Skip to main content

Advertisement

Log in

The Role of Hyperthermia in the Treatment of Peritoneal Surface Malignancies

  • Anesthesiology and Critical Care (JP Cata, Section Editor)
  • Published:
Current Oncology Reports Aims and scope Submit manuscript

Abstract

Purpose of Review

Hyperthermia is used to treat peritoneal surface malignancies (PSM), particularly during hyperthermic intraperitoneal chemotherapy (HIPEC). This manuscript provides a focused update of hyperthermia in the treatment of PSM.

Recent Findings

The heterogeneous response to hyperthermia in PSM can be explained by tumor and treatment conditions. PSM tumors may resist hyperthermia via metabolic and immunologic adaptation. The thermodynamics of HIPEC are complex and require computational fluid dynamics (CFD). The clinical evidence supporting the benefit of hyperthermia is largely observational.

Summary

Continued research will allow clinicians to characterize and predict the individual response of PSM to hyperthermia. The application of hyperthermia in current HIPEC protocols is mostly empirical. Thus, modeling heat transfer with CFD is a necessary task if we are to achieve consistent and reproducible hyperthermia. Although observational evidence suggests a survival benefit of hyperthermia, no clinical trial has tested the individual role of hyperthermia in PSM.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1.

Similar content being viewed by others

References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. Spratt JS, Adcock RA, Muskovin M, Sherrill W, McKeown J. Clinical delivery system for intraperitoneal hyperthermic chemotherapy. Cancer Res. 1980;40(2):256–60.

    CAS  PubMed  Google Scholar 

  2. Bushati M, Rovers KP, Sommariva A, Sugarbaker PH, Morris DL, Yonemura Y, et al. The current practice of cytoreductive surgery and HIPEC for colorectal peritoneal metastases: Results of a worldwide web-based survey of the Peritoneal Surface Oncology Group International (PSOGI). Eur J Surg Oncol. 2018;44(12):1942–8. https://doi.org/10.1016/j.ejso.2018.07.003.

    Article  CAS  PubMed  Google Scholar 

  3. Santullo F, Pacelli F, Abatini C, Attalla El Halabieh M, Fortunato G, Lodoli C, et al. Cytoreduction and hyperthermic intraperitoneal chemotherapy for pseudomyxoma peritonei of appendiceal origin: a single center experience. Front Surg. 2021;8:715119. https://doi.org/10.3389/fsurg.2021.715119.

    Article  PubMed Central  PubMed  Google Scholar 

  4. •• Helderman R, Löke DR, Verhoeff J, Rodermond HM, van Bochove GGW, Boon M, et al. The Temperature-Dependent Effectiveness of Platinum-Based Drugs Mitomycin-C and 5-FU during Hyperthermic Intraperitoneal Chemotherapy (HIPEC) in Colorectal Cancer Cell Lines. Cells. 2020;9(8). https://doi.org/10.3390/cells9081775This research explored the dose-dependent effects of the degree of hyperthermia in cell viability of colorectal cancer cell lines and established a minimum temperature of 41°C.

  5. Sugarbaker PH, Averbach AM, Jacquet P, Stephens AD, Stuart OA. A simplified approach to hyperthermic intraoperative intraperitoneal chemotherapy (HIIC) using a self retaining retractor. Cancer Treat Res. 1996;82:415–21. https://doi.org/10.1007/978-1-4613-1247-5_26.

    Article  CAS  PubMed  Google Scholar 

  6. Benoit L, Cheynel N, Ortega-Deballon P, Giacomo GD, Chauffert B, Rat P. Closed hyperthermic intraperitoneal chemotherapy with open abdomen: a novel technique to reduce exposure of the surgical team to chemotherapy drugs. Ann Surg Oncol. 2008;15(2):542–6. https://doi.org/10.1245/s10434-007-9635-x.

    Article  PubMed  Google Scholar 

  7. •• Quénet F, Elias D, Roca L, Goéré D, Ghouti L, Pocard M, 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. 2021;22(2):256–66. https://doi.org/10.1016/s1470-2045(20)30599-4This landmark randomized controlled trial explored the independent effect of HIPEC after complete cytoreduction and questioned the efficacy of HIPEC in colorectal cancer patients.

    Article  CAS  PubMed  Google Scholar 

  8. •• Klaver CEL, Wisselink DD, Punt CJA, Snaebjornsson P, Crezee J, Aalbers AGJ, et al. Adjuvant hyperthermic intraperitoneal chemotherapy in patients with locally advanced colon cancer (COLOPEC): a multicentre, open-label, randomised trial. Lancet Gastroenterol Hepatol. 2019;4(10):761–70. https://doi.org/10.1016/s2468-1253(19)30239-0This landmark trial was the first to explore the independent effect of HIPEC in PSM of colorectal cancer origin.

