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10.1245/s10434-006-9182-x
Annals of Surgical Oncology 14:484-492 (2007)
© 2007 Society of Surgical Oncology
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Original Article

A Systematic Review on the Efficacy of Cytoreductive Surgery and Perioperative Intraperitoneal Chemotherapy for Pseudomyxoma Peritonei

Tristan D. Yan, BSc (Med) MBBS1, Deborah Black, BSc DipEd MStat PhD2, Renaldo Savady, MD1 and Paul H. Sugarbaker, MD1

1 Peritoneal Surface Malignancy Program, Washington Cancer Institute, Washington Hospital Center, 106 Irving Street, NW, Suite 3900N, Washington, DC 20010, USA
2 School of Public Health and Community Medicine, The University of New South Wales, Sydney, Australia

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


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: The efficacy of cytoreductive surgery (CRS) combined with perioperative intraperitoneal chemotherapy (PIC) for patients with pseudomyxoma peritonei (PMP) remains to be established.

Methods: Searches for all relevant studies prior to March 2006 were performed on six databases. Two reviewers independently appraised each study using a predetermined protocol. The quality of each study was assessed. Clinical effectiveness was synthesized through a narrative review with full tabulation of results of all included studies.

Results: Ten most recent updates from each institution were included for appraisal and data extraction. There were no randomized controlled trials or comparative studies. All included articles were observational studies without control groups. Five studies were relatively large series (n≥100). Two studies had relatively long-term follow-up (48 months and 52 months). The median follow-up in the remaining eight studies was shorter than 3 years (range 19–35 months). The median survival ranged from 51 to 156 months. The 1-, 2-, 3- and 5-year survival rates varied from 80 to 100%, 76 to 96%, 59 to 96% and 52 to 96%, respectively. The overall morbidity rate varied from 33 to 56%. The overall mortality rates ranged from 0 to 18%.

Conclusions: This study reviewed current evidence on CRS and PIC for PMP. Only observational studies were available for evaluation, which demonstrated some promising long-term results, as compared to historical controls. Due to the rarity of this disease, a well-designed prospective multi-institutional study would be meaningful.

Key Words: Pseudomyxoma peritonei • Cytoreductive surgery • Intraperitoneal chemotherapy • Appendiceal neoplasms • Systematic review


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Pseudomyxoma peritonei (PMP) originates mostly from appendiceal epithelial neoplasms and is characterized by mucinous ascites.1–3 This clinicopathologic entity has a unique natural history. Initially the primary tumor enlarges, obstructs the narrow lumen of the appendix, and subsequently this leads to appendiceal perforation.2,3 This event allows mucin producing neoplastic cells to gain access to the free peritoneal cavity. The majority of these tumors are minimally aggressive, so that they rarely cause lymphatic or hematogenous metastases. They do not invade but tend to remain confined within the peritoneal cavity.2,3 As the disease progresses, copious mucinous tumors accumulate at the sites of peritoneal fluid absorption and in the gravity-dependent areas, such as pelvis and retrohepatic space. However, continuous peristaltic movement of the small bowel minimizes tumor implantation on its surface. Most patients undergo an indolent disease process and can remain asymptomatic for a number of years. Eventually, the patients develop terminal starvation because of abdominal distension and increased tumor volume.2

The conventional approach to PMP is surgical debulking repeated as necessary to alleviate pressure effects.4–6 However, this treatment is not definitive and the disease is always left behind in and around lesser sac, root of mesentery and pelvis. Recurrence or disease progression in these areas will eventually cause gastric outlet obstruction, small bowel obstruction, or pelvic outlet obstruction. When repeated surgery is performed to resolve obstructive symptoms, it is associated with increased risks of bowel injury and fistula formation, due to progressively thickened intra-abdominal adhesions encasing the small bowel and mesentery.1,2 Eventually patients managed by repeated surgical debulking die from intestinal obstruction, terminal starvation and/or surgical complications.2

Sugarbaker1,7 proposed a definitive treatment option, which combines cytoreductive surgery (CRS) with perioperative intraperitoneal chemotherapy (PIC). The rationale of this comprehensive locoregional approach is to use CRS to remove all visible tumors, with lysis of adhesions between the bowel loops. This allows intraperitoneal chemotherapy to gain direct contact with any residual tumor cells. The combined modality of the physical and chemical cytoreductions is ideally suited for diseases such as PMP, which is confined within the peritoneal cavity.7–9

