Robert P Rhoads
Virginia Tech, Animal and Poultry Science, Faculty Member
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Heat‐related complications continue to be a major health concern for humans and animals and lead to potentially life‐threatening conditions ranging from heat exhaustion, heat stroke and even death. Heat stress have been shown to alter... more
Heat‐related complications continue to be a major health concern for humans and animals and lead to potentially life‐threatening conditions ranging from heat exhaustion, heat stroke and even death. Heat stress have been shown to alter metabolic and energetic parameters in mammals and may alter glucose metabolism and insulin sensitivity. Therefore, the purpose of this investigation was to determine the extent to which short‐term HS altered markers of insulin signaling in oxidative skeletal muscle. To address this, crossbred gilts (n=8/group) were assigned to thermoneutral (TN; 24° C), HS (37° C), or pair‐fed to HS and kept under TN conditions (PFTN) groups for 12 hours. Following treatment, animals were euthanized and the semitendinosus red (STR) was recovered. HS‐induced changes were not caused by reduced feed intake as TN and PFTN were similar for nearly all measures. Twelve hours of HS increased insulin receptor protein abundance by 54% (p<0.05) and phosphorylated insulin receptor substrate (pIRS1S307) by 56% (p<0.05) compared to TN. Phosphorylation of IRS1 at this site is a negative regulator of insulin signaling. Relative protein abundance and phosphorylation of phosphoinositide 3‐kinase (PI3K) and 3‐phosphoinositide dependent protein kinase‐1 (PDK1) were similar between groups. Phosphorylation of protein kinase B (pAKTs473) was decreased by 53% (p<0.05) in HS compared to TN, which indicates that insulin signaling was suppressed through pIRS1. Conversely, HS increased phosphorylation of protein kinase C (PKC)λ/ζ and pPKCδ protein abundance by 128% and 205%, respectively, compared to TN which are known to stimulate pIRS1S307. Sarcolemma glucose transporter‐4 (Glut4) was decreased by 47% (p<0.05) in HS group compared to TN suggesting reduced glucose uptake. These data suggest that HS induces insulin sensititvity by disturbing insulin signaling via an AKT‐mediated pathway.Support or Funding InformationThis work is supported by USDA grants 2014‐67015‐21627 and 2011‐67003‐30007
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Research Interests: Endocrinology, Chemistry, Animal Science, Free Radicals, Oxidative Stress, and 15 moreAutophagy, Apoptosis, Medicine, Signal Transduction, Biological Sciences, Antioxidants, Internal Medicine, Female, Animals, Catalase, Heat stress, Oxidative phosphorylation, Heat Shock Proteins, Malondialdehyde, and Intracellular
Research Interests: Endocrinology, Chemistry, Animal Science, Free Radicals, Oxidative Stress, and 15 moreAutophagy, Apoptosis, Medicine, Signal Transduction, Biological Sciences, Antioxidants, Internal Medicine, Female, Animals, Catalase, Superoxide Dismutase, Skeletal Muscle, Swine, Heat Shock Proteins, and Malondialdehyde
Heat stress continues to undermine efficient meat production and meat quality. It also jeopardizes human and animal health and wellbeing, regionalizes animal production, and threatens food security. Environmental models predict more... more
Heat stress continues to undermine efficient meat production and meat quality. It also jeopardizes human and animal health and wellbeing, regionalizes animal production, and threatens food security. Environmental models predict more frequent and severe heat waves, even in areas previously considered temperate indicating this problem will continue to have a progressively expanding, deleterious impact on agricultural productivity. Despite the broad, negative impact of heat stress little is known about underlying mechanisms leading to phenotypic outcomes. Because of its mass and energetic demands, skeletal muscle contributes greatly to regulation of systemic metabolism. We have discovered heat stress causes robust but transient oxidative stress and activation of apoptotic signaling in skeletal muscle in as little as two hours. Interestingly, these declined linearly through six hours concomitant with markers of increased autophagy and mitophagy, which would facilitate the removal of damaged mitochondria. Continued heating through 24 h causes a resumption of oxidative stress and autophagic dysfunction with an accumulation of autophagosomes and mitochondria. As mitochondrial injury and autophagic dysregulation appear to be key mediators of hyperthermic muscle dysfunction we propose a model that posits progressive mitochondrial injury leads to production of free radicals that overwhelms antioxidant systems and impairs autophagy facilitating accumulation of damaged, pro-oxidant mitochondria. Ultimately, these aforementioned changes may reduce efficient protein accretion. Our current work is focused on stimulating autophagy and protecting mitochondria during heat stress in an effort to maintain efficient muscle growth.
