Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Animal Production Science Animal Production Science Society
Food, fibre and pharmaceuticals from animals
RESEARCH ARTICLE

The impact of heat stress on intestinal function and productivity in grow-finish pigs

N. K. Gabler A B and S. C. Pearce A
+ Author Affiliations
- Author Affiliations

A Department of Animal Science, Iowa State University, Ames, IA 50011, USA.

B Corresponding author. Email: ngabler@iastate.edu

Animal Production Science 55(12) 1403-1410 https://doi.org/10.1071/AN15280
Submitted: 4 June 2015  Accepted: 18 September 2015   Published: 19 October 2015

Abstract

Heat stress is a physiological condition when animals can no longer regulate their internal euthermic temperature. When livestock such as pigs are subjected to this environmental stress, it can be detrimental to performance, health and well-being, and if severe enough even death. Growing pigs are particularly susceptible to heat stress and one of the major organs first affected by heat stress is the gastrointestinal tract. As a result, reductions in appetite, intestinal function and integrity and increased risk of endotoxemia can modify post-absorptive metabolism and tissue accretion. These changes in intestinal integrity may be a result of altered expression of tight junction proteins, increased circulating endotoxin concentrations and markers of cellular stress (heat shock and hypoxia response), which is evident as early on as 2 h after heat-stress onset. Due to restricted blood flow, the ileum is more severely affected compared with the colon. Interestingly, many of the negative effects of heat stress on intestinal integrity appear to be similar to those observed with pigs reared under reduced nutrient and caloric intakes. Altogether, these depress pig performance and health, and extend days to market. Despite this impact on the gastrointestinal tract, under heat-stress conditions, intestinal glucose transport pathways are upregulated. This review discussed how heat stress (directly and indirectly via reduced feed intake) affects intestinal integrity and how heat stress contributes to decreased growth performance in growing pigs.

Additional keywords: heat shock proteins, hypoxia, nutrient transport.


References

Afrazi A, Sodhi CP, Good M, Jia H, Siggers R, Yazji I, Ma C, Neal MD, Prindle T, Grant ZS, Branca MF, Ozolek J, Chang EB, Hackam DJ (2012) Intracellular heat shock protein-70 negatively regulates TLR4 signaling in the newborn intestinal epithelium. Journal of Immunology (Baltimore, MD.: 1950) 188, 4543–4557.
Intracellular heat shock protein-70 negatively regulates TLR4 signaling in the newborn intestinal epithelium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XlvVKitr0%3D&md5=0729936f980bb3681c267a7151bb2591CAS |

Ashraf S, Zaneb H, Yousaf MS, Ijaz A, Sohail MU, Muti S, Usman MM, Ijaz S, Rehman H (2013) Effect of dietary supplementation of prebiotics and probiotics on intestinal microarchitecture in broilers reared under cyclic heat stress. Journal of Animal Physiology and Animal Nutrition 97, 68–73.
Effect of dietary supplementation of prebiotics and probiotics on intestinal microarchitecture in broilers reared under cyclic heat stress.Crossref | GoogleScholarGoogle Scholar | 23639019PubMed |

Barreau F, Hugot JP (2014) Intestinal barrier dysfunction triggered by invasive bacteria. Current Opinion in Microbiology 17, 91–98.
Intestinal barrier dysfunction triggered by invasive bacteria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXjs1KqurY%3D&md5=389f1bb999ba41fe67b61f81c5d00c8cCAS | 24440560PubMed |

Basu S, Binder RJ, Suto R, Anderson KM, Srivastava PK (2000) Necrotic but not apoptotic cell death releases heat shock proteins, which deliver a partial maturation signal to dendritic cells and activate the NF-kappa B pathway. International Immunology 12, 1539–1546.
Necrotic but not apoptotic cell death releases heat shock proteins, which deliver a partial maturation signal to dendritic cells and activate the NF-kappa B pathway.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXosVWjtbY%3D&md5=6bd28348a5546306b97a3af43cc30ee6CAS | 11058573PubMed |

