Pathophysiological alterations induced by sustained 35-GHz radio-frequency energy heating
-
James R. Jauchem
,
Kathy L. Ryan
Abstract
Background: Exposure to radio-frequency energy (RFE) of millimeter wavelengths results in a relatively high skin-heating rate, with only a moderate rate of core heating. Yet, prolonged RFE exposure eventuates in severe hypotension and death. In this study, we characterized pathophysiological changes associated with prolonged RFE sufficient to induce hypotension.
Methods: Anesthetized rats were exposed to 35-GHz RFE with a power density of 75 mW/cm2. Cardiovascular and temperature parameters were continuously recorded. Blood factors and histopathology were compared between sham (n=6) and exposed (n=12) animals.
Results and conclusions: Using infrared thermography, we confirmed a relatively high temperature (>46 °C) at the skin surface of the irradiated site. Histopathological results included hemorrhage and congestion of blood vessels in the dermis and subcutis of irradiated skin without induction of burn. As in environmental heating, significantly greater levels of serum glucose, creatinine, uric acid, and anion gap were observed in rats exposed to longer-duration RFE (approx. 38-min exposures) than in shorter-duration (approx. 19-min exposures) or sham (time control) animals. However, changes in blood electrolytes or liver enzymes (often seen during heatstroke) were not observed after the RFE exposures. Even without major tissue injury or serum/plasma enzyme and electrolyte changes, rapid cutaneous heating via RFE induced profound hypotension that eventuated in death.
Acknowledgments
We thank Maria R. Tehrany, Heather M. Lehnert, and Julie D. Lovelace (Trinity University, San Antonio, TX), and SSgt. Raul Escarciga (US Air Force) for technical support. Ronald W. Trotter, DVM (US Army), performed the histopathology analyses.
Author contributions: All the authors have accepted responsibility for the entire content of this submitted manuscript and approved submission.
Research funding: None declared.
Employment or leadership: None declared.
Honorarium: None declared.
Competing interests: The funding organization(s) played no role in the study design; in the collection, analysis, and interpretation of data; in the writing of the report; or in the decision to submit the report for publication.
References
1. Jauchem JR. The role of autacoids and the autonomic nervous system in cardiovascular responses to radio-frequency energy heating [review]. Auton Autacoid Pharmacol 2006;26: 121−40.10.1111/j.1474-8673.2006.00362.xSearch in Google Scholar PubMed
2. Kregel KC, Gisolfi CV. Circulatory responses to vasoconstrictor agents during passive heating in the rat. J Appl Physiol 1990;68:1220–7.10.1152/jappl.1990.68.3.1220Search in Google Scholar PubMed
3. Moran DS, Horowitz M, Meiri U, Laor A, Pandolf KB. The physiological strain index applied to heat-stressed rats. J Appl Physiol 1999;86:895–901.10.1152/jappl.1999.86.3.895Search in Google Scholar PubMed
4. Gandhi OP, Riazzi A. Absorption of millimeter waves by human beings and its biological implications. IEEE Trans Microwave Theory Tech 1986;34:228–35.10.1109/TMTT.1986.1133316Search in Google Scholar
5. Alekseev SI, Ziskin MS, Fesenko EE. Frequency dependence of heating of human skin exposed to millimeter waves [Article in Russian]. Biofizika 2012;57:110–14.10.1134/S0006350912010046Search in Google Scholar
