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. 2020 Feb 5;98(3):skaa041. doi: 10.1093/jas/skaa041

Effects of feed removal on thermoregulation and intestinal morphology in pigs recovering from acute hyperthermia

Kouassi R Kpodo 1,2, Alan W Duttlinger 1,2, Jacob M Maskal 1,2, Jay S Johnson 2,✉
PMCID: PMC7205397  PMID: 32020198

Abstract

Feed consumption increases body temperature and may delay a return to euthermia and exacerbate intestinal injury following acute hyperthermia recovery in pigs. Therefore, the study objective was to evaluate the effects of feed removal on body temperature and intestinal morphology in pigs exposed to acute hyperthermia and then rapidly cooled. Twenty-four gilts (78.53 ± 5.46 kg) were exposed to thermoneutral (TN; n = 12 pigs; 21.21 ± 0.31 °C; 61.88 ± 6.93% RH) conditions for 6 h, or heat stress (HS; 38.51 ± 0.60 °C; 36.38 ± 3.40% RH) conditions for 3 h followed by a 3-h recovery period of rapid cooling (HSC;n = 12 pigs; TN conditions and cold water dousing). Within each recovery treatment, one-half of the pigs were provided feed ad libitum (AF; n = 6 pigs per recovery treatment) and one-half of the pigs were not provided feed (NF; n = 6 pigs per recovery treatment). Gastrointestinal (TGI), vaginal (TV), and skin (TSK) temperatures and respiration rate (RR) were recorded every 15 min. Pigs were video-recorded to assess feeding and drinking attempts. Immediately following the 6-h thermal stress period, pigs were euthanized, and intestinal samples were collected to assess morphology. During the HS period, Tv, TGI, TSK, and RR were increased (P < 0.01; 1.63, 2.05, 8.32 °C, and 88 breaths per min, respectively) in HSC vs. TN pigs, regardless of feeding treatment. Gastrointestinal temperature was greater (P = 0.03; 0.97 °C) in HSC + AF vs. HSC + NF pigs from 45 to 180 min of the recovery period. During the recovery period, feeding attempts were greater (P = 0.02; 195.38%) in AF vs. NF pigs. No drinking attempt differences were detected with any comparison (P > 0.05). A decrease (P < 0.01) in jejunum and ileum villus height (24.72% and 26.11%, respectively) and villus height-to-crypt depth ratio (24.03% and 25.29%, respectively) was observed in HSC vs. TN pigs, regardless of feeding treatment. Ileum goblet cells were reduced (P = 0.01; 37.87%) in HSC vs. TN pigs, regardless of feeding treatment. In summary, TGI decreased more rapidly following acute hyperthermia when the feed was removed, and this may have implications toward using feed removal as a strategy to promote acute hyperthermia recovery in pigs.

Keywords: body temperature, cooling, hyperthermia, intestinal morphology, pigs, recovery

Introduction

Heat stress (HS) represents a growing challenge for livestock health and productivity. Pigs are particularly affected by HS due to limited evaporative heat loss capacity resulting from nonfunctional sweat glands (Turnpenny et al., 2000), which is compounded by a lack of wallowing access in commercial facilities. Furthermore, HS susceptibility is exacerbated in heavier pigs (e.g., market weight pigs, sows, and boars) due to a low surface area-to-mass ratio and greater subcutaneous fat depth that can limit heat dissipation capacity (Renaudeau et al., 2012), and in lactating sows due to increased metabolic heat production (Cabezón et al., 2017; Johnson et al., 2019). As a result, HS can reduce production efficiency and product quality for the swine industry and reduce swine welfare (as reviewed by Johnson, 2018). Although management strategies (i.e., cooling pads, floor cooling, evaporative cooling) can be effective in reducing the negative impacts of HS on productivity and welfare (Renaudeau et al., 2012; Parois et al., 2018), morbidity and mortality may be increased in the case of acute hyperthermia. Therefore, it is necessary to develop mitigation strategies to combat acute hyperthermia and promote recovery in pigs.

