Physiological mechanisms through which heat stress compromises reproduction in pigs

Ross, Jason W.; Hale, Benjamin J.; Seibert, Jacob T.; Romoser, Matthew R.; Adur, Malavika K.; Keating, Aileen F.; Baumgard, Lance H.

doi:10.1002/mrd.22859

Cited by 128Effects of Environmental Stressors on LivestockReproductive Physiology in LivestockSperm and Testicular Function

Physiological mechanisms through which heat stress compromises reproduction in pigs

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Ross, Jason W., Hale, Benjamin J., Seibert, Jacob T., Romoser, Matthew R., Adur, Malavika K., Keating, Aileen F., Baumgard, Lance H.·2017·Molecular Reproduction and Development

DOI 10.1002/mrd.22859

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Abstract

Seasonal variations in environmental temperatures impose added stress on domestic species bred for economically important production traits. These heat‐mediated stressors vary on a seasonal, daily, or spatial scale, and negatively impact behavior and reduce feed intake and growth rate, which inevitably lead to reduced herd productivity. The seasonal infertility observed in domestic swine is primarily characterized by depressed reproductive performance, which manifests as delayed puberty onset, reduced farrowing rates, and extended weaning‐to‐estrus intervals. Understanding the effects of heat stress at the organismal, cellular, and molecular level is a prerequisite to identifying mitigation strategies that should reduce the economic burden of compromised reproduction. In this review, we discuss the effect of heat stress on an animal's ability to maintain homeostasis in multiple systems via several hypothalamic‐pituitary‐end organ axes. Additionally, we discuss our understanding of epigenetic programming and how hyperthermia experienced in utero influences industry‐relevant postnatal phenotypes. Further, we highlight the recent recognized mechanisms by which distant tissues and organs may molecularly communicate via extracellular vesicles, a potentially novel mechanism contributing to the heat‐stress response.

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Respiratory rate, core body temperature, rectal temperature, skin temperature, feed, water intake and other physiological responses as well as production performance are affected by heat stress to varying levels.
“Respiratory rate, core body temperature, rectal temperature, skin temperature, feed, water intake and other physiological responses as well as production performance (pregnancy rate, delivery times, estrus time, etc.) are affected by heat stress to varying levels [24,25,26,27,28].”
From Modeling of Heat Stress in Sows—Part 1: Establishment of the Prediction Model for the Equivalent Temperature Index of the Sows (2021) · cites this paper as [28]
Conditions associated with increased insulin signaling (obesity and polycystic ovary syndrome) are associated with reproductive dysfunction.
“Conditions associated with increased insulin signaling (such as obesity and polycystic ovary syndrome) are also associated with reproductive dysfunction [39].”
From Stress and the HPA Axis: Balancing Homeostasis and Fertility. (2017) · cites this paper as [39]

