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Effects of mild heat stress and grain challenge on acid-base balance and rumen tissue histology in lambs¹

N. E. Odongo^*, O. AlZahal^*, M. I. Lindinger, T. F. Duffield, E. V. Valdes, S. P. Terrell and B. W. McBride^*,2

^* Departments of Animal and Poultry Science, and Human Biology and Nutritional Sciences, and and Population Medicine, University of Guelph, Ontario, N1G 2W1 Canada; and and Disney’s Animal Kingdom, Lake Buena Vista, Florida 32837-1000

	Abstract

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The effect of heat stress (HS) and grain challenge (GC) on acid-base balance and rumen tissue histology in lambs was investigated using 24 yearling wether lambs (58 ± 4.5 kg of BW) in a 2 x 2 factorial experiment with repeated measures for day (10, 14, and 17) of sampling. The factors were temperature [thermoneutral zone (TN) vs. HS] and diet (control vs. GC). Lambs were blocked by BW and assigned to 1 of 4 treatments in temperature-controlled rooms: 1) TN (temperature = 18 to 20°C; relative humidity = 30%; 2) TN + GC; 3) HS (temperature = 35°C for 9 h/d, 20°C for 15 h/d; relative humidity = 40%); and 4) HS + GC. Venous blood samples were collected at 1800 on the first day of GC (d 10), in the middle of GC (d 14), and at the end of the trial (d 17) by jugular venipuncture and analyzed for pH, gases, hematocrit, plasma ions, and total protein. After all measurements in live animals were taken on d 17, lambs were slaughtered, and tissue samples were obtained from the ventral sac of the rumen for histological assessment. Except for the concentration of plasma glucose (P = 0.04) and total protein (P < 0.01), there were no (P > 0.05) diet x temperature interactions. With HS, the concentration of Na⁺ and Cl^– in the control group decreased at d 14 and then increased by d 17, and respiration rates in the control group decreased linearly (P < 0.05). Compared with the control group, respiration rates and the concentration of Cl^– in the GC lambs increased linearly over time, whereas the concentration of Na⁺ decreased linearly (P < 0.05) across time. Under HS, the partial pressure of carbon dioxide, total carbon dioxide, the partial pressure of oxygen and oxygen saturation, and the concentration of Mg²⁺, glucose, and HCO₃^– showed quadratic (P < 0.05) responses with time. In both treatments, DMI, base excess of extracellular fluid, base excess of blood, and standard bicarbonate increased linearly (P < 0.05), and hematocrit, plasma protein, Ca²⁺, anion gap, and plasma strong ion difference decreased linearly (P < 0.05) across day. Compared with the control group, the GC group had decreased papillae count in the ruminal ventral sac (1.3 vs. 1.5; P < 0.05). These results suggest that under HS the acidifying effects of GC on acid-base balance in lambs were counteracted in the short-term through respiratory adaptation.

Key Words: acid-base balance • grain challenge • heat stress • rumen tissue histology • sheep

	INTRODUCTION

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Carbohydrates are the primary energy source for herbivores. However, when the carbohydrate supply in the diet is increased abruptly (e.g., after grain engorgement or during adaptation to high-concentrate diets), the supply of total acid in the ruminal mixture is greatly increased and can result in ruminal acidosis (Owens et al., 1998). Ruminal acidosis can damage ruminal and intestinal epithelial tissues, leading to transmigration of bacteria responsible for liver abscesses (Underwood, 1992). However, ruminants suffering from subacute ruminal acidosis do not typically exhibit clinical signs of illness and often go undetected. Prolonged exposure to low ruminal pH can result in systemic acidosis and impose a chronic strain on the animal’s physiological mechanisms and ability to maintain acid-base balance.

