Anastomotic Recurrence after Anterior Resection for Carcinoma:
Lahey Clinic Experience* PAUL N. MANSON, M.D., MARVIN L. CORMAN, M.D., JOHN A. COLLER, M.D., MALCOLM C. VEIDENHEIMER, M.D. Section oJ Colon and Rectal Surgery, Lahey Clinic Foundation, Boston, Massachusetts
R.EYBARDTM first p e r f o r m e d a n t e r i o r resection of the sigrnoid for c a r c i n o m a in 1833 o n a 26-year-old m a n ; the p a t i e n t d i e d f r o m r e c u r r e n t disease one year later. Since t h a t time a n u m b e r of a p p r o a c h e s have b e e n d e v e l o p e d for r e m o v a l of m a l i g n a n t lesions of the d i s t a l large bowel. T h e classic operalion of Miles, 12 the a n t e r i o r resection, 6 a n d the a b d o m i n o a n a l x, e a n d a b d o m i n o s a c r a l 9 p r o c e d u r e s have b e c o m e a s t a n d a r d p a r t of o u r surgical a r m a m e n t a r i u m . Unfortunately, however, o p e r a t i o n s for c a r c i n o m a of the r e c t u m a n d rectosigrnoid are still p l a g u e d by the same c o m p l i c a t i o n s , sepsis 7 a n d r e c u r r e n t disease, 7, 13 w h i c h discouraged surgeons m o r e t h a n 100 years ago. A n a s t o m o t i c r e c u r r e n c e w i t h o p e r a t i v e procedures d e s i g n e d to restore cor~tinuity o f the i n t e s t i n a l tract n o t only signifies a technical f a i l u r e b u t a l m o s t always i n d i c a t e s t h a t the p a t i e n t will d i e f r o m disease. I n o r d e r to assess o u r e x p e r i e n c e w i t h a n a s t o m o t i c recurrence, a r e t r o s p e c t i v e review of a n t e r i o r resection was u n d e r t a k e n for the years 1963 to 1969. O u r d a t a indicate that a g r o u p at h i g h risk for anasto-
m o t i c r e c u r r e n c e can be p r e d i c t e d w i t h preoperative examinations (proctoscopic biopsy) a n d i n t r a o p e r a t i v e e x a m i n a t i o n s (clinical s t a g i n g a n d frozen section). Materials and Methods A n t e r i o r resection, d e f i n e d as a transabd o m i n a l r e s e c t i o n of the r e c t o s i g m o i d colon, was p e r f o r m e d in 152 p a t i e n t s d u r i n g the p e r i o d of study. I n those p a t i e n t s selected, the a n a s t o m o s i s was effected at o r b e l o w the p e r i t o n e a l reflection. T h e perit o n e u m was e i t h e r closed or left open. N o a t t e m p t was m a d e to d i s t i n g u i s h b e t w e e n low a n t e r i o r a n d h i g h a n t e r i o r resections. A l l a n a s t o m o s e s were p e r f o r m e d o p e n , end-to-end, w i t h an i n n e r l a y e r of c h r o m i c c a t g u t s u t u r e s a n d w i t h an o u t e r row of s e r o m u s c u l a r n o n a b s o r b a b l e sutures. N o n e of the seven surgeons w h o p e r f o r m e d these o p e r a t i o n s i r r i g a t e d the rectal s t u m p or p a i n t e d the e n d of the b o w e l to d i s c o u r a g e i m p l a n t a t i o n of t u m o r cells. 4 Bowel p r e p a r a t i o n g e n e r a l l y consisted of a t h o r o u g h m e c h a n i c a l c l e a n s i n g a n d a d m i n i s t r a t i o n of a n o n a b s o r b a b l e sulfa p r e p a r a t i o n . F o r t y two v a r i a b l e s r e l a t i v e to a n a s t o m o t i c recurrence were s u b m i t t e d to c o m p u t e r analysis. F o l l o w - u p i n f o r m a t i o n was a v a i l a b l e for all b u t one patient.j-
* Read at the meeting of the American Society of Colon and Rectal Surgeons, San Francisco, California, May 1 to 8, 1975. Address reprint requests to Dr. Corman: Section of Colon and Rectal Surgery, Lahey Clinic Foundation, 605 Commonwealth Avenue, Boston, Massachusetts 02215.
t Survivors were followed a mean of 79.8 months. 219
Dis. Col. & Reet.
April 1976
Volume 19 Number 3
MANSON, ET AL.
220
TABLE 1. Anterior Resection for Carcinoma Age by Decades (Years) 30-39 40-49 5O-59 60-69 7O-79 80-89 Towm. MEAN
Men
Women
Total
1 7 23 3t 22 2 86 63
0 8 23 21 12 2 66 61
1 15 46 52 34 4: 152 62
'ITABLE2. Anterior Resection for Carcinoma, Lahey Clinic, 1963-1969, Dukes" Classification Number of
Per Cent
Dukes' Stage
Patients
of Series
A
50
32
B
44
29
39 19 152
26 13 100
C D ToTm,
TABLE 3. Anterior Resection for Carcinoma, Gross Characteristics
Major
Number of
Characteristic
Patients
Per Cent of Series
77 47 13 7 4 4
50.6 30.9 8.6 4.6 2.6 2.6
Ulcerating Exophytic Polyp with invasion Villous Perforated Obstructed
Results
T a b l e 1 shows the ages of the patients; the m e a n ages for b o t h m e n a n d w o m e n were a p p r o x i m a t e l y the same, 62 years. T h e r e were two operative deaths, an operative m o r t a l i t y rate of 1.3 per cent. T a b l e 2 d e m o n s t r a t e s the p a t h o l o g i c extent of the t u m o r according to Dukes'
Dis. Col. & Reef.
