Pelvic Exenteration for Locally Advanced ColorectalCarcinoma
JOHN BOEY, M.D., JOHN WONG, PH.D., F.R.A.C.S., G. B. ONG, D.Sc., F.R.C.S.
Pelvic exenteration provided worthwhile palliation and achieveda cumulative five-year survival rate of 38.8% in 49 patients whohad carcinoma of the lower colon or rectum infiltrating ad-joining pelvic viscera. Survival and the disease-free period werenot significantly different after total or posterior exenteration.The stage of disease was the major determinant of outcome:five-year survival rates averaged 51.8% and 28.8% for StagesII and III, respectively. Hospital mortality (26.9%) after totalexenteration was chiefly due to technical mishaps, and the in-clusion of many high-risk but symptomatic elderly patients.Complete clearance of locally advanced colorectal cancer bypelvic exenteration is indicated in fit patients, expecially thosewith Stage II disease.
A N INVASIVE TUMOR, penetrating contiguous pelvicviscera but without disseminated disease, con-
fronts the surgeon in about 6% of large bowel cancers.'For surgery to be curative, all neoplastic tissue mustbe removed. Based on this surgical tenet, pelvic exen-teration evolved in the treatment of advanced colorectalcarcinoma that is confined to the pelvic area. Total ex-enteration comprises the en bloc resection of the rectumand distal colon, bladder and lower ureters, all internalreproductive organs, draining lymph nodes, and thepelvic peritoneum; a permanent colostomy and someform of urinary diversion are then required. Posteriorexenteration in the female is a similar operation exceptthe bladder is preserved because the malignant processdoes not extend to this organ.
Exenteration may be a curative operation for infil-trating tumors localized to the pelvic region, or it mayalso be considered a palliative measure when there islimited extrapelvic metastases. Total exenteration, mostcommonly performed for recurrent carcinoma of thecervix, is only infrequently practiced for colorectal ma-lignancies.2`4 Most surgeons would readily embark onposterior exenteration for a rectal tumor that extendsinto the adjoining uterus. Yet, there is an understand-able reluctance to undertake total exenteration whena similar growth has infiltrated into the base of the
Reprint requests: G. B. Ong, D.Sc., F.R.C.S., Queen Mary Hos-pital, Hong Kong.Submitted for publication: September 22, 1981.
Department of Surgery, University of Hong Kong, QueenMary Hospital, Hong Kong
bladder in a male patient. Certainly the operative mor-tality and quality of survival differ between the twotypes of exenteration, but one might perhaps expecttheir survival to be roughly similar. Thus far, no com-parison of these two operations for colorectal cancerhas been described because few patients meet the cri-teria for exenteration, and individual surgical experi-ence is consequently limited. In Hong Kong, many pa-tients with large bowel neoplasms present in such a latestage' that palliative surgery, even though radical innature, is needed. We, therefore, reviewed our experi-ence in 49 patients who underwent pelvic exenterationfor advanced colorectal carcinoma in order to assess itsrelative merits and current indications.
Patients and Methods
Between 1964 and 1981, 49 of 1040 patients (4.7%)with colorectal adenocarcinoma underwent pelvic ex-enteration as the initial operation for locally advancedtumors. There were 26 males and 23 females, with amean age of 58.3 (± 14.9SD) years. Total exenterationwas performed in 26 patients (including three patientsin whom intestinal continuity could be restored by eitherlow anterior resection or a pull-through procedure fortumors of the proximal rectum), and posterior exen-teration in 23 women (including three patients whounderwent either a low anterior resection or Hartmannoperation along with panhysterectomy). An ileal con-duit was used for urinary diversion after total exenter-ation in 23 patients, and a sigmoid colon conduit in theremaining three. Indications for pelvic exenteration fol-lowed established guidelines for determining resecta-bility of the primary lesion.'34'6 Nearly all patients hadsymptoms referrable to the primary tumor, which waslocated in the rectum in all but three patients. Tumoradherence to either the bladder or internal reproductiveorgans necessitated exenteration in these 49 cases: ma-
lignant infiltration was confirmed histologically in 38patients, whereas 11 had only severe inflammatory re-
action.The following factors that might affect operative
morbidity and mortality, or postoperative survival andrecurrence were examined: age, sex, type of exentera-tion, nature of complications, and stage of disease. Allcases were reclassified according to the American JointCommittee for Cancer Staging and End-Results Re-porting.7'8 For comparison, Stages II and III correspondto the original Duke's Stages B and C, respectively.There were 29 patients with Stage II disease (tumorpenetrating bowel wall without nodal or distant metas-tases), and 17 with Stage III lesions (tumor extendingbeyond bowel wall with lymph node disease). In addi-tion, three patients with locally invasive tumors under-went exenteration but were discovered soon after op-
eration to have liver metastases (two cases) or
supraclavicular lymph nodes (one case), thus placingthem more properly in the Stage IV category.
