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Annals of Surgical Oncology 9:954-960 (2002)
© 2002 Society of Surgical Oncology

ORIGINAL ARTICLES

Radical Resection of Rectal Cancer Primary Tumor Provides Effective Local Therapy in Patients With Stage IV Disease

Garrett M. Nash, MD, Leonard B. Saltz, MD, Nancy E. Kemeny, MD, Bruce Minsky, MD, Sunil Sharma, MD, Gary K. Schwartz, MD, David H. Ilson, MD, Eileen O’Reilly, MD, David P. Kelsen, MD, Daniel R. Nathanson, MD, Martin Weiser, MD, Jose G. Guillem, MD, W. Douglas Wong, MD, Alfred M. Cohen, MD and Philip B. Paty, MD

From the Departments of Surgery (GMN, DRN, MW, JGG, WDW, AMC, PBP), Medicine (LBS, NEK, SS, GKS, DHI, EO, DPK), and Radiation-Oncology (BM), Memorial Sloan-Kettering Cancer Center, New York, New York.

Correspondence: Address correspondence and reprint requests to: Philip B. Paty, MD, Department of Surgery, Memorial Sloan-Kettering Cancer Center, 1275 York Ave., New York, NY 10021; Fax: 212-717-3678; E-mail: patyp{at}mskcc.org


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: The optimal use of radical surgery to palliate primary rectal cancers presenting with synchronous distant metastases is poorly defined. We have reviewed stage IV rectal cancer patients to evaluate the effectiveness of radical surgery without radiation as local therapy.

Methods: Eighty stage IV patients with resectable primary rectal tumors treated with radical rectal surgery without radiotherapy were identified. Sixty-one (76%) patients received chemotherapy; response information was available for 34 patients.

Results: Radical resection was accomplished by low anterior resection (n = 65), abdominoperineal resection (n = 11), and Hartmann’s resection (n = 4). Surgical complications were seen in 12 patients (15%), with 1 death and 4 reoperations. The local recurrence rate was 6% (n = 5), with a median time to local recurrence of 14 months. Only one patient received pelvic radiotherapy as salvage treatment. One patient required subsequent diverting colostomy. Median survival was 25 months. On multivariate analysis, the extent of metastasis and response to chemotherapy were determinants of prolonged survival.

Conclusions: For patients who present with distant metastases and resectable primary rectal cancers, radical surgery without radiotherapy can provide durable local control with acceptable morbidity. The extent of metastatic disease and the response to chemotherapy are the major determinants of survival. Effective systemic chemotherapy should be given high priority in the treatment of stage IV rectal cancer.

Key Words: Surgery • Stage IV • Rectal cancer • Distant metastasis


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Adenocarcinoma of the rectum is a highly treatable and often curable disease. In the absence of metastases, treatment is directed toward control of locoregional disease with the expectation that effective local therapy will cure many patients. Optimized surgical resection can yield local control in up to 90% of patients and can yield overall cure rates of 60% to 80%.1–4 For rectal cancers with transmural extension (T3, T4) or spread to regional lymph nodes (N1, N2), local control and cure by surgery are less certain. In these cases, the addition of adjuvant pelvic radiotherapy and systemic chemotherapy can improve treatment results.5,6 Adjuvant radiotherapy improves local control but has little effect on survival.5,7 Adjuvant chemotherapy improves survival and may also contribute to local control.6 Preoperative sequencing of radiotherapy offers advantages including reduced toxicity, downstaging, and improved sphincter preservation and has become the preferred treatment approach in many centers.8,9

Approximately 20% of patients with rectal cancer have distant metastases that are detectable at the time of presentation and can be assigned before surgery to stage IV (American Joint Committee on Cancer). The vast majority of these patients are not curable by current treatment modalities; however, aggressive treatment is generally indicated to extend the length and quality of life. Control of tumor growth in the pelvis is important to prevent the development of debilitating local symptoms. However, for many patients, control of metastatic cancer is the most crucial requirement to achieve prolonged symptom-free survival. In this setting, the use of chemotherapy may take priority over surgery and radiotherapy. Treatment approaches need to be individualized on the basis of the extent and resectability of both local and distant disease, the presence or absence of rectal obstruction, performance status, and comorbidities. The proper use and timing of radical surgery as local treatment for stage IV rectal cancer is not standardized, and few objective data are available to guide management.