Several recent studies have evaluated the effects of cooling methods on acute hyperthermia recovery in swine (Johnson et al., 2016a, 2016b; Sapkota et al., 2016; Kpodo et al., 2020). However, while some reports have determined that rapid cooling (e.g., return to thermoneutral environment and dousing with cold water) can be an effective method of quickly returning pigs to euthermia and preventing intestinal damage (Kpodo et al., 2020), others have shown that rapid cooling prevents the return of body temperature to euthermia, exacerbates intestinal damage, and increases the whole-body inflammatory response (Johnson et al., 2016a, 2016b; Sapkota et al., 2016). While reasons for these discrepancies are currently unknown, it may be due to study design differences and the effects of feed access (i.e., rapid cooling is only effective in studies where feed was withdrawn) as previously suggested (Kpodo et al., 2020). Therefore, the study objective was to determine the effects of feed removal on thermoregulation and intestinal morphology in pigs that were rapidly cooled following acute hyperthermia. We hypothesized that feed removal during acute hyperthermia and rapid cooling would hasten the return of body temperature to euthermia and reduce morphological indicators of intestinal damage in pigs relative to those that had ad libitum feed access during acute hyperthermia and rapid cooling.

Materials and Methods

Animals and experimental design

All animal procedures were approved by the Purdue University Animal Care and Use Committee (no. 1802001689). Animal care and use standards were based on the Guide for the Care and Use of Agricultural Animals in Research and Teaching (Federation of Animal Science Societies, 2010). The study was conducted in May 2018 at the Purdue University Swine Farm. All pigs selected for the study were housed under thermoneutral (TN) conditions as defined by the Guide for the Care and Use of Agricultural Animals in Research and Teaching (Federation of Animal Science Societies, 2010) prior to the start of the experiment. Twenty-four crossbred gilts [Duroc × (Landrace × Yorkshire); n = 12 per repetition; 78.53 ± 5.46 kg initial body weight] were moved into an environmentally controlled room at the Purdue University swine farm and housed under TN conditions as defined by the Guide for the Care and Use of Agricultural Animals in Research and Teaching (Federation of Animal Science Societies, 2010) one day prior to the thermal challenge. At 1500 hours on the same day, a calibrated Thermochron temperature recorder (iButton model 1921H, calibrated accuracy ± 0.10 °C; resolution = 0.50 °C; Dallas Semi-conductor, Maxim, Irving, TX) attached to a blank controlled internal drug-releasing device (Eazi-Breed; Zoetis, New York, NY) was inserted intravaginally into each pig to record vaginal temperature (TV) as previously described by Johnson and Shade (2017). In addition, each pig was administered a CorTemp temperature sensor (model HT150002, manufacturer calibrated accuracy ± 0.10 °C; resolution = 0.01 °C; HQ, Inc, Palmetto, FL) to monitor gastrointestinal temperature (TGI). The temperature sensor was expected to be located between the duodenum and the jejunum at the time of the experiment as previously described (Johnson et al., 2016b).

The experiment was conducted for 6 h, equally divided into HS and recovery periods (Figure 1). On the day following the TV and TGI temperature sensor administration, pigs were housed in individual pens (1.22 × 2.01 m) and subjected to either TN conditions (n = 6 pigs per repetition; 21.21 ± 0.31 °C; 61.88 ± 6.93% RH) for 6 h (Figure 1), or moved into a pre-heated environmental room at the Purdue University swine farm and exposed to a constant elevated temperature for 3 h (HS period; 38.51 ± 0.60 °C; 36.38 ± 3.40% RH), followed by a 3-h cooling (recovery period) in which TA was rapidly reduced to TN conditions (25.10 ± 3.71 °C; 58.4% RH; Figure 1) and 37.9 liters of cold water (4.0 °C) were poured over each pig’s back every 30 min for 1.5 h (HSC;n = 6 pigs per repetition). The water was poured over the back of each pig between the shoulder blades and moving down to the rump and this process took approximately 10 s. Each room was equipped with two data loggers (HOBO, data logger temp/RH; accuracy ± 0.20 °C; resolution = 0.01 °C; Onset, Bourne, MA) to record ambient temperature (TA) and RH in 15-min intervals. Within each recovery treatment, although feeders were present in all pens, one-half of the pigs had ad libitum access to feed (AF; n = 3 pigs per recovery treatment per repetition) and one-half of the pigs were not provided feed (NF; feeders present in pens but empty; n = 3 pigs per recovery treatment per repetition), but all pigs had ad libitum water access. Pigs with feed access were fed a standard corn and soybean meal diet, which was formulated to meet or exceed the requirements for grow-finish pigs (NRC, 2012).

Figure 1.

Figure 1.

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Ambient temperature by time during the heat stress and recovery periods.

