Cancer immunity and therapy using hyperthermia with immunotherapy, radiotherapy, chemotherapy, and surgery

Yohsuke Yagawa , Keishi Tanigawa , Yasunobu Kobayashi , Masakazu Yamamoto

Journal of Cancer Metastasis and Treatment ›› 2017, Vol. 3 : 218 -30.

PDF
Journal of Cancer Metastasis and Treatment ›› 2017, Vol. 3:218 -30. DOI: 10.20517/2394-4722.2017.35
Review
review-article

Cancer immunity and therapy using hyperthermia with immunotherapy, radiotherapy, chemotherapy, and surgery

Author information +
History +
PDF

Abstract

Hyperthermia is a type of medical modality for cancer treatment using the biological effect of artificially induced heat. Even though the intrinsic effects of elevated body temperature in cancer tissues are poorly understood, increasing the temperature of the body has been recognized as a popular therapeutic method for tumorous lesions as well as infectious diseases since ancient times. Recently accumulated evidence has shown that hyperthermia amplifies immune responses in the body against cancer while decreasing the immune suppression and immune escape of cancer. It also shows that hyperthermia inhibits the repair of damaged cancer cells after chemotherapy or radiotherapy. These perceptions indicate that hyperthermia has potential for cancer therapy in conjunction with immunotherapy, chemotherapy, radiotherapy, and surgery. Paradoxically, the anticancer effect of hyperthermia alone has not yet been adequately exploited because deep heating techniques and devices to aggregate heat effects only in cancer tissues are difficult in practical terms. This review article focuses on the current understanding concerning cancer immunity and involvement of hyperthermia and the innate and adoptive immune system. The potential for combination therapy with hyperthermia and chemotherapy, radiotherapy, and surgery is also discussed.

Keywords

Hyperthermia / cancer immunity / chemosensitizer / radiosensitizer / combination cancer therapy / hyperthermic intraoperative peritoneal chemotherapy

Cite this article

Download citation ▾
Yohsuke Yagawa, Keishi Tanigawa, Yasunobu Kobayashi, Masakazu Yamamoto. Cancer immunity and therapy using hyperthermia with immunotherapy, radiotherapy, chemotherapy, and surgery. Journal of Cancer Metastasis and Treatment, 2017, 3: 218-30 DOI:10.20517/2394-4722.2017.35

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Navin N,Troge J,Rodgers L,Cook K,Levy D,Muthuswamy L,McCombie WR,Wigler M.Tumour evolution inferred by single-cell sequencing..Nature2011;472:90-4 PMCID:PMC4504184

[2]

Griffith KD,Carrasquillo JA,Yang JC,Aebersold P,Yu MY.In vivo distribution of adoptively transferred indium-111-labeled tumor infiltrating lymphocytes and peripheral blood lymphocytes in patients with metastatic melanoma..J Natl Cancer Inst1989;81:1709-17

[3]

Rosenberg SA,Cornetta K,Morgan RA,Karson EM,Yang JC,Merino MJ,Dusty Miller A,French Anderson W.Gene transfer into humans--immunotherapy of patients with advanced melanoma, using tumor-infiltrating lymphocytes modified by retroviral gene transduction..N Engl J Med1990;323:570-8

[4]

Wolchok JD,Maio M,Harmankaya K,Cykowski L,Humphrey R.Four-year survival rates for patients with metastatic melanoma who received ipilimumab in phase II clinical trials..Ann Oncol2013;24:2174-80 PMCID:PMC4081656

[5]

Balar AV.PD-1 and PD-L1 antibodies in cancer: current status and future directions..Cancer Immunol Immunother2017;66:551-64

[6]

Mackowiak PA.Concepts of fever..Arch Intern Med1998;158:1870-81

[7]

Dewey WC,Sapareto SA.Cellular responses to combinations of hyperthermia and radiation..Radiology1977;123:463-74

[8]

Dewhirst MW,Lora-Michiels M,Hoopes PJ.Basic principles of thermal dosimetry and thermal thresholds for tissue damage from hyperthermia..Int J Hyperthermia2003;19:267-94

[9]

Hall EJ.Biological effects of heat..Cancer Res1984;44:s4708-13

[10]

Luk KH,Castro JR,Phillips TL.Clinical experiences with local microwave hyperthermia..Int J Radiat Oncol Biol Phys1981;7:615-9

[11]

