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10.1245/ASO.2006.03.079
Annals of Surgical Oncology 13:635-644 (2006)
© 2006 Society of Surgical Oncology
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Original Article

Prospective Morbidity and Mortality Assessment of Cytoreductive Surgery Plus Perioperative Intraperitoneal Chemotherapy To Treat Peritoneal Dissemination of Appendiceal Mucinous Malignancy

Paul H. Sugarbaker, MD, FACS, FRCS1, Robert Alderman, PA-C1, Gary Edwards, PA-C1, Christina Ellen Marquardt, RN1, Vadim Gushchin, MD1, Jesus Esquivel, MD1 and David Chang, MS2

1 Washington Cancer Institute, 106 Irving Street, N.W., Suite 3900, Washington, District of Columbia 20010
2 Westat, 1441 West Montgomery Avenue, Rockville, Maryland 20850–2062

Correspondence: Address correspondence and reprint requests to: Paul H. Sugarbaker, MD, FACS, FRCS; E-mail: paul.sugarbaker{at}medstar.net.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Appendiceal mucinous neoplasms present, in most patients, with peritoneal dissemination at the time of initial diagnosis. Patients may have a borderline tumor showing disseminated peritoneal adenomucinosis or an aggressive malignancy identified as peritoneal mucinous adenocarcinoma. Patients with these diagnoses were treated by cytoreductive surgery and perioperative intraperitoneal chemotherapy.

Methods: A database was established in 1998 that prospectively evaluated the morbidity and mortality of this group of patients. By using common toxicity grading criteria, 8 categories were scored on a grade of I to V. Grade IV indicated that the adverse event required urgent and definitive intervention: often a return to the operating room or to the surgical intensive care unit. Grade V indicated that the adverse events resulted in the patient’s death. Adverse events were tabulated for each cytoreduction performed in these appendiceal malignancy patients.

Results: There were 356 procedures in patients taken to the operating room who received cytoreductive surgery with peritonectomy procedures plus heated intraoperative intraperitoneal chemotherapy. Only patients who had this combined treatment at our institution were included in the analysis. The total 30-day or inshospital mortality was 2.0%. Nineteen percent of procedures were accompanied by at least one grade IV adverse event, and 11.1% of patients returned to the operating room. The most common category of grade IV complications was hematological (28%), followed by gastrointestinal (26%).

Conclusions: The mortality of 2.0% and the overall grade IV morbidity of 19% in these patients may be acceptable in light of modern standards for the management of gastrointestinal cancer.

Key Words: Cytoreductive surgery • Hyperthermia • Peritonectomy • Intraperitoneal chemotherapy • Mitomycin C • 5-Fluorouracil


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Natural history studies show a prolonged survival of patients with appendiceal mucinous tumors with peritoneal dissemination, but few patients survive past 10 years.1–3 Five studies in which patients received cytoreductive surgery plus intraperitoneal chemotherapy suggested that the median survival may exceed 10 years.4–9 This study was designed to assess the incidence of morbidity and mortality in a large number of patients treated in a uniform fashion in an experienced carcinomatosis treatment center. The goal was to better assess this comprehensive management plan for peritoneal dissemination of mucinous appendiceal malignancies.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Patient Eligibility Criteria
The database for patients with peritoneal surface dissemination was maintained from January 1998 until December 31, 2004. In this group, 473 procedures for appendiceal mucinous tumors were performed; 356 procedures were included in this data analysis. For this article, only (1) major cytoreductive operations that required peritonectomy procedures and (2) visceral resections in which heated intraoperative intraperitoneal chemotherapy was used in patients with a diagnosis of appendiceal epithelial malignancy with peritoneal dissemination were included. Patients were excluded if a reoperative procedure such as a second-look operation occurred, if ostomy closure was a scheduled surgical intervention, or if the procedure was not included in the database, even if heated intraoperative intraperitoneal chemotherapy was used. Reoperative procedures to resect recurrent appendiceal tumor diagnosed at follow-up were included in this database. Appendiceal malignancy patients were not included by the intention-to-treat principle. Patients who were taken to the operating room for cytoreductive surgery combined with intraperitoneal chemotherapy and who had an open-and-close procedure without heated intraoperative intraperitoneal chemotherapy were not included. These eligibility requirements were designed to exclude patients with less extensive procedures from this assessment.

