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RESEARCH ARTICLE

The influence of heat load on Merino sheep. 3. Cytokine and biochemistry profiles

A. M. Lees https://orcid.org/0000-0003-4898-2843 A B E , G. Wijffels C , R. McCulloch C , S. Stockwell C , H. Owen D , M. L. Sullivan A , J. C. W. Olm D , A. J. Cawdell-Smith A and J. B. Gaughan A
+ Author Affiliations
- Author Affiliations

A School of Agriculture and Food Sciences, Animal Science Group, The University of Queensland, Gatton, Qld 4343, Australia.

B Present address: School of Environmental and Rural Science, University of New England, Armidale, NSW 2350, Australia.

C CSIRO Agriculture and Food, Queensland Bioscience Precinct, St Lucia, Qld 4072, Australia.

D School of Veterinary Sciences, The University of Queensland, Gatton, Qld 4343, Australia.

E Corresponding author. Email: a.lees@uqconnect.edu.au

Animal Production Science 60(16) 1940-1948 https://doi.org/10.1071/AN19689
Submitted: 30 November 2019  Accepted: 15 June 2020   Published: 27 July 2020

Abstract

Context: Approximately 2 million sheep are exported from Australia on live export voyages annually. As voyages travel from a southern hemisphere winter to a northern hemisphere summer, production and welfare issues associated with excessive heat load may arise.

Aims: The aim of this study was to evaluate the responses of sheep to incremental heat load under simulated live export conditions, specifically the influence of heat load on the metabolic and inflammatory status of sheep.

Methods: A total of 144 Merino wethers (44.02 ± 0.32 kg) were used in a 29-day climate controlled study using two cohorts of 72 sheep (n = 2), exposed to two treatments: (1) thermoneutral, and (2) hot. Sheep in the hot treatment were exposed to heat load simulated from live export voyages from Australia to the Middle East. Blood samples were collected from all sheep (n = 144) on Day 1, then at 7-day intervals (n = 5) for the duration of each 29-day period. Blood samples were analysed to determine the cytokine, biochemistry and haematology (data not presented here) profiles. Cytokine and biochemical profiles were analysed using a repeated measures model assuming a compound symmetry covariance. The model fitted included terms for cohort and treatment (hot, thermoneutral), and a term for sample collection day (day) and a treatment × day interaction. The subject factor corresponded to the cohort × treatment combinations.

Key results: There were no consistent trends in plasma cytokine and biochemical profiles. Bicarbonate was the only parameter that was influenced by cohort (P = 0.0035), treatment (P = 0.0025), collection (P = 0.0001) and treatment × collection (P = 0.0025). Furthermore, interleukin-6 and glutamate dehydrogenase were the only parameters that were not influenced by cohort (P > 0.295), treatment (P = 0.2567), collection (P > 0.06) or treatment × collection (P = 0.34).

Conclusions: Overall, these data highlight that the metabolic and inflammatory status of sheep exposed to incremental heat load, during a simulated live export voyage from a southern hemisphere winter to a northern hemisphere summer, were not markedly altered.

Implications: These results provide a preliminary evaluation of the inflammatory and metabolic status of sheep on arrival in the Middle East.

Additional keywords: biochemistry, cytokines, electrolytes, haematology, metabolism, histopathology.


References

Abeni F, Calamari L, Stefanini L (2007) Metabolic conditions of lactating Friesian cows during the hot season in the Po valley. 1. Blood indicators of heat stress. International Journal of Biometeorology 52, 87–96.
Metabolic conditions of lactating Friesian cows during the hot season in the Po valley. 1. Blood indicators of heat stress.Crossref | GoogleScholarGoogle Scholar | 17487513PubMed |

Achmadi J, Yanagisawa T, Sano H, Terashima Y (1993) Pancreatic insulin secretory response and insulin action in heat-exposed sheep given a concentrate or roughage diet. Domestic Animal Endocrinology 10, 279–287.
Pancreatic insulin secretory response and insulin action in heat-exposed sheep given a concentrate or roughage diet.Crossref | GoogleScholarGoogle Scholar | 8306632PubMed |

Alhidary IA, Shini S, Al Jassim RAM, Gaughan JB (2012) 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 | 21841087PubMed |

Alhidary IA, Shini S, Al Jassim RAM, Abudabos AM, Gaughan JB (2015) Effects of selenium and vitamin E on performance, physiological response, and selenium balance in heat-stressed sheep. Journal of Animal Science 93, 576–588.
Effects of selenium and vitamin E on performance, physiological response, and selenium balance in heat-stressed sheep.Crossref | GoogleScholarGoogle Scholar | 26020746PubMed |

Armbruster DA, Pry T (2008) Limit of blank, limit of detection and limit of quantitation. The Clinical Biochemist. Reviews / Australian Association of Clinical Biochemists 29, S49–S52.

