Significance of multivisceral resections in oncologic surgery: A systematic review of the literature

Table 1 Patient demographics

Study/Yr	n	Disease	Site
Cukier et al[24], 2012	33	Primary	Colon
Hallet et al[20], 2014	15	Recurrent	Colon
Kumamoto et al[15], 2017	118	Primary	Colon
Leijssen et al[2], 2018	103	Primary	Colon
López-Cano et al[49], 2010	113	Primary	Colon
Rosander et al[7], 2018	121	Primary	Colon
Takahashi et al[12], 2017	84	Primary	Colon
Tei et al[23], 2018	29	Primary	Colon
Chen et al[6], 2011	287; Colon (152); Rectum (135)	Primary recurrent	Colorectal
Eveno et al[58], 2014	152; Colon (81); Rectum (71)	Primary	Colorectal
Fujisawa et al[29], 2002	35; Colon (19); Rectum (17)	Primary recurrent	Colorectal
Hoffmann et al[21], 2012	78; Colon (52); Rectum (26)	Primary	Colorectal
Gezen et al[18], 2012	90; Colon (43); Rectum (47)	Primary	Colorectal
Kim et al[17], 2012	54; Colon (32); Rectum (22)	Primary	Colorectal
Laurence et al[56], 2017	660; Colon/Rectum not specified	Primary	Colorectal
Lehnert et al[8], 2002	201; Colon (139); Rectum (62)	Primary	Colorectal
Li et al[16], 2011	72; Colon (28); Rectum (44)	Primary	Colorectal
Park et al[53], 2011	54; Colon (23); Rectum (31)	Primary	Colorectal
Rizzuto et al[57], 2016	22; Colon (16); Rectum (6)	Primary	Colorectal
Winter et al[1], 2007	63; Colon (46); Rectum (17)	Primary	Colorectal
Bannura et al[55], 2006	30	Primary	Rectal
Crawshaw et al[25], 2015	61	Primary recurrent	Rectal
Derici et al[48], 2008	57	Primary	Rectal
Dinaux et al[50], 2018	29	Primary	Rectal
Dosokey et al[30], 2017	34	Primary	Rectal
Gannon et al[28], 2007	72	Primary recurrent	Rectal
Harris et al[19], 2011	42	Primary	Rectal
Ishiguro et al[54], 2009	93	Primary	Rectal
Mañas et al[13], 2014	30	Primary	Rectal
Nielsen et al[9], 2012	90	Primary recurrent	Rectal
Pellino et al[14], 2018	82	Primary	Rectal
Rottoli et al[10], 2017	46	Primary recurrent	Rectal
Sanfilippo et al[51], 2001	32	Primary	Rectal
Shin et al[22], 2016	22	Primary	Rectal
Smith et al[47], 2012	124	Primary	Rectal
Vermaas et al[11], 2007	35	Primary recurrent	Rectal

Table 2 Patient- and treatment- associated parameters after multivisceral resection for colon and rectal cancers

