7,625
Views
492
CrossRef citations to date
0
Altmetric
Research Article

Thresholds for thermal damage to normal tissues: An update

, , , , , & show all
Pages 320-343 | Received 22 Jul 2010, Accepted 19 Oct 2010, Published online: 18 May 2011

References

  • 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 Hyperthermia 2003; 19: 267–294
  • Sapareto SA, Dewey WC. Thermal dose determination in cancer therapy. Int J Radiat Oncol Biol Phys 1984; 10: 787–800
  • Wiart M, Curiel L, Gelet A, Lyonnet D, Chapelon JY, Rouviere O. Influence of perfusion on high-intensity focused ultrasound prostate ablation: A first-pass MRI study. Magn Reson Med 2007; 58: 119–127
  • Kiyatkin EA, Sharma HS. Permeability of the blood–brain barrier depends on brain temperature. Neuroscience 2009; 161: 926–939
  • Sharma HS. Hyperthermia influences excitatory and inhibitory amino acid neurotransmitters in the central nervous system. An experimental study in the rat using behavioural, biochemical, pharmacological, and morphological approaches. J Neural Transm 2006; 113: 497–519
  • Noor R, Wang CX, Shuaib A. Hyperthermia masks the neuroprotective effects of tissue plaminogen activator. Stroke 2005; 36: 665–669
  • Cremer OL, Diephuis JC, van Soest H, Vaessen PH, Bruens MG, Hennis PJ, Kalkman CJ. Cerebral oxygen extraction and autoregulation during extracorporeal whole body hyperthermia in humans. Anesthesiology 2004; 100: 1101–1107
  • Chou YT, Lai ST, Lee CC, Lin MT. Hypothermia attenuates circulatory shock and cerebral ischemia in experimental heatstroke. Shock 2003; 19: 388–393
  • Mustafa S, Elgazzar AH, Essam H, Gopinath S, Mathew M. Hyperthermia alters kidney function and renal scintigraphy. Am J Nephrol 2007; 27: 315–321
  • Khan VR, Brown IR. The effect of hyperthermia on the induction of cell death in brain, testis, and thymus of the adult and developing rat. Cell Stress Chaperones 2002; 7: 73–90
  • Belay HT, Brown IR. Spatial analysis of cell death and Hsp70 induction in brain, thymus, and bone marrow of the hyperthermic rat. Cell Stress Chaperones 2003; 8: 395–404
  • Schuchmann S, Schmitz D, Rivera C, Vanhatalo S, Salmen B, Mackie K, Sipila ST, Voipio J, Kaila K. Experimental febrile seizures are precipitated by a hyperthermia-induced respiratory alkalosis. Nat Med 2006; 12: 817–823
  • Dube CM, Brewster AL, Richichi C, Zha Q, Baram TZ. Fever, febrile seizures and epilepsy. Trends Neurosci 2007; 30: 490–496
  • Bernard C, Cossart R, Hirsch JC, Esclapez M, Ben-Ari Y. What is GABAergic inhibition? How is it modified in epilepsy?. Epilepsia 2000; 41S6: S90–95
  • Liebregts MT, McLachlan RS, Leung LS. Hyperthermia induces age-dependent changes in rat hippocampal excitability. Ann Neurol 2002; 52: 318–326
  • Brown, TH, Zador, AM. Hippocampus. In: Shepherd GM, editor. Synaptic Organization of the Brain. New York: Oxford University Press, 1990, pp 346–388, third edition
  • Cohen NJ, Eichenbaum H. Memory, Amnesia, and the Hippocampal System. MIT Press, Cambridge, MA 1993
  • Morrison SA, Sleivert GG, Neary JP, Cheung SS. Prefrontal cortex oxygenation is preserved and does not contribute to impaired neuromuscular activation during passive hyperthermia. Appl Physiol Nutr Metab 2009; 34: 66–74