April 1976
classification. Dukes' A lesions are confined to the bowel wall, whereas D u k e s ' B lesions breech the s e r o m u s c u l a r surface of the bowel. W i t h Dukes' C tumors, l y m p h nodes are involved, a n d Dukes' D classilication implies biopsy-proved t u m o r b e y o n d the limits of the surgical resection. T a b l e 3 d e m o n s t r a t e s the macroscopic a p p e a r a n c e of the lesions, a n d in T a b l e 4 the histology of the t u m o r s is shown. T h e m e a n d i a m e t e r of the lesions was 5.2 cm. T a b l e 5 illustrates tmcorrected five-year survival rates according to D u k e s ' classification. As expected, chances for survival decrease as e x t e n t of spread increases. A p p r o x i m a t e l y 77 per cent of anastomoses were b.elow the p e r i t o n e a l reflection a n d 23 per cent were at the p e r i t o n e a l reflect i o n ; 71 per cent of anastomoses w e r e drained. M e a s u r e m e n t by the p a t h o l o g i s t of the n o n f i x e d resected specimens revealed a m e a n l e n g t h of 22 cm. T h e m e a n distance from the distal m a r g i n of resection to the lower edge of the t u m o r was 4.8 cm. T h e m e a n m l m b e r of l y m p h nodes p r e s e n t i n the resected specimen was 8.6, w i t h a m e a n o[ 1.2 l y m p h nodes per s p e c i m e n i n v o l v e d by tumor. P r e o p e r a t i v e l y the m e a n distance of the lower edge of the lesion from the a n a l verge was 12 cm. T h e r e were 18 a n a s t o m o t i c recurrences, a r e c u r r e n c e rate of 1 1.8 per cent. T w o were b e n i g n villous a d e n o m a s that r e c u r r e d after resection of v i l l o u s a d e n o c a r c i n o m a s . If these cases are excluded, the r e c u r r e n c e rate for m a l i g n a n t t u m o r s was 10.5 per cent. H a l f of the r e c u r r e n t lesions were a m e n a b l e to reresection, with a five-year survival rate from time of reresection of 12.5 per cent. T h e other half were n o n r e s e c t a b l e , recurr i n g widely i n b o t h the pelvis a n d anastomosis. T h e times of r e c u r r e n c e r a n g e d from 2 to 38 m o n t h s , w i t h a n l e a n of 16 m o n t h s . Cross-correlations were u n d e r t a k e n u s i n g the c o m p u t e r to i d e n t i f y those factors that
Volume 19 Number 3
221
ANASTOMOTIC RECURRENCE
m i g h t c o n t r i b u t e to recurrence. T a b l e 6 illustrates the r e l a t i o n of the distal m a r g i n of resection a n d the percentage of anastomotic recurrence with that resection ntargin. R a t e of recurrence appears to be relatively c o n s t a n t u n t i l the m a r g i n of resection approaches 7 cm. Curiously, rec u r r e n t disease failed to develop i n the two p a t i e n t s with no m a r g i n of resection. ()ne p a t i e n t is alive and well after 12 years, a n d the other died of other causes a n d was free of disease. T a b l e 7 shows the relation between the lower edge of the lesion m e a s u r e d preoperatively at sigmoidoscopy a n d the percentage of incidence of a n a s t o n t o t i c recurrences at that level. T h e s e d a t a i n d i c a t e that recurrence is 11111(111 less 12:o111111oll when the tlllnor iS above 13 ont. T a b l e 8 illustrates the c o r r e l a t i o n with histologic differentiation. Fretluenc ) of recurrence increases with ttllllOrS that are more poorly ditterentiated. T a b l e 9 d e m o n strates the r e l a t i o n of recurrence to gross mort3hology of the tmnor. IZecurrence occurred ahnost exclusively in those patients who had ulcerati,~g lesions. T a b l e 10 shows the relation ol the stage of the lesion according to Dukes" classification. As expected, the risk of recurrence is greater as the 11111101"he(omcs nlol'e extensive. Discussion Review of the r e l a t i o n s h i p s presented gives an insight into those factors that predispose a p a t i e n t to a n a s t o m o t i c recurrence. By using o u r knowledge of high-risk factors, a more e n l i g h t e n e d decision of the operative a n d follow-up n l a n a g e m e n t of these lesions can perhaps be made. O n e import a n t decision is w h e t h e r or n o t to preserve intestinal continuity. It is well k n o w n that rectal cancers, w h e n resected, have a higher i n c i d e n c e of recurrence t h a n tumors in a more p r o x i m a l location.7. H O u r d a t a s u p p o r t this con-
TABLE 4. Anterior Resection ]or Carcinoma, Histology
Number of
Per Cent
Patients
of Series
Well di fferen tia ted
107
70.4
Moderately differentiated
33
21.7
Type
Poorly differentiated Villous
5
3.3
7
4.6
r|'Am.E 5. .4nterior Resection for Carcinoma, Five-year Survival (Uncorrected)
Number Dukes' Stage of Patients
Number Survived
Per Cent Survived 77.6
A
49
38
B
45
3O
66.6
C D All stages
39 19 152
19 1 88
48.7 5.3 57.9
"I'ABI.E 6. Anlerior Resection for Carcinoma, A ttastomotic Recurrence versus Distal Margin of Resection Distal Margin (cm)
Number of Patients
Number Recurrence
Per Cent Recurrence
0
2
0
0.0
1
10
l
10.0 17.6
2
17
3
3
23
2
8.7
4
24
3
12.5
5
31
6
19.4
6
16
2
12.5
7 >7
14 15
1 o
7.1 0.0
t e n t i o n a n d i n d i c a t e that there is a dramatic decrease i n the frequency of recurrence w h e n the lesion is more t h a n 13 cm from the anal verge. O u r o b s e r v a t i o n s a n d those of other investigators 7. 1~ show that more distal lesions p r e s e n t increased difficulties in terms of both the technical aspects
92 9 -
MANSON,
ET
Dis. Col. & Reet.
