Skip to main content

Colorectal Peritoneal Metastases: Correlating Histopathological Findings and Disease Biology

  • Chapter
  • First Online:
Pathology of Peritoneal Metastases

Abstract

Cytoreductive surgery with or without HIPEC is a potentially curative approach for a small percentage of patients with colorectal peritoneal metastases. In patients undergoing surgery, the survival is significantly prolonged over systemic chemotherapy alone. Locoregional recurrence and disease progression which occurs in over 80% of the patients remains a problem. Completeness of cytoreduction and the surgical peritoneal cancer index (PCI) are the two most important prognostic factors determining treatment outcomes. Even in patients with a low PCI and complete cytoreduction, recurrence is common. Clinical research is focused on searching for molecular markers that can identify poor candidates for the procedure. Some aspects of disease biology and evolution of peritoneal metastases are still poorly understood which could be used to determine patient prognosis and develop different therapeutic approaches. Not all patients benefit from HIPEC, there may be some in whom systemic chemotherapy is not required and prophylactic approaches have failed to prevent PM in clinical trials so far. Neoadjuvant chemotherapy is offered to many patients with both resectable and unresectable disease. The pathological response to chemotherapy has prognostic value but has not been utilized for therapeutic decision making. This chapter focuses on routine histopathological findings that could be further exploited to better evaluate prognosis and treat patients.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 79.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 99.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 129.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Glehen O, Sugarbaker PH, Elias D, et al. Cytoreductive surgery combined with perioperative intraperitoneal chemotherapy for the management of peritoneal carcinomatosis from colorectal cancer: a multi-institutional study. J Clin Oncol. 2004;22:3284–92.

    CAS  PubMed  Google Scholar 

  2. Elias D, Gilly F, Boutitie F, 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. 2010;28(1):63–8.

    PubMed  Google Scholar 

  3. Gelli M, Huguenin JFL, de Baere T, Benhaim L, Mariani A, Boige V, Malka D, Sourouille I, Ducreux M, Elias D, Goéré D. Peritoneal and extraperitoneal relapse after previous curative treatment of peritoneal metastases from colorectal cancer: what survival can we expect? Eur J Cancer. 2018;100:94–103. https://doi.org/10.1016/j.ejca.2018.04.015. Epub 5 Jul 2018.

    Article  PubMed  Google Scholar 

  4. Kwakman R, Schrama AM, van Olmen JP, et al. Clinicopathological parameters in patient selection for cytoreductive surgery and hyperthermic intraperitoneal chemotherapy for colorectal cancer metastases: a meta-analysis. Ann Surg. 2016;263(6):1102–11.

    PubMed  Google Scholar 

  5. Demey K, Wolthuis A, de Buck van Overstraeten A, et al. External validation of the prognostic nomogram (COMPASS) for patients with peritoneal carcinomatosis of colorectal cancer. Ann Surg Oncol. 2017;24(12):3604–8.

    PubMed  Google Scholar 

  6. Sadanandam A, Wang X, de Sousa E, Melo F, Gray JW, Vermeulen L, Hanahan D, Medema JP. Reconciliation of classification systems defining molecular subtypes of colorectal cancer: interrelationships and clinical implications. Cell Cycle. 2014;13:353–7.

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Kelly KJ, Alsayadnasser M, Vaida F, Veerapong J, Baumgartner JM, Patel S, Ahmad S, Barone R, Lowy AM. Does primary tumor side matter in patients with metastatic colon cancer treated with cytoreductive surgery and hyperthermic intraperitoneal chemotherapy? Ann Surg Oncol. 2019;26(5):1421–7. https://doi.org/10.1245/s10434-019-07255-5. Epub 27 Feb 2019.

    Article  PubMed  Google Scholar 

  8. Tonello M, Sommariva A, Pirozzolo G, Mattara G, Pilati P. Colic and rectal tumors with peritoneal metastases treated with cytoreductive surgery and HIPEC: one homogeneous condition or two different diseases? A systematic review and meta-analysis. Eur J Surg Oncol. 2019;45(11):2003–8. https://doi.org/10.1016/j.ejso.2019.06.020. Epub 12 Jun 2019.

    Article  PubMed  Google Scholar 

  9. Bhatt A, Kammar P, Mehta S, et al. Chasing rainbows? The possibility of “cure” in patients with colorectal peritoneal metastases undergoing cytoreductive surgery and HIPEC—a retrospective study by INDEPSO. Indian J Surg Oncol. 2019;10(Suppl 1):49.

