{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,16]],"date-time":"2026-10-16T03:54:42Z","timestamp":1792122882657,"version":"4.4.0"},"reference-count":32,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2022,5,18]],"date-time":"2022-05-18T00:00:00Z","timestamp":1652832000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Surg."],"abstract":"<jats:sec><jats:title>Background<\/jats:title><jats:p>Cytoreductive surgery (CRS) is a technically demanding procedure, and there is considerable debate about its safe application. This study investigated the learning curve for CRS and the clinical outcomes of consecutive patients treated by a single surgeon at a single institution.<\/jats:p><\/jats:sec><jats:sec><jats:title>Methods<\/jats:title><jats:p>We collected 251 consecutive patients who underwent CRS for peritoneal metastases by a single surgeon at Fondazione Policlinico Universitario A. Gemelli IRCCS, between January 2016 and December 2020. The learning curve was estimated using the cumulative summation analysis (CUSUM) for operative time (OT). Risk-adjusted CUSUM (RA-CUSUM) charts were developed using a composite variable (surgical failure), defined as the occurrence of at least one of the following events: major postoperative complications (Clavien\u2013Dindo grade \u22653), blood loss \u2265500\u2005mL, incomplete cytoreduction. Three learning phases were thus derived from the RA-CUSUM analysis, and were compared in terms of perioperative outcomes.<\/jats:p><\/jats:sec><jats:sec><jats:title>Results<\/jats:title><jats:p>CUSUM-OT showed that the operation time improved significantly after the 161<jats:sup>th<\/jats:sup> case. RA-CUSUM analysis allowed to break the CRS learning curve into three different phases: phase 1, \u201cthe learning phase\u201d (cases 1\u201399), phase 2 \u201cthe experienced phase\u201d (cases 100\u2013188), and phase 3, \u201cthe mastership phase\u201d (cases 189\u2013251). The rate of major postoperative complications decreased significantly over the three phases (<jats:italic>p<\/jats:italic>\u2009=\u20090.019). Operative time decreased significantly as well (<jats:italic>p<\/jats:italic>\u2009=\u20090.031) and was significantly shorter in phase 3 with respect to the other two phases (phase 3 vs phase 2: 420\u2005min vs 500\u2005min, <jats:italic>p<\/jats:italic>\u2009=\u20090.017; phase 3 vs phase 1: 420\u2005min vs 503\u2005min, <jats:italic>p<\/jats:italic>\u2009=\u20090.021). Blood loss consistently decreased throughout the three phases (<jats:italic>p<\/jats:italic>\u2009=\u20090.001). The rate of incomplete cytoreduction was significantly lower in phase 3 than in phase 2 (4.8% vs 14.6%, <jats:italic>p<\/jats:italic>\u2009=\u20090.043).<\/jats:p><\/jats:sec><jats:sec><jats:title>Conclusion<\/jats:title><jats:p>The CRS failure rate stabilized after the first 99 cases, and the complete surgical proficiency was achieved after 189 cases. A standardised and mentored learning model is a safer strategy to shorten the learning process, to reduce morbidity and mortality, to improve oncologic outcomes.<\/jats:p><\/jats:sec>","DOI":"10.3389\/fsurg.2022.877970","type":"journal-article","created":{"date-parts":[[2022,5,18]],"date-time":"2022-05-18T06:10:02Z","timestamp":1652854202000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":19,"title":["The Road to Technical Proficiency in Cytoreductive Surgery for Peritoneal Carcinomatosis: Risk-Adjusted Cumulative Summation Analysis"],"prefix":"10.3389","volume":"9","author":[{"given":"Francesco","family":"Santullo","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Carlo","family":"Abatini","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Miriam","family":"Attalla El