AL.
A p r i l 1976
-
TABLE 7.
Lower Edge (cm)
Anterior Resection for Carcinoma, Anastoraotic Recurrence versus Lower Edge o t Lesion
Number of Patients
Per Cent Series
Number Recurrence
Per Cent Recurrence 0.0 30.0 12.5 24.0 10.8 5.5 4.4
6
1
0.7
0
6--7 8-9
10 16 25 37 18 45
6.6 10.5 16.4 24.3 11.8 29.6
3 2 6 4 1 2
10-11
12-13 14-15 )15
of the resection a n d the ability to achieve a d e q u a t e margins. Most recurrences involved tumors that had p e n e t r a t e d the nnlscularis a n d e x t e n d e d i n t o s u r r o u n d i n g tissue. I t is n o t s u r p r i s i n g that 88 per cent o[ r e c u r r e n t m a l i g n a n t lesions in " c u r a t i v e " cases followed resections for this type of lesion. Results of a n a s t o m o t i c recurrence related to the histologic grade o1 the t u m o r i n d i c a t e a d r a m a t i c a l l y increased r e c u r r e n c e with a more poorly differentiated ttmtor. It has been recomtnendedS that p a t i e n t s with poorly differentiated lesions not u n d e r g o a n t e r i o r resection. O n the basis of this report, we most certainly concur. It m i g h t even be a r g u e d that p a t i e n t s w i t h moderately differentiated c a r c i n o m a of the r e c t u m should n o t have an anastomosis. However, previous investigators s. a0, 11.13 have n o t been in a g r e e m e n t a b o u t this relationship. Of interest is the high recurrence rate of villous a d e n o c a r c i n o m a , w i t h two b e n i g n a n d one m a l i g n a n t r e c u r r e n t lesions i n seven patients. ] n the b e n i g n r e c u r r e n t lesions, the distal m a r g i n of resection was ,3 cm i n each instance. T h e surgeon often tends to be less radical w h e n the lower edge of the m m o r is benigaa i n order to effect a satisfactory anastomosis. T h e m a l i g n a n t r e c u r r e n t lesion occurred i n a p a t i e n t w i t h a 5 cm m a r g i n of resection, b u t the t u m o r had i n v a d e d o t h e r pelvic organs.
E x a m i n a t i o n of the gross characteristics of the lesions in those p a t i e n t s with recurfence revealed that, except for villous a d e n o c a r c i n o m a , all r e c u r r e n t t u m o r s were ulcerating. O t h e r investigators 5, 8. to have n o t f o u n d such a clear r e l a t i o n s h i p . Ulcerating lesions tend to be more advanced, more dedifferentiated, a n d more deeply penet r a t i n g t h a n e x o p h y t i c lesions. E v a h l a t i o n of the distal m a r g i n of resection reveals that there is it fairly c o n s t a n t incidence ot r e c u r r e n c e u n t i l a distal margin of 7 cm is reached. I n o u r series, n o recurrence with it m a r g i n greater t h a n 7 cm was found. A clear r e l a t i o n s h i p does n o t a p p e a r between r e c u r r e n c e a n d m a r g i n of resection less t h a n (i cm, however. O t h e r investigators 3. s. 8. i0 confirm this linding. Analysis of r e c u r r e n c e a c c o r d i n g to Dukes' classification reveals that, in the 49 Dukes' A cases, there were two recurfences; 50 per cent of tlie lesions were well differentiated a n d 50 per cent were moderately' differentiated. T h e m e a n m a r g i n of resection was 4.5 cm. It is i n t e r e s t i n g that the only cure after reresection for anastomotic r e c u r r e n c e was in this g r o n p . i n Dukes' B cases, there were five recurrences in 45 patients. N o n e h a d hlood vessel invasion. T h e m e a n m a r g i n of resection was 4.7 cm, a n d the m e a n time of r e c u r r e n c e was 14.2 m o n t h s . T w o of the p a t i e n t s h a d reresection, a n d there was n o five-year
Volume 19 Number 3
ANASTOMOTIC
survivor. Sixty per cent of the recurrences were m o d e r a t e l y differentiated a n d 40 per cent were well differentiated; 60 per cent of the recurrences occurred i n lesions w h i c h had i n v a d e d o t h e r pelvic organs. Six recurrences occurred i n the 39 patients with Dukes' C lesions. T h e o n l y p a t i e n t i n this g r o u p with fewer t h a n five l y m p h nodes i n v o l v e d by t u m o r h a d invasion of o t h e r pelvic organs. Blood vessel i n v a s i o n was p r e s e n t i n o n e t h i r d of patients. R e c u r r e n t disease b e c a m e m a n i f e s t at 17.8 m o n t h s . W h e t h e r any of these patients w o u l d have fared b e t t e r w i t h abdomi n o p e r i n e a l resection, e x t e n d e d l y m p h a t i c dissection, pelvic e x e n t e r a t i o n , or c o m b i n e d a d j u v a n t r a d i a t i o n is a m a t t e r of speculation. T h e r e were three recurrences i n 19 Dukes' D cases. T h e m e a n m a r g i n of resection was 2.6 cm, less t h a n the m e a n for the other gxoups. M a r g i n was obviously c o m p r o m i s e d to p e r m i t a n easier anastomosis i n i n c u r a b l e patients. T h e m e a n time for the d e v e l o p m e n t of r e c u r r e n c e was eight months. I n general, all criteria presented correlate