In April 2004, Bryant et al.10 conducted a systematic review of the Sugarbaker procedure for PMP derived from benign appendiceal mucinous neoplasms. The study included 382 patients and was based on five retrospective reports from three centers.10 However, subsequent to this report there are an increased number of publications on CRS and PIC. Also as experience in this treatment strategy has increased, it has become necessary to demonstrate efficacy not only for benign appendiceal mucinous tumors, but also for peritoneal mucinous carcinomatosis or high grade peritoneal mucinous adenocarcinoma.6,11 After April 2004, eight centers have published an update allowing 863 PMP patients to be evaluated. This study was aimed to provide a systematic review on the current evidence available for the comprehensive treatment regimens for PMP.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Literature Search Strategy
A computer-assisted search in Medline, Pubmed, EMBASE, Cochrane Central Resister of Controlled Trials (CCTR), Cochrane Database of Systematic Reviews (CDSR) and Database of Abstracts of Review of Effectiveness (DARE) covering the period from January 1966 to March 2006 was performed in March 2006 to identify published peer-reviewed medical journals on CRS and PIC for PMP. The reference lists of all retrieved articles were reviewed for further identification of potentially relevant studies. Finally, expert academic surgeons in Washington, DC, USA were asked whether they knew about any important unpublished data. All relevant articles identified were assessed with application of inclusion and exclusion criteria.

Inclusion Criteria
All the participants had a diagnosis of PMP, which was defined clinically on the basis of intraoperative findings as localized or generalized accumulation of mucinous tumors in the peritoneal cavity. PMP included were originated from appendiceal epithelial neoplasms or ovarian neoplasms.

Studies using the combined treatment modality of CRS and PIC as described by Sugarbaker7 were included. CRS consisted of peritonectomy procedures (anterior parietal peritonectomy, omentectomy+splenectomy, right and left subphrenic peritonectomy, pelvic peritonectomy, and lesser omentectomy with stripping of the omental bursa+cholecystectomy) and visceral resections (rectosigmoidectomy, right colectomy, total abdominal colectomy, hysterectomy and small bowel resection).

PIC regimens included intraperitoneal hyperthermic chemotherapy (IPHC) and/or early postoperative intraperitoneal chemotherapy (EPIC) within 7 days of surgery. Intraperitoneal chemotherapy used in the operating room with hyperthermia has been referred to by many different nomenclatures: continuous hyperthermic peritoneal perfusion (CHPP); heated intraoperative intraperitoneal chemotherapy (HIIC); hyperthermic intraperitoneal chemotherapy (HIPEC) or intraperitoneal hyperthermic chemotherapy (IPHC). In this review, IPHC was the designated terminology.

Experimental and observational studies were searched for inclusion. Studies were classified into four levels of evidence—level 1 evidence: randomized controlled trials (RCTs); level 2 evidence: controlled clinical trials; level 3 evidence: controlled observational studies; or level 4 evidence: observational studies without control groups. Studies with survival, disease status, morbidity and mortality, or quality of life as an end-point were included. All studies selected were human trials and in English language.

Exclusion Criteria
Studies reporting the effectiveness of surgical debulking alone for PMP were excluded. Studies reporting the effectiveness of CRS and PIC for peritoneal surface malignancy, without specific documentation of PMP or that included other peritoneal carcinomatosis when reporting aggregate outcomes were excluded. Intra-peritoneal chemotherapy performed more than 7 days after surgery were excluded. Abstracts, editorials and expert opinions were excluded.

Data Extraction and Critical Appraisal
Two reviewers independently appraised each included article, using a critical review checklist consisting of representativeness of sample, explicitness of inclusion criteria, similarity of disease progression at the time of treatment, adequacy of follow-up, objectivity of outcome measures and sub-series analysis, as recommended by the National Health Service Center for Reviews and Dissemination case series quality assessment criteria (University of York).12