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We have previously reported that 24 hours of heat stress (HS) induced free radical injury in oxidative skeletal muscle. In addition, we found widespread aberrant intracellular signaling following 12h of HS. The aim of this investigation... more
We have previously reported that 24 hours of heat stress (HS) induced free radical injury in oxidative skeletal muscle. In addition, we found widespread aberrant intracellular signaling following 12h of HS. The aim of this investigation was to extend our knowledge regarding the early chronology of HS‐mediated intracellular signalling in oxidative skeletal muscle. We hypothesized that 2, 4, and 6 hours of HS would result in increased autophagy and decreased mitochondrial content in oxidative skeletal muscle compared to muscle maintained under thermoneutral (TN) conditions. To address this hypothesis, pigs were assigned to four groups (n=8/group) and housed under TN conditions (21°C) or exposed to HS (37°C) for 2, 4, or 6 hours. Next, animals were euthanized and the semitendinosus red (STR) was collected and analyzed. Compared to TN, relative protein abundance of autophagy initiators phosphoinositide 3‐kinase Class III and Beclin‐1 were increased by 57% and 56%, respectively (p<0.05), following 6 hours of HS. At the same time point, relative abundance of the pre‐autophagosomal structure stabilizer, autophagy‐related protein 16‐1 (ATG16), was increased 59% (p<0.05). Microtubule‐associated protein A/B light chain 3 (LC3)‐I was similar between all four groups but the autophagosome formation marker LC3‐II was increased by 94% (p<0.05) following 6 hours of HS compared to TN. This resulted in a 2‐fold increase in the LC3II/I ratio (p<0.05), which is indicative of increased autophagic flux, though sequstome‐1 (p62) protein abundance was similar between groups. In addition, the mitophagy marker, BCL2/adenovirus E1B protein‐interacting protein 3‐like (BNIP3), was increased by 41% (p<0.05) following 6 hours of HS compared to TN. Relative protein abundance of TCA enzymes, electron transport chain components, and mitochondrial markers was similar between groups. These data demonstrate that short‐term HS induced autophagy/mitophagy. Together with our previous work we also suggest thatbetween 6 and 12 hours of HS the intracellular environment of oxidative skeletal muscle switches from one that promotes autophagy to one that inhibits it.Support or Funding InformationThis work supported by USDA grants 2014‐67015‐21627 and 2011‐67003‐30007.
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Prolonged exposure to high temperatures can result in heat stress (HS), which is characterized by morbidities and mortality in humans and animals and appears to cause organ‐specific injury and dysfunction. We have previously found... more
Prolonged exposure to high temperatures can result in heat stress (HS), which is characterized by morbidities and mortality in humans and animals and appears to cause organ‐specific injury and dysfunction. We have previously found increased free radical injury in skeletal muscle following 24 hours of HS. The purpose of this investigation was to determine the extent to which short‐term HS caused muscle dysfunction in oxidative skeletal muscle. We hypothesized that in oxidative muscle 12 hours of HS would lead to free radical injury, apoptosis, autophagy, and decreased mitochondrial content compared to muscle from thermoneutral (TN) animals. To address this hypothesis, crossbred gilts (n=8/group) were assigned to three groups: TN (24° C), HS (37° C), or pair‐fed to heat stress (PFTN; 24° C) for 12 hours. Following treatment, animals were euthanized and the semitendinosus red (STR) was recovered. TN and PFTN were similar for nearly all measures indicating changes caused by HS were not due to reduced feed intake but due to the hyperthermic environment. The relative abundance of malondialdehyde modified proteins was increased by 36% in HS (p<0.05) compared to TN, which was matched by an inadequate antioxidant response including a 48% and 170% increase in superoxide dismutase (SOD) I and II relative protein abundance, respectively, and a 26% increase in total SOD activity but a 40% reduction in catalase activity in HS compared to TN. Further, HS caused a 103% increase in caspase 3 activation and tended to increase BCL2‐Associated X Protein by 40% (p<0.06) and apoptotic protease activating factor 1 by 66% (p<0.06) indicating increased apoptotic signaling. Despite increased initiation, autophagy appeared to be inhibited by HS as the microtubule‐associated protein A/B‐light chain 3 II/I ratio was decreased by 53% and sequestosome‐1(p62) protein abundance was increased by 40% in HS compared to TN. Markers of mitochondrial content cytochrome c, cytochrome c oxidase IV, voltage dependent anion channel, pyruvate dehydrogenase and prohibitins 1 were increased in HS compared to TN. Increased mitochondrial content is likely reflective of a combination of increased accumulation of damaged mitochondria that fail to be cleared via autophagy and mitochondrial biogenesis. We postulate that in oxidative skeletal muscle HS‐mediated mitochondrial dysfunction is allowed to persist due to a failure of autophagy to clear damaged mitochondria, which results in increased oxidative stress and apoptotic signaling. These data demonstrate widespread aberrant intracellular signaling caused by HS that implicate impaired autophagy as a key feature in HS‐mediated muscle dysfunctionSupport or Funding InformationThis work supported by USDA grants 2014‐67015‐21627 and 2011‐67003‐30007.