Body temperature and respiration rate

During the experiment, TGI, TV, skin temperature (TSK), and respiration rate (RR) were measured for all pigs in 15-min intervals. Gastrointestinal temperature was measured through the CorTemp temperature sensors, and TV was recorded by the pre-programmed iButtons of the vaginal implants. Skin temperature was measured by taking a broadside photo of each pig using an infrared camera (FLIR Model T440, accuracy ± 0.10 °C; resolution = 0.01 °C; emissivity = 0.95; FLIR Systems Inc., USA), and photos were analyzed with FLIR Tools Software (Version 5.13; Wilsonville, OR) by one individual blind to the treatments as previously described (Kpodo et al., 2019). Briefly, TSK was determined by drawing a circle with the FLIR Tools Software on the trunk area (all skin caudal to the neck and dorsal to the elbow and stifle), and the mean, maximum, and minimum temperatures were recorded. RR (breaths per min; bpm) was determined by counting flank movements for 15 s and then multiplying by 4, through visual observation by the same individual.

Consumption attempt recording and analyses

Pigs were video-recorded during the experiment using ceiling-mounted cameras (Panasonic WV-CP254H, Matsushita Electric Industrial Co. Ltd.., Osaka, Japan). Each camera was oriented to capture two pens (one AF and one NF pig). The video data were analyzed in Observer XT 11.5 (Noldus; The Netherlands) using a continuous sampling technique, and consumption attempts (feeding attempts [head in feeder] and drinking attempts [snout in contact with nipple drinker]) were quantified to determine the duration per hour. A percentage of time spent performing the consumption attempt on a per hour basis was calculated for individual pigs and used in the analyses. Consumption attempts were analyzed by two trained individuals who were blind to the treatments. Interobserver variability for consumption attempt duration was determined by having each observer analyze 1 h of video for each treatment combination and then their observations were compared to ensure they maintained an agreement of 90% or greater.

Histology

At the end of the recovery period, all pigs were euthanized, and intestinal samples were collected. Proximal jejunal (2.5 m posterior to the stomach) and ileal (1 m anterior to the ileocecal junction) sections were flushed with phosphate buffer solution and stored in 10% formalin. Tissues were later submitted to the Purdue University Histology and Phenotyping Laboratory for sectioning (5-µm thickness, two sections per slide) and staining in Alcian blue and Giemsa. Three images per section (six images per pig) were taken using a Q-capture Pro 6.0 software (Qimaging, Survey, British Columbia, Canada). Villus height and crypt depth were measured, and goblet cells were counted by a trained individual using ImageJ 1.52b software (National Institute of Health; Bethesda, MD). Mean villus height, crypt depth, villus height-to-crypt depth ratio, and goblet cell count per pig were used in the final analyses.

Statistics

Data were analyzed as a 2 × 2 factorial arrangement (recovery treatment [TN and HSC] and feeding treatment [AF and NF]) using the PROC MIXED procedure in SAS 9.4 (SAS Institute Inc., Cary, NC). The linear additive model used for all data was: Yijk = µ + Ri + Fj + Kk+ R*Fij + eijk, where Y = dependent variable of interest, µ = mean, R = recovery treatment, F = feeding treatment, K = replication, and e = error term. Temperature data were analyzed separately within the HS and recovery periods using repeated measures with an appropriate covariance structure and time (15-min intervals from 0 to 180 min) as the repeated effect as previously described (Johnson et al., 2016a, 2016b; Kpodo et al., 2020). Consumption attempt data were analyzed separately within the HS and recovery periods using repeated measures with an appropriate covariance structure and hour (1 to 3) as the repeated effect. Individual pigs were considered the experimental unit, and repetition was included as a random factor in all analyses. Consumption attempt data were log-transformed to meet normality assumption, and back-transformed LS means are reported for ease of interpretation. Statistical significance was considered at P ≤ 0.05, and a tendency was defined as 0.05 < P ≤ 0.10.

Results

Gastrointestinal temperature

Heat stress period

During the HS period, TGI, minimum TGI, and maximum TGI were increased (P < 0.01; 2.05, 0.76, and 2.69 °C, respectively) in HSC compared with TN pigs (Table 1). A recovery treatment by time interaction was detected (P < 0.01) where TGI was greater in HSC compared to TN pigs at every 15-min time point from 30 to 180 min, but no differences were detected between HSC and TN pigs at 0 and 15 min (Figure 2A). No other TGI differences were detected (P ≥ 0.51) during the HS period (Table 1).

Table 1.