During summer months, ruminants are often subjected to hot environments and/or excessive solar radiation (Early et al., 1991). This heating can result in chronic hyperthermia, causing severe or prolonged inappetence (Bell et al., 1989), which may further exacerbate the increased supply of total acid in the rumen and decrease ruminal pH. Furthermore, acidosis is also experienced by wild herbivores in captive conditions when fed diets that are high in readily fermentable carbohydrates (Clauss et al., 2001). Such herbivores are typically fed high grain diets and/or treats for show and, in subtropical locations, experience periods of moderate to severe heat stress (HS). Animals under these conditions tend not to thrive, and may exhibit impaired health status and inappetence (Bell et al., 1989).

In the current study, lambs were used as a model for captive herbivores. The hypothesis was that lambs exposed to HS and fed high grain diets (grain challenge; GC), would experience acid-base balance perturbation. It was further hypothesized that GC would exacerbate the effects of HS on acid-base balance in lambs. Therefore, the objective of this study was to investigate the effect of HS and GC on blood acid-base balance and rumen tissue histology in lambs.

	MATERIALS AND METHODS

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Animals and Feeding
Twenty-four fully fleeced yearling wether lambs (Canadian Arcott; 58 ± 4.5 kg of BW) of similar nutritional and environmental background obtained from Ponsonby Research Station, University of Guelph, Canada, were used in the study. Before the start of the experiment, ad libitum intake of 90% Timothy hay and 10% Mazuri ADF16 pellets (ADF16; Purina Mills, St. Louis, MO) were recorded daily during the adaptation period to determine DMI. Lambs were fed individually, and water was available all times. All experimental procedures were done with the approval of the University of Guelph Animal Care Committee in accordance with the guidelines of the Canadian Council on Animal Care. The experiment lasted 17 d (10-d adaptation and 7-d measurement).

Grain Challenge
The GC, as described by Keunen et al. (2002), was initiated on d 10 and continued daily through to d 17. This model was originally developed to induce subacute ruminal acidosis in dairy cows. We validated the procedure using 2 rumen-fistulated ewes to determine the substitution rate of grain pellets that would reduce ruminal pH to <6.0 for 5 to 6 h/d. We challenged the ewes by restricting hay intake to 35% of ad libitum intake and replacing it with 55% ADF16 pellets and 10% wheat-barley pellets (WBP, 50% ground wheat, 50% ground barley; Floradale Feed Mill Ltd., Guelph, ON, Canada).

Briefly, the feeding schedule during GC was as follows: 1) at 0700, ewes were offered one-half of their hay and one-third of their ADF-16 allocation for the day; 2) at 0900, hay and ADF16 that had not been consumed were removed, and the ewes were offered half of their WBP allowance for the day; 3) at 1100, the WBP that had not been consumed was removed, and ewes were offered the second third of their ADF16 allocation; 4) at 1300, ADF16 that had not been consumed was removed, and the ewes were offered the second half of their WBP allowance; 5) at 1500, the WBP that had not been consumed was removed, and the ewes were offered the final third of their ADF16 allocation; and 6) at 1700, ewes were offered the remainder of their hay allowance and all feed weigh-backs for the day. The feed was left with the ewes overnight, and the cycle was repeated the next day.

The amount of hay, ADF16, and WBP consumed by each ewe was recorded daily and orts weighed each morning before the day’s feeding. The chemical composition of the feed ingredients is presented in Table 1. Both ewes consumed all the WBP within 2 min of being offered. By replacing 65% of the ad libitum chopped (2-in. sieve) hay intake with 55% ADF16 and 10% WBP, we achieved a ruminal pH <6.0 for 5 to 6 h/d. Ruminal pH was greatest just before the morning feeding and gradually decreased as fermentation of the dietary carbohydrates commenced (Keunen et al., 2002).

Measurements
Samples of the feed ingredients and orts were taken daily and frozen. The feed samples were pooled weekly and analyzed at Agri-Food Laboratories (Guelph, ON, Canada) using AOAC (1990) procedures. Dry matter was determined by oven drying at 60°C for 48 h (method 930.15), CP by macro-Kjeldahl (method 984.13), ADF (method 973.18c), and minerals (Ca, P, Mg, and K) by inductively coupled plasma spectroscopy (method 945.46). Neutral detergent fiber was determined as described by Van Soest et al. (1991).