Study	Resection margin (R0 vs R1)	Local and distant recurrence	Most common resected organs	Lymph node involvement	Age	Blood loss(mL)	Pre-operative (Chemo)-radiation	Complications (AI;SSI;IAA) (Re-OP)	Prognostic factors/con-clusions
Cukier et al[24]	R0: 100%	LR: 6%; DR: 18%	Small bowel (56%); Bladder/ Ureter (54%)	N0: 79% N1: 21%	64	NR	RCTX:100%	6%; 18%; NR (9%)	No statistical difference in terms of disease-free survival when analyzing subgroups stratified by nodal-status ypN0 vs ypN1: (P = 0.29)
Hallet et al[20]	R0: 87%	LR: 13%; DR: 13%	Colon (87%) Small bowel (47%) Bladder (40%)	N0: 70% N1: 30%	60.2	1500	RCTX:100%	NR	Neoadjuvant RCTX for recurrent colon cancer is feasible; no addition of toxicity (radiation plus MVR)
Kumamoto et al[15]	R0: 95%	LR: R0: 1.8% R1: 66.7%; DR: NR	Small bowel (14%) Bladder (12%) Colorectum (11%)	N0: 62% N1: 28% N2: 10%	64	48	CTX: 4.4%	(0.8%; 2.5%; 0.8%) (0%)	R1-resection and N+ status predictors of poor prognosis Laparoscopic approach: Feasible, low conversion, low R1-rate
Leijssen et al[2]	R0: 89%	LR: 14.5%; DR: 10.9%	Small intestine (31%); Reproductive organs (9%); Bladder (7%)	NR	69	NR	NR	(1.8%; 3.6%; NR) (2%)	Patients with T4-cancer not undergoing MVR had a significantly poorer outcome regarding overall-, disease-free and cancer-specific survival
López-Cano et al[49]	R0: 85%	LR: 23%; DR: 19%	Small intestine (42%) Oophorectomy (28%) Bladder (19%)	N0: 35% N1: 32% N2: 34%	71	NR	0%	(NR; 10%; NR) (8%)	Poorly differentiated tumors and stage IV were associated with a poor survival; significant predictors of disease progression: Venous invasion (RR 2.34) and four or more positive lymph nodes (RR 3.99)
Rosander et al[7]	R0: 93%	LR: R0: 7% R1: 33% DR: 14%	Bowel (45%) Ovaries (24%) Bladder (partial/total): 22%/19% Uterus/Vagina (17%)	N0: 71% N1: 19% N2: 10%	67	NR	CTX: 27% RT: 1% RCTX: 5%	(8%; 7%; 7%) (14%)	Female sex, low tumor stage, and adjuvant CTX, and N - but not tumor infiltration per se, were independently associated with better overall survival
Takahashi et al[12]	R0: 96%	LR: 2%	Bowel (38%); Uterus/Ovaries (5%); Bladder (11%)	NR	68.5- 71.5	Lap. completion: 50; Conversion: 366; Lap overall: 57.5; open: 321	CTX: open: 25% lap: 6%	(4%; NR; NR) (NR)	Overall- and disease-free survival (multivariate) was shorter in the males; operative approach did not affect overall- and disease-free survival
Tei et al[23]	R0: 93%-100%	LR: NR; DR: 24%	Small intestine (38%); Bladder (17%); Ovaries (14%)	N0: 48% N1: 24% N2: 28%	70	60-220	NR	(3%; 17%; 10%) (3%)	S-MVR and M-MVR do not differ significantly in terms of blood loss, operative time and number of harvested lymph nodes. No difference in occurrence of complications
Chen et al[6]	NR	NR	Colon cancer: small bowel (40%); Rectal cancer: Bladder (36%)	NR	NR	NR	NR	NR	Multivariate analysis showed that adhesion pattern was independently associated with overall survival among both colon (P = 0.00001) and rectal (P = 0.0002) cancer patients
Eveno et al[58]	R0: 90%	NR	Vagina (25%); Small bowel (23%); Bladder (20%); Ovaries/Uter-us (each 19%)	N0: 55% N1: 25% N2: 19%	63	NR	RT: 8%; CT: 2%; RCTX: 27%	(3%, 4%; NR) (9%)	Patients with resection of multiple organs had a better survival rate than patients with single organ resection (P = 0.0469)
Fujisawa et al[29]	NR	NR	Bladder (partial/total): 54%/34%	NR	59	NR	0%	NR	Complication rate was higher in pat; undergoing cystectomy vs partial cystectomy (58.3% vs 10.5%)