Effects of rapid cooling after acute hyperthermia on thermoregulatory parameters in pigs with or without feed access

Recovery treatment Feeding treatment P-value1
Parameter TN HSC AF NF SEM R F
Heat stress period
 TGI, °C 39.89 41.94 40.98 40.84 0.21 <0.01 0.51
 Min TGI, °C 39.58 40.34 39.99 39.93 0.15 <0.01 0.68
 Max TGI, °C 40.26 42.95 41.58 41.63 0.30 <0.01 0.87
 TV, °C 38.91 40.54 39.70 39.75 0.15 <0.01 0.76
 Min TV, °C 38.76 38.90 38.86 38.79 0.09 0.03 0.21
 Max TV, °C 39.03 41.50 40.16 40.37 0.22 <0.01 0.42
 TSK, °C 32.43 40.75 36.47 36.71 0.15 <0.01 0.13
 Min TSK, °C 31.34 38.06 34.52 34.88 0.28 <0.01 0.26
 Max TSK, °C 33.26 41.89 37.40 37.75 0.23 <0.01 0.15
 RR, bpm 40 128 82 86 4 <0.01 0.17
Recovery period
 TGI, °C 39.90 40.76 40.59 40.08 0.19 <0.01 0.01
 Min TGI, °C 39.59 39.71 39.93 39.37 0.20 0.54 0.01
 Max TGI, °C 40.20 42.86 41.53 41.54 0.28 <0.01 0.98
 TV, °C 38.84 39.22 39.04 39.02 0.17 0.04 0.90
 Min TV, °C 38.69 38.53 38.60 38.62 0.15 0.21 0.87
 Max TV, °C 38.98 41.33 40.05 40.26 0.25 <0.01 0.47
 TSK, °C 32.33 31.43 31.69 32.08 0.25 <0.01 0.16
 Min TSK, °C 31.43 27.75 29.45 29.73 0.27 <0.01 0.33
 Max TSK, °C 32.63 37.49 35.03 35.09 0.33 <0.01 0.17
 RR, bpm 33 53 42 44 2 <0.01 0.21
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1Differences at P ≤ 0.05.

Figure 2.

Figure 2.

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Effects of recovery treatment on body temperature indices recorded every 15 min during the heat stress and recovery periods on (A) gastrointestinal temperature, (B) vaginal temperature, (C) skin temperature, and (D) respiration rate in pigs with or without feed access. Error bars at each 15-min time point indicate ± 1 SEM. *,^Symbols indicate differences (P < 0.05) comparing recovery treatment by time. a,b,cLetters indicate differences (P < 0.05) comparing recovery treatment by feeding treatment by time at each 15-min time point.

Recovery period

During the recovery period, TGI and maximum TGI were increased (P < 0.01; 0.86 and 2.66 °C, respectively) in HSC compared to TN pigs, regardless of feeding treatment (Table 1). Overall, TGI and minimum TGI were greater (P = 0.01; 0.51 and 0.56 °C, respectively) in AF compared to NF pigs, regardless of recovery treatment (Table 1). Minimum TGI tended to be greater (P = 0.10) in HSC + AF (40.16 ± 0.21 °C) compared to HSC + NF (39.26 ± 0.20 °C) and TN + NF (39.48 ± 0.21 °C) pigs, but no differences were detected between HSC + NF and TN + NF pigs (data not presented). In addition, no minimum TGI differences were detected for TN + AF (39.69 ± 0.20 °C) compared to TN + NF, HSC + AF, and HSC + NF pigs, respectively (data not presented). Gastrointestinal temperature was greater overall (P = 0.03; 2.41 °C) from 0 to 30 min in HSC compared to TN pigs, regardless of feeding treatment (Figure 2A). An increase in TGI was detected (P = 0.03; 0.97 °C) in HSC + AF compared to HSC + NF pigs from 45 to 180 min, and in HSC + AF compared to TN + AF and TN + NF pigs (1.36 and 1.64 °C, respectively) from 45 to 75 min (Figure 2A). Gastrointestinal temperature was greater (P = 0.03; 0.84 °C) in HSC + AF compared to TN + NF pigs from 90 to 135 min (Figure 2A). No other TGI differences were detected (P > 0.05) during the recovery period (Table 1; Figure 2A).

Vaginal temperature

Heat stress period

During the HS period, TV, minimum TV, and maximum TV were greater (P ≤ 0.03; 1.63, 0.14, and 2.47 °C, respectively) in HSC compared to TN pigs, regardless of feeding treatment (Table 1). Vaginal temperature was greater overall (P < 0.01; 1.85 °C) in HSC compared to TN pigs at every time point except 0 and 15 min, regardless of feeding treatment (Figure 2B). No other TV differences were detected (P ≥ 0.27) during the HS period (Table 1).