Database
The database was completed by a physician’s assistant (R.A. or G.E.) as the hospital discharge summary was being dictated. These records were then reviewed by the senior attending and other attending surgeons on a monthly basis at a surgical team meeting. Data were entered into the computer by a nurse (C.E.M.). Data analysis was performed by a professional statistician (D.C.).

The database was constructed specifically to evaluate patients treated for carcinomatosis. It consisted of 47 adverse events arranged within 8 categories by organ system. The categories and a list of the adverse events that were scored for each patient are listed in Table 1Go. For each adverse event, a grade was assigned. For a grade I adverse event, the diagnosis was established, but no treatment was required. For grade II, the adverse event required medical treatment for resolution. For grade III, the adverse was potentially serious but was resolved conservatively, often with an invasive intervention for resolution. This was often a computed tomographic or ultrasound-guided diagnostic or therapeutic intervention. For grade IV, the adverse event required definitive urgent intervention—often a return to the operating room or to the surgical intensive care unit. A grade V adverse event led to the patient’s death (Table 2Go).


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  		TABLE 1. Appendiceal peritoneal surface malignancy postoperative morbidity/mortality database: 8 categories of events and 47 adverse events were scored
 

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  		TABLE 2. Peritoneal surface malignancy postoperative morbidity/mortality database: grades I to V were assigned by increasing severity to 47 adverse events
 
Cytoreductive Surgery
The goal of surgery in these patients was to visibly clear the abdomen and pelvis of disease. This required a series of peritonectomy procedures and visceral resections.10–12 Peritonectomy procedures included omentectomy with or without splenectomy, right and left subphrenic peritonectomy, pelvic peritonectomy, total anterior parietal peritonectomy, and peritonectomy of the omental bursa with or without cholecystectomy. The visceral resections included rectosigmoidectomy, right colectomy, total abdominal colectomy, hysterectomy, small-bowel resection, and total gastrectomy.13 All were scored as a single visceral resection except for total abdominal colectomy, which was considered two resections. Normal peritoneum or normal visceral structures were not resected; peritoneum or viscera was resected if layered by mucinous tumor that could not be removed by gauze debridement.

Surgical Management
A mechanical bowel preparation was used on all patients; oral antibiotics were not administered. Intrajugular or subclavian central venous catheters were used during surgery in all patients. During surgery, patients received cefazolin 1 g every 4 hours and metronidazole 500 mg every 4 hours. These antibiotics were begun approximately 1 hour before the surgical procedure and were continued throughout the cytoreduction. No antibiotics were used after surgery except to treat a specific organism that caused clinically significant infection identified in follow-up. Prophylaxis for venous thrombosis and pulmonary embolus was limited to the use of sequential compression devices that were applied to the leg but not to the thigh. These sequential compression devices were used throughout the hospitalization except when the patient was ambulating or up in a chair. No prophylactic anticoagulants were used; intravenous heparin was used to treat an identified venous thrombosis or pulmonary embolus. No antiemetics were used unless the patients were specifically bothered by the early postoperative intraperitoneal 5-fluorouracil. Filgrastim (Amgen, Thousand Oaks, CA) was used if the total white blood cell count decreased to <2000 THOUS/MCL. Treatment was with 400 µg/day until neutrophil counts rebounded to normal. Granulocyte colony-stimulating factors were not used prophylactically. No presplenectomy or post-splenectomy vaccination was ordered on any of these patients. Closed-suction drains remained in place after surgery in all patients. One drain was placed beneath the right hemidiaphragm, another was placed beneath the left hemidiaphragm, and two were left in the pelvis. A fifth closed-suction drain was placed within the subcutaneous space. Thoracostomy tubes were used whenever a patient had a subphrenic peritonectomy. Tubes were removed in the second postoperative week as drainage diminished. Gastrostomy tubes were never used. Jejunostomy tubes were never used. All patients received postoperative intravenous feeding until their caloric intake was adequate to allow it to be discontinued.