  • Racinais S, Gaoua N, Grantham J. Hyperthermia impairs short-term memory and peripheral motor drive transmission. J Physiol 2008; 586: 4751–4762
  • Ekimova IV. Changes in the metabolic activity of neurons in the anterior hypothalamic nuclei in rats during hyperthermia, fever, and hypothermia. Neurosci Behav Physiol 2003; 33: 455–460
  • Swanson LW, Sawchenko PE. Hypothalamic integration: Organization of the paraventricular and supraoptic nuclei. Annu Rev Neurosci 1983; 6: 269–324
  • Scheller D, Kolb J, Tegtmeier F. Lactate and pH change in close correlation in the extracellular space of the rat brain during cortical spreading depression. Neurosci Lett 1992; 135: 83–86
  • Ying W, Han SK, Miller JW, Swanson RA. Acidosis potentiates oxidative neuronal death by multiple mechanisms. J Neurochem 1999; 73: 1549–1556
  • Staub F, Mackert B, Kempski O, Peters J, Baethmann A. Swelling and death of neuronal cells by lactic acid. J Neurol Sci 1993; 119: 79–84
  • Kenney MJ, Fels RJ. Forebrain and brain stem neural circuits contribute to altered sympathetic responses to heating in senescent rats. J Appl Physiol 2003; 95: 1986–1993
  • DiBona GF, Kopp UC. Neural control of renal function. Physiol Rev 1997; 77: 75–197
  • Malpas SC, Ramchandra R, Guild SJ, McBryde F, Barrett CJ. Renal sympathetic nerve activity in the development of hypertension. Curr Hypertens Rep 2006; 8: 242–248
  • Sato MA, Morrison SF, Lopes OU, Colombari E. Differentiated hemodynamic changes controlled by splanchnic nerve. Auton Neurosci 2006; 126–127: 202–210
  • Xu D, Pollock M. Experimental nerve thermal injury. Brain 1994; 117: 375–384
  • Patton HD, Fuchs AF, Hille B, Scher AM, Steiner R. Textbook of Physiology: Exciable Cells and Neurophysiolgy. Philadelphia: Saunders, 1989, 21st edition
  • Monafo WW, Eliasson SG. Sciatic nerve function following hindlimb thermal injury. J Surg Res 1987; 43: 344–350
  • McDannold N, Vykhodtseva N, Jolesz FA, Hynynen K. MRI investigation of the threshold for thermally induced blood–brain barrier disruption and brain tissue damage in the rabbit brain. Magn Reson Med 2004; 51: 913–923
  • Hynynen K, McDannold N, Martin H, Jolesz FA, Vykhodtseva N. The threshold for brain damage in rabbits induced by bursts of ultrasound in the presence of an ultrasound contrast agent (Optison). Ultrasound Med Biol 2003; 29: 473–481
  • Chen L, Wansapura JP, Heit G, Butts K. Study of laser ablation in the in vivo rabbit brain with MR thermometry. J Magn Reson Imaging 2002; 16: 147–152
  • McDannold N, Moss M, Killiany R, Rosene DL, King RL, Jolesz FA, Hynynen K. MRI-guided focused ultrasound surgery in the brain: Tests in a primate model. Magn Reson Med 2003; 49: 1188–1191
  • Cohen ZR, Zaubermann J, Harnof S, Mardor Y, Nass D, Zadicario E, Hananel A, Castel D, Faibel M, Ram Z. Magnetic resonance imaging-guided focused ultrasound for thermal ablation in the brain: A feasibility study in a swine model. Neurosurgery 2007; 60: 593–600, discussion
  • Aktas C, Kanter M. A morphological study on Leydig cells of scrotal hyperthermia applied rats in short-term. J Mol Histol 2009; 40: 31–39
  • Kanter M, Aktas C. Effects of scrotal hyperthermia on Leydig cells in long-term: A histological, immunohistochemical and ultrastructural study in rats. J Mol Histol 2009; 40(2)123–30