    Article  PubMed  Google Scholar 

  9. Dewey WC. Arrhenius relationships from the molecule and cell to the clinic. Int J Hyperth. 2009;25(1):3–20. https://doi.org/10.1080/02656730902747919.

    Article  CAS  Google Scholar 

  10. Dewhirst MW, Viglianti BL, Lora-Michiels M, Hanson M, Hoopes PJ. Basic principles of thermal dosimetry and thermal thresholds for tissue damage from hyperthermia. Int J Hyperth. 2003;19(3):267–94. https://doi.org/10.1080/0265673031000119006.

    Article  CAS  Google Scholar 

  11. Kampinga HH. Cell biological effects of hyperthermia alone or combined with radiation or drugs: a short introduction to newcomers in the field. Int J Hyperth. 2006;22(3):191–6. https://doi.org/10.1080/02656730500532028.

    Article  CAS  Google Scholar 

  12. Imashiro C, Takeshita H, Morikura T, Miyata S, Takemura K, Komotori J. Development of accurate temperature regulation culture system with metallic culture vessel demonstrates different thermal cytotoxicity in cancer and normal cells. Sci Rep. 2021;11(1):21466. https://doi.org/10.1038/s41598-021-00908-0.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  13. Kabakov A, Yakimova A, Matchuk O. Molecular chaperones in cancer stem cells: determinants of stemness and potential targets for antitumor therapy. Cells. 2020;9(4). https://doi.org/10.3390/cells9040892.

  14. Mivechi NF, Shi XY, Hahn GM. Stable overexpression of human HSF-1 in murine cells suggests activation rather than expression of HSF-1 to be the key regulatory step in the heat shock gene expression. J Cell Biochem. 1995;59(2):266–80. https://doi.org/10.1002/jcb.240590215.

    Article  CAS  PubMed  Google Scholar 

  15. Tu Y, Tian Y, Wu Y, Cui S. Clinical significance of heat shock proteins in gastric cancer following hyperthermia stress: indications for hyperthermic intraperitoneal chemoperfusion therapy. Oncol Lett. 2018;15(6):9385–91. https://doi.org/10.3892/ol.2018.8508.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  16. Finka A, Mattoo RU, Goloubinoff P. Meta-analysis of heat- and chemically upregulated chaperone genes in plant and human cells. Cell Stress Chaperones. 2011;16(1):15–31. https://doi.org/10.1007/s12192-010-0216-8.

    Article  CAS  PubMed  Google Scholar 

  17. Mazzaferro V, Coppa J, Carrabba MG, Rivoltini L, Schiavo M, Regalia E, et al. Vaccination with autologous tumor-derived heat-shock protein gp96 after liver resection for metastatic colorectal cancer. Clin Cancer Res. 2003;9(9):3235–45.

    CAS  PubMed  Google Scholar 

  18. Akyol S, Gercel-Taylor C, Reynolds LC, Taylor DD. HSP-10 in ovarian cancer: expression and suppression of T-cell signaling. Gynecol Oncol. 2006;101(3):481–6. https://doi.org/10.1016/j.ygyno.2005.11.014.

    Article  CAS  PubMed  Google Scholar 

  19. Chandawarkar RY, Wagh MS, Srivastava PK. The dual nature of specific immunological activity of tumor-derived gp96 preparations. J Exp Med. 1999;189(9):1437–42. https://doi.org/10.1084/jem.189.9.1437.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  20. Sedlacek AL, Kinner-Bibeau LB, Binder RJ. Phenotypically distinct helper NK cells are required for gp96-mediated anti-tumor immunity. Sci Rep. 2016;6:29889. https://doi.org/10.1038/srep29889.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  21. Carr NJ. New insights in the pathology of peritoneal surface malignancy. J Gastrointest Oncol. 2021;12(Suppl 1):S216–s29. https://doi.org/10.21037/jgo-2020-01.

    Article  PubMed Central  PubMed  Google Scholar 

  22. Atallah D, Marsaud V, Radanyi C, Kornprobst M, Rouzier R, Elias D, et al. Thermal enhancement of oxaliplatin-induced inhibition of cell proliferation and cell cycle progression in human carcinoma cell lines. Int J Hyperth. 2004;20(4):405–19. https://doi.org/10.1080/02656730310001637325.