We have retrospectively reviewed stage IV patients who were treated with radical surgery without radiotherapy, to define outcomes, prognostic factors, and patient selection. Surgical morbidity, local recurrence (LR), and survival were the principal outcome data collected. Our overall goal was to assess the effectiveness and optimal use of radical surgery for stage IV rectal cancer.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Patients
From January 1991 to December 2000, 335 consecutive patients with stage IV rectal cancer treated with surgery were entered in a prospective database maintained by the Colorectal Surgery Service at Memorial Hospital. Patients were excluded if they had local excision, fulguration, or diverting colostomy (n = 128), received preoperative radiotherapy (n = 66), received postoperative adjuvant radiotherapy (n = 43), or had incomplete records (n = 18). The remaining 80 patients were analyzed in this study, and their clinical characteristics are listed in Table 1. All tumors were located in the rectum, with 23 tumors (29%) located <6 cm from the anal verge, 48 in the mid rectum (7–11 cm), and 9 in the upper rectum (12–16 cm). All had documented distant metastases, and all were treated with radical resection of the rectum. Seventy patients had a single site of metastatic disease, nine had two sites of metastatic disease, and one had four sites of metastatic disease. Eighteen patients had metastatic lesions replacing >=50% of the liver. LR was defined as recurrence in the pelvis, excluding carcinomatosis. Median follow-up was 21 months (range, 1–110 months). Each patient’s cancer status at last follow-up was defined as no evidence of disease, alive with disease, dead of disease, or dead of unknown cause.


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  		TABLE 1. Patient characteristics (n = 80)
 
Pathologic Staging
According to the American Joint Committee on Cancer, all tumors were classified as stage IV at the time of surgery. There were 5 pT2 cases, 70 pT3 cases, and 5 pT4 cases. There were 21 pN0 cases, 36 pN1 cases, and 23 pN2 cases. Two primary tumors were well or well to moderately differentiated, 65 primary tumors were moderately differentiated, 8 were poorly to moderately differentiated, and 5 were poorly differentiated. Fifty-four tumors had lymphovascular or neural invasion. Sixteen tumors were classified as mucinous.

Surgical Treatment
Sharp mesorectal excision was performed on all patients. Sixty-five patients had a low anterior resection with primary anastomosis, 11 had an abdominoperineal resection, and 4 had a Hartmann’s resection. Two rectal tumors had positive microscopic resection margins. Twenty-two patients had complete gross resection of all primary and metastatic disease, of which 11 were synchronous and 11 were interval resections. Each of the resections of metastatic disease was performed for a single site of disease, including 19 liver metastases, 2 peritoneal metastases, and 1 pulmonary metastasis. Three patients who underwent hepatic resection did so after initiation of systemic chemotherapy with stabilization or response of metastatic disease. Complications of radical surgery were identified by chart review.

Chemotherapy
Documentation of chemotherapy treatment was available for 61 patients (76%) (Table 2). Perioperative systemic chemotherapy regimens, including 5-fluorouracil plus leucovorin and irinotecan plus 5-fluorouracil and leucovorin, were delivered to 57 patients; 4 patients received preoperative and postoperative systemic therapy, and 53 received only postoperative chemotherapy. Among the four patients not receiving perioperative systemic chemotherapy, three received postoperative hepatic arterial infusion chemotherapy and one received postoperative intraperitoneal chemotherapy. For the purpose of this study, the response to chemotherapy was defined by tumor response to the first chemotherapy regimen given and was based on comparison of pre- and postchemotherapy computed tomography (CT) scans. Response data were available for 34 of the 61 patients treated with chemotherapy (Table 3). Chemotherapy responses were defined by reduction in the diameter of liver, lung, or nodal metastases on the first posttreatment CT scan report.


