI	1.035 (1.007-1.064)	0.016	1.082(1.035-1.131)	0.000
Prophylactic ileostomy condition
No	Reference
Yes	1.733 (1.004-2.99)	0.048	1.936 (1.086-3.449)	0.025

BMI: Body mass index; VFA: Visceral fat area; SMI: Skeletal muscle index; SML: Skeletal muscle loss; OR: Odds ratio; CI: Confidence interval.