Metabolic modulation of the biological effects of ionizing radiation and chemotherapy (review)

Cover Page


Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription or Fee Access

Abstract

The review presents general information about the tumor cell microenvironment, its role in the development and progression of the malignant process and the results of antitumor therapy. The analysis showed that the development of methods for influencing the key metabolic targets of tumor cells and their microenvironment is a promising direction in experimental and clinical oncology. Some approaches to inducing metabolic modulation are considered: inhibitors of cellular pumps, hyperglycemia and hyperthermia. The therapeutic effect of the first two induction options is based on modulation of the acid-base balance (pH) of the tumor. The biological effect of hyperthermia is broader and directly depends on the severity and direction of the temperature-exposure mode of heating. Ultimately, such changes lead to an increase in the damaging effect of ionizing radiation and drugs on the tumor. Despite the fact that the composition of the microenvironment is heterogeneous and varies depending on the type of tumor, some specific cells and mediators are present in all its types. Therefore, the developed treatment methods can be universal for most tumor locations.

The literature analysis suggests that there is objective experimental and clinical evidence supporting the use of metabolic modulators in antitumor therapy.

Full Text

Restricted Access

About the authors

Orazakhmet K. Kurpeshev

Siberian Research Institute of Hyperthermia

Author for correspondence.
Email: kurpeshev-ok@yandex.ru
ORCID iD: 0000-0003-3219-1596
SPIN-code: 2467-6046

MD, Dr. Sci. (Medicine)

Russian Federation, Iskitim

Viktor V. Pasov

Tsyb Medical Radiological Research Centre — branch of the National Medical Research Radiological Centre

Email: pasov@mrrc.obninsk.ru
ORCID iD: 0000-0003-0387-1648
SPIN-code: 8778-2401

MD, Dr. Sci. (Medicine)