6. Frei MR, Ryan KL, Berger RE, Jauchem JR. Sustained 35-GHz radiofrequency irradiation induces circulatory failure. Shock 1995;4:289–93.10.1097/00024382-199510000-00010Search in Google Scholar PubMed
7. Ryan KL, Frei MR, Berger RE, Jauchem JR. Does nitric oxide mediate circulatory failure induced by 35-GHz microwave heating? Shock 1996;6:71–6.10.1097/00024382-199607000-00015Search in Google Scholar PubMed
8. Tafolla TJ, Trachtenberg DJ, Aho JA. From niche to necessity: integrating nonlethal weapons into essential enabling capabilities. Joint Forces Quarterly 2012;71–9.Search in Google Scholar
9. Jauchem JR, Frei MR. Cardiorespiratory changes during microwave-induced lethal heat stress and β-adrenergic blockade. J Appl Physiol 1994;77:434–40.10.1152/jappl.1994.77.1.434Search in Google Scholar PubMed
10. Refinetti R, Carlisle HJ. Thermoregulation during pentobarbital and ketamine anesthesia in rats. J Physiol 1989;83:300–3.Search in Google Scholar
11. Nelson DA, Walters TJ, Ryan KL, Emerton KB, Hurt WD, Ziriax JM, et al. Inter-species extrapolation of skin heating resulting from millimeter wave irradiation: modeling and experimental results. Health Phys 2003;84:608–15.10.1097/00004032-200305000-00006Search in Google Scholar PubMed
12. Liu ZF, Li BL, Tong HS, Tang YQ, Xu QL, Guo JQ, et al. Pathological changes in the lung and brain of mice during heat stress and cooling treatment. World J Emerg Med 2011;2:50–3.10.5847/wjem.j.1920-8642.2011.01.009Search in Google Scholar PubMed PubMed Central
13. Ryan KL, Frei MR, Jauchem JR. Circulatory failure induced by 35 GHz microwave heating: effects of chronic nitric oxide synthesis inhibition. Shock 1997;7:70–6.10.1097/00024382-199701000-00010Search in Google Scholar PubMed
14. Ryan KL, Lovelace JD, Frei MR, Jauchem JR. Administration of a nitric oxide donor does not affect hypotension induced by 35-GHz microwave heating. Methods Find Exp Clin Pharmacol 1997;19:455–64.10.1097/00024382-199701000-00010Search in Google Scholar
15. Ryan KL, Walters TJ, Tehrany MR, Lovelace JD, Jauchem JR. Age does not affect thermal and cardiorespiratory responses to microwave heating in calorically restricted rats. Shock 1997;8:55–60.10.1097/00024382-199707000-00009Search in Google Scholar PubMed
16. Lin MT, Liu HH, Yang YL. Involvement of interleukin-1 receptor mechanisms in development of arterial hypotension in rat heatstroke. Am J Physiol 1997;273:H2072–7.10.1152/ajpheart.1997.273.4.H2072Search in Google Scholar PubMed
17. Millenbaugh NJ, Kiel JL, Ryan KL, Blystone RV, Kalns JE, Brott BJ, et al. Comparison of blood pressure and thermal responses in rats exposed to millimeter wave energy or environmental heat. Shock 2006;25:625–32.10.1097/01.shk.0000209550.11087.fdSearch in Google Scholar PubMed
18. Jauchem JR, Frei MR. Cardiovascular changes in unanesthetized and ketamine-anesthetized Sprague-Dawley rats exposed to 2.8-GHz radiofrequency radiation. Lab Anim Sci 1991;41:70–5.Search in Google Scholar
19. Epstein Y, Hadad E, Shapiro Y. Pathological factors underlying hyperthermia [review]. J Therm Biol 2004;29:487–94.10.1016/j.jtherbio.2004.08.018Search in Google Scholar
20. Chao TC, Sinniah R, Pakiam JE. Acute heat stroke deaths. Pathology 1981;13:145–56.10.3109/00313028109086837Search in Google Scholar PubMed
21. Kielblock AJ, Strydom NB, Burger FJ, Pretorius PJ, Manjoo M. Cardiovascular origins of heatstroke pathophysiology: an anesthetized rat model. Aviat Space Environ Med 1982;53:171–8.Search in Google Scholar
