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  • Review Article
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Advances in the management of peritoneal malignancies

Nature Reviews Clinical Oncology volume 19, pages 698–718 (2022)Cite this article

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Abstract

Peritoneal surface malignancies (PSMs) are usually associated with a poor prognosis. Nonetheless, in line with advances in the management of most abdominopelvic metastatic diseases, considerable progress has been made over the past decade. An improved understanding of disease biology has led to the more accurate prediction of neoplasia aggressiveness and the treatment response and has been reflected in the proposal of new classification systems. Achieving complete cytoreductive surgery remains the cornerstone of curative-intent treatment of PSMs. Alongside centralization in expert centres, enabling the delivery of multimodal and multidisciplinary strategies, preoperative management is a crucial step in order to select patients who are most likely to benefit from surgery. Depending on the specific PSM, the role of intraperitoneal chemotherapy and of perioperative systemic chemotherapy, in particular, in the neoadjuvant setting, is established in certain scenarios but questioned in several others, although more prospective data are required. In this Review, we describe advances in all aspects of the management of PSMs including disease biology, assessment and improvement of disease resectability, perioperative management, systemic therapy and pre-emptive management, and we speculate on future research directions.

Key points

  • Pathological, molecular and genetic biomarkers should be integrated into the selection processes for appropriate multidisciplinary, palliative or curative management of peritoneal surface malignancies (PSMs).

  • Centralization of curative treatment in PSM-specific expert centres is needed to decrease the incidence of postoperative complications and improve survival outcomes owing to better patient selection, surgical expertise and perioperative care.

  • The combination of functional imaging (MRI, PET–CT) with appropriate laparoscopy improves the preoperative assessment of resectability of patients with peritoneal metastases, which is the most important determinant of eligibility for curative treatment.

  • Perioperative prehabilitation and enhanced postoperative recovery (ERAS) pathways should be integrated into curative management, especially in patients >70 years of age who require specific comprehensive geriatric assessments.

  • Intraperitoneal chemotherapy (HIPEC, PIPAC, NIPEC or EPIC) has an important role in the management of PSM and requires further evaluation in the neoadjuvant, consolidative therapy and pre-emptive settings.

  • The role of perioperative systemic chemotherapy, targeted therapy and immunotherapy should be evaluated in specific studies involving patients with PSMs, considering the common chemoresistance to systemic treatments in these patients.

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Fig. 1: Example of a multimodal preoperative work-up.
Fig. 2: Effects of prehabilitation and use of an enhanced recovery programme on recovery after cytoreductive surgery.
Fig. 3: Key aspects of the rationale for delivering intraperitoneal chemotherapy.

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References

  1. Cortés-Guiral, D. et al. Primary and metastatic peritoneal surface malignancies. Nat. Rev. Dis. Prim. 7, 91 (2021).

    Article  PubMed  Google Scholar 

  2. Sadeghi, B. et al. Peritoneal carcinomatosis from non-gynecologic malignancies: results of the EVOCAPE 1 multicentric prospective study. Cancer 88, 358–363 (2000).

    Article  CAS  PubMed  Google Scholar 

  3. Chu, D. Z., Lang, N. P., Thompson, C., Osteen, P. K. & Westbrook, K. C. Peritoneal carcinomatosis in nongynecologic malignancy. A prospective study of prognostic factors. Cancer 63, 364–367 (1989).

    Article  CAS  PubMed  Google Scholar 

  4. Jayne, D. G., Fook, S., Loi, C. & Seow-Choen, F. Peritoneal carcinomatosis from colorectal cancer. Br. J. Surg. 89, 1545–1550 (2002).

    Article  CAS  PubMed  Google Scholar 

  5. Sugarbaker, P. H. Peritonectomy procedures. Ann. Surg. 221, 29–42 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Arquillière, J., Glehen, O. & Passot, G. Cytoreductive surgery in peritoneal carcinomatosis. J. Visc. Surg. 158, 258–264 (2021).

    Article  PubMed  Google Scholar 

  7. Chi, D. S. et al. Improved optimal cytoreduction rates for stages IIIC and IV epithelial ovarian, fallopian tube, and primary peritoneal cancer: a change in surgical approach. Gynecol. Oncol. 94, 650–654 (2004).

    Article  PubMed  Google Scholar 

  8. Glehen, O., Mohamed, F. & Gilly, F. N. Peritoneal carcinomatosis from digestive tract cancer: new management by cytoreductive surgery and intraperitoneal chemohyperthermia. Lancet Oncol. 5, 219–228 (2004).

    Article  PubMed  Google Scholar 

  9. Glehen, O. et al. Toward curative treatment of peritoneal carcinomatosis from nonovarian origin by cytoreductive surgery combined with perioperative intraperitoneal chemotherapy: a multi-institutional study of 1290 patients. Cancer 116, 5608–5618 (2010).

    Article  PubMed  Google Scholar 

  10. Speeten, K. V., der, Lemoine, L. & Sugarbaker, P. Overview of the optimal perioperative intraperitoneal chemotherapy regimens used in current clinical practice. Pleura Peritoneum 2, 63–72 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  11. Bristow, R. E., Tomacruz, R. S., Armstrong, D. K., Trimble, E. L. & Montz, F. J. Survival effect of maximal cytoreductive surgery for advanced ovarian carcinoma during the platinum era: a meta-analysis. J. Clin. Oncol. 20, 1248–1259 (2002).

    Article  PubMed  Google Scholar 

  12. Elias, D. et al. Peritoneal colorectal carcinomatosis treated with surgery and perioperative intraperitoneal chemotherapy: retrospective analysis of 523 patients from a multicentric French study. J. Clin. Oncol. 28, 63–68 (2010).

    Article  PubMed  Google Scholar 

  13. Kusamura, S. et al. The role of hyperthermic intraperitoneal chemotherapy in pseudomyxoma peritonei after cytoreductive surgery. JAMA Surg. 156, e206363 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  14. Jacquet, P. & Sugarbaker, P. H. Clinical research methodologies in diagnosis and staging of patients with peritoneal carcinomatosis. Cancer Treat. Res. 82, 359–374 (1996).

    Article  CAS  PubMed  Google Scholar 

  15. Goere, D. et al. Complete cytoreductive surgery plus HIPEC for peritoneal metastases from unusual cancer sites of origin: results from a worldwide analysis issue of the peritoneal surface oncology group international (PSOGI). Int. J. Hyperthermia 33, 520–527 (2017).

    Article  PubMed  Google Scholar 

  16. Chirurgie, A. Fde et al. Peritoneal carcinomatosis from gastric cancer: a multi-institutional study of 159 patients treated by cytoreductive surgery combined with perioperative intraperitoneal chemotherapy. Ann. Surg. Oncol. 17, 2370–2377 (2010).

    Article  Google Scholar 

  17. Bakrin, N. et al. Peritoneal carcinomatosis treated with cytoreductive surgery and hyperthermic intraperitoneal chemotherapy (HIPEC) for advanced ovarian carcinoma: a French multicentre retrospective cohort study of 566 patients. Eur. J. Surg. Oncol. 39, 1435–1443 (2013).

    Article  CAS  PubMed  Google Scholar 

  18. Villeneuve, L. et al. A new internet tool to report peritoneal malignancy extent. PeRitOneal malignancy stage evaluation (PROMISE) application. Eur. J. Surg. Oncol. 42, 877–882 (2016).

    Article  CAS  PubMed  Google Scholar 

  19. Chapel, D. B. et al. Malignant peritoneal mesothelioma: prognostic significance of clinical and pathologic parameters and validation of a nuclear-grading system in a multi-institutional series of 225 cases. Mod. Pathol. 34, 380–395 (2020).

    Article  PubMed  Google Scholar 

  20. Benzerdjeb, N. et al. Combined grade and nuclear grade are prognosis predictors of epithelioid malignant peritoneal mesothelioma: a multi-institutional retrospective study. Virchows Arch. 479, 927–936 (2021).

    Article  PubMed  Google Scholar 

  21. Panou, V. et al. Frequency of germline mutations in cancer susceptibility genes in malignant mesothelioma. J. Clin. Oncol. 36, 2863–2871 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Chirac, P. et al. Genomic copy number alterations in 33 malignant peritoneal mesothelioma analyzed by comparative genomic hybridization array. Hum. Pathol. 55, 72–82 (2016).

    Article  CAS  PubMed  Google Scholar 

  23. Alakus, H. et al. BAP1 mutation is a frequent somatic event in peritoneal malignant mesothelioma. J. Transl. Med. 13, 122 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  24. Joseph, N. M. et al. Genomic profiling of malignant peritoneal mesothelioma reveals recurrent alterations in epigenetic regulatory genes BAP1, SETD2, and DDX3X. Mod. Pathol. 30, 246–254 (2017).

    Article  CAS  PubMed  Google Scholar 

  25. Leblay, N. et al. BAP1 is altered by copy number loss, mutation, and/or loss of protein expression in more than 70% of malignant peritoneal mesotheliomas. J. Thorac. Oncol. 12, 724–733 (2017).

    Article  PubMed  Google Scholar 

  26. Shrestha, R. et al. BAP1 haploinsufficiency predicts a distinct immunogenic class of malignant peritoneal mesothelioma. Genome Med. 11, 8 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  27. Deraco, M. et al. In Pathology of Peritoneal Metastases (eds Glehen, O. & Bhatt, A.) 117–129 (Springer, 2020) https://doi.org/10.1007/978-981-15-3773-8_6.

  28. Carbone, M. et al. BAP1 and cancer. Nat. Rev. Cancer 13, 153–159 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Sugarbaker, P. H. et al. Pseudomyxoma peritonei. A cancer whose biology is characterized by a redistribution phenomenon. Ann. Surg. 219, 109–111 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Carr, N. J. et al. A consensus for classification and pathologic reporting of pseudomyxoma peritonei and associated appendiceal neoplasia: the results of the Peritoneal Surface Oncology Group International (PSOGI) mModified Delphi process. Am. J. Surg. Pathol. 40, 14–26 (2016).

    Article  PubMed  Google Scholar 

  31. Lin, Y. L. et al. Consensuses and controversies on pseudomyxoma peritonei: a review of the published consensus statements and guidelines. Orphanet J. Rare Dis. 16, 85 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  32. Valasek, M. A. & Pai, R. K. An update on the diagnosis, grading, and staging of appendiceal mucinous neoplasms. Adv. Anat. Pathol. 25, 38–60 (2018).

    Article  PubMed  Google Scholar 

  33. Levine, E. A. et al. Prognostic molecular subtypes of low-grade cancer of the appendix. J. Am. Coll. Surg. 222, 493–503 (2016).

    Article  PubMed  Google Scholar 

  34. Vaira, M. et al. In Pathology of Peritoneal Metastases (eds Glehen, O. & Bhatt, A.) 163–173 (Springer, 2020).

  35. Su, J. et al. Prognostic molecular classification of appendiceal mucinous neoplasms treated with cytoreductive surgery and hyperthermic intraperitoneal chemotherapy. Ann. Surg. Oncol. 27, 1439–1447 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  36. Moaven, O. et al. Clinical implications of genetic signatures in appendiceal cancer patients with incomplete cytoreduction/HIPEC. Ann. Surg. Oncol. 27, 5016–5023 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  37. Ajani, J. A. et al. Gastric adenocarcinoma. Nat. Rev. Dis. Prim. 3, 17036 (2017).

    Article  PubMed  Google Scholar 

  38. Gao, D. et al. Cdh1 regulates cell cycle through modulating the Claspin/Chk1 and the Rb/E2F1 pathways. Mol. Biol. Cell 20, 3305–3316 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Cancer Genome Atlas Research Network. Comprehensive molecular characterization of gastric adenocarcinoma. Nature 513, 202–209 (2014).

    Article  Google Scholar 

  40. Cristescu, R. et al. Molecular analysis of gastric cancer identifies subtypes associated with distinct clinical outcomes. Nat. Med. 21, 449–456 (2015).

    Article  CAS  PubMed  Google Scholar 

  41. Wang, K. et al. Whole-genome sequencing and comprehensive molecular profiling identify new driver mutations in gastric cancer. Nat. Genet. 46, 573–582 (2014).

    Article  CAS  PubMed  Google Scholar 

  42. Oh, S. C. et al. Clinical and genomic landscape of gastric cancer with a mesenchymal phenotype. Nat. Commun. 9, 1777 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  43. Tanaka, Y. et al. Multi-omic profiling of peritoneal metastases in gastric cancer identifies molecular subtypes and therapeutic vulnerabilities. Nat. Cancer 2, 962–977 (2021).

    Article  CAS  PubMed  Google Scholar 

  44. Wang, R. et al. Multiplex profiling of peritoneal metastases from gastric adenocarcinoma identified novel targets and molecular subtypes that predict treatment response. Gut 69, 18–31 (2020).