Basuroy S, Sheth P, Kuppuswamy D, Balasubramanian S, Ray RM, Rao RK (2003) Expression of kinase-inactive c-Src delays oxidative stress-induced disassembly and accelerates calcium-mediated reassembly of tight junctions in the Caco-2 cell monolayer. The Journal of Biological Chemistry 278, 11916–11924.
Expression of kinase-inactive c-Src delays oxidative stress-induced disassembly and accelerates calcium-mediated reassembly of tight junctions in the Caco-2 cell monolayer.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXisVOnsrw%3D&md5=3037def4bed6f0316719ce57582a1474CAS | 12547828PubMed |

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 |

Boddicker RL, Seibert JT, Johnson JS, Pearce SC, Selsby JT, Gabler NK, Lucy MC, Safranski TJ, Rhoads RP, Baumgard LH, Ross JW (2014) Gestational heat stress alters postnatal offspring body composition indices and metabolic parameters in pigs. PLoS One 9, e110859
Gestational heat stress alters postnatal offspring body composition indices and metabolic parameters in pigs.Crossref | GoogleScholarGoogle Scholar | 25383953PubMed |

Bouchama A, Parhar RS, el-Yazigi A, Sheth K, al-Sedairy S (1991) Endotoxemia and release of tumor necrosis factor and interleukin 1 alpha in acute heatstroke. Journal of Applied Physiology 70, 2640–2644.

Bouchama A, Kwaasi A, Dehbi M, Al Mohanna F, Eldali A, El-Sayed R, Tbakhi A, Alzahrani AS, Roberts AG (2007) Glucocorticoids do not protect against the lethal effects of experimental heatstroke in baboons. Shock (Augusta, Ga.) 27, 578–583.
Glucocorticoids do not protect against the lethal effects of experimental heatstroke in baboons.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXls1GksLY%3D&md5=fb873562f135c69fd7e9798e31e131beCAS |

Brestensky M, Heger J, Nitrayova S, Patras P (2012) Total tract digestibility of nitrogen in pigs exposed to high environmental temperatures. Journal of Animal Science 90, 101–103.
Total tract digestibility of nitrogen in pigs exposed to high environmental temperatures.Crossref | GoogleScholarGoogle Scholar | 23365296PubMed |

Campos PH, Merlot E, Damon M, Noblet J, Le Floc’h N (2014) High ambient temperature alleviates the inflammatory response and growth depression in pigs challenged with Escherichia coli lipopolysaccharide. Veterinary Journal (London, England) 200, 404–409.
High ambient temperature alleviates the inflammatory response and growth depression in pigs challenged with Escherichia coli lipopolysaccharide.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXnsFeqs7c%3D&md5=ad98279abcd3521c4821016f10ea4d13CAS |

Chang M, Alsaigh T, Kistler EB, Schmid-Schönbein GW (2012) Breakdown of mucin as barrier to digestive enzymes in the ischemic rat small intestine. PLoS One 7, e40087
Breakdown of mucin as barrier to digestive enzymes in the ischemic rat small intestine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XpvVaitrg%3D&md5=6e691127c5f14407023e082ec682a957CAS | 22768227PubMed |

Chauhan SS, Celi P, Leury BJ, Clarke IJ, Dunshea FR (2014) Dietary antioxidants at supranutritional doses improve oxidative status and reduce the negative effects of heat stress in sheep. Journal of Animal Science 92, 4897–4908.
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%2BC2cXitVyju7nP&md5=361022cb6de141a829112e0b2675d451CAS | 25349340PubMed |

Collin A, van Milgen J, Dubois S, Noblet J (2001) Effect of high temperature and feeding level on energy utilization in piglets. Journal of Animal Science 79, 1849–1857.