Manning MR,Miller RC,Connor WG.Clinical hyperthermia: results of a phase I trial employing hyperthermia alone or in combination with external beam or interstitial radiotherapy..Cancer1982;49:205-16

[12]

Gabriele P,Ragona R,Sannazzari GL.Hyperthermia alone in the treatment of recurrences of malignant tumors. Experience with 60 lesions..Cancer1990;66:2191-5

[13]

Masunaga S,Uto Y,Suzuki M,Kinashi Y.The usefulness of continuous administration of hypoxic cytotoxin combined with mild temperature hyperthermia, with reference to effects on quiescent tumour cell populations..Int J Hyperthermia2005;21:305-18

[14]

Song CW.Effect of local hyperthermia on blood flow and microenvironment: a review..Cancer Res1984;44:s4721-30

[15]

Lepock JR,Heynen MP,Waters B,Kruuv J.Increased thermostability of thermotolerant CHL V79 cells as determined by differential scanning calorimetry..J Cell Physiol1990;142:628-34

[16]

Abe M,Takahashi M,Matsuda C,Morita K,Sugahara T.Multi-institutional studies on hyperthermia using an 8-MHz radiofrequency capacitive heating device (Thermotron RF-8) in combination with radiation for cancer therapy..Cancer1986;58:1589-95

[17]

Song CW,Lee CK.Capacitive heating of phantom and human tumors with an 8 MHz radiofrequency applicator (Thermotron RF-8)..Int J Radiat Oncol Biol Phys1986;12:365-72

[18]

Hegyi G,Szasz A.Oncothermia: a new paradigm and promising method in cancer therapies..Acupunct Electrother Res2013;38:161-97

[19]

Sulyok I,Stift A,Lebherz-Eichinger D,Spittler A.Effect of preoperative fever-range whole-body hyperthermia on immunological markers in patients undergoing colorectal cancer surgery..Br J Anaesth2012;109:754-61

[20]

Ostberg JR,Patel R.Regulatory potential of fever-range whole body hyperthermia on Langerhans cells and lymphocytes in an antigen-dependent cellular immune response..J Immunol2001;167:2666-70

[21]

Banchereau J,Caux C,Lebecque S,Pulendran B.Immunobiology of dendritic cells..Annu Rev Immunol2000;18:767-811

[22]

Steinman RM.The dendritic cell system and its role in immunogenicity..Annu Rev Immunol1991;9:271-96

[23]

Förster R,Breitfeld D,Renner-Müller I,Lipp M.CCR7 coordinates the primary immune response by establishing functional microenvironments in secondary lymphoid organs..Cell1999;99:23-33

[24]

Banchereau J.Dendritic cells and the control of immunity..Nature1998;392:245-52

[25]

Gunn MD,Tam C,Rosen SD.A chemokine expressed in lymphoid high endothelial venules promotes the adhesion and chemotaxis of naive T lymphocytes..Proc Natl Acad Sci U S A1998;95:258-63 PMCID:PMC18193

[26]

Ngo VN,Gunn MD,Riminton DS,Browning JL,Cyster JG.Lymphotoxin alpha/beta and tumor necrosis factor are required for stromal cell expression of homing chemokines in B and T cell areas of the spleen..J Exp Med1999;189:403-12 PMCID:PMC2192983

[27]

Luther SA,Hyman PL,Cyster JG.Coexpression of the chemokines ELC and SLC by T zone stromal cells and deletion of the ELC gene in the plt/plt mouse..Proc Natl Acad Sci U S A2000;97:12694-9 PMCID:PMC18826

[28]

Yoshida R,Kitaura M,Imai T.Secondary lymphoid-tissue chemokine is a functional ligand for the CC chemokine receptor CCR7..J Biol Chem1998;273:7118-22

[29]

Sallusto F,Lanzavecchia A.The role of chemokine receptors in primary, effector, and memory immune responses..Annu Rev Immunol2000;18:593-620

[30]

Stein JV,Luo Y,Nakano H,Matsuzawa A,Dorf ME.The CC chemokine thymus-derived chemotactic agent 4 (TCA-4, secondary lymphoid tissue chemokine, 6Ckine, exodus-2) triggers lymphocyte function-associated antigen 1-mediated arrest of rolling T lymphocytes in peripheral lymph node high endothelial venules..J Exp Med2000;191:61-76 PMCID:PMC2195804

[31]

Tangemann K,Giblin P.A high endothelial cell-derived chemokine induces rapid, efficient, and subset-selective arrest of rolling T lymphocytes on a reconstituted endothelial substrate..J Immunol1998;161:6330-7

