1Department of Veterinary Medicine, Faculty of Veterinary Medicine, University of Ibadan, Nigeria
2Department of Veterinary Physiology ad Biochemistry, Faculty of Veterinary Medicine, University of Ibadan, Nigeria
Receive Date: 14 December 2023,
Revise Date: 30 January 2024,
Accept Date: 08 February 2024
Abstract
Heat stress is a limiting factor for livestock productivity in many countries. This study was designed to evaluate the influence of exposure of exotic pigs to high environmental temperatures on physiology, oxidative stress biomarkers and productivity. Multiparous sows (n = 40) in two equal groups (Groups N and H) were investigated. The pen temperature, relative humidity and Temperature-Humidity Index (THI) were measured for 30 days. The skin temperature, respiratory rate and rectal temperature were measured weekly. Haematology, serum biochemistry and oxidative biomarkers were also evaluated. The production records, including farrowing events (NFE), number of piglets at birth (NPB), number of piglets at weaning (NPW) and piglet mortality (NPM) were obtained per sow for the preceding 24 months. Data were analyzed using descriptive statistics and a student T-test at P+0.99 0C, 48.90+7.94 %) compared to Group N (25.21+0.94 0C, 58.97+6.21 %). The THI was higher in Group H (78.40+1.99). There was a significant increase in skin surface temperature and respiratory rate in Group H (37.70+1.40 0C and 39.70+4.28 bpm) with a slight increase in rectal temperature compared to Group N (33.86+0.95 0C and 35.79+2.89 bpm). There was a slight increase in PCV, blood urea nitrogen and a decrease in the levels of sodium, chloride, and bicarbonate in sows in Group H. There was a significant increase in hydrogen peroxide generation, nitric oxide contents and malondialdehyde levels, with a decrease in superoxide dismutase activity and glutathione content in Group H when compared to Group N. There was a reduction in farrowing events (N = 3.45+0.20; H = 3.00+ 0.19), number of piglets at birth (N = 29.15+1.92; H = 27.95+ 2.44), the number of piglets at weaning (N = 27.65+1.89; H = 25.90+ 2.25), and an increase in piglet mortality (N = 1.5+0.21; H = 2.05+0.42) in sows exposed to higher temperatures. The orientation of the pig housing in the north-south direction reduced its effectiveness. Exotic sows exposed to heat stress had altered physiology, experienced oxidative stress, were prone to renal and hepatic injury, and had reduced productivity. Adequate thermal comfort should be ensured in pig husbandry in the tropics for optimal health and productivity.
ABIOLA, J. O., OMOTOSHO, O. O., and IGADO, O. O., 2017. Meningoencephalocele, bilateral anorchia with radial and fibular hemimelia in a piglet. Journal of Morphological Science, 34 (3) p. 152-155. https://doi.org/10.4322/jms.107716
ABDEL-AZIZ, H. O., HAMDAN, H. M., and RAGAB, E. E., 2018. The histological effects of zinc oxide nanoparticles on the kidney of adult male rabbits. Sohag Medical Journal, 22(2), 297-301. https://doi.org/10.21608/smj.2018.40959
AHMED, M. O., OGEDENGBE, K., and LAWAL, N. S., 2022. Innovative Trend Analysis of Hydro-Meteorological variables in Ibadan, Nigeria. Journal of Fundamental and Applied Sciences. 14(1), 288-311. doi: http://dx.doi.org/10.4314/jfas.v14i1.15
AJAYI, A. E., and OLUFAYO, A. A., 1998. The sequence of wetanddrydays at Ibadan and Onne (sub-humid zone of Nigeria). Nigerian journal of technology 21(1):38-44
AO, X., and KIM, I.H., 2020. Effects of grape seed extract on performance, immunity, antioxidant capacity, and meat quality in Pekin ducks. Poultry Science 99, 2078–2086. https://doi.org/10.1016/j.psj.2019.12.014
ADEBIYI, O. A., MUIBI, M. A., and ALABA, O., 2017. Performance and behavioural characteristics of Pigs as affected by types and duration of evaporative cooling. Nigerian Journal of Animal Science 2017 (2):103 – 113
BING XIA, WEIDA WU, WEI FANG, XIAOBIN WEN, JINGJING XIE, and HONGFU ZHANG, 2022. Heat stress-induced mucosal barrier dysfunction is potentially associated with gut microbiota dysbiosis in pigs, Animal Nutrition 8. Pp. 289-299, https://doi.org/10.1016/j.aninu.2021.05.012.
