Impacts of previous heatstroke history on physiological parameters eHSP72 and biomarkers of oxidative stress in military working dogs

Bruchim, Yaron; Aroch, Itamar; Nivy, Ran; Baruch, Shelly; Abbas, Atallah; Frank, Ilan; Fishelson, Yuval; Codner, Carolina; Horowitz, Michal

doi:10.1007/s12192-019-01020-z

Original Paper
Published: 11 August 2019

Impacts of previous heatstroke history on physiological parameters eHSP72 and biomarkers of oxidative stress in military working dogs

Yaron Bruchim^1,2,
Itamar Aroch¹,
Ran Nivy¹,
Shelly Baruch¹,
Atallah Abbas²,
Ilan Frank³,
Yuval Fishelson³,
Carolina Codner¹ &
Michal Horowitz²

Cell Stress and Chaperones volume 24, pages 937–946 (2019)Cite this article

324 Accesses
2 Citations
Metrics details

Abstract

Heatstroke (HS) is an acute, progressive life-threatening emergency. Animals, including military working dogs (IDFMWD), rapidly activate cytoprotective processes, e.g., heat shock proteins (HSPs) and antioxidative molecules, in response to heat stress. We hypothesized that serum HSPs (eHSP72) and oxidative stress markers would differ in IDFMWD with a history of HS compared with controls and thus could be used to detect susceptibility to recurrent HS. eHSPs concentration, oxidative stress markers, and systemic physiological parameters were studied in dogs with and without histories of HS, undergoing indoor or outdoor training. Treadmill physical performance tests (PPTs) were conducted indoors at 22 °C (groups C-I and HS-I) or outdoors under heat stress conditions of 36 °C; 60% humidity (groups C-O and HS-O). Pre-, immediately post-, and 45 min post-PPT heart rate (HR), respiratory rate, and rectal temperature (T_re) were recorded in all dogs. Likewise, blood samples were collected and eHSP72, venous blood gas analysis, and lactate and creatine kinase activity (CK) were assayed. Serum uric acid (sUA) and total serum redox potential (TRP) were measured only in the indoor group. Immediately post-PPT under both environmental conditions, T_re, HR, eHSP, sUA, and TRP (only measured in indoor PPT) significantly (P < 0.05) increased, whereas venous blood pH and bicarbonate decreased significantly (P < 0.05). Between groups comparisons demonstrated significant differences in basal HR and post-PPT T_re immediately after outdoor PPT. eHSP72 induction, CK, sUA, and serum TRP remained significantly higher in the HS group during post-PPT recovery. Taken together, animals with a history of HS have different results, and this signature of previous HS may predict altered heat sensitivity.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

