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Outcomes in Peritoneal Dissemination from Signet Ring Cell Carcinoma of the Appendix Treated with Cytoreductive Surgery and Hyperthermic Intraperitoneal Chemotherapy

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Outcomes in Peritoneal Dissemination from Signet Ring Cell Carcinoma of the Appendix Treated with Cytoreductive Surgery and Hyperthermic Intraperitoneal Chemotherapy Ann Surg Oncol (2019) 26:473–481 https://doi.org/10.1245/s10434-018-7007-3 ORIGINAL ARTICLE – GASTROINTESTINAL ONCOLOGY Outcomes in Peritoneal Dissemination from Signet Ring Cell Carcinoma of the Appendix Treated with Cytoreductive Surgery and Hyperthermic Intraperitoneal Chemotherapy Carlos Munoz-Zuluaga, MD1 , Armando Sardi, MD, FACS1 , Mary Caitlin King, BSc1, Carol Nieroda, MD1, Michelle Sittig, RN1 , Ryan MacDonald, PhD2, and Vadim Gushchin, MD FACS1 1The Institute for Cancer Care, Mercy Medical Center, Baltimore, MD; 2Center for Clinical Excellence, Mercy Medical Center, Baltimore, MD ABSTRACT positive HGMCP-S (PFS: 3.4 vs 1.5 years, p = 0.03; OS: Background. Cytoreductive surgery and hyperthermic 5.6 vs 2.1 months, p = 0.021). intraperitoneal chemotherapy (CRS/HIPEC) is standard Conclusions. The aggressive histology of HGMCP-S is treatment for peritoneal dissemination from appendiceal associated with poor OS, has fewer abnormal TM, and is cancer (AC); however, its role in high-grade histopatho- more likely to have positive LN. However, CRS/HIPEC logic subtypes (high-grade mucinous carcinoma peritonei can achieve a 5-year survival of 25%, which may improve [HGMCP] and HGMCP with signet ring cells [HGMCP- to 51% with negative LN. S]) is controversial due to their aggressive behavior. This study analyzed clinical outcomes of high-grade AC after CRS/HIPEC. BACKGROUND Methods. A prospective database of CRS/HIPEC proce- dures for HGMCP performed from 1998–2017 was Appendiceal cancer (AC) is a rare malignancy, with reviewed. Perioperative variables and survival were only 1.2 cases per 100,000 people/year in the US.1 It typ- analyzed. ically presents as acute appendicitis and is diagnosed Results. Eighty-six HGMCP and 65 HGMCP-S were incidentally in 1% of appendectomies.2 AC represents a identified. HGMCP had more positive tumor markers (TM) heterogeneous group of clinically and morphologically (CEA/CA-125/CA-19-9) than HGMCP-S (63% vs 40%, distinct tumors, including colonic-type adenocarcinoma, p = 0.005). HGMCP had higher Peritoneal Cancer Index mucinous adenocarcinoma, goblet cell adenocarcinoma, (32 vs 26, p = 0.097) and was less likely to have positive and neuroendocrine carcinoma.3–7 lymph nodes (LN) than HGMCP-S (28% vs 69%, Mucinous adenocarcinomas comprise 50% of ACs, p = \ 0.001). Complete cytoreduction was achieved in including a spectrum of histopathologic subtypes, ranging 84% and 83%, respectively. PFS at 3- and 5-years was 59% from low- to high-grade mucinous carcinoma peritonei and 48% for HGMCP vs 31% and 14% for HGMCP-S. (LGMCP, HGMCP) to HGMCP with signet ring cells Median PFS was 4.3 and 1.6 years, respectively (HGMCP-S), each with different prognoses.8–11 (p \ 0.001). OS at 3- and 5-years was 84% and 64% in Mucinous neoplasms are usually diagnosed at advanced HGMCP vs 38% and 25% in HGMCP-S. Median OS was stages, with extensive peritoneal disease.3 Mucinous AC is 7.5 and 2.2 years, respectively (p \ 0.001). LN negative biologically and histopathologically distinct from colorec- HGMCP-S had longer median PFS and OS than LN tal cancer and resistant to conventional colorectal treatment.12–14 Although standard treatment for peritoneal dissemination (PD) from AC is cytoreductive surgery and Ó Society of Surgical Oncology 2018 hyperthermic intraperitoneal chemotherapy (CRS/HIPEC), First Received: 31 July 2018; it is controversial in high-grade histopathologies, such as Published Online: 6 December 2018 HGMCP or the more aggressive HGMCP-S, due to their A. Sardi, MD, FACS e-mail: [email protected] 474 C. Munoz-Zuluaga et al. poor prognosis.15 We analyzed the perioperative charac- if their levels were [ 5 ng/mL, 35 U/mL, and 37 U/mL, teristics and clinical outcomes of patients with HGMCP respectively. and HGMCP-S from AC treated with CRS/HIPEC. Cytoreductive Surgery/Hyperthermic Intraperitoneal PATIENTS AND METHODS Chemotherapy (CRS/HIPEC) Procedure A retrospective review of a prospective institutional Under general anesthesia, a midline xiphopubic incision database with 673 CRS/HIPEC procedures performed from was made and the PCI score was assessed. Resections were 1998 to 2017 was conducted. PD from AC occurred in 406 performed with the objective of reducing tumor to micro- patients undergoing CRS/HIPEC with an Eastern Cooper- scopic levels. After resection, the CC score was recorded. ative Oncology Group (ECOG) performance status score of HIPEC was performed using the closed technique with 0–2, no evidence of extra-abdominal disease, and imaging mitomycin C for 90 min for a total dose of 40 mg (30 mg or diagnostic laparoscopy demonstrating resectable dis- initially and 10 mg after 30 min) at 41–42 °C. After per- ease. Patient characteristics, surgical variables, and fusion, gastrointestinal