    PubMed  PubMed Central  Google Scholar 

  10. Yonemura Y, Canbay E, Ishibashi H. Prognostic factors of peritoneal metastases from colorectal cancer following cytoreductive surgery and perioperative chemotherapy. Sci World J. 2013;2013:978394. https://doi.org/10.1155/2013/978394.

    Article  Google Scholar 

  11. Passot G, You B, Boschetti G, Fontaine J, Isaac S, Decullier E, Maurice C, Vaudoyer D, Gilly FN, Cotte E, Glehen O. Pathological response to neoadjuvant chemotherapy: a new prognosis tool for the curative management of peritoneal colorectal carcinomatosis. Ann Surg Oncol. 2014;21(8):2608–14. https://doi.org/10.1245/s10434-014-3647-0.

    Article  PubMed  Google Scholar 

  12. Kinzler KW, Vogelstein B. Lessons from hereditary colorectal cancer. Cell. 1996;87:159–70.

    CAS  PubMed  Google Scholar 

  13. Baran B, Mert Ozupek N, Yerli Tetik N, Acar E, Bekcioglu O, Baskin Y. Difference between left-sided and right-sided colorectal cancer: a focused review of literature. Gastroenterol Res. 2018;11(4):264–73. https://doi.org/10.14740/gr1062w.

    Article  CAS  Google Scholar 

  14. Paschke S, Jafarov S, Staib L, et al. Are colon and rectal cancer two different tumor entities? A proposal to abandon the term colorectal cancer. Int J Mol Sci. 2018;19(9):2577. https://doi.org/10.3390/ijms19092577. Published 30 Aug 2018.

    Article  CAS  PubMed Central  Google Scholar 

  15. Hugen N, Brown G, Glynne-Jones R, de Wilt JH, Nagtegaal ID. Advances in the care of patients with mucinous colorectal cancer. Nat Rev Clin Oncol. 2016;13(6):361–9. https://doi.org/10.1038/nrclinonc.2015.140. Epub 1 Sept 2015.

    Article  CAS  PubMed  Google Scholar 

  16. Bosman FT, Carneiro F, Hruban RH, Theise ND. WHO classification of tumours of the digestive system. 4th ed. Geneva: World Health Organization Classification of Tumours; 2010.

    Google Scholar 

  17. Hugen N, van Beek JJP, de Wilt JHW, Nagtegaal ID. Insight into mucinous colorectal carcinoma: clues from etiology. Ann Surg Oncol. 2014;21(9):2963–70. https://doi.org/10.1245/s10434-014-3706-6.

    Article  PubMed  Google Scholar 

  18. Hugen N, Simons M, Halilovic A, van der Post RS, Bogers AJ, Marijnissen-van Zanten MA, et al. The molecular background of mucinous carcinoma beyond MUC2. J Pathol Clin Res. 2015;1(1):3–17. https://doi.org/10.1002/cjp2.1.

    Article  CAS  PubMed  Google Scholar 

  19. Pande R, Sunga A, Levea C, Wilding GE, Bshara W, Reid M, Fakih MG. Significance of signet-ring cells in patients with colorectal cancer. Dis Colon Rectum. 2008;51:50–5.

    PubMed  Google Scholar 

  20. Yun SO, Cho YB, Lee WY, et al. Clinical significance of signet-ring-cell colorectal cancer as a prognostic factor. Ann Coloproctol. 2017;33(6):232–8. https://doi.org/10.3393/ac.2017.33.6.232.

    Article  PubMed  PubMed Central  Google Scholar 

  21. Jayne D. Molecular biology of peritoneal carcinomatosis. Cancer Treat Res. 2007;134:21–33.

    CAS  PubMed  Google Scholar 

  22. Murphy EM, Sexton R, Moran BJ. Early results of surgery in 123 patients with pseudomyxoma peritonei from a perforated appendiceal neoplasm. Dis Colon Rectum. 2007;50:37–42.

    PubMed  Google Scholar 

  23. Sugarbaker PH. Peritoneum as the first-line of defense in carcinomatosis. J Surg Oncol. 2007;95:93–6.

    PubMed  Google Scholar 

  24. Kostić Z, Cuk V, Bokun R, Ignjatović D, Usaj-Knezević S, Ignjatović M. Detection of free cancer cells in peritoneal cavity in patients surgically treated for gastric adenocarcinoma. Vojnosanit Pregl. 2006;63:349–56.