with one a n o t h e r . U l c e r a t i n g lesions tend to be less well differentiated a n d tend to i n v a d e deeper t h a n exophytic lesions. T h e s e are the lesions that show the highest rate of recurrence. T h e n u m b e r of p a t i e n t s in this series is n o t large, a n d thus it is difficult to draw conclusions with statistical significance. However, we have identified a n u m b e r of factors that seem to increase the risk of recurrence. Based on these findings the following o b s e r v a t i o n s can be made. 1. T h e incidence of r e c u r r e n c e appears to decrease d r a m a t i c a l l y w i t h the distal m a r g i n i n excess of 7 cm. 2. T h e i n c i d e n c e of r e c u r r e n c e is increased w i t h m a r g i n s less t h a n 6 cm. 3. T h e
i n c i d e n c e of r e c u r r e n c e is in-
223
RECURRENCE
TABLE 8. Anterior Resection for Carcinoma, Anastomotic Recurrence versus Histology
Type Well differentiated Moderately differentiated Poorly differentiated Villous TOTAL
Number of Patients
Number Recurrence
Per Cent Recurrence
107
5
4.7
33
6
18.2
5 7
4 3 (2 benign) 18
80.0 42.9
152
11.8
TABLE 9. Anterior Resection for Carcinoma, Anastomotic Recurrence versus Gross Morphology Type
Number of Patients
Number Per Cent Recurrence Recurrence
Ulcerating Exophytic Polyp with invasion Villous
77 47
15 0
19 0
13 7
0 43
Perforating Obstructing
4 4
0 3 (2 benign) 0 0
0 0
TABLE 10. Anterior Resection for Carcinoma, Anastomotic Malignant Recurrence versus Dukes" Classification
Dukes' Stage
Number of Patients
Number Recurred
Per Cent Recurred
A
49
2
4.1
B
45
5
11.1
C D
39 19
6 3
15.3 15.8
creased with resection of more distal lesions. T h e incidence of r e c u r r e n c e u l c e r a t i n g lesions is high.
with
5. T h e i n c i d e n c e of r e c u r r e n c e exophytic lesions is low.
with
4.
MANSON, ET AL.
224 6.
The
incidence
of
poorly differentiated prohibitively high.
recurrence tumors
with seems
7.
The i n c i d e n c e of r e c u r r e n c e with moderately differentiated l e s i o n s is high.
8.
The
incidence
of
recurrence
with
w e l l - d i f f e r e n t i a t e d l e s i o n s is low. 9.
The incidence of recurrence when the t u m o r h a s b r e e c h e d t h e b o w e l w a l l is high.
Ilk
T h e i n c i d e n c e of r e c u r r e n c e i n c r e a s e s with increased lymph node involvelnent.
1 1. T h e i n c i d e n c e of r e c u r r e n c e i n l e s i o n s i n v a d i n g o t h e r p e l v i c o r g a n s is h i g h . Summary A r e t r o s p e c t i v e s t u d y of 152 p a t i e n t s w h o underwent anterior resection for carcinoma of t h e r e c t u m a n d r e c t o s i g m o i d f r o m 1963 t o 1969 is p r e s e n t e d . E i g h t e e n a n a s t o m o t i c recurrences (two benign) were observed. Factors associated with high recurrence rates are discussed, and a scheme for identif i c a t i o n of t h o s e p a t i e n t s i n h i g h - r i s k g r o u p s is p r e s e n t e d . T h e v a l u e of t h i s s t u d y lies in facilitating decisions involving operative and postoperative management of d i s t a l colonic lesions. References 1. Babcock WW: Radical single stage extirpation for cancer of the large bowel, with retained functional anus. Surg Gynecol Obstet 85: 1, 1947
Dis. Col. & Rect.
April 1976
2. Bacon HE: Evolution of sphincter muscle preservation and re-establishment of continuity in the operative treatment of rectal and sigmoidal cancer. Surg Gynecol Obstet 81: 113, 1945 3. Buckwalter JA Jr, Kent T H : Prognosis and surgical pathology of carcinoma of the colon. Surg Gynecol Obstet 136: 465, 1973 4. Cole WH, Packard D, Sonthwick HW: Carcinoma of the colon with special reference to prevention of recurrence. JAMA 155: 1549, 1954 5. Deddish MR, Stearns MW Jr: Anterior resection for carcinoma of the rectum and rectosigmoid area. Ann Snrg 154: 961, 1961 6. Dixon CF: Anterior resection for malignant lesions of the upper part of the rectum and lower part of the sigvnoid. Ann Surg 128:425, 1948 7. Goligher JC: Further reflections on preservation of the anal sphincters in the radical treatment of rectal cancer. Proc R Soc Med 55: 341, 1962 8. Goligher JC, Dukes CE, Bussey HJ: Local recurrences after sphincter-saving excisions for carcinoma of the rectum and rectosigmoid. Br J Surg 39: 199, 1951 9. Localio SA: Abdominal-transsacral resection and anastomosis for midrectal carcinoma. Surg Gynecol Obstet 132: 123, 1971 10. Lofg-ren, EP, ~Vaugh JM, Dockerty MB: Local recurrence of carcinoma after anterior resection of the rectum and the sigmoid: Relationship with the length of normal mucosa excised distal to the lesion. Arch Surg 74: 825, 1957 11. Mayo CW, Schlicke CP: Carcinoma of the colon and rectum: A study of metastasis and recurrences. Surg Gynecol Obstet 74: 83, 1942 12. Miles WE: A method of performing abdominoperineal excision for carcinoma of the rectum and of the terminal portion of the pelvic colon. Lancet 2: 1812, 1908 13. Morson BC, Vaughan EG, Bussey HJ: Pelvic recurrences after excision of rectum for carcinoma. Br Med J 2:'13, 1963 14. Reybard JF: Memoire sur une tumeur cancereuse affectant l's iliaque de colon. Bull Acad Med Paris 9: 1031, 1843-44