Hoffmann et al[21]	R0: 95%	LR: 2%	53%: 1 add. Organ 27%: 2 add; organs	NR	69	NR	RCTX (rectal): 35%	(9%; 9%; NR) (19%)	No significant differences in overall survial: Colon vs rectal cancer (P = 0839); lap vs open (P = 0.610); emergency vs planned (P = 0.674), pN0 vs pN1 (P = 0.658)
Gezen et al[18]	R0: 91%	NR	Ovaries: 27%; Bladder: 26%; Small bowel: 21%; Uterus: 19%	NR	59	450 (non-MVR: 250)	NR	(2%; 3%; 1%) (2%)	MVR do not alter the rates of sphincter-saving procedures, morbidity and 30-d mortality
Kim et al[17]	R0: 71%	LR: 7.7% (lap) and 27.3% (open) P = 0.144) DR: 15.4% (lap) vs 45.5% (open) P = 0.091)	Small bowel: 10%; Bladder: 10%; Seminal vesicle: 13%; Prostate: 6%	NR	68	lap: 269; open: 638	RCTX: 50% of rectal cancer patients	(12%; 8%; NR) (NR)	No adverse long-term oncologic outcomes of laparoscopic MVR were observed
Laurence et al[56]	NR	NR	NR	NR	64	NR	RT: 62%	NR	Female gender, tumor grade 2, MVR were significant protective factors of mortality
Lehnert et al[8]	R0: 65% R1: 9% R2: 26%	LR: 7% DR: 13% Both: 4%	Small bowel: 29%; Bladder: 24%; Uterus: 13%	NR	64	< 1000 mL: 37%; 1000-2000 mL: 13%; > 2000 mL: 10%	RT/CT/RCTX: 40% of R0 resected patients	(5%; 9%; 1%)	Intraoperative blood loss, age older than 64 and UICC stage but not histologic tumor infiltration vs inflammation were prognostic factors
Li et al[16]	NR	LR at 5 years: 15% DR: 14%	Bladder (partial/total): 56%/19%	NR	67	Partial cystectomy: 0; Urologic reconstruction: 1700	0%	(19%; 25; 6%) (4%)	Negative prognostic factors: Age older than 70 years; receiving palliative resection and not involvement of the bladder dome
Park et al[53]	NR	NR	Small bowel: 24%; Ovary: 17%; Bladder 14%	NR	64	NR	NR	(6%; 11%; 9%) (NR)	MVR was associated with a two times higher complications rate compared to standard resections
Rizzuto et al[57]	R0: 91%	NR	Small bowel: 36%; Bladder: 27%; Vagina/Uterus/Ovaries: Each 22%	N0: 50% N+: 50%	62	NR	RCTX: 28%	(11%; 14%; 5%) (NR)	Patients with rectal cancer and occlusive disease had worse prognosis
Winter et al[1]	R0: 89%	LR: 14%	Bladder (partial): 84%	N0: 65% N1: 35%	63	NR	RCTX: 37%	(3%; NR; NR) (NR)	Bladder reconstruction is achievable in most patients; margin- and node-negative patients benefit the most
Banamura et al[56]	NR	LR: 13%; DR. 23%: Both: 20%	APR: 30%; PPE: 70%	NR	57	NR	RCTX: 20%	(3%; 27%; NR) (NR)	PPE showed prolonged operative time, higher postoperative complications, a trend towards a poor prognosis in recurrence and survival
Crawshaw et al[25]	R0: 87%	LR: 16%	Bladder: 49%; Vagina: 38%; Prostate: 31%; Uterus: 31%; Ovaries: 20%; Small bowel: 10%	NR	62	800	RCTX: 90%	(NR; 7%; 12%) (NR)	Sphincter perseveration did not affect oncologic outcomes
Derici et al[48]	R0: 75%	LR: 18%	Adnexa: 47%; Uterus: 32%; Bladder: 30%	NR	60	NR	RCTX: 51%	(7%; 19%; NR) (NR)	Lymph node status pN0 (P = 0.007) and R0 resection (P = 0.005) were independently significant factors in the multivariate analysis for overall survival
Dinaux et al[50]	R0: 100%	LR. 3%; DR: 21%	Bladder: 28%; Prostate: 21%; Ovaries: 20%; Uterus: 20%	NR	55	NR	CTX. 100%; RCTX: 97%	(3%; 14%; 3%) (NR)	Chance of overall mortality significantly increased for patients; who underwent MVR, for administra-tion of adjuvant CTX, for Pn+ and ypN+ status
Dosokey et al[30]	NR	LR. 3% DR: 11%	Vagina: 50%; Prostate: 30%; Bladder: 33%	NR	66	549	CTX: 97% RT: 92%	(16%; NR; NR) (NR)	Patients with APR only had a longer 5 yr overall survival and a longer disease-free survival compared to patients undergoing MVR