  • Paul C, Murray AA, Spears N, Saunders PT. A single, mild, transient scrotal heat stress causes DNA damage, subfertility and impairs formation of blastocysts in mice. Reproduction 2008; 136: 73–84
  • Wang C, Cui YG, Wang XH, Jia Y, Sinha Hikim A, Lue YH, Tong JS, Qian LX, Sha JH, Zhou ZM, Hull L, Leung A, Swerdloff RS. Transient scrotal hyperthermia and levonorgestrel enhance testosterone-induced spermatogenesis suppression in men through increased germ cell apoptosis. J Clin Endocrinol Metab 2007; 92: 3292–3304
  • Luo Q, Li Z, Huang X, Yan J, Zhang S, Cai YZ. Lycium barbarum polysaccharides: Protective effects against heat-induced damage of rat testes and H2O2-induced DNA damage in mouse testicular cells and beneficial effect on sexual behavior and reproductive function of hemicastrated rats. Life Sci 2006; 79: 613–621
  • Banks S, King SA, Irvine DS, Saunders PT. Impact of a mild scrotal heat stress on DNA integrity in murine spermatozoa. Reproduction 2005; 129: 505–514
  • Paul C, Teng S, Saunders PT. A single, mild, transient scrotal heat stress causes hypoxia and oxidative stress in mouse testes, which induces germ cell death. Biol Reprod 2009; 80: 913–919
  • Perez-Crespo M, Pintado B, Gutierrez-Adan A. Scrotal heat stress effects on sperm viability, sperm DNA integrity, and the offspring sex ratio in mice. Mol Reprod Dev 2008; 75: 40–47
  • Lue Y, Wang C, Liu YX, Hikim AP, Zhang XS, Ng CM, Hu ZY, Li YC, Leung A, Swerdloff RS. Transient testicular warming enhances the suppressive effect of testosterone on spermatogenesis in adult cynomolgus monkeys (Macaca fascicularis). J Clin Endocrinol Metab 2006; 91: 539–545
  • Lue YH, Lasley BL, Laughlin LS, Swerdloff RS, Hikim AP, Leung A, Overstreet JW, Wang C. Mild testicular hyperthermia induces profound transitional spermatogenic suppression through increased germ cell apoptosis in adult cynomolgus monkeys (Macaca fascicularis). J Androl 2002; 23: 799–805
  • Seror O, Lepetit-Coiffe M, Le Bail B, de Senneville BD, Trillaud H, Moonen C, Quesson B. Real time monitoring of radiofrequency ablation based on MR thermometry and thermal dose in the pig liver in vivo. Eur Radiol 2008; 18: 408–416
  • Anderson CD, Lin WC, Beckham J, Mahadevan-Jansen A, Buttemere CR, Pierce J, Nicoud IB, Wright Pinson C, Chari RS. Fluorescence spectroscopy accurately detects irreversible cell damage during hepatic radiofrequency ablation. Surgery 2004; 136: 524–531
  • Lepetit-Coiffe M, Quesson B, Seror O, Dumont E, Le Bail B, Moonen CT, Trillaud H. Real-time monitoring of radiofrequency ablation of rabbit liver by respiratory-gated quantitative temperature MRI. J Magn Reson Imaging 2006; 24: 152–159
  • Kopelman D, Inbar Y, Hanannel A, Freundlich D, Castel D, Perel A, Greenfeld A, Salamon T, Sareli M, Valeanu A, Papa M. Magnetic resonance-guided focused ultrasound surgery (MRgFUS): Ablation of liver tissue in a porcine model. Eur J Radiol 2006; 59: 157–162
  • Zderic V, Foley J, Luo W, Vaezy S. Prevention of post-focal thermal damage by formation of bubbles at the focus during high intensity focused ultrasound therapy. Med Phys 2008; 35: 4292–4299
  • Hemmila MR, Foley DS, Casetti AV, Soldes OS, Hirschl RB, Bartlett RH. Perfusion induced hyperthermia for oncologic therapy with cardiac and cerebral protection. ASAIO J 2002; 48: 350–354