Lahey Clinic Experience* PAUL N. MANSON, M.D., MARVIN L. CORMAN, M.D., JOHN A. COLLER, M.D., MALCOLM C. VEIDENHEIMER, M.D. Section oJ Colon and Rectal Surgery, Lahey Clinic Foundation, Boston, Massachusetts
R.EYBARDTM first p e r f o r m e d a n t e r i o r resection of the sigrnoid for c a r c i n o m a in 1833 o n a 26-year-old m a n ; the p a t i e n t d i e d f r o m r e c u r r e n t disease one year later. Since t h a t time a n u m b e r of a p p r o a c h e s have b e e n d e v e l o p e d for r e m o v a l of m a l i g n a n t lesions of the d i s t a l large bowel. T h e classic operalion of Miles, 12 the a n t e r i o r resection, 6 a n d the a b d o m i n o a n a l x, e a n d a b d o m i n o s a c r a l 9 p r o c e d u r e s have b e c o m e a s t a n d a r d p a r t of o u r surgical a r m a m e n t a r i u m . Unfortunately, however, o p e r a t i o n s for c a r c i n o m a of the r e c t u m a n d rectosigrnoid are still p l a g u e d by the same c o m p l i c a t i o n s , sepsis 7 a n d r e c u r r e n t disease, 7, 13 w h i c h discouraged surgeons m o r e t h a n 100 years ago. A n a s t o m o t i c r e c u r r e n c e w i t h o p e r a t i v e procedures d e s i g n e d to restore cor~tinuity o f the i n t e s t i n a l tract n o t only signifies a technical f a i l u r e b u t a l m o s t always i n d i c a t e s t h a t the p a t i e n t will d i e f r o m disease. I n o r d e r to assess o u r e x p e r i e n c e w i t h a n a s t o m o t i c recurrence, a r e t r o s p e c t i v e review of a n t e r i o r resection was u n d e r t a k e n for the years 1963 to 1969. O u r d a t a indicate that a g r o u p at h i g h risk for anasto-
m o t i c r e c u r r e n c e can be p r e d i c t e d w i t h preoperative examinations (proctoscopic biopsy) a n d i n t r a o p e r a t i v e e x a m i n a t i o n s (clinical s t a g i n g a n d frozen section). Materials and Methods A n t e r i o r resection, d e f i n e d as a transabd o m i n a l r e s e c t i o n of the r e c t o s i g m o i d colon, was p e r f o r m e d in 152 p a t i e n t s d u r i n g the p e r i o d of study. I n those p a t i e n t s selected, the a n a s t o m o s i s was effected at o r b e l o w the p e r i t o n e a l reflection. T h e perit o n e u m was e i t h e r closed or left open. N o a t t e m p t was m a d e to d i s t i n g u i s h b e t w e e n low a n t e r i o r a n d h i g h a n t e r i o r resections. A l l a n a s t o m o s e s were p e r f o r m e d o p e n , end-to-end, w i t h an i n n e r l a y e r of c h r o m i c c a t g u t s u t u r e s a n d w i t h an o u t e r row of s e r o m u s c u l a r n o n a b s o r b a b l e sutures. N o n e of the seven surgeons w h o p e r f o r m e d these o p e r a t i o n s i r r i g a t e d the rectal s t u m p or p a i n t e d the e n d of the b o w e l to d i s c o u r a g e i m p l a n t a t i o n of t u m o r cells. 4 Bowel p r e p a r a t i o n g e n e r a l l y consisted of a t h o r o u g h m e c h a n i c a l c l e a n s i n g a n d a d m i n i s t r a t i o n of a n o n a b s o r b a b l e sulfa p r e p a r a t i o n . F o r t y two v a r i a b l e s r e l a t i v e to a n a s t o m o t i c recurrence were s u b m i t t e d to c o m p u t e r analysis. F o l l o w - u p i n f o r m a t i o n was a v a i l a b l e for all b u t one patient.j-
* Read at the meeting of the American Society of Colon and Rectal Surgeons, San Francisco, California, May 1 to 8, 1975. Address reprint requests to Dr. Corman: Section of Colon and Rectal Surgery, Lahey Clinic Foundation, 605 Commonwealth Avenue, Boston, Massachusetts 02215.
t Survivors were followed a mean of 79.8 months. 219
Dis. Col. & Reet.
April 1976
Volume 19 Number 3
MANSON, ET AL.
220
TABLE 1. Anterior Resection for Carcinoma Age by Decades (Years) 30-39 40-49 5O-59 60-69 7O-79 80-89 Towm. MEAN
Men
Women
Total
1 7 23 3t 22 2 86 63
0 8 23 21 12 2 66 61
1 15 46 52 34 4: 152 62
'ITABLE2. Anterior Resection for Carcinoma, Lahey Clinic, 1963-1969, Dukes" Classification Number of
Per Cent
Dukes' Stage
Patients
of Series
A
50
32
B
44
29
39 19 152
26 13 100
C D ToTm,
TABLE 3. Anterior Resection for Carcinoma, Gross Characteristics
Major
Number of
Characteristic
Patients
Per Cent of Series
77 47 13 7 4 4
50.6 30.9 8.6 4.6 2.6 2.6
Ulcerating Exophytic Polyp with invasion Villous Perforated Obstructed
Results
T a b l e 1 shows the ages of the patients; the m e a n ages for b o t h m e n a n d w o m e n were a p p r o x i m a t e l y the same, 62 years. T h e r e were two operative deaths, an operative m o r t a l i t y rate of 1.3 per cent. T a b l e 2 d e m o n s t r a t e s the p a t h o l o g i c extent of the t u m o r according to Dukes'
Dis. Col. & Reef.