    PubMed  Google Scholar 

  25. Joyce JA, Pollard JW. Microenvironmental regulation of metastasis. Nat Rev Cancer. 2009;9(4):239–52.

    CAS  PubMed  Google Scholar 

  26. Sluiter N, De Cuba E, Kwakman R, Kazemier G, Meijer G, Te Velde EA. Adhesion molecules in peritoneal dissemination: function, prognostic relevance and therapeutic options. Clin Exp Metastasis. 2016;33:401–16.

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Lemoine L, Sugarbaker P, Van der Speeten K. Pathophysiology of colorectal peritoneal carcinomatosis: role of the peritoneum. World J Gastroenterol. 2016;22(34):7692–707. https://doi.org/10.3748/wjg.v22.i34.7692.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Yonemura Y, Kawamura T, Bandou E, Tsukiyama G, Endou Y, Miura M. The natural history of free cancer cells in the peritoneal cavity. In: Gonzalez-Moreno S, editor. Advances in peritoneal surface oncology. Berlin: Springer-Verlag Berlin Heidelberg; 2007. p. 11–23.

    Google Scholar 

  29. Yonemura Y, Endo Y, Obata T, Sasaki T. Recent advances in the treatment of peritoneal dissemination of gastrointestinal cancers by nucleoside antimetabolites. Cancer Sci. 2007;98:11–8.

    CAS  PubMed  Google Scholar 

  30. Shimotsuma M, Shields JW, Simpson-Morgan MW, et al. Morpho-physiological function and role of omental milky spots as omentum associated lymphoid tissue (OALT) in the peritoneal cavity. Lymphology. 1993;26:90–101.

    CAS  PubMed  Google Scholar 

  31. Ge W, Chen G, Fan XS. Pathway of peritoneal carcinomatosis maybe hematogenous metastasis rather than peritoneal seeding. Oncotarget. 2017;8(25):41549–54. https://doi.org/10.18632/oncotarget.14607.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Bae SJ, Shin US, Ki YJ, Cho SS, Moon SM, Park SH. Role of peritoneal lavage cytology and prediction of prognosis and peritoneal recurrence after curative surgery for colorectal cancer. Ann Coloproctol. 2014;30:266–73.

    PubMed  PubMed Central  Google Scholar 

  33. Cotte E, Peyrat P, Piaton E, et al., EVOCAPE Group. Lack of prognostic significance of conventional peritoneal cytology in colorectal and gastric cancers: results of EVOCAPE 2 multicentre prospective study. Eur J Surg Oncol. 2013;39:707–714.

    Google Scholar 

  34. Sugarbaker PH. Surgical management of carcinomatosis from colorectal cancer. Clin Colon Rectal Surg. 2005;18(3):190–203. https://doi.org/10.1055/s-2005-916280.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Sugarbaker PH. Observations concerning cancer spread within the peritoneal cavity and concepts supporting an ordered pathophysiology. In: Sugarbaker PH, editor. Peritoneal carcinomatosis: principles of management. Boston, MA: Kluwer Academic Publisher; 1995. p. 80–99.

    Google Scholar 

  36. Bhatt A, Yonemura Y, Benzerdjeb N, Mehta S, Mishra S, Parikh L, Kammar P, et al. Pathological assessment of cytoreductive surgery specimens and its unexplored prognostic potential—a prospective multi-centric study. Eur J Surg Oncol. 2019;45(12):2398–2404. https://doi.org/10.1016/j.ejso.2019.07.019.

  37. Boogerd LSF, Hoogstins CES, Schaap DP, et al. Safety and effectiveness of SGM-101, a fluorescent antibody targeting carcinoembryonic antigen, for intraoperative detection of colorectal cancer: a dose-escalation pilot study. Lancet Gastroenterol Hepatol. 2018;45(12):2398–404.

    Google Scholar 

  38. Hentzen JEKR, Rovers KP, Kuipers H, van der Plas WY, Been LB, Hoogwater FJH, van Ginkel RJ, Hemmer PHJ, van Dam GM, de Hingh IHJT, Kruijff S. Impact of synchronous versus metachronous onset of colorectal peritoneal metastases on survival outcomes after cytoreductive surgery (CRS) with hyperthermic intraperitoneal chemotherapy (HIPEC): a multicenter, retrospective, observational study. Ann Surg Oncol. 2019;26(7):2210–21. https://doi.org/10.1245/s10434-019-07294-y. Epub 15 Mar 2019.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Harlaar NJ, Koller M, de Jongh SJ, et al. Molecular fluorescence-guided surgery of peritoneal carcinomatosis of colorectal origin: a single-centre feasibility study. Lancet Gastroenterol Hepatol. 2016;1:283–90.