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

References

Andress M, & Goodnight, M. E. (2013). Heatstroke in a military working dog. US Army Med Dep J, 34-37
Argaud, L., Ferry, T., Le, Q. H., Marfisi, A., Ciorba, D., Achache, P., . . . Robert, D. (2007). Short- and long-term outcomes of heatstroke following the 2003 heat wave in Lyon, France. Arch Intern Med, 167(20), 2177–2183. https://doi.org/10.1001/archinte.167.20.ioi70147
Aroch I, Segev G, Loeb E, Bruchim Y (2009) Peripheral nucleated red blood cells as a prognostic indicator in heatstroke in dogs. J Vet Intern Med 23(3):544–551
Article CAS PubMed Google Scholar
Bruchim Y, Aroch I, Eliav A, Abbas A, Frank I, Kelmer E, Codner C, Segev G, Epstein Y, Horowitz M (2014) Two years of combined high-intensity physical training and heat acclimatization affect lymphocyte and serum HSP70 in purebred military working dogs. J Appl Physiol (1985) 117(2):112–118. https://doi.org/10.1152/japplphysiol.00090.2014
Article CAS Google Scholar
Bruchim Y, Kelmer E, Cohen A, Codner C, Segev G, Aroch I (2017) Hemostatic abnormalities in dogs with naturally occurring heatstroke. J Vet Emerg Crit Care (San Antonio) 27:315–324. https://doi.org/10.1111/vec.12590
Article Google Scholar
Bruchim Y, Klement E, Saragusty J, Finkeilstein E, Kass P, Aroch I (2006) Heat stroke in dogs: a retrospective study of 54 cases (1999-2004) and analysis of risk factors for death. J Vet Intern Med 20(1):38–46
PubMed Google Scholar
Bruchim Y, Segev G, Kelmer E, Codner C, Marisat A, Horowitz M (2016) Hospitalized dogs recovery from naturally occurring heatstroke; does serum heat shock protein 72 can provide prognostic biomarker? Cell Stress Chaperones 21(1):123–130. https://doi.org/10.1007/s12192-015-0645-5
Article CAS PubMed Google Scholar
Carter R 3rd, Cheuvront SN, Williams JO, Kolka MA, Stephenson LA, Sawka MN, Amoroso PJ (2005) Epidemiology of hospitalizations and deaths from heat illness in soldiers. Med Sci Sports Exerc 37(8):1338–1344
Article PubMed Google Scholar
Chevion S, Roberts MA, Chevion M (2000) The use of cyclic voltammetry for the evaluation of antioxidant capacity. Free Radic Biol Med 28(6):860–870
Article CAS PubMed Google Scholar
Dehbi M, Baturcam E, Eldali A, Ahmed M, Kwaasi A, Chishti MA, Bouchama A (2010) Hsp-72, a candidate prognostic indicator of heatstroke. Cell Stress Chaperones 15(5):593–603. https://doi.org/10.1007/s12192-010-0172-3
Article CAS PubMed PubMed Central Google Scholar
Drobatz KJ, Macintire DK (1996) Heat-induced illness in dogs: 42 cases (1976-1993). J Am Vet Med Assoc 209(11):1894–1899
CAS PubMed Google Scholar
Epstein Y, Moran DS, Shapiro Y, Sohar E, Shemer J (1999) Exertional heat stroke: a case series. Med Sci Sports Exerc 31(2):224–228
Article CAS PubMed Google Scholar
Epstein Y, Roberts WO (2011) The pathopysiology of heat stroke: an integrative view of the final common pathway. Scand J Med Sci Sports 21(6):742–748
Article CAS PubMed Google Scholar
Epstein Y, Yanovich R, Heled Y (2016) Heat tolerance test or race simulation test for return to activity after heat stroke. Med Sci Sports Exerc 48(7):1428. https://doi.org/10.1249/MSS.0000000000000904
Article PubMed Google Scholar
Flanagan SW, Moseley PL, Buettner GR (1998) Increased flux of free radicals in cells subjected to hyperthermia: detection by electron paramagnetic resonance spin trapping. FEBS Lett 431(2):285–286
Article CAS PubMed Google Scholar
Hemmelgarn C, Gannon K (2013a) Heatstroke: clinical signs, diagnosis, treatment, and prognosis. Compend Contin Educ Vet 35(7):E3
PubMed Google Scholar
Hemmelgarn C, Gannon K (2013b) Heatstroke: thermoregulation, pathophysiology, and predisposing factors. Compend Contin Educ Vet 35(7):E4
PubMed Google Scholar
Hinchcliff KW, Reinhart GA, DiSilvestro R, Reynolds A, Blostein-Fujii A, Swenson RA (2000) Oxidant stress in sled dogs subjected to repetitive endurance exercise. Am J Vet Res 61(5):512–517
Article CAS PubMed Google Scholar
Horowitz M (2002) From molecular and cellular to integrative heat defense during exposure to chronic heat. Comp Biochem Physiol A Mol Integr Physiol 131(3):475–483
Article PubMed Google Scholar
Kampa IS, Frascella DW (1977) Blood uric acid levels during hyperthermic stress. Life Sci 20(8):1373–1376
Article CAS PubMed Google Scholar
Kazman JB, Heled Y, Lisman PJ, Druyan A, Deuster PA, O’Connor FG (2013) Exertional heat illness: the role of heat tolerance testing. Curr Sports Med Rep 12(2):101–105. https://doi.org/10.1249/JSR.0b013e3182874d27
Article PubMed Google Scholar
Kazman JB, Purvis DL, Heled Y, Lisman P, Atias D, Van Arsdale S, & Deuster PA (2015). Women and exertional heat illness: identification of gender specific risk factors. US Army Med Dep J, 58-66
King MA, Clanton TL, Laitano O (2016) Hyperthermia, dehydration, and osmotic stress: unconventional sources of exercise-induced reactive oxygen species. Am J Phys Regul Integr Comp Phys 310(2):R105–R114. https://doi.org/10.1152/ajpregu.00395.2015
Article Google Scholar
Kohen R, Vellaichamy E, Hrbac J, Gati I, Tirosh O (2000) Quantification of the overall reactive oxygen species scavenging capacity of biological fluids and tissues. Free Radic Biol Med 28(6):871–879
Article CAS PubMed Google Scholar
Lenchner I, Segev G, Ari TB, Kohen R, Sirota R, Bruchim Y (2017) Serial evaluation of serum total reduction power potential by cyclic voltammetry in 30 dogs with gastric dilatation and volvulus- a randomised, controlled (lidocaine vs placebo), clinical trial. Res Vet Sci 117:92–96. https://doi.org/10.1016/j.rvsc.2017.11.019