Venous blood samples were collected by jugular venipuncture at 1800 of the first day of GC (d 10), in the middle of GC (d 14), and at the end of the trial (d 17) in 6-mL sodium heparin vacutainers (Becton Dickinson, Franklin Lakes, NJ). Within 3 min of collection, blood samples were analyzed for blood pH, partial pressure of CO₂ (pCO₂), partial pressure of O₂, and for the concentration of plasma Na⁺, K⁺, Cl^–, ionized Ca²⁺, and glucose, and for hematocrit with the use of selective electrodes (StatProfile 5 blood gas/ion analyzer, Nova Biomedical Corp., Waltham, MA). From the directly measured results, O₂ saturation, base excess of blood (BE-B), base excess of extracellular fluid (BE-ECF), bicarbonate (HCO₃^–), standard HCO₃^– (Sbc), total CO₂ (TCO₂), O₂ content, normalized Ca, anion gap [(Na⁺ + K⁺) – (Cl^– + HCO₃^–); Emmet and Narins, 1977], and osmolarity were calculated. Plasma strong ion difference (SID) was obtained from the equation: SID (mEq/ L) = [(Na⁺ + K⁺) – Cl^–; Stewart, 1983]. Blood was then centrifuged for 15 min (2,500 x g) using a Beckman tabletop centrifuge (model TJ-6RS; Palo Alto, CA), and the plasma was analyzed for total protein using a clinical refractometer (model SPT-T2-NE; Atago Co. Ltd., Tokyo, Japan) and Mg²⁺ (Hitachi 911; Laboratory Services Division, University of Guelph, ON, Canada).

Urine samples for pH determination, animal weights, and respiration rates were also obtained on days 10, 14, and 17. Urine samples were collected at 1800 in plastic centrifuge tubes using plastic funnels placed over the animal’s sheath and fastened around the animal’s body using rubber tie-down cords. Respiration rates were determined between 1300 and 1600 on each day of observation by counting breaths taken in 15-s intervals. Two technicians each recorded 2 measurements per animal per day.

After taking all measurements in the live animals on d 17, lambs were killed by captive bolt stunning and exsanguination. Immediately upon evisceration, ruminal contents were removed, and tissue samples were obtained from the ventral sac of the rumen for histological assessment as described by Walton et al. (2001). Briefly, histological sections were stained with hematoxylin and eosin, embedded in paraffin wax, and sectioned as described by Holle and Birtles (1990). Morphometric measurements of the ventral rumen were determined using computer-aided light microscope image analysis (BioQuant System IV; R & M Biometrics, Nashville, TN) according to Bird et al. (1994). Five rumen papillae per slide were selected at random for analysis. Papillae surface area was obtained as papillae height x papillae width.

Statistical Analysis
The repeated measurements of DMI, respiration rates, and acid-base measurements were analyzed using PROC MIXED of SAS (v. 9.1; SAS Inst., Inc., Cary, NC). To identify time dependent changes, and interactions between time and diet and time and temperature, the model evaluated the effects of control vs. GC under different temperature regimes using linear and quadratic orthogonal contrasts. Tissue histology data were analyzed using GLM procedures of SAS. The model used for these analyses was

in which Y_ij = the dependent variable, µ = overall mean, _i = effect of HS (_i = 1, 2), ß_j = effect of GC (_j = 1, 2), ß_ij = effect of interaction of HS and GC, and _ij = random residual error. Treatment means were compared using Tukey’s multiple comparison procedure, and effects were considered significant at a probability of P < 0.05. Data are expressed as mean ± SE, which represents the pooled SE for the model.

