Sarcopenia adversely impacts clinical outcomes in patients undergoing pancreaticoduodenectomy: A systematic review and meta-analysis

Table 1 General characteristics of the included studies

Ref.	Region	Diagnosed period	Sarcopenia/no sarcopenia			Prevalence of sarcopenia	Study design
			Sample size	Sex ratio	Median age
Nishida et al[10], 2016	Japan	January 2010 to December 2014	132/134	70/111	68.79/66.17	49.62%	Cohort study
Sandini et al[11], 2016	Italy	2007 to February 2015	30/94	10/53	-/-	24.19%	Cohort study
Takagi et al[12], 2017	Japan	January 2007 to May 2013	55/164	36/107	-/-	25.11%	Cohort study
Stretch et al[13], 2018	Canada	2003 to 2011	50/73	29/42	68.50/66.10	40.65%	Cohort study
Tankel et al[14], 2018	Israel	December 2014 to February 2017	16/45	8/24	75.0/64.0	26.23%	Cohort study
Umetsu et al[6], 2018	Japan	February 2008 to March 2015	48/17	12/35	71.02/61.77	73.85%	Cohort study
Centonze et al[15], 2020	Italy	2010 to 2017	36/74	20/42	70.93/64.94	32.73%	Cohort study
Xu et al[16], 2020	China	January 2016 to December 2018	59/93	-/-	-/-	38.82%	Cohort study
Peng et al[17], 2021	China	October 2005 to August 2018	20/96	12/56	72.1/65.0	17.24%	Cohort study
Pessia et al[18], 2021	Italy	June 2013 to May 2019	32/36	-/-	-/-	47.06%	Cohort study
Duan et al[19], 2021	China	January 2014 to December 2019	108/157	52/84	62.70/55.30	40.75%	Cohort study
Nauheim et al[20], 2022	United States	October 2017 to January 2020	83/250	40/121	70.6/65.4	24.92%	Cohort study
Aoki et al[21], 2022	Japan	January 2016 to March 2020	19/161	15/87	77.9/71.0	10.56%	Cohort study
Umezawa et al[7], 2022	Japan	January 2006 to April 2020	44/44	35/30	73/70.5	50.00%	Cohort study
La Vaccara et al[5], 2023	Italy	February 2004 to January 2016	54/28	37/13	-/-	65.85%	Cohort study
Cai et al[22], 2023	China	January 2018 to January 2021	47/82	28/50	65.4/60.7	36.43%	Cohort study

