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

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.