	RESULTS AND DISCUSSION

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All lambs consumed all the WBP within 2 min. The eating patterns and amounts consumed by the lambs were essentially identical to those of the 2 ewes used to test and validate the GC model. It is therefore likely that the ruminal pH profiles of <6.0 for 5 to 6 h/d were achieved in all the GC lambs, similar to that seen in the 2 fistulated ewes. If it did indeed occur, this reduction in ruminal pH would be attributed to 2 factors: 1) the acidogenic effects of the combination of WBP and ADF16 in increasing the proportion of readily fermentable carbohydrate in the diet (Giger-Reverdin and Sauvant 2001); and 2) decreasing the dietary cation-anion difference [DCAD; (Na⁺ + K⁺) – (Cl^– + S^2–); Block, 1994] from 573 mEq/kg of DM when lambs were fed the Timothy hay and ADF16 diet to 422 mEq/kg of DM on the GC diet.

Except for the concentrations of plasma glucose (P = 0.04) and plasma protein (P < 0.01), there were no (P > 0.05) diet x temperature interactions. The diet x temperature interaction term was therefore removed from the model, and emphasis was placed on the effects of GC vs. control diets under different temperature regimes using linear and quadratic orthogonal contrasts.

Thermoneutral Environment
The main effects of GC on DMI, respiration rates, blood pH, blood gases, hematocrit, plasma ions, and plasma protein for lambs in the 20°C environment are presented in Table 2. There was a quadratic (P < 0.05) time x diet effect on the concentration of glucose and plasma protein and a linear (P < 0.05) time x diet effect on blood pH, pCO₂, the concentration of Na⁺, TCO₂, HCO₃^–, normalized Ca, and osmolarity (Table 2). Plasma protein in the control group increased at d 14 and then decreased by d 17, whereas plasma protein in the GC group decreased at d 14 and then increased by d 17. The concentration of glucose in the control group decreased (P < 0.05) at d 14 and then increased at d 17, whereas the concentration of glucose in the GC group increased (P < 0.05) linearly.

Introduction of readily fermentable starch into a diet increases the availability of free glucose and stimulates the growth of most ruminal bacteria, thereby increasing production of VFA and decreasing ruminal pH (Owens et al., 1998). Dietary cation-anion difference also directly affects the plasma and systemic acid-base state through plasma SID. Therefore, a decreased quantity of dietary strong cations (Na⁺ + K⁺) in the presence of maintained or increased strong anions (Cl^– + S^2–) will decrease SID. Dietary cation-anion difference of a feed is therefore a major determinant of plasma SID as the strong ions enter the blood from the digestive tract (Riond, 2001). It has been shown that a DCAD of less than 250 mEq/kg may result in metabolic acidosis by decreasing blood pH and the concentration of Na⁺, K⁺, Mg²⁺, HCO₃^–, and pCO₂ and increasing concentration of plasma Cl^–, as well as increasing the urinary excretion of K⁺, Na⁺, Cl^–, and Ca²⁺ ions (Block, 1984; Tucker et al., 1988; McKenzie et al., 2003). The DCAD of the control groups was neutral with respect to blood acid-base balance and thus was not expected to generate a systemic alkalosis or acidosis.

Heat Stress Environment
The main effects of GC on DMI, respiration rates, blood pH, blood gases, hematocrit, plasma ions, and concentration of plasma protein for lambs in the 35°C environment is presented in Table 3. Homeotherms have optimal temperature zones (the TN zone) within which no additional energy above maintenance is required to heat or cool the animal (Berman et al., 1985). For adult sheep with full fleece, the TN zone is between –12 and 32°C (Taylor, 1992). A main effect of temperature in both the control and GC diet lambs was increased respiration rates, consistent with previous reports in sheep (Dixon et al., 1999; Srikandakumar et al., 2003) and high-producing dairy cows in a subtropical environment (Berman et al., 1985). There was a quadratic (P < 0.05) time x diet effect on the concentration of Cl^–, Na⁺, and osmolarity, and a linear (P < 0.05) time x diet effect on respiration rates and plasma protein (Table 3). The concentration of Na⁺ and Cl^– ions in the control group decreased at d 14 and then increased by d 17; the respiration rates in the control group decreased linearly (P < 0.05), and the respiration rates and concentration of Cl^– in the GC group increased linearly across time. The concentration of Na⁺ in the GC group decreased linearly (P < 0.05; Table 2). For both the control and GC groups, time had a quadratic (P < 0.05) effect on pCO₂, partial pressure of O₂, O₂ saturation, and the concentration of Mg²⁺, glucose, HCO₃^–, and TCO₂ (Table 3), whereas DMI, BE-ECF, BE-B, and Sbc increased linearly (P < 0.05), and hematocrit, plasma protein, Ca²⁺, anion gap, and SID decreased linearly (P < 0.05).