    Article  CAS  Google Scholar 

  23. Henderson E, Kempf M, Yip C, Davenport L, Jones E, Kong S, et al. The lethal heat dose for 50% primary human fibroblast cell death is 48 °C. Arch Dermatol Res. 2021. https://doi.org/10.1007/s00403-021-02217-y.

  24. de Bree E, Katsougkri D, Polioudaki H, Tsangaridou E, Michelakis D, Zoras O, et al. Hyperthermia During Intraperitoneal Chemotherapy With Paclitaxel or Docetaxel for Ovarian Cancer: Is There Any Benefit? Anticancer Res. 2020;40(12):6769–80. https://doi.org/10.21873/anticanres.14700.

    Article  CAS  PubMed  Google Scholar 

  25. Bespalov VG, Alvovsky IK, Tochilnikov GV, Stukov AN, Vyshinskaya EA, Semenov AL, et al. Comparative efficacy evaluation of catheter intraperitoneal chemotherapy, normothermic and hyperthermic chemoperfusion in a rat model of ascitic ovarian cancer. Int J Hyperth. 2018;34(5):545–50. https://doi.org/10.1080/02656736.2017.1375161.

    Article  CAS  Google Scholar 

  26. Jacquet P, Averbach A, Stuart OA, Chang D, Sugarbaker PH. Hyperthermic intraperitoneal doxorubicin: pharmacokinetics, metabolism, and tissue distribution in a rat model. Cancer Chemother Pharmacol. 1998;41(2):147–54. https://doi.org/10.1007/s002800050721.

    Article  CAS  PubMed  Google Scholar 

  27. •• Xie F, Van Bocxlaer J, Colin P, Carlier C, Van Kerschaver O, Weerts J, et al. PKPD Modeling and Dosing Considerations in Advanced Ovarian Cancer Patients Treated with Cisplatin-Based Intraoperative Intraperitoneal Chemotherapy. AAPS J. 2020;22(5):96. https://doi.org/10.1208/s12248-020-00489-2This study has pioneered the pharmacokinetic and pharmacodynamic modeling in humans of peritoneal chemotherapy and the impact of hyperthermia in the rate of systemic absorption of cisplatin.

    Article  CAS  PubMed  Google Scholar 

  28. Cesna V, Sukovas A, Jasukaitiene A, Silkuniene G, Paskauskas S, Dambrauskas Z, et al. Stimulated upregulation of HO-1 is associated with inadequate response of gastric and ovarian cancer cell lines to hyperthermia and cisplatin treatment. Oncol Lett. 2019;18(2):1961–8. https://doi.org/10.3892/ol.2019.10489.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  29. Sukovas A, Silkuniene G, Trumbeckaite S, Jasukaitiene A, Degutyte-Fomins L, Mildaziene V, et al. Hyperthermia potentiates cisplatin cytotoxicity and negative effects on mitochondrial functions in OVCAR-3 cells. J Bioenerg Biomembr. 2019;51(4):301–10. https://doi.org/10.1007/s10863-019-09805-8.

    Article  CAS  PubMed  Google Scholar 

  30. • Kanamori T, Miyazaki N, Aoki S, Ito K, Hisaka A, Hatakeyama H. Investigation of energy metabolic dynamism in hyperthermia-resistant ovarian and uterine cancer cells under heat stress. Sci Rep. 2021;11(1):14726. https://doi.org/10.1038/s41598-021-94031-9This research studies metabolic adaptation as a mechanism of resistance of malignant cells to temperature cytotoxicity.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  31. Kong XX, Jiang S, Liu T, Liu GF, Dong M. Paclitaxel increases sensitivity of SKOV3 cells to hyperthermia by inhibiting heat shock protein 27. Biomed Pharmacother = Biomedecine & pharmacotherapie. 2020;132:110907. https://doi.org/10.1016/j.biopha.2020.110907.

    Article  CAS  Google Scholar 

  32. Kimura A, Ogata K, Altan B, Yokobori T, Mochiki E, Yanai M, et al. Nuclear heat shock protein 110 expression is associated with poor prognosis and hyperthermo-chemotherapy resistance in gastric cancer patients with peritoneal metastasis. World J Gastroenterol. 2017;23(42):7541–50. https://doi.org/10.3748/wjg.v23.i42.7541.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  33. Hatakeyama H, Wu SY, Lyons YA, Pradeep S, Wang W, Huang Q, et al. Role of CTGF in Sensitivity to Hyperthermia in Ovarian and Uterine Cancers. Cell Rep. 2016;17(6):1621–31. https://doi.org/10.1016/j.celrep.2016.10.020.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  34. Lis R, Touboul C, Mirshahi P, Ali F, Mathew S, Nolan DJ, et al. Tumor associated mesenchymal stem cells protects ovarian cancer cells from hyperthermia through CXCL12. Int J Cancer. 2011;128(3):715–25. https://doi.org/10.1002/ijc.25619.