Russian Federation, Obninsk

Anatoly I. Pilipenko

Research and Production Enterprise "Istok" named after A.I. Shokin

Email: aipilipenko@istokmw.ru
Russian Federation, Fryazino

Gleb A. Ulasov

Research and Production Enterprise "Istok" named after A.I. Shokin

Email: gaulasov@istokmw.ru
Russian Federation, Fryazino

References

  1. Kushlinsky NE, Nemtsova MV. Molecular mechanisms of tumor growth. Medical news. 2014;9:29–37. EDN: TIKZDJ
  2. Chekhun VF, Berezhnaya NM. Physiological system of connective tissue and oncogenesis. III. Formation of resistance to chemotherapeutic drugs. Oncology. 2017;19(3):156–170. (In Russ.)
  3. Hoeckel M, Vaupel P. Tumor hypoxia: definitions and current clinical, biologic, and molecular aspects. J Natl Cancer Inst. 2001;93:266–276. EDN: ISMMLN doi: 10.1093/jnci/93.4.266
  4. Horsman MR, Vaupel P. Pathophysiological Basis for the Formation of the Tumor Microenvironment. Front Oncol. 2016;6:66. doi: 10.3389/fonc.2016.00066.
  5. Jarosz-Biej M, Smolarczyk R, Cichon T, Kułach N. Tumor Microenvironment as A “Game Changer” in Cancer Radiotherapy. Int J Mol Sci. 2019;20:3212. EDN: DSLFZF doi: 10.3390/ijms20133212
  6. Korkaya H, Orsulic S. Editorial: The Tumor Microenvironment: Recent Advances and Novel Therapeutic Approaches. Front Cell Dev Biol. 2020;8:586176. EDN: TYLWRF doi: 10.3389/fcell.2020.586176
  7. Baghban R, Roshangar L, Jahanban-Esfahlan R, et al. Tumor microenvironment complexity and therapeutic implications at a glance. Cell Communication and Signaling. 2020;18:59. EDN: XKVQZD doi: 10.1186/s12964-020-0530-4
  8. Riaz N, Morris L, Havel JJ, et al. The role of neoantigens in response to immune checkpoint blockade. Int Immunol. 2016;28(8):411–419.
  9. Reits EA, Hodge JW, Herberts CA, et al. Radiation modulates the peptide repertoire, enhances MHC class I expression, and induces successful antitumor immunotherapy. J Exp Med. 2006;203:1259–1271. doi: 10.1084/jem.20052494
  10. Lugade AA, Moran JP, Gerber SA, et al. Local radiation therapy of B16 melanoma tumors increases the generation of tumor antigen-specific effector cells that traffic to the tumor. J Immunol. 2005;174:7516–7523. doi: 10.4049/jimmunol.174.12.7516
  11. Arnold KM, Flynn NJ, Raben A, et al. The Impact of Radiation on the Tumor Microenvironment AP: Effect of Dose and Fractionation Schedules. Cancer Growth and Metastasis. 2018;11:1–17. doi: 10.1177/11790644187616
  12. Postow MA, Callahan MK, Barker CA, at al. Immunologic correlates of the abscopal effect in a patient with melanoma. N Engl J Med. 2012;366:925–931. EDN: YCJKXV doi: 10.1056/NEJMoa1112824
  13. Oei AL, Korangath P, Mulka K, et al. Enhancing the abscopal effect of radiation and immune checkpoint inhibitor therapies with magnetic nanoparticle hyperthermia in a model of metastatic breast cancer. Int J Hyperthermia. 2019;36(Supl.1):47–63. EDN: XYTTDP doi: 10.1080/02656736.2019.1685686
  14. Song CW, Lee YJ, Griffin RJ, et al. Indirect tumor cell death after high-dose hypofractionated irradiation: implications for stereotactic body radiation therapy and stereotactic radiation surgery. Int J Radiat Oncol Biol Phys. 2015;93:166–172. doi: 10.1016/j.ijrobp.2015.05.016
  15. Brown JM, Carlson DJ, Brenner DJ. The tumor radiobiology of SRS and SBRT: are more than the 5 R’s involved? Int J Radiat Oncol Biol Phys. 2014;88:254–262. doi: 10.1016/j.ijrobp.2013.07.022
  16. Golden EB, Formenti SC. Is tumor (R)ejection by the immune system the “5th R” of radiobiology? Oncoimmunology. 2014;3(1):e28133. doi: 10.4161/onci.28133
  17. Barcellos-Hoff MH. Remodeling of the irradiated tumor microenvironment: the fifth R of radiobiology. In: Tofilon PJ. and Camphausen K. eds. Increasing the Therapeutic Ratio of Radiotherapy. 2016:135–149.
