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10.1245/ASO.2005.03.039
Annals of Surgical Oncology 12:65-71 (2005)
© 2005 Society of Surgical Oncology
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Original Article

Long-Term Survival of Peritoneal Carcinomatosis of Colorectal Origin

Vic J. Verwaal, MD, PhD1, Serge van Ruth, MD, PhD1, Arjen Witkamp, MD, PhD1, Henk Boot, MD, PhD2, Gooike van Slooten, MD1 and Frans A. N. Zoetmulder, MD, PhD1

1 Department of Surgery, The Netherlands Cancer Institute, Plesmanlaan 121, 1066 CX Amsterdam, The Netherlands
2 Department of Gastroenterology, The Netherlands Cancer Institute, Plesmanlaan 121, 1066 CX Amsterdam, The Netherlands

Correspondence: Address correspondence and reprint requests to: Vic J. Verwaal, MD, PhD; E-mail: v.verwaal{at}nki.nl


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Peritoneal carcinomatosis of colorectal cancer is probably best treated by cytoreduction and hyperthermic intraperitoneal chemotherapy (HIPEC). In The Netherlands Cancer Institute, this treatment has been performed since 1995. The long tradition of this treatment enabled us to study long-term survival in detail.

Methods: Between 1995 and 2003, 117 patients were treated by cytoreduction and HIPEC. The aim of the cytoreduction was to remove all visible tumor. After the cytoreduction, the abdomen was perfused with mitomycin C (35 mg/m2) at 40°C to 41°C for 90 minutes. Survival was calculated by the Kaplan-Meier method. Survival was also analyzed for the following subgroups: no residual tumor, residual tumor ≤ 2.5 mm, and more residual tumor. Hazard ratios for each of the seven abdominal regions were calculated to determine the influence on survival.

Results: The median survival was 21.8 months. The 1-, 3-, and 5-year survival rates were 75%, 28%, and 19%, respectively. The Kaplan-Meier curve reached a plateau of 18% at 54 months. In 59 patients a complete cytoreduction was achieved, and in 41 patients there was minimal residual disease. The median survival of these patient groups was 42.9 and 17.4 months, respectively. When gross macroscopic tumor was left behind, as was the case in 17 patients, the median survival was 5 months. Involvement of the small bowel before cytoreduction was associated with poorer outcome.

Conclusions: Cytoreduction followed by HIPEC showed a median survival of 21 months. From 3 years on, a consistent group of 18% of patients stayed alive.

Key Words: Colorectal cancer • Peritoneal carcinomatosis • HIPEC • Long-term survival


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Peritoneal carcinomatosis is a manifestation of colorectal cancer characterized by free-floating tumor cells that reseed on the peritoneal surface. After implantation on the peritoneal surfaces, the malignant cells may form tumor nodules throughout the abdominal cavity.1 Peritoneal carcinomatosis is present in approximately 10% of patients with colorectal cancer at the time of first diagnosis and in approximately 25% of patients with recurrent disease.2–4 Although peritoneal carcinomatosis is frequently found in combination with distant metastases, it seems to be the only site of disease in approximately 25% to 35% of patients.5,6

The treatment of peritoneal carcinomatosis of colorectal origin is shifting from a minimalist approach to very active management.7,8 Cytoreduction followed by hyperthermic intraperitoneal chemotherapy (HIPEC) is the most proactive way of dealing with peritoneal carcinomatosis. This treatment has been established by a number of phase II studies and even a phase III study.6,9–12 In the phase III study, significantly better survival was found when this treatment was compared with palliative surgery and systemic chemotherapy.

The potential improvement in survival has to be balanced against the side effects of this intensive treatment.13 A number of studies report complication rates (mostly related to surgery) as high as 30%.14,15 Although most complications are surgery related, HIPEC probably increases their effects.

The above-mentioned complication rates are acceptable only if long-term survival can be expected. In The Netherlands Cancer Institute, this treatment has been performed since 1995. The long tradition of this treatment enabled us to study long-term survival.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Between November 1995 and August 2003, 117 patients with peritoneal carcinomatosis of colorectal origin were treated with cytoreduction and HIPEC at The Netherlands Cancer Institute. Sixty-four patients were male, and 53 were female, with a median age of 53 years. The first 36 patients were entered onto phase I and II studies. The next 48 patients were entered onto a randomized phase III study, and the remaining 33 patients were treated after this study.