Corfield AP (2015) Mucins: a biologically relevant glycan barrier in mucosal protection. Biochimica et Biophysica Acta 1850, 236–252.
Mucins: a biologically relevant glycan barrier in mucosal protection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtlOltbzL&md5=26c18fdffd5002643ee4b2ea1526836cCAS | 24821013PubMed |

Cruzen SM, Boddicker RL, Graves KL, Johnson TP, Arkfeld EK, Baumgard LH, Ross JW, Safranski TJ, Lucy MC, Lonergan SM (2015) Carcass composition of market weight pigs subjected to heat stress in utero and during finishing. Journal of Animal Science 93, 2587–2596.
Carcass composition of market weight pigs subjected to heat stress in utero and during finishing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtVCkt7fP&md5=c3769ae512f2b400b72108dda9ec6069CAS | 26020353PubMed |

De Maio A, Vazquez D (2013) Extracellular heat shock proteins: a new location, a new function. Shock (Augusta, Ga.) 40, 239–246.
Extracellular heat shock proteins: a new location, a new function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsVyru7nF&md5=746e6239918c78fd6ccd2b875a620535CAS |

Dokladny K, Moseley PL, Ma TY (2006) Physiologically relevant increase in temperature causes an increase in intestinal epithelial tight junction permeability. The American Journal of Physiology 290, G204–G212.

Dokladny K, Ye D, Kennedy JC, Moseley PL, Ma TY (2008) Cellular and molecular mechanisms of heat stress-induced up-regulation of occludin protein expression: regulatory role of heat shock factor-1. American Journal of Pathology 172, 659–670.
Cellular and molecular mechanisms of heat stress-induced up-regulation of occludin protein expression: regulatory role of heat shock factor-1.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXktVKhurg%3D&md5=72b99fedb87c50be8a56a1bb124a32cdCAS | 18276783PubMed |

Dörfel MJ, Huber O (2012) Modulation of tight junction structure and function by kinases and phosphatases targeting occludin. Journal of Biomedicine and Biotechnology
Modulation of tight junction structure and function by kinases and phosphatases targeting occludin.Crossref | GoogleScholarGoogle Scholar | 22315516PubMed |

Egberts HJ, Vellenga L, van Dijk JE, Mouwen JM (1991) Intestinal permeability in piglets during transmissible gastroenteritis. Zentralblatt fur Veterinarmedizin. Reihe A. 38, 157–164.
Intestinal permeability in piglets during transmissible gastroenteritis.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3MzhsVSnug%3D%3D&md5=e40a0f2ded743f417d724fcb9d95d260CAS | 1830439PubMed |

Eltzschig HK, Carmeliet P (2011) Hypoxia and inflammation. The New England Journal of Medicine 364, 656–665.
Hypoxia and inflammation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXitFykt78%3D&md5=f0a918256a7098187fc7d76bf20e13bdCAS | 21323543PubMed |

Environmental Protection Agency (2014) Climate change. Availalble at http://www.epa.gov/climatechange [Verified 4 March 2014]

Fang CW, Yao YM, Shi ZG, Yu Y, Wu Y, Lu LR, Sheng ZY (2002) Lipopolysaccharide-binding protein and lipopolysaccharide receptor CD14 gene expression after thermal injury and its potential mechanism(s). The Journal of Trauma 53, 957–967.
Lipopolysaccharide-binding protein and lipopolysaccharide receptor CD14 gene expression after thermal injury and its potential mechanism(s).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XpsleitL0%3D&md5=36b471b22c702a9771d211ff902750c9CAS | 12435950PubMed |

Garriga C, Hunter RR, Amat C, Planas JM, Mitchell MA, Moreto M (2006) Heat stress increases apical glucose transport in the chicken jejunum. The American Journal of Physiology 290, R195–R201.

Greer SN, Metcalf JL, Wang Y, Ohh M (2012) The updated biology of hypoxia-inducible factor. The EMBO Journal 31, 2448–2460.
The updated biology of hypoxia-inducible factor.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XmsFCgu78%3D&md5=f3fb20b726102f42ec9c374c8f2b8288CAS | 22562152PubMed |

Grenz A, Clambey E, Eltzschig HK (2012) Hypoxia signaling during intestinal ischemia and inflammation. Current Opinion in Critical Care 18, 178–185.
Hypoxia signaling during intestinal ischemia and inflammation.Crossref | GoogleScholarGoogle Scholar | 22322265PubMed |

Groschwitz KR, Hogan SP (2009) Intestinal barrier function: molecular regulation and disease pathogenesis. The Journal of Allergy and Clinical Immunology 124, 3–20.
Intestinal barrier function: molecular regulation and disease pathogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXnsl2gu7k%3D&md5=852406f2f0b9a321e5167187d61b6893CAS | 19560575PubMed |