Beatty DT, Barnes A, Taylor E, Pethick D, McCarthy M, Maloney SK (2006) Physiological responses of Bos taurus and Bos indicus cattle to prolonged, continuous heat and humidity. Journal of Animal Science 84, 972–985.
Physiological responses of Bos taurus and Bos indicus cattle to prolonged, continuous heat and humidity.Crossref | GoogleScholarGoogle Scholar | 16543576PubMed |

Beatty DT, Barnes A, Fleming PA, Taylor E, Maloney SK (2008) The effect of fleece on core and rumen temperature in sheep. Journal of Thermal Biology 33, 437–443.
The effect of fleece on core and rumen temperature in sheep.Crossref | GoogleScholarGoogle Scholar |

Bouchama A, Knochel JP (2002) Medical progress: heat stroke. The New England Journal of Medicine 346, 1978–1988.
Medical progress: heat stroke.Crossref | GoogleScholarGoogle Scholar | 12075060PubMed |

Brook A, Short B (1960) Sweating in sheep. Australian Journal of Agricultural Research 11, 557–569.
Sweating in sheep.Crossref | GoogleScholarGoogle Scholar |

Carroll JA, Burdick Sanchez NC (2014) Bill E. Kunkle interdisciplinary beef symposium: overlapping physiological responses and endocrine biomarkers that are indicative of stress responsiveness and immune function in beef cattle. Journal of Animal Science 92, 5311–5318.
Bill E. Kunkle interdisciplinary beef symposium: overlapping physiological responses and endocrine biomarkers that are indicative of stress responsiveness and immune function in beef cattle.Crossref | GoogleScholarGoogle Scholar | 25085405PubMed |

Department of Agriculture and Fisheries (2009) ‘Animal care and protection act 2001.’ (Queensland Government: Brisbane)

Department of Agriculture Fisheries and Forestry (2011) Australian standards for the export of livestock (version 2.3) 2011 and The Australian position statement of the export of livestock, Australian Government. Avalable at: http://www.agriculture.gov.au/ [Verified 18 May 2016]

Erridge C, Bennett-Guerrero E, Poxton IR (2002) Structure and function of lipopolysaccharides. Microbes and Infection 4, 837–851.
Structure and function of lipopolysaccharides.Crossref | GoogleScholarGoogle Scholar | 12270731PubMed |

Gnauck A, Lentle RG, Kruger MC (2016) Chasing a ghost?: issues with the determination of circulating levels of endotoxin in human blood. Critical Reviews in Clinical Laboratory Sciences 53, 197–215.
Chasing a ghost?: issues with the determination of circulating levels of endotoxin in human blood.Crossref | GoogleScholarGoogle Scholar | 26732012PubMed |

Hall DM, Baumgardner KR, Oberley TD, Gisolfi CV (1999) Splanchnic tissues undergo hypoxic stress during whole body hyperthermia. American Journal of Physiology. Gastrointestinal and Liver Physiology 276, G1195–G1203.
Splanchnic tissues undergo hypoxic stress during whole body hyperthermia.Crossref | GoogleScholarGoogle Scholar |

Hall DM, Buettner GR, Oberley LW, Xu L, Matthes RD, Gisolfi CV (2001) Mechanisms of circulatory and intestinal barrier dysfunction during whole body hyperthermia. American Journal of Physiology. Heart and Circulatory Physiology 280, H509–H521.
Mechanisms of circulatory and intestinal barrier dysfunction during whole body hyperthermia.Crossref | GoogleScholarGoogle Scholar | 11158946PubMed |

Itoh F, Obara Y, Rose MT, Fuse H, Hashimoto H (1998) Insulin and glucagon secretion in lactating cows during heat exposure. Journal of Animal Science 76, 2182–2189.
Insulin and glucagon secretion in lactating cows during heat exposure.Crossref | GoogleScholarGoogle Scholar | 9734870PubMed |

han TM, Malik S, Diju IU (2010) Correlation between plasma thyroid hormones and liver enzymes level in thyrotoxic cases and controls in Hazara Division. Journal of Ayub Medical College 22, 176–179.