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Güzeloğlu, A., Ambrose, D. J., Kassa, T., Díaz, T., Thatcher, M.-J., & Thatcher, W. W. (2001) · Animal Reproduction Science · doi:10.1016/s0378-4320(01)00082-3 · Cited by 96 · see citing works
The effect of heat stress on gene expression, synthesis of steroids, and apoptosis in bovine granulosa cells
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Testicular Function in Boars Exposed to Elevated Ambient Temperature1
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Heat stress induces autophagy in pig ovaries during follicular development
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Epigenetics in fertilization and preimplantation embryo development
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Environmental Heat Effects on Bovine Luteinizing Hormone
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Gestational Heat Stress Alters Postnatal Offspring Body Composition Indices and Metabolic Parameters in Pigs
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Heat stress diminishes gonadotropin receptor expression and enhances susceptibility to apoptosis of rat granulosa cells
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Effects of in utero heat stress on postnatal body composition in pigs: I. Growing phase1,2
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Influence of sex and gonadal status of sheep on cortisol secretion in response to ACTH and on cortisol and LH secretion in response to stress: importance of different stressors
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A role for gastrointestinal endotoxins in enhancement of heat tolerance by physical fitness
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Reproductive epigenetics
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Effects of Glucocorticoids on Maturation of Pig Oocytes and Their Subsequent Fertilizing Capacity In Vitro1
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Heat stress impairs mice granulosa cell function by diminishing steroids production and inducing apoptosis
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Insulin induces myocardial protection and Hsp70 localization to plasma membranes in rat hearts
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Effect of two types of stress (heat shock/high temperature and malnutrition/serum deprivation) on porcine ovarian cell functions and their response to hormones
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Increased sow nutrition during midgestation affects muscle fiber development and meat quality, with no consequences on growth performance1
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Effect of light regimen under various ambient temperatures on sow and litter performance1
Prunier, A., Dourmad, J.-Y., & Etienne, M. L. (1994) · Journal of Animal Science · doi:10.2527/1994.7261461x · Cited by 70 · see citing works
In vitro thermal stress induces apoptosis and reduces development of porcine parthenotes
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Effects of in utero heat stress on postnatal body composition in pigs: II. Finishing phase1
Johnson, J. S., Sanz-Fernandez, M. V., Patience, J. F., Ross, J. W., Gabler, N. K., Lucy, M. C., Safranski, T. J., Rhoads, R. P., & Baumgard, L. H. (2015) · Journal of Animal Science · doi:10.2527/jas.2014-8355 · Cited by 69 · see citing works
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Effect of Season and Outdoor Climate on Litter Size at Birth in Purebred Landrace and Yorkshire Sows in Thailand
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The involvement of cell death and survival in neural tube defects: a distinct role for apoptosis and autophagy?
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Looking Ahead Perspective: Where Will the Future of Exercise Biology Take Us?
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Effects of breed and season on performance of lactating sows in a tropical humid climate1
Gourdine, J.-L., Bidanel, J. P., Noblet, J., & Renaudeau, D. (2006) · Journal of Animal Science · doi:10.2527/2006.842360x · Cited by 58 · see citing works
Characterization of the Constitutive Pig Ovary Heat Shock Chaperone Machinery and Its Response to Acute Thermal Stress or to Seasonal Variations1
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Do Molecular Chaperones Have to Be Proteins?
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Effect of LPS on Reproductive System at the Level of the Pituitary of Anestrous Ewes
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Oocyte developmental competence is reduced in sows during the seasonal infertility period
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Identification of sow-specific risk factors for late pregnancy loss during the seasonal infertility period in pigs
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Mitochondrial Dysfunction Influences Apoptosis and Autophagy in Porcine Parthenotes Developing In Vitro
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Epigenetic control of translation regulation: Alterations in histone H3 lysine 9 post‐translation modifications are correlated with the expression of the translation initiation factor 2B (Eif2b5) during thermal control establishment
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Heat Stress Alters Ovarian Insulin-Mediated Phosphatidylinositol-3 Kinase and Steroidogenic Signaling in Gilt Ovaries1
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Effects of mammalian <i>in utero</i> heat stress on adolescent body temperature
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Heat stress‐induced apoptosis in porcine in vitro fertilized and parthenogenetic preimplantation‐stage embryos
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Studies on substantially increased proteins in follicular fluid of bovine ovarian follicular cysts using 2-D PAGE and MALDI-TOF MS
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Nutritional and physiological responses of finishing pigs exposed to a permanent heat exposure during three weeks
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A differential autophagic response to hyperglycemia in the developing murine embryo
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Thermal Stress Alters Postabsorptive Metabolism During Pre- and Postnatal Development
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Heat Shock Protein 70 and Sex Steroid Receptors in the Follicular Structures of Induced Ovarian Cysts
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Genome‐wide methylation profile following prenatal and postnatal dietary omega‐3 fatty acid supplementation in pigs
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Effects of acute heat stress on skeletal muscle gene expression associated with energy metabolism in rats
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Exploring breeding opportunities for reduced thermal sensitivity of feed intake in the lactating sow1
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Heat Transfer between Animal and Environment
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In utero heat stress increases postnatal core body temperature in pigs1,2
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Presence of an aromatase inhibitor, possibly heat shock protein 90, in dominant follicles of cattle
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Expression of prostaglandin G/H synthase (PGHS) and heat shock protein-70 (HSP-70) in the corpus luteum (CL) of prostaglandin F2α-treated immature superovulated rats
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The seasonal breeding pattern of sows in seven confinement herds
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Role of PI 3‐Kinase and SH‐PTP2 in Insulin Action
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Glucocorticoids Inhibit Kisspeptin Neurons during Stress-Induced Reproductive Inhibition
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2 of the 140 references couldn’t be matched to a known paper.