    Article  CAS  PubMed  Google Scholar 

  35. Liu G, Zhao H, Ding Q, Li H, Liu T, Yang H, et al. CDK6 is stimulated by hyperthermia and protects gastric cancer cells from hyperthermia-induced damage. Mol Med Rep. 2021;23(4). https://doi.org/10.3892/mmr.2021.11879.

  36. Sulyok I, Fleischmann E, Stift A, Roth G, Lebherz-Eichinger D, Kasper D, et al. Effect of preoperative fever-range whole-body hyperthermia on immunological markers in patients undergoing colorectal cancer surgery. Br J Anaesth. 2012;109(5):754–61. https://doi.org/10.1093/bja/aes248.

    Article  CAS  PubMed  Google Scholar 

  37. Kobayashi Y, Ito Y, Ostapenko VV, Sakai M, Matsushita N, Imai K, et al. Fever-range whole-body heat treatment stimulates antigen-specific T-cell responses in humans. Immunol Lett. 2014;162(1 Pt A):256–61. https://doi.org/10.1016/j.imlet.2014.09.014.

    Article  CAS  PubMed  Google Scholar 

  38. Zynda ER, Grimm MJ, Yuan M, Zhong L, Mace TA, Capitano M, et al. A role for the thermal environment in defining co-stimulation requirements for CD4(+) T cell activation. Cell Cycle (Georgetown, Tex). 2015;14(14):2340–54. https://doi.org/10.1080/15384101.2015.1049782.

    Article  CAS  PubMed Central  Google Scholar 

  39. Ahlers O, Hildebrandt B, Dieing A, Deja M, Böhnke T, Wust P, et al. Stress induced changes in lymphocyte subpopulations and associated cytokines during whole body hyperthermia of 41.8-42.2 degrees C. Eur J Appl Physiol. 2005;95(4):298–306. https://doi.org/10.1007/s00421-005-0009-4.

    Article  CAS  PubMed  Google Scholar 

  40. Roth L, Eshmuminov D, Laminger F, Koppitsch C, Schneider M, Graf TR, et al. Systemic inflammatory response after hyperthermic intraperitoneal chemotherapy (HIPEC): The perfusion protocol matters! Eur J Surg Oncol. 2019;45(9):1734–9. https://doi.org/10.1016/j.ejso.2019.03.036.

    Article  PubMed  Google Scholar 

  41. Schooneveldt G, Kok HP, Bakker A, Geijsen ED, Rasch CRN, Rosette J, et al. Clinical validation of a novel thermophysical bladder model designed to improve the accuracy of hyperthermia treatment planning in the pelvic region. Int J Hyperth. 2018;35(1):383–97. https://doi.org/10.1080/02656736.2018.1506164.

    Article  Google Scholar 

  42. Ladhari T, Szafnicki K. Modelling of some aspects of a biomedical process: application to the treatment of digestive cancer (HIPEC). 3 Biotech. 2018;8(4):190. https://doi.org/10.1007/s13205-018-1211-5.

    Article  PubMed Central  PubMed  Google Scholar 

  43. Löke DR, Helderman R, Franken NAP, Oei AL, Tanis PJ, Crezee J, et al. Simulating drug penetration during hyperthermic intraperitoneal chemotherapy. Drug Deliv. 2021;28(1):145–61. https://doi.org/10.1080/10717544.2020.1862364.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  44. Rettenmaier MA, Mendivil AA, Gray CM, Chapman AP, Stone MK, Tinnerman EJ, et al. Intra-abdominal temperature distribution during consolidation hyperthermic intraperitoneal chemotherapy with carboplatin in the treatment of advanced stage ovarian carcinoma. Int J Hyperth. 2015;31(4):396–402. https://doi.org/10.3109/02656736.2015.1007399.

    Article  CAS  Google Scholar 

  45. Furman MJ, Picotte RJ, Wante MJ, Rajeshkumar BR, Whalen GF, Lambert LA. Higher flow rates improve heating during hyperthermic intraperitoneal chemoperfusion. J Surg Oncol. 2014;110(8):970–5. https://doi.org/10.1002/jso.23776.