Gannon et al[28]	R0: 90%	Primary: LR: 9%, LR + DR: 13%, DR: 22%; Recurrent: LR: 4%, LR + DR: 48%, DR:15%	TPE: 47% SLE: 47% PPE: 33%	NR	52	NR	RCTX: 85%	(NR; 4%; 11%) (4%)	A significant difference in 5-yr disease-free survival was found between primary and recurrent tumors (52% vs 13%, P < 0.01)
Harris et al[19]	R0: 93%	LR: 7%	Bladder+ Prostate: 55% Uterus: 24%	N0: 52% N1: 29% N2: 17% N3: 2%	62	NR	RCTX: 74%	(5%; 5%; 21%) (20%)	Association with worse overall survival in multivariate analysis: Metastatic disease, pT4N1 stage, vascular invasion
Ishiguro et al[54]	R0: 98%	LR: 9% DR: 25%	Uterus+ Bladder+ Rectum: 89%	N0: 57% N+: 43%	55	NR	RCTX: 14%	(4%; 23%; 8%) (9%)	Patients with positive lateral pelvic lymph node had a higher probability to recur and a decreased 5-yr over all survival
Mañas et al[13]	R0: 73%	LR: 37% DR: 35%	Uterus/Ovaries (each): 53%; Vagina; 27%; Seminal vesicle: 23%	N0: 40% N1: 27% N2: 34%	68	NR	RCTX: 20%	(13%; 53%; 10%) (NR)	Multivariate analysis showed that nodal involvement was independent predictor of poor survival (> 4 pos; nodes RR: 9.06 (P = 0.006)
Nielsen et al[9]	Primary:R0: 66% Recurrent: R0: 38%	NR	TPE with sacrectomy: 22%	NR	63	NR	RT: 65%	(4%; 20%; 7%) (NR)	There was no statistically significant difference in overall survival between primary and recurrent disease when comparing R0 resections
Pellino et al[14]	R0: 77%	LR: 16% DR: 22%	Not clearly specified	N0: 13% N1: 29% N2: 43%	62	NR	RT: 54%	(NR; 37%; 10%) (10%)	Perioperative complications were independent predictors of shorter survival (HR 3.53)
Rottoli et al[10]	Primary: R0 71%, Recurrent: R0: 56%	Primary: LR: 18% DR: 29% Both: 7%; Recurrent: LR: 22% DR: 33% Both: 17%	Sacrectomy: Primary: 18% Recurrent: 22%)	N0: 41% N1: 15% N2: 37%	57	Primary: 600 Recurrent: 750	65% (not specified)	NR	The long-term disease-free survival of patients undergoing pelvic exenteration is significantly worse when the procedure is performed for recurrent rectal cancer, regardless of the tumor involvement of the resection margins
Sanfilippo et al[51]	NR	LR: 20% DR: 44%	Vagina: 66%; Bladder/Prostate: 14%; Bladder/Vagina: 6%; Vagi-na/Uterus/O-varies: 6%	N0: 72% N1: 9% N2: 9%	55	NR	RCTX: 100%	(NR; 19%; 6%) (9%)	No significant association with pelvic control rate and age, sex, cN-stage, tumor distance from the anal verge, clinical tumor length, tumor circumference, tumor mobility, obstruction, grade, neoadjuvant CTX, and MVR
Shin et al[22]	R0: 100%	LR: 4%	Prostate: 36%; Vagina: 23%; Small bowel: 14%; Bladder wall: 14%	N0: 41% N1: 46% N2: 14%	54	225	RCTX: 82%	(NR; 17%; 17%) (13%)	Robotic MVR including resection of lateral pelvic lymph nodes is feasible with acceptable morbidity and no conversion
Smith et al[47]	R0: 85%	LR: 19%	Vagina: 52%; Uterus: 23%; Bladder: 11%	N0: 60% N+: 40%	63	NR	RCTX: 73% RT: 2%	(6%; 19%; 6%) (at least 1%)	5-yr overall survival in stage I-III: Tumor category (T3-4 vs T0-2: HR 2.80), Node category (N1-2 vs N0: HR 1.75), Involved resection margin: HR = 2.19), lymphovascu-lar invasion (L0 vs L1: HR 1.56)
Vermaas et al[11]	Primary:R0: 82%; Recurrent: R0: 58%	LR at 5-yr: Primary: 12%; Recurrent: 40%	TPE: 83% TPE an sacral bone: 11%; TPE with coccygeal bone: 6%	N0: 37% N1: 6% N2: 6%	58	NR	RT: 97%	(NR; 26%; NR) (9%)	Patients with recurrent rectal cancers have a higher rate of complications, a high distant metastasis rate and a poor overall survival