[32]

Bossi G.CTL secretory lysosomes: biogenesis and secretion of a harmful organelle..Semin Immunol2005;17:87-94

[33]

de Saint Basile G,Fischer A.Molecular mechanisms of biogenesis and exocytosis of cytotoxic granules..Nat Rev Immunol2010;10:568-79

[34]

Anel A,Boyer C,Golstein P.T cell receptor-induced Fas ligand expression in cytotoxic T lymphocyte clones is blocked by protein tyrosine kinase inhibitors and cyclosporin A..Eur J Immunol1994;24:2469-76

[35]

Gooden MJ,Leffers N,Nijman HW.The prognostic influence of tumour-infiltrating lymphocytes in cancer: a systematic review with meta-analysis..Br J Cancer2011;105:93-103 PMCID:PMC3137407

[36]

Topalian SL,Brahmer JR,Smith DC,Powderly JD,Sosman JA,Leming PD,Antonia SJ,Drake CG,Chen L,Anders RA,McMiller TL,Korman AJ,Agrawal S,Kollia GD,Wigginton JM.Safety, activity, and immune correlates of anti-PD-1 antibody in cancer..N Engl J Med2012;366:2443-54 PMCID:PMC3544539

[37]

Brahmer JR,Wollner I,Picus J,Stankevich E,Salay TM,Gilson MM,Selby M,Anders R,Korman AJ,Lowy I.Phase I study of single-agent anti-programmed death-1 (MDX-1106) in refractory solid tumors: safety, clinical activity, pharmacodynamics, and immunologic correlates..J Clin Oncol2010;28:3167-75 PMCID:PMC4834717

[38]

Zhang HG,Cohen P.Hyperthermia on immune regulation: a temperature's story..Cancer Lett2008;271:191-204

[39]

Chen Q,Clancy KA,Wang WC,Rose-John S,Baumann H.Fever-range thermal stress promotes lymphocyte trafficking across high endothelial venules via an interleukin 6 trans-signaling mechanism..Nat Immunol2006;7:1299-308

[40]

Vardam TD,Appenheimer MM,Wang WC,Evans SS.Regulation of a lymphocyte-endothelial-IL-6 trans-signaling axis by fever-range thermal stress: hot spot of immune surveillance..Cytokine2007;39:84-96 PMCID:PMC2756671

[41]

Ostberg JR,Repasky EA.Thermal regulation of dendritic cell activation and migration from skin explants..Int J Hyperthermia2003;19:520-33

[42]

Kobayashi Y,Ostapenko VV,Matsushita N,Shimizu K,Tanigawa K.Fever-range whole-body heat treatment stimulates antigen-specific T-cell responses in humans..Immunol Lett2014;162:256-61

[43]

Mace TA,Kilpatrick C,Lee CT,Minderman H.Differentiation of CD8+ T cells into effector cells is enhanced by physiological range hyperthermia..J Leukoc Biol2011;90:951-62 PMCID:PMC3206471

[44]

Minamiya Y,Takahashi N,Toda H,Konno H,Ogawa J.Expression of the chemokine receptor CCR6 correlates with a favorable prognosis in patients with adenocarcinoma of the lung..Tumour Biol2011;32:197-202

[45]

Grakoui A,Sumen C,Shaw AS,Dustin ML.The immunological synapse: a molecular machine controlling T cell activation..Science1999;285:221-7

[46]

Monks CR,Kupfer H,Kupfer A.Three-dimensional segregation of supramolecular activation clusters in T cells..Nature1998;395:82-6

[47]

Ostberg JR,Repasky EA.Induction of stress proteins in a panel of mouse tissues by fever-range whole body hyperthermia..Int J Hyperthermia2002;18:552-62

[48]

Tsan MF.Heat shock proteins and immune system..J Leukoc Biol2009;85:905-10

[49]

Srivastava PK,Blachere NE.Heat shock proteins transfer peptides during antigen processing and CTL priming..Immunogenetics1994;39:93-8

[50]

Binder RJ.Peptides chaperoned by heat-shock proteins are a necessary and sufficient source of antigen in the cross-priming of CD8+ T cells..Nat Immunol2005;6:593-9

[51]

Breloer M,Moré SH,Fleischer B.Heat shock proteins as "danger signals": eukaryotic Hsp60 enhances and accelerates antigen-specific IFN-gamma production in T cells..Eur J Immunol2001;31:2051-9

[52]