    Article  PubMed  Google Scholar 

  46. Facy O, Al Samman S, Magnin G, Ghiringhelli F, Ladoire S, Chauffert B, et al. High pressure enhances the effect of hyperthermia in intraperitoneal chemotherapy with oxaliplatin: an experimental study. Ann Surg. 2012;256(6):1084–8. https://doi.org/10.1097/SLA.0b013e3182582b38.

    Article  PubMed  Google Scholar 

  47. Romanovsky AA. The thermoregulation system and how it works. Handb Clin Neurol. 2018;156:3–43. https://doi.org/10.1016/b978-0-444-63912-7.00001-1.

    Article  PubMed  Google Scholar 

  48. •• Löke DR, Helderman R, Rodermond HM, Tanis PJ, Streekstra GJ, Franken NAP, et al. Demonstration of treatment planning software for hyperthermic intraperitoneal chemotherapy in a rat model. Int J Hyperth. 2021;38(1):38–54. https://doi.org/10.1080/02656736.2020.1852324The authors propose the use of computational fluid dynamics in the development of a model to predict the core temperatures and chemotherapy concentrations.

    Article  CAS  Google Scholar 

  49. Paruch M. Mathematical Modeling of Breast Tumor Destruction Using Fast Heating during Radiofrequency Ablation. Materials (Basel, Switzerland). 2019;13(1). https://doi.org/10.3390/ma13010136.

  50. Schooneveldt G, Kok HP, Balidemaj E, Geijsen ED, van Ommen F, Sijbrands J, et al. Improving hyperthermia treatment planning for the pelvis by accurate fluid modeling. Med Phys. 2016;43(10):5442. https://doi.org/10.1118/1.4961741.

    Article  CAS  PubMed  Google Scholar 

  51. Schooneveldt G, Löke DR, Zweije R, Helderman RFCPA, Kok HP, Crezee H. Experimental validation of a thermophysical fluid model for use in a hyperthermia treatment planning system. Int J Heat Mass Transf. 2020;152:119495. https://doi.org/10.1016/j.ijheatmasstransfer.2020.119495.

    Article  CAS  Google Scholar 

  52. Löke DR, Helderman R, Sijbrands J, Rodermond HM, Tanis PJ, Franken NAP, et al. A four-inflow construction to ensure thermal stability and uniformity during hyperthermic intraperitoneal chemotherapy (HIPEC) in rats. Cancers. 2020;12(12). https://doi.org/10.3390/cancers12123516.

  53. Crezee J, Lagendijk JJ. Temperature uniformity during hyperthermia: the impact of large vessels. Phys Med Biol. 1992;37(6):1321–37. https://doi.org/10.1088/0031-9155/37/6/009.

    Article  CAS  PubMed  Google Scholar 

  54. Kok HP, Gellermann J, van den Berg CA, Stauffer PR, Hand JW, Crezee J. Thermal modelling using discrete vasculature for thermal therapy: a review. Int J Hyperth. 2013;29(4):336–45. https://doi.org/10.3109/02656736.2013.801521.

    Article  Google Scholar 

  55. Kok HP, Kotte A, Crezee J. Planning, optimisation and evaluation of hyperthermia treatments. Int J Hyperth. 2017;33(6):593–607. https://doi.org/10.1080/02656736.2017.1295323.

    Article  CAS  Google Scholar 

  56. Habash RWY. Therapeutic hyperthermia. Handb Clin Neurol. 2018;157:853–68. https://doi.org/10.1016/b978-0-444-64074-1.00053-7.

    Article  PubMed  Google Scholar 

  57. Cinar Y, Senyol AM, Duman K. Blood viscosity and blood pressure: role of temperature and hyperglycemia. Am J Hypertens. 2001;14(5 Pt 1):433–8. https://doi.org/10.1016/s0895-7061(00)01260-7.

    Article  CAS  PubMed  Google Scholar 

  58. Stammers AH, Vang SN, Mejak BL, Rauch ED. Quantification of the effect of altering hematocrit and temperature on blood viscosity. J Extra Corpor Technol. 2003;35(2):143–51.

    PubMed  Google Scholar 

  59. Khnouf R, Karasneh D, Abdulhay E, Abdelhay A, Sheng W, Fan ZH. Microfluidics-based device for the measurement of blood viscosity and its modeling based on shear rate, temperature, and heparin concentration. Biomed Microdevices. 2019;21(4):80. https://doi.org/10.1007/s10544-019-0426-5.

