Multi-institutional experience of diffuse intra-abdominal multicystic peritoneal mesothelioma
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1 Original article Multi-institutional experience of diffuse intra-abdominal multicystic peritoneal mesothelioma T. C. Chua 1,T.D.Yan 1,2, M. Deraco 3,O.Glehen 4,B.J.Moran 5 and P. H. Sugarbaker 6,onbehalf of the Peritoneal Surface Oncology Group 1 University of New South Wales Department of Surgery, St George Hospital, Sydney, and 2 The Baird Institute for Applied Heart and Lung Surgical Research, Newtown, New South Wales, Australia, 3 National Cancer Institute of Milan, Milan, Italy, 4 Hospices Civils de Lyon and Université Lyon, Centre Hospitalier Lyon Sud, Pierre Bénite, France, 5 North Hampshire Hospital, Basingstoke, UK, and 6 Washington Cancer Institute, Washington, DC, USA Correspondence to: Dr T. D. Yan, University of New South Wales Department of Surgery, St George Hospital, Sydney, New South Wales 2217, Australia ( tristan.yan@hotmail.com) Background: This study was undertaken to measure survival of patients with multicystic peritoneal mesothelioma treated by cytoreductive surgery and hyperthermic intraperitoneal chemotherapy through a multi-institutional collaboration. Methods: A multi-institutional data registry, established by the Peritoneal Surface Oncology Group, was used to identify patients with peritoneal mesothelioma and the subgroup with multicystic tumours, treated by cytoreductive surgery and hyperthermic intraperitoneal chemotherapy. Outcomes for this subgroup are reported. The primary endpoint was overall survival. A secondary endpoint was the incidence of treatment-related complications. Results: Of 405 patients with peritoneal mesothelioma, 26 (6 4 per cent) had multicystic tumours. There were 20 women and six men with a mean(s.d.) age of 42(12) years. The median peritoneal carcinomatosis index (PCI) was 14 (range 6 39). There was no perioperative mortality. Six patients developed grade III or IV complications. After a median follow-up of 54 (range 5 129) months, all 26 patients were still alive. Conclusion: Multicystic peritoneal mesothelioma appears to be a distinct subtype of peritoneal mesothelioma, where long-term survival may be achieved through cytoreductive surgery and hyperthermic intraperitoneal chemotherapy. Paper accepted 22 July 2010 Published online 24 September 2010 in Wiley Online Library ( DOI: /bjs.7263 Introduction Peritoneal mesothelioma accounts for approximately onethird of all mesothelioma, the greater proportion occurring in the pleura 1. Recognized histological variants are epithelioid and sarcomatoid mesothelioma 1. Intermediate variants where the tumour possesses both epithelioid and sarcomatoid features are known as biphasic mesothelioma 1. Together, these three variants account for the majority of mesothelioma. There remains a distinct variant of mesothelioma that is non-epithelioid and non-sarcomatoid, of which the multicystic lesion has been most commonly described. To date, there are about 100 case reports of multicystic mesothelioma. This lesion is rarely seen in the thorax; there are only two reported patients with multicystic mesothelioma arising from the pleura 2,3. Multicystic mesothelioma is thought to be unrelated to asbestos exposure. Patients often have a history of previous surgery, pelvic inflammatory disease or endometriosis, suggesting that chronic peritoneal irritation might be a precipitating stimulus 1,4. The rarity of the condition has led to difficulties in understanding the clinical behaviour of this tumour and the optimal approach to treatment. There is no unanimous agreement whether this is a benign or malignant condition 5. Accumulating sufficient patients to compile a representative series to guide clinical practice is unlikely to be possible. A multi-institutional data registry on peritoneal mesothelioma was therefore established during the Sixth Peritoneal Surface Oncology Meeting in Lyons in November This study aimed to report the clinical outcome of multicystic peritoneal mesothelioma as a subgroup analysis from this registry, with a focus 2010 British Journal of Surgery Society Ltd British Journal of Surgery 2011; 98: 60 64