Ramp U,Heikaus S,Grimm MO,Gabbert HE.Expression of heat shock protein 70 in renal cell carcinoma and its relation to tumor progression and prognosis..Histol Histopathol2007;22:1099-107

[53]

Mashaghi A,Minde DP,Kityk R,Mayer MP,Bukau B.Alternative modes of client binding enable functional plasticity of Hsp70..Nature2016;539:448-51

[54]

Wang Y,Tsan MF.Induction of cytokines by heat shock proteins and concanavalin A in murine splenocytes..Cytokine2005;32:149-54

[55]

Terunuma H,Dewan Z,Yamamoto N.Potential role of NK cells in the induction of immune responses: implications for NK cell-based immunotherapy for cancers and viral infections..Int Rev Immunol2008;27:93-110

[56]

Pandha H,John J.Loss of expression of antigen-presenting molecules in human pancreatic cancer and pancreatic cancer cell lines..Clin Exp Immunol2007;148:127-35 PMCID:PMC1868855

[57]

Koopman LA,van der Slik AR,Fleuren GJ.Multiple genetic alterations cause frequent and heterogeneous human histocompatibility leukocyte antigen class I loss in cervical cancer..J Exp Med2000;191:961-76 PMCID:PMC2193119

[58]

Madjd Z,Pinder SE,Durrant LG.Total loss of MHC class I is an independent indicator of good prognosis in breast cancer..Int J Cancer2005;117:248-55

[59]

Kitamura H,Asanuma H,Sato N.Down-regulation of HLA class I antigens in prostate cancer tissues and up-regulation by histone deacetylase inhibition..J Urol2007;178:692-6

[60]

Djajadiningrat RS,Heideman DA,de Jong J.Classic and nonclassic HLA class I expression in penile cancer and relation to HPV status and clinical outcome..J Urol2015;193:1245-51

[61]

Cheng M,Xiao W,Tian Z.NK cell-based immunotherapy for malignant diseases..Cell Mol Immunol2013;10:230-52 PMCID:PMC4076738

[62]

Screpanti V,Grandien A.Impact of FASL-induced apoptosis in the elimination of tumor cells by NK cells..Mol Immunol2005;42:495-9

[63]

Takeda K,Smyth MJ,Yamaguchi N,Iwakura Y,Okumura K.Involvement of tumor necrosis factor-related apoptosis-inducing ligand in surveillance of tumor metastasis by liver natural killer cells..Nat Med2001;7:94-100

[64]

Dayanc BE,Ostberg JR.Dissecting the role of hyperthermia in natural killer cell mediated anti-tumor responses..Int J Hyperthermia2008;24:41-56

[65]

Ostberg JR,Yuan M,Repasky EA.Enhancement of natural killer (NK) cell cytotoxicity by fever-range thermal stress is dependent on NKG2D function and is associated with plasma membrane NKG2D clustering and increased expression of MICA on target cells..J Leukoc Biol2007;82:1322-31

[66]

Terunuma H,Toki A,Nishino N,MIE Nieda M,Teranishi Y.Effects of hyperthermia on the host immune system: from NK cell-based science to clinical application..Thermal Med2012;28:1-9

[67]

Bettelli E,Gao W,Strom TB,Weiner HL.Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells..Nature2006;441:235-8

[68]

Smyth MJ,Swann J,Godfrey DI.CD4+CD25+ T regulatory cells suppress NK cell-mediated immunotherapy of cancer..J Immunol2006;176:1582-7

[69]

Sakaguchi S,Onishi Y,Yamaguchi T.Regulatory T cells: how do they suppress immune responses?.Int Immunol2009;21:1105-11

[70]

Oleinika K,Graham GJ.Suppression, subversion and escape: the role of regulatory T cells in cancer progression..Clin Exp Immunol2013;171:36-45 PMCID:PMC3530093

[71]

Curiel TJ.Tregs and rethinking cancer immunotherapy..J Clin Invest2007;117:1167-74 PMCID:PMC1857250

[72]

Terunuma H,Deng X,Onishi T,Abe H.Mild hyperthermia modulates the relative frequency of lymphocyte cell subpopulations: an increase in a cytolytic NK cell subset and a decrease in a regulatory T cell subset..Thermal Med2007;23:41-7

[73]

Guo J,Sheng X,Qu L,Liu Y,Huo L,Lin B.Intratumoral injection of dendritic cells in combination with local hyperthermia induces systemic antitumor effect in patients with advanced melanoma..Int J Cancer2007;120:2418-25