Grubbs JK, Fritchen AN, Huff-Lonergan E, Gabler NK, Lonergan SM (2013) Selection for residual feed intake alters the mitochondria protein profile in pigs. Journal of Proteomics 80, 334–345.
Selection for residual feed intake alters the mitochondria protein profile in pigs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXktFWntrs%3D&md5=22994ddaae7f6bca0cbb9d3511c6b806CAS | 23403255PubMed |

Hall DM, Baumgardner KR, Overley TD, Gisolfi CV (1999) Splanchnic tissues undergo hypoxic stress during whole body hyperthermia. The American Journal of Physiology 276, G1195–G1203.

Hall DM, Buettner GR, Oberley LW, Xu L, Matthes RD, Gisolfi CV (2001) Mechanisms of circulatory and intestinal barrier dysfunction during whole body hyperthermia. The American Journal of Physiology 280, H509–H521.

Horowitz M (2002) From molecular and cellular to integrative heat defense during exposure to chronic heat. Comparative Biochemistry and Physiology. Part A, Molecular & Integrative Physiology 131, 475–483.
From molecular and cellular to integrative heat defense during exposure to chronic heat.Crossref | GoogleScholarGoogle Scholar |

Jacobi SK, Moeser AJ, Blikslager AT, Rhoads JM, Corl BA, Harrell RJ, Odle J (2013) Acute effects of rotavirus and malnutrition on intestinal barrier function in neonatal piglets. World Journal of Gastroenterology 19, 5094–5102.
Acute effects of rotavirus and malnutrition on intestinal barrier function in neonatal piglets.Crossref | GoogleScholarGoogle Scholar | 23964143PubMed |

Johansson ME, Thomsson KA, Hansson GC (2009) Proteomic analyses of the two mucus layers of the colon barrier reveal that their main component, the Muc2 mucin, is strongly bound to the Fcgbp protein. Journal of Proteome Research 8, 3549–3557.
Proteomic analyses of the two mucus layers of the colon barrier reveal that their main component, the Muc2 mucin, is strongly bound to the Fcgbp protein.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXms1ensL4%3D&md5=927bdb6d16437e17a72d4af2f1103ccaCAS | 19432394PubMed |

Johansson ME, Sjovall H, Hansson GC (2013) The gastrointestinal mucus system in health and disease. Nature Reviews. Gastroenterology & Hepatology 10, 352–361.
The gastrointestinal mucus system in health and disease.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXptVOlsrc%3D&md5=7a0021678f01f2922db6995e3f2ad092CAS |

Johnson JS, Sanz Fernandez MV, Gutierrez NA, Patience JF, Ross JW, Gabler NK, Lucy MC, Safranski TJ, Rhoads RP, Baumgard LH (2015a) Effects of in utero heat stress on postnatal body composition in pigs: I. Growing phase. Journal of Animal Science 93, 71–81.
Effects of in utero heat stress on postnatal body composition in pigs: I. Growing phase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXkt1WksLg%3D&md5=812f206a744909712aa114ba5d2cb6baCAS | 25568358PubMed |

Johnson JS, Sanz Fernandez MV, Patience JF, Ross JW, Gabler NK, Lucy MC, Safranski TJ, Rhoads RP, Baumgard LH (2015b) Effects of in utero heat stress on postnatal body composition in pigs: II. Finishing phase. Journal of Animal Science 93, 82–92.
Effects of in utero heat stress on postnatal body composition in pigs: II. Finishing phase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXkt1Wrsrs%3D&md5=4395e19245b4ac3ca1acff5a1f642c02CAS | 25568359PubMed |

Ke Q, Costa M (2006) Hypoxia-inducible factor-1 (HIF-1). Molecular Pharmacology 70, 1469–1480.
Hypoxia-inducible factor-1 (HIF-1).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFygsbjI&md5=c107c9527ef57955bf20ad9b458fca05CAS | 16887934PubMed |

Kim YS, Ho SB (2010) Intestinal goblet cells and mucins in health and disease: recent insights and progress. Current Gastroenterology Reports 12, 319–330.
Intestinal goblet cells and mucins in health and disease: recent insights and progress.Crossref | GoogleScholarGoogle Scholar | 20703838PubMed |