    Article  CAS  PubMed  Google Scholar 

  60. Katić K, Li R, Kingma B, Zeiler W. Modelling hand skin temperature in relation to body composition. J Therm Biol. 2017;69:139–48. https://doi.org/10.1016/j.jtherbio.2017.07.003.

    Article  PubMed  Google Scholar 

  61. Bhattacharya A, Mahajan RL. Temperature dependence of thermal conductivity of biological tissues. Physiol Meas. 2003;24(3):769–83. https://doi.org/10.1088/0967-3334/24/3/312.

    Article  CAS  PubMed  Google Scholar 

  62. Coccolini F, Corbella D, Finazzi P, Brambillasca P, Benigni A, Prussiani V, et al. Time course of cytokines, hemodynamic and metabolic parameters during hyperthermic intraperitoneal chemotherapy. Minerva Anestesiol. 2016;82(3):310–9.

    PubMed  Google Scholar 

  63. Reis ACV, Kusamura S, Azmi N, Fumagalli L, Piccioni F, Valenza F, et al. Hemodynamic and respiratory implications of high intra-abdominal pressure during HIPEC. Eur J Surg Oncol. 2020;46(10 Pt A):1896–901. https://doi.org/10.1016/j.ejso.2020.02.006.

    Article  PubMed  Google Scholar 

  64. • Kim MH, Yoo YC, Bai SJ, Lee KY, Kim N, Lee KY. Physiologic and hemodynamic changes in patients undergoing open abdominal cytoreductive surgery with hyperthermic intraperitoneal chemotherapy. J Int Med Res. 2021;49(1):300060520983263. https://doi.org/10.1177/0300060520983263This research explores the hemodynamic implications expected in patients undergoing CRS/HIPEC and establishes principles of the expected response to abdominal hyperthermia.

    Article  CAS  PubMed  Google Scholar 

  65. Ceelen W, De Somer F, Van Nieuwenhove Y, Vande Putte D, Pattyn P. Effect of perfusion temperature on glucose and electrolyte transport during hyperthermic intraperitoneal chemoperfusion (HIPEC) with oxaliplatin. Eur J Surg Oncol. 2013;39(7):754–9. https://doi.org/10.1016/j.ejso.2012.07.120.

    Article  CAS  PubMed  Google Scholar 

  66. Sessler DI, Sessler AM. Experimental determination of heat flow parameters during induction of general anesthesia. Anesthesiology. 1998;89(3):657–65. https://doi.org/10.1097/00000542-199809000-00015.

    Article  CAS  PubMed  Google Scholar 

  67. • Hendrix RJ, Kassira JP, Lambert LA. Elevated Maximum Core Body Temperature During Hyperthermic Intraperitoneal Chemoperfusion (HIPEC) is Associated with Increased Postoperative Complications. Ann Surg Oncol. 2020;27(1):232–9. https://doi.org/10.1245/s10434-019-07495-5The authors established severe core-body hyperthermia as an independent prognostic factor of postoperative complications after CRS/ HIPEC.

    Article  PubMed  Google Scholar 

  68. Goldenshluger M, Zippel D, Ben-Yaacov A, Dux J, Yalon T, Zendel A, et al. Core Body Temperature but Not Intraabdominal Pressure Predicts Postoperative Complications Following Closed-System Hyperthermic Intraperitoneal Chemotherapy (HIPEC) Administration. Ann Surg Oncol. 2018;25(3):660–6. https://doi.org/10.1245/s10434-017-6279-3.

    Article  CAS  PubMed  Google Scholar 

  69. •• Yurttas C, Hoffmann G, Tolios A, Haen SP, Schwab M, Königsrainer I, et al. Systematic Review of Variations in Hyperthermic Intraperitoneal Chemotherapy (HIPEC) for Peritoneal Metastasis from Colorectal Cancer. J Clin Med. 2018;7(12). doi: https://doi.org/10.3390/jcm7120567. This systematic review addresses the wide variation in protocols and practices of HIPEC reported in the literature, with a comprehensive look into its main components.

  70. • Guerra-Londono CE, Owusu-Agyemang P, Corrales G, Rofaeil MM, Feng L, Fournier K, et al. Risk of Intraoperative Hyperthermia and Outcomes in Adults Undergoing Cytoreductive Surgery (CRS) with Hyperthermic Intraperitoneal Chemotherapy (HIPEC). Ann Surg Oncol. 2021. https://doi.org/10.1245/s10434-021-10929-8. Describes the risk factors of bladder hyperthermia and proposes bladder hyperthermia as a potential predictor for improved recurrence-free and overall survival.