  18. Steel GG, Mcmillan TJ, Peacock JH. Letter to the Editor. The 5Rs of Radiobiology. Int J Radiat Biol. 1989;56(6):1045–1048. doi: 10.1080/09553008914552491
  19. Osinsky SP. Microenvironment of tumor cells and tumor progression. Health of Ukraine. 2013. Oncology, Lecture. ZU_2012_Onko_5.qxd 12/18/2012. P. 34–36. Available from: https://health-ua.com/pics/pdf/ZU_2012_Onko_5-6/34-36.pdf
  20. Peltanova B, Raudenska M, Masarik M. Effect of tumor microenvironment on pathogenesis of the head and neck squamous cell carcinoma: a systematic review. Mol Cancer. 2019;18:63. doi: 10.1186/s12943-019-0983-5
  21. Romero-Garcia S, Lopez-Gonzalez JS, Báez-Viveros JL, et al. Tumor cell metabolism. An integral view. Cancer Biol Ther. 2011;12(11):939–948. doi: 10.4161/cbt.12.11.18140
  22. Pilborough AE, Lambert DW, Khurram SA. Extranodal extension in oral cancer: A role for the nodal microenvironment? J Oral Pathol Med. 2019;48:863–870. doi: 10.1111/jop.12870
  23. Gandhi P, Kaur M, Punia RS, et al. Myofibroblasts as important diagnostic and prognostic indicators of oral squamous cell carcinoma: An immunohistochemical study using alpha-smooth muscle actin antibody. J Oral Maxillofac Pathol. 2022;26:156–160. doi: 10.4103/jomfp.jomfp_389_20
  24. Johnson DE, Burtness B, Leemans CR, et al. Head and neck squamous cell carcinoma. Nat Rev Dis Primers. 2020;6(1):92. doi: 10.1038/s41572-020-00224-3
  25. Chubenko VA, Moiseenko VM. Metabolic therapy and its prospects in the treatment of patients with malignant tumors. RosOncoWeb. Internet portal of the Russian Society of Clinical Oncology. 04/12/2022. (In Russ.) Available from: https://rosoncoweb.ru/news/oncology/2022/04/12/?ysclid=lilwy601vd14058594
  26. Oleinik EK, Shibaev MI, Ignatiev KS, et al. Tumor microenvironment: formation of an immune profile. Medical Immunology. 2020;22(2):207–220. EDN: QEZBBN doi: 10.15789/1563-0625-TMT-1909
  27. Bitsadze VO, Slukhanchuk EV, Solopova AG, et al. The role of the microenvironment in tumor growth and spread. Obstetrics, Gynecology and Reproduction. 2024;18(1):96–111. doi: 10.17749/2313-7347/ob.gyn.rep.2024.489
  28. Koontongkaew S. The tumor microenvironment contribution to development, growth, invasion and metastasis of head and neck squamous cell carcinomas. J Cancer. 2013;4(1):66–83. doi: 10.7150/jca.5112
  29. Bienkowska KJ, Hanley CJ, Thomas GJ. Cancer-Associated Fibroblasts in Oral Cancer: A Current Perspective on Function and Potential for Therapeutic Targeting. Front Oral Health. 2021;2:686337. doi: 10.3389/froh.2021.686337
  30. Ji X, Zhu X, Lu X. Effect of cancer-associated fibroblasts on radiosensitivity of cancer cells. Future Oncol. 2017;13:1537–1550.
  31. Boxberg M, Leising L, Steiger K, et al. Composition and Clinical Impact of the Immunologic Tumor Microenvironment in Oral Squamous Cell Carcinoma. J Immunol. 2019;202(1):278–291. doi: 10.4049/jimmunol.1800242
  32. Vaupel P, Kallinowski F, Okunieff P. Blood flow, oxygen and nutrient supply, and metabolic micro-environment of human tumors: a review. Cancer Res. 1989;49:6449–6465.
  33. Vladimirova LYu, Abramova NA, Shikhlyarova AI. Metabolic modulation of the antitumor effect of cytostatics in experiment and clinic. Journal of Malignant Tumors. 2014;3:42–47. doi: 10.18027/2224-5057-2014-3-42-47
  34. Song CW, Griffin R, Park HJ. Influence of Tumor pH on Therapeutic Response. In.: Cancer Drug Resistance, 2006. Chapter 2. P. 21–42.
  35. Bogdanov AA, Bogdanov AA, Moiseenko VM. Alkalization of the tumor microenvironment: are there any prospects as a target for therapy? Practical Oncology. 2022;23(3):143–159. doi: 10.31917/2303143