Article CAS PubMed Google Scholar
Leon-Lopez J, Calderon-Soto C, Perez-Sanchez M, Feriche B, Iglesias X, Chaverri D, Rodreguez FA (2018) Oxidative stress in elite athletes training at moderate altitude and at sea level. Eur J Sport Sci 18:1–10. https://doi.org/10.1080/17461391.2018.1453550
Article Google Scholar
Ligumsky M, Klar A, Siguencia J, Arnon R, Gati I, Kohen R (2005) Changes in reducing power profile of gastric juice in patients with active duodenal ulcer. Biomed Pharmacother 59(7):345–350. https://doi.org/10.1016/j.biopha.2005.07.001
Article CAS PubMed Google Scholar
Lisman P, Kazman JB, O’Connor FG, Heled Y, Deuster PA (2014) Heat tolerance testing: association between heat intolerance and anthropometric and fitness measurements. Mil Med 179(11):1339–1346. https://doi.org/10.7205/MILMED-D-14-00169
Article PubMed Google Scholar
Moran DS, Eli-Berchoer L, Heled Y, Mendel L, Schocina M, Horowitz M (2006) Heat intolerance: does gene transcription contribute? J Appl Physiol (1985) 100(4):1370–1376. https://doi.org/10.1152/japplphysiol.01261.2005
Article CAS Google Scholar
Moran DS, Erlich T, Epstein Y (2007) The heat tolerance test: an efficient screening tool for evaluating susceptibility to heat. J Sport Rehabil 16(3):215–221
Article PubMed Google Scholar
Patton MG, Gillum TL, Szymanski MC, Gould LM, Lauterbach CJ, Vaughan RA, Kuennen MR (2018) Heat acclimation increases mitochondrial respiration capacity of C2C12 myotubes and protects against LPS-mediated energy deficit. Cell Stress Chaperones 23:871–883. https://doi.org/10.1007/s12192-018-0894-1
Article CAS PubMed PubMed Central Google Scholar
Ruell PA, Simar D, Periard JD, Best S, Caillaud C, Thompson MW (2014) Plasma and lymphocyte Hsp72 responses to exercise in athletes with prior exertional heat illness. Amino Acids 46(6):1491–1499. https://doi.org/10.1007/s00726-014-1721-3
Article CAS PubMed Google Scholar
Sautin YY, Johnson RJ (2008) Uric acid: the oxidant-antioxidant paradox. Nucleosides Nucleotides Nucleic Acids 27(6):608–619. https://doi.org/10.1080/15257770802138558
Article CAS PubMed PubMed Central Google Scholar
Schermann H, Heled Y, Fleischmann C, Ketko I, Schiffmann N, Epstein Y, Yanovich R (2017) The validity of the heat tolerance test in prediction of recurrent exertional heat illness events. J Sci Med Sport 21:549–552. https://doi.org/10.1016/j.jsams.2017.10.001
Article PubMed Google Scholar
Segev G, Aroch I, Savoray M, Kass PH, Bruchim Y (2015) A novel severity scoring system for dogs with heatstroke. J Vet Emerg Crit Care (San Antonio) 25(2):240–247. https://doi.org/10.1111/vec.12284
Article Google Scholar
Shapiro Y, Rosenthal T, Sohar E (1973) Experimental heatstroke. A model in dogs. Arch Intern Med 131(5):688–692
Article CAS PubMed Google Scholar
Stacey MMJ, Delves SK, Woods DR, Britland SE, Macconnachie L, Allsopp AJ, Brett SJ, Fallowfield JL, Boos CJ (2017) Heart rate variability and plasma nephrines in the evaluation of heat acclimatisation status. Eur J Appl Physiol 118:165–174. https://doi.org/10.1007/s00421-017-3758-y
Article CAS PubMed PubMed Central Google Scholar
Stojsih SE, Baker JL, Les CM, Bir CA (2014) Review of canine deaths while in service in US civilian law enforcement (2002-2012). J Spec Oper Med 14(4):86–91
PubMed Google Scholar
Tsukimori K, Yoshitomi T, Morokuma S, Fukushima K, Wake N (2008) Serum uric acid levels correlate with plasma hydrogen peroxide and protein carbonyl levels in preeclampsia. Am J Hypertens 21(12):1343–1346. https://doi.org/10.1038/ajh.2008.289
Article CAS PubMed Google Scholar
Walsh RC, Koukoulas I, Garnham A, Moseley PL, Hargreaves M, Febbraio MA (2001) Exercise increases serum Hsp72 in humans. Cell Stress Chaperones 6(4):386–393
Article CAS PubMed PubMed Central Google Scholar
Wang JL, Ke DS, Lin MT (2005) Heat shock pretreatment may protect against heatstroke-induced circulatory shock and cerebral ischemia by reducing oxidative stress and energy depletion. Shock 23(2):161–167
Article CAS PubMed Google Scholar
Wijerathne BT, Pilapitiya SD, Vijitharan V, Farah MM, Wimalasooriya YV, Siribaddana SH (2016) Exertional heat stroke in a young military trainee: is it preventable? Mil Med Res 3:8. https://doi.org/10.1186/s40779-016-0078-1
Article PubMed PubMed Central Google Scholar
Wyttenbach A, Sauvageot O, Carmichael J, Diaz-Latoud C, Arrigo AP, Rubinsztein DC (2002) Heat shock protein 27 prevents cellular polyglutamine toxicity and suppresses the increase of reactive oxygen species caused by huntingtin. Hum Mol Genet 11(9):1137–1151
Article CAS PubMed Google Scholar
Xiao C, Wu T, Ren A, Pan Q, Chen S, Wu F, Li X, Wang R, Hightower LE, Tanguay RM (2003) Basal and inducible levels of Hsp70 in patients with acute heat illness induced during training. Cell Stress Chaperones Retrieved fromhttp://www.ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=PubMed&dopt=Citation&list_uids=12820658, 8:86–92
Article CAS PubMed PubMed Central Google Scholar
Yadav D, Lee ES, Kim HM, Choi E, Lee EY, Lim JS, Ahn SV, Koh SB, Chung CH (2015) Prospective study of serum uric acid levels and incident metabolic syndrome in a Korean rural cohort. Atherosclerosis 241(1):271–277. https://doi.org/10.1016/j.atherosclerosis.2015.04.797
Article CAS PubMed Google Scholar