Halabieh","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Federica","family":"Ferracci","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Claudio","family":"Lodoli","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lorenzo","family":"Barberis","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Francesco","family":"Giovinazzo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andrea","family":"Di Giorgio","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fabio","family":"Pacelli","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2022,5,18]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"263","DOI":"10.1200\/JCO.2011.37.1039","article-title":"Treatment of colorectal peritoneal carcinomatosis with systemic chemotherapy: A pooled analysis of North Central Cancer Treatment Group phase III trials N9741 and N9841","volume":"30","author":"Franko","year":"2012","journal-title":"J Clin Oncol"},{"key":"B2","doi-asserted-by":"publisher","first-page":"307","DOI":"10.1002\/jso.23222","article-title":"Modest advances in survival for patients with colorectal-associated peritoneal carcinomatosis in the era of modern chemotherapy","volume":"107","author":"Zani","year":"2013","journal-title":"J Surg Oncol"},{"key":"B3","doi-asserted-by":"publisher","DOI":"10.1186\/s12957-021-02320-4","article-title":"Postoperative oxaliplatin-based hyperthermic intraperitoneal chemotherapy: an effective and safe palliative treatment option for colorectal cancer with peritoneal metastasis","author":"Sun","year":"2021","journal-title":"World J Surg Oncol"},{"key":"B4","doi-asserted-by":"publisher","first-page":"119","DOI":"10.1016\/j.critrevonc.2019.06.014","article-title":"Systematic review of published literature on oxaliplatin and mitomycin C as chemotherapeutic agents for hyperthermic intraperitoneal chemotherapy in patients with peritoneal metastases from colorectal cancer","volume":"142","author":"Wisselink","year":"2019","journal-title":"Crit Rev Oncol Hematol"},{"key":"B5","doi-asserted-by":"publisher","first-page":"6979","DOI":"10.3748\/wjg.v19.i41.6979","article-title":"Peritoneal carcinomatosis","volume":"19","author":"Coccolini","year":"2013","journal-title":"World J Gastroenterol"},{"key":"B6","doi-asserted-by":"publisher","first-page":"e17","DOI":"10.1016\/j.ejso.2018.10.086","article-title":"A UNICANCER phase III trial of hyperthermic intra-peritoneal Chemotherapy (HIPEC) for colorectal peritoneal carcinomatosis. PRODIGE 7","volume":"45","author":"Quenet","year":"2019","journal-title":"Eur J Surg Oncol"},{"key":"B7","doi-asserted-by":"publisher","first-page":"230","DOI":"10.1056\/nejmoa1708618","article-title":"Hyperthermic intraperitoneal chemotherapy in ovarian cancer","volume":"378","author":"van Driel","year":"2018","journal-title":"N Engl J Med"},{"key":"B8","doi-asserted-by":"publisher","first-page":"247","DOI":"10.1007\/978-0-387-48993-3_15","article-title":"Peritonectomy procedures","volume":"221","author":"Sugarbaker","year":"2007","journal-title":"Peritoneal Carcinomatosis: A Multidisciplinary Approach"},{"key":"B9","doi-asserted-by":"publisher","first-page":"e186847","DOI":"10.1001\/jamanetworkopen.2018.6847","article-title":"Morbidity and mortality rates following cytoreductive surgery combined with hyperthermic intraperitoneal chemotherapy compared with other high-risk surgical oncology procedures","volume":"2","author":"Foster","year":"2019","journal-title":"JAMA Netw Open"},{"key":"B10","doi-asserted-by":"publisher","first-page":"85","DOI":"10.1002\/jso.25939","article-title":"Cytoreductive surgery and hyperthermic intraperitoneal chemotherapy: Technical considerations and the learning curve","volume":"122","author":"Vining","year":"2020","journal-title":"J Surg Oncol"},{"key":"B11","doi-asserted-by":"publisher","DOI":"10.1007\/s11605-021-05073-3","article-title":"Clinical and