Other than the expected differences in sex distribu-tion, the patients undergoing either type of exenterationwere broadly comparable (Table 1).
Statistical analysis was by the corrected chi square
test, the Mann-Whitney test for nonparametric data,and the Lee-Desu comparison of actuarial survival de-rived by the Berkson and Gage life-table method.9-"Survival data pertain only to patients discharged homein order to distinguish deaths caused by malignant re-
currence from those due to operation. Statistical sig-nificance was accepted at the 5% level (two-tailed unlessotherwise specified).
Results
Morbidity and Mortality
Nine of the 49 patients ( 18.4%) died during the post-operative period (30-day mortality, 12.2%). Seven of26 patients (26.9%) died after total exenteration, in-cluding three who expired more than a month afteroperation (30-day mortality, 15.4%). Deaths were uni-formly caused by major postoperative complications(Table 2): urinary or fecal fistulae with pelvic sepsis(four patients), bronchopneumonia with respiratoryfailure (four patients), and bleeding (one patient). Post-mortem examinations, performed in eight of the ninepatients who died, confirmed the absence of both ex-
trapelvic as well as residual malignancy.The combined mortality of total and posterior ex-
enteration was significantly higher in patients older than65 years (n = 18, 33.3% mortality) than those 65 years
or below (n = 31, 9.7% mortality) (one-tailed p = 0.05,corrected chi square test). The patients who died aftertotal exenteration were much older than those who sur-
TABLE 1. Comparison of Patients who Underwent Total orPosterior Pelvic Exenteration
* NS = not significant.t Corrected chi square test.
vived the operation (median age 67.0 and 56.3 years,respectively; one-tailed p = 0.03, Mann-Whitney test).The stage of disease did not appear to influence mor-tality.
Survival
The cumulative five-year survival rate for the 40 dis-charged patients was 38.8% (excluding one recurrence-free death). In this small series, the type of exenterationdid not significantly affect either the overall or thestage-matched survival: total and posterior exenterationhad five-year results of 30.4% and 44.1%, respectively(Figs. 1, 3). Survival was chiefly determined by thestage of disease (Figs. 2, 3). Overall, Stage II patientshad a five-year survival rate of 51.8%, which was sig-nificantly better than that of Stage III and Stage IVpatients (28.8% and 0%, respectively; p = 0.001 and p= 0.0003, respectively) (Fig. 2). There was no discern-ible difference in prognosis between Stage III and StageIV groups, and it is possible that occult distant metas-tases may not have been detected in some Stage IIIpatients. The three patients with Stage IV disease died3, 13, and 22 months after operation.
Recurrence
Malignancy eventually recurred in 23 of the 40 pa-tients (57.5%) discharged from hospital. Pelvic or per-ineal recurrence developed in five Stage III or-Stage IVpatients after total exenteration, which represent localrecurrence rates for these two stages of 66.7% and
4G, AND ONG Ann. Surg. - April 1982
EXENTERATION FOR COLORECTAL CANCER 515TABLE 2. Postoperative Complications after Pelvic Exenteration
* Number of patients who died given in parentheses.t Pneumothorax (1), urinary retention (2), urinary tract infection
(3), and median nerve palsy (1).
100%, respectively. There was no local recurrent diseasein any patient with Stage II disease treated by totalexenteration. Six of the seven local relapses after pos-terior exenteration produced disabling symptoms, in-cluding bowel or ureteric obstruction, and pelvic sepsis.The median interval before local recurrence appearedin these 12 patients was ten months (range 3 to 26months). Their median survival time was 14.5 months(range 3 to 27 months), and all but one has died oftheir underlying malignancy.