Perioperative Intraperitoneal Chemotherapy
After the cytoreduction was complete but before intestinal anastomoses or repair of seromuscular tears, the complete abdomen and pelvis were irrigated with a warm mitomycin C chemotherapy solution. The target temperature for entire abdomen was 41.5°C. Three liters of 1.5% dextrose peritoneal dialysis solution was used as a carrier solution for the chemotherapy.14

During the 90 minutes of heated intraoperative intraperitoneal chemotherapy, the skin edges were elevated to maintain an abdominopelvic reservoir.15 Manual distribution of the warm chemotherapy solution was maintained by the surgeon’s double-gloved hand. The intraperitoneal temperature was kept at <43°C, and the core temperature was kept at <39°C by decreasing the temperature of the heater circulator fluid. Urine output was monitored every 15 minutes and maintained at >150 mL every 15 minutes by forced diuresis and diuretics. After the completion of heated intraoperative intraperitoneal chemotherapy, bowel anastomoses, plication of seromuscular tears, and abdominal closure occurred.

The tubes and drains positioned for the heated intraoperative intraperitoneal chemotherapy were preserved for early postoperative intraperitoneal chemotherapy with 5-fluorouracil.14 A dose of 600 mg/m2 in 1 L of 1.5% dextrose peritoneal dialysis solution was used. After instillation, gravity distribution of the chemotherapy solution was effected by turning the patient from the full right lateral position to the full left lateral position and back every half hour. Patients were flat in bed to minimize pooling of chemotherapy solution in the pelvis. Gravity distribution was maintained for the first 6 hours of the 5-fluorouracil chemotherapy instillation. The dwell time was 23 hours, with a drainage time of 1 hour.

By the intention-to-treat principle, all patients were to receive early postoperative intraperitoneal 5-fluorouracil. However, postoperative bleeding, hemodynamic instability after surgery, or other complications early in the postoperative period sometimes made the early postoperative intraperitoneal 5-fluorouracil difficult or impossible to administer. A requirement for prolonged ventilatory support was not used as an indication to hold the 5-fluorouracil or to discontinue its use. Because of the small number of patients who did not receive early postoperative intraperitoneal chemotherapy and because of postoperative complications, a special assessment of the morbidity and mortality related to early postoperative intraperitoneal chemotherapy use was not attempted.

Systemic chemotherapy after the combined treatments (surgery plus perioperative intraperitoneal chemotherapy) was not recommended for patients whose histological type was disseminated peritoneal adenomucinosis. However, it was recommended for patients with peritoneal mucinous adenocarcinoma.16,17


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Demographic Information
In these 356 patients, the median age was 48 years (range, 29–72 years). Fifty-seven percent of the patients were male. Only 11% of patients had no prior abdominal surgery. The median number of peritonectomy procedures was 4 (range, 3–6). The median number of visceral resections was 2 (range, 0–5). Eleven percent of patients had a temporary ileostomy, 10% had a temporary jejunostomy, and 13% retained a permanent ileostomy. In 59% of patients, the histopathologic diagnosis was disseminated peritoneal adenomucinosis, and 41% it was peritoneal mucinous carcinoma or intermediate type. Five percent of patients had positive lymph nodes. The median length of stay was 21 days (range, 11–82 days). Eighty-nine percent of patients had a completeness of cytoreduction (CC) score of CC-1. There were no CC-0 resections.

Deaths
There were 7 deaths (2.0%) in the group of 356 patients. The causes of death, premorbid conditions, and other associated adverse events in the patients who died are listed in Table 3Go. One patient had a fatal pulmonary embolus, and three patients had sudden unexplained deaths. All seven patients who died underwent autopsy.


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  		TABLE 3. Postoperative mortality in 7 (2.0%) of 356 patients who had cytoreductive surgery and perioperative intraperitoneal chemotherapy for peritoneal surface dissemination of a mucinous appendiceal tumor
 
Overall Morbidity
In the 356 procedures, no adverse events were recorded in 92 (25.8%). There were no grade III or IV adverse events in 213 (59.8%). There were no grade IV adverse events in 288 (81.0%).