    Article  CAS  PubMed  Google Scholar 

  45. Bettington, M. et al. The serrated pathway to colorectal carcinoma: current concepts and challenges. Histopathology 62, 367–386 (2013).

    Article  PubMed  Google Scholar 

  46. Zajac, O. et al. Tumour spheres with inverted polarity drive the formation of peritoneal metastases in patients with hypermethylated colorectal carcinomas. Nat. Cell Biol. 20, 296–306 (2018).

    Article  CAS  PubMed  Google Scholar 

  47. Guinney, J. et al. The consensus molecular subtypes of colorectal cancer. Nat. Med. 21, 1350–1356 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Ubink, I. et al. Histopathological and molecular classification of colorectal cancer and corresponding peritoneal metastases. Br. J. Surg. 105, e204–e211 (2018).

    Article  CAS  PubMed  Google Scholar 

  49. Heinemann, V., Stintzing, S., Kirchner, T., Boeck, S. & Jung, A. Clinical relevance of EGFR- and KRAS-status in colorectal cancer patients treated with monoclonal antibodies directed against the EGFR. Cancer Treat. Rev. 35, 262–271 (2009).

    Article  CAS  PubMed  Google Scholar 

  50. Deng, G. et al. BRAF mutation is frequently present in sporadic colorectal cancer with methylated hMLH1, but not in hereditary nonpolyposis colorectal cancer. Clin. Cancer Res. 10, 191–195 (2004).

    Article  CAS  PubMed  Google Scholar 

  51. Arjona-Sanchez, A. et al. RAS mutation decreases overall survival after optimal cytoreductive surgery and hyperthermic intraperitoneal chemotherapy of colorectal peritoneal metastasis: a modification proposal of the peritoneal surface disease severity score. Ann. Surg. Oncol. 26, 2595–2604 (2019).

    Article  CAS  PubMed  Google Scholar 

  52. Schneider, M. A. et al. Mutations of RAS/RAF proto-oncogenes impair survival after cytoreductive surgery and HIPEC for peritoneal metastasis of colorectal origin. Ann. Surg. 268, 845–853 (2018).

    Article  PubMed  Google Scholar 

  53. Cohen, R., Pudlarz, T., Delattre, J.-F., Colle, R. & Andre, T. Molecular targets for the treatment of metastatic colorectal cancer. Cancers 12, 2350 (2020).

    Article  CAS  PubMed Central  Google Scholar 

  54. Pietrantonio, F. et al. ALK, ROS1, and NTRK rearrangements in metastatic colorectal cancer. J. Natl Cancer Inst. 109, djx089 (2017).

    Article  Google Scholar 

  55. André, T. et al. Pembrolizumab in microsatellite-instability–high advanced colorectal cancer. N. Engl. J. Med. 383, 2207–2218 (2020).

    Article  PubMed  Google Scholar 

  56. Sallum, L. F. et al. WT1, p53 and p16 expression in the diagnosis of low- and high-grade serous ovarian carcinomas and their relation to prognosis. Oncotarget 9, 15818–15827 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  57. Moore, K. et al. Maintenance olaparib in patients with newly diagnosed advanced ovarian cancer. N. Engl. J. Med. 379, 2495–2505 (2018).

    Article  CAS  PubMed  Google Scholar 

  58. Miller, R. E. et al. ESMO recommendations on predictive biomarker testing for homologous recombination deficiency and PARP inhibitor benefit in ovarian cancer. Ann. Oncol. 31, 1606–1622 (2020).

    Article  CAS  PubMed  Google Scholar 

  59. Chiang, Y.-C., Lin, P.-H. & Cheng, W.-F. Homologous recombination deficiency assays in epithelial ovarian cancer: current status and future direction. Front. Oncol. 11, 675972 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  60. Ubink, I. et al. Organoids from colorectal peritoneal metastases as a platform for improving hyperthermic intraperitoneal chemotherapy. Br. J. Surg. 106, 1404–1414 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Narasimhan, V. et al. Medium-throughput drug screening of patient-derived organoids from colorectal peritoneal metastases to direct personalized therapy. Clin. Cancer Res. 26, 3662–3670 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Votanopoulos, K. I. et al. Appendiceal cancer patient-specific tumor organoid model for predicting chemotherapy efficacy prior to initiation of treatment: a feasibility study. Ann. Surg. Oncol. 26, 139–147 (2019).

    Article  PubMed  Google Scholar 

  63. Letai, A. Functional precision cancer medicine — moving beyond pure genomics. Nat. Med. 23, 1028–1035 (2017).

    Article  CAS  PubMed  Google Scholar 

  64. Roy, P. et al. Organoids as preclinical models to improve intraperitoneal chemotherapy effectiveness for colorectal cancer patients with peritoneal metastases: preclinical models to improve HIPEC. Int. J. Pharm. 531, 143–152 (2017).

    Article  CAS  PubMed  Google Scholar 

  65. Mazzocchi, A. R., Rajan, S. A. P., Votanopoulos, K. I., Hall, A. R. & Skardal, A. In vitro patient-derived 3D mesothelioma tumor organoids facilitate patient-centric therapeutic screening. Sci. Rep. 8, 2886 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  66. Votanopoulos, K. I. et al. Model of patient-specific immune-enhanced organoids for immunotherapy screening: feasibility study. Ann. Surg. Oncol. 27, 1956–1967 (2020).

    Article  PubMed  Google Scholar 

  67. Dhanisha, S. S., Guruvayoorappan, C., Drishya, S. & Abeesh, P. Mucins: structural diversity, biosynthesis, its role in pathogenesis and as possible therapeutic targets. Crit. Rev. Oncol. Hematol. 122, 98–122 (2018).

    Article  PubMed  Google Scholar 

  68. Rhodes, J. M. Usefulness of novel tumour markers. Ann. Oncol. 10, S118–S121 (1999).

    Article  Google Scholar 

  69. Young, R. H. Pseudomyxoma peritonei and selected other aspects of the spread of appendiceal neoplasms. Semin. Diagn. Pathol. 21, 134–150 (2004).

    Article  PubMed  Google Scholar 

  70. O’Connell, J. T., Tomlinson, J. S., Roberts, A. A., McGonigle, K. F. & Barsky, S. H. Pseudomyxoma peritonei is a disease of MUC2-expressing goblet cells. Am. J. Pathol. 161, 551–564 (2002).

    Article  PubMed  PubMed Central  Google Scholar 

  71. Lohani, K. et al. Pseudomyxoma peritonei: inflammatory responses in the peritoneal microenvironment. Ann. Surg. Oncol. 21, 1441–1447 (2014).

    Article  PubMed  Google Scholar 

  72. O’Connell, J. T., Hacker, C. M. & Barsky, S. H. MUC2 is a molecular marker for pseudomyxoma peritonei. Mod. Pathol. 15, 958–972 (2002).

    Article  PubMed  Google Scholar 

  73. Amini, A., Masoumi-Moghaddam, S., Ehteda, A. & Morris, D. L. Secreted mucins in pseudomyxoma peritonei: pathophysiological significance and potential therapeutic prospects. Orphanet J. Rare Dis. 9, 71 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  74. Huang, Y. et al. Intraoperative macroscopic tumour consistency is associated with overall survival after cytoreductive surgery and intraperitoneal chemotherapy for appendiceal adenocarcinoma with peritoneal metastases: a retrospective observational study. Am. J. Surg. 217, 704–712 (2019).

    Article  PubMed  Google Scholar 

  75. Nagtegaal, I. D. et al. The 2019 WHO classification of tumours of the digestive system. Histopathology 76, 182–188 (2020).

    Article  PubMed  Google Scholar 

  76. Benesch, M. G. K. & Mathieson, A. Epidemiology of signet ring cell adenocarcinomas. Cancers 12, 1544 (2020).

    Article  PubMed Central  Google Scholar 

  77. Berger, Y. et al. Correlation between intraoperative and pathological findings for patients undergoing cytoreductive surgery and hyperthermic intraperitoneal chemotherapy. Ann. Surg. Oncol. 26, 1103–1109 (2019).

    Article  CAS  PubMed  Google Scholar 

  78. Bhatt, A. et al. The pathologic peritoneal cancer index (PCI) strongly differs from the surgical PCI in peritoneal metastases arising from various primary tumors. Ann. Surg. Oncol. 10, 3–12 (2020).

    Google Scholar 

  79. Sessa, C. et al. ESMO–ESGO consensus conference recommendations on ovarian cancer: pathology and molecular biology, early and advanced stages, borderline tumours and recurrent disease. Ann. Oncol. 30, 672–705 (2019).

    Article  PubMed  Google Scholar 

  80. Bois, Adu et al. Role of surgical outcome as prognostic factor in advanced epithelial ovarian cancer: a combined exploratory analysis of 3 prospectively randomized phase 3 multicenter trials: by the Arbeitsgemeinschaft Gynaekologische Onkologie Studiengruppe Ovarialkarzinom (AGO-OVAR) and the Groupe d’Investigateurs Nationaux Pour les Etudes des Cancers de l’Ovaire (GINECO). Cancer 115, 1234–1244 (2009).

    Article  PubMed  Google Scholar 

  81. Harter, P. et al. Randomized trial of cytoreductive surgery for relapsed ovarian cancer. N. Engl. J. Med. 385, 2123–2131 (2021).

    Article  PubMed  Google Scholar 

  82. Quenet, F. et al. Cytoreductive surgery plus hyperthermic intraperitoneal chemotherapy versus cytoreductive surgery alone for colorectal peritoneal metastases (PRODIGE 7): a multicentre, randomised, open-label, phase 3 trial. Lancet Oncol. 22, 256–266 (2021).

    Article  CAS  PubMed  Google Scholar 

  83. Franko, J. et al. Prognosis of patients with peritoneal metastatic colorectal cancer given systemic therapy: an analysis of individual patient data from prospective randomised trials from the analysis and research in cancers of the digestive system (ARCAD) database. Lancet Oncol. 17, 1709–1719 (2016).

    Article  PubMed  Google Scholar 

  84. Elias, D. et al. Complete cytoreductive surgery plus intraperitoneal chemohyperthermia with oxaliplatin for peritoneal carcinomatosis of colorectal origin. J. Clin. Oncol. 27, 681–685 (2009).

    Article  PubMed  Google Scholar 

  85. Chua, T. C. et al. Early- and long-term outcome data of patients with pseudomyxoma peritonei from appendiceal origin treated by a strategy of cytoreductive surgery and hyperthermic intraperitoneal chemotherapy. J. Clin. Oncol. 30, 2449–2456 (2012).

    Article  PubMed  Google Scholar 

  86. Yan, T. D. et al. Cytoreductive surgery and hyperthermic intraperitoneal chemotherapy for malignant peritoneal mesothelioma: multi-institutional experience. J. Clin. Oncol. 27, 6237–6242 (2009).

    Article  PubMed  Google Scholar 

  87. Govaerts, K. et al. Appendiceal tumours and pseudomyxoma peritonei: literature review with PSOGI/EURACAN clinical practice guidelines for diagnosis and treatment. Eur. J. Surg. Oncol. 47, 11–35 (2021).

    Article  CAS  PubMed  Google Scholar 

  88. Kusamura, S. et al. Peritoneal mesothelioma: PSOGI/EURACAN clinical practice guidelines for diagnosis, treatment and follow-up. Eur. J. Surg. Oncol. 47, 36–59 (2021).

    Article  CAS  PubMed  Google Scholar 

  89. Ansari, N. et al. Cytoreductive surgery and hyperthermic intraperitoneal chemotherapy in 1000 patients with perforated appendiceal epithelial tumours. Eur. J. Surg. Oncol. 42, 1035–1041 (2016).

    Article  CAS  PubMed  Google Scholar 

  90. Chia, C. S. et al. Patients with peritoneal carcinomatosis from gastric cancer treated with cytoreductive surgery and hyperthermic intraperitoneal chemotherapy: is cure a possibility? Ann. Surg. Oncol. 23, 1971–1979 (2016).

    Article  CAS  PubMed  Google Scholar 

  91. Brandl, A., Yonemura, Y., Glehen, O., Sugarbaker, P. & Rau, B. Long term survival in patients with peritoneal metastasised gastric cancer treated with cytoreductive surgery and HIPEC: a multi-institutional cohort from PSOGI. Eur. J. Surg. Oncol. 47, 172–180 (2021).

    Article  PubMed  Google Scholar 

  92. Bonnot, P.-E. et al. Cytoreductive surgery with or without hyperthermic intraperitoneal chemotherapy for gastric cancer with peritoneal metastases (CYTO-CHIP study): a propensity score analysis. J. Clin. Oncol. 37, 2028–2040 (2019).

    Article  CAS  PubMed  Google Scholar 

  93. Bonnot, P. E. et al. Prognosis of poorly cohesive gastric cancer after complete cytoreductive surgery with or without hyperthermic intraperitoneal chemotherapy (CYTO-CHIP study). Br. J. Surg. 108, 1225–1235 (2021).