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Climate Change and Livestock Production: A Literature Review
Cheng, M.-X., McCarl, B., & Fei, C. (2022) · Atmosphere · doi:10.3390/atmos13010140 · Cited by 375 · see citing works
Stress and the HPA Axis: Balancing Homeostasis and Fertility.
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“Conditions associated with increased insulin signaling (such as obesity and polycystic ovary syndrome) are also associated with reproductive dysfunction [39].”
Background
Heat stress adaptations in pigs
Mayorga, E. J., Renaudeau, D., Ramirez, B. C., Ross, J. W., & Baumgard, L. H. (2018) · Animal Frontiers · doi:10.1093/af/vfy035 · Cited by 218 · see citing works
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Effect of heat stress on growth and production performance of livestock and poultry: Mechanism to prevention
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Heat Stress-Mediated Activation of Immune–Inflammatory Pathways
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Heat stress affects fecal microbial and metabolic alterations of primiparous sows during late gestation
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Functions of manganese in reproduction
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Heat stress in pigs and broilers: role of gut dysbiosis in the impairment of the gut-liver axis and restoration of these effects by probiotics, prebiotics and synbiotics
Ringseis, R., & Eder, K. (2022) · Journal of Animal Science and Biotechnology/Journal of animal science and biotechnology · doi:10.1186/s40104-022-00783-3 · Cited by 96 · see citing works
Biology of heat stress; the nexus between intestinal hyperpermeability and swine reproduction
Mayorga, E. J., Ross, J. W., Keating, A. F., Rhoads, R. P., & Baumgard, L. H. (2020) · Theriogenology · doi:10.1016/j.theriogenology.2020.05.023 · Cited by 91 · see citing works
Self-citation
Use of Different Cooling Methods in Pig Facilities to Alleviate the Effects of Heat Stress—A Review
Godyń, D., Herbut, P., Angrecka, S., & Vieira, F. M. C. (2020) · Animals · doi:10.3390/ani10091459 · Cited by 85 · see citing works
A controlled heat stress during late gestation affects thermoregulation, productive performance, and metabolite profiles of primiparous sow
He, J., Zheng, W., Lu, M., Yang, X., Xue, Y., & Yao, W. (2019) · Journal of Thermal Biology · doi:10.1016/j.jtherbio.2019.01.011 · Cited by 62 · see citing works
Effect of Curcumin Supplement in Summer Diet on Blood Metabolites, Antioxidant Status, Immune Response, and Testicular Gene Expression in Hu Sheep
Jiang, Z., Wan, Y., Li, P., Yang, X., Cui, W., Chen, Q., Chen, J., Wang, F., & Mao, D. (2019) · Animals · doi:10.3390/ani9100720 · Cited by 62 · see citing works
The effect of recovery from heat stress on circulating bioenergetics and inflammatory biomarkers
Abuajamieh, M., Kvidera, S. K., Mayorga, E. J., Kaiser, A., Lei, S. M., Seibert, J. T., Horst, E. A., Sanz-Fernandez, M. V., Ross, J. W., Selsby, J. T., et al. (2018) · Journal of Animal Science · doi:10.1093/jas/sky345 · Cited by 52 · see citing works
Self-citation
Characterization of the acute heat stress response in gilts: III. Genome-wide association studies of thermotolerance traits in pigs
Kim, K., Seibert, J. T., Edea, Z., Graves, K. L., Kim, E.-S., Keating, A. F., Baumgard, L. H., Ross, J. W., & Rothschild, M. F. (2018) · Journal of Animal Science · doi:10.1093/jas/sky131 · Cited by 51 · see citing works
Self-citation
In utero heat stress alters postnatal phenotypes in swine
Johnson, J. S., Stewart, K. R., Safranski, T. J., Ross, J. W., & Baumgard, L. H. (2020) · Theriogenology · doi:10.1016/j.theriogenology.2020.05.013 · Cited by 49 · see citing works
Self-citation