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  		TABLE 2. Chemotherapy data (n = 80)
 

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  		TABLE 3. Response of metastasis to chemotherapy (n = 61)
 
Statistics
The {chi}2 distribution was used for analysis of categorical data. Survival was determined with the Kaplan-Meier method, and distributions were compared by use of the log-rank test. Multivariate analysis was performed with Cox regression.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Surgical Morbidity
Postoperative complications were identified in 15% of patients (n = 12). One postoperative death occurred because of respiratory failure in a patient with lung, liver, retroperitoneal lymph node, and peritoneal metastases. There were four reoperations for complications, one each for bleeding and anastomotic leak and two for bowel obstructions. There were seven other abdominal complications, consisting of three pelvic abscesses and four partial small-bowel obstructions. The abscesses were drained percutaneously, and the partial small-bowel obstructions resolved with conservative management. Of the 12 patients with postoperative complications, there were 7 readmissions within 60 days of the initial surgery. The median length of hospital stay for all patients was 9 days, and for patients with surgical morbidity it was 23 days.

Colostomy
Fifteen patients (19%) required colostomy at initial resection. One patient required a postoperative colostomy because of anastomotic leak. No other colostomies were documented during the follow-up period (median, 21 months). The total proportion of patients requiring colostomy was 20%.

Local Recurrence
The overall LR rate was 6% (n = 5), with a median time to LR of 20 months (range, 2–63 months). The actuarial local control rate at 2 years was 94% (Fig. 1). The sites of LR were the presacral space, perineum, vagina, bladder, and pelvic cul-de-sac. There were too few events to correlate LR with other variables. Surgical salvage of LR was attempted for four patients, and complete resection was achieved in each case. Subsequent LR was not detected for any of these patients. The fifth patient with LR was treated by chemoradiation. Median survival after LR was 15 months (range, 4–41 months). The overall median survival for the LR group was 49 months (range, 8–80 months) (Table 4).



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  		FIG. 1. Proportion of survivors free of local recurrence. NED, no evidence of disease; AWD, alive with disease; DUN, dead of unknown cause.

 

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  		TABLE 4. Characteristics of patients with local recurrence (LR)
 
Survival
At last follow-up, 9 patients had no evidence of disease, 10 were alive with disease, 57 were dead of disease, and 4 were dead of unknown cause. Median survival was 25 months (range, 22–29 months) but ranged from 5 to 85 months in selected groups (Fig. 2, Table 5). On univariate analysis, the extent of liver metastasis, the number of metastasis sites, lymphovascular or neural invasion, complete resection, major response to chemotherapy, major or minor response to chemotherapy, and progression with chemotherapy were statistically significant determinants of survival (P < .05). Variables that were not statistically significant by univariate analysis were age, obstruction, distance from the anal verge, tumor stage, mucinous tumor, tumor differentiation, nodal stage, and type of operation. On multivariate analysis, the extent of metastasis and the objective response to initial chemotherapy were strong and independent determinants of prolonged survival (Figs. 3 and 4).



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  		FIG. 2. Survival after surgery (entire cohort). NED, no evidence of disease; AWD, alive with disease; DUN, dead of unknown cause.

 

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  		TABLE 5. Analysis of variables affecting survival
 


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  		FIG. 3. Survival after surgery, stratified by extent of liver replacement. NED, no evidence of disease; AWD, alive with disease; DUN, dead of unknown cause. P value by Cox regression analysis.