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Heat stress (HS) poses a major threat to human health and agricultural production. Oxidative stress and mitochondrial dysfunction appear to play key roles in muscle injury caused by HS. We hypothesized that mitoquinol (MitoQ), would... more
Heat stress (HS) poses a major threat to human health and agricultural production. Oxidative stress and mitochondrial dysfunction appear to play key roles in muscle injury caused by HS. We hypothesized that mitoquinol (MitoQ), would alleviate oxidative stress and cellular dysfunction in skeletal muscle during HS. To address this, crossbred barrows (male pigs) were treated with placebo or MitoQ (40 mg/d) and were then exposed to thermoneutral (TN; 20 °C) or HS (35 °C) conditions for 24 h. Pigs were euthanized following the environmental challenge and the red portion of the semitendinosus (STR) was collected for analysis. Unexpectedly, malondialdehyde concentration, an oxidative stress marker, was similar between environmental and supplement treatments. Heat stress decreased LC3A/B-I (p < 0.05) and increased the ratio of LC3A/B-II/I (p < 0.05), while p62 was similar among groups suggesting increased degradation of autophagosomes during HS. These outcomes were in disagreement with our previous results in muscle from gilts (female pigs). To probe the impact of biological sex on HS-mediated injury in skeletal muscle, we compared STR from these barrows to archived STR from gilts subjected to a similar environmental intervention. We confirmed our previous findings of HS-mediated dysfunction in muscle from gilts but not barrows. These data also raise the possibility that muscle from gilts is more susceptible to environment-induced hyperthermia than muscle from barrows.
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Hyperthermic pigs differ metabolically, including altered insulin profiles, reduced lipolysis, and compromised intestinal integrity, leading to lower lean tissue and elevated adipose tissue mass. T...
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There is a variety of conditions in a farm animal's life when nutrient utilisation is prioritised towards agriculturally unproductive purposes. Two well-known examples that markedly reduce production efficiency are heat stress and... more
There is a variety of conditions in a farm animal's life when nutrient utilisation is prioritised towards agriculturally unproductive purposes. Two well-known examples that markedly reduce production efficiency are heat stress and ketosis. Decreased feed intake, experienced in both cases, is unable to fully account for decreased productivity. In addition, both ketosis and heat stress are characterised by a negative energy balance, body weight loss, inflammation and hepatic steatosis.
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Heat stress (HS) alters animal metabolism causing reduced performance (muscle growth) while increasing the incidence of disease and mortality. HS is particularly detrimental in the swine industry where the global economic burden of heat... more
Heat stress (HS) alters animal metabolism causing reduced performance (muscle growth) while increasing the incidence of disease and mortality. HS is particularly detrimental in the swine industry where the global economic burden of heat stress is in the billions of dollars annually. Excess environmental heat promotes a HS response increasing the expression of heat shock factors and heat shock proteins which coordinate a shift in metabolic substrate preference. The net result of these changes is a metabolic phenotype with limited lipid oxidation that relies on aerobic and anaerobic glycolysis as a predominant source of energy production. This study was designed to evaluate the effect of HS on substrate utilization and overall animal metabolic rate in growing pigs. Crossbred barrows (15.2±2.4 kg) were exposed to 5 days of TN (thermal neutral, 24 C°) or HS ( 35 C°) (n=8 per treatment), after a 5‐day acclimation period (24 C°). Pigs were fed ad libitum and monitored regularly for respir...