All data were extracted from the relevant articles’ texts, tables and figures. The outcomes were selected for presentation if reported in more than one trial and they included survival, disease status, morbidity, mortality, blood loss, operation duration, hospital stay, prognostic factors, and quality of life. A meta-analysis was not appropriate because all studies lack a comparator. Clinical effectiveness was synthesized through a narrative review with full tabulation of results of all included studies. Discrepancies between the two reviewers were resolved by discussion and consensus. The final results were checked by the senior author.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Quantity of Evidence
Abstracts of 598 publications were identified through searching the electronic database. Initial evaluation of these abstracts identified 97 potentially relevant publications. Manual search of the reference lists identified further six potentially relevant publications. Experts in peritoneal surface oncology identified three additional recent studies. When the inclusion and exclusion criteria were applied to all 106 publications, 37 articles remained for assessment (Table 1Go).11,13–48 Serial publications reporting accumulating numbers of patients or increased length of follow-up were identified. Ten most recent or complete update(s) from eight institutions were included for appraisal and data extraction (Table 2Go).30,31,35,36,40,42,44,46–48 Two studies had survival as the primary outcome measures30,36; two studies had morbidity and mortality as primary outcome measures31,35; the remaining six studies documented both survival and morbidity and mortality outcome measures.40,42,44,46–48


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  		TABLE 1. Summary of outcomes presented in relevant publications of cytoreductive surgery combined with perioperative intraperitoneal chemotherapy for pseudomyxoma peritonei
 

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  		TABLE 2. Literature review of most recent updates on cytoreductive surgery (CRS) combined with perioperative intraperitoneal chemotherapy (PIC) for pseudomyxoma peritonei
 
Quality of Evidence
There were no randomized controlled trials or comparative studies found. All ten included articles were observational studies without control groups and were classified as level 4 evidence.30,31,35,36,40,42,44,46–48

All reports originated from specialized tertiary referral centers.30,31,35,36,40,42,44,46–48 Overall 863 PMP patients were included for assessment. Five studies were relatively large series (n≥100)30,31,35,36,40 and the remaining five series had fewer than 100 patients.42,44,46–48 Four studies reported PMP originating from appendiceal epithelial neoplasms exclusively.30,31,40,48 Another four studies reported PMP originating mainly from appendiceal epithelial neoplasms, representing 86–97% of their sample population.35,36,42,46 In the remaining two studies the origin(s) of PMP could not be ascertained.44,47 One study included patients diagnosed with PMP and appendiceal non-mucinous peritoneal carcinomatosis, adenocarcinoid and carcinoid appendiceal tumors, therefore not representative of target population.40 The remaining nine studies included patients diagnosed with PMP only.30,31,35,36,42,44,46–48 However, in all nine studies no indication of representativeness of sample was provided.30,31,35,36,42,44,46–48

Seven studies used explicit priori inclusion criteria.31,35,36,40,44,46,48 All studies included patients at different points in their disease progression.30,31,35,36,40,42,44,46–48 For treatment of PMP to be considered effective, follow-up of 10 years would be preferred. However, due to rarity of this disease, only two studies had a relatively long-term follow-up (48 months and 52 months).30,36 The median follow-up in the remaining eight studies was shorter than 3 years (range 22–35 months).31,35,40,42,44,46–48 All 10 studies were judged unclear on adequacy of follow-up.30,31,35,36,40,42,44,46–48 Death or alive, morbidity and mortality were objective outcome measures. Blinding was not documented. Nine studies attempted to analyze the data according to significant prognostic variables.30,31,35,36,40,42,44,46,48 However, it was not clear if there was sufficient distribution of prognostic factors.30,31,35,36,40,42,44,46,48

Assessment of Survival
Effectiveness of CRS and PIC on survival is demonstrated in Table 3Go.30,36,40,42,44,46–48 The median survival ranged from 51 to 156 months.30,40,42 The median survival was not reached at the last time of contact in the remaining studies.36,44,46–48 The 1-, 2-, 3- and 5-year survival rates varied from 80 to 100%, 76 to 96%, 59 to 96% and 52 to 96%, respectively.30,36,40,44,46–48 One study reported 10-year survival of 55%.30


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  		TABLE 3. Effectiveness of cytoreductive surgery combined with perioperative intraperitoneal chemotherapy for pseudomyxoma peritonei
 
Assessment of Recurrence
Effectiveness of CRS and PIC on recurrence is demonstrated in Table 3Go.30,36,44 Three studies documented disease status.30,36,44 At the completion of the study, 47–74% of patients had no evidence of disease, 5–15% of patients were alive with disease, and 0–32% of patients died of disease.30,36,44