Lambert GP (2008) Intestinal barrier dysfunction, endotoxemia, and gastrointestinal symptoms: the ‘canary in the coal mine’ during exercise heat-stress. Medicine and Sport Science 53, 61–73.
Intestinal barrier dysfunction, endotoxemia, and gastrointestinal symptoms: the ‘canary in the coal mine’ during exercise heat-stress.Crossref | GoogleScholarGoogle Scholar | 19208999PubMed |

Lambert GP (2009) Stress-induced gastrointestinal barrier dysfunction and its inflammatory effects. Journal of Animal Science 87, E101–E108.
Stress-induced gastrointestinal barrier dysfunction and its inflammatory effects.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1M3mtVSrug%3D%3D&md5=40fcc87ab05b1757d7f6ca5074c39310CAS | 18791134PubMed |

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 | 1:CAS:528:DC%2BD38XjtVKjtLY%3D&md5=e42b10376c7e181e3bd640da923f706eCAS | 11896046PubMed |

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 | 1:CAS:528:DC%2BD28XksFyhtrc%3D&md5=701efd42be7a09fd571b7ede63b5aa8eCAS | 16239608PubMed |

Lim CL, Wilson G, Brown L, Coombes JS, Mackinnon LT (2007) Pre-existing inflammatory state compromises heat tolerance in rats exposed to heat stress. The American Journal of Physiology 292, R186–R194.

Loboda A, Jozkowicz A, Dulak J (2010) HIF-1 and HIF-2 transcription factors–similar but not identical. Molecules and Cells 29, 435–442.
HIF-1 and HIF-2 transcription factors–similar but not identical.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmslShsbk%3D&md5=5d9abc25fd3837353dea26048088c685CAS | 20396958PubMed |

Majmundar AJ, Wong WJ, Simon MC (2010) Hypoxia-inducible factors and the response to hypoxic stress. Molecular Cell 40, 294–309.
Hypoxia-inducible factors and the response to hypoxic stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlCjtr%2FN&md5=d93feed705a17a89c8abf8ad3ebf832cCAS | 20965423PubMed |

Mani V, Harris AJ, Keating AF, Weber TE, Dekkers JC, Gabler NK (2013) Intestinal integrity, endotoxin transport and detoxification in pigs divergently selected for residual feed intake. Journal of Animal Science 91, 2141–2150.
Intestinal integrity, endotoxin transport and detoxification in pigs divergently selected for residual feed intake.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXotl2gtrs%3D&md5=31df433e616807cd46b02504a730408eCAS | 23463550PubMed |

Montilla SIR, Johnson TP, Pearce SC, Gardan-Salmon D, Gabler NK, Ross JW, Rhoads RP, Baumgard LH, Lonergan SM, Selsby JT (2014) Heat stress causes oxidative stress but not inflammatory signaling in porcine skeletal muscle. Temperature 1, 42–50.
Heat stress causes oxidative stress but not inflammatory signaling in porcine skeletal muscle.Crossref | GoogleScholarGoogle Scholar |

Moser LA, Carter M, Schultz-Cherry S (2007) Astrovirus increases epithelial barrier permeability independently of viral replication. Journal of Virology 81, 11937–11945.
Astrovirus increases epithelial barrier permeability independently of viral replication.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1aisrfE&md5=711b49c9169abe8bf5e5191d197e1b05CAS | 17699569PubMed |

Musch MW, Walsh-Reitz MM, Chang EB (2006) Roles of ZO-1, occludin, and actin in oxidant-induced barrier disruption. The American Journal of Physiology 290, G222–G231.