22. Takamata A, Nose H, Mack GW, Morimoto T. Control of total peripheral resistance during hyperthermia in rats. J Appl Physiol 1990;69:1087–92.10.1152/jappl.1990.69.3.1087Search in Google Scholar PubMed
23. Heled Y, Fleischmann C, Epstein Y. Cytokines and their role in hyperthermia and heat stroke [review]. J Basic Clin Physiol Pharmacol 2013;24:85–96.10.1515/jbcpp-2012-0040Search in Google Scholar
24. Jauchem JR, Ryan KL, Lovelace JD, Frei MR. Effects of esmolol on 35-GHz microwave-induced lethal heat stress. J Auton Pharmacol 1997;17:165–73.10.1046/j.1365-2680.1997.00453.xSearch in Google Scholar PubMed
25. Tucker LE, Stanford J, Graves B, Swetnam J, Hamburger S, Anwar A. Classical heatstroke: clinical and laboratory assessment. South Med J 1985;78:20–5.10.1097/00007611-198501000-00006Search in Google Scholar PubMed
26. Vertrees RA, Deyo DJ, Tao W, Brunston RL Jr, Zwischenberger JB. Parallel dialysis normalizes serum chemistries during venovenous perfusion induced hyperthermia. ASAIO J 1997;43:M806–11.10.1097/00002480-199709000-00096Search in Google Scholar
27. Hall WW, Wakefield EG. A study of experimental heat-stroke. J Am Med Assoc 1927;89:177–82.10.1001/jama.1927.02690030009005Search in Google Scholar
28. Zhou RO, Liu JW, Zhang D, Zhang Q. Heatstroke model for desert dry-heat environment and observed organ damage. Am J Emerg Med 2014;31:573−9.10.1016/j.ajem.2014.02.017Search in Google Scholar
29. Hemmelgarn C, Gannon K. Heatstroke: clinical signs, diagnosis, treatment, and prognosis. Compend Contin Educ Vet 2012;35:E3.Search in Google Scholar
30. Mehta SR, Jaswal DS. Heat stroke. Med J Armed Forces India 2003;59:140–3.10.1016/S0377-1237(03)80062-XSearch in Google Scholar
31. Niu KC, Lin MT, Chang CP. Hyperbaric oxygen improves survival in heatstroke rats by reducing multiorgan dysfunction and brain oxidative stress. Eur J Pharmacol 2007;569:94–102.10.1016/j.ejphar.2007.04.037Search in Google Scholar
32. Kampa IS, Frascella DW. Blood uric acid levels during hyperthermic stress. Life Sci 1977;20:1373–6.10.1016/0024-3205(77)90363-0Search in Google Scholar
33. Bouchama A, De Vol EB. Acid-base alterations in heatstroke. Intensive Care Med 2001;27:680–5.10.1007/s001340100906Search in Google Scholar PubMed
34. Hubbard RW, Criss RE, Elliott LP, Kelly C, Matthew WT, Bowers WD, et al. Diagnostic significance of selected serum enzymes in a rat heatstroke model. J Appl Physiol Respir Environ Exerc Physiol 1979;46:334–9.10.1152/jappl.1979.46.2.334Search in Google Scholar PubMed
35. Epstein Y, Moran DS, Shapiro Y. Exertional heatstroke in the Israeli Defence Forces. In: Pandolf KB, Burr RE, editors. Medical aspect of harsh environments. Washington, DC: Office of the Surgeon General, Department of the Army, United States of America, 2001:281−88.Search in Google Scholar
36. Harrison MH. Effects on thermal stress and exercise on blood volume in humans. Physiol Rev 1985;65:149–209.10.1152/physrev.1985.65.1.149Search in Google Scholar PubMed
37. Burger FJ, Engelbrecht FM. Changes in blood composition in experimental heatstroke. S Afr Med J 1967;41:718–21.Search in Google Scholar
38. McKenzie P, LeCount ER. Heat stroke. With a second study of cerebral edema. J Am Med Assoc 1918;71:260–3.10.1001/jama.1918.02600300024008Search in Google Scholar