    PubMed  Google Scholar 

  40. Kusamura S, Baratti D, Zaffaroni N, Villa R, Laterza B, Balestra MR, et al. Pathophysiology and biology of peritoneal carcinomatosis. World J Gastrointest Oncol. 2010;2(1):12–8.

    PubMed  PubMed Central  Google Scholar 

  41. Verwaal VJ, van Tinteren H, van Ruth S, et al. Predicting the survival of patients with peritoneal carcinomatosis of colorectal origin treated by aggressive cytoreduction and hyperthermic intraperitoneal chemotherapy. Br J Surg. 2004;91:739–46.

    CAS  PubMed  Google Scholar 

  42. Rovers KP, Simkens GA, Punt CJ, van Dieren S, Tanis PJ, de Hingh IH. Perioperative systemic therapy for resectable colorectal peritoneal metastases: sufficient evidence for its widespread use? A critical systematic review. Crit Rev Oncol Hematol. 2017;114:53–62. https://doi.org/10.1016/j.critrevonc.2017.03.028.

    Article  PubMed  Google Scholar 

  43. Burz C, Pop VV, Buiga R, Daniel S, Samasca G, Aldea C, Lupan I. Circulating tumor cells in clinical research and monitoring patients with colorectal cancer. Oncotarget. 2018;9(36):24561–71. https://doi.org/10.18632/oncotarget.25337.

    Article  PubMed  PubMed Central  Google Scholar 

  44. Melero JT, Ortega FG, Gonzalez AM, Carmona-Saez P, Garcia Puche JL, Sugarbaker PH, Delgado M, Lorente JA, Serrano MJ. Prognostic factor analysis of circulating tumor cells in peripheral blood of patients with peritoneal carcinomatosis of colon cancer origin treated with cytoreductive surgery plus an intraoperative hyperthermic intraperitoneal chemotherapy procedure (CRS + HIPEC). Surgery. 2016;159(3):728–35. https://doi.org/10.1016/j.surg.2015.09.013. Epub 28 Oct 2015.

    Article  PubMed  Google Scholar 

  45. Silverman PM. The subperitoneal space: mechanisms of tumour spread in the peritoneal cavity, mesentery, and omentum. Cancer Imaging. 2003;4(1):25–9. https://doi.org/10.1102/1470-7330.2003.0027.

    Article  PubMed  PubMed Central  Google Scholar 

  46. Carmignani CP, Sugarbaker TA, Bromley CM, Sugarbaker PH. Intraperitoneal cancer dissemination: mechanisms of the patterns of spread. Cancer Metastasis Rev. 2003;22:465–72.

    PubMed  Google Scholar 

  47. Sugarbaker PH. Colorectal cancer: prevention and management of metastatic disease. Biomed Res Int. 2014;2014:782890.

    PubMed  PubMed Central  Google Scholar 

  48. Passot G, Vaudoyer D, Cotte E, You B, Isaac S, Gilly FN, et al. Progression following neoadjuvant systemic chemotherapy may not be a contraindication to a curative approach for colorectal carcinomatosis. Ann Surg. 2012;256:125–9.

    PubMed  Google Scholar 

  49. Goere D, Glehen O, Quenet F, Ducreux M, Guilloit JM, Texier M, Benhamou E, Elias D. Results of a randomized phase 3 study evaluating the potential benefit of a second-look surgery plus HIPEC in patients at high risk of developing colorectal peritoneal metastases (PROPHYLOCHIP-NTC01226394). J Clin Oncol. 2018;36(15 Suppl):3531.

    Google Scholar 

  50. Klaver CEL, Stam R, Sloothaak DAM, et al. Colorectal cancer at high risk of peritoneal metastases; long term outcomes of a pilot study on adjuvant laparoscopic HIPEC and future perspectives. Oncotarget. 2017;8:51200–9.

    PubMed  PubMed Central  Google Scholar 

  51. Sobhani I, Itti E, Luciani A, Baumgaertner I, Layese R, André T, Ducreux M, Gornet JM, Goujon G, Aparicio T, Taieb J, Bachet JB, Hemery F, Retbi A, Mons M, Flicoteaux R, Rhein B, Baron S, Cherrak I, Rufat P, Le Corvoisier P, de’Angelis N, Natella PA, Maoulida H, Tournigand C, Durand Zaleski I, Bastuji-Garin S. Colorectal cancer (CRC) monitoring by 6-monthly 18FDG-PET/CT: an open-label multicentre randomised trial. Ann Oncol. 2018;29(4):931–7. https://doi.org/10.1093/annonc/mdy031.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Low RN. Preoperative and surveillance MR imaging of patients undergoing cytoreductive surgery and heated intraperitoneal chemotherapy. J Gastrointest Oncol. 2016;7(1):58–71. https://doi.org/10.3978/j.issn.2078-6891.2015.115.