Recovery period

During the recovery period, TV and maximum TV were greater (P ≤ 0.04; 0.38 and 2.35 °C, respectively) in HSC pigs compared to TN pigs, regardless of feeding treatment (Table 1). Vaginal temperature was greater (P = 0.02; 1.53 °C) from 0 to 30 min in HSC compared to TN pigs, regardless of feeding treatment. At 45 min of the recovery period, TV was greater (P = 0.02; 0.56 °C) in HSC + AF compared to TN + AF pigs (Figure 2B). No other TV differences were detected (P ≥ 0.21) during the recovery period (Table 1; Figure 2B).

Skin temperature

Heat stress period

During the HS period, TSK was greater (P < 0.01; 8.32 °C) in HSC compared to TN pigs, regardless of feeding treatment (Table 1; Figure 2C). Minimum TSK and maximum TSK were increased (P < 0.01; 6.72 and 8.63 °C, respectively) in HSC compared to TN pigs, regardless of feeding treatment (Table 1). No other TSK differences were detected (P ≥ 0.13) during the HS period (Table 1).

Recovery period

During the recovery period, overall TSK and minimum TSK were reduced (P < 0.01; 0.90 and 3.68 °C, respectively) in HSC compared to TN pigs, regardless of feeding treatment (Table 1). Overall, maximum TSK was greater (P < 0.01; 4.86 °C) in HSC compared to TN pigs, regardless of feeding treatment (Table 1). Skin temperature was greater (P < 0.01; 3.72 °C) from 0 to 30 min but reduced (2.71 °C) from 60 to 165 min in HSC compared to TN pigs, regardless of feeding treatment (Figure 2C). No other TSK differences were observed (P ≥ 0.16) during the recovery period (Table 1; Figure 2C).

Respiration rate

Heat stress period

During the HS period, RR was increased (P < 0.01; 88 bpm) in HSC compared to TN pigs, regardless of feeding treatment (Table 1; Figure 2D). No other RR differences were observed (P ≥ 0.17) during the HS period (Table 1; Figure 2D).

Recovery period

During the recovery period, RR was greater overall (P < 0.01; 20 bpm) in HSC compared to TN pigs, regardless of feeding treatment (Table 1). Respiration rate was greater (P < 0.01; 33 bpm), from 0 to 105 min in HSC compared to TN pigs, regardless of feeding treatment (Figure 2D). No other RR differences were observed (P ≥ 0.28) during the recovery period (Table 1; Figure 2D).

Feeding and drinking attempts

Heat stress period

During the HS period, feeding attempts were reduced overall (P < 0.01; 90.38%) in HSC compared to TN pigs, regardless of feeding treatment (Table 2). Drinking attempts tended to be increased overall (P = 0.07) in TN + NF (1.41 ± 0.14%) compared to TN + AF (0.43 ± 0.04%) pigs, but no differences were detected between TN + AF or TN + NF compared to HSC + AF (1.20 ± 0.12%) and HSC + NF (0.69 ± 0.07%) pigs (data not presented). No other feeding and drinking attempt differences were detected (P ≥ 0.55) during the HS period (Table 2; Figure 3A and B).

Table 2.

Effects of rapid cooling after acute hyperthermia on feeding and drinking attempts in pigs with or without feed access

Recovery treatment Feeding treatment P-value1
Parameter TN HSC AF NF SEM R F
Heat stress period
 Feeding, % 1.56 0.15 1.04 0.67 0.44 <0.01 0.56
 Drinking, % 0.92 0.95 0.82 1.05 0.42 0.83 0.55
Recovery period
 Feeding, % 1.18 1.39 1.92 0.65 0.56 0.99 0.02
 Drinking, % 0.85 1.59 1.05 1.40 0.50 0.13 0.43
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1Differences at P ≤ 0.05.

Figure 3.

Figure 3.

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Effects of recovery treatment on (A) feeding attempts and (B) drinking attempts as % of hour during the heat stress and the recovery periods in pigs with or without access to feed. Error bars at each hour indicate ± 1 SEM. No differences observed (P > 0.05).

Recovery period

During the recovery period, feeding attempts were greater (P = 0.02; 195.38%) in AF compared to NF pigs, regardless of recovery treatment (Table 2). No other feeding or drinking attempt differences were detected (P ≥ 0.13) during the recovery period (Table 2; Figure 3A and B).