CTX: Chemotherapy; MVR: Multivisceral resection; S-MVR: Single-port MVR; M-MVR: Multi-port MVR; HR: Hazard ratio; RR: Relative risk; APR: Abdominoperioneal resection; PPE: Posterior pelvic exenteration; RCTX: Chemoradiotherapy; TPE: Total pelvic exenteration; LR: Local recurrence; DR: Distant recurrence; AI: Anastomotic insufficiency; SSI: Surgical site infections; IAA: Intraabdominal abscess; RT: Radiotherapy; NR: Not reported.

Table 3 Morbidity, mortality and survival rates after multivisceral resection for colon and rectal cancer

Study	Follow-up (mo)	Morbidity (%)	Mortality (%)	Survival1	Stage IV disease (%)	True pT4b (%)
Cukier et al[24]	36	36	0	3-yr OS: 85.9%; 3-yr DFS: 73.7%	0	67
Hallet et al[20]	54	33.3	0	90%; 5-yr DFS: 63.5%	0	50
Kumamoto et al[15]	32	17.8	0.8	87%	12	45
Leijssen et al[2]	48.5	25	0	5-yr OS (pT3): 63%; 5-yr OS (pT4): 70%	0	24
López-Cano et al[49]	74.9	47.8	7.1	48%; 5-yr DFS: 46.3 mo	20	65
Rosander et al[7]	28	37% (≥ Grade III)	5	60.8% for the infiltration group; 86.9% for the inflammation group	0	63
Takahashi et al[12]	48.4	LAP: 7 OPEN: 36	0	3-ys OS (open): 79.8%; (lap): 92.8%	25	50
Tei et al[23]	34	37.9	0	3-yr OS Stage II-III (S-MVR/M-MVR): 81.8%/80.0% 3-yr DFS Stage II-III (S-MVR/M-MVR: 58.3%/70.0%	28	34
Chen et al[6]	NR	11.5	NR	59% (Colon/inflammation) 39% (Colon/invasion) 63% (Rectum/inflammation); 42% (Rectum/invasion)	54	55
Eveno et al[58]	48	12	1.3	77%; 3-yr OS (without stage IV disease): 89%; 5-yr DFS: 58%	13	65
Fujisawa et al[29]	42 (mean)	NR	NR	3-yr OS (colon/bladder sparing): 90%; (colon/nonsparing): 67%; 3 yr OS (rectal/bladder sparing): 50%; (rectal/nonsparing): 67%	NR	NR
Hoffmann et al[21]	NR	34.6	7.7	55% (if curative)	49	63
Gezen et al[18]	25 (mean)	24.4	4.4	69.4%	12	34
Kim et al[17]	35/40 (mean)	LAP: 21 OPEN: 44	0	LAP: 60.5%; OPEN 48%	33	44
Laurence et al[56]	NR	NR	NR	52.7%	3	NR
Lehnert et al[8]	71	33	7.5	51%	5	50
Li et al[16]	64.3	61	5.6	50%; 59%: if curative	21	47
Park et al[53]	NR	35.2	3.1	58%	0	44
Rizzuto et al[57]	NR	55	0	3-yr OS (non-occlusive): 58.4%; (occlusive): 33.3%	0	77
Winter et al[1]	84	18	1.5	57%; 61% (R0); 17% (R1) 77% (R0, N0); 28% (R0, N+)	NR	54
Banmura et al[56]	32	50	0	Local recurrence rate: 30%	33	63
Crawshaw et al[25]	27.8	57.4	0	49.2%; 5-yr DFS: 45.3%	0	39
Derici et al[48]	40.4 (mean)	38.6	3.5	49%; 3-yr OS: 81.6%	0	58
Dinaux et al[50]	38.2	72.4	0	OS: 45 mo	0	24
Dosokey et al[30]	32 (mean)	39	0	67%; 5-yr DFS: 79%	0	NR
Gannon et al[28]	40	43	0	48%; Primary: 65% Recurrent: 22%; 5-yr DFS. 38%; Primary: 52% Recurrent: 13%	NR	NR
Harris et al[19]	30	50	0	5-yr OS (R0): 48%; R1/R2: 33%	14	52
Ishiguro et al[54]	40	39.8	2.2	52%; 5-yr DFS: 46%	NR	49
Mañas et al[13]	28.8	76.6	10	36.7%	20	67
Nielsen et al[9]	12	51	2.2	5-yr OS (primary): 46%; (recurrent):17%	0	NR
Pellino et al[14]	NR	54.9	2.4	67%	NR	70
Rottoli et al[10]	32.5/56.6	33 Primary: 32% Recurrent: 33%	4	5-yr DFS (primary): 46% (recurrent): 24%	NR	NR
Sanfilippo et al[51]	NR	25	NR	4-yr OS: 69%	0	44
Shin et al[22]	30	41.7	0	80%	27	23
Smith et al[47]	NR	47.6	0.8	53.3%; M0: 59%	20	44
Vermaas et al[11]	28 (mean)	69; Primary: 61; Recurrent: 83	3	52% (primary); 3-yr OS (recurrent): 32%	NR	43