Variability of piglet birth weights: A systematic review and meta‐analysis
Moreira, R. H. R., Perez-Palencia, J. Y., Moita, V. H. C., Caputo, L. S. S., Saraiva, A., Andretta, I., Ferreira, R. A., & de Abreu, M. L. T. (2019) · Journal of Animal Physiology and Animal Nutrition · doi:10.1111/jpn.13264 · Cited by 46 · see citing works
Impact of environmental temperature on production traits in pigs
Rauw, W. M., de Mercado, E., Gomez‐Raya, L., Cortés, L. A. G., Ciruelos, J. J., & Izquierdo, E. G. (2020) · Scientific Reports · doi:10.1038/s41598-020-58981-w · Cited by 45 · see citing works
Effects of dietary chromium propionate on growth performance, metabolism, and immune biomarkers in heat-stressed finishing pigs1
Mayorga, E. J., Kvidera, S. K., Seibert, J. T., Horst, E. A., Abuajamieh, M., Al‐Qaisi, M., Lei, S., Ross, J. W., Johnson, C. D., Kremer, B., et al. (2018) · Journal of Animal Science · doi:10.1093/jas/sky484 · Cited by 33 · see citing works
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Effect of Heat Stress and Feeding Management on Growth Performance and Physiological Responses of Finishing Pigs.
Serviento, A. M., Labussière, E., Castex, M., & Renaudeau, D. (2020) · Journal of Animal Science · doi:10.1093/jas/skaa387 · Cited by 29 · see citing works
Boron Attenuates Heat Stress–Induced Apoptosis by Inhibiting Endoplasmic Reticulum Stress in Mouse Granulosa Cells
Xiong, Y., Jin, E., Yin, Q., Che, C., & He, S. (2020) · Biological Trace Element Research · doi:10.1007/s12011-020-02180-1 · Cited by 32 · see citing works
Effects of heat stress and insulin sensitizers on pig adipose tissue
Seibert, J. T., Abuajamieh, M., Sanz-Fernandez, M. V., Johnson, J. S., Kvidera, S. K., Horst, E. A., Mayorga, E. J., Lei, S. M., Patience, J. F., Ross, J. W., et al. (2018) · Journal of Animal Science · doi:10.1093/jas/skx067 · Cited by 30 · see citing works
Self-citation
Controlled elevated temperatures during early-mid gestation cause placental insufficiency and implications for fetal growth in pregnant pigs
Zhao, W., Liu, F., Bell, A. W., Le, H. H., Cottrell, J. J., Leury, B. J., Green, M. P., & Dunshea, F. R. (2020) · Scientific Reports · doi:10.1038/s41598-020-77647-1 · Cited by 29 · see citing works
Impact of heat stress during the follicular phase on porcine ovarian steroidogenic and phosphatidylinositol-3 signaling
Dickson, M. J., Hager, C. L., Al‐Shaibi, A., Thomas, P. Q., Baumgard, L. H., Ross, J. W., & Keating, A. F. (2018) · Journal of Animal Science · doi:10.1093/jas/sky144 · Cited by 28 · see citing works
Self-citation
Genome-Wide Transcriptome and Metabolome Analyses Provide Novel Insights and Suggest a Sex-Specific Response to Heat Stress in Pigs
Srikanth, K., Park, J., Ji, S. Y., Kim, K. H., Lee, Y. K., Kumar, H., Kim, M., Baek, Y.-C., Kim, H., Jang, G.-W., et al. (2020) · Genes · doi:10.3390/genes11050540 · Cited by 28 · see citing works
Ways to reduce adverse effects of stress in pigs using nutritional factors
Bogolyubov, N. V., Chabaev, M. G., Fomichev, Y. P., Tsis, E. Y., Semenova, A., & Nekrasov, R. V. (2019) · Ukrainian Journal of Ecology · doi:10.15421/2019_70 · Cited by 26 · see citing works
Transcriptome analysis identifies genes and co-expression networks underlying heat tolerance in pigs
He, Y., Maltecca, C., Tiezzi, F., Lozada‐Soto, E. A., & Flowers, W. L. (2020) · BMC Genetics · doi:10.1186/s12863-020-00852-4 · Cited by 24 · see citing works
Differentiating between the effects of heat stress and lipopolysaccharide on the porcine ovarian heat shock protein response1
Seibert, J. T., Adur, M. K., Schultz, R. B., Thomas, P. Q., Kiefer, Z. E., Keating, A. F., Baumgard, L. H., & Ross, J. W. (2019) · Journal of Animal Science · doi:10.1093/jas/skz343 · Cited by 23 · see citing works
Self-citation