Adverse Events by Grade
There were grade III adverse events in 143 procedures. In many of these procedures, there was more than a single grade III adverse event. Figure 1Go displays the grade III adverse events. Line sepsis and urinary tract infection each accounted for 17% of the grade III adverse events. Low hemoglobin between 6.5 and 7.9 g/dl was responsible for 14% of the grade III adverse events.


Figure 1
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  		FIG. 1. Grade III adverse events occurred in 143 (40%) of 356 procedures. Because some procedures had more than a single adverse event, there were a total of 197 grade III adverse events. The incidence of these 197 adverse events is shown

 
In 67 procedures (19%), there was a grade IV adverse event. Some of these patients had more than a single grade IV adverse event in a single procedure. The hematological category accounted for 28% of the adverse events, the gastrointestinal category for 26%, and the cardiovascular category for 16% (Fig. 2Go).


Figure 2
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  		FIG. 2. Grade IV adverse events occurred in 67 (19%) of 356 procedures. Because some procedures had more than a single adverse event, there were a total of 80 grade IV adverse events. The incidence of these 80 adverse events is shown.

 
Grade IV Events Resulting in a Return to the Operating Room
A special study was made of the grade IV events that resulted in a return to the operating room. Overall, 40 procedures (11.2%) required a return to the operating room. The most common, accounting for 29% of reoperations, was fistula. Anastomotic leak caused 19% of the complications that necessitated reoperation. Postoperative bleeding accounted for 18%, and compartment syndrome accounted for 19 % (Fig. 3Go).


Figure 3
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  		FIG. 3. Cause for return to the operating room in 40 procedures (11.2%). The predominant cause for each reoperative procedure is listed.

 
Grade IV Events Not Requiring a Return to the Operating Room
There were 47 grade IV events in 20 procedures (5.6%) that did not require a return to the operating room. The most common grade IV event that did not require a return to the operating room was profound neutropenia with a white blood cell count of <1000 (20%). Respiratory distress that necessitated reintubation with an oral tracheal tube occurred in 14%; 9% were reintubated in the surgical intensive care unit. Nine percent of patients were disoriented and combative and presented with nearly complete deterioration of their mental status (Fig. 4Go).


Figure 4
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  		FIG. 4. Grade IV adverse events that did not require a return to the operating room occurred in 20 (5.6%) of 356 procedures. Because some procedures had more than a single adverse event that did not require a return to the operating room, there were a total of 47 adverse events. The incidence of these 47 adverse events is shown. ARDS, acute respiratory distress syndrome; UTI, urinary tract infection.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
At our institution, the management of peritoneal surface malignancy requires an integration of extensive surgery combined with intraperitoneal chemotherapy administered as a planned part of the surgical event. From a theoretical perspective, only perioperative chemotherapy given into the peritoneal cavity before fibrous entrapment of cancer cells can be expected to eradicate residual microscopic disease present throughout the abdomen and pelvis after cytoreduction.18 It is clear, however, that the effects of this regional chemotherapy are not limited to the peritoneal space. The profound effect that these treatments have on wound healing is supported by the increased incidence of fistula and anastomotic leakage reported to date. Also, the hematological toxicity in up to 20% of patients treated shows that intraperitoneal chemotherapy may have profound systemic manifestations. The immune suppression from neutropenia combined with septic surgical complications can be a lethal series of events.19

This article represents the 10th effort of our group to tabulate adverse events in patients with peritoneal surface malignancy and begin to understand their causes. In 1987, Sugarbaker et al.20 reported on 14 patients who had a curative approach to treatment of malignant pseudomyxoma peritonei. In these 14 patients, there were 5 complications; the most common was postoperative peritonitis, thought to be related to a postoperative accumulation of large volumes of undrained ascites. Sugarbaker and Jablonski21 reported in 1995 on 181 patients treated by cytoreductive surgery and early postoperative intraperitoneal mitomycin C and 5-fluorouracil. There was a 1.5% mortality. Risk was low for postoperative fistula in patients who were free of risk factors (1.8%). However, patients who had intestinal obstruction, prior abdominal or pelvic radiotherapy, or prior intraperitoneal chemotherapy had a 26% (19 of 72 patients) incidence of postoperative fistula. All of these patients had early postoperative intraperitoneal chemotherapy as a planned part of the cytoreductive surgery.