  • Haveman J, Smals OA, Rodermond HM. Effects of hyperthermia on the rat bladder: A pre-clinical study on thermometry and functional damage after treatment. Int J Hyperthermia 2003; 19: 45–57
  • Greenhalgh DG, Lawless MB, Chew BB, Crone WA, Fein ME, Palmieri TL. Temperature threshold for burn injury: An oximeter safety study. J Burn Care Rehabil 2004; 25: 411–415
  • Werner MU, Lassen B, Pedersen JL, Kehlet H. Local cooling does not prevent hyperalgesia following burn injury in humans. Pain 2002; 98: 297–303
  • Landsberg R, DeRowe A, Katzir A, Shtabsky A, Fliss DM, Gil Z. Laser-induced hyperthermia for treatment of granulation tissue growth in rats. Otolaryngol Head Neck Surg 2009; 140: 480–486
  • Ichinoseki-Sekine N, Naito H, Saga N, Ogura Y, Shiraishi M, Giombini A, Giovannini V, Katamoto S. Changes in muscle temperature induced by 434 MHz microwave hyperthermia. Br J Sports Med 2007; 41: 425–429
  • Rabkin BA, Zderic V, Crum LA, Vaezy S. Biological and physical mechanisms of HIFU-induced hyperecho in ultrasound images. Ultrasound Med Biol 2006; 32: 1721–1729
  • Sokka SD, King R, Hynynen K. MRI-guided gas bubble enhanced ultrasound heating in in vivo rabbit thigh. Phys Med Biol 2003; 48: 223–241
  • Mougenot C, Quesson B, de Senneville BD, de Oliveira PL, Sprinkhuizen S, Palussiere J, Grenier N, Moonen CT. Three-dimensional spatial and temporal temperature control with MR thermometry-guided focused ultrasound (MRgHIFU). Magn Reson Med 2009; 61: 603–614
  • Nosaka K, Muthalib M, Lavender A, Laursen PB. Attenuation of muscle damage by preconditioning with muscle hyperthermia 1-day prior to eccentric exercise. Eur J Appl Physiol 2007; 99: 183–192
  • Morrison SA, Sleivert GG, Cheung S. Aerobic influence on neuromuscular function and tolerance during passive hyperthermia. Med Sci Sports Exerc 2006; 38: 1754–1761
  • He X, McGee S, Coad JE, Schmidlin F, Iaizzo PA, Swanlund DJ, Kluge S, Rudie E, Bischof JC. Investigation of the thermal and tissue injury behaviour in microwave thermal therapy using a porcine kidney model. Int J Hyperthermia 2004; 20: 567–593
  • Nakada SY, Jerde TJ, Warner TF, Wright AS, Haemmerich D, Mahvi DM, Lee FT, Jr. Bipolar radiofrequency ablation of the kidney: Comparison with monopolar radiofrequency ablation. J Endourol 2003; 17: 927–933
  • Ogan K, Roberts WW, Wilhelm DM, Bonnell L, Leiner D, Lindberg G, Kavoussi LR, Cadeddu JA. Infrared thermography and thermocouple mapping of radiofrequency renal ablation to assess treatment adequacy and ablation margins. Urology 2003; 62: 146–151
  • Lee JM, Han JK, Choi SH, Kim SH, Lee JY, Shin KS, Han CJ, Choi BI. Comparison of renal ablation with monopolar radiofrequency and hypertonic-saline-augmented bipolar radiofrequency: In vitro and in vivo experimental studies. Am J Roentgenol 2005; 184: 897–905
  • Diederich CJ, Nau WH, Kinsey A, Ross T, Wootton J, Juang T, Butts-Pauly K, Rieke V, Chen J, Bouley DM, Sommer G. Catheter-based ultrasound devices and MR thermal monitoring for conformal prostate thermal therapy. Conf Proc IEEE Eng Med Biol Soc, Vancouver, BC 20–25 Aug., 2008; 2008: 3664–3668
  • Nau WH, Diederich CJ, Ross AB, Butts K, Rieke V, Bouley DM, Gill H, Daniel B, Sommer G. MRI-guided interstitial ultrasound thermal therapy of the prostate: A feasibility study in the canine model. Med Phys 2005; 32: 733–743