    Article  CAS  PubMed  Google Scholar 

  94. Kusamura, S. et al. Multicentre study of the learning curve and surgical performance of cytoreductive surgery with intraperitoneal chemotherapy for pseudomyxoma peritonei. Br. J. Surg. 101, 1758–1765 (2014).

    Article  CAS  PubMed  Google Scholar 

  95. Passot, G. et al. A perioperative clinical pathway can dramatically reduce failure-to-rescue rates after cytoreductive surgery for peritoneal carcinomatosis: a retrospective study of 666 consecutive cytoreductions. Ann. Surg. 265, 806–813 (2017).

    Article  PubMed  Google Scholar 

  96. Noiret, B. et al. Centralization and oncologic training reduce postoperative morbidity and failure-to-rescue rates after cytoreductive surgery and hyperthermic intraperitoneal chemotherapy for peritoneal surface malignancies: study on a 10-year national french practice. Ann. Surg. 272, 847–854 (2020).

    Article  PubMed  Google Scholar 

  97. Stang, N. L. et al. Incidence and survival of peritoneal malignant mesothelioma between 1989 and 2015: a population-based study. Cancer Epidemiol. 60, 106–111 (2019).

    Article  PubMed  Google Scholar 

  98. Villeneuve, L. et al. The RENAPE observational registry: rationale and framework of the rare peritoneal tumors French patient registry. Orphanet J. Rare Dis. 12, 37–39 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Cavaliere, F. et al. Prognostic factors and oncologic outcome in 146 patients with colorectal peritoneal carcinomatosis treated with cytoreductive surgery combined with hyperthermic intraperitoneal chemotherapy: Italian multicenter study S.I.T.I.L.O. Eur. J. Surg. Oncol. 37, 148–154 (2011).

    Article  CAS  PubMed  Google Scholar 

  100. Manzanedo, I. et al. Cytoreductive surgery and hyperthermic intraperitoneal chemotherapy (HIPEC) for gastric cancer with peritoneal carcinomatosis: multicenter study of Spanish Group of Peritoneal Oncologic Surgery (GECOP). Ann. Surg. Oncol. 26, 2615–2621 (2019).

    Article  PubMed  Google Scholar 

  101. Arjona-Sánchez, Á. et al. A minimally invasive approach for peritonectomy procedures and hyperthermic intraperitoneal chemotherapy (HIPEC) in limited peritoneal carcinomatosis: the American society of peritoneal surface malignancies (ASPSM) multi-institution analysis. Surg. Endosc. 33, 854–860 (2018).

    Article  PubMed  Google Scholar 

  102. Kusamura, S. et al. Learning curve, training program, and monitorization of surgical performance of peritoneal surface malignancies centers. Surg. Oncol. Clin. N. Am. 27, 507–517 (2018).

    Article  PubMed  Google Scholar 

  103. Reuss, A. et al. TRUST: trial of radical upfront surgical therapy in advanced ovarian cancer (ENGOT ov33/AGO-OVAR OP7). Int. J. Gynecol. Cancer 29, 1327 (2019).

    Article  PubMed  Google Scholar 

  104. Mariani, A. et al. Strategies for managing intraoperative discovery of limited colorectal peritoneal metastases. Ann. Surg. Oncol. 26, 1437–1444 (2019).

    Article  PubMed  Google Scholar 

  105. Faron, M. et al. Linear relationship of peritoneal cancer index and survival in patients with peritoneal metastases from colorectal cancer. Ann. Surg. Oncol. 23, 114–119 (2016).

    Article  PubMed  Google Scholar 

  106. Goéré, D. et al. Extent of colorectal peritoneal carcinomatosis: attempt to define a threshold above which HIPEC does not offer survival benefit: a comparative study. Ann. Surg. Oncol. 22, 2958–2964 (2015).

    Article  PubMed  Google Scholar 

  107. van’t Sant, I. et al. Diagnostic performance of imaging for the detection of peritoneal metastases: a meta-analysis. Eur. Radiol. 30, 3101–3112 (2020).

    Article  Google Scholar 

  108. Mohkam, K. et al. Resectability of peritoneal carcinomatosis: learnings from a prospective cohort of 533 consecutive patients selected for cytoreductive surgery. Ann. Surg. Oncol. 23, 1261–1270 (2016).

    Article  PubMed  Google Scholar 

  109. Sugarbaker, P. H. & Low, R. N. (eds) Pictorial Essays On Peritoneal Metastases Imaging: CT, MRI and PET-CT (Nova Science Publishers, 2020).

  110. Low, R. N., Barone, R. M. & Rousset, P. Peritoneal MRI in patients undergoing cytoreductive surgery and HIPEC: history, clinical applications, and implementation. Eur. J. Surg. Oncol. 47, 65–74 (2021).

    Article  PubMed  Google Scholar 

  111. Dohan, A. et al. Evaluation of the peritoneal carcinomatosis index with CT and MRI. Br. J. Surg. 104, 1244–1249 (2017).

    Article  CAS  PubMed  Google Scholar 

  112. Sant, I. V. T. et al. Diffusion-weighted MRI assessment of the peritoneal cancer index before cytoreductive surgery. Br. J. Surg. 106, 491–498 (2019).

    Article  Google Scholar 

  113. Delhorme, J.-B. et al. Appendiceal tumors and pseudomyxoma peritonei: French Intergroup Clinical Practice Guidelines for diagnosis, treatments and follow-up (RENAPE, RENAPATH, SNFGE, FFCD, GERCOR, UNICANCER, SFCD, SFED, SFRO, ACHBT, SFR). Dig. Liver Dis. 54, 30–39 (2022).

    Article  CAS  PubMed  Google Scholar 

  114. Menassel, B. et al. Preoperative CT and MRI prediction of non-resectability in patients treated for pseudomyxoma peritonei from mucinous appendiceal neoplasms. Eur. J. Surg. Oncol. 42, 558–566 (2016).

    Article  CAS  PubMed  Google Scholar 

  115. Lehmann, K. et al. 18FDG-PET-CT improves specificity of preoperative lymph-node staging in patients with intestinal but not diffuse-type esophagogastric adenocarcinoma. Eur. J. Surg. Oncol. 43, 196–202 (2017).

    Article  CAS  PubMed  Google Scholar 

  116. Kim, S.-J. & Lee, S.-W. Diagnostic accuracy of 18F-FDG PET/CT for detection of peritoneal carcinomatosis; a systematic review and meta-analysis. Br. J. Radiol. 91, 20170519 (2018).

    Article  PubMed  Google Scholar 

  117. Sugarbaker, P. H. et al. Concerning CT features used to select patients for treatment of peritoneal metastases, a pictoral essay. Int. J. Hyperthermia 33, 497–504 (2017).

    Article  PubMed  Google Scholar 

  118. Chandramohan, A. et al. Communicating imaging findings in peritoneal mesothelioma: the impact of ‘PAUSE’ on surgical decision-making. Insights Imaging 12, 174 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  119. Chandramohan, A., Thrower, A., Smith, S. A., Shah, N. & Moran, B. “PAUSE”: a method for communicating radiological extent of peritoneal malignancy. Clin. Radiol. 72, 972–980 (2017).

    Article  CAS  PubMed  Google Scholar 

  120. Lennartz, S. et al. Iodine overlays to improve differentiation between peritoneal carcinomatosis and benign peritoneal lesions. Eur. Radiol. 30, 3968–3976 (2020).

    Article  CAS  PubMed  Google Scholar 

  121. Darras, K. E. et al. Virtual monoenergetic reconstruction of contrast-enhanced CT scans of the abdomen and pelvis at 40 keV improves the detection of peritoneal metastatic deposits. Abdom. Radiol. 44, 422–428 (2019).

    Article  Google Scholar 

  122. Thivolet, A. et al. Spectral photon-counting CT imaging of colorectal peritoneal metastases: initial experience in rats. Sci. Rep. 10, 13394 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Zhao, L. et al. Role of [68Ga]Ga-DOTA-FAPI-04 PET/CT in the evaluation of peritoneal carcinomatosis and comparison with [18F]-FDG PET/CT. Eur. J. Nucl. Med. Mol. I 48, 1944–1955 (2021).

    Article  CAS  Google Scholar 

  124. Kuten, J. et al. Head-to-head comparison of [68Ga]Ga-FAPI-04 and [18F]-FDG PET/CT in evaluating the extent of disease in gastric adenocarcinoma. Eur. J. Nucl. Med. Mol. Imaging 49, 743–750 (2022).

    Article  CAS  PubMed  Google Scholar 

  125. van’t Sant, I. et al. Seeing the whole picture: added value of MRI for extraperitoneal findings in CRS-HIPEC candidates. Eur. J. Surg. Oncol. 48, 462–469 (2022).

    Article  Google Scholar 

  126. Wang, W. et al. Are positron emission tomography-computed tomography (PET-CT) scans useful in preoperative assessment of patients with peritoneal disease before cytoreductive surgery (CRS) and hyperthermic intraperitoneal chemotherapy (HIPEC)? Int. J. Hyperthermia 34, 524–531 (2018).

    Article  PubMed  Google Scholar 

  127. Vuysere, S. D. et al. Accuracy of whole-body diffusion-weighted MRI (WB-DWI/MRI) in diagnosis, staging and follow-up of gastric cancer, in comparison to CT: a pilot study. BMC Med. Imaging 21, 18 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  128. Dresen, R. C. et al. Whole-body diffusion-weighted MRI for operability assessment in patients with colorectal cancer and peritoneal metastases. Cancer Imaging 19, 1 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  129. Brendle, C. et al. Assessment of metastatic colorectal cancer with hybrid imaging: comparison of reading performance using different combinations of anatomical and functional imaging techniques in PET/MRI and PET/CT in a short case series. Eur. J. Nucl. Med. Mol. I 43, 123–132 (2016).

    Article  CAS  Google Scholar 

  130. Eisenhauer, E. A. et al. New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur. J. Cancer 45, 228–247 (2009).

    Article  CAS  PubMed  Google Scholar 

  131. Bhatt, A. et al. Patterns of peritoneal dissemination and response to systemic chemotherapy in common and rare peritoneal tumours treated by cytoreductive surgery: study protocol of a prospective, multicentre, observational study. BMJ Open 11, e046819 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  132. Bhatt, A. et al. Clinical and radiologic predictors of a pathologic complete response to neoadjuvant chemotherapy (NACT) in patients undergoing cytoreductive surgery for colorectal peritoneal metastases: results of a prospective multi-center study. Ann. Surg. Oncol. 28, 3840–3849 (2021).

    Article  PubMed  Google Scholar 

  133. Liberale, G. et al. Accuracy of FDG-PET/CT in colorectal peritoneal carcinomatosis: potential tool for evaluation of chemotherapeutic response. Anticancer Res. 37, 929–934 (2017).

    Article  CAS  PubMed  Google Scholar 

  134. Park, S. J. et al. Reduction of cycles of neoadjuvant chemotherapy for advanced epithelial ovarian, fallopian or primary peritoneal cancer (ROCOCO): study protocol for a phase III randomized controlled trial. BMC Cancer 20, 385 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Sala, E. et al. Advanced ovarian cancer: multiparametric MR imaging demonstrates response- and metastasis-specific effects. Radiology 263, 149–159 (2012).

    Article  PubMed  Google Scholar 

  136. Himoto, Y. et al. Computed tomography–derived radiomic metrics can identify responders to immunotherapy in ovarian cancer. JCO Precis. Oncol. 3, 1–13 (2019).

    Google Scholar 

  137. Nougaret, S. et al. Radiomics and radiogenomics in ovarian cancer: a literature review. Abdom. Radiol. 46, 2308–2322 (2021).

    Article  CAS  Google Scholar 

  138. Mikkelsen, M. S. et al. Assessment of peritoneal metastases with DW-MRI, CT, and FDG PET/CT before cytoreductive surgery for advanced stage epithelial ovarian cancer. Eur. J. Surg. Oncol. 47, 2134–2141 (2021).

    Article  PubMed  Google Scholar 

  139. Engbersen, M. P. et al. Dedicated MRI staging versus surgical staging of peritoneal metastases in colorectal cancer patients considered for CRS-HIPEC; the DISCO randomized multicenter trial. BMC Cancer 21, 464 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Passot, G. et al. Multicentre study of laparoscopic or open assessment of the peritoneal cancer index (BIG-RENAPE). Br. J. Surg. 105, 663–667 (2018).

    Article  CAS  PubMed  Google Scholar 

  141. Iversen, L. H., Rasmussen, P. C. & Laurberg, S. Value of laparoscopy before cytoreductive surgery and hyperthermic intraperitoneal chemotherapy for peritoneal carcinomatosis. Br. J. Surg. 100, 285–292 (2013).