In a further analysis of the risk of postoperative fistula, Murio and Sugarbaker22 studied this problem after cytoreductive surgery and perioperative intra-peritoneal chemotherapy. The clinical features that correlated with fistula formation were preoperative bowel obstruction, prior intra-abdominal chemotherapy or radiotherapy, and cytoreductive surgery as a reoperative event. Fernandez-Trigo and Sugarbak-er23 attempted to critique the management of postoperative gastrointestinal fistula in this group of patients. They advocated a selective approach to treatment based on the postoperative day for diagnosis of the fistula and the extent of peritoneal contamination. In 1993, Esquivel et al.24 studied patients who had induction treatment with systemic mitomycin C and intraperitoneal 5-fluorouracil. They reported a 38% complication rate but no deaths in this group of patients. As a result of these findings, induction intraperitoneal chemotherapy was not recommended unless a minimal cytoreduction was planned.

Jacquet et al.25 in 1996 performed a prospective analysis of morbidity and mortality in 60 patients treated for carcinomatosis by cytoreductive surgery and heated intraoperative intraperitoneal chemotherapy with a closed-abdomen technique. The grade 3 and 4 morbidity was 35%; anastomotic leak and small-bowel perforation were the most common complications. There was a 5% mortality rate. These were the first 60 patients treated with heated intra-operative intraperitoneal chemotherapy at the Washington Cancer Institute and constituted the early part of a learning curve for our institution. Schnake et al.19 in 1999 showed that profound neutropenia associated with cytoreductive surgery resulted in death in most patients. Also in 1999, Stephens et al.26 reported a prospective analysis of 200 patients treated by cytoreductive surgery with intraperitoneal chemotherapy by using an open-abdomen technique whereby the heat and the chemotherapy solution were more uniformly distributed. The overall grade 3 and 4 morbidity was 27%, and pancreatitis (6%) was the most common complication. Morbidity was statistically significantly correlated with the duration of operation, the number of peritonectomy procedures and resections, and the number of suture lines. In Stephens’ study, the mortality was 1.5%.

This study showed little overall change in morbidity and mortality as compared with the Stephens study;26 this reflects a position high on the learning curve for our group for peritoneal surface malignancy treatments for appendiceal mucinous tumors. Newer management plans with diseases such as malignant peritoneal mesothelioma do not show such favorable statistics.27 Other clinical research groups interested in the management of peritoneal surface malignancy have reviewed their data on this subject. In 2001, Elias et al.28 reviewed their experience with 64 patients treated for colorectal carcinomatosis. The postoperative mortality rate was 9.3%, and the morbidity rate was 55%. The most severe complications were seen in patients who required the most extensive surgery. Butterworth et al.29 reported on 11 patients who underwent cytoreductive surgery with intra-peritoneal chemotherapy over a 6-year time period. Their morbidity was 56%, and mortality was 11%. The high morbidity and mortality may relate to a very early experience with this treatment plan by this group. Glehen et al.30 in 2003 collected their experience on 216 consecutive procedures in which cytoreductive surgery was used with closed heated intraoperative intraperitoneal chemotherapy. There were seven deaths (3.2%). The morbidity was 24.5%, and the most frequent complications were digestive fistula (6.5%) and hematological toxicity (4.6%). The morbidity was statistically linked to the extent of carcinomatosis, the duration of operation, and the extent of the resections and peritonectomy procedure. Pilati et al.31 studied 34 patients who had a complete cytoreduction for colon carcinomatosis. They showed a 35% morbidity rate and no mortality. Shen et al.32 reported on 77 patients, with a perioperative morbidity of 30 patients and a 12% mortality rate. Ahmad et al.33 in 2004 reported on 35 cytoreductive procedures, with a 27% major perioperative complication rate and no postoperative deaths. Verwaal et al.34 reported on 102 patients. They showed grade III to V toxicity in 65% of patients and a gastrointestinal fistula rate of 18% (18 patients). Patients with a blood loss exceeding 6 L and three or more anastomoses had a statistically significantly increased postoperative complication rate. The mortality rate in this series was 8%. Schmidt et al.35 had an overall morbidity rate of 34% in their 67 patients. Digestive fistula occurred in nine of these patients; abscess, in five; and postoperative bleeding, in five. The extent of surgery was the main factor affecting the complication rate. The postoperative mortality rate was 4.5%. Recently, Kusamura et al.36 from Milan reported a 12% incidence of morbidity and a .9% incidence of mortality in a consecutive series of 209 procedures involving cytoreductive surgery and heated intraoperative intraperitoneal chemotherapy.