Patients with histologically proven peritoneal carcinomatosis of colorectal origin without evidence of liver or lung metastases, up to 70 years old, and fit to undergo major surgery were eligible for this therapy. Both synchronous and metachronous carcinomatosis were included. Written informed consent was required for patients who participated in the trials.

Treatment Schedule
The entire treatment consisted of surgical cytoreduction plus intraperitoneal chemotherapy, followed by adjuvant systemic chemotherapy. The objective of cytoreduction was to leave no macroscopic tumor behind. If this was not feasible, then the aim was reframed to leave no tumor thicker than 2.5 mm, because this is the maximum penetration depth at which a dose advantage of intraperitoneal mitomycin C can be expected.

Maximum exposure was obtained by opening the abdominal cavity from xiphoid to pubis and dividing all adhesions. Resection of the peritoneum was performed as described by Sugarbaker.16 Infiltrated viscera were (partly) resected. Restrictions were made on the extent of surgery as far as it was compatible with sufficient postoperative function.

The perfusion method used for HIPEC is described in detail elsewhere by Witkamp et al.17 The inflow temperature of the perfusate was 41°C to 42°C. As soon as this temperature was reached, mitomycin C was added in three fractions (one half, one fourth, and one fourth of the total dose) with a 30-minute interval. For patients in the phase II study, the dose of mitomycin C was increased stepwise from 25 to 40 mg/m2. All other patients were treated with mitomycin C 35 mg/m2. After completion of 90 minutes of perfusion, the fluid was drained from the abdomen.

The continuity of the gastrointestinal tract was restored after the perfusion was finished. Single-layer hand-sutured anastomoses were used. A colostomy was routinely made in case of a rectum resection. A gastrostomy was used to allow the stomach to drain, and a transgastric jejunal feeding tube was placed for enteral nutrition.

Patients stayed in the intensive care unit until they were stable with respect to cardiac and pulmonary function. Close watch was kept for any sign of abdominal sepsis, which was an indication for relaparotomy at an early stage.

Systemic adjuvant chemotherapy was given for 6 months with the modified Laufman regimen18 (5-fluorouracil 400 mg/m2 and leucovorin 80 mg/m2 weekly). If patients had been treated with 5-fluorouracil within a year before HIPEC, they were treated with irinotecan (350 mg/m2 every 3 weeks) instead of 5-fluorouracil.19,20

Grading Tumor Amount
The spread and thickness of tumor was measured in seven regions of the abdomen: pelvis, right lower abdomen, omentum/transverse colon, small bowel/mesentery, subhepatic space/stomach, right subphrenic space, and left subphrenic space. For each region, a semiquantitative score was allocated by measuring the maximum thickness of the largest nodules (none, 0; <20 mm, 1; 20–50 mm, 2; >50 mm, 3). In case of confluent nodules, the maximum thickness of the resulting plaque was used.

The result of cytoreduction was determined according to the maximum thickness of tumor nodules left behind at any place in the abdomen. No residual macroscopic tumor was graded as an R1 resection, and residual macroscopic tumor ≤ 2.5 mm was recorded as an R2a resection; if more disease was left behind, this was graded as an R2b resection.

Statistical Analyses
Survival was measured from the date of cytoreduction and HIPEC until death or the date of last follow-up in censored cases. The median survival and the 1-, 2-, 3-, 4-, and 5-year survival rates were determined for the entire patient population and for each cytoreduction category. The survival differences between categories were tested with the log-rank test. The relation between affected region and survival was analyzed with Cox regression analysis.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Data on 117 consecutive patients were analyzed with a median follow-up of 46 months. The colorectal cancer was located in the colon in 95 patients. Thirty-three patients had a right-sided colon cancer, 15 patients had a left-sided colon cancer, and in 47 patients the tumor was located in the sigmoid. In 15 patients, the carcinomatosis was based on an appendix cancer and in 5 patients on rectal cancer. The location of the primary tumor was not known in two patients. Sixty-seven patients had synchronous carcinomatosis, and 50 had carcinomatosis metachronous with the colorectal cancer.