2 Multicystic peritoneal mesothelioma 61 on survival following radical surgical cytoreduction and locoregional chemotherapy. Methods Ethics approval was obtained from institutional review boards or local ethics committees of participating institutions for waiver of patient consent for this anonymized study. Of patients with peritoneal mesothelioma identified between October 1989 and February 2009, those with a histological diagnosis of multicystic peritoneal mesothelioma treated by cytoreductive surgery (CRS) followed by hyperthermic intraperitoneal chemotherapy (HIPEC) with or without early postoperative intraperitoneal chemotherapy (EPIC) were included in this study. Exclusion criteria were peritoneal mesothelioma secondary to pleural mesothelioma and extra-abdominal metastasis identified during preoperative investigations. Standardized clinical data on consecutive patients from each institution were entered into a central database. Follow-up data from most recent reviews included clinical examination and assessment of abdominopelvic computed tomography scans. Each institution confirmed that the pooled data represented consecutive operative procedures performed in the study period by participating surgeons. An anonymized data form was created to retrieve relevant information on clinical data (age, sex, date of surgery, extent of previous surgical intervention and performance status), pathological data (histopathological subtype, presence of lymph node metastasis, presence of extra-abdominal metastasis, Peritoneal Cancer Index (PCI), completeness of cytoreduction) and treatmentrelated data (use of HIPEC with or without EPIC; duration of surgery; presence of cardiac, respiratory, gastrointestinal, renal and haematological morbidity; presence of grade III or IV toxicity according to National Cancer Institute Common Toxicity Criteria; duration of hospital stay; and use of pemetrexed-based combination chemotherapy). The volume and extent of the tumour deposits were recorded prospectively using the PCI 6. This combines lesion size (0 to 3) with tumour distribution (regions 0 to 12), to quantify the extent of disease as a numerical score (ranging from 0 to 39) 6. Peritonectomy was performed only at the sites of disease involvement with intent to remove all intraperitoneal tumour deposits together with involved peritoneum. CRS was performed as described previously 7. In short, peritonectomy procedures included total anterior parietal peritonectomy, omentectomy with splenectomy, right and left subphrenic peritonectomy, pelvic peritonectomy, and lesser omentectomy with cholecystectomy 7. The sites and volumes of residual disease following CRS were recorded prospectively using the completeness of cytoreduction (CC) score 6 : CC-0, no visible evidence of disease; CC-1, residual tumours less than 2 5 mm in diameter; CC-2, residual tumours between 2 5 mm and 2 5 cm in diameter; CC-3, residual tumours over 2 5 cm in diameter or a confluence of tumour nodules present at any site. Statistical analysis All patients who underwent cytoreduction, irrespective of the completeness of cytoreduction or perioperative intraperitoneal chemotherapy regimen, were analysed on an intention-to-treat basis. Values are given as mean(s.d.) unless stated otherwise. Perioperative mortality was defined as any death that occurred during the same hospital admission or within 30 days after surgery. Perioperative mortality was included in the overall survival analysis. Overall survival was used as the primary endpoint, and was determined from the date of surgery. Survival analysis was performed by means of the Kaplan Meier method, with statistical comparison using the log rank test. P < was considered statistically significant. All statistical analyses were performed using SPSS for Windows version 17.5 (SPSS, Munich, Germany). Results Between October 1989 and February 2009, 405 patients were included in the multi-institutional peritoneal mesothelioma database. Of these, 26 (6 4 per cent) had multicystic peritoneal mesothelioma diagnosed during operation or at previous surgery and underwent CRS with HIPEC. The mean age at the time of CRS was 42(12) years. There were 20 women and six men. Twelve had undergone previous operations. Data on previous treatments were unknown in 14 patients. The median PCI was 14 (range 6 39), with a mean of 17(9). Nineteen patients had CC-0 cytoreduction, five had CC-1 and two CC-2. All patients had localized regional disease within the peritoneal cavity, with no evidence of lymph node, extraperitoneal or visceral metastasis. No patient received pemetrexed-based combination chemotherapy. All patients received HIPEC with cisplatin (50 mg/m 2 ) with or without doxorubicin (15 mg/m 2 ). Doxorubin was used as part of the HIPEC regimen in 22 patients. All HIPEC procedures were performed during surgery