BROWN-BRANDL, T. M., R. A. EIGENBERG, J. A. NIENABER, and S. D. KACHMAN. 2001. Thermoregulatory profile of a newer genetic line of pigs. Livestock Production Science 71: 253-260. https://doi.org/10.1016/S0301-6226(01)00184-1
BUHIMSCHI, I. A., SAADE, G. R. CHWALISZ, K., and GARFIELD, R. E., 1998. The nitric oxide pathway in preeclampsia: pathophysiological implications. Human Reproduction Update 4: 25-42. https://doi.org/10.1093/humupd/4.1.25
CELI, P. 2011. Biomarkers of oxidative stress in ruminant medicine. Immunopharmacology and Immunotoxicology 33: 233-240. https://doi.org/10.3109/08923973.2010.514917
CHAUDHARY, S. S., SINGH, V. K., UPADHYAY, R. C., PURI, G., ODEDARA, A. B., and PATEL, P. A., 2015. Evaluation of physiological and biochemical responses in different seasons in Surti buffaloes. Veterinary World 8, 727–731. https://doi.org/10.14202/vetworld.2015.727-731
CUI, Y., HAO, Y., LI J., BAO, W., LI, G., GAO, Y., and GU, X., 2016. Chronic Heat Stress Induces Immune Response, Oxidative Stress Response, and Apoptosis of Finishing Pig Liver: A Proteomic Approach. International Journal of Molecular Sciences 17(5) :393. https://doi.org/10.3390/ijms17050393.
CUTLER, R. S., FAHY, V. A., CRONIN, G. M., and SPICER, E. M., 2006. Preweaning mortality. In BE Straw, JJ Zimmerman, S D’Alliare, DJ Taylor, eds. Diseases of Swine, 9th ed. Ames, IA: Blackwell Publishing, pp. 1005–1006.
D’ALLAIRE, S., DROLET, R., and BRODEUR, D., 1996. Sow mortality associated with high ambient temperatures. The Canadian Veterinary Journal 37, 237–239. PMID: 8801022, PMCID: PMC1576357
EGBINOLA, C. N., and AMOBICHUKWU A. C., 2013. Climate Variation Assessment Based on Rainfall and Temperature in Ibadan, South-Western, Nigeria. Journal of Environment and Earth Science. Vol. 3, No.11
GODYĆ, D., HERBUT, P., ANGRECKA, S., and CORRÊA VIEIRA, F. M., 2020 Use of differentcooling methods in pig facilities to alleviate the effects of heatstress—a review. Animals. 10(9):1459. https://doi.org/10.3390/ani10091459
GONYOU, H.W., LERMAY, S.P., and ZHANG, Y., 2006. Effects of the environment on productivity and disease. In BE Straw, JJ Zimmerman, S D’Allaire, DJ Taylor, eds. Diseases of Swine, 9th ed. Ames, IA: Blackwell Publishing, pp. 1027–1038.
GUPTA, M., KUMAR, S., DANGI, S. S., and JANGIR, B. L., 2013. Physiological, biochemical and molecular responses to thermal stress in goats. International Journal of Livestock Research 3, 27–38. https://doi.org/10.5455/ijlr.20130502081121
HABIG, W. H., PABST, M. J., and JACOBY, W. B., 1974. Glutathione-S-transferase activity: The first enzymatic step in Mercapturic Acid formation. Journal of Biological Chemistry, 249, 7130–7139. PMID: 4436300
HASSAN, F. A., MAHROSE, K.M., and BASYONY, M.M., 2016. Effects of grape seed extract as a natural antioxidant on growth performance, carcass characteristics and antioxidant status of rabbits during heat stress. Archives of Animal Nutrition 70 (2), 141–154. https://doi.org/10.1080/1745039x.2016.1139609.
HOSSEINI-VASHANA, S. J., SAFDARI-ROSTAMABADA, M., PIRAYB, A. H., and SARIR, H., 2019. The growth performance, plasma biochemistry indices, immune system, antioxidant status, and intestinal morphology of heat stressed broiler chickens fed grape (Vitis vinifera) pomace. Animal Feed Science and Technology 259, 114343. https://doi.org/10.1016/j.anifeedsci.2019.114343
HUYNH, T. T. T., AARNINK, A. J. A., TRUONG, C. T., KEMP B., and VERSTEGEN, M. W. A., 2006: Effects of tropical climate and water-cooling methods on growing pigs’ responses. Livestock Science, 104(3): 278-291. https://doi.org/10.1016/j.livsci.2006.04.029
IGBOKWE, I. O., and MADUKA, C. V., 2018. Disease burden affecting pig production in Nigeria: Review of current issues and challenges. Revue D'élevage et de Médecine Vétérinaire Des Pays Tropicaux. 71 (1-2): 87-95 https://doi.org/10.19182/remvt.31290
JOHNSON, J. S., and BAUMGARD, L. H., 2019. PHYSIOLOGY SYMPOSIUM: Postnatal consequences of in utero heat stress in pigs. Journal of Animal Science 97(2):962-971. https://doi.org/10.1093/jas/sky472.