Nickel W, Seedorf M (2008) Unconventional mechanisms of protein transport to the cell surface of eukaryotic cells. Annual Review of Cell and Developmental Biology 24, 287–308.
Unconventional mechanisms of protein transport to the cell surface of eukaryotic cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlOgtbbJ&md5=957c4bb3b9537b458c8b9abd53482868CAS | 18590485PubMed |

O’Neill LA, Hardie DG (2013) Metabolism of inflammation limited by AMPK and pseudo-starvation. Nature 493, 346–355.
Metabolism of inflammation limited by AMPK and pseudo-starvation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXptlKntg%3D%3D&md5=ae8e37fc588480af23da492febf44c54CAS | 23325217PubMed |

Pearce SC, Mani V, Boddicker RL, Johnson JS, Weber TE, Ross JW, Baumgard LH, Gabler NK (2012) Heat stress reduces barrier function and alters intestinal metabolism in growing pigs. Journal of Animal Science 90, 257–259.
Heat stress reduces barrier function and alters intestinal metabolism in growing pigs.Crossref | GoogleScholarGoogle Scholar | 23365348PubMed |

Pearce SC, Gabler NK, Ross JW, Escobar J, Patience JF, Rhoads RP, Baumgard LH (2013a) The effects of heat stress and plane of nutrition on metabolism in growing pigs. Journal of Animal Science 91, 2108–2118.
The effects of heat stress and plane of nutrition on metabolism in growing pigs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXotl2gsbg%3D&md5=77b493ac57a3563192a572e4e5cffea1CAS | 23463563PubMed |

Pearce SC, Mani V, Boddicker RL, Johnson JS, Weber TE, Ross JW, Rhoads RP, Baumgard LH, Gabler NK (2013b) Heat stress reduces intestinal barrier integrity and favors intestinal glucose transport in growing pigs. PLoS One 8, e70215
Heat stress reduces intestinal barrier integrity and favors intestinal glucose transport in growing pigs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXht1yqu7vL&md5=60a7d489a186ca38cb6be54c0eef3f0eCAS | 23936392PubMed |

Pearce SC, Mani V, Weber TE, Rhoads RP, Patience JF, Baumgard LH, Gabler NK (2013c) 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 |

Pearce SC, Sanz-Fernandez MV, Hollis JH, Baumgard LH, Gabler NK (2014) Short-term exposure to heat stress attenuates appetite and intestinal integrity in growing pigs. Journal of Animal Science 92, 5444–5454.
Short-term exposure to heat stress attenuates appetite and intestinal integrity in growing pigs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtV2gsLc%3D&md5=ef58a9177e38c4efd7529b84ddf448a8CAS | 25367514PubMed |

Pearce SC, Sanz Fernandez MV, Torrison J, Wilson ME, Baumgard LH, Gabler NK (2015) Dietary organic zinc attenuates heat-stress induced changes in pig intestinal integrity and metabolism. Journal of Animal Science
Dietary organic zinc attenuates heat-stress induced changes in pig intestinal integrity and metabolism.Crossref | GoogleScholarGoogle Scholar |

Petrof EO, Ciancio MJ, Chang EB (2004) Role and regulation of intestinal epithelial heat shock proteins in health and disease. Chinese Journal of Digestive Diseases 5, 45–50.
Role and regulation of intestinal epithelial heat shock proteins in health and disease.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXks1Sgtbs%3D&md5=7307689afa58413742cf80f0e76f391dCAS | 15612656PubMed |

Prosser C, Stelwagen K, Cummins R, Guerin P, Gill N, Milne C (2004) Reduction in heat-induced gastrointestinal hyperpermeability in rats by bovine colostrum and goat milk powders. Journal of Applied Physiology 96, 650–654.
Reduction in heat-induced gastrointestinal hyperpermeability in rats by bovine colostrum and goat milk powders.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2c%2FhvVCktQ%3D%3D&md5=00a26e5407113a424c9ab77b167960d5CAS | 14527963PubMed |

Qi H, Wang P, Liu C, Li M, Wang S, Huang Y, Wang F (2011) Involvement of HIF-1α in MLCK-dependent endothelial barrier dysfunction in hypoxia. Cellular Physiology and Biochemistry 27, 251–262.
Involvement of HIF-1α in MLCK-dependent endothelial barrier dysfunction in hypoxia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXkt1Khu7g%3D&md5=70e05a135c6090b538f109bd13e0c8ffCAS | 21471714PubMed |