molecular features in patients undergoing cytoreductive surgery and hyperthermic intraperitoneal chemotherapy for peritoneal carcinosis from colorectal cancer","author":"Di Giorgio","year":"2021","journal-title":"J. Gastrointest Surg"},{"key":"B12","doi-asserted-by":"publisher","first-page":"715119","DOI":"10.3389\/fsurg.2021.715119","article-title":"Cytoreduction and hyperthermic intraperitoneal chemotherapy for pseudomyxoma peritonei of appendiceal origin: A single center experience","volume":"8","author":"Santullo","year":"2021","journal-title":"Front Surg"},{"key":"B13","doi-asserted-by":"publisher","first-page":"441","DOI":"10.1093\/biostatistics\/1.4.441","article-title":"Monitoring surgical performance using risk-adjusted cumulative sum charts","volume":"1","author":"Steiner","year":"2000","journal-title":"Biostatistics"},{"key":"B14","doi-asserted-by":"publisher","DOI":"10.1007\/s13304-021-01034-2","article-title":"Cytoreductive surgery and mitomycin C hyperthermic intraperitoneal chemotherapy with CO2 recirculation (HIPEC-CO2) for colorectal cancer peritoneal metastases: analysis of short-term outcomes","author":"Rotolo","year":"2021","journal-title":"Updates Surg"},{"key":"B15","doi-asserted-by":"publisher","first-page":"187","DOI":"10.1097\/SLA.0b013e3181b13ca2","article-title":"The clavien-dindo classification of surgical complications: Five-year experience","volume":"250","author":"Clavien","year":"2009","journal-title":"Ann Surg"},{"key":"B16","doi-asserted-by":"publisher","first-page":"4499","DOI":"10.1245\/s10434-020-09501-7","article-title":"Impact of perioperative blood transfusions on outcomes after hyperthermic intraperitoneal chemotherapy: A propensity-matched analysis","volume":"28","author":"Kubi","year":"2021","journal-title":"Ann Surg Oncol"},{"key":"B17","doi-asserted-by":"publisher","first-page":"1141","DOI":"10.1111\/anae.14331","article-title":"Association of anaesthetists guidelines: cell salvage for peri-operative blood conservation 2018","volume":"73","author":"Klein","year":"2018","journal-title":"Anaesthesia"},{"key":"B18","doi-asserted-by":"publisher","first-page":"829","DOI":"10.1111\/anae.13489","article-title":"AAGBI guidelines: the use of blood components and their alternatives 2016","volume":"71","author":"Klein","year":"2016","journal-title":"Anaesthesia"},{"key":"B19","doi-asserted-by":"publisher","first-page":"63","DOI":"10.1200\/JCO.2009.23.9285","article-title":"Peritoneal colorectal carcinomatosis treated with surgery and perioperative intraperitoneal chemotherapy: Retrospective analysis of 523 patients from a multicentric french study","volume":"28","author":"Elias","year":"2010","journal-title":"J Clin Oncol"},{"key":"B20","doi-asserted-by":"publisher","DOI":"10.1016\/j.ejso.2020.02.012","article-title":"Appendiceal tumours and pseudomyxoma peritonei: Literature review with PSOGI\/EURACAN clinical practice guidelines for diagnosis and treatment","volume":"47","author":"Govaerts","year":"2021","journal-title":"Eur J Surg Oncol"},{"key":"B21","doi-asserted-by":"publisher","first-page":"36","DOI":"10.1016\/j.ejso.2020.02.011","article-title":"Peritoneal mesothelioma: PSOGI\/EURACAN clinical practice guidelines for diagnosis, treatment and follow-up","volume":"47","author":"Kusamura","year":"2021","journal-title":"Eur J Surg Oncol"},{"key":"B22","doi-asserted-by":"publisher","first-page":"2870","DOI":"10.1007\/s00464-020-07724-z","article-title":"Evaluation of a single surgeon\u2019s learning curve of laparoscopic pancreaticoduodenectomy: risk-adjusted cumulative summation analysis","volume":"35","author":"Kim","year":"2021","journal-title":"Surg Endosc"},{"key":"B23","doi-asserted-by":"publisher","first-page":"1408","DOI":"10.1002\/bjs.5863","article-title":"Learning curve of combined