Assessment of Perioperative Outcomes
Effectiveness of CRS and PIC on perioperative outcomes is demonstrated in Table 4Go. 31,35,40,42,44,46–48 The overall morbidity rate varied from 33 to 56%.31,35,40,42,44,46–48 Hematological toxicity rate varied from 4 to 9%.31,40,44 Blood loss ranged from 2100 to 8000 cm3.35,42 Mean operation duration ranged from 6.0 to 12.6 h.40,42,44,48 Reoperation rates for postoperative adverse events were 11 and 21% as reported in two studies.31,42 The overall mortality rates ranged from 0 to 18%.31,35,42,44,46–48 The median and mean hospital stay ranged from 16 to 21 days31,35,46 and 26 to 29 days42,48, respectively.


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  		TABLE 4. Morbidity and mortality of cytoreductive surgery combined with perioperative intraperitoneal chemotherapy for pseudomyxoma peritonei
 
Assessment of Quality of Life
No studies were identified focusing on the quality of life after CRS and IPHC for PMP alone. Two studies by McQuellon et al.38,39 reported the short-term and long-term quality of life outcomes in patients who underwent CRS and IPHC for peritoneal carcinomatosis, including PMP as a subset of the study population. They found that 64 patients in the short-term study decreased overall quality of life after surgery compared with baseline, but then returned to baseline or better within 3–6 months of surgery.38 A follow-up study of seventeen 3-year-survivors demonstrated that more than 90% of patients had minimal to no limitations of activity and had functional assessments that compared favorably to national reference values for their respective age groups.39


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
In the past, it was thought that PMP was a benign disease process and patients were treated with surgical debulking with evacuation of ascites.4–6 However, accurate historical controls of uniformly treated patients are not available, partly due to the rarity of the disease. In 1994, Gough et al.4 reported a 10-year survival of 32% in 56 PMP patients who underwent serial debulking procedures and selectively treated with intraperitoneal radiotherapy or chemotherapy between 1957 and 1983. In 2005, Miner et al.5 reported a 10-year survival of 21% in 97 PMP patients who were treated with serial debulking, systemic chemotherapy and/or delayed intermittent intraperitoneal 5-fluorouracil over a 22-year period. These reports demonstrated that serial debulking surgery with various adjuvant therapies may prolong survival, achieving a long-term survival of 20–30%. Some would support the use of this traditional approach. Although a subset of these patients may remain asymptomatic for many years, the disease almost always recurs and patients often re-present with gastrointestinal obstructive symptoms, commonly caused by the build-up of mucus or postoperative intra-abdominal adhesions. Over time each repeated debulking procedure becomes more ineffective and sometimes more dangerous due to the risk of bowel injury and subsequent fistula formation.2,10 In addition, in some patients the disease may not remain indolent throughout its clinical course. Yan et al.25 showed that some patients underwent transitions from a less aggressive to a more aggressive histopathologic type over time and with repeated surgical interventions.

Sugarbaker proposed a comprehensive treatment approach involving CRS and PIC.1,7 CRS is used to maximally remove any peritoneal tumors together with complete lysis of adhesions between the bowel loops. This is followed by adjuvant intraperitoneal chemotherapy. The timing and route of the chemotherapy delivery are critical, as it is given before the formation of any adhesions and it allows direct chemotherapy and tumor-cell contact, without necessarily increasing systemic toxicity.8,9 Hyperthermia has been shown to potentiate chemotherapy penetration and cytotoxic effects.49,50 Most recent updates by Sugarbaker et al.30 demonstrated a median survival of 156 months and 5- and 10-year survival of 72 and 55% in 501 PMP patients who underwent CRS and PIC. In this study, the uniform treatment approach using CRS combined with PIC has shown improved 10-year survival, as compared with historical controls.