 


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  		FIG. 4. Survival after surgery, stratified by response to chemotherapy. NED, no evidence of disease; AWD, alive with disease; DUN, dead of unknown cause. P value by Cox regression analysis.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Deciding the mode of local therapy for rectal cancer in the presence of metastatic disease is complex. In approaching this patient population, the treating surgeon has to consider the symptoms, the resectability of local and distant disease, the safety and potential efficacy of chemotherapy, the role of radiotherapy, and the risks and benefits of surgical intervention. At our institution, two thirds of patients with stage IV rectal cancer who undergo any type of surgical intervention have radical resection of the rectum. The goals of radical surgery in this setting are eliminating bleeding and obstruction, preventing local tumor progression, and preparing the patient for systemic chemotherapy. To assess the effectiveness and proper use of radical surgery, we chose to study a cohort of 80 patients who did not receive preoperative or postoperative pelvic radiotherapy. Our first aim was to assess the risk and benefit associated with radical surgery by evaluating surgical morbidity and local control. Our second aim was to assess factors that affect survival and may therefore help surgeons identify patients who survive long enough to benefit from rectal resection.

Analysis of this cohort of patients reveals that radical surgery for stage IV rectal cancer has acceptable morbidity and provides excellent local control. The morbidity associated with rectal resection was low and quite acceptable when one considers the advanced stage of the tumors and their expected natural history if not resected. Radical surgery necessitated permanent colostomy in 16 cases (20%), but no subsequent colostomies were required. We observed a 1% perioperative mortality rate and a 4% reoperation rate. Perhaps the most important finding of this study was the low rate of LR (6%), which provides a strong justification for surgical intervention. Moreover, the five patients who did develop LR were treated effectively at the time of local relapse. Four had surgical resection with no subsequent LR, and one had a good response to chemoradiation. Thus, in this study, the vast majority of patients achieved safe, rapid, and durable local control, and all were spared the time delay, toxicity, and marrow suppression associated with pelvic radiotherapy. These outcome data support the use of rectal resection without perioperative pelvic radiation for local treatment of rectal cancers that are considered by the surgeon to be fully resectable with low morbidity.

Despite its overall effectiveness and low morbidity, radical resection may not have benefited all of the patients treated in our series. Eleven patients died within 6 months of operation, and it is likely that a portion of these patients could have been palliated successfully without radical surgery. For those patients whose expected survival is short but who present with impending rectal obstruction, alternative therapies—such as fulguration, laser ablation, and endoscopic stenting—are available that have minimal risk, require little or no hospitalization, and allow systemic chemotherapy to begin immediately. Of note in this series, patients who did not go on to receive postoperative chemotherapy fared poorly. Of the 69 patients with sufficient records for assessment, 61 did receive postoperative chemotherapy, and 8 did not. In the latter group, the median survival was only 7 months. It would therefore seem that radical surgery offers the greatest benefit to patients who are fit and able to receive aggressive chemotherapy and is of questionable benefit to those who are not.

To provide more insight into patient survival and the appropriateness of radical surgery in this population, we examined the factors associated with duration of survival in the entire cohort of 80 patients. In multivariate analysis, the extent of liver metastasis was the one factor at presentation that predicted poor survival. Among the 70 patients with liver metastases, the patients with >50% replacement of the liver (n = 18) had a 4-fold higher rate of cancer death than those who had <50% replacement of the liver (n = 52). The median survival was 12 months compared with 26 months. Neither the size of the rectal tumor nor the presence of obstruction (inability to pass the colonoscope) was associated with the length of survival. It is important to note that the presence of extensive liver metastases was such a strong predictor of poor survival that surgical exploration and resection provided little additional prognostic information. Other sites of tumor spread, regional lymph node status, and histopathologic features of the primary tumor, although significant on univariate analysis of survival, were outweighed by the extent of liver metastasis on multivariate analysis. Therefore, radiographic staging seems to be sufficient for judging the extent of disease and its effect on patient survival. The dominant influence of extent of liver replacement in determining survival seen in this study is consistent with prior data reported from our institution.10,11