[74]

Terunuma H.Kokura S,Ohnishi T.Potentiating immune system by hyperthermia.Hyperthermic oncology from bench to bedside2016;SingaporeSpringer Singapore127-35

[75]

Hatzfeld-Charbonnier AS,Castera L,Velu T,Mortier L.Influence of heat stress on human monocyte-derived dendritic cell functions with immunotherapeutic potential for antitumor vaccines..J Leukoc Biol2007;81:1179-87 PMCID:PMC2254491

[76]

Tanigawa K,Kobayashi Y.Effects of fever-range hyperthermia on t cell-mediated immunity: possible combination of hyperthermia and t cell-based cancer immunotherapy.Available from: https://link.springer.com/chapter/10.1007/978-981-10-0719-4_31#citeas. [Last accessed on 19 Oct 2017]

[77]

Mallory M,Jones GC,Simone CB, 2nd..Therapeutic hyperthermia: The old, the new, and the upcoming..Crit Rev Oncol Hematol2016;97:56-64

[78]

Jorritsma JB,Kampinga HH.DNA polymerase activity in heat killing and hyperthermic radiosensitization of mammalian cells as observed after fractionated heat treatments..Radiat Res1986;105:307-19

[79]

Weichselbaum RR,Little JB.Inherently radioresistant cells exist in some human tumors..Proc Natl Acad Sci U S A1985;82:4732-5 PMCID:PMC390978

[80]

Weichselbaum RR,Ahmed-Swan S.Radiobiological characterization of 53 human tumor cell lines..Int J Radiat Biol1989;56:553-60

[81]

Vaupel P.Tumor microenvironmental physiology and its implications for radiation oncology..Semin Radiat Oncol2004;14:198-206

[82]

Masunaga S,Suzuki M,Kinashi Y.Inhibition of repair of radiation-induced damage by mild temperature hyperthermia, referring to the effect on quiescent cell populations..Radiat Med2007;25:417-25

[83]

Jorritsma JB,Scaf AH.Strand break repair, DNA polymerase activity and heat radiosensitization in thermotolerant cells..Int J Hyperthermia1985;1:131-45

[84]

Devun F,Huerre M,Sun JS,Dutreix M.Colorectal cancer metastasis: the DNA repair inhibitor Dbait increases sensitivity to hyperthermia and improves efficacy of radiofrequency ablation..Radiology2014;270:736-46

[85]

Ohguri T,Korogi Y.Clinical results of systemic chemotherapy combined with regional hyperthermia..Thermal Med2007;23:49-61

[86]

Hettinga JV,Kampinga HH.Reduction of cellular cisplatin resistance by hyperthermia--a review..Int J Hyperthermia1997;13:439-57

[87]

Da Silva VF,Raaphorst GP.Hyperthermic potentiation of BCNU toxicity in BCNU-resistant human glioma cells..J Neurooncol1991;11:37-41

[88]

Correale P,La Placa M,Di Genova G,Terrosi C,Giorgi G,Cusi MG.Chemotherapeutic drugs may be used to enhance the killing efficacy of human tumor antigen peptide-specific CTLs..J Immunother2008;31:132-47

[89]

Sugarbaker PH,Vidal-Jove J,DeBruijn EA.Pharmacokinetics of the peritoneal-plasma barrier after systemic mitomycin C administration..Cancer Treat Res1996;82:41-52

[90]

Los G,Pinedo HM.Response of peritoneal solid tumours after intraperitoneal chemohyperthermia treatment with cisplatin or carboplatin..Br J Cancer1994;69:235-41 PMCID:PMC1968708

[91]

Yonemura Y,Li Y,Glehen O,Morris D,Gonzaletz-Moreno S,Piso P,Batlett D,Mizumoto A,Mahtem H.A comprehensive treatment for peritoneal metastases from gastric cancer with curative intent..Eur J Surg Oncol2016;42:1123-31

[92]

Fujishima Y,Kimura Y,Katayama K.MUC2 protein expression status is useful in assessing the effects of hyperthermic intraperitoneal chemotherapy for peritoneal dissemination of colon cancer..Int J Oncol2012;40:960-4 PMCID:PMC3584614

[93]

Cravioto-Villanueva A,Luna-Perez P,Ramirez ML,Montiel H.Cytoreductive surgery with hyperthermic intraperitoneal chemotherapy (HIPEC) delivered via a modified perfusion system for peritoneal carcinomatosis of colorectal origin..Surg Today2016;46:979-84