Raleigh DR, Boe DM, Yu D, Weber CR, Marchiando AM, Bradford EM, Wang Y, Wu L, Schneeberger EE, Shen L, Turner JR (2011) Occludin S408 phosphorylation regulates tight junction protein interactions and barrier function. Journal of Cellular Biology 193, 565–582.
Occludin S408 phosphorylation regulates tight junction protein interactions and barrier function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXlvFKmsb8%3D&md5=b48ad1455d3922f3206c1accca5d26acCAS |

Renaudeau D, Gourdine JL, St-Pierre NR (2011) A meta-analysis of the effects of high ambient temperature on growth performance of growing-finishing pigs. Journal of Animal Science 89, 2220–2230.
A meta-analysis of the effects of high ambient temperature on growth performance of growing-finishing pigs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXoslCisb4%3D&md5=492819bacc9ecb4cbbe1a1cf5eb74810CAS | 21297065PubMed |

Renaudeau D, Collin A, Yahav S, de Basilio V, Gourdine JL, Collier RJ (2012) Adaptation to hot climate and strategies to alleviate heat stress in livestock production. Animal 6, 707–728.
Adaptation to hot climate and strategies to alleviate heat stress in livestock production.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC38ngsFejtw%3D%3D&md5=0b5520dcb6568a368cb976de20aa98fbCAS | 22558920PubMed |

Renaudeau D, Frances G, Dubois S, Gilbert H, Noblet J (2013) Effect of thermal heat stress on energy utilization in two lines of pigs divergently selected for residual feed intake. Journal of Animal Science 91, 1162–1175.
Effect of thermal heat stress on energy utilization in two lines of pigs divergently selected for residual feed intake.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmsFKntLg%3D&md5=d5a5696c100495595405c3445e7b5d07CAS | 23296816PubMed |

Semenza GL (2007) Hypoxia-inducible factor 1 (HIF-1) pathway. Science’s STKE 407, cm8 [Review]

Seppet E, Gruno M, Peetsalu A, Gizatullina Z, Nguyen HP, Vielhaber S, Wussling MH, Trumbeckaite S, Arandarcikaite O, Jerzembeck D, Sonnabend M, Jegorov K, Zierz S, Striggow F, Gellerich FN (2009) Mitochondria and energetic depression in cell pathophysiology. International Journal of Molecular Sciences 10, 2252–2303.
Mitochondria and energetic depression in cell pathophysiology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmvVCmur4%3D&md5=4ac0d9840249cf74b51030f0960f53e6CAS | 19564950PubMed |

Singh IS, Hasday JD (2013) Fever, hyperthermia and the heat shock response. International Journal of Hyperthermia 29, 423–435.
Fever, hyperthermia and the heat shock response.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXht1SlsbbM&md5=e6cb9c33fb63ad9e73b472023baceee8CAS | 23863046PubMed |

Song R, Foster DN, Shurson GC (2011) Effects of feeding diets containing bacitracin methylene disalicylate to heat-stressed finishing pigs. Journal of Animal Science 89, 1830–1843.
Effects of feeding diets containing bacitracin methylene disalicylate to heat-stressed finishing pigs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnsVWkt7k%3D&md5=0fc59fd927ac77705e467195a57816b5CAS | 21297060PubMed |

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 |

Toghyani M, Shivazad M, Gheisari A, Bahadoran R (2012) Chromium supplementation can alleviate the negative effects of heat stress on growth performance, carcass traits, and meat lipid oxidation of broiler chicks without any adverse impacts on blood constituents. Biological Trace Element Research 146, 171–180.
Chromium supplementation can alleviate the negative effects of heat stress on growth performance, carcass traits, and meat lipid oxidation of broiler chicks without any adverse impacts on blood constituents.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XksVeqs7Y%3D&md5=b9a84ad3603e4a26613c03131eb58bbbCAS | 22006223PubMed |

Turner JR (2006) Molecular basis of epithelial barrier regulation: from basic mechanisms to clinical application. American Journal of Pathology 169, 1901–1909.
Molecular basis of epithelial barrier regulation: from basic mechanisms to clinical application.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhvV2itQ%3D%3D&md5=2f5d53069ef9cfbc3f94c7d99bd3246cCAS | 17148655PubMed |