Histology

Jejunal villus height and villus height-to-crypt depth ratio were reduced overall (P < 0.01; 24.72% and 24.03%, respectively) in HSC compared to TN pigs, regardless of feeding treatment (Table 3). Jejunal goblet cell count tended to be decreased (P = 0.08; 29.95%) in AF compared to NF pigs, regardless of recovery treatment (Table 3). No other jejunal histology differences were observed (P ≥ 0.42; Table 3).

Table 3.

Effects of rapid cooling after acute hyperthermia on intestinal morphology in pigs with or without feed access

Recovery treatment Feeding treatment P-value1
Parameter TN HSC AF NF SEM R F
Jejunum
 Villus height, µm 442.61 333.20 387.01 388.80 27.28 <0.01 0.95
 Crypt depth, µm 301.28 293.75 300.72 294.31 17.56 0.70 0.74
 Villus height: crypt depth 1.54 1.17 1.33 1.38 0.09 <0.01 0.63
 Goblet cells2 7.96 6.80 6.08 8.68 1.33 0.42 0.08
Ileum
 Villus height, µm 379.12 280.14 325.74 333.52 24.39 <0.01 0.74
 Crypt depth, µm 220.76 217.97 219.18 219.55 12.92 0.85 0.98
 Villus height: crypt depth 1.74 1.30 1.50 1.54 0.10 <0.01 0.71
 Goblet cells 18.46 11.47 14.03 15.91 2.26 0.01 0.47
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1Differences at P ≤ 0.05.

2Tendencies at 0.05 < P ≤ 0.10. Mean number of goblet cells per villi.

Ileal villus height and villus height-to-crypt depth ratio were reduced (P < 0.01; 26.11% and 25.29%, respectively) in HSC pigs compared to TN pigs, regardless of feeding treatment (Table 3). Ileal goblet cell count was reduced overall (P = 0.01; 37.87%) in HSC compared to TN pigs, regardless of feeding treatment (Table 3). No other ileal histology differences were observed (P ≥ 0.47; Table 3).

Discussion

Acute hyperthermia is characterized by an uncontrolled increase in body temperature when thermoregulatory mechanisms are overwhelmed by metabolic and environmental heat loads (Bouchama and Knochel, 2002; Smith, 2005). Without a rapid return of body temperature to euthermia, acute hyperthermia can lead to organ damage and increased rates of morbidity and mortality (Gaudio and Grissom, 2016). As such, rapid cooling has been evaluated as a management tool to alleviate the negative impacts of acute hyperthermia in pigs (Johnson et al., 2016a, 2016b; Sapkota et al., 2016; Kpodo et al., 2020), but results are conflicting depending on whether pigs have feed access or do not have feed access during acute hyperthermia recovery. Specifically, in studies where feed access was allowed (Johnson et al., 2016a, 2016b; Sapkota et al., 2016), the return of TGI to euthermia was delayed during rapid cooling, whereas in studies where feed access was not allowed, TGI quickly returned to euthermia during rapid cooling (Kpodo et al., 2020). In the current study, in agreement with the hypothesis, the return of TGI to euthermia during the recovery period was more rapid in HSC + NF vs. HSC + AF pigs. However, no other body temperature indices (i.e., RR, TSK, TV) differences were detected for recovery treatment by feeding treatment interactions. Because TGI was reduced more rapidly in HSC + NF compared to HSC + AF pigs in the absence of greater heat dissipation (i.e., increased RR or TSK; Blatteis, 1998), this likely indicates that feed removal was responsible for the more rapid decrease in TGI for HSC + NF pigs as previously suggested (Kpodo et al., 2020).