    Article  CAS  PubMed  Google Scholar 

  142. Sell, N. M. et al. Staging laparoscopy not only saves patients an incision, but may also help them live longer. Ann. Surg. Oncol. 25, 1009–1016 (2018).

    Article  PubMed  Google Scholar 

  143. Allen, C. J. et al. Yield of peritoneal cytology in staging patients with gastric and gastroesophageal cancer. J. Surg. Oncol. 120, 1350–1357 (2019).

    Article  PubMed  Google Scholar 

  144. Blackshaw, G. R. J. C. et al. Laparoscopy significantly improves the perceived preoperative stage of gastric cancer. Gastric Cancer 6, 225–229 (2003).

    Article  PubMed  Google Scholar 

  145. Sarela, A. I., Lefkowitz, R., Brennan, M. F. & Karpeh, M. S. Selection of patients with gastric adenocarcinoma for laparoscopic staging. Am. J. Surg. 191, 134–138 (2006).

    Article  PubMed  Google Scholar 

  146. Passot, G. et al. Postoperative outcomes of laparoscopic vs open cytoreductive surgery plus hyperthermic intraperitoneal chemotherapy for treatment of peritoneal surface malignancies. Eur. J. Surg. Oncol. 40, 957–962 (2014).

    Article  CAS  PubMed  Google Scholar 

  147. Dong, D. et al. Development and validation of an individualized nomogram to identify occult peritoneal metastasis in patients with advanced gastric cancer. Ann. Oncol. 30, 431–438 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  148. Jiang, Y. et al. Predicting peritoneal recurrence and disease-free survival from CT images in gastric cancer with multitask deep learning: a retrospective study. Lancet Digital Heal. 4, e340–e350 (2022).

    Article  Google Scholar 

  149. Passot, G. et al. Pathological response to neoadjuvant chemotherapy: a new prognosis tool for the curative management of peritoneal colorectal carcinomatosis. Ann. Surg. Oncol. 21, 2608–2614 (2014).

    Article  PubMed  Google Scholar 

  150. Goere, D. et al. Second-look surgery plus hyperthermic intraperitoneal chemotherapy versus surveillance in patients at high risk of developing colorectal peritoneal metastases (PROPHYLOCHIP-PRODIGE 15): a randomised, phase 3 study. Lancet Oncol. 21, 1147–1154 (2020).

    Article  CAS  PubMed  Google Scholar 

  151. Bhatt, A. et al. Prospective correlation of the radiological, surgical and pathological findings in patients undergoing cytoreductive surgery for colorectal peritoneal metastases: implications for the preoperative estimation of the peritoneal cancer index. Colorectal Dis. 22, 2123–2132 (2020).

    Article  CAS  PubMed  Google Scholar 

  152. Bhatt, A. & Glehen, O. Extent of peritoneal resection for peritoneal metastases: looking beyond a complete cytoreduction. Ann. Surg. Oncol. 27, 1458–1470 (2020).

    Article  PubMed  Google Scholar 

  153. Veys, I. et al. ICG-fluorescence imaging for detection of peritoneal metastases and residual tumoral scars in locally advanced ovarian cancer: a pilot study. J. Surg. Oncol. 117, 228–235 (2018).

    Article  PubMed  Google Scholar 

  154. Zapardiel, I. et al. Utility of intraoperative fluorescence imaging in gynecologic surgery: systematic review and consensus statement. Ann. Surg. Oncol. 28, 3266–3278 (2021).

    Article  PubMed  Google Scholar 

  155. Bhatt, A. & Glehen, O. ASO author reflections: tailoring the extent of peritoneal resection for peritoneal metastases according to the primary tumor site. Ann. Surg. Oncol. 27, 1471–1472 (2020).

    Article  PubMed  Google Scholar 

  156. Baratti, D., Kusamura, S., Cabras, A. D. & Deraco, M. Cytoreductive surgery with selective versus complete parietal peritonectomy followed by hyperthermic intraperitoneal chemotherapy in patients with diffuse malignant peritoneal mesothelioma: a controlled study. Ann. Surg. Oncol. 19, 1416–1424 (2012).

    Article  PubMed  Google Scholar 

  157. Bhatt, A. et al. Total parietal peritonectomy can be performed with acceptable morbidity for patients with advanced ovarian cancer after neoadjuvant chemotherapy: results from a prospective multi-centric study. Ann. Surg. Oncol. 28, 1118–1129 (2021).

    Article  PubMed  Google Scholar 

  158. Sinukumar, S. et al. A comparison of outcomes following total and selective peritonectomy performed at the time of interval cytoreductive surgery for advanced serous epithelial ovarian, fallopian tube and primary peritoneal cancer–a study by INDEPSO. Eur. J. Surg. Oncol. 47, 75–81 (2021).

    Article  PubMed  Google Scholar 

  159. Lawrence, V. A. et al. Functional independence after major abdominal surgery in the elderly. J. Am. Coll. Surg. 199, 762–772 (2004).

    Article  PubMed  Google Scholar 

  160. Christensen, T. & Kehlet, H. Postoperative fatigue. World J. Surg. 17, 220–225 (1993).

    Article  CAS  PubMed  Google Scholar 

  161. Baratti, D. et al. Postoperative complications after cytoreductive surgery and hyperthermic intraperitoneal chemotherapy affect long-term outcome of patients with peritoneal metastases from colorectal cancer: a two-center study of 101 patients. Dis. Colon Rectum 57, 858–868 (2014).

    Article  CAS  PubMed  Google Scholar 

  162. Ditmyer, M. M., Topp, R. & Pifer, M. Prehabilitation in preparation for orthopaedic surgery. Orthop. Nurs. 21, 43–54 (2002).

    Article  PubMed  Google Scholar 

  163. Hübner, M. et al. Guidelines for perioperative care in cytoreductive surgery (CRS) with or without hyperthermic IntraPEritoneal chemotherapy (HIPEC): enhanced recovery after surgery (ERAS®) Society Recommendations — Part I: preoperative and intraoperative management. Eur. J. Surg. Oncol. 46, 2292–2310 (2020).

    Article  PubMed  Google Scholar 

  164. Hübner, M. et al. Guidelines for perioperative care in cytoreductive surgery (CRS) with or without hyperthermic IntraPEritoneal chemotherapy (HIPEC): enhanced recovery after surgery (ERAS®) society recommendations–Part II: postoperative management and special considerations. Eur. J. Surg. Oncol. 46, 2311–2323 (2020).

    Article  PubMed  Google Scholar 

  165. Dhiman, A. et al. Guide to enhanced recovery for cancer patients undergoing surgery: ERAS for patients undergoing cytoreductive surgery with or without HIPEC. Ann. Surg. Oncol. 28, 6955–6964 (2021).

    Article  PubMed  Google Scholar 

  166. Vashi, P. G. et al. The relationship between baseline nutritional status with subsequent parenteral nutrition and clinical outcomes in cancer patients undergoing hyperthermic intraperitoneal chemotherapy. Nutr. J. 12, 118–118 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  167. Mills, E. et al. Smoking cessation reduces postoperative complications: a systematic review and meta-analysis. Am. J. Med. 124, 144–154.e8 (2011).

    Article  PubMed  Google Scholar 

  168. Thomsen, T., Villebro, N. & Møller, A. M. Interventions for preoperative smoking cessation. Cochrane Database Syst. Rev. 3, CD002294 (2014).

    Google Scholar 

  169. Iqbal, U. et al. Preoperative patient preparation in enhanced recovery pathways. J. Anaesthesiol. Clin. Pharmacol. 35, S14–S23 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  170. Pouwels, S. et al. Preoperative exercise therapy for elective major abdominal surgery: a systematic review. Int. J. Surg. 12, 134–140 (2014).

    Article  PubMed  Google Scholar 

  171. Boukili, I. E. et al. Prehabilitation before major abdominal surgery: evaluation of the impact of a perioperative clinical pathway, a pilot study. Scand. J. Surg. 111, 145749692210833 (2022).

    Article  Google Scholar 

  172. Alyami, M. et al. Cytoreductive surgery and hyperthermic intraperitoneal chemotherapy for peritoneal carcinomatosis in the elderly: a case-controlled, multicenter study. Ann. Surg. Oncol. 23, 737–745 (2016).

    Article  PubMed  Google Scholar 

  173. Dion, L. et al. Ovarian cancer in the elderly: time to move towards a more logical approach to improve prognosis — a study from the FRANCOGYN Group. J. Clin. Med. 9, 1339 (2020).

    Article  PubMed Central  Google Scholar 

  174. Gagniere, J. et al. Cytoreductive surgery and hyperthermic intraperitoneal chemotherapy for the elderly: is it reasonable? a meta-analysis. Ann. Surg. Oncol. 25, 709–719 (2018).

    Article  PubMed  Google Scholar 

  175. Rubenstein, L. Z., Stuck, A. E., Siu, A. L. & Wieland, D. Impacts of geriatric evaluation and management programs on defined outcomes: overview of the evidence. J. Am. Geriatr. Soc. 39, 8S–16S (1991).

    Article  CAS  PubMed  Google Scholar 

  176. Soubeyran, P. et al. Screening for vulnerability in older cancer patients: the ONCODAGE prospective multicenter cohort study. PLoS ONE 9, e115060 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  177. Hamaker, M. E. et al. Frailty screening methods for predicting outcome of a comprehensive geriatric assessment in elderly patients with cancer: a systematic review. Lancet Oncol. 13, e437–e444 (2012).

    Article  PubMed  Google Scholar 

  178. Wildiers, H. et al. International society of geriatric oncology consensus on geriatric assessment in older patients with cancer. J. Clin. Oncol. 32, 2595–2603 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  179. Mohanty, S. et al. Optimal perioperative management of the geriatric patient: a best practices guideline from the american college of surgeons NSQIP and the American Geriatrics Society. J. Am. Coll. Surg. 222, 930–947 (2016).

    Article  PubMed  Google Scholar 

  180. Minnella, E. M. et al. Patients with poor baseline walking capacity are most likely to improve their functional status with multimodal prehabilitation. Surgery 160, 1070–1079 (2016).

    Article  PubMed  Google Scholar 

  181. Roche, M. et al. Feasibility of a prehabilitation programme dedicated to older patients with cancer before complex medical–surgical procedures: the PROADAPT pilot study protocol. BMJ Open 11, e042960 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  182. Falandry, C. et al. Interventions to improve physical performances of older people with cancer before complex medico-surgical procedures. Medicine 99, e21780 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  183. Cederholm, T. et al. GLIM criteria for the diagnosis of malnutrition – a consensus report from the global clinical nutrition community. Clin. Nutr. 38, 1–9 (2019).

    Article  CAS  PubMed  Google Scholar 

  184. Boereboom, C., Doleman, B., Lund, J. N. & Williams, J. P. Systematic review of pre-operative exercise in colorectal cancer patients. Tech. Coloproctol. 20, 81–89 (2016).

    Article  CAS  PubMed  Google Scholar 

  185. Launay-Savary, M.-V. et al. Are enhanced recovery programs in colorectal surgery feasible and useful in the elderly? A systematic review of the literature. J. Visc. Surg. 154, 29–35 (2017).

    Article  PubMed  Google Scholar 

  186. Dedrick, R. L. Theoretical and experimental bases of intraperitoneal chemotherapy. Semin. Oncol. 12 (3 Suppl. 4), 1–6 (1985).

    CAS  PubMed  Google Scholar 

  187. Dedrick, R. L., Myers, C. E., Bungay, P. M. & DeVita, V. T. Pharmacokinetic rationale for peritoneal drug administration in the treatment of ovarian cancer. Cancer Treat. Rep. 62, 1–11 (1978).

    CAS  PubMed  Google Scholar 

  188. Ceelen, W. P. & Flessner, M. F. Intraperitoneal therapy for peritoneal tumors: biophysics and clinical evidence. Nat. Rev. Clin. Oncol. 7, 108–115 (2010).

    Article  PubMed  Google Scholar 

  189. Nagy, J. A., Chang, S.-H., Shih, S.-C., Dvorak, A. M. & Dvorak, H. F. Heterogeneity of the tumor vasculature. Semin. Thromb. Hemost. 36, 321–331 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  190. Heldin, C.-H., Rubin, K., Pietras, K. & Östman, A. High interstitial fluid pressure – an obstacle in cancer therapy. Nat. Rev. Cancer 4, 806–813 (2004).

    Article  CAS  PubMed  Google Scholar 

  191. Spratt, J. S., Adcock, R. A., Muskovin, M., Sherrill, W. & McKeown, J. Clinical delivery system for intraperitoneal hyperthermic chemotherapy. Cancer Res. 40, 256–260 (1980).