  71. Kyang LS, Alzahrani NA, Valle SJ, Rahman MK, Arrowaili A, Liauw W, et al. Long-term survival outcomes of cytoreductive surgery and perioperative intraperitoneal chemotherapy: Single-institutional experience with 1225 cases. J Surg Oncol. 2019;120(4):794–802. https://doi.org/10.1002/jso.25642.

    Article  PubMed  Google Scholar 

  72. Polderdijk MCE, Brouwer M, Haverkamp L, Ziesemer KA, Tenhagen M, Boerma D, et al. Outcomes of combined peritoneal and local treatment for patients with peritoneal and limited liver metastases of colorectal origin: a systematic review and meta-analysis. Ann Surg Oncol. 2021. https://doi.org/10.1245/s10434-021-10925-y.

  73. Franko J, Shi Q, Meyers JP, Maughan TS, Adams RA, Seymour MT, 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. 2016;17(12):1709–19. https://doi.org/10.1016/s1470-2045(16)30500-9.

    Article  PubMed  Google Scholar 

  74. Helm JH, Miura JT, Glenn JA, Marcus RK, Larrieux G, Jayakrishnan TT, et al. Cytoreductive surgery and hyperthermic intraperitoneal chemotherapy for malignant peritoneal mesothelioma: a systematic review and meta-analysis. Ann Surg Oncol. 2015;22(5):1686–93. https://doi.org/10.1245/s10434-014-3978-x.

    Article  PubMed  Google Scholar 

  75. Wang Y, Ren F, Chen P, Liu S, Song Z, Ma X. Effects of CytoReductive surgery plus hyperthermic IntraPEritoneal chemotherapy (HIPEC) versus CytoReductive surgery for ovarian cancer patients: A systematic review and meta-analysis. Eur J Surg Oncol. 2019;45(3):301–9. https://doi.org/10.1016/j.ejso.2018.10.528.

    Article  PubMed  Google Scholar 

  76. •• Verwaal VJ, van Ruth S, de Bree E, van Sloothen GW, van Tinteren H, Boot H, 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. 2003;21(20):3737–43. https://doi.org/10.1200/jco.2003.04.187This landmark study established high-quality evidence in favor of CRS/HIPEC over systemic chemotherapy.

    Article  PubMed  Google Scholar 

  77. • Gangi A, Shah R. The landmark series: appendiceal primary peritoneal surface malignancy. Ann Surg Oncol. 2021. https://doi.org/10.1245/s10434-021-10856-8This comprehensive review summarizes the landmark studies guiding surgical oncology in appendiceal neoplasms.

  78. Goéré D, Glehen O, Quenet F, Guilloit JM, Bereder JM, Lorimier G, 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. 2020;21(9):1147–54. https://doi.org/10.1016/s1470-2045(20)30322-3.

    Article  CAS  PubMed  Google Scholar 

  79. Zivanovic O, Chi DS, Zhou Q, Iasonos A, Konner JA, Makker V, 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. 2021;39(23):2594–604. https://doi.org/10.1200/jco.21.00605.

    Article  CAS  PubMed  Google Scholar 

  80. • van Driel WJ, Koole SN, Sonke GS. Hyperthermic intraperitoneal chemotherapy in ovarian cancer. N Engl J Med. 2018;378(14):1363–4. https://doi.org/10.1056/NEJMc1802033This recent trial explores the independent effect of HIPEC in ovarian cancer.

    Article  PubMed  Google Scholar 

  81. Antonio CCP, Alida GG, Elena GG, Rocío GS, Jerónimo MG, Luis ARJ, et al. Cytoreductive surgery with or without HIPEC after neoadjuvant chemotherapy in ovarian cancer: a phase 3 clinical trial. Ann Surg Oncol. 2021. https://doi.org/10.1245/s10434-021-11087-7.

  82. Koole SN, Kieffer JM, Sikorska K, Schagen van Leeuwen JH, Schreuder HWR, Hermans RH, et al. Health-related quality of life after interval cytoreductive surgery with or without hyperthermic intraperitoneal chemotherapy (HIPEC) in patients with stage III ovarian cancer. Eur J Surg Oncol 2021;47(1):101-107. https://doi.org/10.1016/j.ejso.2019.05.006.