April 1976
classification. Dukes' A lesions are confined to the bowel wall, whereas D u k e s ' B lesions breech the s e r o m u s c u l a r surface of the bowel. W i t h Dukes' C tumors, l y m p h nodes are involved, a n d Dukes' D classilication implies biopsy-proved t u m o r b e y o n d the limits of the surgical resection. T a b l e 3 d e m o n s t r a t e s the macroscopic a p p e a r a n c e of the lesions, a n d in T a b l e 4 the histology of the t u m o r s is shown. T h e m e a n d i a m e t e r of the lesions was 5.2 cm. T a b l e 5 illustrates tmcorrected five-year survival rates according to D u k e s ' classification. As expected, chances for survival decrease as e x t e n t of spread increases. A p p r o x i m a t e l y 77 per cent of anastomoses were b.elow the p e r i t o n e a l reflection a n d 23 per cent were at the p e r i t o n e a l reflect i o n ; 71 per cent of anastomoses w e r e drained. M e a s u r e m e n t by the p a t h o l o g i s t of the n o n f i x e d resected specimens revealed a m e a n l e n g t h of 22 cm. T h e m e a n distance from the distal m a r g i n of resection to the lower edge of the t u m o r was 4.8 cm. T h e m e a n m l m b e r of l y m p h nodes p r e s e n t i n the resected specimen was 8.6, w i t h a m e a n o[ 1.2 l y m p h nodes per s p e c i m e n i n v o l v e d by tumor. P r e o p e r a t i v e l y the m e a n distance of the lower edge of the lesion from the a n a l verge was 12 cm. T h e r e were 18 a n a s t o m o t i c recurrences, a r e c u r r e n c e rate of 1 1.8 per cent. T w o were b e n i g n villous a d e n o m a s that r e c u r r e d after resection of v i l l o u s a d e n o c a r c i n o m a s . If these cases are excluded, the r e c u r r e n c e rate for m a l i g n a n t t u m o r s was 10.5 per cent. H a l f of the r e c u r r e n t lesions were a m e n a b l e to reresection, with a five-year survival rate from time of reresection of 12.5 per cent. T h e other half were n o n r e s e c t a b l e , recurr i n g widely i n b o t h the pelvis a n d anastomosis. T h e times of r e c u r r e n c e r a n g e d from 2 to 38 m o n t h s , w i t h a n l e a n of 16 m o n t h s . Cross-correlations were u n d e r t a k e n u s i n g the c o m p u t e r to i d e n t i f y those factors that
Volume 19 Number 3
221
ANASTOMOTIC RECURRENCE
m i g h t c o n t r i b u t e to recurrence. T a b l e 6 illustrates the r e l a t i o n of the distal m a r g i n of resection a n d the percentage of anastomotic recurrence with that resection ntargin. R a t e of recurrence appears to be relatively c o n s t a n t u n t i l the m a r g i n of resection approaches 7 cm. Curiously, rec u r r e n t disease failed to develop i n the two p a t i e n t s with no m a r g i n of resection. ()ne p a t i e n t is alive and well after 12 years, a n d the other died of other causes a n d was free of disease. T a b l e 7 shows the relation between the lower edge of the lesion m e a s u r e d preoperatively at sigmoidoscopy a n d the percentage of incidence of a n a s t o n t o t i c recurrences at that level. T h e s e d a t a i n d i c a t e that recurrence is 11111(111 less 12:o111111oll when the tlllnor iS above 13 ont. T a b l e 8 illustrates the c o r r e l a t i o n with histologic differentiation. Fretluenc ) of recurrence increases with ttllllOrS that are more poorly ditterentiated. T a b l e 9 d e m o n strates the r e l a t i o n of recurrence to gross mort3hology of the tmnor. IZecurrence occurred ahnost exclusively in those patients who had ulcerati,~g lesions. T a b l e 10 shows the relation ol the stage of the lesion according to Dukes" classification. As expected, the risk of recurrence is greater as the 11111101"he(omcs nlol'e extensive. Discussion Review of the r e l a t i o n s h i p s presented gives an insight into those factors that predispose a p a t i e n t to a n a s t o m o t i c recurrence. By using o u r knowledge of high-risk factors, a more e n l i g h t e n e d decision of the operative a n d follow-up n l a n a g e m e n t of these lesions can perhaps be made. O n e import a n t decision is w h e t h e r or n o t to preserve intestinal continuity. It is well k n o w n that rectal cancers, w h e n resected, have a higher i n c i d e n c e of recurrence t h a n tumors in a more p r o x i m a l location.7. H O u r d a t a s u p p o r t this con-
TABLE 4. Anterior Resection ]or Carcinoma, Histology
Number of
Per Cent
Patients
of Series
Well di fferen tia ted
107
70.4
Moderately differentiated
33
21.7
Type
Poorly differentiated Villous
5
3.3
7
4.6
r|'Am.E 5. .4nterior Resection for Carcinoma, Five-year Survival (Uncorrected)
Number Dukes' Stage of Patients
Number Survived
Per Cent Survived 77.6
A
49
38
B
45
3O
66.6
C D All stages
39 19 152
19 1 88
48.7 5.3 57.9
"I'ABI.E 6. Anlerior Resection for Carcinoma, A ttastomotic Recurrence versus Distal Margin of Resection Distal Margin (cm)
Number of Patients
Number Recurrence
Per Cent Recurrence
0
2
0
0.0
1
10
l
10.0 17.6
2
17
3
3
23
2
8.7
4
24
3
12.5
5
31
6
19.4
6
16
2
12.5
7 >7
14 15
1 o
7.1 0.0
t e n t i o n a n d i n d i c a t e that there is a dramatic decrease i n the frequency of recurrence w h e n the lesion is more t h a n 13 cm from the anal verge. O u r o b s e r v a t i o n s a n d those of other investigators 7. 1~ show that more distal lesions p r e s e n t increased difficulties in terms of both the technical aspects
92 9 -
MANSON,
ET
Dis. Col. & Reet.