¹if not specified 5-yr OS is reported. S-MVR: Single-port laparoscopic multivisceral resection; M-MVR: Multi-port laparoscopic multivisceral resection; NR: Not reported.

Table 4 Patient- and treatment- associated parameters of minimal-invasive multivisceral resection for colon and rectal cancer

Study	Resection margin (R0 vs R1)	Lymph-node harvest (n)	Conversion rate	Reason for conversion	Blood loss (mL)	Operative time (min)	LOS (d)
Kumamoto et al[15]	R0: 95%	26	6.8%	Excessive tumor fixation (n = 4); Suspicion of invasion to the duodenum (n = 2); Intraperitoneal adhesion (n = 2)	49	254	11
Takahashi et al[12]	R0: 96%	34 Open: 33	12%	The conversion rate was highest in cases involving the urinary tract (40%)	50; Open: 321	279; Open: 255	14; Open: 22.5
Tei et al[23]	R0: S-MVR: 100%; M-MVR: 93%	S-MVR: 30; M-MVR: 25	S-MVR M-MVR: 14%; M-MVR Open: 33%	Small intestine involvement	S-MVR: 60; M-MVR: 220	S-MVR: 222; M-MVR: 255	S-MVR: 11; M-MVR: 18
Kim et al[17]	R0: 71%	34; Open: 40	7.9%	NR	268; Open: 637	330; Open: 257	21.9; Open: 21
Shin et al[22]	R0: 100%	20	4.5%	Unable to tolerate Trendelenburg position and intraperitoneal adhesions	225	421	4.5

LOS: Length of hospital stay; S-MVR: Single-port multivisceral resection; M-MVR: Multi-port MVR.

Table 5 Patient- and treatment- associated parameters after multivisceral resection for gastric cancer