The other factor strongly associated with survival was the response to the patient’s first chemotherapy regimen. It should be recognized that over the 10-year period of this retrospective study, a variety of chemotherapy protocols were used as the first treatment regimen. These regimens included weekly and monthly dosing schedules of 5-fluorouracil plus leucovorin, irinotecan alone, irinotecan plus 5-fluorouracil and leucovorin, combined systemic/intrahepatic chemotherapy (three patients), and combined systemic/intraperitoneal chemotherapy (one patient). Objective response to chemotherapy, based on reduction in metastasis size on CT scan, was assessable from the available records in only 34 patients, which represented 56% of those known to have received chemotherapy. However, despite the small number of assessable patients, the benefit of effective chemotherapy was clearly evident. Any reduction in metastasis size (complete response, partial response, or minor response) proved to be the most significant statistical predictor of survival for the chemotherapy-treated group as a whole (median survival, 29 months for responders vs. 18 months for stable/progressive disease). However, the most impressive survival benefit was observed for patients with major responses to chemotherapy (85 months median survival for complete or partial response [n = 7] vs. 18 months for minor response, stable disease, or progression [n = 27]). Conversely, patients whose disease progressed on their initial chemotherapy regimen fared poorly (12 months median survival [n = 9] vs. 28 months for patients with any response or stable disease [n = 25]). Taken as a whole, these data indicate that effective chemotherapy is the most important therapeutic intervention for prolongation of patient survival.

Although major complications of radical rectal surgery were uncommon, surgery can result in a reduction of performance status and may therefore in some cases delay or prevent the initiation of systemic chemotherapy. Giving chemotherapy as initial therapy, before surgical intervention, ensures systemic treatment and may be a preferable treatment strategy for some patients. Our results suggest that patients with multiple sites of metastatic disease, advanced liver metastases, or poor performance status that does not permit aggressive systemic chemotherapy are poor candidates for initial radical surgery. In addition, those patients who have progressive disease on initial chemotherapy may be better served by trials of other chemotherapy regimens or symptomatic care rather than radical surgery.

Other investigators have recommended definitive chemoradiation for control of local disease in stage IV rectal cancer.12 They reason that resection does not eliminate the risk of pelvic recurrence, that colostomy may adversely affect quality of life, and that resection is associated with a high risk of treatment-related complications. Although their arguments may be relevant for certain patients with advanced disease, high comorbidity, or both, our series demonstrates the successful use of radical surgery in many stage IV patients. We found that the risk of pelvic recurrence after rectal resection was low. In our study, the 2-year actuarial local control rate was 94%. Furthermore, the overall colostomy rate in our surgery group (20%) was not different from the rate in their chemoradiation group (18%). Our treatment-related morbidity (15%) was also similar to theirs (11%).

We conclude that radical surgery is a safe and effective means of gaining local control for properly selected patients with stage IV rectal cancer. Perioperative morbidity is acceptable, and durable local control is achieved rapidly and effectively. However, patient survival is highly variable, and we believe that the prognostic factors identified in this study can be helpful in the use and timing of radical surgery. For patients with relatively limited metastatic disease detectable on preoperative imaging, survival for 2 years or longer is typical. In these patients, initiating treatment with either surgical resection or chemotherapy may be appropriate, depending on the extent of local symptoms, performance status, and comorbidities. Delaying resection of metastatic disease allows for radiographic confirmation of disease response to chemotherapy and would optimize use of a growing number of chemotherapeutic regimens. For patients with more advanced metastatic disease, a survival range of 6 to 18 months was seen in our series. In this setting, the degree of response to chemotherapy seems to be the most important predictor of disease control and survival. By reserving resective surgery for patients whose tumors respond to chemotherapy, patients with little hope of systemic disease control are spared the risks of radical surgery. Conversely, patients whose tumors respond to chemotherapy are downstaged and may then be considered for interval resection on the basis of their clinical course. With careful patient selection and skillful surgery, radical rectal resection can benefit many patients with stage IV rectal cancer.


   Footnotes
 
We retrospectively reviewed 80 patients with stage IV rectal cancer to evaluate the effectiveness of radical surgery without radiotherapy as local therapy. Surgical complications were seen in 15% of patients, and local recurrences were seen in only 6%.

Received for publication March 16, 2002. Accepted for publication August 1, 2002.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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