The tumor-node-metastasis classification of the primary tumor showed a T4 tumor in 61 patients and a T3 tumor in 52 patients. In two patients, the primary tumor was T2. In 24 patients the primary tumor was graded as N0, in 34 patients as N1, and in 12 patients as N2. In the remaining 47 patients, the N status could not be determined.

Table 1Go shows the percentage in which a region was affected before and after the cytoreduction. The pelvis and the omentum were affected in almost all patients. The ileocecal region was cleared in most patients. If tumor deposits had to be left behind, this was in the subhepatic space, on the mesentery of the small bowel, and in the right subphrenic space.


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  		TABLE 1. Percentage of peritoneal carcinomatosis per region before and after cytoreduction and percentage of clearance per region in 117 patients treated by cytoreduction plus hyperthermic intraperitoneal chemotherapy for peritoneal carcinomatosis
 
Many organs were resected. The omentum and ovaries were resected in female patients. The rectum was resected in 51.3% of the patients, parts of the colon were resected in 41% of patients, and ileocecal resections were performed in 58% of the patients. Forty-eight percent of the patients needed a colostomy. In the upper abdomen, partial stomach resections were performed in 10% of the patients, and 56% needed one or more small-bowel resections. A splenectomy was performed in 11 patients.

The cytoreductions were macroscopically complete (R1) in 59 patients. In 44 patients minimal residual tumor was left behind (R2a), and in 14 patients gross macroscopic tumor was left behind (R2b).

Of the 117 treated patients, 7 (6%) died of treatment-related causes. Three of these patients had gross incomplete resections (R2b), and the other four had minimal residual disease.

The median survival of the entire study population was 21.8 months (95% confidence interval [CI], 19.0–25.5 months). The 1-, 3-, and 5-year survival probability was .75 (95% CI, .65–.82), .28 (95% CI, .18–.38), and .19 (95% CI, .10–.29), respectively.

Patients in whom six or all seven regions were affected had a median survival time of only 11.2 months (95% CI, 5.0–20.8 months), whereas this was 25.5 months (95% CI, 19.7–33.4 months) when fewer regions were affected. The survival was also strongly correlated with the degree of completeness of the cytoreduction (Fig. 1Go). In patients in whom the cytoreduction was macroscopically complete, the median survival was 42.9 months (95% CI, 22.8–not reached). In this group, the 1-, 3-, and 5-year survival probability was .94 (95% CI, .83–.98), .56 (95% CI, .38–.71), and .43 (95% CI, .25–.60), respectively. When residual tumor was left behind that was not thicker than 2.5 mm, then the median survival was 17.4 months (95% CI, 12.0–20.8 months). The 1- and 3-year survival was .66 (95% CI, .49–.79) and .09 (95% CI, .02–.20). Only one of these patients survived >5 years. The median survival of the patients who had a gross incomplete cytoreduction was only 5.0 months (95% CI, 2.7–9.5 months).



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  		FIG. 1. Kaplan-Meier curve by results of cytoreduction in 117 patients treated for peritoneal carcinomatosis of colorectal origin by cytoreduction plus hyperthermic intraperitoneal chemotherapy.

 
In patients in whom complete cytoreduction was achieved, involvement of the small bowel before the cytoreduction was related to decreased survival. Hazard ratios per region of patients with complete cytoreduction are listed in Table 2Go. If tumor was left behind in the abdomen, no specific region dominated the effect on survival. Table 3Go lists the hazard ratios for regions with residual disease.


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  		TABLE 2. Hazard ratios for survival per affected region in 59 patients treated by complete cytoreduction plus hyperthermic intraperitoneal chemotherapy for peritoneal carcinomatosis
 