The strong treatment rationales and promising results have led to establishment of numerous international treatment centers in the USA and in nearly all countries in Europe, especially in the last 10 years. However, the results of CRS and IPHC for PMP should be interpreted with cautions due the several reasons. First, surgical interventions may vary among institutions, due to level of experience and surgeons’ techniques. Second, number of patients and length of follow-up in some of the studies may not be adequate to confidently predict long-term survival. Third, results of CRS combined with IPHC versus serial debulking should be interpreted with knowledge that these treatment strategies have not been compared directly. A phase III trial would be ideal. However, it will be difficult to do in the current setting because they would need to compare a potentially curative treatment option with a palliative procedure, thus patients are not likely to accept randomization. Also it may not be practical, as a sufficient number of patients and a long-term follow-up of at least 10 years are required to demonstrate statistical differences. However, the fact that RCTs are difficult to perform should not constitute a plea against randomization. Further data from a randomized trial in a multi-institutional setting to clarify the efficacy of IPHC would be desirable. The optimal study would be randomizing patients to CRS with IPHC versus CRS without IPHC after complete cytoreduction.

In the United States, 28 treatment centers currently perform CRS and PIC for peritoneal surface malignancy. In the UK, CRS combined with PIC has become a part of the healthcare system. In 1994, Moran et al.51 initiated their treatment program in Basing-stoke and have performed the combined treatment for 85 PMP from appendiceal tumors in their most recent report. A second treatment center was established in 2002 in Manchester due to increased demand. In Holland, CRS and IPHC has become the standard of care for PMP and The Netherlands Cancer Institute is performing 50 cytoreductions every year. In Sydney, Australia the number of PMP patients referred for CRS and PIC increased four folds in the last 2 years and at any given time there are 20–30 patients on the waiting list and the waiting time for surgery is up to 6 months.

Pseudomyxoma peritonei has a unique natural history. A new standard of care is now available.1 This clinicopathologic entity should be regarded as a stand-alone disease. As more patients are treated in this uniform manner, meaningful histopathologic assessment and identification of prognostic parameters are made possible. CRS and PIC are associated with moderate to high morbidity and morality rates and clearly, careful selection of patients who are most likely to benefit from this combined treatment is utmost important. Ronnett et al.11 reviewed histopathologic features of 109 patients who underwent CRS and PIC for PMP by a single surgeon. They found that there is an increased invasiveness in histopathology in this disease, ranging from the lower end of the spectrum–diffuse peritoneal adenomucinosis (DPAM), to the upper end of the spectrum–peritoneal mucinous carcinomatosis (PMCA). The differences in histopathology determined the prognosis of these patients.11,26 Poorly differentiated PMCA may behave similarly to colorectal carcinoma in their patterns of local invasion and systemic spread.26,36 These patients often have a rapidly progressive clinical course.

However, confusion still exists regarding the histopathologic nomenclature for this disease. In earlier classifications of appendiceal neoplasms, numerous designations were used, such as malignant mucoceles, colloid carcinoma, cystadenoma and cystadenocarcinoma, etc. In a recent study by Misdraji et al.,6 a different histopathologic classification was proposed. They classified the appendiceal mucinous tumors into low-grade appendiceal mucinous neoplasms (LAMN) and high-grade mucinous adenocarcinomas (MACA). However, in this study, follow-up data were available only in 66 of 107 patients and patients underwent variety of treatments by different surgeons over a 50-year period. The procedures performed in these patients were mainly appendectomy with or without serial debulking procedures. Thirty of the 66 patients with follow-up data had disease confined in the appendix and seven patients had localized peritoneal disease involving the ovary or the fallopian tube.6

In the present systematic review, nearly all institutions performing CRS and PIC used Ronnett criteria for PMP classification and they all demonstrated patients with PMCA had a less favorable prognosis.30,36,40,44,46,48 Although much progress has been made, greater knowledge regarding the histopathology of this disease and the surgical implications of these findings are needed. Perhaps a prospective multi-institutional trial is indicated to standardize the histopathologic classification for pseudomyxoma peritonei. We suggest that Ronnett criteria should be further clarified to create a standardized nomenclature for treatment centers performing CRS and PIC. Other factors such as extent of prior surgery, lymphatic or hematogenous metastases, and completeness of cytoreduction will be potentially important stratification parameters for patients with pseudomyxoma peritonei.

In conclusion, this study reported current data on CRS and PIC for PMP. Only observational studies were available for evaluation, which demonstrated some promising long-term results, as compared to the historical controls.


   ACKNOWLEDGMENTS
 
Tristan D. Yan, a surgical oncology research fellow, is supported by Foundation for Applied Research in Gastrointestinal Oncology and Medstar Research Institute.

Received for publication June 10, 2006. Accepted for publication June 14, 2006.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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