    CAS  PubMed  Google Scholar 

  192. Issels, R. D. Hyperthermia adds to chemotherapy. Eur. J. Cancer 44, 2546–2554 (2008).

    Article  CAS  PubMed  Google Scholar 

  193. Reymond, M. A. et al. Feasibility of therapeutic pneumoperitoneum in a large animal model using a microvaporisator. Surg. Endosc. 14, 51–55 (2000).

    Article  CAS  PubMed  Google Scholar 

  194. Reis, A. C. V. et al. Hemodynamic and respiratory implications of high intra-abdominal pressure during HIPEC. Eur. J. surg. Oncol. 46, 1896–1901 (2020).

    Article  PubMed  Google Scholar 

  195. Sugarbaker, P. H. & Jablonski, K. A. Prognostic features of 51 colorectal and 130 appendiceal cancer patients with peritoneal carcinomatosis treated by cytoreductive surgery and intraperitoneal chemotherapy. Ann. Surg. 221, 124–132 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  196. der Speeten, K. V. & Lemoine, L. In Management of Peritoneal Metastases: Cytoreductive Surgery, HIPEC and Beyond (ed. Bhatt A.) 79–102 (Springer, 2017).

  197. Urano, M., Kuroda, M. & Nishimura, Y. For the clinical application of thermochemotherapy given at mild temperatures. Int. J. Hyperthermia 15, 79–107 (1999).

    Article  CAS  PubMed  Google Scholar 

  198. Leunig, M. et al. Interstitial fluid pressure in solid tumors following hyperthermia: possible correlation with therapeutic response. Cancer Res. 52, 487–490 (1992).

    CAS  PubMed  Google Scholar 

  199. Hettinga, J. et al. Mechanism of hyperthermic potentiation of cisplatin action in cisplatin-sensitive and -resistant tumour cells. Br. J. Cancer 75, 1735–1743 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  200. Hettinga, J. V., Konings, A. W. & Kampinga, H. H. Reduction of cellular cisplatin resistance by hyperthermia-a review. Int. J. Hyperthermia 13, 439–457 (1997).

    Article  CAS  PubMed  Google Scholar 

  201. Wallner, K. E. & Li, G. C. Effect of drug exposure duration and sequencing on hyperthermic potentiation of mitomycin-C and cisplatin. Cancer Res. 47, 493–495 (1987).

    CAS  PubMed  Google Scholar 

  202. Yurttas, C. et al. Systematic review of variations in hyperthermic intraperitoneal chemotherapy (HIPEC) for peritoneal metastasis from colorectal cancer. J. Clin. Med. 7, 567 (2018).

    Article  PubMed Central  Google Scholar 

  203. Bhatt, A. et al. HIPEC methodology and regimens: the need for an expert consensus. Ann. Surg. Oncol. 28, 9098–9113 (2021).

    Article  PubMed  Google Scholar 

  204. Driel, W. Jvan et al. Hyperthermic intraperitoneal chemotherapy in ovarian cancer. N. Engl. J. Med. 378, 230–240 (2018).

    Article  PubMed  Google Scholar 

  205. Yang, X.-J. et al. Cytoreductive surgery and hyperthermic intraperitoneal chemotherapy improves survival of patients with peritoneal carcinomatosis from gastric cancer: final results of a phase iii randomized clinical trial. Ann. Surg. Oncol. 18, 1575–1581 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  206. Park, E. J. et al. Pharmacologic properties of the carrier solutions for hyperthermic intraperitoneal chemotherapy: comparative analyses between water and lipid carrier solutions in the rat model. Ann. Surg. Oncol. 25, 3185–3192 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  207. Piché, N. et al. Rationale for heating oxaliplatin for the intraperitoneal treatment of peritoneal carcinomatosis: a study of the effect of heat on intraperitoneal oxaliplatin using a murine model. Ann. Surg. 254, 138–144 (2011).

    Article  PubMed  Google Scholar 

  208. Bespalov, V. G. et al. Comparative efficacy evaluation of catheter intraperitoneal chemotherapy, normothermic and hyperthermic chemoperfusion in a rat model of ascitic ovarian cancer. Int. J. Hyperthermia 34, 545–550 (2017).

    Article  PubMed  Google Scholar 

  209. Raue, W. et al. Multimodal approach for treatment of peritoneal surface malignancies in a tumour-bearing rat model. Int. J. Colorectal Dis. 25, 245–250 (2010).

    Article  PubMed  Google Scholar 

  210. Ortega-Deballon, P. et al. Which method to deliver hyperthermic intraperitoneal chemotherapy with oxaliplatin? An experimental comparison of open and closed techniques. Ann. Surg. Oncol. 17, 1957–1963 (2010).

    Article  PubMed  Google Scholar 

  211. Helderman, R. F. C. P. A. et al. Preclinical in vivo-models to investigate HIPEC; current methodologies and challenges. Cancers 13, 3430 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  212. Lemoine, L. et al. Body surface area-based versus concentration-based intraperitoneal perioperative chemotherapy in a rat model of colorectal peritoneal surface malignancy: pharmacologic guidance towards standardization. Oncotarget 10, 1407–1424 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  213. Löffler, M. W. et al. Pharmacodynamics of oxaliplatin-derived platinum compounds during hyperthermic intraperitoneal chemotherapy (HIPEC): an emerging aspect supporting the rational design of treatment protocols. Ann. Surg. Oncol. 24, 1650–1657 (2017).

    Article  PubMed  Google Scholar 

  214. Elekonawo, F. M. K. et al. Effect of intraperitoneal chemotherapy concentration on morbidity and survival. BJS Open 4, 293–300 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  215. Löke, D. R. et al. Simulating drug penetration during hyperthermic intraperitoneal chemotherapy. Drug Deliv. 28, 145–161 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  216. Prabhu, A. et al. Effect of oxaliplatin-based chemotherapy on chemosensitivity in patients with peritoneal metastasis from colorectal cancer treated with cytoreductive surgery and hyperthermic intraperitoneal chemotherapy: proof-of-concept study. BJS Open 5, zraa075 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  217. Hübner, M. et al. Pressurized IntraPeritoneal aerosol chemotherapy - practical aspects. Eur. J. Surg. Oncol. 43, 1102–1109 (2017).

    Article  PubMed  Google Scholar 

  218. Alyami, M. et al. Pressurised intraperitoneal aerosol chemotherapy: rationale, evidence, and potential indications. Lancet Oncol. 20, e368–e377 (2019).

    Article  PubMed  Google Scholar 

  219. Davigo, A. et al. PIPAC versus HIPEC: cisplatin spatial distribution and diffusion in a swine model. Int. J. Hyperthermia 37, 144–150 (2020).

    Article  CAS  PubMed  Google Scholar 

  220. Solass, W. et al. Reproducibility of the peritoneal regression grading score for assessment of response to therapy in peritoneal metastasis. Histopathology 74, 1014–1024 (2019).

    Article  PubMed  Google Scholar 

  221. Solaß, W., Hetzel, A., Nadiradze, G., Sagynaliev, E. and Reymond, M.A. Description of a novel approach for intraperitoneal drug delivery and the related device. Surg. Endosc. 26, 1849–1855 (2012).

    Article  PubMed  Google Scholar 

  222. Kurtz, F. et al. Feasibility, safety, and efficacy of pressurized intraperitoneal aerosol chemotherapy (PIPAC) for peritoneal metastasis: a registry study. Gastroent Res. Pract. 2018, 2743985 (2018).

    Article  Google Scholar 

  223. Rovers, K. P. et al. Pressurized intraperitoneal aerosol chemotherapy (oxaliplatin) for unresectable colorectal peritoneal metastases: a multicenter, single-arm, phase II trial (CRC-PIPAC). Ann. Surg. Oncol. 28, 5311–5326 (2021).

    Article  PubMed  Google Scholar 

  224. Tempfer, C. B. et al. A phase I, single-arm, open-label, dose escalation study of intraperitoneal cisplatin and doxorubicin in patients with recurrent ovarian cancer and peritoneal carcinomatosis. Gynecol. Oncol. 150, 23–30 (2018).

    Article  CAS  PubMed  Google Scholar 

  225. Kepenekian, V. et al. Non-resectable malignant peritoneal mesothelioma treated with pressurized intraperitoneal aerosol chemotherapy (PIPAC) plus systemic chemotherapy could lead to secondary complete cytoreductive surgery: a cohort study. Ann. Surg. Oncol. 29, 2104–2113 (2022).

    Article  PubMed  Google Scholar 

  226. Ellebaek, S. B. et al. Pressurized intraperitoneal aerosol chemotherapy (PIPAC)-directed treatment of peritoneal metastasis in end-stage colo-rectal cancer patients. Pleura Peritoneum 5, 20200109 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  227. Alyami, M. et al. Pressurized intraperitoneal aerosol chemotherapy (PIPAC) for unresectable peritoneal metastasis from gastric cancer. Eur. J. Surg. Oncol. 47, 123–127 (2020).

    Article  PubMed  Google Scholar 

  228. Ndaw, S. et al. Occupational exposure to platinum drugs during intraperitoneal chemotherapy. Biomonitoring and surface contamination. Toxicol. Lett. 298, 171–176 (2018).

    Article  CAS  PubMed  Google Scholar 

  229. Clerc, D. et al. Current practice and perceptions of safety protocols for the use of intraperitoneal chemotherapy in the operating room: results of the IP-OR international survey. Pleura Peritoneum 6, 39–45 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  230. Tempfer, C., Giger-Pabst, U., Hilal, Z., Dogan, A. & Rezniczek, G. A. Pressurized intraperitoneal aerosol chemotherapy (PIPAC) for peritoneal carcinomatosis: systematic review of clinical and experimental evidence with special emphasis on ovarian cancer. Arch. Gynecol. Obstet. 298, 243–257 (2018).

    Article  PubMed  Google Scholar 

  231. Hübner, M. et al. Consensus guidelines for pressurized intraperitoneal aerosol chemotherapy: technical aspects and treatment protocols. Eur. J. Surg. Oncol. 48, 789–794 (2022).

    Article  PubMed  Google Scholar 

  232. Dumont, F. et al. A phase I dose-escalation study of oxaliplatin delivered via a laparoscopic approach using pressurised intraperitoneal aerosol chemotherapy for advanced peritoneal metastases of gastrointestinal tract cancers. Eur. J. Cancer 140, 37–44 (2020).

    Article  CAS  PubMed  Google Scholar 

  233. Taibi, A. et al. Feasibility and safety of oxaliplatin-based pressurized intraperitoneal aerosol chemotherapy with or without intraoperative intravenous 5-fluorouracil and leucovorin for colorectal peritoneal metastases: a multicenter comparative cohort study. Ann. Surg. Oncol. 29, 5243–5251 (2022).

    Article  PubMed  Google Scholar 

  234. Sande, L. V. D. et al. Intraperitoneal aerosolization of albumin-stabilized paclitaxel nanoparticles (AbraxaneTM) for peritoneal carcinomatosis–a phase I first-in-human study. Pleura Peritoneum 3, 20180112 (2018).

    Google Scholar 

  235. Sgarbura, O. et al. MESOTIP: phase II multicenter randomized trial evaluating the association of PIPAC and systemic chemotherapy vs. systemic chemotherapy alone as 1st-line treatment of malignant peritoneal mesothelioma. Pleura Peritoneum 4, 20190010 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  236. Eveno, C., Jouvin, I. & Pocard, M. PIPAC EstoK 01: pressurized intraperitoneal aerosol chemotherapy with cisplatin and doxorubicin (PIPAC C/D) in gastric peritoneal metastasis: a randomized and multicenter phase II study. Pleura Peritoneum 3, 20180116 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  237. Alyami, M. et al. Unresectable peritoneal metastasis treated by pressurized intraperitoneal aerosol chemotherapy (PIPAC) leading to cytoreductive surgery and hyperthermic intraperitoneal chemotherapy. Eur. J. Surg. Oncol. 47, 128–133 (2021).

    Article  PubMed  Google Scholar 

  238. Tate, S. J., Sande, L. V., de, Ceelen, W. P., Torkington, J. & Parker, A. L. The feasibility of pressurised intraperitoneal aerosolised virotherapy (PIPAV) to administer oncolytic adenoviruses. Pharm 13, 2043 (2021).

    CAS  Google Scholar 

  239. Sugarbaker, P. H., Stuart, O. A., Vidal-Jove, J., Pessagno, A. M. & DeBruijn, E. A. Peritoneal Carcinomatosis: Principles Of Management (Springer, 1996).

  240. Flessner, M. F. The transport barrier in intraperitoneal therapy. Am. J. Physiol. Ren. Physiol. 288, F433–F342 (2005).