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Background Dietary calcium and phosphorus are required for bone and muscle development. Deficiencies of these macrominerals reduce bone mineral and muscle accretion potentially via alterations of mesenchymal stem cell (MSC) and satellite... more
Background Dietary calcium and phosphorus are required for bone and muscle development. Deficiencies of these macrominerals reduce bone mineral and muscle accretion potentially via alterations of mesenchymal stem cell (MSC) and satellite cell (SC) activities. Objectives With increasing interest in the role of early-life events on lifetime health outcomes, we aimed to elucidate the impact of dietary calcium and phosphorus, from deficiency through excess, on MSC and SC characteristics during neonatal development. Methods Neonatal pigs [30 females, 1-d-old, 1.46 ± 0.04 kg body weight (BW)] were fed milk replacers for 16 d that were isonitrogenous and isocaloric with a consistent ratio of calcium to phosphorus, but either 25% deficient (calcium: 0.78%; phosphorus: 0.60%; CaPD), adequate (calcium: 1.08%; phosphorus: 0.84%; CaPA), or 25% in excess (calcium: 1.38%; phosphorus: 1.08%; CaPE) of calcium and phosphorus requirements based on sow-milk composition and extrapolation from NRC requi...
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This information was presented the 2015 Herd Health and Nutrition Conference, organized by the PRO-DAIRY Program in the College of Agriculture and Life Sciences at Cornell University. Softcover copies of the entire conference proceedings... more
This information was presented the 2015 Herd Health and Nutrition Conference, organized by the PRO-DAIRY Program in the College of Agriculture and Life Sciences at Cornell University. Softcover copies of the entire conference proceedings may be purchased at http:// ansci.cornell.edu/dm/ or by calling (607) 255-4478.
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Heat stress negatively influences the global pork industry and undermines genetic, nutritional, management and pharmaceutical advances in management, feed and reproductive efficiency. Specifically, heat stress-induced economic losses... more
Heat stress negatively influences the global pork industry and undermines genetic, nutritional, management and pharmaceutical advances in management, feed and reproductive efficiency. Specifically, heat stress-induced economic losses result from poor sow performance, reduced and inconsistent growth, decreased carcass quality, mortality, morbidity, and processing issues caused by less rigid adipose tissue (also known as flimsy fat). When environmental conditions exceed the pig’s thermal neutral zone, nutrients are diverted from product synthesis (meat, fetus, milk) to body temperature maintenance thereby compromising efficiency. Unfortunately, genetic selection for both increased litter size and leaner phenotypes decreases pigs’ tolerance to heat, as enhanced fetal development and protein accretion results in increased basal heat production. Additionally, research has demonstrated that in utero heat stress negatively and permanently alters post-natal body temperature and body composi...
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Substantial economic losses in animal agriculture result from animals experiencing heat stress (HS). Pigs are especially susceptible to HS, resulting in reductions in growth, altered body composition, and compromised substrate metabolism.... more
Substantial economic losses in animal agriculture result from animals experiencing heat stress (HS). Pigs are especially susceptible to HS, resulting in reductions in growth, altered body composition, and compromised substrate metabolism. In this study, an artificial high-intensity sweetener and capsaicin (CAPS-SUC; Pancosma, Switzerland) were supplemented in combination to mitigate the adverse effects of HS on pig performance. Forty cross-bred barrows (16.2 ± 6 kg) were assigned to one of five treatments: thermal neutral controls (TN) (22 ± 1.2 °C; 38%–73% relative humidity) with ad libitum feed, HS conditions with ad libitum feed with (HS+) or without (HS−) supplementation, and pair-fed to HS with (PF+) or without supplementation (PF−). Pigs in heat-stressed treatments were exposed to a cyclical environmental temperature of 12 h at 35 ± 1.2 °C with 27%–45% relative humidity and 12 h at 30 ± 1.1 °C with 24%–35% relative humidity for 21 d. Supplementation (0.1 g/kg feed) began 7 d b...