Turner JR (2009) Intestinal mucosal barrier function in health and disease. Nature Reviews. Immunology 9, 799–809.
Intestinal mucosal barrier function in health and disease.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlSqsb3J&md5=7ad0f80fbc87e4c685cfbb06a0996bc4CAS | 19855405PubMed |

Van Why SK, Mann AS, Ardito T, Thulin G, Ferris S, Macleod MA, Kashgarian M, Siegel NJ (2003) Hsp27 associates with actin and limits injury in energy depleted renal epithelia. Journal of the American Society of Nephrology 14, 98–106.
Hsp27 associates with actin and limits injury in energy depleted renal epithelia.Crossref | GoogleScholarGoogle Scholar | 12506142PubMed |

Webel DM, Finck BN, Baker DH, Johnson RW (1997) Time course of increased plasma cytokines, cortisol, and urea nitrogen in pigs following intraperitoneal injection of lipopolysaccharide. Journal of Animal Science 75, 1514–1520.

Wheelock JB, Rhoads RP, Vanbaale MJ, Sanders SR, Baumgard LH (2010) Effects of heat stress on energetic metabolism in lactating Holstein cows. Journal of Dairy Science 93, 644–655.
Effects of heat stress on energetic metabolism in lactating Holstein cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1CjtLY%3D&md5=efe9ce05fb26a5d6eb876885db73c7f3CAS | 20105536PubMed |

Wright EM, Loo DD (2000) Coupling between Na+, sugar, and water transport across the intestine. Annals of the New York Academy of Sciences 915, 54–66.
Coupling between Na+, sugar, and water transport across the intestine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXntVChtw%3D%3D&md5=3b0b2a0edec1716cc33182132df2bfabCAS | 11193601PubMed |

Yan Y, Zhao Y, Wang H, Fan M (2006) Pathophysiological factors underlying heatstroke. Medical Hypotheses 67, 609–617.
Pathophysiological factors underlying heatstroke.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XmtlGlsL4%3D&md5=3bde3a72f339b2b686ab3a00092b7456CAS | 16631316PubMed |

Yang PC, He SH, Zheng PY (2007) Investigation into the signal transduction pathway via which heat stress impairs intestinal epithelial barrier function. Journal of Gastroenterology and Hepatology 22, 1823–1831.
Investigation into the signal transduction pathway via which heat stress impairs intestinal epithelial barrier function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlOltbzM&md5=cdd68f7b85182407824fb0dab0825880CAS | 17914957PubMed |

Yu LC, Turner JR, Buret AG (2006) LPS/CD14 activation triggers SGLT-1-mediated glucose uptake and cell rescue in intestinal epithelial cells via early apoptotic signals upstream of caspase-3. Experimental Cell Research 312, 3276–3286.
LPS/CD14 activation triggers SGLT-1-mediated glucose uptake and cell rescue in intestinal epithelial cells via early apoptotic signals upstream of caspase-3.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XpvFGgurg%3D&md5=bc98c5559b9d7aa870649e1d35b62288CAS | 16860318PubMed |

Yu LC, Huang CY, Kuo WT, Sayer H, Turner JR, Buret AG (2008) SGLT-1-mediated glucose uptake protects human intestinal epithelial cells against Giardia duodenalis-induced apoptosis. International Journal for Parasitology 38, 923–934.
SGLT-1-mediated glucose uptake protects human intestinal epithelial cells against Giardia duodenalis-induced apoptosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmtlSktbw%3D&md5=1749d1b9fe6bc52aca816f0a63ac0289CAS | 18281046PubMed |

Zeferino CP, Komiyama CM, Fernandes S, Sartori JR, Teixeira PS, Moura AS (2013) Carcass and meat quality traits of rabbits under heat stress. Animal 7, 518–523.
Carcass and meat quality traits of rabbits under heat stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvVCnsLk%3D&md5=cb2b66e8d4da7b03cefe6419094beb5bCAS | 23031323PubMed |

Zhang Q, Li Q, Wang C, Li N, Li J (2012) Redistribution of tight junction proteins during EPEC infection in vivo. Inflammation 35, 23–32.
Redistribution of tight junction proteins during EPEC infection in vivo.Crossref | GoogleScholarGoogle Scholar | 21170673PubMed |