    Article  CAS  Google Scholar 

  241. Wilson, R. B. Hypoxia, cytokines and stromal recruitment: parallels between pathophysiology of encapsulating peritoneal sclerosis, endometriosis and peritoneal metastasis. Pleura Peritoneum 3, 20180103 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  242. Seebauer, C. T. et al. Peritoneal carcinomatosis of colorectal cancer is characterized by structural and functional reorganization of the tumor microenvironment inducing senescence and proliferation arrest in cancer cells. Oncoimmunology 5, e1242543 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  243. Wang, E. et al. Abundant intratumoral fibrosis prevents lymphocyte infiltration into peritoneal metastases of colorectal cancer. PLoS ONE 16, e0255049 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  244. Morgan, R. D. et al. Objective responses to first-line neoadjuvant carboplatin–paclitaxel regimens for ovarian, fallopian tube, or primary peritoneal carcinoma (ICON8): post-hoc exploratory analysis of a randomised, phase 3 trial. Lancet Oncol. 22, 277–288 (2021).

    Article  CAS  PubMed  Google Scholar 

  245. Ray-Coquard, I. et al. Olaparib plus bevacizumab as first-line maintenance in ovarian cancer. N. Engl. J. Med. 381, 2416–2428 (2019).

    Article  CAS  PubMed  Google Scholar 

  246. Coleman, R. L. et al. Veliparib with first-line chemotherapy and as maintenance therapy in ovarian cancer. N. Engl. J. Med. 381, 2403–2415 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  247. Ledermann, J. A. et al. Newly diagnosed and relapsed epithelial ovarian carcinoma: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann. Oncol. 24, vi24–vi32 (2013).

    Article  PubMed  Google Scholar 

  248. Winter-Roach, B. A., Kitchener, H. C. & Dickinson, H. O. Adjuvant (post-surgery) chemotherapy for early stage epithelial ovarian cancer. Cochrane Database Syst. Rev. 1, CD004706 (2009).

    Google Scholar 

  249. ICON1. International collaborative ovarian neoplasm trial 1: a randomized trial of adjuvant chemotherapy in women with early-stage ovarian cancer. J. Natl Cancer Inst. 95, 125–132 (2003).

    Article  Google Scholar 

  250. McGuire, W. P. et al. Cyclophosphamide and cisplatin compared with paclitaxel and cisplatin in patients with stage III and stage IV ovarian cancer. N. Engl. J. Med. 334, 1–6 (1996).

    Article  CAS  PubMed  Google Scholar 

  251. Piccart, M. J. et al. Randomized intergroup trial of cisplatin-paclitaxel versus cisplatin-cyclophosphamide in women with advanced epithelial ovarian cancer: three-year results. J. Natl Cancer Inst. 92, 699–708 (2000).

    Article  CAS  PubMed  Google Scholar 

  252. Aghajanian, C. et al. OCEANS: a randomized, double-blind, placebo-controlled phase III trial of chemotherapy with or without bevacizumab in patients with platinum-sensitive recurrent epithelial ovarian, primary peritoneal, or fallopian tube cancer. J. Clin. Oncol. 30, 2039–2045 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  253. Pujade-Lauraine, E. et al. Bevacizumab combined with chemotherapy for platinum-resistant recurrent ovarian cancer: the AURELIA open-label randomized phase III trial. J. Clin. Oncol. 32, 1302–1308 (2014).

    Article  CAS  PubMed  Google Scholar 

  254. Perren, T. J. et al. A phase 3 trial of bevacizumab in ovarian cancer. N. Engl. J. Med. 365, 2484–2496 (2011).

    Article  CAS  PubMed  Google Scholar 

  255. Burger, R. A. et al. Incorporation of bevacizumab in the primary treatment of ovarian cancer. N. Engl. J. Med. 365, 2473–2483 (2011).

    Article  CAS  PubMed  Google Scholar 

  256. Martín, A. G. et al. Exploratory outcome analyses according to stage and/or residual disease in the ICON7 trial of carboplatin and paclitaxel with or without bevacizumab for newly diagnosed ovarian cancer. Gynecol. Oncol. 152, 53–60 (2019).

    Article  Google Scholar 

  257. Monk, B. J. et al. Chemotherapy with or without avelumab followed by avelumab maintenance versus chemotherapy alone in patients with previously untreated epithelial ovarian cancer (JAVELIN Ovarian 100): an open-label, randomised, phase 3 trial. Lancet Oncol. 22, 1275–1289 (2021).

    Article  CAS  PubMed  Google Scholar 

  258. Pujade-Lauraine, E. et al. Avelumab alone or in combination with chemotherapy versus chemotherapy alone in platinum-resistant or platinum-refractory ovarian cancer (JAVELIN Ovarian 200): an open-label, three-arm, randomised, phase 3 study. Lancet Oncol. 22, 1034–1046 (2021).

    Article  CAS  PubMed  Google Scholar 

  259. Konstantinopoulos, P. A. et al. TOPACIO/Keynote-162 (NCT02657889): a phase 1/2 study of niraparib + pembrolizumab in patients (pts) with advanced triple-negative breast cancer or recurrent ovarian cancer (ROC) — results from ROC cohort. J. Clin. Oncol. 36 (suppl. 15), Abstr. 106 (2018).

    Article  Google Scholar 

  260. Drew, Y. et al. 1190PD Phase II study of olaparib + durvalumab (MEDIOLA): updated results in germline BRCA-mutated platinum-sensitive relapsed (PSR) ovarian cancer (OC). Ann. Oncol. 30, v485–v486 (2019).

    Article  Google Scholar 

  261. Zsiros, E. et al. Efficacy and safety of pembrolizumab in combination with Bevacizumab and oral metronomic cyclophosphamide in the treatment of recurrent ovarian cancer. JAMA Oncol. 7, 78–85 (2021).

    Article  PubMed  Google Scholar 

  262. Breuer, E. et al. Site of recurrence and survival after surgery for colorectal peritoneal metastasis. J. Natl Cancer Inst. 113, djab001 (2021).

    Article  Google Scholar 

  263. Franko, J. Therapeutic efficacy of systemic therapy for colorectal peritoneal carcinomatosis: surgeon’s perspective. Pleura Peritoneum 3, 20180102 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  264. Cutsem, E. V., Cervantes, A., Nordlinger, B., Arnold, D. & Group, E. G. W. Metastatic colorectal cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann. Oncol. 25, iii1–iii9 (2014).

    Article  PubMed  Google Scholar 

  265. Nordlinger, B. et al. Perioperative FOLFOX4 chemotherapy and surgery versus surgery alone for resectable liver metastases from colorectal cancer (EORTC 40983): long-term results of a randomised, controlled, phase 3 trial. Lancet Oncol. 14, 1208–1215 (2013).

    Article  CAS  PubMed  Google Scholar 

  266. Loupakis, F. et al. Initial therapy with FOLFOXIRI and bevacizumab for metastatic colorectal cancer. N. Engl. J. Med. 371, 1609–1618 (2014).

    Article  PubMed  Google Scholar 

  267. Cremolini, C. et al. Upfront FOLFOXIRI plus bevacizumab and reintroduction after progression versus mFOLFOX6 plus bevacizumab followed by FOLFIRI plus bevacizumab in the treatment of patients with metastatic colorectal cancer (TRIBE2): a multicentre, open-label, phase 3, randomised, controlled trial. Lancet Oncol. 21, 497–507 (2020).

    Article  CAS  PubMed  Google Scholar 

  268. Ychou, M. et al. Induction chemotherapy (CT) with FOLFIRINOX or FOLFOX/FOLFIRI, plus cetuximab (CET) or bevacizumab (BEV) (by RAS status), in patients (pts) with primarily unresectable colorectal liver metastases (CRLM): results of the randomized UNICANCER PRODIGE 14-ACCORD 21 (METHEP-2) trial. J. Clin. Oncol. 36 (suppl. 15), Abstr. 3535 (2018).

    Article  Google Scholar 

  269. Rovers, K. et al. LBA-6 Safety, feasibility, tolerability, and preliminary efficacy of perioperative systemic therapy for resectable colorectal peritoneal metastases: pilot phase of a randomised trial (CAIRO6). Ann. Oncol. 31, S243 (2020).

    Article  Google Scholar 

  270. Rovers, K. P. et al. Perioperative systemic therapy vs cytoreductive surgery and hyperthermic intraperitoneal chemotherapy alone for resectable colorectal peritoneal metastases. JAMA Surg. 156, 710–720 (2021).

    Article  PubMed  Google Scholar 

  271. Rovers, K. P. et al. Adjuvant systemic chemotherapy vs active surveillance following up-front resection of isolated synchronous colorectal peritoneal metastases. JAMA Oncol. 6, e202701 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  272. Beal, E. W. et al. Impact of neoadjuvant chemotherapy on the outcomes of cytoreductive surgery and hyperthermic intraperitoneal chemotherapy for colorectal peritoneal metastases: a multi-institutional retrospective review. J. Clin. Med. 9, 748 (2020).

    Article  CAS  PubMed Central  Google Scholar 

  273. Waite, K. & Youssef, H. The role of neoadjuvant and adjuvant systemic chemotherapy with cytoreductive surgery and heated intraperitoneal chemotherapy for colorectal peritoneal metastases: a systematic review. Ann. Surg. Oncol. 24, 705–720 (2017).

    Article  PubMed  Google Scholar 

  274. Chau, I. et al. Multivariate prognostic factor analysis in locally advanced and metastatic esophago-gastric cancer-pooled analysis from three multicenter, randomized, controlled trials using individual patient data. J. Clin. Oncol. 22, 2395–2403 (2004).

    Article  PubMed  Google Scholar 

  275. Kim, J. G. et al. Prognostic factors for survival of patients with advanced gastric cancer treated with cisplatin-based chemotherapy. Cancer Chemoth Pharm. 61, 301–307 (2008).

    Article  CAS  Google Scholar 

  276. Thomassen, I. et al. Chemotherapy as palliative treatment for peritoneal carcinomatosis of gastric origin. Acta Oncol. 53, 429–432 (2013).

    Article  PubMed  Google Scholar 

  277. Shitara, K. et al. Nab-paclitaxel versus solvent-based paclitaxel in patients with previously treated advanced gastric cancer (ABSOLUTE): an open-label, randomised, non-inferiority, phase 3 trial. Lancet Gastroenterol. Hepatol. 2, 277–287 (2017).

    Article  PubMed  Google Scholar 

  278. KINOSHITA, J. et al. Comparative study of the antitumor activity of Nab-paclitaxel and intraperitoneal solvent-based paclitaxel regarding peritoneal metastasis in gastric cancer. Oncol. Rep. 32, 89–96 (2014).

    Article  CAS  PubMed  Google Scholar 

  279. Kang, Y.-K. et al. Nivolumab in patients with advanced gastric or gastro-oesophageal junction cancer refractory to, or intolerant of, at least two previous chemotherapy regimens (ONO-4538-12, ATTRACTION-2): a randomised, double-blind, placebo-controlled, phase 3 trial. Lancet 390, 2461–2471 (2017).

    Article  CAS  PubMed  Google Scholar 

  280. Janjigian, Y. Y. et al. First-line nivolumab plus chemotherapy versus chemotherapy alone for advanced gastric, gastro-oesophageal junction, and oesophageal adenocarcinoma (CheckMate 649): a randomised, open-label, phase 3 trial. Lancet 398, 27–40 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  281. Shitara, K. et al. Efficacy and safety of pembrolizumab or pembrolizumab plus chemotherapy vs chemotherapy alone for patients with first-line, advanced gastric cancer: the KEYNOTE-062 phase 3 randomized clinical trial. JAMA Oncol. 6, 1571–1580 (2020).

    Article  PubMed  Google Scholar 

  282. Takahashi, Y. et al. Real-world effectiveness of nivolumab in advanced gastric cancer: the DELIVER trial (JACCRO GC-08). Gastric Cancer 25, 235–244 (2022).

    Article  CAS  PubMed  Google Scholar 

  283. Goere, D., Glehen, O., Mariette, C., Auperin, A. & Elias, D. Results of a phase II randomized study evaluating the potential benefit of a postoperative intraperitoneal immunotherapy after resection of peritoneal metastases from gastric carcinoma metastases (IIPOP-NCT01784900). J. Clin. Oncol. 35 (suppl. 15), Abstr. 4064 (2017).

    Article  Google Scholar 

  284. Thadi, A. et al. Early investigations and recent advances in intraperitoneal immunotherapy for peritoneal metastasis. Vaccines 6, 54 (2018).

    Article  CAS  PubMed Central  Google Scholar 

  285. Vogelzang, N. J. et al. Phase III study of pemetrexed in combination with cisplatin versus cisplatin alone in patients with malignant pleural mesothelioma. J. Clin. Oncol. 21, 2636–2644 (2003).

    Article  CAS  PubMed  Google Scholar 

  286. Jänne, P. A. et al. Open-label study of pemetrexed alone or in combination with cisplatin for the treatment of patients with peritoneal mesothelioma: outcomes of an expanded access program. Clin. Lung Cancer 7, 40–46 (2005).