  83. Gremonprez F, Gossye H, Ceelen W. Use of hyperthermia versus normothermia during intraperitoneal chemoperfusion with oxaliplatin for colorectal peritoneal carcinomatosis: A propensity score matched analysis. Eur J Surg Oncol. 2019;45(3):366–70. https://doi.org/10.1016/j.ejso.2018.08.023.

    Article  PubMed  Google Scholar 

  84. Koemans WJ, van der Kaaij RT, Wassenaar ECE, Boerma D, Boot H, Sikorska K, et al. Tumor characteristics and clinical outcome of peritoneal metastasis of gastric origin treated with a hyperthermic intraperitoneal chemotherapy procedure in the PERISCOPE I trial. J Surg Oncol. 2021;123(4):904–10. https://doi.org/10.1002/jso.26366.

    Article  PubMed  Google Scholar 

  85. Badgwell B, Ikoma N, Murphy MB, Wang X, Estrella J, Roy-Chowdhuri S, et al. A Phase II Trial of Cytoreduction, Gastrectomy, and Hyperthermic Intraperitoneal Perfusion with Chemotherapy for Patients with Gastric Cancer and Carcinomatosis or Positive Cytology. Ann Surg Oncol. 2021;28(1):258–64. https://doi.org/10.1245/s10434-020-08739-5.

    Article  PubMed  Google Scholar 

  86. Yurttas C, Horvath P, Fischer I, Meisner C, Nadalin S, Königsrainer I, et al. A Prospective, Phase I/II, Open-Label Pilot Trial to Assess the Safety of Hyperthermic Intraperitoneal Chemotherapy After Oncological Resection of Pancreatic Adenocarcinoma. Ann Surg Oncol. 2021;28(13):9086–95. https://doi.org/10.1245/s10434-021-10187-8.

    Article  PubMed Central  PubMed  Google Scholar 

  87. Liu S, Zhong Z, Yi W, Yu Z, Zhang Z, Xia G, et al. Effect of Hyperthermic Intraperitoneal Perfusion Chemotherapy Combined with Radical Surgery and Capecitabine on Stage III Gallbladder Cancer. Canadian journal of gastroenterology & hepatology. 2021;2021:4006786. https://doi.org/10.1155/2021/4006786.

    Article  Google Scholar 

  88. El Hajj H, Vanseymortier M, Hudry D, Bogart E, Abdeddaim C, Leblanc E, et al. Rationale and study design of the CHIPPI-1808 trial: a phase III randomized clinical trial evaluating hyperthermic intraperitoneal chemotherapy (HIPEC) for stage III ovarian cancer patients treated with primary or interval cytoreductive surgery. ESMO open. 2021;6(2):100098. https://doi.org/10.1016/j.esmoop.2021.100098.

    Article  PubMed Central  PubMed  Google Scholar 

  89. Rovers KP, Bakkers C, Simkens G, Burger JWA, Nienhuijs SW, Creemers GM, et al. Perioperative systemic therapy and cytoreductive surgery with HIPEC versus upfront cytoreductive surgery with HIPEC alone for isolated resectable colorectal peritoneal metastases: protocol of a multicentre, open-label, parallel-group, phase II-III, randomised, superiority study (CAIRO6). BMC Cancer. 2019;19(1):390. https://doi.org/10.1186/s12885-019-5545-0.

    Article  PubMed Central  PubMed  Google Scholar 

  90. Farrell R, Burling M, Lee YC, Pather S, Robledo K, Mercieca-Bebber R, et al. Clinical Trial Protocol for HyNOVA: Hyperthermic and Normothermic intraperitoneal chemotherapy following interval cytoreductive surgery for stage III epithelial OVArian, fallopian tube and primary peritoneal cancer (ANZGOG1901/2020). J Gynecol Oncol. 2021. https://doi.org/10.3802/jgo.2022.33.e1.

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Carlos E. Guerra-Londono.

Ethics declarations

Human and Animal Rights and Informed Consent

This article does not contain any studies with animal subjects performed by any of the authors. This article cites an already published retrospective study by Dr. Guerra-Londono on human subjects, which was performed with the permission of the corresponding institutional review board that waived the requirement of informed consent.

Conflict of Interest

The authors declare no conflicts of interest.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

This article is part of the Topical Collection on Anesthesiology and Critical Care

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Guerra-Londono, C.E., Tarazona, C.G., Sánchez-Monroy, J.A. et al. The Role of Hyperthermia in the Treatment of Peritoneal Surface Malignancies. Curr Oncol Rep 24, 875–887 (2022). https://doi.org/10.1007/s11912-022-01275-3

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11912-022-01275-3

Keywords

Navigation