  36. Calcinotto A, Filipazzi P, Grioni M, et al. Modulation of microenvironment acidity reverses anergy in human and murine tumor-infiltrating T lymphocytes. Cancer Res. 2012;72:2746–2756. EDN: TWXAVT
  37. Choi ED, Li VV, Turkmenov AM, Derkembayeva JS, et al. Therapeutic properties of sodium bicarbonate (literature review). Ural Med J. 2020;191(8):55–60. EDN: FKXLKL doi: 10.25694/URMJ.2020.08.10
  38. Mahoney BP, Raghunand N, Baggett B, Gillies RJ. Tumor acidity, ion trapping and chemotherapeutics. I. Acid pH affects the distribution of chemotherapeutic agents in vitro. Biochem Pharmacol. 2003;66(7):1207–1218. doi: 10.1016/s0006-2952(03)00467-2
  39. Vaupel P, Piazena H, Notter M, et al. From Localized Mild Hyperthermia to Improved Tumor Oxygenation: Physiological Mechanisms Critically Involved in Oncologic Thermo-Radio-Immunotherapy. Cancers (Basel). 2023;15(5):1394. doi: 10.3390/cancers15051394
  40. Zhang J, Zhang Y, Mo F, et al. The Roles of HIF-1α in Radiosensitivity and Radiation-Induced Bystander Effects Under Hypoxia. Front Cell Dev Biol. 2021;9:637454. doi: 10.3389/fcell.2021.637454
  41. Ciaccia AG, Koumenis C, Denko N. The influence of tumor hypoxia on malignant progression. Tumor hypoxia: pathophysiology, clinical significance and therapeutic perspectives. Eds P. Vaupel, D. Kelleher. Stuttgart: Wiss enschaftlicheVerlagsgesellchaft. 1999:115–124.
  42. Fukumura D, Xu L, Chen Y, et al. Hypoxia and acidisis independently upregulate vascular endothelial grovth factor trauscription in brain tumors in vivo. Cancer Res. 2001;61:6020–6024.
  43. Pokorn E, Zicha D, Chaloupkov A, et al. Two Dynamic Morphotypes of Sarcoma Cells, Asymmetric Stellate and Triangle with Leading Lamella, are Related to Malignancy. Folia Biol (Praha). 2003;49(1):33–39.
  44. Volk T, Jähde E, Fortmeyer HP, et al. pH in human tumour xenografts: effect of intravenous administration of glucose. Br J Cancer. 1993;68(3):492–500. doi: 10.1038/bjc.1993.375
  45. Eaton AF, Merkulova M, Brown D. The H(+)-ATPase (V-ATPase): from proton pump to signaling complex in health and disease. Am J Physiol Cell Physiol. 2021;320(3):C392-c414. doi: 10.1152/ajpcell.00442.2020
  46. Hu Y, Lou J, Jin Z, et al. Advances in research on the regulatory mechanism of NHE1 in tumors (Review). Oncol Lett. 2021;21(4):273. doi: 10.3892/ol.2021.12534
  47. McDonald PC, Chafe SC, Supuran CT, Dedhar S. Cancer Therapeutic Targeting of Hypoxia Induced Carbonic Anhydrase IX: From Bench to Bedside. Cancers (Basel). 2022;14(14):3297. doi: 10.3390/cancers14143297
  48. Wang BY, Zhang J, Wang JL, et al. Intermittent high dose proton pump inhibitor enhances the antitumor effects of chemotherapy in metastatic breast cancer. J Exp Clin Cancer Res. 2015;34(1):85. doi: 10.1186/s13046-015-0194-x
  49. Zhang JL, Liu M, Yang Q, et al. Effects of omeprazole in improving concurrent chemoradiotherapy efficacy in rectal cancer. World J Gastroenterol. 2017;23(14):2575–2584. doi: 10.3748/wjg.v23.i14.2575
  50. Stratford IJ. Reduction of tumour intracellular pH and enhancement of melphalan cytotoxicity by the ionophore Nigericin. Int J Cancer. 1995;60(2):264–268. doi: 10.1002/ijc.2910600222
  51. Miraglia E, Viarisio D, Riganti C, et al. Na+/H+ exchanger activity is increased in doxorubicin-resistant human colon cancer cells and its modulation modifies the sensitivity of the cells to doxorubicin. Int J Cancer. 2005;115(6):924–929. doi: 10.1002/ijc.20959
  52. Murakami T, Shibuya I, Ise T, et al. Elevated expression of vacuolar proton pump genes and cellular PH in cisplatin resistance. Int J Cancer. 2001;93(6):869–874. doi: 10.1002/ijc.1418
  53. Wojtkowiak JW, Verduzco D, Schramm KJ, Gillies RJ. Drug resistance and cellular adaptation to tumor acidic pH microenvironment. Mol Pharm. 2011;8(6):2032–2038. doi: 10.1021/mp200292c