    Article  PubMed  Google Scholar 

  287. Carteni, G. et al. Malignant peritoneal mesothelioma — results from the International Expanded Access Program using pemetrexed alone or in combination with a platinum agent. Lung Cancer 64, 211–218 (2009).

    Article  CAS  PubMed  Google Scholar 

  288. Obasaju, C. K. et al. Single-arm, open label study of pemetrexed plus cisplatin in chemotherapy naïve patients with malignant pleural mesothelioma: outcomes of an expanded access program. Lung Cancer 55, 187–194 (2007).

    Article  PubMed  Google Scholar 

  289. Kepenekian, V. et al. Diffuse malignant peritoneal mesothelioma: evaluation of systemic chemotherapy with comprehensive treatment through the RENAPE database: multi-institutional retrospective study. Eur. J. Cancer 65, 69–79 (2016).

    Article  CAS  PubMed  Google Scholar 

  290. Deraco, M., Baratti, D., Hutanu, I., Bertuli, R. & Kusamura, S. The role of perioperative systemic chemotherapy in diffuse malignant peritoneal mesothelioma patients treated with cytoreductive surgery and hyperthermic intraperitoneal chemotherapy. Ann. Surg. Oncol. 20, 1093–1100 (2013).

    Article  PubMed  Google Scholar 

  291. Naffouje, S. A., Tulla, K. A. & Salti, G. I. The impact of chemotherapy and its timing on survival in malignant peritoneal mesothelioma treated with complete debulking. Med. Oncol. 35, 69 (2018).

    Article  PubMed  Google Scholar 

  292. Disselhorst, M. J. et al. Ipilimumab and nivolumab in the treatment of recurrent malignant pleural mesothelioma (INITIATE): results of a prospective, single-arm, phase 2 trial. Lancet Respir. Med. 7, 260–270 (2019).

    Article  CAS  PubMed  Google Scholar 

  293. Baas, P. et al. First-line nivolumab plus ipilimumab in unresectable malignant pleural mesothelioma (CheckMate 743): a multicentre, randomised, open-label, phase 3 trial. Lancet 397, 375–386 (2021).

    Article  CAS  PubMed  Google Scholar 

  294. Raghav, K. et al. Clinical efficacy of immune checkpoint inhibitors in patients with advanced malignant peritoneal mesothelioma. JAMA Netw. Open 4, e2119934 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  295. Maio, M. et al. Tremelimumab as second-line or third-line treatment in relapsed malignant mesothelioma (DETERMINE): a multicentre, international, randomised, double-blind, placebo-controlled phase 2b trial. Lancet Oncol. 18, 1261–1273 (2017).

    Article  CAS  PubMed  Google Scholar 

  296. Desai, A. et al. OA08.03 Phase II trial of pembrolizumab (NCT02399371) in previously-treated malignant mesothelioma (MM): final analysis. J. Thorac. Oncol. 13, S339 (2018).

    Article  Google Scholar 

  297. Fennell, D. A. et al. Nivolumab versus placebo in patients with relapsed malignant mesothelioma (CONFIRM): a multicentre, double-blind, randomised, phase 3 trial. Lancet Oncol. 22, 1530–1540 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  298. Blackham, A. U. et al. Perioperative systemic chemotherapy for appendiceal mucinous carcinoma peritonei treated with cytoreductive surgery and hyperthermic intraperitoneal chemotherapy. J. Surg. Oncol. 109, 740–745 (2014).

    Article  PubMed  Google Scholar 

  299. Lu, P. et al. Systemic chemotherapy and survival in patients with metastatic low-grade appendiceal mucinous adenocarcinoma. J. Surg. Oncol. 120, 446–451 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  300. Turner, K. M. et al. Assessment of neoadjuvant chemotherapy on operative parameters and outcome in patients with peritoneal dissemination from high-grade appendiceal cancer. Ann. Surg. Oncol. 20, 1068–1073 (2013).

    Article  PubMed  Google Scholar 

  301. Lieu, C. H. et al. Systemic chemotherapy and surgical cytoreduction for poorly differentiated and signet ring cell adenocarcinomas of the appendix. Ann. Oncol. 23, 652–658 (2012).

    Article  CAS  PubMed  Google Scholar 

  302. Bijelic, L., Kumar, A. S., Stuart, O. A. & Sugarbaker, P. H. Systemic chemotherapy prior to cytoreductive surgery and hipec for carcinomatosis from appendix cancer: impact on perioperative outcomes and short-term survival. Gastroenterol. Res. Pract. 2012, 163284 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  303. Shapiro, J. F. et al. Modern systemic chemotherapy in surgically unresectable neoplasms of appendiceal origin: a single-institution experience. Cancer 116, 316–322 (2010).

    Article  PubMed  Google Scholar 

  304. Munoz-Zuluaga, C. A. et al. Systemic chemotherapy before cytoreductive surgery and hyperthermic intraperitoneal chemotherapy (CRS/HIPEC) in patients with high-grade mucinous carcinoma peritonei of appendiceal origin. Eur. J. Surg. Oncol. 45, 1598–1606 (2019).

    Article  PubMed  Google Scholar 

  305. Baratti, D. et al. Pseudomyxoma peritonei: clinical pathological and biological prognostic factors in patients treated with cytoreductive surgery and hyperthermic intraperitoneal chemotherapy (HIPEC). Ann. Surg. Oncol. 15, 526–534 (2007).

    Article  PubMed  Google Scholar 

  306. Milovanov, V. et al. Systemic chemotherapy (SC) before cytoreductive surgery and hyperthermic intraperitoneal chemotherapy (CRS/HIPEC) in patients with peritoneal mucinous carcinomatosis of appendiceal origin (PMCA). Eur. J. Surg. Oncol. 41, 707–712 (2015).

    Article  CAS  PubMed  Google Scholar 

  307. Choe, J. H. et al. Improved survival with anti-VEGF therapy in the treatment of unresectable appendiceal epithelial neoplasms. Ann. Surg. Oncol. 22, 2578–2584 (2015).

    Article  CAS  PubMed  Google Scholar 

  308. Kus, T. et al. Prediction of peritoneal recurrence in patients with gastric cancer: a multicenter study. J. Gastrointest. Cancer 52, 634–642 (2021).

    Article  PubMed  Google Scholar 

  309. Willett, C. G., Tepper, J. E., Cohen, A. M., Orlow, E. & Welch, C. E. Failure patterns following curative resection of colonic carcinoma. Ann. Surg. 200, 685–690 (1984).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  310. Minton, J. P. et al. Results of a 400-patient carcinoembryonic antigen second-look colorectal cancer study. Cancer 55, 1284–1290 (1985).

    Article  CAS  PubMed  Google Scholar 

  311. Elias, D. et al. Results of systematic second-look surgery in patients at high risk of developing colorectal peritoneal carcinomatosis. Ann. Surg. 247, 445–450 (2008).

    Article  PubMed  Google Scholar 

  312. Sugarbaker, P. H. Revised guidelines for second-look surgery in patients with colon and rectal cancer. Clin. Transl. Oncol. 12, 621–628 (2010).

    Article  PubMed  Google Scholar 

  313. Honoré, C., Goere, D., Souadka, A., Dumont, F. & Elias, D. Definition of patients presenting a high risk of developing peritoneal carcinomatosis after curative surgery for colorectal cancer: a systematic review. Ann. Surg. Oncol. 20, 183–192 (2013).

    Article  PubMed  Google Scholar 

  314. Sugarbaker, P. H. Second-look surgery for colorectal cancer: revised selection factors and new treatment options for greater success. Int. J. Surg. Oncol. 2011, 915078 (2011).

    PubMed  Google Scholar 

  315. Sammartino, P. et al. Proactive management for gastric, colorectal and appendiceal malignancies: preventing peritoneal metastases with hyperthermic intraperitoneal chemotherapy (HIPEC). Indian J. Surg. Oncol. 7, 215–224 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  316. Rekhraj, S. et al. Can intra-operative intraperitoneal free cancer cell detection techniques identify patients at higher recurrence risk following curative colorectal cancer resection: a meta-analysis. Ann. Surg. Oncol. 15, 60–68 (2008).

    Article  PubMed  Google Scholar 

  317. Katoh, H. et al. Prognostic significance of peritoneal tumour cells identified at surgery for colorectal cancer. Br. J. Surg. 96, 769–777 (2009).

    Article  CAS  PubMed  Google Scholar 

  318. Tan, K.-L., Tan, W.-S., Lim, J.-F. & Eu, K.-W. Krukenberg tumors of colorectal origin: a dismal outcome — experience of a tertiary center. Int. J. Colorectal Dis. 25, 233–238 (2009).

    Article  PubMed  Google Scholar 

  319. Cheynel, N. et al. Incidence, patterns of failure, and prognosis of perforated colorectal cancers in a well-defined population. Dis. Colon Rectum 52, 406–411 (2009).

    Article  PubMed  Google Scholar 

  320. van Santvoort, H. C. et al. Peritoneal carcinomatosis in t4 colorectal cancer: occurrence and risk factors. Ann. Surg. Oncol. 21, 1686–1691 (2014).

    Article  PubMed  Google Scholar 

  321. Trilling, B. et al. Intraperitoneal-free cancer cells represent a major prognostic factor in colorectal peritoneal carcinomatosis. Dis. Colon Rectum 59, 615–622 (2016).

    Article  CAS  PubMed  Google Scholar 

  322. Bhatt, A. et al. Patients with extensive regional lymph node involvement (pN2) following potentially curative surgery for colorectal cancer are at increased risk for developing peritoneal metastases: a retrospective single-institution study. Colorectal Dis. 21, 287–296 (2019).

    Article  CAS  PubMed  Google Scholar 

  323. Klaver, C. E. L. et al. Locally advanced colorectal cancer: true peritoneal tumor penetration is associated with peritoneal metastases. Ann. Surg. Oncol. 25, 212–220 (2018).

    Article  PubMed  Google Scholar 

  324. Arrizabalaga, N. B. et al. Prophylactic HIPEC in pT4 colon tumors: proactive approach or overtreatment? Ann. Surg. Oncol. 27, 1094–1100 (2020).

    Article  PubMed  Google Scholar 

  325. Veld, J. V. et al. Synchronous and metachronous peritoneal metastases in patients with left-sided obstructive colon cancer. Ann. Surg. Oncol. 27, 2762–2773 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  326. Elias, D. et al. Results of systematic second-look surgery plus HIPEC in asymptomatic patients presenting a high risk of developing colorectal peritoneal carcinomatosis. Ann. Surg. 254, 289–293 (2011).

    Article  CAS  PubMed  Google Scholar 

  327. Stewart, C. J. R., Hillery, S. & Plattell, C. Protocol for the examination of specimens from patients with primary carcinomas of the colon and rectum. Arch. Pathol. Lab. Med. 133, 1182–1193 (2009). 1359-60-author reply 1360-1.

    Article  Google Scholar 

  328. Panarelli, N. C., Schreiner, A. M., Brandt, S. M., Shepherd, N. A. & Yantiss, R. K. Histologic features and cytologic techniques that aid pathologic stage assessment of colonic adenocarcinoma. Am. J. Surg. Pathol. 37, 1252–1258 (2013).

    Article  PubMed  Google Scholar 

  329. Frankel, W. L. & Jin, M. Serosal surfaces, mucin pools, and deposits, oh my: challenges in staging colorectal carcinoma. Mod. Pathol. 28 (Suppl. 1), S95–S108 (2015).

    Article  PubMed  Google Scholar 

  330. Klaver, C. E. L. et al. Interobserver, intraobserver, and interlaboratory variability in reporting pT4a colon cancer. Virchows Arch. 476, 219–230 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  331. Sun, Z. et al. A novel subclassification of pT2 gastric cancers according to the depth of muscularis propria invasion. Ann. Surg. 249, 768–775 (2009).

    Article  PubMed  Google Scholar 

  332. Park, D. J. et al. Subclassification of pT2 gastric adenocarcinoma according to depth of invasion (pT2a vs pT2b) and lymph node status (pN). Surgery 141, 757–763 (2007).

    Article  PubMed  Google Scholar 

  333. Klaver, C. E. L. et al. Adjuvant hyperthermic intraperitoneal chemotherapy in patients with locally advanced colon cancer (COLOPEC): a multicentre, open-label, randomised trial. Lancet Gastroenterol. Hepatol. 4, 761–770 (2019).

    Article  PubMed  Google Scholar 

  334. Baratti, D. et al. Hyperthermic intraperitoneal chemotherapy (HIPEC) at the time of primary curative surgery in patients with colorectal cancer at high risk for metachronous peritoneal metastases. Ann. Surg. Oncol. 24, 167–175 (2017).