JOLLOW, D. J., MITCHELL, J. R., and ZAMPAGLIONE, N., 1974. Bromobenzene-induced liver necrosis. Protective role of glutathione and evidence for 3, 4- bromobenzene oxide as the hepatotoxic metabolite. Pharmacology 11(3): 151–169. https://doi.org/10.1159/000136485 32.
KLEM, T. B., BLEKEN, E., MORBERG, H., THORESEN, S. I., and FRAMSTAD, T., 2010. Hematologic and biochemical reference intervals for Norwegian crossbreed grower pigs. Veterinary Clinical Pathology 39:221–226. https://doi.org/10.1111/j.1939-165X.2009.00199.x.
LACETERA N 2019. Impact of climate change on animal health and welfare. Animal Frontiers 9, 26–31. https://doi.org/10.1093/af/vfy030
LARSON-MEYER, D. E., INGOLD, B. C., FENSTERSEIFER, S. R., AUSTIN, K. J., WECHSLER, P. J., HOLLIS, B. W., MAKOWSKI, A. J., and ALEXANDER, B.M., 2017 Sun exposure in pigs increases the vitamin D nutritional quality of pork. PLoS One. 12(11):e0187877. https://doi.org/10.1371/journal.pone.0187877.
LU, T., HARPER A., ZHAO J., ESTIENNE M., and DALLOUL R., 2014. Supplementing antioxidants to pigs fed diets high in oxidants: I. Effects on growth performance, liver function, and oxidative status. Journal of animal science 92: 5455-5463. https://doi.org/10.2527/jas.2013-7109
MAYORGA, E. J.; DAVID, R., RAMIREZ, B. C., ROSS J. W. and BAUMGARD, L. H. Heat stress adaptations in pigs. Animal Frontiers. v. 9. No. 1. p. 54–61. 2019. https://doi.org/10.1093/af/vfy035
MISRA H. P. and FRIDOVICH I. 1972. The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. Journal of Biological Chemistry 247(10):3170–3175. https://doi.org/10.1016/S0021-9258(19)45228- 9
MU, C., HAO, X., ZHANG, X., ZHAO, J. and ZHANG, J. 2021. Effects of high-concentrate diet supplemented with grape seed procyanidins on the colonic fermentation, colonic morphology, and inflammatory response in lambs. Animal Feed Science and Technology. 281, 115118 https://doi.org/10.1016/j.anifeedsci.2021.115118.
MUTUA J. Y., MARSHALL K., PAUL B. K. and NOTENBAERT A. M. O. 2020. A methodology for mapping current and future heat stress risk in pigs. Animal, 14(9). https://doi.org/10.1017/S1751731120000865.
NAZIFI S., SAEB M., ROWGHANI E. and KAVEH K. 2003. The influences of thermal stress on serum biochemical parameters of Iranian fat-tailed sheep and their correlation with triiodothyronine (T3), thyroxine (T4) and cortisol concentrations. Comparative Clinical Pathology 12, 135–139. https://doi.org/10.1007/s00580-003-0487-x
NOAA: National Oceanic and Atmospheric Administration. 1976. Livestock Hot Weather Stress. Operations Manual Letter c-31- 76. Kansas City.
OGUNDIJO O. A., OMOTOSHO O. O., AL-MUSTAPHA A. I., ABIOLA J. O. AWOSANYA E. J., ODUKOYA A, OWOICHO S., OYEWO M., IBRAHIM A. ORUM T. G., NANVEN M. B., BOLAJOKO M. B., LUKA P. and ADEYEMO O. K. 2023. A multi-state survey of farm-level preparedness towards African swine fever outbreak in Nigeria, Acta Tropica, 246. https://doi.org/10.1016/j.actatropica.2023.106989
OKORUWA M. I 2014. Effect of heat stress on thermoregulatory, live bodyweight and physiological responses of dwarf goats in southern Nigeria. European Science Journal 10, 255–264. Corpus ID: 261543298
OLALEYE, S. B., ADARAMOYE, O. A., ERIGBALI, P. P., and ADENIYI, O. S., 2007. Lead exposure increases oxidative stress in the gastric mucosa of HCl/ ethanol-exposed rats. World Journal of Gastroenterology, 13, 5121–5126. https://doi.org/10.3748/wjg.v13.i38.5121.