AL.
A p r i l 1976
-
TABLE 7.
Lower Edge (cm)
Anterior Resection for Carcinoma, Anastoraotic Recurrence versus Lower Edge o t Lesion
Number of Patients
Per Cent Series
Number Recurrence
Per Cent Recurrence 0.0 30.0 12.5 24.0 10.8 5.5 4.4
6
1
0.7
0
6--7 8-9
10 16 25 37 18 45
6.6 10.5 16.4 24.3 11.8 29.6
3 2 6 4 1 2
10-11
12-13 14-15 )15
of the resection a n d the ability to achieve a d e q u a t e margins. Most recurrences involved tumors that had p e n e t r a t e d the nnlscularis a n d e x t e n d e d i n t o s u r r o u n d i n g tissue. I t is n o t s u r p r i s i n g that 88 per cent o[ r e c u r r e n t m a l i g n a n t lesions in " c u r a t i v e " cases followed resections for this type of lesion. Results of a n a s t o m o t i c recurrence related to the histologic grade o1 the t u m o r i n d i c a t e a d r a m a t i c a l l y increased r e c u r r e n c e with a more poorly differentiated ttmtor. It has been recomtnendedS that p a t i e n t s with poorly differentiated lesions not u n d e r g o a n t e r i o r resection. O n the basis of this report, we most certainly concur. It m i g h t even be a r g u e d that p a t i e n t s w i t h moderately differentiated c a r c i n o m a of the r e c t u m should n o t have an anastomosis. However, previous investigators s. a0, 11.13 have n o t been in a g r e e m e n t a b o u t this relationship. Of interest is the high recurrence rate of villous a d e n o c a r c i n o m a , w i t h two b e n i g n a n d one m a l i g n a n t r e c u r r e n t lesions i n seven patients. ] n the b e n i g n r e c u r r e n t lesions, the distal m a r g i n of resection was ,3 cm i n each instance. T h e surgeon often tends to be less radical w h e n the lower edge of the m m o r is benigaa i n order to effect a satisfactory anastomosis. T h e m a l i g n a n t r e c u r r e n t lesion occurred i n a p a t i e n t w i t h a 5 cm m a r g i n of resection, b u t the t u m o r had i n v a d e d o t h e r pelvic organs.
E x a m i n a t i o n of the gross characteristics of the lesions in those p a t i e n t s with recurfence revealed that, except for villous a d e n o c a r c i n o m a , all r e c u r r e n t t u m o r s were ulcerating. O t h e r investigators 5, 8. to have n o t f o u n d such a clear r e l a t i o n s h i p . Ulcerating lesions tend to be more advanced, more dedifferentiated, a n d more deeply penet r a t i n g t h a n e x o p h y t i c lesions. E v a h l a t i o n of the distal m a r g i n of resection reveals that there is it fairly c o n s t a n t incidence ot r e c u r r e n c e u n t i l a distal margin of 7 cm is reached. I n o u r series, n o recurrence with it m a r g i n greater t h a n 7 cm was found. A clear r e l a t i o n s h i p does n o t a p p e a r between r e c u r r e n c e a n d m a r g i n of resection less t h a n (i cm, however. O t h e r investigators 3. s. 8. i0 confirm this linding. Analysis of r e c u r r e n c e a c c o r d i n g to Dukes' classification reveals that, in the 49 Dukes' A cases, there were two recurfences; 50 per cent of tlie lesions were well differentiated a n d 50 per cent were moderately' differentiated. T h e m e a n m a r g i n of resection was 4.5 cm. It is i n t e r e s t i n g that the only cure after reresection for anastomotic r e c u r r e n c e was in this g r o n p . i n Dukes' B cases, there were five recurrences in 45 patients. N o n e h a d hlood vessel invasion. T h e m e a n m a r g i n of resection was 4.7 cm, a n d the m e a n time of r e c u r r e n c e was 14.2 m o n t h s . T w o of the p a t i e n t s h a d reresection, a n d there was n o five-year
Volume 19 Number 3
ANASTOMOTIC
survivor. Sixty per cent of the recurrences were m o d e r a t e l y differentiated a n d 40 per cent were well differentiated; 60 per cent of the recurrences occurred i n lesions w h i c h had i n v a d e d o t h e r pelvic organs. Six recurrences occurred i n the 39 patients with Dukes' C lesions. T h e o n l y p a t i e n t i n this g r o u p with fewer t h a n five l y m p h nodes i n v o l v e d by t u m o r h a d invasion of o t h e r pelvic organs. Blood vessel i n v a s i o n was p r e s e n t i n o n e t h i r d of patients. R e c u r r e n t disease b e c a m e m a n i f e s t at 17.8 m o n t h s . W h e t h e r any of these patients w o u l d have fared b e t t e r w i t h abdomi n o p e r i n e a l resection, e x t e n d e d l y m p h a t i c dissection, pelvic e x e n t e r a t i o n , or c o m b i n e d a d j u v a n t r a d i a t i o n is a m a t t e r of speculation. T h e r e were three recurrences i n 19 Dukes' D cases. T h e m e a n m a r g i n of resection was 2.6 cm, less t h a n the m e a n for the other gxoups. M a r g i n was obviously c o m p r o m i s e d to p e r m i t a n easier anastomosis i n i n c u r a b l e patients. T h e m e a n time for the d e v e l o p m e n t of r e c u r r e n c e was eight months. I n general, all criteria presented correlate with one a n o t h e r . U l c e r a t i n g lesions tend to be less well differentiated a n d tend to i n v a d e deeper t h a n exophytic lesions. T h e s e are the lesions that show the highest rate of recurrence. T h e n u m b e r of p a t i e n t s in this series is n o t large, a n d thus it is difficult to draw conclusions with statistical significance. However, we have identified a n u m b e r of factors that seem to increase the risk of recurrence. Based on these findings the following o b s e r v a t i o n s can be made. 1. T h e incidence of r e c u r r e n c e appears to decrease d r a m a t i c a l l y w i t h the distal m a r g i n i n excess of 7 cm. 2. T h e i n c i d e n c e of r e c u r r e n c e is increased w i t h m a r g i n s less t h a n 6 cm. 3. T h e