  54. Faes S, Uldry E. Acidic pH reduces VEGF-mediated endothelial cell responses by Down regulation of VEGFR-2; relevance for antiangiogenic therapies. Oncotarget. 2016;7(52):86026–86038. doi: 10.18632/oncotarget.13323
  55. Faes S, Duval AP. Acidic tumor microenvironment abrogates the efficacy of mTORC1 inhibitors. Mol Cancer. 2016;15:78. doi: 10.1186/s12943-016-0562-y
  56. Hamaguchi R. Effects of Alkalization Therapy on Chemotherapy Outcomes in Advanced Pancreatic Cancer: A Retrospective Case-Control Study. In Vivo. 2020;34:2623–2629. doi: 10.21873/invivo.12080
  57. Chao M, Wu H, Jin K, et al. A nonrandomized cohort and a randomized study of local control of large hepatocarcinoma by targeting intratumoral lactic acidosis. eLife. 2016;5:e15691. doi: 10.7554/eLife.15691
  58. Chernikova NA, Koklina AV. The relationship between diabetes and cancer. Analytical review. Proceedings of the conference of young scientists of the Federal State Budgetary Educational Institution of Further Professional Education “Russian Medical Academy of Continuing Professional Education” of the Ministry of Health of Russia “Topical Issues of Endocrinology”. 2017. Journal for continuing medical education of medical. Endocrinology: news, opinions, training. 2017;2:118–120. (In Russ.)
  59. Ryu TY, Park J, Scherer PE. Hyperglycemia as a Risk Factor for Cancer Progression. Diabetes Metab J. 2014;38:330–336. doi: 10.4093/dmj.2014.38.5.330
  60. Ramteke P, Deb A, Shepal V, Bhat MK. Hyperglycemia Associated Metabolic and Molecular Alterations in Cancer Risk, Progression, Treatment, and Mortality. Cancers. 2019;11:1402. doi: 10.3390/cancers11091402
  61. Berdov BA, Kurpeshev OK, Mardinsky YuS. The influence of hyperthermia and hyperglycemia on the effectiveness of radiation therapy in cancer patients. Russ Oncol J. 1996;1:12–16. (In Russ.)
  62. Kurpeshev ОК, Mardynskiy YuS, Maksimov SA, Medvedev VS. Combined treatment of patients with oral cancer by “conditional and dynamical” regime of fractional radiotherapy and loco-regional hyperthermia. Siberian Medical Review. 2011;1(67):80–83. (In Russ.)
  63. Derr RL, Ye X, Islas MU, et al. Association between hyperglycemia and survival in patients with newly diagnosed glioblastoma. J Clin Oncol. 2009;27:7:1082–1086. EDN: MJWYWF
  64. Li XP, Chen Z, Meng ZQ, et al. Concurent hyperglycemia does not influence the long-term prognosis of unresectable hepatocellular carcinomas. World J Gastroent. 2003;9(8):1848–1852. doi: 10.3748/wjg.v9.i8.1848
  65. Newell K, Franchi A, Pouyssegur J, Tannok I. Studies with glycolysis-deficient cells suggest that production of lastic acid is not the only cause of tumor acidity. Proc Natl Acad Sci. USA. 1993;90:1127–1131. doi: 10.1073/pnas.90.3.1127
  66. Gerards MC, van der Velden DL, Baars JW, et al. Impact of hyperglycemia on the efficacy of chemotherapy-A systematic review of preclinical studie. Crit Rev Oncol Hematol. 2017;113:235–241. doi: 10.1016/j.critrevonc.2017.03.007
  67. Leeper D, Engin K, Wang JH, et al. Effect of I.V. Glucose Versus Combined I.V. Plus Oral Glucose on Human Tumour Extracellular Ph for Potential Sensitization to Thermoradiotherapy. International Journal of Hyperthermia. 1998;14(3):257–269. doi: 10.3109/02656739809018231
  68. Yarmonenko SP. Hypoxic tumor cells are a target for targeted modification of radiosensitivity during radiation therapy. Medical radiology. 1983;26(3):9–12. (In Russ.)
  69. Osinsky S, Bubnovskaja L, Sergienko T. Tumour pH under induced hyperglycemia and efficacy of chemotherapy. Anticancer Res. 1987;7(2):199–201. EDN: XLXBTZ