OMOTOSHO O.O, EMIKPE B.O., LASISI O. T and OLADUNJOYE V. O. 2016. Pig Slaughtering in Southwestern Nigeria: Peculiarities, Animal Welfare Concerns and Public Health Implications. African Journal of Infectious Diseases. 10(2): 146 – 155. https://doi.org/10.21010/ajid.v10i2.11
OYAGBEMI, A. A., OMOBOWALE, T. O., AKINRINDE, A. S., SABA, A. B., OGUNPOLU, B. S., and DARAMOLA, O., 2015. Lack of reversal of oxidative damage in renal tissues of lead acetate-treated rats. Environmental Toxicology, 30, 1235–1243. https://doi.org/10.1002/tox.21994
PATRA, A.K. and KAR, I., 2021. Heat stress on microbiota composition, barrier integrity, and nutrient transport in gut, production performance, and its amelioration in farm animals, 63 (2), 211–247. https://doi.org/10.5187/jast.2021.e48.
PHS (Public Health Service) (2015). Public health service policy on humane care and the use of laboratory animals. Washington, DC: US Department of Health and Human Services. Available at https://olaw.nih.gov/policies-laws/phs-policy.htm accessed 10 December 2022
POLLMANN, D. S. 2010. Seasonal effects on sow herds: industry experience and management strategies. Journal of Animal Science 88 (Suppl. 3):9 (Abstr) available at https://www.asas.org/docs/midwest/2010mwabstract.pdf?sfvrsn=5372c05e_2
PRAGNA, P., SEJIAN, V., SOREN, N.M., BAGATH, M., KRISHNAN, G., BEENA, V., DEVI, P.I., and BHATTA, R., 2018. Summer season induced rhythmic alterations in metabolic activities to adapt to heat stress in three indigenous (Osmanabadi, Malabari and Salem Black) goat breeds. Biological Rhythm Research 49, 551–565. https://doi.org/10.1080/09291016.2017.1386891
RANA, M. S., HASHEM, M. A., SAKIB, M. N., and KUMAR, A., 2014. Effect of heat stress on blood parameters in indigenous sheep. Journal of Bangladesh Agriculture 12, 91–94. https://doi.org/10.3329/jbau.v12i1.21253
RENAUDEAU, D., A. COLLIN, S. YAHAV, V. DE BASILIO, GOURDINE, J. L., and COLLIER, R. J., 2012. Adaptation to hot climate and strategies to alleviate heat stress in livestock production. Animal 6:707–728. https://doi.org/10.1017/s1751731111002448
RAUW, W. M., MAYORGA, E. J., LEI, S. M., DEKKERS, J. C. M., PATIENCE, J. F., GABLER, N. K., LONERGAN, S. M., and BAUMGARD, L H., 2017. Effects of Diet and Genetics on Growth Performance of Pigs in Response to Repeated Exposure to Heat Stress. Front. Genet. 8:155. https://doi.org/10.3389/fgene.2017.00155
ROJAS-DOWNING, M. M., NEJADHASHEMI, A. P., HARRIGAN, T., and WOZNICKI, S. A., 2017. Climate change and livestock: impacts, adaptation, and mitigation. Climate Risk Management 16, 145–163. https://doi.org/10.1016/j.crm.2017.02.001
ROTRUCK, J. T,, POPE, A. L., GANTHER, H. E., SWANSON, A. B., HAFEMAN, D. G., and HOEKSTRA, W. G., 1973 Selenium: biochemical role as a component of glutathione peroxidase. Science 179: 588e90. https://doi.org/10.1126/science.179.4073.588
SEJIAN, V., BHATTA, R., GAUGHAN, J.B., DUNSHEA, F.R., and LACETERA, N., 2018. Review: Adaptation of animals to heat stress, Animal, Volume 12, Supplement 2, Pages s431-s444, ISSN 1751-7311, https://doi.org/10.1017/S1751731118001945.