    Article  PubMed  PubMed Central  Google Scholar 

  53. Kim J, Park EY, Kim O, Schilder JM, Coffey DM, Cho CH, Bast RC Jr. Cell origins of high-grade serous ovarian cancer. Cancers (Basel). 2018;10(11):433. https://doi.org/10.3390/cancers10110433.

    Article  CAS  PubMed Central  Google Scholar 

  54. Honoré C, Gelli M, Francoual J, Benhaim L, Elias D, Goéré D. Ninety percent of the adverse outcomes occur in 10% of patients: can we identify the populations at high risk of developing peritoneal metastases after curative surgery for colorectal cancer? Int J Hyperthermia. 2017;33(5):505–10. https://doi.org/10.1080/02656736.2017.1306119.

    Article  PubMed  Google Scholar 

  55. Bhatt A, Yonemura Y, Mehta S, Benjerdjeb N, Kammar P, Parikh L, et al. Target region resection in patients undergoing cytoreductive surgery for peritoneal metastases-is it necessary in absence of visible disease? Eur J Surg Oncol. 2019;46(4):582–89. https://doi.org/10.1016/j.ejso.2019.11.495.

  56. Jonjić N, Peri G, Bernasconi S, Sciacca FL, Colotta F, Pelicci P, Lanfrancone L, Mantovani A. Expression of adhesion molecules and chemotactic cytokines in cultured human mesothelial cells. J Exp Med. 1992;176:1165–74.

    PubMed  Google Scholar 

  57. Klein CL, Bittinger F, Skarke CC, Wagner M, Köhler H, Walgenbach S, Kirkpatrick CJ. Effects of cytokines on the expression of cell adhesion molecules by cultured human omental mesothelial cells. Pathobiology. 1995;63:204–12.

    CAS  PubMed  Google Scholar 

  58. Müller J, Yoshida T. Interaction of murine peritoneal leukocytes and mesothelial cells: in vitro model system to survey cellular events on serosal membranes during inflammation. Clin Immunol Immunopathol. 1995;75:231–8.

    PubMed  Google Scholar 

  59. Alzahrani NA, Valle SJ, Fisher OM, Sugarbaker PH, Yonemura Y, Glehen O, Goere D, Honore C, Brigand C, de Hingh I, Verwaal VJ, Deraco M, Baratti D, Kusamura S, Pocard M, Piso P, Maerz L, Marchal F, Moran B, Levine EA, Dumont F, Pezet D, Abboud K, Kozman MA, Liauw W, Morris DL, Peritoneal Surface Oncology Group International (PSOGI) and Big-RENAPE Groups. Iterative cytoreductive surgery with or without hyperthermic intraperitoneal chemotherapy for colorectal peritoneal metastases: a multi-institutional experience. J Surg Oncol. 2019;119:336–46.

    CAS  PubMed  Google Scholar 

  60. Brandl A, Weiss S, von Winterfeld M, Krannich A, Feist M, Pratschke J, Raue W, Rau B. Predictive value of peritoneal cancer index for survival in patients with mucinous peritoneal malignancies treated with cytoreductive surgery and hyperthermic intraperitoneal chemotherapy: a single centre experience. Int J Hyperthermia. 2018;34(5):512–7. https://doi.org/10.1080/02656736.2017.1351627. Epub 26 Jul 2017.

    Article  PubMed  Google Scholar 

  61. Sugarbaker PH. Peritonectomy procedures. Ann Surg. 1995;221(1):29–42.

    CAS  PubMed  PubMed Central  Google Scholar 

  62. Moran BJ, Tzivanakis A. The concept of “Obstruction-Free Survival” as an outcome measure in advanced colorectal cancer management. Pleura Peritoneum. 2018;3(1):20180101. https://doi.org/10.1515/pp-2018-0101.

    Article  PubMed  PubMed Central  Google Scholar 

  63. Quenet F, Elias D, Roca L, et al. A UNICANCER phase III trial of hyperthermic intra-peritoneal chemotherapy (HIPEC) for colorectal peritoneal carcinomatosis (PC): PRODIGE 7. Proc Am Soc Clin Oncol. 2018;36:LBA3503. (abstr).