  70. Tagi-Zade SB. Effect of hyperglycemia on tumor growth in rats. Vopr Oncol. 1971;17(2):75–80.
  71. Letyagin VP, Poddubny IK, Sokolov IG, et al. Induced short-term hyperglycemia in the complex treatment of locally advanced breast cancer. Problems of Oncology. 1984;30(7):63–65. (In Russ.)
  72. Krimker VM, Goldobenko GV, Ozhiganov EL, et al. The use of artificial hyperglycemia in radiation treatment of patients with rectal cancer. Problems of Oncology. 1986;32(10):40–46. (In Russ.)
  73. Zharkov VV, Demidchik YuE, Khodina TV. Survival of lung cancer patients with combined treatment using hyperglycemia. Medical radiology. 1991;4:36–38. (In Russ.)
  74. Izhanov MT. Therapeutic pathomorphosis in hyperglycemia and chemoradiotherapy treatment of locally advanced breast cancer. Proceedings of the conference “Modern aspects of diagnosis and treatment of breast cancer”. Russian scientific and practical conference. September 24–25, 2008, Tomsk. Siberian Journal of Oncology. 2008;7(Appendix N 1):59–60. (In Russ.) Available from: https://onco.tnimc.ru/journal/arkhiv/2008/2008-god-prilojenie-%E2%84%961/
  75. Stubbs M, McSheely PMJ, Griffits JR, Bashford CL. Causes and coseqences of tumor acidity and implications for treatment. Mol Med Today. 2000;6:15–19. doi: 10.1016/s1357-4310(99)01615-9
  76. Atema A, Buurman KJH, Noreboom E, Smets LA. Potentiation of DNA-adduct formation and cytotoxicity of platinum-containing drugs by low pH. Int J Cancer. 1993;54:166–172. doi: 10.1002/ijc.2910540126
  77. Laurencot CM, Kennedy KA. Influence of pH on the cytotoxicity of cisplatin in EMT6 mouse mammary tumor cells. Oncol Res. 1995;7:371–379.
  78. Wike-Hooley JK, Haveman J, Reinhold HS. The relevance of tumor pH to the treatment of malignant disease. Radiother Oncol. 1984;2:343–366. doi: 10.1016/s0167-8140(84)80077-8
  79. Yadgarova NS, Egamov ER, Malikov MA, et al. Chemoradiation therapy modified by artificial hyperglycemia in the treatment of locally advanced cancer of the oral mucosa of stage III-IV. Materials of the IV Congress of Oncologists and Radiologists of the SNG. Baku, 2006. P. 103. (In Russ.)
  80. Bykov VL, Martynyuk LA, Rosenfeld LG, et al. Local hyperthermia and hyperglycemia in LOR-oncology. Medical radiology. 1987;32(1):47–49. (In Russ.)
  81. Kurpeshev OK. Possibilities and prospects for the use of hyperthermia in medicine. J Clinical Medicine. 1996;(1):14–16. (In Russ.)
  82. Kurpeshev OK. Hyperthermia in the treatment of patients with non-oncological diseases. Russian Journal of Physiotherapy, Balneology and Rehabilitation. 2020;19(6):400–412. doi: 10.17816/1681-3456-2020-19-6-9
  83. Kurpeshev OK. New possibilities of therapeutic hyperthermia. Russian Journal of Physiotherapy, Balneology and Rehabilitation. 2021;20(5):429–448. doi: 10.17816/rjpbr79779
  84. Kurpeshev OK, van der Zee J. Analysis of the results of randomized trials on hyperthermia in oncology. Medical radiology and radiation safety. 2018;63(3):52–67. doi: 10.12737/article_5b179d60437d54.24079640
  85. Kurpeshev OK, Van der Zee J. Hyperthermia in conservative and palliative treatment of cancer patients. Part I. Loco-regional hyperthermia. Medical Radiology and Radiation Safety. 2022;67(1):87–98. doi: 10.12737/1024-6177-2022-67-1-87-98
  86. Kurpeshev OK, Van der Zee J. Hyperthermia in conservative and palliative treatment of cancer patients. Part II. Whole body hyperthermia. Medical Radiology and Radiation Safety. 2022;67(2):43–58. doi: 10.33266/1024-6177-2022-67-2-43-58
  87. Kurpeshev OK, van der Zee J. Locoregional hyperthermia of malignant tumors: methods, thermometry, equipment. Medical Radiology and Radiation Safety. 2017;62(5):52–63. doi: 10.12737/article_59f30321207ef4.88932385