Distant metastases (lung, liver, bones, and wide-spread peritoneal seeding) developed after total and
t More than one complication in some of the 25 patients who hadpostoperative morbidity.
posterior exenteration in eight instances each, with fiveof these accompanied by local recurrences.The five-year disease-free rates among those who sur-
vived total and posterior exenteration were 22.2% and36.4%, respectively (Fig. 1). Stage II patients remainedasymptomatic much longer than Stage III patients fol-lowing total exenteration (p = 0.001) (Fig. 4). For pa-tients with equivalent stages of disease, the type of ex-enteration did not significantly affect either the survivalor the disease-free period after operation (Figs. 3, 4).
Discussion
Extensive yet localized carcinoma of the rectum andtoi lower colon pose a formidable surgical problem. Left
*L. TE SLNMVAVL 19 untreated, the very absence of distant metastases sub-09 PE* SRVIVAL 21 jects such patients to the vexing sequelae of unre-
A\ \.\ ' TE DISEASE -FREE PERIOD 19 strained proliferation of the primary growth-intestinal0 '\ \12 PE DISEASE - F and ureteric obstruction, fistulization, unremitting deep
i ' \\\ pelvic pain, and abscess formation.'12 A diverting co-Z 0.7 T lostomy under these circumstances does not abolish lo-> \ \ \ SEM cal symptoms, and yields an average survival rate of
06 1 nine months.'3 Likewise, incomplete resection affordsonly fleeting palliation: rampant growth of residual tu-mor, usually occurring soon after incomplete resection,
O05 T- A3 gives rise to recrudescent and progressive symptoms in
U.4 6 ". \ nearly all cases, and long-term survival is exceedinglya A\AX _ A_ _ff_-- - A- - - rare.''2 Improved methods of radiotherapy have pal-
0. ' \- 1 2.. liated some patients, and even produced a few long-term>1|\ )1 survivors.'4"5 However, radiation treatment is more
~~Ii ~20.2 ;--- -- --o-0-__ often adjunctive to surgery in these situations, and it0.2-
TE vs PE p occasionally converts a previously "inoperable" lesionSURVIVAL 0.55 into a resectable one.'6 Chemotherapy is scarcely ef-
DISEASE-FREE PERIOD 0o66 fective in relieving symptoms due to the large tumorburden in these cases.
0 1 2 3 4 5 6 7 8 Concern with both the quality as well as the lengthof survival provided the major impetus to pelvic exen-
YEARS POST- OP teration for advanced colorectal carcinoma. Against theusual course of less radically treated cases, about 70%
FIG. 1. Actuarial survival and disease-free period of patients dis- of patie o survive teated caseeof70lcharged after pelvic exenteration according to the type of operation of patients who survive exenteration remain free of pel-performed. Numbers indicate patients at risk for that interval. TE vic or perineal disease. '7 For comparison, local recur-= total exenteration; PE = posterior exenteration. rence rates after wide resection of rectal cancers without
VOl. 195 * NO. 4
BOEY, WONG, AND ONG Ann. Surg. * April 1982
adjacent organ involvement range between 11.9% and31.7%.1821 In that recurrent local disease accounts forabout 20% of deaths due to rectal carcinoma, 19,22 pelvicexenteration may enhance survival by preventing thiscause of death. As noted in an another study,' pelvicrecurrences following total exenteration are mostly con-fined to patients with Stage III or Stage IV lesions. Inthis series, local relapses, which were accompanied bydistant metastases in one-half of the cases, becamemanifest about ten months after surgery with deathensuing some 41/2 months afterwards.Not only are tumor-related symptoms alleviated, but
even prolonged survival is possible with pelvic exenter-ation. Including the three palliative exenterations forStage IV disease, the cumulative five-year survival ratewas 38.8% among the discharged patients. The stageof disease more so than the type of exenteration is theprimary determinant of recurrence and survival. Itshould be emphasized that despite extensive local in-vasion, lymphatic spread is unexpectedly absent inmany patients'7-a situation found in the 29 Stage IIpatients (59.2% of all cases). Regional nodal involve-ment confers a poorer prognosis,' and the five-year sur-vival rate among all Stage III patients was considerablylower than that of Stage II patients. There was no sig-nificant difference in survival between Stage III and
1.C
a
a
c
c
C
C
C
FIG.of dis
\
\\13STAGEL
0 fl 24A m 13
1.0
0.9
0
z
l)
z0I-
0a.0a.
