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In Vivo Model of Pseudomyxoma Peritonei for Novel Candidate Drug Discovery

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In Vivo Model of Pseudomyxoma Peritonei for Novel Candidate Drug Discovery ANTICANCER RESEARCH 29: 4051-4056 (2009) In Vivo Model of Pseudomyxoma Peritonei for Novel Candidate Drug Discovery TERENCE C. CHUA, JAVED AKTHER, PENG YAO and DAVID L. MORRIS Department of Surgery, University of New South Wales, St. George Hospital, Kogarah, Sydney, NSW 2217, Australia Abstract. Pseudomyxoma peritonei (PMP) is a clinical mucinous implants accumulating in the pelvis and condition characterized by diffuse intraabdominal spread of subphrenic regions are often daunting to general surgeons mucinous tumor implants that form on peritoneal surfaces. To (2). Traditional treatments include repeated abdominal complement the efficacy of cytoreductive surgery, an effective lavage of mucin, limited debulking of tumor and systemic cytotoxic drug is required as an intraperitoneal agent for chemotherapy (3). However, these treatments are unable to microscopic cytoreduction locoregionally. To develop a model adequately combat the reaccumulation of mucin that for drug discovery, human pseudomyxoma peritonei tumor characterizes the failure of these treatments. implants consisting of a mixture of mucin and epithelial cells Over the last two decades, cytoreductive surgery and were injected into the peritoneal cavity of CBH/rnu/rnu rats. perioperative intraperitoneal chemotherapy comprising of A fixed quantity of tumor (2 ml) was implanted in each of the hyperthermic intraperitoneal chemotherapy (HIPEC) using 9 male rats. Over 90 days, all rats developed PMP indicating mitomycin C with or without postoperative intraperitoneal that this in vivo animal model may become useful platform in chemotherapy (EPIC) using 5-fluorouracil has emerged to a drug discovery program to allow drug efficacy testing become the standard of care in specialized centers (4, 5). A against human PMP. systematic review reporting the results of this treatment in 10 specialized institutions of 863 patients showed a 5-year Pseudomyxoma peritonei (PMP) is a clinical syndrome that survival ranging between 52 to 96% from the time of is characterised by diffuse spread of intra-abdominal tumor cytoreductive surgery (6). Ten-year overall survival rates implants that follow from the perforation of a mucinous have also been reported to be about 85% (7, 8). The survival appendiceal or ovarian neoplasm (1). These mucinous outcomes of this combined modality treatment is based implants form on the parietal and serosal peritoneum and largely on the concept of locoregional therapy where ranges in its viscosity from purely liquid to a semi-solid like extensive surgery to remove the tumor implants together with texture. The epithelial cells within the mucin proliferate and the administration of heated chemotherapy serves to target results in continuous production of mucin. Despite the microscopic residual disease. extensive intraperitoneal spread of this tumor, it rarely Despite the success of this treatment on prolonging invades into organs and almost never metastasizes through survival, treatment failure is common and is often associated the blood stream or lymphatics. This mucinous material with the grade of the tumor (9). To improve the recurrence- remains intra-abdominally and accumulates to eventually free survival, it is of utmost importance that effective cause severe abdominal distension and anorexia from cytotoxic therapy be developed to complement the surgical compression of the small bowel, which are the main cause procedure. This will reduce the need for repeated treatment of morbidity and mortality in untreated patients. The and the risk of morbidity from subsequent cytoreductive intraoperative findings of extensive carcinomatosis with surgeries. Here, we report the outcomes of our efforts at developing an in vivo PMP model from our laboratory’s drug discovery program. Correspondence to: Professor David L. Morris, Department of Materials and Methods Surgery, University of New South Wales, St. George Hospital, Kogarah, Sydney, NSW 2217, Australia. Tel: +61 02 91132070, Animals. Male CBH/rnu/rnu rats (n=9) weighing between 200-250 Fax: +61 02 91133997, e-mail: [email protected] g were purchased from the Biological Resources Centre of the University of New South Wales and were housed in the PC2 facility Key Words: Pseudomyxoma peritonei, experimental model, at the St. George Hospital. The purchase of the rats and the peritoneal carcinomatosis, intraperitoneal chemotherapy. experimental conduct of this study was approved by the University 0250-7005/2009 $2.00+.40 4051 ANTICANCER RESEARCH 29: 4051-4056 (2009) of New South Wales Animal Ethics Committee (approval no. 06- Histopathological findings. Figure 2 is a representative 114B). The animals were kept