reconstruction was completed as postoperative outcomes from the first CRS/HIPEC of indicated and chest tubes were placed when diaphragmatic patients with high-grade histopathologies were analyzed. peritonectomy was performed. Immediately following the procedure, patients were transferred to the intensive care Histopathology unit until clinically stable, and then transferred to the inpatient oncology unit.19 All tissue samples from previous biopsies and CRS/ HIPEC were reviewed. Previously, specimens were clas- Surgical Complications sified according to the histopathologic classification of Ronnett et al.;8 however, following the results of the 2016 Surgical complications were graded according to the Peritoneal Surface Oncology Group International expert Clavien–Dindo classification.20 Grade III/IV surgical panel consensus, alternative terminology has been used, complications were considered major complications, with defining disseminated peritoneal adenomucinosis (DPAM) Grade V indicating death.21 as LGMCP, peritoneal mucinous carcinomatosis (PMCA) as HGMCP, and PMCA with signet ring cells (PMCA-S) as Follow-Up HGMCP-S.10,16 In this study, HGMCP-S comprises any lesion with any component of signet ring cells (SRCs), Standard follow-up included immediate postoperative excluding degenerative cells within pools of mucin that follow-up after hospital discharge, followed by physical mimic SRC. Patients with LGMCP as well as goblet cell examinations, imaging studies, and tumor markers (TMs) carcinoids of the appendix were excluded from this every 6 months for 5 years, yearly until the tenth year, or analysis. sooner when symptomatic. Recurrence was only considered in patients after complete cytoreduction with evidence of disease Prognostic Scores on imaging, elevated TMs, and/or clinical presentation (e.g. bowel obstruction). If considered amenable to cytoreduction, Intraoperative Peritoneal Cancer Index (PCI) score additional CRS/HIPEC procedures were offered. estimated disease burden, as previously described by Jac- quet et al.17 PCI \ 20 was considered low tumor burden Statistical Analysis and PCI C 20 was considered high tumor burden. Completeness of cytoreduction (CC) score specified the Categorical perioperative variables were assessed using quality of cytoreduction. Complete cytoreduction was Chi square tests, and continuous perioperative variables defined as no visible residual tumor (CC-0) or tumor were compared using the independent sample Student’s t test nodules \ 2.5 mm in size (CC-1), while incomplete or Mann–Whitney U test when not normally distributed. cytoreduction was defined as residual tumor C 2.5 mm Overall survival (OS) and progression-free survival (PFS) (CC-2/CC-3).15,18 were calculated using the Kaplan–Meier method. The log- rank test determined statistically significant differences Tumor Markers (TMs) between curves, while multivariate Cox regression analysis determined differences in OS and PFS, adjusting for Preoperative carcinoembryonic antigen (CEA), cancer covariates. PFS was only calculated for patients who had a antigen (CA) 125, and CA 19-9 were considered elevated complete cytoreduction (CC-0/1) from the date of first CRS/ CRS/HIPEC in Appendiceal SRC Carcinoma 475 TABLE 1 Patient Characteristics HGMCP [n = 86] HGMCP-S [n = 65] p Value characteristics Age at diagnosis, years [mean ± SD (range)] 52 ± 14 (23–77) 53 ± 10 (32–74) 0.554 Age at surgery, years [mean ± SD (range)] 53 ± 13 (23–79) 54 ± 10 (32–74) 0.705 Female 50 (58) 40 (62) 0.673 Preoperative SC 34 (40) 40 (62) 0.007 Any TM positive 52/82 (63) 25/63 (40) 0.005 CEA positive 38/81 (47) 17/62 (27) 0.018 CA-125 positive 29/78 (37) 16/61 (26) 0.171 CA 19-9 positive 31/77 (40) 16/59 (27) 0.110 Time to CRS/HIPEC, months [median (range)] 5.0 (1–182) 4.5 (0–89) 0.031 Disease burden, PCI [median (range)] 32 (0–39) 26 (0–39) 0.097 Operative time, min) [median (range)] 645 (285–991) 595 (284–1160) 0.048 Length of stay, days [median (range)] 10 (6–72) 9 (6–30) 0.213 Complete cytoreduction, CC-0/1 72 (84) 54 (83) 0.916 Positive lymph nodes 24 (28) 45 (69) \ 0.001 Grade III/IV surgical complications 20 (23) 9 (14) 0.210 30-day mortality 0 (0) 0 (0) NA Postoperative SC 34/83 (41) 38/61 (62) 0.018 Follow-up time, years [median (range)] 4.3 (0–12.6) 4.4 (0.5–7.9) 0.212 Status Alive 49 (57) 19 (29) NA No evidence of disease 40 (47) 13 (20) NA Alive with disease 9 (10) 6 (9) NA Death 36 (42) 44 (68) NA Dead of disease 31 (36) 44 (68) NA Dead of other causes 5 (6) 0 (0) NA Lost to follow-up 1 (1) 2 (3) NA Bold text indicates statistically significant variables Data are expressed as n (%) unless otherwise specified CA cancer antigen, CEA carcinoembryonic antigen, CRS cytoreductive surgery, HGMCP high-grade mucinous carcinoma peritonei, HGMCP-S high-grade mucinous carcinoma peritonei with signet ring cells, HIPEC hyperthermic intraperitoneal chemotherapy, NA not applicable, PCI Peritoneal Cancer Index, SC systemic chemotherapy, SD standard deviation, TM tumor marker HIPEC to the date of radiographic/pathologic evidence of HGMCP and 65/79 [82%] HGMCP-S) and 45 had aborted recurrent disease or death of disease.
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