Lambert GP, Gisolfi CV, Berg DJ, Moseley PL, Oberley LW, Kregel KC (2002) Selected contribution: hyperthermia-induced intestinal permeability and the role of oxidative and nitrosative stress. Journal of Applied Physiology 92, 1750–1761.
Selected contribution: hyperthermia-induced intestinal permeability and the role of oxidative and nitrosative stress.Crossref | GoogleScholarGoogle Scholar | 11896046PubMed |

Lees AM, Sullivan ML, Olm JCW, Cawdell-Smith AJ, Gaughan JB (2020a) The influence of heat load on Merino sheep. 1. Growth, performance, behaviour and climate. Animal Production Science
The influence of heat load on Merino sheep. 1. Growth, performance, behaviour and climate.Crossref | GoogleScholarGoogle Scholar |

Lees AM, Sullivan ML, Olm JCW, Cawdell-Smith AJ, Gaughan JB (2020b) The influence of heat load on Merino sheep. 2. Body temperature, wool surface temperature and respiratory dynamics Animal Production Science
The influence of heat load on Merino sheep. 2. Body temperature, wool surface temperature and respiratory dynamicsCrossref | GoogleScholarGoogle Scholar |

Leon LR, Blaha MD, DuBose DA (2006) Time course of cytokine, corticosterone, and tissue injury responses in mice during heat strain recovery. Journal of Applied Physiology 100, 1400–1409.
Time course of cytokine, corticosterone, and tissue injury responses in mice during heat strain recovery.Crossref | GoogleScholarGoogle Scholar | 16239608PubMed |

Lepherd ML, Canfield PJ, Hunt GB, Bosward KL (2009) Haematological, biochemical and selected acute phase protein reference intervals for weaned female Merino lambs. Australian Veterinary Journal 87, 5–11.
Haematological, biochemical and selected acute phase protein reference intervals for weaned female Merino lambs.Crossref | GoogleScholarGoogle Scholar | 19178470PubMed |

Lomborg SR, Nielsen LR, Heegaard PMH, Jacobsen S (2008) Acute phase proteins in cattle after exposure to complex stress. Veterinary Research Communications 32, 575–582.
Acute phase proteins in cattle after exposure to complex stress.Crossref | GoogleScholarGoogle Scholar | 18461465PubMed |

Macfarlane W, Morris R, Howard B (1958) Heat and water in tropical Merino sheep. Australian Journal of Agricultural Research 9, 217–228.
Heat and water in tropical Merino sheep.Crossref | GoogleScholarGoogle Scholar |

Mader TL, Gaughan JB, Johnson LJ, Hahn GL (2010) Tympanic temperature in confined beef cattle exposed to excessive heat load. International Journal of Biometeorology 54, 629–635.
Tympanic temperature in confined beef cattle exposed to excessive heat load.Crossref | GoogleScholarGoogle Scholar | 19404683PubMed |

Marai IFM, El-Darawany AA, Fadiel A, Abdel-Hafez MAM (2007) Physiological traits as affected by heat stress in sheep: a review. Small Ruminant Research 71, 1–12.
Physiological traits as affected by heat stress in sheep: a review.Crossref | GoogleScholarGoogle Scholar |

Mohri M, Rezapoor H (2009) Effects of heparin, citrate, and EDTA on plasma biochemistry of sheep: comparison with serum. Research in Veterinary Science 86, 111–114.
Effects of heparin, citrate, and EDTA on plasma biochemistry of sheep: comparison with serum.Crossref | GoogleScholarGoogle Scholar | 18572209PubMed |

Munford RS (2005) Invited review: detoxifying endotoxin: time, place and person. Journal of Endotoxin Research 11, 69–84.
Invited review: detoxifying endotoxin: time, place and person.Crossref | GoogleScholarGoogle Scholar | 15949133PubMed |

National Health and Medical Research Council (1997/2013) ‘Australian code for the care and use of animals for scientific purposes’ (National Health and Medical Research Council: Canberra)

Nazifi S, Gheisari HR, Poorabbas H (1999) The influences of thermal stress on serum biochemical parameters of Dromedary camels and their correlation with thyroid activity. Comparative Haematology International 9, 49–54.
The influences of thermal stress on serum biochemical parameters of Dromedary camels and their correlation with thyroid activity.Crossref | GoogleScholarGoogle Scholar |

O’Brien MD, Rhoads RP, Sanders SR, Duff GC, Baumgard LH (2010) Metabolic adaptations to heat stress in growing cattle. Domestic Animal Endocrinology 38, 86–94.
Metabolic adaptations to heat stress in growing cattle.Crossref | GoogleScholarGoogle Scholar | 19783118PubMed |

