Exhaled breath condensate hydrogen peroxide concentration, a novel biomarker for assessment of oxidative stress in sheep during heat stress
Surinder S. Chauhan A B D , Pietro Celi C , Brian Leury A , Fan Liu A and Frank R. Dunshea A
+ Author Affiliations
- Author Affiliations
A Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, Parkville, Vic. 3010, Australia.
B Department of Animal Husbandry, Government of Himachal Pradesh, Shimla – 171005, India.
C Faculty of Veterinary Science, University of Sydney, Narellan, NSW 2567, Australia.
D Corresponding author. Email: chauhans@student.unimelb.edu.au
Animal Production Science 56(7) 1105-1112 https://doi.org/10.1071/AN14070
Submitted: 4 February 2014 Accepted: 2 December 2014 Published: 21 April 2015
Abstract
The present study aimed to measure hydrogen peroxide (H2O2) in exhaled breath condensate (EBC) as an index of oxidative stress induced by heat stress (HS) and to evaluate the antioxidant potential of supranutritional levels of selenium (Se) and vitamin E under HS conditions in sheep. Thirty-two Merino × Poll Dorset ewes (in two replicates) were acclimated to indoor individual pen feeding of a pelleted control diet (0.24 g Se and 10 IU of vitamin E/kg DM) for 1 week. Sheep were then randomly allocated to a 2 × 2 factorial design with the respective factors being dietary Se (0.24 and 1.20 mg/kg DM as Sel-Plex) and vitamin E (10 and 100 IU/kg DM) for 2 weeks. After 1 week acclimation to the diets the sheep were placed in metabolism cages in one of two climatic chambers set to either thermoneutral (18−21°C and 40–50% relative humidity) or HS (28−40°C and 30–40% relative humidity) conditions for 1 week. Average respiration rate and rectal temperature were increased (P < 0.001) during HS. Similarly, H2O2 concentration in EBC and plasma reactive oxygen metabolites were increased significantly (P = 0.041 and P = 0.002, respectively), in sheep exposed to HS. The EBC H2O2 concentration was reduced (P < 0.05) in sheep fed the diet supplemented with supranutritional levels of both Se and vitamin E. Sheep supplemented with antioxidants also had lower respiration rates (191 vs 232 breaths/min, P = 0.012) and rectal temperature (40.33 vs 40.58°C, P = 0.039) under peak HS (1300 hours and 1700 hours) compared with those on the control diet indicating an improved capacity to handle HS. These data suggest that the H2O2 concentration in EBC can be utilised as a novel biomarker to demonstrate oxidative stress induced by HS in sheep.
Additional keywords: reactive oxygen species, selenium, vitamin E.
References
Alhidary IA, Shini S, Al Jassim RAM, Gaughan JB (2012a) Physiological responses of Australian Merino wethers exposed to high heat load. Journal of Animal Science 90, 212–220.| Physiological responses of Australian Merino wethers exposed to high heat load.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XnvFOiuw%3D%3D&md5=d0b5a99e0ef95d6b6bd7a62cfffcf9f5CAS | 21841087PubMed |
Alhidary IA, Shini S, Al Jassim RAM, Gaughan JB (2012b) Effect of various doses of injected selenium on performance and physiological responses of sheep to heat load. Journal of Animal Science 90, 2988–2994.
| Effect of various doses of injected selenium on performance and physiological responses of sheep to heat load.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsVKku7vK&md5=6ed43c71b69c33c4582b7d1b6daf89acCAS | 22585786PubMed |
Behne D, Kyriakopoulos A (2001) Mammalian selenium-containing proteins. Annual Review of Nutrition 21, 453–473.
| Mammalian selenium-containing proteins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlvFyrsr8%3D&md5=68272f95b25866a76fea42e063313d18CAS | 11375445PubMed |
Bernabucci U, Ronchi B, Lacetera N, Nardone A (2002) Markers of oxidative status in plasma and erythrocytes of transition dairy cows during hot season. Journal of Dairy Science 85, 2173–2179.