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  		TABLE 3. Hazard ratios for survival per region with residual tumor in 59 patients after treatment by cytoreduction plus hyperthermic intraperitoneal chemotherapy for peritoneal carcinomatosis
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
In the past decade, a number of groups have reported on results of cytoreduction combined with intraperitoneal chemotherapy. The Sugarbaker group has been the most productive. They published an article in 1999 on 385 patients affected by appendiceal malignancies and showed a 5-year survival rate of 30%.21 In a similar study, Loggie et al.10 made a clear distinction between patients who had a complete cytoreduction and patients who had an incomplete cytoreduction. In this study, a complete cytoreduction resulted in a median survival of 28 months, and those who had an incomplete cytoreduction survived a median of 10 months. A comparable result was found by Shen et al.,6 who showed improved survival after complete cytoreduction. The 3-year survival rate in their study was 68% for those who underwent a complete cytoreduction, versus 21% for the others. In Europe, Piso et al.11 found a remarkable 4-year survival rate of 75%. Even in incompletely cytoreduced patients, the 4-year survival rate was 40%, whereas after complete cytoreduction this was 90%. Elias et al.9 concluded from their experience in Paris that a 50% 2-year survival could be reached, and the group of Beaujard22 in Lyon found a median survival of 16 months in patients who underwent successful cytoreduction. The Roman study of Cavaliere et al.23 showed a 2-year survival of 61%. At The Netherlands Cancer Institute, a median survival of 22 months was found in a randomized trial comparing cytoreduction plus HIPEC followed by systemic adjuvant chemotherapy with palliative surgery and systemic chemotherapy.12 In the present study, which includes all patients treated for peritoneal carcinomatosis by cytoreduction and HIPEC at The Netherlands Cancer Institute (including the patients in the previously mentioned randomized trial), a median survival of 42.9 months and a 5-year survival rate of 43% were found in patients in whom a complete cytoreduction was achieved.

Selecting patients for cytoreduction and HIPEC is difficult. With respect to survival and to complication rates, the key issue is to select patients in whom it is feasible to reach a complete cytoreduction. The best information to select these patients is gathered during the laparotomy in which peritoneal carcinomatosis is diagnosed.13,24 It is, therefore, of the utmost importance that the operative notes provide full details of the procedure during which the carcinomatosis is found. This means that a description of the findings should be accompanied by an explanation of the attempts made to explore the abdomen. A standardized form on which operative findings can be reported would be helpful. An example of such a form is displayed in Fig. 2Go.



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  		FIG. 2. Registration form for patients affected by peritoneal carcinomatosis of colorectal origin.

 
Cytoreduction plus HIPEC is a combined treatment modality, but surgical groups—not medical oncologists—perform most studies concerning HI-PEC. Still, a typical study on this subject provides full data on the HIPEC itself, whereas data on the surgery performed for cytoreduction are often poorly presented. In this study, the extent of surgery is given by describing the number of resections. The data indicate that the small bowel and its mesentery is the limiting factor for survival. Once it has been affected and cleared from tumor, it still remains the region that indicates poor outcome. The reason for this is that a minimal length of bowel should be preserved for maintaining adequate nutritional and fluid uptake. This limits the possibility for resection of all affected bowel and mesentery. Furthermore, it is likely that not all the peritoneal surface on the bowel and mesentery is optimally exposed to the perfusion fluid because of short cuts between inflow and outflow catheters.

The large number of resected organs not only results in high complication rates, but also affects the remaining function. McQuellon et al.25,26 studied quality of life after cytoreduction plus HIPEC. They found no long-lasting impairment of the quality of life after cytoreduction plus HIPEC. This probably means that the remaining abdominal function is adequate for a "normal" well-being.

The question of which part of the combination treatment is effective—cytoreduction or HIPEC—is still open. From this analysis, it is clear that a macroscopic complete resection (R1) is a basic necessity for a good outcome. Nevertheless, this does not exclude that HIPEC is the condition making an R1 resection worthwhile. A randomized study in which one arm consists of cytoreduction and the other arm of cytoreduction and HIPEC would answer the question of whether an element of the treatment can be left out. Such a study should enroll at least 400 patients and therefore should be a multicenter study. A protocol for such a study is currently being developed at The Netherlands Cancer Institute.

Recent developments in the medical treatment of stage VI colon carcinoma have brought promising results. These developments will provide an opportunity to improve adjuvant treatment after HIPEC. They also provide an opportunity to test newer agents in the HIPEC setting, e.g., intraperitoneal oxaliplatin.

In conclusion, cytoreduction and HIPEC can result in long-term survival in patients with peritoneal carcinomatosis of colorectal origin. Therefore, this treatment should be considered for all patients in whom a complete cytoreduction of the abdominal cavity is feasible. If a complete cytoreduction cannot be accomplished, then patients are not expected to benefit much from this treatment.


   ACKNOWLEDGMENTS
 
The authors thank Harm van Tinteren for his statistical advice and Omgo Nieweg for his linguistic advice.

Received for publication March 18, 2004. Accepted for publication August 23, 2004.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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