0s2
0.7
0.4
'\ \
\' '
A \5
2A
02[
SITAGLIL ni. PE. IL
IL * 12 o 12
m A 6 n 7
SEM
I
\\\ \ 1 2
\ ff ~~2
_ __A A __ -_- A _ -z
I'
DE sTAGES P
TE : vsM 0.002
PE lvsm o0osA
0.1
1 2 3 4 5 6 7 8
YEARS POST- OP
FIG. 3. Actuarial survival of discharged patients according to the typeof exenteration and stage of disease. Numbers indicate patients atrisk for that interval. TE = total exenteration; PE = posterior exen-teration.
-\ -\X T3 Stage IV patients. Even though this latter group livedfor only an average of one year after operation, their
1- \ \T existing preoperative symptoms were greatly improvedSEM by palliative exenteration.
).7 A\. Survival tends to be lower after total than after pos-terior exenteration. Though not statistically significant,this difference also conforms to the observed trend of
4X__T. . female patients living slightly longer than males with).5- I cancers of the colon and rectum.202324 Our five-year
2 survival rate of 30.4% after total exenteration compares).4-A with the average of 35% reported in a collected series
of 118 patients.'7 In this study, pelvic exenteration for-----\ \.- , . ' . . Stage II and Stage III disease had five-year survival
jl rates of 51.8% and 28.8% respectively. Corresponding12\ STAGES P figures achieved by conventional resection of less lo-
II Vs1m 0.001 cally-invasive rectal lesions are 57% and 25%, respec-M.1 U11 vs]Z Q003 tively.8 It appears that the need for complete tumor
M vsjI 0.41 clearance should supercede undue concern over the par-o* ticular organs to be removed, and should dictate the1 2 3 4 5 6 7 8 extent of surgical extirpation. For large tumors adher-
ent to or penetrating the uterus, the addition of pan-YEARS POST-OP hysterectomy does not appreciably reduce the quality
2. Actuarial survival of discharged patients according to the stage of life and may well enhance survival. However, even;ease. Numbers indicate patients at risk for that interval. though total cystectomy does compromise the quality
516
0'z5
z00-a.
a0
nal
\
Vol. 195 - No. 4 EXENTERATION FOR COLORECTAL CANCER 517
1 £~S IL L H.vL
09 \ \ 12 o 12
m A 6 a 7
0 TzO0.7 ' SEM
0.6-_ \ PE nm 11'4CO) 0
oo 2
0.
OL2- ~~QE STAGS P.TE fl1'vex 0.001
0 1 2 3 4 5 6 7 8
YEARS POST- OP
FIG. 4. Actuarial disease-free period for discharged patients accordingto the type of exenteration and stage of disease. Numbers refer topatients at risk for that interval TE = total exenteration; PE = pos-terior exenteration.
of survival, the ominous fate following incomplete ex-cision would argue for total exenteration when thoroughtumor clearance demands this. Total exenteration isunavoidable when there is malignant infiltration intothe trigonal and distal ureteric area; however, it is sel-dom necessary in dealing with colonic tumors that im-pinge upon the dome of the bladder: in most of thesecases, the area of infiltration is limited, the bladdermucosa spared, and a partial cystectomy is usually ad-equate.25 In contrast to other series where the tumorwas located in the distal colon in one-quarter to one-half of cases,"7 only two of our 26 patients who under-went total exenteration had lesions located above theperitoneal reflection.
Total exenteration should never be undertaken lightly.The operative mortality is high, particularly with initialattempts, and ranges from 8 to 49%.1-4,26 By contrast,posterior exenteration in this study bore a hospital mor-tality rate of 8.7%, which is in keeping with the reportedexperience.27'28 For total exenteration, our 30-day mor-tality of 15.4% is similar to the average (30-day) rateof 15.3% observed in 124 collected cases with advancedcolorectal lesions.612"17'27'29.30 Deaths were due to op-erative complications that led to pelvic sepsis as well
as respiratory failure in frail, elderly individuals. Likeother investigators,1"4 our hospital mortality rate of26.9% for total exenteration has declined with experi-ence: whereas five of 13 patients died after operationin the early part of this series, only two died among thesubsequent 13 patients. These improved immediate re-sults have followed greater attention to the technicaldetails of the urinary conduit reconstruction, and alsobetter nutritional and respiratory care during the peri-operative period.6 Mortality is significantly higher inpatients above 65 years old3' because of pre-existingmedical conditions, and five of our 12 patients in thisage group died after total exenteration. Even abdomi-noperineal resection and low anterior resection bear amortality rate of 11% to 23% in elderly patients,32 andone must carefully weigh the likelihood of palliationand cure by total exenteration against the substantialmortality incurred in older individuals with associatedmedical conditions. Most patients over 65 years old withStage III disease confirmed at laparotomy may not ben-efit from total exenteration because their median dis-ease-free period of 5.5 months hardly justifies their pro-hibitively high operative risks.