| Markers of oxidative status in plasma and erythrocytes of transition dairy cows during hot season.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnsV2nsrk%3D&md5=738485d99013695af61379a9db3087f6CAS | 12362449PubMed |
Bernabucci U, Lacetera N, Baumgard LH, Rhoads RP, Ronchi B, Nardone A (2010) Metabolic and hormonal acclimation to heat stress in domesticated ruminants. Animal 4, 1167–1183.
| Metabolic and hormonal acclimation to heat stress in domesticated ruminants.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38vptFyrtw%3D%3D&md5=29642efcd04e40c8905b3edf00b63abfCAS | 22444615PubMed |
Calamari L, Petrera F, Abeni F, Bertin G (2011) Metabolic and hematological profiles in heat stressed lactating dairy cows fed diets supplemented with different selenium sources and doses. Livestock Science 142, 128–137.
| Metabolic and hematological profiles in heat stressed lactating dairy cows fed diets supplemented with different selenium sources and doses.Crossref | GoogleScholarGoogle Scholar |
Cathcart MP, Love S, Hughes KJ (2012) The application of exhaled breath gas and exhaled breath condensate analysis in the investigation of the lower respiratory tract in veterinary medicine: A review. Veterinary Journal (London, England) 191, 282–291.
| The application of exhaled breath gas and exhaled breath condensate analysis in the investigation of the lower respiratory tract in veterinary medicine: A review.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC383mtFeluw%3D%3D&md5=e4c78a02f5c6a0ddf2ad5b8327969debCAS |
Celi P (2011) Biomarkers of oxidative stress in ruminant medicine. Immunopharmacology and Immunotoxicology 33, 233–240.
| Biomarkers of oxidative stress in ruminant medicine.Crossref | GoogleScholarGoogle Scholar | 20849293PubMed |
Celi P, Merlo M, Da Dalt L, Stefani A, Barbato O, Gabai G (2011) Relationship between late embryonic mortality and the increase in plasma advanced oxidised protein products (AOPP) in dairy cows. Reproduction, Fertility and Development 23, 527–533.
| Relationship between late embryonic mortality and the increase in plasma advanced oxidised protein products (AOPP) in dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXlsFKnsL0%3D&md5=820f88b29d71d8704f0abca761bb65beCAS |
Čepelak I, Dodig S (2007) Exhaled breath condensate: a new method for lung disease diagnosis. Clinical Chemistry and Laboratory Medicine 45, 945–952.
| Exhaled breath condensate: a new method for lung disease diagnosis.Crossref | GoogleScholarGoogle Scholar | 17867983PubMed |
Chauhan SS, Celi P, Leury BJ, Dunshea FR (2012) Supranutritional levels of antioxidants maintains feed intake and reduces heat stress in sheep. Journal of Animal Science 90, 672
Chauhan SS, Celi P, Leury BJ, Liu F, Dunshea FR (2013) Dietary selenium/vitamin E at supranutritional doses ameliorate effect of heat stress on physiological parameters and acid base balance in sheep. Annals of Nutrition & Metabolism 63, 1525
Chauhan SS, Celi P, Leury BJ, Clarke IJ, Dunshea FR (2014a) Dietary antioxidants at supranutritional doses improve oxidative status and reduce the negative effects of heat stress in sheep. Journal of Animal Science 92, 3364–3374.
| Dietary antioxidants at supranutritional doses improve oxidative status and reduce the negative effects of heat stress in sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtlKnur3F&md5=07c310b789d460b19bc52ab54df3809dCAS | 24894002PubMed |
Chauhan SS, Celi P, Ponnampalam EN, Leury BJ, Liu F, Dunshea FR (2014b) Antioxidant dynamics in the live animal and implications for ruminant health and product (meat/milk) quality: role of vitamin E and selenium. Animal Production Science 54, 1525–1536.