A prospective morbidity/mortality analysis such as this may be of great help to the team managing these complex cases. A regular review of the individual patient assessments can help to maintain a high quality of patient care and lead to changes in management that would optimize a standard operating procedure. For example, this study showed a high incidence of serious urinary tract infections. The Foley catheter in these patients having extensive pelvic peritonectomy is required for a minimum of 10 days. This led to a very high incidence of urinary tract infections, especially in women. A recent new technique for improved catheter drainage may reduce the incidence of urinary tract infection. Also, a high incidence of central venous line infection with the subclavian route was noted. Also, there was an unexpectedly high incidence of thrombosis from the subclavian vein catheter. Currently, all intraoperative central venous monitoring is performed through an intrajugular line to minimize venous thrombosis. This line is removed at 7 days and replaced by a peripheral central line, and this has improved the problem with central venous infection. The anastomotic leak rate and the fistula rate have been diminished by an increased use of diverting ostomy—especially the high diverting jejunostomy when esophagojejunal anastomosis is performed.13 The previous high incidence of grade III pancreatitis (7%) has been reduced to a grade II complication by the conscientious placement of multiple closed-suction drains around the body and tail of the pancreas when an extensive removal of the investing fascia of the pancreas is required by cytoreduction.26

Table 4Go presents data from peritoneal surface malignancy treatment centers in the United States and Europe. The morbidity ranges from 20% to 50%. The mortality varies from 1% to 10%. In our data, for three of the four patients who died suddenly, autopsy did not show a predominant and clear cause for death. Sudden unexplained death was probably from cardiac arrhythmia in this group of patients heavily traumatized by surgery and chemotherapy treatment. Prolonged cardiac monitoring has been initiated in this group of patients.


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  		TABLE 4. Literature review of morbidity and mortality for the treatment of peritoneal surface malignancy
 
The combination of an enteric complication with profound neutropenia was lethal in one of our patients. Patients with hematological toxicity in the absence of a major enteric complication recover their neutrophils well with the help of bone marrow stimulants over the course of 5 to 10 days. Also, patients with an enteric leak often require reoperation, but with early diagnosis, a rapid recovery is expected, possibly with a new ostomy being constructed. However, the combination of enteric leak and grade IV hematological toxicity is very poorly tolerated and often may lead to the patient’s death.

In this study we tried to limit the eligibility requirements to further refine the information that was made available regarding the treatment of carcinomatosis. Only patients with carcinomatosis from appendiceal malignancy were included. Only patients who had a major cytoreduction that was accompanied by heated intraoperative intraperitoneal chemotherapy were included. Colorectal cancer patients, peritoneal mesothelioma patients, and ovarian cancer patients, often treated in the same manner, were excluded. As carcinomatosis treatments become more widely applied, this refinement of the data recorded will allow groups to compare patients and treatments that are more uniform. Rather than all patients treated for carcinomatosis being reported together, the different disease states should in the future be separated. It is possible that there are some differences in the morbidity and mortality rates between appendiceal malignancy with carcinomatosis and colorectal cancer with carcinomatosis. To date, these differences are not clear, but they certainly may exist.

Received for publication March 15, 2005. Accepted for publication December 6, 2005.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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