Study	Resection margin (R0 vs R1)	Most common resected organs	Lymph node involvement	Age	Blood transfusion	Complications (AI) (Re-OP)	Other prognostic factors
Carboni et al[39], 2005	R0 61.5%; R1 27.7%; R2 10.8%	Spleen: 48%; Pancreas: 43%; Colon: 25%	86.2%	61	NR	(1.5%) (1.5%)	Lymph-node involvement and metastatic disease
Colen et al[37], 2004	NR	Spleen: 62%; Pancreas 57%; Colon: 24%	NR	67.5	NR	0% (NR)	NR
D'Amato et al[38], 2004	R0: 69%	Pancreas: 62%; Colon: 12%	NR	NR	NR	(0%) (NR)	NR
Jeong et al[43], 2009	R0: 78.3%; R+: 21.7%	Spleen: 47%; Pancreas: 61%; Colon: 24%	N+: 90.1%	59	NR	(6.7%) (11%)	Lymph-node and lymphovascular involvement
Kim et al[35], 2009	R0: 43%; R1: 15%; R2: 74%	Spleen: 38%; Pancreas: 29%; Colon: 56%	NR	NR	NR	(2.9%) (0%)	histologic type, M stage, peritoneal metastasis, curability and treatment groups
Martin et al[36], 2002	R0: 100%	Spleen: 67%; Pancreas: 19%; Colon: 6%; Liver: 4% Gallbladder: 7%	N0: 35% N+: 65%	66	NR	(NR) (NR)	Lymph-node involvement and > pT3
Oñate-Ocaña et al[32], 2008	R0: 58.1%; R1: 18.9%; R2: 23%	Spleen: 68%; Pancreas: 26%; Colon: 12%; Liver: 9%	NR	NR	NR	(NR) (NR)	NR
Ozer et al[44], 2009	NR	Pancreas: 54%; Colon: 32%; Liver: 18%	NR	58	NR	(8.9%) (NR)	Advanced age, lymph node involvement, and resection of more than 1 additional organ were significant prognostic factors for survival.
Persiani et al[46], 2008	R0: 320; R1: 39; R2: 29%	Spleen: 84%; Pancreas: 25%; Colon: 10%	NR	63.4	NR	(NR) (NR)	Splenectomy, D2 lymphadenectomy, and age greater than 64 yr were the only factors predictive of overall morbidity
Shchepotin et al[33], 1998	NR	Spleen: 43%; Pancreas: 69%; Colon: 45% Liver: 29%	N+: 38.8%	NR	NR	(3.7%) (NR)	NR
Isozaki et al[45], 2000	NR	Pancreas + Spleen: 36%; Pancreatoduodenectomy: 7%	N0 = 13%; N1 = 36%; N2 = 25%; N3 = 12%	NR	NR	(NR) (NR)	Location of the tumor, lymph node metastasis, histological depth of invasion, and extent of lymph node dissection
Molina et al[40], 2019	R0: 94%	Pancreas (49%); Spleen (34%) Liver (29%).	N+: 80%	64,5	NR	(NR) (NR)	Lymph-node involvement and R1-status
Mita et al[42], 2017	R0: 82.5%; R1: 17.5%	Spleen 29.1%; Pancreas: 46.6%; Colon: 13.6%; Liver: 11.7%	N+: 84.5%	70	NR	(NR) (NR)	Resection status
Vladov et al[38], 2015	R0: 75%	Spleen: 76.7%; Pancreas:40%; Colon: 18.3%; Liver 15%	NR	NR	NR	(NR) (NR)	NR
Tran et al[31], 2015	R1: 15.5	Spleen: 48%; Pancreas:27% Liver 14% Colon: 13%	N0: 34.5%	64	NR	(11.5%) (13.8%)	MVR with pancreatectomy, was significantly associated with decreased survival, along with T-stage, N stage, perineural invasion, and
Pacelli et al[34], 2013	R0: 38.4%	Pancreas 46; Colon 43	N+: 89.3%	NR	NR	(7%) (NR)	Lymph-node involvement and incomplete resection

MVR: Multivisceral resection; NR: Not reported; AI: Anastomotic insufficiency.

Table 6 Morbidity, mortality and survival rates after multivisceral resection for gastric cancer

Study	n	Follow-up (mo)	Morbidity (%)	Mortality (%)	Survival	Stage IV (%)	True pT4b (%)
Carboni et al[39], 2005	65	13	27.7	12.3	OS: 21.8 mo	46	80
Colen et al[37], 2004	21	NR	39	10	OS: 30 mo	NR	38
D'Amato et al[38], 2004	52	NR	34.6	1.9	OS: 31 mo	NR	NR
Jeong et al[43], 2009	71	17.6	26.8	NR	3-yr OS: 36.4%	76	63
Kim et al[35], 2009	34	NR	11.8	0	OS: 37.8 mo	38	NR
Martin et al[36], 2002	268	NR	39.2	NR	OS: 63 mo	NR	21
Oñate-Ocaña et al[32], 2008	74	NR	26.9	NR	OS: 30.5 mo	NR	14-38
Ozer et al[44], 2009	56	10.8	37.5	12.5	3-yr OS: 53.3%	62	66
Persiani et al[46], 2008	51	NR	16.2	2.3	NR	79	19.6
Shchepotin et al[33], 1998	353	NR	31.2	13.6	5-yr OS: 25%	NR	89.0
Isozaki et al[45], 2000	86	NR	NR	NR	5-yr OS: 35%	NR	53
Molina et al[40], 2019	35	31	46	3	5-yr OS. 34%	NR	40
Mita et al[42], 2017	103	23.0	37.9	1.0	3-yr OS: 42.1%	0	57
Vladov et al[38], 2015	60	NR	28.3	6.7	5-yr OS: 24.1%	NR	70
Tran et al[31], 2015	159	NR	59.8	4.3	5-yr OS: MVR with pancreatectomy: 20%; MVR without: 36%	0	67
Pacelli et al[34], 2013	112	18.7	33.9	3,6	5-yr OS: 27.2%	NR	88

OS: Overall survival; NR: Not reported; MVR: Multivisceral resection.