| Antioxidant dynamics in the live animal and implications for ruminant health and product (meat/milk) quality: role of vitamin E and selenium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhsVWjtrbL&md5=675ed93bb340ad66adb0584d18062983CAS |
Collier RJ, Dahl GE, VanBaale MJ (2006) Major advances associated with environmental effects on dairy cattle. Journal of Dairy Science 89, 1244–1253.
| Major advances associated with environmental effects on dairy cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xjt1SjsLk%3D&md5=e4e701d9d9559448117be644c1c5457dCAS | 16537957PubMed |
Deaton CM, Marlin DJ, Smith NC, Smith KC, Newton RJ, Gower SM, Cade SM, Roberts CA, Harris PA, Schroter RC, Kelly FJ (2004) Breath condensate hydrogen peroxide correlates with both airway cytology and epithelial lining fluid ascorbic acid concentration in the horse. Free Radical Research 38, 201–208.
| Breath condensate hydrogen peroxide correlates with both airway cytology and epithelial lining fluid ascorbic acid concentration in the horse.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhsFKktbk%3D&md5=18f18cab386df0687bc7173946df4a7eCAS | 15104214PubMed |
Di Trana A, Celi P, Claps S, Fedele V, Rubino R (2006) The effect of hot season and nutrition on the oxidative status and metabolic profile in dairy goats during mid lactation. Animal Science 82, 717–722.
| The effect of hot season and nutrition on the oxidative status and metabolic profile in dairy goats during mid lactation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFOitA%3D%3D&md5=8cb377b2150acf9cf569051986a2fd2cCAS |
Dunshea FR, Leury BJ, Fahri F, DiGiacomo K, Hung A, Chauhan S, Clarke IJ, Collier R, Little S, Baumgard L, Gaughan JB (2013) Amelioration of thermal stress impacts in dairy cows. Animal Production Science 53, 965–975.
| Amelioration of thermal stress impacts in dairy cows.Crossref | GoogleScholarGoogle Scholar |
Hefnawy AE, Tortora-Perez JL (2010) The importance of selenium and the effects of its deficiency in animal health. Small Ruminant Research 89, 185–192.
| The importance of selenium and the effects of its deficiency in animal health.Crossref | GoogleScholarGoogle Scholar |
Hunt J (2002) Exhaled breath condensate: an evolving tool for noninvasive evaluation of lung disease. The Journal of Allergy and Clinical Immunology 110, 28–34.
| Exhaled breath condensate: an evolving tool for noninvasive evaluation of lung disease.Crossref | GoogleScholarGoogle Scholar | 12110814PubMed |
Kharitonov SA, Barnes PJ (2002) Biomarkers of some pulmonary diseases in exhaled breath. Biomarkers 7, 1–32.
| Biomarkers of some pulmonary diseases in exhaled breath.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xis1WhtL0%3D&md5=0e80db128e45023934167bf19347c6d2CAS | 12101782PubMed |
Knobloch H, Becher G, Decker M, Reinhold P (2008) Evaluation of H2O2 and pH in exhaled breath condensate samples: methodical and physiological aspects. Biomarkers 13, 319–341.
| Evaluation of H2O2 and pH in exhaled breath condensate samples: methodical and physiological aspects.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXks1ejtL4%3D&md5=06b91a37cfafaeace65cd7700c219411CAS | 18415804PubMed |
Kostikas K, Papatheodorou G, Psathakis K, Panagou P, Loukides S (2003) Oxidative stress in expired breath condensate of patients with COPD. Chest 124, 1373–1380.
| Oxidative stress in expired breath condensate of patients with COPD.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXovF2hs70%3D&md5=ca3fc70b85c23d1903a38be42bd52b60CAS | 14555568PubMed |
Liu ZF, Sun XG, Tang J, Tang YQ, Tong HS, Wen Q, Liu YS, Su L (2011) Intestinal inflammation and tissue injury in response to heat stress and cooling treatment in mice. Molecular Medicine Reports 4, 437–443.