    Google Scholar 

  64. Sgarbura O, Samalin E, Carrere S, Mazard T, de Forges H, Alline M, Pissas MH, Portales F, Ychou M, Quenet F. Preoperative intraperitoneal oxaliplatin for unresectable peritoneal carcinomatosis of colorectal origin: a pilot study. Pleura Peritoneum. 2016;1(4):209–15. https://doi.org/10.1515/pp-2016-0018. Epub 21 Dec 2016.

    Article  PubMed  PubMed Central  Google Scholar 

  65. Mirnezami R, Mehta AM, Chandrakumaran K, Cecil T, Moran BJ, Carr N, Verwaal VJ, Mohamed F, Mirnezami AH. Cytoreductive surgery in combination with hyperthermic intraperitoneal chemotherapy improves survival in patients with colorectal peritoneal metastases compared with systemic chemotherapy alone. Br J Cancer. 2014;111(8):1500–8.

    CAS  PubMed  PubMed Central  Google Scholar 

  66. Sluiter NR, Rovers KP, Salhi Y, Vlek SL, Coupé VMH, Verheul HMW, Kazemier G, de Hingh IHJT, Tuynman JB. Metachronous peritoneal metastases after adjuvant chemotherapy are associated with poor outcome after cytoreduction and HIPEC. Ann Surg Oncol. 2018;25(8):2347–56. https://doi.org/10.1245/s10434-018-6539-x. Epub 31 May 2018.

    Article  PubMed  PubMed Central  Google Scholar 

  67. Klaver CEL, Wisselink DD, Punt CJA, Snaebjornsson P, Crezee J, Aalbers AGJ, et al., COLOPEC Collaborators Group. Adjuvant hyperthermic intraperitoneal chemotherapy in patients with locally advanced colon cancer (COLOPEC): a multicentre, open-label, randomised trial. Lancet Gastroenterol Hepatol. 2019;4(10):761–770. https://doi.org/10.1016/S2468-1253(19)30239-0. Epub 29 Jul 2019.

  68. Schneider MA, Eden J, Pache B, Laminger F, Lopez-Lopez V, Steffen T, Hübner M, Kober F, Roka S, Campos PC, Roth L, Gupta A, Siebenhüner A, Kepenekian V, Passot G, Gertsch P, Glehen O, Lehmann K. Mutations of RAS/RAF proto-oncogenes impair survival after cytoreductive surgery and HIPEC for peritoneal metastasis of colorectal origin. Ann Surg. 2018;268(5):845–53.

    PubMed  Google Scholar 

  69. Graf W, Cashin PH, Ghanipour L, et al. Prognostic impact of BRAF and KRAS mutation in patients with colorectal and appendiceal peritoneal metastases scheduled for CRS and HIPEC. Ann Surg Oncol. 2020;27:293–300. https://doi.org/10.1245/s10434-019-07452-2.

    Article  PubMed  Google Scholar 

  70. Massalou D, Benizri E, Chevallier A, et al. Peritoneal carcinomatosis of colorectal cancer: novel clinical and molecular outcomes. Am J Surg. 2017;213(2):377–87.

    PubMed  Google Scholar 

  71. de Cuba EM, de Hingh IH, Sluiter NR, Kwakman R, Coupé VM, Beliën JA, Verwaal VJ, Meijerink WJ, Delis-van Diemen PM, Bonjer HJ, Meijer GA, Te Velde EA. Angiogenesis-related markers and prognosis after cytoreductive surgery and hyperthermic intraperitoneal chemotherapy for metastatic colorectal cancer. Ann Surg Oncol. 2016;23(5):1601–8. https://doi.org/10.1245/s10434-015-5023-0. Epub 4 Jan 2016.

    Article  PubMed  PubMed Central  Google Scholar 

  72. Jacquet P. Sugarbaker PH Current methodologies for clinical assessment of patients with peritoneal carcinomatosis. J Exp Clin Cancer Res. 1996;15:49–58.

    Google Scholar 

  73. Swellengrebel HA, Zoetmulder FA, Smeenk RM, Antonini N, Verwaal VJ. Quantitative intra-operative assessment of peritoneal carcinomatosis—a comparison of three prognostic tools. Eur J Surg Oncol. 2009;35(10):1078–84. https://doi.org/10.1016/j.ejso.2009.02.010. Epub 13 Mar 2009.

    Article  CAS  PubMed  Google Scholar 

  74. Harmon RL, Sugarbaker PH. Prognostic indicators in peritoneal carcinomatosis from gastrointestinal cancer. Int Semin Surg Oncol. 2005;2(1):3. https://doi.org/10.1186/1477-7800-2-3.