modality treatment in peritoneal surface disease","volume":"94","author":"Smeenk","year":"2007","journal-title":"Br J Surg"},{"key":"B24","doi-asserted-by":"publisher","first-page":"348","DOI":"10.1097\/SLA.0b013e3182436c28","article-title":"Multidimensional analysis of the learning curve for cytoreductive surgery and hyperthermic intraperitoneal chemotherapy in peritoneal surface malignancies","volume":"255","author":"Kusamura","year":"2012","journal-title":"Ann Surg"},{"key":"B25","doi-asserted-by":"publisher","first-page":"930","DOI":"10.1016\/j.ejso.2014.03.001","article-title":"Cytoreductive surgery plus perioperative intraperitoneal chemotherapy in pseudomyxoma peritonei: aspects of the learning curve","volume":"40","author":"Andr\u00e9asson","year":"2014","journal-title":"Eur J Surg Oncol"},{"key":"B26","doi-asserted-by":"publisher","first-page":"1673","DOI":"10.1245\/s10434-014-4111-x","article-title":"Institutional learning curve of cytoreductive surgery and hyperthermic intraperitoneal chemoperfusion for peritoneal malignancies","volume":"22","author":"Polanco","year":"2015","journal-title":"Ann Surg Oncol"},{"key":"B27","doi-asserted-by":"publisher","first-page":"148","DOI":"10.1245\/s10434-018-6992-6","article-title":"Morbidity and mortality following cytoreductive surgery and hyperthermic intraperitoneal chemotherapy: Data from the DGAV StuDoQ registry with 2149 consecutive patients","volume":"26","author":"Piso","year":"2019","journal-title":"Ann Surg Oncol"},{"key":"B28","doi-asserted-by":"publisher","first-page":"527","DOI":"10.1007\/s00423-019-01805-x","article-title":"Evaluation of cytoreductive surgery and HIPEC for peritoneal surface malignancies: analysis of 384 consecutive cases","volume":"404","author":"Narasimhan","year":"2019","journal-title":"Langenbeck's Arch Surg"},{"key":"B29","doi-asserted-by":"publisher","first-page":"312","DOI":"10.1002\/jso.23231","article-title":"Learning curve for cytoreductive surgery and hyperthermic intraperitoneal chemotherapy in peritoneal surface malignancies: analysis of two centres","volume":"107","author":"Kusamura","year":"2013","journal-title":"J Surg Oncol"},{"key":"B30","doi-asserted-by":"publisher","first-page":"573","DOI":"10.1016\/j.jamcollsurg.2013.12.013","article-title":"Intraperitoneal chemotherapy for peritoneal surface malignancy: Experience with 1,000 patients","volume":"218","author":"Levine","year":"2014","journal-title":"J Am Coll Surg"},{"key":"B31","doi-asserted-by":"publisher","first-page":"796","DOI":"10.1002\/jso.24248","article-title":"What made hyperthermic intraperitoneal chemotherapy an effective curative treatment for peritoneal surface malignancy: A 25-year experience with 1,125 procedures","volume":"113","author":"Passot","year":"2016","journal-title":"J Surg Oncol"},{"key":"B32","doi-asserted-by":"publisher","first-page":"122","DOI":"10.3978\/j.issn.2078-6891.2015.099","article-title":"Impact of surgical volume of centers on post-operative outcomes from cytoreductive surgery and hyperthermic intra-peritoneal chemoperfusion","volume":"7","author":"Rajeev","year":"2016","journal-title":"J Gastrointest Oncol"}],"container-title":["Frontiers in Surgery"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fsurg.2022.877970\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,5,18]],"date-time":"2022-05-18T06:10:07Z","timestamp":1652854207000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fsurg.2022.877970\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,5,18]]},"references-count":32,"alternative-id":["10.3389\/fsurg.2022.877970"],"URL":"https:\/\/doi.org\/10.3389\/fsurg.2022.877970","relation":{},"ISSN":["2296-875X"],"issn-type":[{"value":"2296-875X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,5,18]]},"article-number":"877970"}}