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Adverse weather conditions are a large constraint to maximizing farm animal productivity. Heat stress, in particular, compromises almost every metric of animal agriculture profitability. Suboptimal production during HS was traditionally... more
Adverse weather conditions are a large constraint to maximizing farm animal productivity. Heat stress, in particular, compromises almost every metric of animal agriculture profitability. Suboptimal production during HS was traditionally thought to result from hypophagia. However, independent of inadequate nutrient consumption, HS affects a plethora of endocrine, physiological, metabolic, circulatory, and immunological variables. Mounting evidence suggest that direct effects of HS originating at the gastrointestinal tract precede the observed effects on the aforementioned systems. Heat stress compromises intestinal barrier integrity causing the appearance of luminal contents, e.g. endotoxin, in circulation. Endotoxin stimulates both a classic immune response with local and systemic inflammatory reactions as well as directly acting on numerous organs and tissues. Once activated, leukocytes switch from oxidative phosphorylation to aerobic glycolysis where the glucose requirement of an ...
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Heat stress can negatively impact pig health and performance but the effects of heat stress on skeletal muscle mitochondrial function are largely unknown. We hypothesized that mitochondrial function and capacity would be impaired in heat... more
Heat stress can negatively impact pig health and performance but the effects of heat stress on skeletal muscle mitochondrial function are largely unknown. We hypothesized that mitochondrial function and capacity would be impaired in heat stressed (HS) compared to thermoneutral (TN) pigs but mitochondrially-targeted coenzyme Q (MitoQ) supplementation would rescue the impairment. Oxidative portions of the semitendinosus muscle were evaluated from TN and HS gilts receiving no supplementation (CON) or MitoQ for 2 d prior to and during the 24h environmental heat treatment (n = 8 per group). Mitochondrial oxidative phosphorylation (P) and electron transfer (E) capacities were determined via high resolution respirometry and mitochondrial volume density and function were quantified by citrate synthase (CS) and cytochrome c oxidase activities, respectively. Data were analyzed using linear models in SAS v9.4 with fixed effects of heat, MitoQ treatment (trt), and heat×trt interaction. There we...
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Heat stress (HS) occurs when internal body temperatures are elevated above a thermoneutral zone in response to extreme environmental temperatures. In the U.S. dairy industry, HS results in economic loss due to decreased feed intake, milk... more
Heat stress (HS) occurs when internal body temperatures are elevated above a thermoneutral zone in response to extreme environmental temperatures. In the U.S. dairy industry, HS results in economic loss due to decreased feed intake, milk quality, and milk yield. Previous work has demonstrated increased plasma urea nitrogen in heat stressed dairy cattle which is thought to originate from increased skeletal muscle proteolysis, however this has not been empirically established. The objective of this investigation was to determine the extent to which HS promotes proteolysis in skeletal muscle of dairy cattle. We hypothesized HS would increase activation of the calpain and proteasome systems in skeletal muscle. To test this hypothesis, following a 3-d acclimation period in individual box stalls, all lactating dairy cows were held under thermoneutral (TN) conditions for 4-d for collection of baseline measures and then exposed to TN or HS conditions for 7-d followed by a biopsy of semitend...
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ABSTRACTBackgroundLow-birth-weight (LBWT) neonates grow at a slower rate than their normal-birth-weight (NBWT) counterparts and may develop hypoglycemia postnatally.ObjectiveWe investigated whether dietary lipid supplementation would... more
ABSTRACTBackgroundLow-birth-weight (LBWT) neonates grow at a slower rate than their normal-birth-weight (NBWT) counterparts and may develop hypoglycemia postnatally.ObjectiveWe investigated whether dietary lipid supplementation would enhance growth and improve glucose production in LBWT neonatal pigs.MethodsTwelve 3-d-old NBWT (1.606 kg) crossbred pigs were matched to 12 LBWT (1.260 kg) same-sex littermates. At 6 d of age, 6 pigs in each group were fed a low-energy (LE) or a high-energy (HE) isonitrogenous formula containing 5.2% and 7.3% fat, respectively. Body composition was assessed using dual-energy X-ray absorptiometry; plasma glucose and glycerol kinetics were assessed using stable isotope tracers. After killing, weights of skeletal muscles and visceral organs were measured. Data were analyzed by ANOVA for a 2 × 2 factorial design; temporal effects were investigated using repeated-measures analysis.ResultsLipid supplementation did not affect body weight of LBWT or NBWT pigs. ...