  88. Hokland SL, Nielsen T, Busk M, Horsman MR. Imaging tumour physiology and vasculature to predict and assess response to heat. Int J Hyperthermia. 2010;26(3):264–272. doi: 10.3109/02656730903585982
  89. Kurpeshev OK, van der Zee J. Experimental basis for the use of hyperthermia in oncology. Medical radiology and radiation safety. 2018;63(1):57–77. doi: 10.12737/article_5a8556b4be3e24.36808227
  90. Van der Heijden AG, Dewhirst MW. Effects of hyperthermia in neutralizing mechanisms of drug resistance in non-muscleinvasive bladder cancer. Int J Hyperthermia. 2016;32(4):434–445. doi: 10.3109/02656736.2016.1155761
  91. Kurpeshev OK, Tsyb AF, Mardynsky YuS, Berdov BA. Mechanisms of development and ways of overcoming chemoresistance of tumors. Part 4. Experimental principles and practical results of the use of whole body hyperthermia in the treatment of chemoresistant tumors. Russian Journal of Oncology. 2003;3:50–53. (In Russ.)
  92. Habash RWY, Bansa R, Krewski D, Alhafid HT. Thermal Therapy, Part 2: Hyperthermia Techniques. Critical ReviewsTM in Biomedical Engineering, 2006;34(6):491–542.
  93. Kok HP, Cressman ENK, Ceelen W, et al. Heating technology for malignant tumors: a review. Int J Hyperthermia. 2020;37(1):711–741. doi: 10.1080/02656736.2020.1779357
  94. Kosterev VV, Kramer-Ageev EA, Mazokhin VN, et al. Development of a novel method to enhance the therapeutic effect on tumours by simultaneous action of radiation and heating. Int J Hyperthermia. 2015;31(4):443–452. doi: 10.3109/02656736.2015.1026413
  95. Mazokhin VN, Overin AE. “Yakhta” electromagnetic hyperthermia installations in the treatment of patients with malignant neoplasms. Microwave Electronics and Microelectronics. 2017;1:117–121.
  96. Gabriele P, Orecchia R, Madon E, et al. The cost of hyperthermia: nine years experience at the Radiation Therapy Department of the Turin University. Tumori. 1994;80(5):327–331. doi: 10.1177/030089169408000502
  97. De Wit GA, de Charro FT, van der Zee J, van Rhoon GC. Economic evaluation of a new cancer treatment: hyperthermia in the management of advanced pelvic cancer. Int Soc of Techn Asses in Health Care. Meeting. 1994. Abst. № 203.
  98. Van der Zee J, Gonzalez Gonzalez D. The Duth Deep Hyperthermia Trial: results in cervical cancer. Int J Hyperthermia. 2006;18:1–12. doi: 10.1080/02656730110091919
  99. Koole SN, van Lieshout C, van Driel WJ, et al. Cost Effectiveness of Interval Cytoreductive Surgery With Hyperthermic Intraperitoneal Chemotherapy in Stage III Ovarian Cancer on the Basis of a Randomized Phase III Trial. J Clin Oncol. 2019;37(23):2041–2050. doi: 10.1200/JCO.19.00594
  100. Kim JH, Chun SY, Lee DE, et al. Cost-effectiveness of hyperthermic intraperitoneal chemotherapy following interval cytoreductive surgery for stage III-IV ovarian cancer from a randomized controlled phase III trial in Korea (KOV-HIPEC-01). Gynecol Oncol. 2023;170:19–24. doi: 10.1016/j.ygyno.2022.12.02

Supplementary files

Supplementary Files
Action
1. JATS XML
Download
2. Fig. 1. Schematic representation of the relationship between the tumor vascular network and its microenvironment. On the left are shown the growth of tumor cells around a capillary and the gradients of oxygen and nutrients as they move away from the vessel. On the right is a block diagram showing the role of various factors of the tumor microenvironment that influence its development.

Download (400KB)
Indexing metadata

Copyright (c) 2024 Eco-Vector

License URL: https://eco-vector.com/for_authors.php#07
СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: ПИ № ФС 77 - 86496 от 11.12.2023 г. 
СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: ЭЛ № ФС 77 - 80673 от 23.03.2021 г.