under specific pathogen-free histological display of the mucinous tumor obtained from the conditions with free access to autoclaved food and water. rat that is characterized by pools of mucin with strips of cellular tissue of columnar mucinous epithelium with goblet Tumor collection. Three patients with histologically proven PMP consented to retrieval of tumor specimen at the time of operation. cells on the surface of the bowel mucosa. Accompanying Mucinous tumors were collected after a laparotomy but before serosal fibrinous material and minimal acute inflammatory cytoreductive surgery in sterile containers and immediately response to the pool of mucin is also evident in the brought to the animal facility. The tumor was processed under hematoxylin and eosin staining at ×10 magnifications. sterile conditions to remove cellular debris such that the remaining tumor extract contained pure mucin with the Discussion accompanying epithelial cells. Tumor implantation. Nude rats were given buprenorphine (0.01 We demonstrate the feasibility of establishing an in vivo mg/kg) 30 min prior to surgery for pain management. model of pseudomyxoma peritonei in immune-compromised Anaesthesia for surgery was performed using isoflurane. Mini- nude rats which may serve as a platform for drug discovery laparotomy was performed using a lower middle incision of 3 whereby intraperitoneal efficacy of various compounds may cm. Intraperitoneal tumor inoculation was performed by injecting be subjected to in vivo experimenting after proving its effects the patient’s tumor specimen under the right lower quadrant of in vitro. To our knowledge, this model represents the first of the abdomen (1 mL) and the left lower quadrant of the abdomen an animal model for DPAM type PMP, which from our (1 mL). Each patient’s tumor was implanted in three rats. After the procedure the wound was closed by sutures. Animals were institution’s experience accounts for almost 70% of all PMP monitored daily for a maximum of 90 days for the development histological subtypes (10). of intraperitoneal tumor. A previous PMP model was reported by Flatmark et al. (11) using a similar method as reported in this study where Post-mortem. At the end of 90 days, all 9 rats underwent a human tumor tissue were implanted in the peritoneal cavity laparotomy with an extended incision from the xiphisternum to the of nude mice to establish the orthotopic models. In their pelvis. Intraabdominal inspection was performed. Tumors in rats study however, peritoneal mucinous carcinomatosis were obtained and sent for routine histology analysis. The specimens were fixed in 10% buffered formalin, embedded in intermediate (PMCA-I) subtype tumor were used. This paraffin, cut with a microtome to 4 μm and stained with histological subtype is one of three as described by Ronnett hematoxylin and eosin. et al., comprising DPAM, PMCA-I and PMCA. DPAM arises from a low-grade appendiceal mucinous tumor and Results is characterized by widespread peritoneal deposits of abundant pools of extracellular mucin with strips of Patients. Tumor specimens were taken from three patients: proliferative mucinous columnar epithelium with little a 66-year-old female, 72-year-old male, and a 56-year-old cytologic atypia or mitotic activity. This subtype has been male with biopsy-proven pseudomyxoma peritonei arising shown to be the most indolent type of PMP and following from an appendiceal mucinous neoplasm during cytoreductive surgery and perioperative intraperitoneal cytoreductive surgery combined with perioperative chemotherapy, long-term survival with 5-year survival rates intraperitoneal chemotherapy. All patients had extensive between 75% to 90% may be reached (10, 7, 8). PMCA intraperitoneal mucinous tumor with a score of 22, 24 and consists of abundant mucinous epithelium, forming glands 38 on the peritoneal cancer index respectively. All patients and/or signet ring cells and commonly have severe underwent a complete cytoreduction (CC0/1). Final cytological atypia and are poorly differentiated histopathological examination of the tumor from all three architecturally. Histological variants with intermediate patients revealed disseminated peritoneal adeno-mucinosis features of both DPAM and PMCA are termed PMCA- (DPAM). intermediate, which are essentially DPAM but have additional cellular foci containing well differentiated Gross pathological findings. All 9 rats developed visible mucinous carcinoma. Clinical outcome studies following evidence of peritoneal mucinous implants. Tumor implants treatment of this less common group have been shown to were widespread and the distribution in the peritoneal cavity be poorer as compared to patients with DPAM (8, 13-16). included the parietal and serosal peritoneum, small bowel Hence, the use of a DPAM model for biological and mesentry, omentum, paracolic gutters, liver,
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