39. Shapiro Y, Rosenthal T, Sohar E. Experimental heatstroke. A model in dogs. Arch Intern Med 1973;131:688–92.10.1001/archinte.1973.00320110072010Search in Google Scholar
40. Sohal RS, Sun SC, Colcolough HL, Burch GE. Heat stroke. An electron microscopic study of endothelial cell damage and disseminated intravascular coagulation. Arch Intern Med 1968;122:43–7.10.1001/archinte.1968.00300060045008Search in Google Scholar
41. Danielsen L, Thomsen HK, Nielsen O, Aalund O, Nielsen KG, Karlsmark T, et al. Electrical and thermal injuries in pig skin – evaluated and compared by light microscopy. Forensic Sci Int 1978;12:211–25.10.1016/0379-0738(78)90006-3Search in Google Scholar
42. Moritz AR. Studies of thermal injury: III. The pathology and pathogenesis of cutaneous burns. An experimental study. Am J Pathol 1947;23:915–41.Search in Google Scholar
43. Zhang D, Spielmann A, Wang L, Ding G, Huang F, Gu Q, et al. Mast-cell degranulation induced by physical stimuli involves the activation of transient-receptor-potential channel TRPV2. Physiol Res 2012;61:113–24.10.33549/physiolres.932053Search in Google Scholar
44. Jauchem JR, Ryan KL, Tehrany MR. Effects of histamine receptor blockade on cardiovascular changes induced by 35 GHz radio frequency radiation heating. Auton Autacoid Pharmacol 2004;24:17–28.10.1111/j.1474-8673.2004.00309.xSearch in Google Scholar
45. Millenbaugh NJ, Roth C, Sypniewska R, Chan V, Eggers JS, Kiel JL, et al. Gene expression changes in the skin of rats induced by prolonged 35 GHz millimeter-wave exposure. Radiat Res 2008;169:288–300.10.1667/RR1121.1Search in Google Scholar
46. Onarheim H, Lund T, Reed R. Thermal skin injury: I. acute hemodynamic effects of fluid resuscitation with lactated Ringer’s, plasma, and hypertonic saline (2,400 mosmol/l) in the rat. Circ Shock 1989;27:13–24.Search in Google Scholar
47. Rav-Acha M, Hadad E, Epstein Y, Heled Y, Moran DS. Fatal exertional heat stroke: a case series. Am J Med Sci 2004;328:84–7.10.1097/00000441-200408000-00003Search in Google Scholar
48. Ryan KL, Tehrany MR, Jauchem JR. Nitric oxide does not contribute to the hypotension of heatstroke. J Appl Physiol 2001;90:961–70.10.1152/jappl.2001.90.3.961Search in Google Scholar
49. Ryan KL, Jauchem JR, Tehrany MR, Boyle HL. Platelet-activating factor does not mediate circulatory failure induced by 35-GHz microwave heating. Methods Find Exp Clin Pharmacol 2002;24:279–86.10.1358/mf.2002.24.5.802305Search in Google Scholar
50. Horowitz M, Robinson SD. Heat shock proteins and the heat shock response during hyperthermia and its modulation by altered physiological conditions. Prog Brain Res 2007;162:433–46.10.1016/S0079-6123(06)62021-9Search in Google Scholar
51. Walters TJ, Ryan KL, Mason PA. Regional distribution of Hsp70 in the CNS of young and old food-restricted rats following hyperthermia. Brain Res Bull 2001;55:367–74.10.1016/S0361-9230(01)00502-0Search in Google Scholar
52. Epstein Y, Roberts WO. The pathophysiology of heat stroke: an integrative view of the final common pathway. Scand J Med Sci Sports 2011;21:742–8.10.1111/j.1600-0838.2011.01333.xSearch in Google Scholar PubMed
53. Singh LP, Kapoor M, Singh SB. Heat: not black, not white. It’s gray!!! [review]. J Basic Clin Physiol Pharmacol 2013;24:209–24.10.1515/jbcpp-2012-0080Search in Google Scholar