Table 2 Clinical and surgical characteristics of the included studies

Ref.	Surgical procedure	Sarcopenia/no sarcopenia			Measurements of sarcopenia	Sarcopenia definition
		Original cancer type	BMI	Outcomes
Nishida et al[10], 2016	PD	Pancreatic tumor = 80/83; bile duct tumor = 42/40; other malignant disease = 9/10; benign disease = 1/1	21.15 ± 3.45/22.89 ± 3.67	Complications (C-D ≥ III), wound infection, pancreatic fistula, death	L3 SMI	Males < 43 cm2/m2 with BMI < 25 kg/m2, < 53 cm2/m2 with BMI ≥ 25 kg/m2; females < 41 cm2/m2
Sandini et al[11], 2016	Whipple or pylorus-preserving PD	-	-	Wound infection, urinary tract infection, pneumonia, pancreatic fistula, biliary fistula	CT TAMA	Males < 43 cm2/m2 with BMI < 25 kg/m2, < 53 cm2/m2 with BMI ≥ 25 kg/m2; females < 41 cm2/m2
Takagi et al[12], 2017	PD	Pancreatic adenocarcinoma = 25/61; bile duct carcinoma = 7/20; periampullar adenocarcinoma = 10/18; duodenal adenocarcinoma = 1/9; intraductal papillary mucinous neoplasm = 6/26; others = 6/30	21.70 ± 3.00/22.00 ± 3.40	Overall complications, wound infection, bacteremia, urinary tract infection, pneumonia, pancreatic fistula, total length of hospital stay, death	CT L3 SBI	Male < 68.5 cm2/m2; female < 52.5 cm2/m2
Stretch et al[13], 2018	Whipple	Pancreatic tumor = 37/47; non-pancreatic tumor = 13/26	23.5 ± 3.6/26.3 ± 6.5	Complications (C-D ≥ III), total length of hospital stay	CT L3 SMI	Male < 47.7 cm2/m2; female < 36.5 cm2/m2
Tankel et al[14], 2018	Pylorus-preserving PD	-	21.9 ± 2.0/25.0 ± 3.2	Complications (C-D ≥ III), pancreatic fistula, total length of hospital stay	CT L3 TPAI	Male < 83.41 cm2/m2; female < 65.28 cm2/m2
Umetsu et al[6], 2018	Whipple	Distal cholangiocarcinoma = 48/17	21.70 ± 2.63/24.34 ± 2.84	Complications (C-D ≥ III), pancreatic fistula, death	CT L3 PMI	Male < 5.93 cm2/m2; female < 3.54 cm2/m2
Centonze et al[15], 2020	Whipple	Pancreatic carcinoma or pancreatitis = 21/44; other = 15/30	25.36 ± 3.86/24.35 ± 2.27	Wound infection, bacteremia, urinary tract infection, pancreatic fistula, biliary fistula	CT L3 HUAC	Male < 16.37 HU; female < 14.21 HU
Xu et al[16], 2020	PD	-	-	Overall complications, total length of hospital stay, death	CT L3 TPAI	Male < 4.78 cm2/m2; female < 3.46 cm2/m2
Peng et al[17], 2021	PD	Pancreatic cancer = 20/96	21.2 ± 2.2/22.9 ± 2.80	Complications (C-D ≥ III), total length of hospital stay	CT L3 SMI	Male < 42.2 cm2/m2; female < 33.9 cm2/m2
Pessia et al[18], 2021	PD	Pancreatic head adenocarcinoma = 32/36	19.60/21.40	Complications (C-D ≥ III)	CT L3 SMI	Male < 52.4 cm2/m2; female < 38.5 cm2/m2
Duan et al[19], 2021	Pylorus-preserving PD	Pancreatic ductal adenocarcinoma = 48/77; pancreatic cystic tumor = 14/20; pancreatic neuroendocrine tumors = 6/9; periampullar tumor = 35/43; trauma = 1/3; others = 4/5	22.50 ± 4.1/23.20 ± 3.9	Overall complications, pneumonia, pancreatic fistula, biliary fistula, total length of hospital stay, death	CT L3 SMI	Male < 47.32 cm2/m2; female < 40.65 cm2/m2
Nauheim et al[20], 2022	PD	Pancreatic ductal adenocarcinoma = 50/141; periampullar/duodenal carcinoma = 10/24; cholangiocarcinoma = 3/8; other = 6/10; benign/premalignant = 14/67	25.9 ± 4.4/27.9 ± 5.5	Overall complications, complications (C-D ≥ III), wound infection, urinary tract infection; pneumonia, pancreatic fistula, death	CT L3 PMI	Lowest quartile
Aoki et al[21], 2022	PD	Pancreatic carcinoma = 14/69; bile duct carcinoma = 2/21; intraductal papillary mucinous neoplasm = 2/40; periampullar carcinoma = 1/13; others = 0/18	20.14 ± 1.36/22.11 ± 3.52	Complications (C-D ≥ III), wound infection, bacteremia, pneumonia, pancreatic fistula	EWGSOP2	Male: SMI < 7 kg/m2; grip strength < 27 kg; gait speed < 0.8 m/s; female: SMI < 6 kg/m2; grip strength < 16 kg; gait speed < 0.8 m/s
Umezawa et al[7], 2022	PD	Distal cholangiocarcinoma = 44/44	21.47 ± 3.45/22.37 ± 3.07	Complications (C-D ≥ III)	CT L3 PMI	Male < 6.36 cm2/m2; female < 3.98 cm2/m2
La Vaccara et al[5], 2023	PD	Periampullary cancers = 54/28	-	Urinary tract infection, pneumonia, pancreatic fistula, biliary fistula	CT L3 SMI	Male < 55.4 m2/m2; female < 38.9 cm2/m2
Cai et al[22], 2023	PD	Periampullar neoplasms = 47/82	21.50 ± 2.50/24.20 ± 3.30	Pancreatic fistula, biliary fistula	CT L3 SMI	Male < 44.2 cm2/m2; female < 33.9 cm2/m2

SMI: Skeletal muscle index; TAMA: Total abdominal muscle area; SBI: SMA/BSA index; TPA: Total psoas muscle area index; PMI: Psoas muscle mass index; PD: Pancreaticoduodenectomy; BMI: Body mass index; C-D: Clavien-Dindo.

Table 3 Study quality evaluation

Ref.	Selection of study population	Comparability between the two groups	Outcome indicators	Total quality assessment score
Nishida et al[10]	4	2	1	7
Sandini et al[11]	4	2	1	7
Takagi et al[12]	4	2	2	8
Stretch et al[13]	4	2	3	9
Tankel et al[14]	4	2	1	7
Umetsu et al[6]	4	2	2	8
Centonze et al[15]	4	2	2	8
Xu et al[16]	4	2	1	7
Peng et al[17]	3	2	1	6
Pessia et al[18]	4	2	2	8
Duan et al[19]	4	2	2	8
Nauheim et al[20]	4	2	2	8
Aoki et al[21]	4	2	3	9
Umezawa et al[7]	4	2	1	7
La Vaccara et al[5]	4	2	2	8
Cai et al[22]	4	2	3	9