[94]

Cummins KA,Votanopoulos KI,Stewart JH.Peritoneal dissemination from high-grade appendiceal cancer treated with cytoreductive surgery (CRS) and hyperthermic intraperitoneal chemotherapy (HIPEC)..J Gastrointest Oncol2016;7:3-9 PMCID:PMC4754307

[95]

Sugarbaker PH.Peritoneal metastases from adrenal cortical carcinoma treated by cytoreductive surgery and hyperthermic intraperitoneal chemotherapy..Tumori2016;102:588-92

[96]

Gnanamony M.Chemoresistance in pancreatic cancer: Emerging concepts..Oncol Lett2017;13:2507-13

[97]

Boland CR.Microsatellite instability in colorectal cancer..Gastroenterology2010;138:2073-87 PMCID:PMC3037515

[98]

Ribic CM,Moore MJ,French AJ,Hamilton SR,Gryfe R,Tu D,Gallinger S.Tumor microsatellite-instability status as a predictor of benefit from fluorouracil-based adjuvant chemotherapy for colon cancer..N Engl J Med2003;349:247-57 PMCID:PMC3584639

[99]

Bonadonna G.Dose-response effect of adjuvant chemotherapy in breast cancer..N Engl J Med1981;304:10-5

[100]

Shimizu K,Aruga A,Takasaki K.Clinical utilization of postoperative dendritic cell vaccine plus activated T-cell transfer in patients with intrahepatic cholangiocarcinoma..J Hepatobiliary Pancreat Sci2012;19:171-8

[101]

Sjoquist KM,Smithers BM,Simes RJ,Gebski V.Survival after neoadjuvant chemotherapy or chemoradiotherapy for resectable oesophageal carcinoma: an updated meta-analysis..Lancet Oncol2011;12:681-92

[102]

Du D,Qian H,Tang X,Liu W.The effects of the CCR6/CCL20 biological axis on the invasion and metastasis of hepatocellular carcinoma..Int J Mol Sci2014;15:6441-52 PMCID:PMC4013639

[103]

Klevebro F,Johnson E,Myrnäs T,Jacobsen AB,Tsai JA,Lindblad M,Nilsson M.Morbidity and mortality after surgery for cancer of the oesophagus and gastro-oesophageal junction: a randomized clinical trial of neoadjuvant chemotherapy vs. neoadjuvant chemoradiation..Eur J Surg Oncol2015;41:920-6

[104]

Stahl M,Stuschke M,Meyer HJ,Langer P,Bitzer M,Budach W.Phase III comparison of preoperative chemotherapy compared with chemoradiotherapy in patients with locally advanced adenocarcinoma of the esophagogastric junction..J Clin Oncol2009;27:851-6

[105]

Kitamura K,Watanabe M,Yasuda M,Saku M.Prospective randomized study of hyperthermia combined with chemoradiotherapy for esophageal carcinoma..J Surg Oncol1995;60:55-8

[106]

Issels RD,Verweij J,Reichardt P,Abdel-Rahman S,Salat C,Vujaskovic Z,Jauch KW,Ploner F,Mansmann U,Blay JY,European Society for Hyperthermic Oncology (ESHO)..Neo-adjuvant chemotherapy alone or with regional hyperthermia for localised high-risk soft-tissue sarcoma: a randomised phase 3 multicentre study..Lancet Oncol2010;11:561-70

[107]

Kimura F,Yoshidome H,Miyazaki M.Immunosuppression following surgical and traumatic injury..Surg Today2010;40:793-808

[108]

Sacerdote P,Gaspani L,Maucione A,Ammatuna M.The effects of tramadol and morphine on immune responses and pain after surgery in cancer patients..Anesth Analg2000;90:1411-4

[109]

Tsuchiya Y,Yoshioka I,Matsuo M,Tsukada K.Increased surgical stress promotes tumor metastasis..Surgery2003;133:547-55

[110]

van der Zee J.Heating the patient: a promising approach?.Ann Oncol2002;13:1173-84

[111]

Feldmann HJ,Molls M.Hyperthermia--its actual role in radiation oncology. Part III: Clinical rationale and results in deep seated tumors..Strahlenther Onkol1995;171:251-64

[112]

Haveman J,Wondergem J,Hulshof MC.Effects of hyperthermia on the peripheral nervous system: a review..Int J Hyperthermia2004;20:371-91

AI Summary AI Mindmap
PDF

35

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/