Based on this study, we believe pelvic exenterationshould be judiciously considered in fit patients with lo-cally advanced colorectal carcinoma in the absence ofextensive extrapelvic metastases, especially those withfavorable Stage II disease. Although total exenterationis a more formidable operation than posterior exenter-ation, its five-year survival rate of 30.4% still representsa desirable goal. More widespread adoption of totalexenteration is predicated on an acceptably low oper-ative mortality, and this is only likely to be achievedin specialized referral centers where accumulated ex-perience and optimal rehabilitation can be provided.Finally, adjunctive radio- and chemotherapy deservefurther evaluation to salvage those patients who even-tually succumb with recurrent disease despite pelvicexenteration.
Acknowledgments
Computer facilities were made available through the courtesy ofthe Center of Computer Studies and Applications, University of HongKong, Hong Kong.
References1. Butcher HR Jr, Spujut HJ. An evaluation of pelvic exenteration
for advanced carcinoma of the lower colon. Cancer 1959;12:681-687.
2. Kiselow M, Butcher HR Jr, Bricker EM. Results of the radicalsurgical treatment of advanced pelvic cancer: a fifteen-yearstudy. Ann Surg 1967; 166:428-436.
3. Symmonds RE, Pratt JH, Webb MJ. Exenteration operations:experience with 198 patients. Am J Obstet Gynecol 1975;121:907-918.
18. Moosa AR, Ree PC, Marks JE, et al. Factors influencing localrecurrence after abdominoperineal resection for cancer of therectum and rectosigmoid. Br J Surg 1975; 62:727-730.
19. Welch JP, Donaldson GA. The clinical correlation of an autopsy
study of recurrent colorectal cancer. Ann Surg 1979; 189:496-502.
20. Enker WE, Laffer UT, Block GE. Enhanced survival of patientswith colon and rectal cancer is based upon wide anatomic re-section. Ann Surg 1979; 190:350-360.
21. Veazey PR, McBride CM. Pelvic recurrence of cancer after ab-dominoperineal resection of the rectum. South Med J 1979;72:1545-1553.
22. Morson BC, Vaughan EG, Bussey JJR. Pelvic recurrence afterexcision of rectum for carcinoma. Br Med J 1963; 2:13-18.
23. End Results in Cancer, Report No. 4. Bethesda, MD: Departmentof Health Education and Welfare, US Public Health Service,National Institutes of Health, 1972; 51-68.
24. Clarke DN, Jones PF, Needham CD. Outcome in colorectal car-cinoma: seven-year study of a population. Br Med J 1980;1:431-435.
25. Quan SHQ, Sehdev MK. Pelvic surgery concomitant with bowelresection for carcinoma. Surg Clin N Am 1974; 54:881-886.
26. Inguilla W, Cosmi EV. Pelvic exenteration for advanced carci-noma of the cervix. Am J Obstet Gynecol 1967; 99:1083-1086.
27. Bacon HE, Zaber WF. Panhysterectomy concomitant with bowelresection for carcinoma: 75 cases. Surgery 1965; 57:370-376.
28. Block IR, Enquist IF. A more radical resection for carcinoma ofthe rectum in the female. Surg Gynecol Obstet 1964; 119:1328-1332.
29. Brunschwig A, Daniel W. Pelvic exenteration operations: withsummary of sixty-six cases surviving more than five years. AnnSurg 1960; 151:571-576.
30. Bricker EM, Butcher HR Jr, Lawler WH Jr, McAfee CA. Sur-gical treatment of advanced and recurrent cancer of the pelvicviscera: an evaluation of ten years experience. Ann Surg 1960;152:388-402.
31. Barber HRK. Relative prognostic significance of preoperative andpostoperative findings in pelvic extenteration. Surg Clin N Am1969; 49:431-447.
32. Block GE, Enker WE. Survival after operations for rectal car-cinoma in patients over 70 years of age. Ann Surg 1971;174:521-529.