    Article  PubMed  Google Scholar 

  335. Koh, J.-L., Yan, T. D., Glenn, D. & Morris, D. L. Evaluation of preoperative computed tomography in estimating peritoneal cancer index in colorectal peritoneal carcinomatosis. Ann. Surg. Oncol. 16, 327–333 (2009).

    Article  PubMed  Google Scholar 

  336. Nordlinger, B. et al. Adjuvant regional chemotherapy and systemic chemotherapy versus systemic chemotherapy alone in patients with stage II-III colorectal cancer: a multicentre randomised controlled phase III trial. Lancet Oncol. 6, 459–468 (2005).

    Article  CAS  PubMed  Google Scholar 

  337. Sloothaak, D. A. M. et al. Intraperitoneal chemotherapy as adjuvant treatment to prevent peritoneal carcinomatosis of colorectal cancer origin: a systematic review. Br. J. Cancer 111, 1112–1121 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  338. Bennouna, J. et al. Rationale and design of the IROCAS study: multicenter, international, randomized phase 3 trial comparing adjuvant modified (m) FOLFIRINOX to mFOLFOX6 in patients with high-risk stage III (pT4 and/or N2) colon cancer — A UNICANCER GI-PRODIGE Trial. Clin. Colorectal Cancer 18, e69–e73 (2019).

    Article  PubMed  Google Scholar 

  339. Al-Batran, S.-E. et al. Perioperative chemotherapy with fluorouracil plus leucovorin, oxaliplatin, and docetaxel versus fluorouracil or capecitabine plus cisplatin and epirubicin for locally advanced, resectable gastric or gastro-oesophageal junction adenocarcinoma (FLOT4): a randomised, phase 2/3 trial. Lancet 393, 1948–1957 (2019).

    Article  PubMed  Google Scholar 

  340. Arjona-Sánchez, Á. et al. HIPECT4: multicentre, randomized clinical trial to evaluate safety and efficacy of hyperthermic intra-peritoneal chemotherapy (HIPEC) with mitomycin C used during surgery for treatment of locally advanced colorectal carcinoma. BMC cancer 18, 183–188 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  341. Koga, S. et al. Prophylactic therapy for peritoneal recurrence of gastric cancer by continuous hyperthermic peritoneal perfusion with mitomycin C. Cancer 61, 232–237 (1988).

    Article  CAS  PubMed  Google Scholar 

  342. Zhu, L. et al. Prophylactic chemotherapeutic hyperthermic intraperitoneal perfusion reduces peritoneal metastasis in gastric cancer: a retrospective clinical study. BMC Cancer 20, 827 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  343. Yonemura, Y. et al. Intraoperative chemohyperthermic peritoneal perfusion as an adjuvant to gastric cancer: final results of a randomized controlled study. Hepatogastroenterol 48, 1776–1782 (2001).

    CAS  Google Scholar 

  344. Brenkman, H. J. F., Päeva, M., Hillegersberg, R., van, Ruurda, J. P. & Mohammad, N. H. Prophylactic hyperthermic intraperitoneal chemotherapy (HIPEC) for gastric cancer — a systematic review. J. Clin. Med. 8, 1685 (2019).

    Article  CAS  PubMed Central  Google Scholar 

  345. Glehen, O. et al. GASTRICHIP: D2 resection and hyperthermic intraperitoneal chemotherapy in locally advanced gastric carcinoma: a randomized and multicenter phase III study. BMC Cancer 14, 183 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  346. Argani, P. et al. Pediatric mesothelioma with ALK fusions. Am. J. Surg. Pathol. 45, 653–661 (2021).

    Article  PubMed  PubMed Central  Google Scholar 

  347. Desmeules, P. et al. A subset of malignant mesotheliomas in young adults are associated with recurrent EWSR1/FUS-ATF1 fusions. Am. J. Surg. Pathol. 41, 980–988 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  348. Argani, P. et al. EWSR1/FUS-CREB fusions define a distinctive malignant epithelioid neoplasm with predilection for mesothelial-lined cavities. Mod. Pathol. 33, 2233–2243 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  349. Raghav, K. et al. Efficacy, safety and biomarker analysis of combined PD-L1 (atezolizumab) and VEGF (bevacizumab) blockade in advanced malignant peritoneal mesothelioma. Cancer Discov. 11, 2738–2747 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  350. Khanna, S. et al. Malignant mesothelioma effusions are infiltrated by CD3+ T cells highly expressing PD-L1 and the PD-L1+ tumor cells within these effusions are susceptible to ADCC by the anti–PD-L1 antibody avelumab. J. Thorac. Oncol. 11, 1993–2005 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  351. Valmary-Degano, S. et al. Immunohistochemical evaluation of two antibodies against PD-L1 and prognostic significance of PD-L1 expression in epithelioid peritoneal malignant mesothelioma: a RENAPE study. Eur. J. Surg. Oncol. 43, 1915–1923 (2017).

    Article  CAS  PubMed  Google Scholar 

  352. Chapel, D. B. et al. Tumor PD-L1 expression in malignant pleural and peritoneal mesothelioma by Dako PD-L1 22C3 pharmDx and Dako PD-L1 28-8 pharmDx assays. Hum. Pathol. 87, 11–17 (2019).

    Article  CAS  PubMed  Google Scholar 

  353. Arjona-Sánchez, Á. et al. A proposal for modification of the PSOGI classification according to the Ki-67 proliferation index in pseudomyxoma peritonei. Ann. Surg. Oncol. 29, 126–136 (2022).

    Article  PubMed  Google Scholar 

  354. Tokunaga, R. et al. Molecular profiling of appendiceal adenocarcinoma and comparison with right-sided and left-sided colorectal cancer. Clin. Cancer Res. 25, 3096–3103 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  355. Koopman, M. et al. Deficient mismatch repair system in patients with sporadic advanced colorectal cancer. Br. J. Cancer 100, 266–273 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  356. Liu, X. et al. High PD-L1 expression in gastric cancer (GC) patients and correlation with molecular features. Pathol. Res. Pract. 216, 152881 (2020).

    Article  CAS  PubMed  Google Scholar 

  357. Fuchs, C. S. et al. Safety and efficacy of pembrolizumab monotherapy in patients with previously treated advanced gastric and gastroesophageal junction cancer: phase 2 clinical KEYNOTE-059 Trial. JAMA Oncol. 4, e180013 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  358. Wang, F. et al. Safety, efficacy and tumor mutational burden as a biomarker of overall survival benefit in chemo-refractory gastric cancer treated with toripalimab, a PD-1 antibody in phase Ib/II clinical trial NCT02915432. Ann. Oncol. 30, 1479–1486 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  359. Drakes, M. L. et al. Stratification of ovarian tumor pathology by expression of programmed cell death-1 (PD-1) and PD-ligand- 1 (PD-L1) in ovarian cancer. J. Ovarian Res. 11, 43 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  360. Hamanishi, J. et al. Programmed cell death 1 ligand 1 and tumor-infiltrating CD8+ T lymphocytes are prognostic factors of human ovarian cancer. Proc. Natl Acad. Sci. USA 104, 3360–3365 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  361. Verwaal, V. J. et al. Randomized trial of cytoreduction and hyperthermic intraperitoneal chemotherapy versus systemic chemotherapy and palliative surgery in patients with peritoneal carcinomatosis of colorectal cancer. J. Clin. Oncol. 21, 3737–3743 (2003).

    Article  PubMed  Google Scholar 

  362. Verwaal, V. J., Bruin, S., Boot, H., van Slooten, G. & van Tinteren, H. 8-year follow-up of randomized trial: cytoreduction and hyperthermic intraperitoneal chemotherapy versus systemic chemotherapy in patients with peritoneal carcinomatosis of colorectal cancer. Ann. Surg. Oncol. 15, 2426–2432 (2008).

    Article  PubMed  Google Scholar 

  363. Cashin, P. H. et al. Cytoreductive surgery and intraperitoneal chemotherapy versus systemic chemotherapy for colorectal peritoneal metastases: a randomised trial. Eur. J. Cancer 53, 155–162 (2016).

    Article  CAS  PubMed  Google Scholar 

  364. Lemoine, L. et al. Body surface area-based vs concentration-based perioperative intraperitoneal chemotherapy after optimal cytoreductive surgery in colorectal peritoneal surface malignancy treatment: COBOX trial. J. Surg. Oncol. 119, 999–1010 (2019).

    Article  CAS  PubMed  Google Scholar 

  365. Zivanovic, O. et al. Secondary cytoreduction and carboplatin hyperthermic intraperitoneal chemotherapy for platinum-sensitive recurrent ovarian cancer: an MSK team ovary phase II study. J. Clin. Oncol. 39, 2594–2604 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  366. Fagotti, A. et al. Randomized trial of primary debulking surgery versus neoadjuvant chemotherapy for advanced epithelial ovarian cancer (SCORPION-NCT01461850). Int. J. Gynecol. Cancer 30, 1657–1664 (2020).

    Article  PubMed  Google Scholar 

  367. Lim, M. C. et al. Survival after hyperthermic intraperitoneal chemotherapy and primary or interval cytoreductive surgery in ovarian cancer. JAMA Surg. 157, 374–383 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  368. Levine, E. A. et al. A multicenter randomized trial to evaluate hematologic toxicities after hyperthermic intraperitoneal chemotherapy with oxaliplatin or mitomycin in patients with appendiceal tumors. J. Am. Coll. Surg. 226, 434–443 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  369. Wallner, K. E., Banda, M. & Li, G. C. Hyperthermic enhancement of cell killing by mitomycin C in mitomycin C-resistant Chinese hamster ovary cells. Cancer Res. 47, 1308–1312 (1987).

    CAS  PubMed  Google Scholar 

  370. Harrison, L. E., Bryan, M., Pliner, L. & Saunders, T. Phase I trial of pegylated liposomal doxorubicin with hyperthermic intraperitoneal chemotherapy in patients undergoing cytoreduction for advanced intra-abdominal malignancy. Ann. Surg. Oncol. 15, 1407–1413 (2008).

    Article  PubMed  Google Scholar 

  371. Huang, Y., Alzahrani, N. A., Liauw, W., Traiki, T. B. & Morris, D. L. Early postoperative intraperitoneal chemotherapy for low-grade appendiceal mucinous neoplasms with pseudomyxoma peritonei: is it beneficial? Ann. Surg. Oncol. 24, 176–183 (2017).

    Article  PubMed  Google Scholar 

  372. Sugarbaker, P. H. & Chang, D. Cytoreductive surgery plus HIPEC with and without NIPEC for malignant peritoneal mesothelioma: a propensity-matched analysis. Ann. Surg. Oncol. 28, 7109–7117 (2021).

    Article  PubMed  Google Scholar 

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Acknowledgements

The authors thank L. Villeneuve (of the Service de Recherche et d’Epidémiologie Cliniques, Hôpital Lyon Sud, Hospices Civils de Lyon, Université Claude Bernard Lyon-1) for assistance with obtaining relevant articles for this Review.

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Authors and Affiliations

  1. Surgical Oncology Department, Hôpital Lyon Sud, Hospices Civils de Lyon, Pierre Bénite, France

    Vahan Kepenekian, Naoual Bakrin, Guillaume Passot & Olivier Glehen

  2. CICLY – EA3738, Université Claude Bernard Lyon I (UCBL1), Lyon, France

    Vahan Kepenekian, Nazim Benzerdjeb, Naoual Bakrin, Guillaume Passot, Pascal Rousset & Olivier Glehen

  3. Department of Surgical Oncology, Zydus hospital, Ahmedabad, Gujarat, India

    Aditi Bhatt

  4. Medical Oncology Department, Hôpital Lyon Sud, Hospices Civils de Lyon, Pierre Bénite, France

    Julien Péron

  5. Laboratoire de Biométrie et Biologie Evolutive, Equipe Biostatistique-Santé, UCBL1, Lyon, France

    Julien Péron

  6. Department of General Surgery and Surgical Oncology, Oncology Center, King Khalid Hospital, Najran, Saudi Arabia

    Mohammad Alyami

  7. Department of Pathology, Institut de Pathologie Multisite, Hospices Civils de Lyon, UCBL1, Lyon, France

    Nazim Benzerdjeb

  8. Department of Onco-Geriatry, Hôpital Lyon Sud, Hospices Civils de Lyon, Lyon, France

    Claire Falandry

  9. Department of Radiology, Hôpital Lyon Sud, Hospices Civils de Lyon, UCBL1, Lyon, France

    Pascal Rousset

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O.G. has acted as a consultant for Gamida. The other authors declare no competing interests.

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Nature Reviews Clinical Oncology thanks C. Chan, I. de Hingh and D. L. Morris for their contribution to the peer review of this work.

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Kepenekian, V., Bhatt, A., Péron, J. et al. Advances in the management of peritoneal malignancies. Nat Rev Clin Oncol 19, 698–718 (2022). https://doi.org/10.1038/s41571-022-00675-5

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