Loukides S, Bouros D, Papatheodorou G, Panagou P, Siafakas N (2002) The relationships among hydrogen peroxide in expired breath condensate, airway inflammation, and asthma severity. Chest 121, 338–346.
| The relationships among hydrogen peroxide in expired breath condensate, airway inflammation, and asthma severity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XitVWmsLo%3D&md5=89144b7f0b8fa479661d7d066dda4d5aCAS | 11834641PubMed |
Loukides S, Bakakos P, Kostikas K (2010) Exhaled breath condensate: hydrogen peroxide. In ‘Exhaled biomarkers’. (Eds I Horvath, JC DeJongste) pp. 162–172. (European Respiratory Society: Plymouth, UK)
Lykkesfeldt J, Svendsen O (2007) Oxidants and antioxidants in disease: oxidative stress in farm animals. Veterinary Journal (London, England) 173, 502–511.
| Oxidants and antioxidants in disease: oxidative stress in farm animals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXlt1Sis74%3D&md5=3743a1696f160cbbe0e0d43dce92bf38CAS |
Marai IFM, Ayyat MS, Abd El-Monem UM (2001) Growth performance and reproductive traits at first parity of New Zealand White female rabbits as affected by heat stress and its alleviation under Egyptian conditions. Tropical Animal Health and Production 33, 451–462.
| Growth performance and reproductive traits at first parity of New Zealand White female rabbits as affected by heat stress and its alleviation under Egyptian conditions.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38%2Fkt1Oitg%3D%3D&md5=af41e71de90f78f5e284ba5c95509a8cCAS |
Maseko T, Dunshea F, Howell K, Cho H-J, Rivera L, Furness J, Ng K (2014) Selenium-enriched Agaricus bisporus mushroom protects against increase in gut permeability ex vivo and up-regulates glutathione peroxidase 1 and 2 in hyperthermally-induced oxidative stress in rats. Nutrients 6, 2478–2492.
| Selenium-enriched Agaricus bisporus mushroom protects against increase in gut permeability ex vivo and up-regulates glutathione peroxidase 1 and 2 in hyperthermally-induced oxidative stress in rats.Crossref | GoogleScholarGoogle Scholar | 24962481PubMed |
Mashaly MM, Hendricks GL, Kalama MA, Gehad AE, Abbas AO, Patterson PH (2004) Effect of heat stress on production parameters and immune responses of commercial laying hens. Poultry Science 83, 889–894.
| Effect of heat stress on production parameters and immune responses of commercial laying hens.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2czgsVansw%3D%3D&md5=0905bc366a56ce5f50a4dac3457b31a5CAS | 15206614PubMed |
Mitchell JB, Russo A (1983) Thiols, thiol depletion, and thermosensitivity. Radiation Research 95, 471–485.
| Thiols, thiol depletion, and thermosensitivity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXltVeht7w%3D&md5=2c3824a162a8c11198ce187fc5f61022CAS | 6611860PubMed |
Pearce SC, Mani V, Weber TE, Rhoads RP, Patience JF, Baumgard LH, Gabler NK (2013) Heat stress and reduced plane of nutrition decreases intestinal integrity and function in pigs. Journal of Animal Science 91, 5183–5193.
| Heat stress and reduced plane of nutrition decreases intestinal integrity and function in pigs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhslKktrfN&md5=314c75f492ca65429992934e2bb368f6CAS | 23989867PubMed |
Po E, Williams C, Muscatello G, Celi P (2013) Assessment of oxidative stress biomarkers in exhaled breath condensate and blood of Thoroughbred foals. Veterinary Journal (London, England) 196, 269–271.
| Assessment of oxidative stress biomarkers in exhaled breath condensate and blood of Thoroughbred foals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsVemtLnM&md5=10ac19dd58c6f2304efc769fa883ab1cCAS |
Ranade R, Talukder S, Muscatello G, Celi P (2014) Assessment of oxidative stress biomarkers in exhaled breath condensate and blood of dairy heifer calves from birth to weaning. Veterinary Journal (London, England) 202, 583–587.