Download references

Author information

Authors and Affiliations

The Hebrew University Veterinary Teaching Hospital, Koret School of Veterinary Medicine, The Hebrew University of Jerusalem, Jerusalem, Israel
Yaron Bruchim, Itamar Aroch, Ran Nivy, Shelly Baruch & Carolina Codner
Laboratory of Environmental Physiology, Faculty of Dentistry, The Hebrew University of Jerusalem, Jerusalem, Israel
Yaron Bruchim, Atallah Abbas & Michal Horowitz
Israel Defense Force Military Working Dog Unit, Jerusalem, Israel
Ilan Frank & Yuval Fishelson

Authors

Yaron Bruchim
View author publications
You can also search for this author in PubMed Google Scholar
Itamar Aroch
View author publications
You can also search for this author in PubMed Google Scholar
Ran Nivy
View author publications
You can also search for this author in PubMed Google Scholar
Shelly Baruch
View author publications
You can also search for this author in PubMed Google Scholar
Atallah Abbas
View author publications
You can also search for this author in PubMed Google Scholar
Ilan Frank
View author publications
You can also search for this author in PubMed Google Scholar
Yuval Fishelson
View author publications
You can also search for this author in PubMed Google Scholar
Carolina Codner
View author publications
You can also search for this author in PubMed Google Scholar
Michal Horowitz
View author publications
You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Yaron Bruchim or Michal Horowitz.

Ethics declarations

The study included 22 healthy IDFMWD purebred Belgium Malinois military working dogs and was approved by the Commission of Animal Experiments Israel Ministry of Defense (12011)

Additional information

Publisher’s note

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

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Bruchim, Y., Aroch, I., Nivy, R. et al. Impacts of previous heatstroke history on physiological parameters eHSP72 and biomarkers of oxidative stress in military working dogs. Cell Stress and Chaperones 24, 937–946 (2019). https://doi.org/10.1007/s12192-019-01020-z

Download citation

Received: 16 April 2019
Revised: 02 July 2019
Accepted: 05 July 2019
Published: 11 August 2019
Issue Date: September 2019
DOI: https://doi.org/10.1007/s12192-019-01020-z

Keywords

Heatstroke
Serum HSP72
Low molecular weight antioxidants
Serum biochemical profile
Dogs