3 62 T. C. Chua, T. D. Yan, M. Deraco, O. Glehen, B. J. Moran and P. H. Sugarbaker Fig. 1 Representative computed tomography scan demonstrating thin-walled cystic structures located within the pelvis after CRS, but with variations in exposure techniques (open or closed), drugs used, duration ( min) and intraperitoneal temperature (40 43 C). Three patients received EPIC with paclitaxel (20 mg per m 2 per day) between 1 and 5 days after surgery. The mean duration of operation was 9(2) h. Four patients had packed-cell transfusions of more than 5 units. Overall, seven patients developed postoperative complications of which six had grade III or IV complications. Grade III/IV complications were not associated with any clinicopathological or treatment factors. There were no perioperative deaths. The median length of hospital stay was 15 (range 9 42) days. All patients complied with arrangements for follow-up. The median follow-up time was 54 (range 5 129) months with a mean of 53(34) months. At the time of last a Thin-walled cyst b Omentum replaced by cysts c Dissection d Surgical specimen Fig. 2 Intraoperative demonstration of multicystic peritoneal mesothelioma: a thin-walled cyst structure arising from the anterior parietal peritoneum/peritoneum of the anterior abdominal wall, b omentum extensively replaced by cysts, c dissection of diseased omentum including cysts and d surgical specimen demonstrating cysts of various sizes excised using peritonectomy procedures
4 Multicystic peritoneal mesothelioma 63 follow-up, all patients were alive. Twenty-five had no evidence of disease and one patient was alive with disease. Kaplan Meier analysis was not possible, but 12 patients have survived for more than 5 years. No clinicopathological or treatment-related variables were associated with survival. Discussion Multicystic peritoneal mesothelioma, first described in , is considered an extremely rare tumour. Most of the evidence in the published literature comes from case reports. The aetiology remains unknown, unlike that of the more common malignant peritoneal mesothelioma, where asbestos exposure is important 9. Simian virus 40, a DNA virus that blocks tumour suppressor genes, is also relevant, leading to atypical mesothelial proliferation and superficial non-invasive lesions of the mesothelium contributing to mesotheliomagenesis 10,11. Simplistically, multicystic peritoneal mesotheliomas are thought to develop as a result of peritoneal reactive proliferation secondary to previous intra-abdominal surgery, trauma, infection or endometriosis. The condition is characterized by the presence of single or multiple thin-walled translucent cysts filled with mucinous or gelatinous fluid involving the peritoneal surfaces of intra-abdominal viscera and the parietal peritoneum (Figs 1 and 2). Microscopically, the cysts are multilocular, thin-walled, and lined by a single layer of attenuated or cuboidal mesothelial cells with or without cytological atypia. Accompanying features include hyaline fibrous septa that may contain foci of inflammatory cellular infiltrates and granulation tissue. Symptoms commonly include non-specific abdominal pain, pelvic pain, dyspareunia, hernia, early satiety and constipation. In severe cases, this disease leads to severe pain, bowel obstruction and cachexia. Clinical behaviour, however, usually follows a benign course. Recurrences following surgical debulking are common, and may become an eventual contributor to treatment failure and mortality. This contrasts to diffuse malignant peritoneal mesothelioma where there is a propensity for both direct peritoneal spread and lymphatic dissemination 1,12. The present study indicates that long-term disease control and survival is possible in this distinct disease entity by treatment with CRS and HIPEC. All patients had moderate amounts of peritoneal disease (median PCI 14), often considered to represent disseminated intraabdominal metastases where treatment should be directed towards palliation. After CRS and HIPEC, all patients remained alive after a median follow-up of 4 5 years. Exploratory analysis of clinical and treatment-related data showed no association with survival. Given that recurrences are frequent in patients who undergo standard debulking operations 8,13,14, CRS combined with HIPEC in the present study seems to have provided good disease control. This management option appears to be associated with greater morbidity than standard debulking operations and its application in a benign condition may