Pigs reduce voluntary feed intake to decrease metabolic heat load during times of acute hyperthermia (Pearce et al., 2014; Rauw et al., 2017). Upon removal of the environmental insult (i.e., return of TA to TN conditions and/or rapid cooling) however, voluntary feed intake returns to normal (Xin and DeShazer, 1992) and feeding behavior increases rapidly within the first hour in growing-finishing pigs (Johnson et al., 2016b). A rapid increase in feed intake has the potential to add metabolic heat to the body (i.e., heat of nutrient processing; Cervantes et al., 2018) and delay the return of body temperature to euthermia during acute hyperthermia recovery. In the current study, there was an overall increase in feeding attempts for AF compared to NF pigs during the recovery period. When considering the lack of thermoregulatory differences (e.g., RR and TSK), the increase in feeding attempts (and likely feed intake) may explain the decreased rate of reduction in TGI for HSC + AF vs. HSC + NF pigs during the recovery period. However, although an overall increase in feeding attempts during the recovery period was observed in AF vs. NF pigs, no feeding attempt differences were observed between HSC + AF and HSC + NF pigs, which is surprising considering the numerical increase in feeding attempts during the recovery period for HSC + AF pigs. While reasons for the lack of feeding attempt differences are currently unclear, it is possible that HSC + AF pigs may have had fewer feeding attempts but consumed more feed at each attempt leading to the increase in metabolic heat production and ultimately TGI compared to HSC + NF pigs during the recovery period. Unfortunately, due to study design, this hypothesis cannot be confirmed in the present experiment. Alternatively, discrepancies between the current study and previous results (Johnson et al., 2016b) may be due to experimental design differences. Pigs in the present study remained in the HS room and TA was decreased over 1 h to TN conditions, whereas pigs in the previous study (Johnson et al., 2016b) were immediately moved from HS to TN conditions before water dousing. This means that TA remained elevated for pigs in the present study for a longer period of time when compared to the previous study (Johnson et al., 2016b), and this may have initially reduced their feeding attempts because feeding behavior is influenced by TA (Xin and DeShazer, 1992). Regardless of the reason, the delayed return of TGI to euthermia in HSC + AF compared to HSC + NF pigs independent of thermoregulatory differences may indicate that feed removal could be combined with rapid cooling for a faster return of TGI to euthermia as previously hypothesized (Kpodo et al., 2020).

A swift return of body temperature to euthermia is important to restore thermoregulatory function and reduce the negative effects of acute hyperthermia on organ function (Pease et al., 2009). Acute hyperthermia results from the inability of the body to maintain its internal temperature homeostasis due to unbalanced heat dissipation and heat loads (Bouchama and Knochel, 2002). In the current study, regardless of feeding treatment, exposure to HS conditions resulted in marked increases in all body temperature and thermoregulatory measures (e.g., TV, TSK, TGI, and RR) when compared to TN conditions, suggesting that HSC pigs were suffering from hyperthermia during the HS period. The lack of recovery treatment by feeding treatment differences on body temperature is not surprising since heat-stressed animals decrease feed intake as a strategy to reduce metabolic heat load and combat hyperthermia (Pearce et al., 2014; Ma et al., 2019). Although feed intake was not measured in the present study, the similar feeding attempts between HSC + AF and HSC + NF pigs suggests that HSC + AF pigs may have reduced their feed intake during the HS challenge, thereby reducing metabolic heat production and limiting a feed intake-induced body temperature increase.

While no feeding and recovery treatment interactions were observed for thermoregulatory measures during the HS period, all body temperature measures were reduced over time from 0 to 180 min for HSC pigs during the recovery period. These results agree with previous reports in acutely hyperthermic pigs that are rapidly cooled (Johnson et al., 2016a, 2016b; Kpodo et al., 2020) and were expected because rapid cooling increases the temperature gradient between the core and the skin (Casa et al., 2007) leading to a decrease in body temperature over time in multiple species (Vaile et al., 2011; Walker et al., 2014; Sawicka et al., 2015). Although body temperature was reduced in both the current and previous studies Johnson et al., 2016a, 2016b; Kpodo et al., 2020), HSC pigs in the present study had a more rapid reduction in body temperature to euthermia over time during the recovery period when compared to studies where pigs were provided feed ad libitum (Johnson et al., 2016a, 2016b). While reasons for this discrepancy cannot be completely explained by this experiment, it may be due to body mass differences in which pigs in the current study were approximately 10.1 kg lighter compared to the Johnson et al.’s (2016b) study and approximately 59.3 kg lighter compared to pigs in the Johnson et al.’s (2016a) study. This is because the surface area-to-mass ratio is greater in younger and/or smaller pigs (Renaudeau et al., 2012), which can allow for improved heat dissipation (Blatties, 1998). In addition, although body temperature measures were reduced in HSC pigs over time during the recovery period, these measures remained elevated overall when compared to TN-exposed pigs despite the fact that HSC pigs returned to euthermia by the end of the recovery period. It is likely that the greater body temperature for HSC pigs at the beginning of the recovery period was the driver for this observed increase. An alternative explanation may be that the overall increase in body temperature indices for HSC compared to TN pigs may have been due to a decrease in heat dissipation capacity through the skin due to cold water dousing as previously observed (Marlin et al., 1998; Johnson et al., 2016a, 2016b). Because an increase in TSK is generally associated with greater blood flow to the skin and heat dissipation to the environment (Blatteis, 1998), the observed reduction in TSK may suggest that vasoconstriction occurred leading to a decrease in heat transfer and a maintenance in body temperature above that of TN pigs during the recovery period as a whole.