Oliver SR, Phillips NA, Novosad VL, Bakos MP, Talbert EE, Clanton TL (2012) Hyperthermia induces injury to the intestinal mucosa in the mouse: evidence for an oxidative stress mechanism. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 302, R845–R853.
Hyperthermia induces injury to the intestinal mucosa in the mouse: evidence for an oxidative stress mechanism.Crossref | GoogleScholarGoogle Scholar | 22237593PubMed |

Rhoads RP, Baumgard LH, Suagee JK (2013) 2011 and 2012 early careers achievement awards: metabolic priorities during heat stress with an emphasis on skeletal muscle. Journal of Animal Science 91, 2492–2503.
2011 and 2012 early careers achievement awards: metabolic priorities during heat stress with an emphasis on skeletal muscle.Crossref | GoogleScholarGoogle Scholar | 23408824PubMed |

Ronchi B, Lacetera N, Bernabucci U, Nardone A, Verini Supplizi A (1999) Distinct and common effects of heat stress and restricted feeding on metabolic status of Holstein heifers. Zootecnica e Nutrizione Animale 25, 11–20.

Russell KE, Roussel AJ (2007) Evaluation of the ruminant serum chemistry profile. The Veterinary Clinics of North America. Food Animal Practice 23, 403–426.
Evaluation of the ruminant serum chemistry profile.Crossref | GoogleScholarGoogle Scholar | 17920455PubMed |

Savage DB, Nolan JV, Godwin IR, Mayer DG, Aoetpah A, Nguyen T, Baillie ND, Rheinberger TE, Lawlor C (2008) Water and feed intake responses of sheep to drinking water temperature in hot conditions. Australian Journal of Experimental Agriculture 48, 1044–1047.
Water and feed intake responses of sheep to drinking water temperature in hot conditions.Crossref | GoogleScholarGoogle Scholar |

Scharf B, Carroll JA, Riley DG, Chase CC, Coleman SW, Keisler DH, Weaber RL, Spiers DE (2010) Evaluation of physiological and blood serum differences in heat-tolerant (Romosinuano) and heat-susceptible (Angus) Bos taurus cattle during controlled heat challenge. Journal of Animal Science 88, 2321–2336.
Evaluation of physiological and blood serum differences in heat-tolerant (Romosinuano) and heat-susceptible (Angus) Bos taurus cattle during controlled heat challenge.Crossref | GoogleScholarGoogle Scholar | 20190161PubMed |

Singleton KD, Wischmeyer PE (2006) Oral glutamine enhances heat shock protein expression and improves survival following hyperthermia. Shock 25, 295–299.
Oral glutamine enhances heat shock protein expression and improves survival following hyperthermia.Crossref | GoogleScholarGoogle Scholar | 16552363PubMed |

Srikandakumar A, Johnson EH, Mahgoub O (2003) Effect of heat stress on respiratory rate, rectal temperature and blood chemistry in Omani and Australian Merino sheep. Small Ruminant Research 49, 193–198.
Effect of heat stress on respiratory rate, rectal temperature and blood chemistry in Omani and Australian Merino sheep.Crossref | GoogleScholarGoogle Scholar |

St-Pierre NR, Cobanov B, Schnitkey G (2003) Economic losses from heat stress by US livestock industries. Journal of Dairy Science 86, E52–E77.
Economic losses from heat stress by US livestock industries.Crossref | GoogleScholarGoogle Scholar |

Stockman CA, Barnes AL, Maloney SK, Taylor E, McCarthy M, Pethick D (2011) Effect of prolonged exposure to continuous heat and humidity similar to long haul live export voyages in Merino wethers. Animal Production Science 51, 135–143.
Effect of prolonged exposure to continuous heat and humidity similar to long haul live export voyages in Merino wethers.Crossref | GoogleScholarGoogle Scholar |

Temim S, Chagneau A-M, Peresson R, Tesseraud S (2000) Chronic heat exposure alters protein turnover of three different skeletal muscles in finishing broiler chickens fed 20 or 25% protein diets. The Journal of Nutrition 130, 813–819.
Chronic heat exposure alters protein turnover of three different skeletal muscles in finishing broiler chickens fed 20 or 25% protein diets.Crossref | GoogleScholarGoogle Scholar | 10736335PubMed |

Tian Y-F, Lin C-H, Hsu S-F, Lin M-T (2013) Melatonin improves outcomes of heatstroke in mice by reducing brain inflammation and oxidative damage and multiple organ dysfunction. Mediators of Inflammation 2013, 1–8.
Melatonin improves outcomes of heatstroke in mice by reducing brain inflammation and oxidative damage and multiple organ dysfunction.Crossref | GoogleScholarGoogle Scholar |