    Article  PubMed  PubMed Central  Google Scholar 

  75. Mehta AM, Bignell MB, Alves S, Dayal SP, Mohamed F, Cecil TD, et al. Risk of ovarian involvement in advanced colorectal or appendiceal tumors involving the peritoneum. Dis Colon Rectum. 2017;60:691–6.

    PubMed  Google Scholar 

  76. Evers DJ, Verwaal VJ. Indication for oophorectomy during cytoreduction for intraperitoneal metastatic spread of colorectal or appendiceal origin. Br J Surg. 2011;98(2):287–92. https://doi.org/10.1002/bjs.7303.

    Article  CAS  PubMed  Google Scholar 

  77. Young RH. From Krukenberg to today: the ever present problems posed by metastatic tumors in the ovary: part I. Historical perspective, general principles, mucinous tumors including the Krukenberg tumor. Adv Anat Pathol. 2006;13(5):205–27.

    PubMed  Google Scholar 

  78. Woodruff JD, Novak ER. The Krukenberg tumor: study of 48 cases from the ovarian tumor registry. Obstet Gynecol. 1960;15:351–60.

    CAS  PubMed  Google Scholar 

  79. Kiyokawa T, Young RH, Scully RE. Krukenberg tumors of the ovary: a clinicopathologic analysis of 120 cases with emphasis on their variable pathologic manifestations. Am J Surg Pathol. 2006;30(3):277–99.

    PubMed  Google Scholar 

  80. Elias D, Honoré C, Dumont F, Ducreux M, Boige V, Malka D, Burtin P, Dromain C, Goéré D. Results of systematic second-look surgery plus HIPEC in asymptomatic patients presenting a high risk of developing colorectal peritoneal carcinomatosis. Ann Surg. 2011;254(2):289–93. https://doi.org/10.1097/SLA.0b013e31822638f6.

    Article  CAS  PubMed  Google Scholar 

  81. Honoré C, Goéré D, Souadka A, et al. Definition of patients presenting a high risk of developing peritoneal carcinomatosis after curative surgery for colorectal cancer: a systematic review. Ann Surg Oncol. 2013;20:183–92.

    PubMed  Google Scholar 

  82. Kubeček O, Laco J, Špaček J, Petera J, Kopecký J, Kubečková A, Filip S. The pathogenesis, diagnosis, and management of metastatic tumors to the ovary: a comprehensive review. Clin Exp Metastasis. 2017;34(5):295–307.

    PubMed  PubMed Central  Google Scholar 

  83. Shah B, Tang WH, Karn S. Transcoelomic spread and ovarian seeding during ovulation: a possible pathogenesis of Krukenberg tumor. J Cancer Res Ther. 2017;13(1):152–3.

    PubMed  Google Scholar 

  84. Wu F, Zhao X, Mi B, Feng LU, Yuan NA, Lei F, Li M, Zhao X. Clinical characteristics and prognostic analysis of Krukenberg tumor. Mol Clin Oncol. 2015;3(6):1323–8.

    PubMed  PubMed Central  Google Scholar 

  85. Agnes A, Biondi A, Ricci R, Gallotta V, D’Ugo D, Persiani R. Krukenberg tumors: seed, route and soil. Surg Oncol. 2017;26(4):438–45.

    PubMed  Google Scholar 

  86. Yada-Hashimoto N, Yamamoto T, Kamiura S, Seino H, Ohira H, Sawai K, et al. Metastatic ovarian tumors: a review of 64 cases. Gynecol Oncol. 2003;89:314–7.

    PubMed  Google Scholar 

  87. Yamanishi Y, Koshiyama M, Ohnaka M, Ueda M, Ukita S, Hishikawa K, Nagura M, Kim T, Hirose M, Ozasa H, Shirase T. Pathways of metastases from primary organs to the ovaries. Obstet Gynecol Int. 2011;2011:612817. https://doi.org/10.1155/2011/612817.

    Article  PubMed  PubMed Central  Google Scholar 

  88. Mori Y, Nyuya A, Yasui K, Toshima T, Kawai T, Taniguchi F, Kimura K, Inada R, Nishizaki M, Haraga J, Nakamura K, Umeda Y, Kishimoto H, et al. Clinical outcomes of women with ovarian metastases of colorectal cancer treated with oophorectomy with respect to their somatic mutation profiles. Oncotarget. 2018;9:16477–88.