  • Ross AB, Diederich CJ, Nau WH, Rieke V, Butts RK, Sommer G, Gill H, Bouley DM. Curvilinear transurethral ultrasound applicator for selective prostate thermal therapy. Med Phys 2005; 32: 1555–1565
  • Pauly KB, Diederich CJ, Rieke V, Bouley D, Chen J, Nau WH, Ross AB, Kinsey AM, Sommer G. Magnetic resonance-guided high-intensity ultrasound ablation of the prostate. Top Magn Reson Imaging 2006; 17: 195–207
  • Chopra R, Tang K, Burtnyk M, Boyes A, Sugar L, Appu S, Klotz L, Bronskill M. Analysis of the spatial and temporal accuracy of heating in the prostate gland using transurethral ultrasound therapy and active MR temperature feedback. Phys Med Biol 2009; 54: 2615–2633
  • Kinsey AM, Diederich CJ, Rieke V, Nau WH, Pauly KB, Bouley D, Sommer G. Transurethral ultrasound applicators with dynamic multi-sector control for prostate thermal therapy: In vivo evaluation under MR guidance. Med Phys 2008; 35: 2081–2093
  • Mencucci R, Ambrosini S, Ponchietti C, Marini M, Vannelli GB, Menchini U. Ultrasound thermal damage to rabbit corneas after simulated phacoemulsification. J Cataract Refract Surg 2005; 31: 2180–2186
  • Takahashi Y, Igaki M, Suzuki A, Takahashi G, Dogru M, Tsubota K. The effect of periocular warming on accommodation. Ophthalmology 2005; 112: 1113–1118
  • Kandulla J, Elsner H, Birngruber R, Brinkmann R. Noninvasive optoacoustic online retinal temperature determination during continuous-wave laser irradiation. J Biomed Optics 2006; 11: 041111
  • Blackie CA, Solomon JD, Greiner JV, Holmes M, Korb DR. Inner eyelid surface temperature as a function of warm compress methodology. Optom Vis Sci 2008; 85: 675–683
  • Melodelima D, Salomir R, Chapelon JY, Theillere Y, Moonen C, Cathignol D. Intraluminal high intensity ultrasound treatment in the esophagus under fast MR temperature mapping: In vivo studies. Magn Reson Med 2005; 54: 975–982
  • Lambert GP, Gisolfi CV, Berg DJ, Moseley PL, Oberley LW, Kregel KC. Selected contribution: Hyperthermia-induced intestinal permeability and the role of oxidative and nitrosative stress. J Appl Physiol 2002; 92: 1750–1761, discussion 49
  • Sugiura M, Kuwabara Y, Mitani M, Sato A, Shinoda N, Kimura M, Yano M, Mitsui A, Suzuki T, Fujii Y. Effect of whole body hyperthermia on ischemia and reperfusion injury of rat intestine: Real-time ATP change studied using P-31-MRS. Eur Surg Res 2002; 34: 306–312
  • Eriksson AR, Albrektsson T. Temperature threshold levels for heat-induced bone tissue injury: A vital-microscopic study in the rabbit. J Prosthetic Dentistry 1983; 50: 101–107
  • Alvarado R, Mahon B, Valadez C, Caufield M, Wadhwani S, Hambleton C, Siziopikou KP, Dickler AT, Gatta J, Dowlatshahi K. Thermal ablation of the goat mammary gland as a model for post-lumpectomy treatment of breast cancer: Preliminary observations. Int J Hyperthermia. 2009; 25: 47–55
  • Yoshida N, Kristiansen A, Liberman MC. Heat stress and protection from permanent acoustic injury in mice. J Neurosci 1999; 19: 10116–10124
  • Murakoshi M, Yoshida N, Kitsunai Y, Iida K, Kumano S, Suzuki T, Kobayashi T, Wada H. Effects of heat stress on Young's modulus of outer hair cells in mice. Brain research 2006; 1107: 121–130

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.