| Assessment of oxidative stress biomarkers in exhaled breath condensate and blood of dairy heifer calves from birth to weaning.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhvVOltL%2FK&md5=a637babd2cabe096905f3341869cc4a5CAS |
Reinhold P, Knobloch H (2010) Exhaled breath condensate: lessons learned from veterinary medicine. Journal of Breath Research 4, 017001
| Exhaled breath condensate: lessons learned from veterinary medicine.Crossref | GoogleScholarGoogle Scholar | 21386203PubMed |
Reinhold P, Jaeger J, Schroeder C (2006) Evaluation of methodological and biological influences on thecollection and composition of exhaled breath condensate Biomarkers 11, 118–142.
| Evaluation of methodological and biological influences on thecollection and composition of exhaled breath condensateCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XkslCjtrw%3D&md5=0561a70159cbdcf408f4a2457c5d3443CAS | 16766389PubMed |
Rooke JA, Robinson JJ, Arthur JR (2004) Effects of vitamin E and selenium on the performance and immune status of ewes and lambs. The Journal of Agricultural Science 142, 253–262.
| Effects of vitamin E and selenium on the performance and immune status of ewes and lambs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVGitrnM&md5=8de17b6cec841823bc66b056b81ef945CAS |
Shahid SK, Kharitonov SA, Wilson NM, Bush A, Barnes PJ (2005) Exhaled 8-isoprostane in childhood asthma. Respiratory Research 6, 79
| Exhaled 8-isoprostane in childhood asthma.Crossref | GoogleScholarGoogle Scholar | 16042771PubMed |
Sivakumar AVN, Singh G, Varshney VP (2010) Antioxidants supplementation on acid base balance during heat stress in goats. Asian-Australasian Journal of Animal Sciences 23, 1462–1468.
| Antioxidants supplementation on acid base balance during heat stress in goats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsVCitbY%3D&md5=b322663118f4b0fc290cc96c9f9d2ccbCAS |
Stolarek R, Bialasiewicz P, Krol M, Nowak D (2010) Breath analysis of hydrogen peroxide as a diagnostic tool. Clinica Chimica Acta 411, 1849–1861.
| Breath analysis of hydrogen peroxide as a diagnostic tool.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1OgsLrJ&md5=5e55ec6532e64b8eeb57539240598800CAS |
Tappel AL (1978) Glutathione peroxidase and hydroperoxides. Methods in Enzymology 52, 506–513.
| Glutathione peroxidase and hydroperoxides.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXjsFertw%3D%3D&md5=39ba0efebc44ac3237ff0370c3acac63CAS | 672654PubMed |
Trevisan M, Browne R, Ram M, Muti P, Freudenheim J, Carosella AM, Armstrong D (2001) Correlates of markers of oxidative status in the general population. American Journal of Epidemiology 154, 348–356.
| Correlates of markers of oxidative status in the general population.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MvltVWhuw%3D%3D&md5=939fc8353c958877bc69173a94cd8923CAS | 11495858PubMed |
Vitali A, Segnalini M, Bertocchi L, Bernabucci U, Nardone A, Lacetera N (2009) Seasonal pattern of mortality and relationships between mortality and temperature-humidity index in dairy cows. Journal of Dairy Science 92, 3781–3790.
| Seasonal pattern of mortality and relationships between mortality and temperature-humidity index in dairy cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXptVWku74%3D&md5=573701375b0ba6e530421201564f90fbCAS | 19620660PubMed |
West JW (2003) Effects of heat-stress on production in dairy cattle. Journal of Dairy Science 86, 2131–2144.
| Effects of heat-stress on production in dairy cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXks1GitbY%3D&md5=7b043c21aad453e2d51c2497fb379a10CAS | 12836950PubMed |