Probiotic-prebiotic therapeutic potential: A new horizon of microbial biotherapy to reduce female reproductive complications
Rani, K., Kaur, G., & Ali, S. A. (2023) · PharmaNutrition · doi:10.1016/j.phanu.2023.100342 · Cited by 24 · see citing works
Cardiac performance and heart gene network provide dynamic responses of bay scallop Argopecten irradians irradians exposure to marine heatwaves
Zhu, X., Zhang, J., Li, M., Hou, X., Liu, A., Dong, X., Wang, W., Xing, Q., Huang, X., Wang, S., et al. (2023) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2023.163594 · Cited by 22 · see citing works
Effect of heat stress on pig production and its mitigation strategies: a review
Katiyar, R., Gonmei, C., Deori, S., Singh, M., Abedin, S. N., Rautela, R., Singh, N. S., Chakravarty, H., Das, M., Choudhury, B. U., et al. (2025) · Tropical Animal Health and Production · doi:10.1007/s11250-025-04387-7 · Cited by 20 · see citing works
Modeling of Heat Stress in Sows—Part 1: Establishment of the Prediction Model for the Equivalent Temperature Index of the Sows
Cao, M., Zong, C., Wang, X., Teng, G., Zhuang, Y., & Lei, K. (2021) · Animals · doi:10.3390/ani11051472 · Cited by 19 · see citing works
Heat/Cold Stress and Methods to Mitigate Its Detrimental Impact on Pork and Poultry Meat: A Review
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208 Molecular mechanisms through which heat stress compromises reproduction in pigs
Ross, J. W., Hale, B. J., Seibert, J. T., Romoser, M. R., Adur, M. K., Keating, A. F., & Baumgard, L. H. (2019) · Journal of Animal Science · doi:10.1093/jas/skz122.212
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Effects of heat stress on physiological, endocrine, and reproductive functions in swine: review
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Authors: Ross, J. W., Hale, B. J., Seibert, J. T., Romoser, M. R., Adur, M. K., Keating, A. F., & Baumgard, L. H.
Affiliations: Iowa State University (US)
Corresponding author: Ross, Jason W.
ORCID: Ross, Jason W.
Hale, Benjamin J.
Seibert, Jacob T.
Keating, Aileen F.
Baumgard, Lance H.
Venue: Molecular Reproduction and Development
Publisher: Wiley
Published: 2017-09
Volume: 84
Issue: 9
Pages: 934-945
ISSN: 1040-452X (ISSN-L)
1098-2795
DOI: 10.1002/mrd.22859
OpenAlex: W2725359221
Cited by: 128
References: 140
Citations by year: 2026: 11 · 2025: 20 · 2024: 16 · 2023: 12 · 2022: 18 · 2021: 12 · 2020: 19 · 2019: 8 · 2018: 9 · 2017: 3
FWCI: 1.30
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: onlinelibrary.wiley.com/termsAndConditions#vor (vor, 17 d)
Locations: Molecular Reproduction and Development (publishedVersion)
PubMed (publishedVersion)
Iowa State University Digital Repository (Iowa State University) (submittedVersion)
Funders: National Pork Board
Iowa Pork Producers Association
National Institute of Food and Agriculture (2011‐67003‐30007)
Topics: Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Effects of Environmental Stressors on Livestock
Life Sciences › Agricultural and Biological Sciences › Agronomy and Crop Science › Reproductive Physiology in Livestock
Health Sciences › Medicine › Reproductive Medicine › Sperm and Testicular Function
Keywords: heat stress, swine reproduction, seasonal infertility, puberty onset, farrowing rate, hypothalamic-pituitary-gonadal axis, hypothalamic-pituitary-adrenal axis, epigenetic programming, extracellular vesicles, inter-organ communication, thermoregulation, heat stress mitigation
MeSH terms: Animals, Female, Hypothalamo-Hypophyseal System, Infertility, Male, Swine, Swine Diseases, Heat Stress Disorders

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Physiological mechanisms through which heat stress compromises reproduction in pigs

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