i n c i d e n c e of r e c u r r e n c e is in-
223
RECURRENCE
TABLE 8. Anterior Resection for Carcinoma, Anastomotic Recurrence versus Histology
Type Well differentiated Moderately differentiated Poorly differentiated Villous TOTAL
Number of Patients
Number Recurrence
Per Cent Recurrence
107
5
4.7
33
6
18.2
5 7
4 3 (2 benign) 18
80.0 42.9
152
11.8
TABLE 9. Anterior Resection for Carcinoma, Anastomotic Recurrence versus Gross Morphology Type
Number of Patients
Number Per Cent Recurrence Recurrence
Ulcerating Exophytic Polyp with invasion Villous
77 47
15 0
19 0
13 7
0 43
Perforating Obstructing
4 4
0 3 (2 benign) 0 0
0 0
TABLE 10. Anterior Resection for Carcinoma, Anastomotic Malignant Recurrence versus Dukes" Classification
Dukes' Stage
Number of Patients
Number Recurred
Per Cent Recurred
A
49
2
4.1
B
45
5
11.1
C D
39 19
6 3
15.3 15.8
creased with resection of more distal lesions. T h e incidence of r e c u r r e n c e u l c e r a t i n g lesions is high.
with
5. T h e i n c i d e n c e of r e c u r r e n c e exophytic lesions is low.
with
4.
MANSON, ET AL.
224 6.
The
incidence
of
poorly differentiated prohibitively high.
recurrence tumors
with seems
7.
The i n c i d e n c e of r e c u r r e n c e with moderately differentiated l e s i o n s is high.
8.
The
incidence
of
recurrence
with
w e l l - d i f f e r e n t i a t e d l e s i o n s is low. 9.
The incidence of recurrence when the t u m o r h a s b r e e c h e d t h e b o w e l w a l l is high.
Ilk
T h e i n c i d e n c e of r e c u r r e n c e i n c r e a s e s with increased lymph node involvelnent.
1 1. T h e i n c i d e n c e of r e c u r r e n c e i n l e s i o n s i n v a d i n g o t h e r p e l v i c o r g a n s is h i g h . Summary A r e t r o s p e c t i v e s t u d y of 152 p a t i e n t s w h o underwent anterior resection for carcinoma of t h e r e c t u m a n d r e c t o s i g m o i d f r o m 1963 t o 1969 is p r e s e n t e d . E i g h t e e n a n a s t o m o t i c recurrences (two benign) were observed. Factors associated with high recurrence rates are discussed, and a scheme for identif i c a t i o n of t h o s e p a t i e n t s i n h i g h - r i s k g r o u p s is p r e s e n t e d . T h e v a l u e of t h i s s t u d y lies in facilitating decisions involving operative and postoperative management of d i s t a l colonic lesions. References 1. Babcock WW: Radical single stage extirpation for cancer of the large bowel, with retained functional anus. Surg Gynecol Obstet 85: 1, 1947
Dis. Col. & Rect.
April 1976
2. Bacon HE: Evolution of sphincter muscle preservation and re-establishment of continuity in the operative treatment of rectal and sigmoidal cancer. Surg Gynecol Obstet 81: 113, 1945 3. Buckwalter JA Jr, Kent T H : Prognosis and surgical pathology of carcinoma of the colon. Surg Gynecol Obstet 136: 465, 1973 4. Cole WH, Packard D, Sonthwick HW: Carcinoma of the colon with special reference to prevention of recurrence. JAMA 155: 1549, 1954 5. Deddish MR, Stearns MW Jr: Anterior resection for carcinoma of the rectum and rectosigmoid area. Ann Snrg 154: 961, 1961 6. Dixon CF: Anterior resection for malignant lesions of the upper part of the rectum and lower part of the sigvnoid. Ann Surg 128:425, 1948 7. Goligher JC: Further reflections on preservation of the anal sphincters in the radical treatment of rectal cancer. Proc R Soc Med 55: 341, 1962 8. Goligher JC, Dukes CE, Bussey HJ: Local recurrences after sphincter-saving excisions for carcinoma of the rectum and rectosigmoid. Br J Surg 39: 199, 1951 9. Localio SA: Abdominal-transsacral resection and anastomosis for midrectal carcinoma. Surg Gynecol Obstet 132: 123, 1971 10. Lofg-ren, EP, ~Vaugh JM, Dockerty MB: Local recurrence of carcinoma after anterior resection of the rectum and the sigmoid: Relationship with the length of normal mucosa excised distal to the lesion. Arch Surg 74: 825, 1957 11. Mayo CW, Schlicke CP: Carcinoma of the colon and rectum: A study of metastasis and recurrences. Surg Gynecol Obstet 74: 83, 1942 12. Miles WE: A method of performing abdominoperineal excision for carcinoma of the rectum and of the terminal portion of the pelvic colon. Lancet 2: 1812, 1908 13. Morson BC, Vaughan EG, Bussey HJ: Pelvic recurrences after excision of rectum for carcinoma. Br Med J 2:'13, 1963 14. Reybard JF: Memoire sur une tumeur cancereuse affectant l's iliaque de colon. Bull Acad Med Paris 9: 1031, 1843-44