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Muscle hypertrophy is limited in low-birth-weight (LBWT) neonates, suggesting a reduction in protein synthesis and increased protein degradation. Sixteen pairs of 1-d old normal-birth-weight (NBWT) and LBWT littermates (n = 16) were... more
Muscle hypertrophy is limited in low-birth-weight (LBWT) neonates, suggesting a reduction in protein synthesis and increased protein degradation. Sixteen pairs of 1-d old normal-birth-weight (NBWT) and LBWT littermates (n = 16) were euthanized and the longissimus dorsi (LD) was sampled for protein abundance and kinase phosphorylation profiles measures. Eukaryotic initiation factor (eIF) 4E and eIF4G abundance, and assembly of the active eIF4E-eIF4G complex was less for LBWT than for NBWT pig muscles. Similarly, eIF3f abundance was reduced in muscle of LBWT compared with NBWT pig and was associated with diminished ribosomal protein S6 kinase 1 (S6K1) phosphorylation. This decrease was linked to a lower phosphorylation of programmed cell death protein 4 (PDCD4) in LBWT pig muscle. By contrast, PDCD4 abundance was greater in muscle of LBWT than NBWT group, suggesting lower release and availability of eIF4A from PDCD4-eIF4A complex. Moreover, protein abundance of eIF4A was lower in LBWT...
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During the transition from pregnancy to lactation, dairy cows experience a 70% reduction in plasma IGF-I. This reduction has been attributed to decreased hepatic IGF-I production. IGF-I circulates predominantly in multi-protein complexes... more
During the transition from pregnancy to lactation, dairy cows experience a 70% reduction in plasma IGF-I. This reduction has been attributed to decreased hepatic IGF-I production. IGF-I circulates predominantly in multi-protein complexes consisting of one molecule each of IGF-I, IGF binding protein-3 and the acid labile subunit (ALS). Recent studies in the mouse have shown that absence of ALS results in accelerated turnover and severely depressed concentration of plasma IGF-I. These observations suggest that reduced plasma ALS could be a second factor contributing to the fall of plasma IGF-I in peri-parturient cows. This possibility has not been studied due to the lack of bovine ALS reagents. To address this, we isolated the bovine ALS cDNA and used its sequence to develop a ribonuclease protection assay (RPA) and a bovine ALS antiserum. Using the RPA, ALS mRNA abundance was approximately fivefold higher in liver than in lung, small intestine, adipose tissue, kidney and heart, but w...
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Study objectives were to determine the effects of rapamycin (Rapa) on biomarkers of metabolism and inflammation during acute heat stress (HS) in growing pigs. Crossbred barrows (n = 32; 63.5 ± 7.2 kg body weight [BW]) were blocked by... more
Study objectives were to determine the effects of rapamycin (Rapa) on biomarkers of metabolism and inflammation during acute heat stress (HS) in growing pigs. Crossbred barrows (n = 32; 63.5 ± 7.2 kg body weight [BW]) were blocked by initial BW and randomly assigned to 1 of 4 environmental-therapeutic treatments: 1) thermoneutral (TN) control (n = 8; TNCon), 2) TN and Rapa (n = 8; TNRapa), 3) HS control (n = 8; HSCon), or 4) HS and Rapa (n = 8; HSRapa). Following 6 d of acclimation to individual pens, pigs were enrolled in two experimental periods (P). During P1 (10 d), pigs were fed ad libitum and housed in TN conditions (21.3 ± 0.2°C). During P2 (24 h), HSCon and HSRapa pigs were exposed to constant HS (35.5 ± 0.4°C), while TNCon and TNRapa pigs remained in TN conditions. Rapamycin (0.15 mg/kg BW) was orally administered twice daily (0700 and 1800 hours) during both P1 and P2. HS increased rectal temperature and respiration rate compared to TN treatments (1.3°C and 87 breaths/min,...
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Heat stress is a health and economic issue in every dairy-producing area in North America. The economic impact of heat stress on American animal agriculture is almost $2 billion annually
Isolation of the cDNA encoding the acid labile subunit (ALS) of the 150 kDa IGF-binding protein complex in cattle and ALS regulation