54. Walters TJ, Ryan KL, Belcher JC, Doyle JM, Tehrany MR, Mason PA. Regional brain heating during microwave exposure (2.06 GHz), warm-water immersion, environmental heating and exercise. Bioelectromagnetics 1998;19:341−53.10.1002/(SICI)1521-186X(1998)19:6<341::AID-BEM2>3.0.CO;2-1Search in Google Scholar
55. Blalock A. Principles of surgical care: shock and other problems. St. Louis: C.V. Mosby, 1940.10.1097/00007611-194009000-00028Search in Google Scholar
56. Gann DS, Drucker WR. Hemorrhagic shock [review]. J Trauma Acute Care Surg 2013;75:888–95.10.1097/TA.0b013e3182a686edSearch in Google Scholar
©2016 by De Gruyter
Articles in the same Issue
- Frontmatter
- Behavior and Neuroprotection
- Neuroprotective effect of hydroxy safflor yellow A against cerebral ischemia-reperfusion injury in rats: putative role of mPTP
- Anti-hyperalgesic and anti-nociceptive potentials of standardized grape seed proanthocyanidin extract against CCI-induced neuropathic pain in rats
- Protective effects of forced exercise against nicotine-induced anxiety, depression and cognition impairment in rat
- Oxidative Stress
- Effects of long-term administration of aspartame on biochemical indices, lipid profile and redox status of cellular system of male rats
- Protective effect of dietary fenugreek (Trigonella foenum-graecum) seeds and garlic (Allium sativum) on induced oxidation of low-density lipoprotein in rats
- Metabolism
- Anti-diabetic effects of aqueous prickly lettuce (Lactuca scariola Linn.) leaves extract in alloxan-induced male diabetic rats treated with nickel (II)
- Sildenafil, a phosphodiesterase type 5 inhibitor, attenuates diabetic nephropathy in STZ-induced diabetic rats
- Inflammation
- Evaluation of analgesic, anti-inflammatory, thrombolytic and hepatoprotective activities of roots of Premna esculenta (Roxb)
- Evaluation of anti-inflammatory potential of the ethanolic extract of the Saussurea lappa root (costus) on adjuvant-induced monoarthritis in rats
- Miscellaneous
- Pathophysiological alterations induced by sustained 35-GHz radio-frequency energy heating
Articles in the same Issue
- Frontmatter
- Behavior and Neuroprotection
- Neuroprotective effect of hydroxy safflor yellow A against cerebral ischemia-reperfusion injury in rats: putative role of mPTP
- Anti-hyperalgesic and anti-nociceptive potentials of standardized grape seed proanthocyanidin extract against CCI-induced neuropathic pain in rats
- Protective effects of forced exercise against nicotine-induced anxiety, depression and cognition impairment in rat
- Oxidative Stress
- Effects of long-term administration of aspartame on biochemical indices, lipid profile and redox status of cellular system of male rats
- Protective effect of dietary fenugreek (Trigonella foenum-graecum) seeds and garlic (Allium sativum) on induced oxidation of low-density lipoprotein in rats
- Metabolism
- Anti-diabetic effects of aqueous prickly lettuce (Lactuca scariola Linn.) leaves extract in alloxan-induced male diabetic rats treated with nickel (II)
- Sildenafil, a phosphodiesterase type 5 inhibitor, attenuates diabetic nephropathy in STZ-induced diabetic rats
- Inflammation
- Evaluation of analgesic, anti-inflammatory, thrombolytic and hepatoprotective activities of roots of Premna esculenta (Roxb)
- Evaluation of anti-inflammatory potential of the ethanolic extract of the Saussurea lappa root (costus) on adjuvant-induced monoarthritis in rats
- Miscellaneous
- Pathophysiological alterations induced by sustained 35-GHz radio-frequency energy heating