    PubMed  PubMed Central  Google Scholar 

  89. Bignell MB, Mehta AM, Alves S, Chandrakumaran K, Dayal SP, Mohamed F, Cecil TD, Moran BJ. Impact of ovarian metastases on survival in patients treated with cytoreductive surgery and hyperthermic intraperitoneal chemotherapy for peritoneal malignancy originating from appendiceal and colorectal cancer. Colorectal Dis. 2018;20(8):704–10. https://doi.org/10.1111/codi.14057.

    Article  CAS  PubMed  Google Scholar 

  90. Delhorme JB, Triki E, Romain B, Meyer N, Rohr S, Brigand C. Routine second-look after surgical treatment of colonic peritoneal carcinomatosis. J Visc Surg. 2015;152(3):149–54. https://doi.org/10.1016/j.jviscsurg.2015.01.002. Epub 31 Jan 2015.

    Article  CAS  PubMed  Google Scholar 

  91. Shen P, et al. Peritoneal surface disease from colorectal cancer: comparison with the hepatic metastases surgical paradigm in optimally resected patients. Ann Surg Oncol. 2008;15(12):3422–32.

    PubMed  Google Scholar 

  92. Solass W, Sempoux C, Carr NJ, Detlefsen S, Bibeau F. Peritoneal sampling and histological assessment of therapeutic response in peritoneal metastasis: proposal of the Peritoneal Regression Grading Score (PRGS). Pleura Peritoneum. 2016;1:99–107.

    PubMed  PubMed Central  Google Scholar 

  93. Bibeau F, Gil H, Castan F, et al. Comment on “Histopathologic evaluation of liver metastases from colorectal cancer in patients treated with FOLFOXIRI plus bevacizumab”. Br J Cancer. 2013;109:3127–9.

    CAS  PubMed  PubMed Central  Google Scholar 

  94. Chang HHL, Leeper WR, Chan G, Quan D, Driman DK. Infarct-like necrosis: a distinct form of necrosis seen in colorectal carcinoma liver metastases treated with perioperative chemotherapy. Am J Surg Pathol. 2012;36(4):570–6.

    PubMed  Google Scholar 

  95. Becker K, Mueller JD, Schulmacher C, Ott K, Fink U, Busch R, et al. Histomorphology and grading of regression in gastric carcinoma treated with neoadjuvant chemotherapy. Cancer. 2003;98:1521–30.

    PubMed  Google Scholar 

  96. Chirieac LR, Swisher SG, Correa AM, et al. Signet-ring cell or mucinous histology after preoperative chemoradiation and survival in patients with esophageal or esophagogastric junction adenocarcinoma. Clin Cancer Res. 2005;11:2229–36.

    CAS  PubMed  Google Scholar 

  97. Shia J, McManus M, Guillem JG, et al. Significance of acellular mucin pools in rectal carcinoma after neoadjuvant chemoradiotherapy. Am J Surg Pathol. 2011;35:127–34.

    PubMed  Google Scholar 

  98. Lim S-B, Hong S-M, Yu CS, et al. Prevalence and clinical significance of acellular mucin in locally advanced rectal cancer patients showing pathologic complete response to preoperative chemoradiotherapy. Am J Surg Pathol. 2013;37:47–52.

    PubMed  Google Scholar 

  99. Rubbia-Brandt L, et al. Importance of histological tumor response assessment in predicting the outcome in patients with colorectal liver metastases treated with neo-adjuvant chemotherapy followed by liver surgery. Ann Oncol. 2007;18(2):299–304.

    CAS  PubMed  Google Scholar 

  100. Blazer DG 3rd, et al. Pathologic response to preoperative chemotherapy: a new outcome end point after resection of hepatic colorectal metastases. J Clin Oncol. 2008;26(33):5344–51.

    PubMed  Google Scholar 

  101. Sugarbaker PH. Preoperative assessment of cancer patients with peritoneal metastases for complete cytoreduction. Indian J Surg Oncol. 2016;7(3):295–302.

    PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Olivier Glehen .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2020 Springer Nature Singapore Pte Ltd.

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Bhatt, A., Glehen, O. (2020). Colorectal Peritoneal Metastases: Correlating Histopathological Findings and Disease Biology. In: Glehen, O., Bhatt, A. (eds) Pathology of Peritoneal Metastases. Springer, Singapore. https://doi.org/10.1007/978-981-15-3773-8_4

Download citation

  • DOI: https://doi.org/10.1007/978-981-15-3773-8_4

  • Published:

  • Publisher Name: Springer, Singapore

  • Print ISBN: 978-981-15-3772-1

  • Online ISBN: 978-981-15-3773-8

  • eBook Packages: MedicineMedicine (R0)

Publish with us

Policies and ethics