SHILJA, S., SEJIAN V., BAGATH, M., MECH, A., DAVID, C. G., KURIEN, E. K., VARMA, G., and BHATTA, R., 2016. Adaptive capability as indicated by behavioural and physiological responses, plasma HSP70 level, and PBMC HSP70 mRNA expression in Osmanabadi goats subjected to combined (heat and nutritional) stressors. International Journal of Biometeorology 60, 1311–1323. https://doi.org/10.1007/s00484-015-1124-5
SIRINI, A.M., and AMARAKOON, B. K., 2017. Regulation of oxidative stress in weaned piglets challenged with Escherichia coli. A Thesis submitted to Faculty of Graduate studies of The University of Manitoba. Available at https://mspace.lib.umanitoba.ca/items/52199d05-9e68-4d0f-9a77-dda5f1627475. Accessed December 1, 2023
STENDER, D. R., HARMON, J. D., WEISS, J. D., and COX, D., 2003. Comparison of different styles of swine finishing facilities within a uniform production system. Appl. Eng. Agric. 19, 79–82. https://doi.org/10.13031/2013.12734
TANG, L. P., LIU, Y. L., ZHANG, J. X., DING, K. N., LU, M. H., and HE, Y.M., 2022. Heat stress in broilers of liver injury effects of heat stress on oxidative stress and autophagy in liver of broilers. Poultry Science 101(10). https://doi.org/10.1016/j.psj.2022.102085
TURNER, A. G., ANDERSON, P. H., and MORRIS, H. A., 2012. Vitamin D and bone health. Scandinavian Journal of Clinical and Laboratory Investigation 243: 65–72. https://doi.org/10.3109/00365513.2012.681963
UCHIIDE, I., IHARA, T., and SUGAMATA, M., 2002. Pathological evaluation of the rat endometriosis model. Fertility and sterility 78: 782-786. https://doi.org/10.1016/s0015-0282(02)03327-7.
URKMEZ, E., and BIRICIK, H., 2022. Grape seed extract supplementation in heat-stressed preweaning dairy calves: I. Effects on antioxidant status, inflammatory response, hematological and physiological parameters, Animal Feed Science and Technology, 292. https://doi.org/10.1016/j.anifeedsci.2022.115421.
VALKO, M., RHODES, C., MONCOL, J., IZAKOVIC, M., and MAZUR, M., 2006. Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chemico-biological interactions 160: 1-40. https://doi.org/10.1016/j.cbi.2005.12.009.
VARASTEH, S., BRABER, S., AKBARI, P., GARSSEN, J., and FINK-GREMMELS, J., 2015 Differences in susceptibility to heat stress along the chicken intestine and the protective effects of galacto-oligosaccharides. PLOS ONE. 10:e0138975. https://doi.org/10.1371/journal.pone.0138975.
VARSHNEY, R., and KALE, R. K., 1990. Effect of calmodulin antagonists on radiation induced lipid peroxidation in microsomes. International Journal of Biological Macromolecules 158: 733-441. https://doi.org/10.1080/09553009014552121
WOLFF S. F. 1994 Ferrous ion oxidation in the presence of ferric ion indicator xylenol orange for measurement of hydrogen peroxides. Methods Enzymol 233(2):182–189. https://doi.org/10.1016/0003-2697(92)90122-n
VERMEER, H. M., and AARNINK A. J. A.,2023. Review on heat stress in pigs on farm. EU Reference Centre for Animal Welfare (Pigs). Wageningen Livestock Research, The Netherlands. Available at https://edepot.wur.nl/587090 Accessed on January 18, 2023.
ZHAO, W, ARTAIZ, O. IQBAL, Y., LE, H.H., DIGIACOMO, K, LEURY, B.J., FOTHERGILL, L.J., FURNESS, J.B., LIU, F., GREEN, M.P., FINGER, B.J., NAVARRO, M., ROURA, E., D'SOUZA, D.N., DUNSHEA, F.R., PLUSH, K.J., and COTTRELL, J.J., 2022. Heat stress of gilts around farrowing causes oxygen insufficiency in the umbilical cord and reduces piglet survival, animal, 16 (11). https://doi.org/10.1016/j.animal.2022.100668.
ZHONG, R. Z., and ZHOU, D.W., 2013. Oxidative stress and role of natural plant derived antioxidants in animal reproduction. Journal of Integrative Agriculture 12: 1826-1838. https://doi.org/10.1016/S2095-3119(13)60412-8
ZULOVICH, J. M. 2012. Effect of the Environment on Health. In Diseases of Swine, Tenth Edition. Edited by Jeffrey J. Zimmerman, Locke A. Karriker, Alejandro Ramirez, Kent J. Schwartz, Gregory W. Stevenson. pp 60-66. John Wiley & Sons, Inc. Published 2012 by John Wiley & Sons, Inc.