be controversial. As long-term disease control is achieved, however, it seems worthwhile subjecting fit individuals to this combined procedure to achieve the best chance of cure. Despite having an indolent nature, disease invariably recurs or persists if treated inadequately and this was the case in 12 patients in this series who had previously undergone surgery before being treated with CRS and HIPEC. More importantly, in patients who are untreated or inadequately treated, there is a possibility of developing invasive disease as a result of chronic cellular changes that might lead to malignant transformation 15,16. The success of this treatment must be emphasized given its role in other indolent disease processes such as pseudomyxoma peritonei 17. It remains debatable whether debulking surgery should be the first-line treatment, with CRS and HIPEC reserved as a second-line option given its potential morbidity. This controversy is unlikely to be resolved without a prospective comparison of treatments and this is surely not feasible given the rarity of this condition. Contributors Members of the Peritoneal Surface Oncology Group are: T. C. Chua, T. D. Yan and D. L. Morris (University of New South Wales Department of Surgery, St George Hospital, Sydney, Australia), M. Deraco, D. Baratti and S. Kusamura (National Cancer Institute of Milan, Milan, Italy), D. Elias (Institut Gustave Roussy, Villejuif, France), O. Glehen and F. N. Gilly (Hospices Civils de Lyon and Université Lyon, Centre Hospitalier Lyon Sud, Pierre Bénite, France), E. A. Levine and P. Shen (Wake Forest University, Winston-Salem, North Carolina, USA), P. H. Sugarbaker (Washington Cancer Institute, Washington, DC, USA), B. J. Moran and F. Mohamed (North Hampshire Hospital, Basingstoke, UK), G. Glockzin and P. Piso (University Medical Centre, Regensburg, Germany). Acknowledgements The authors thank all individual members from various institutions who together as part of the Peritoneal Surface Oncology Group International contributed to the multi-institutional peritoneal mesothelioma database. For
5 64 T. C. Chua, T. D. Yan, M. Deraco, O. Glehen, B. J. Moran and P. H. Sugarbaker information on the Peritoneal Surface Oncology Group International, see com/index.html. The authors declare no conflict of interest. References 1 Attanoos RL, Gibbs AR. Pathology of malignant mesothelioma. Histopathology 1997; 30: Haraguchi S, Koizumi K, Kawamoto M, Tanaka S. Video-assisted thoracoscopic excision of a benign cystic mesothelioma of pleura. Jpn J Thorac Cardiovasc Surg 1998; 46: Umezu H, Kuwata K, Ebe Y, Yamamoto T, Naito M, Yamato Y et al. Microcystic variant of localized malignant mesothelioma accompanying an adenomatoid tumor-like lesion. Pathol Int 2002; 52: Kannerstein M, Churg J. Peritoneal mesothelioma. Hum Pathol 1977; 8: Ross MJ, Welch WR, Scully RE. Multiocular peritoneal inclusion cysts (so-called cystic mesothelioma). Cancer 1989; 64: Jacquet P, Sugarbaker PH. Clinical research methodologies in diagnosis and staging of patients with peritoneal carcinomatosis. Cancer Treat Res 1996; 82: Sugarbaker PH. Peritonectomy procedures. Ann Surg 1995; 221: Mennemeyer R, Smith M. Multicystic, peritoneal mesothelioma: a report with electron microscopy of a case mimicking intra-abdominal cystic hygroma (lymphangioma). Cancer 1979; 44: Boffetta P. Epidemiology of peritoneal mesothelioma: a review. Ann Oncol 2007; 18: Robinson BWS, Lake RA. Advances in malignant mesothelioma. NEnglJMed2005; 353: Shivapurkar N, Harada K, Reddy J, Scheuermann RH, Xu Y, McKenna RW et al. Presence of simian virus 40 DNA sequences in human lymphomas. Lancet 2002; 359: Averbach AM, Sugarbaker PH. Peritoneal mesothelioma: treatment approach based on natural history. Cancer Treat Res 1996; 81: Hutchinson R, Sokhi GS. Multicystic peritoneal mesothelioma: not a benign condition. Eur J Surg 1992; 158: Cusatelli P, Altavilla G, Marchetti M. Benign cystic mesothelioma of peritoneum: a case report. Eur J Gynaecol Oncol 1997; 18: DeStephano DB, Wesley JR, Heidelberger KP, Hutchinson RJ, Blane CE, Coran AG. Primitive cystic hepatic neoplasm of infancy with mesothelial differentiation: report of a case. Pediatr Pathol 1985; 4: González-Moreno S, Yan H, Alcorn KW, Sugarbaker PH. Malignant transformation of benign cystic mesothelioma of the peritoneum. J Surg Oncol 2002; 79: Sugarbaker PH. New standard of care for appendiceal epithelial neoplasms and pseudomyxoma peritonei syndrome? Lancet Oncol 2006; 7:
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