To maximize heat dissipation, hyperthermic mammals divert blood to the periphery by a combination of subcutaneous vasodilation and gastrointestinal tract vasoconstriction (Hales et al., 1979; Romanovsky and Blatteis, 1996). However, these physiological changes deprive enterocytes of oxygen and nutrients, resulting in increased intestinal permeability and morphological indicators of intestinal damage (Hall et al., 1999; Lambert, 2009). Morphological indicators of intestinal damage resulting from HS exposure such as reduced villus height, crypt depth, and villus height-to-crypt depth ratio are well-documented (Johnson et al., 2016b; Kumar et al., 2017; Abuajamieh et al., 2018). In accordance with these reports, villus height and villus height-to-crypt depth ratio were reduced in both the jejunum and ileum of HSC compared to TN pigs, likely indicating that HSC pigs had compromised intestinal function relative to TN-exposed pigs. However, despite the recovery treatment differences observed, no intestinal morphology differences were detected between HSC + AF and HSC + NF pigs, and these data are contrary to the previous study in which rapidly cooled pigs with feed access had increased intestinal damage (Johnson et al., 2016b). However, this discrepancy may be explained by the almost 5-fold reduction in feeding attempts during the first hour of recovery for pigs in the current study vs. the previous study (Johnson et al., 2016b) since rapid refeeding after fasting is associated with greater intestinal damage in pigs (Lallès and David, 2011). While reasons for this difference are currently unclear, it may be due to sex differences since pigs in the present study were all gilts and the previous study only used barrows (Johnson et al., 2016b). Alternatively, because pigs in the previous study were larger, they may have been more motivated to consume feed because larger pigs have greater average daily feed intake (Duttlinger et al., 2019). Regardless of the reason, these results may imply that the rate of refeeding after acute hyperthermia could be an important factor that influences the amount of intestinal damage that occurs during acute hyperthermia recovery; however, this hypothesis would have to be confirmed in subsequent studies.

In addition to its negative effects on villus height and crypt depth, acute hyperthermia reduces goblet cell count and activity (Ashraf et al., 2013; Abuajamieh et al., 2018). Goblet cells are epithelial cells that produce mucins, the principal component of the protective mucus layers of the intestine (Birchenough et al., 2015), which lubricate the intestine and prevent bacteria adhesion to the epithelium (Kim and Ho, 2010; Broom, 2018). In the present study, although no differences were observed in the jejunum, ileal goblet cell count was reduced in HSC compared to TN pigs, and this is consistent with previous reports in heat-stressed pigs (Johnson et al., 2018) and quails (Sandikci et al., 2004). The decrease in goblet cell count suggests reduced mucin production and potentially compromised intestinal function that could lead to greater susceptibility to infection due to increased bacterial adhesion (Kim and Ho, 2010; Broom, 2018). Despite the fact that overall recovery treatment differences were observed for goblet cell counts, no feeding treatment-related differences were detected. This is consistent with the lack of villus height and crypt depth differences and may be due to the aforementioned decrease in refeeding attempts during the recovery phase in the current study when compared with the previous report (Johnson et al., 2016b).

Conclusions

We hypothesized that feed withdrawal would contribute to a more rapid return of body temperature to euthermia and reduce hyperthermia-induced intestinal damage in pigs. In agreement with the hypothesis, it was determined that feed removal hastened the return of TGI to euthermia. However, contrary to the hypothesis, feed removal did not prevent intestinal damage as indicated by morphological measures. Regardless, these data suggest that feed removal may accelerate the return of TGI to euthermia when pigs are rapidly cooled after acute hyperthermia, which is a key element for a favorable prognosis.

Acknowledgments

We would like to thank the employees at the USDA-ARS Livestock Behavior Research Unit for assistance in daily animal care and data collection. Mention of trade names or commercial products in this article is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture.

Glossary

Abbreviations

AF

feed access

BPM

breaths per min

e

error term

F

feeding treatment

HS

heat stress

HSC

heat stress followed by rapid cooling

K

replication

MAX

maximum

MIN

minimum

NF

no feed access

R

recovery treatment

RH

relative humidity

RR

respiration rate

TGI

gastrointestinal temperature

TN

thermoneutral

TSK

skin temperature

TV

vaginal temperature

Conflict of interest statement

The authors declare no real or perceived conflicts of interest.

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