It is apparent that examination of traditional acid-base variables (pH, pCO₂, HCO₃^–) indicates an absence of significant acid-base disturbance, and indeed blood pH was maintained within normal ranges (7.31 to 7.53; Duncan and Prasse, 1994) throughout the experiment. A deeper examination of independent physicochemical variables that contribute to acid-base balance shows that changes in some independent variables contributed to an acidifying effect on plasma, and others contributed to an alkalizing effect.

Respiratory disorders are manifested by changes in plasma pCO₂ (Stewart, 1983), and pCO₂ is an independent variable in acid-base control (Stewart, 1983). In addition, 2 other independent variables also determine acid-base status: the SID, which is the difference between the combined concentrations of the strong (completely dissociated) cations and strong anions; and the sum of the concentrations of the associated and dissociated nonvolatile weak acids, mainly albumin and phosphate (Figge et al., 1991; Wilkes, 1998). The weak acids contribute the remaining charges to satisfy the principle of electroneutrality, such that SID – (CO₂ + A–) = 0. A_tot = AH + A–, in which AH + A– is the sum of the concentrations of the associated and dissociated nonvolatile weak acids (Figge et al., 1991). Besides the concentration of H⁺, the other dependent variables include the concentration of HCO₃^– CO₃^2– and OH^–. The physico chemical approach to acid-base disturbance also follows these two important physical laws: 1) electroneutrality, which dictates that in aqueous solutions, the sum of all positively charged ions must equal the sum of all negatively charged ions; and 2) conservation of mass, which means that the amount of a substance remains constant unless it is added to or generated, removed, or destroyed.

Heat stress resulted in decreased plasma SID that was attributed to a decrease in the concentration of Na⁺ because there were no changes in other plasma strong ion concentrations. Taken alone, this decrease in SID had a mild acidifying effect on blood pH. The absence of a decreased blood pH is therefore attributed to the tendencies for decreased pCO₂ and the concentration of A_tot (from plasma protein) at d 10 and 14, both of which contribute to a mild alkalizing effect and thus counteracting the contribution of decreased SID.

Mechanically, decreases in the concentration of plasma Na⁺, SID, plasma protein, and A_tot in response to HS have been associated with plasma volume expansion as a physiological heat acclimation response in humans (Bass et al., 1955; Convertino, 1991) and horses (Lindinger et al., 2000). However, the mechanisms by which SID were decreased in the control and GC groups seem different. The reduction in SID for the GC group can be attributed to the large dietary intake of Cl^–. This result is consistent with that of Escobosa et al. (1984), who fed dairy cows a diet containing 1.67% Cl^– during moderate HS and reported decreased blood pH and pCO₂, and urine pH, compared with a control diet of 0.34% Cl^–. In the current study, the decease in SID in the control diet lambs was attributed to a simultaneous decrease in the concentration of plasma Na⁺, as discussed previously, because there were no changes in other plasma strong ion concentrations.

The only measures consistently affected by the main effect of GC in both temperature regimes were the concentration of plasma glucose and Cl^–. In the control group at 20°C, the concentration of glucose decreased at d 14 and then increased at d 17, whereas the concentration of glucose in the GC group at 20°C increased linearly (Table 2). The concentration of Cl^– in the control group at 35°C decreased at d 14 and then increased by d 17, whereas the concentration of Cl^– in the GC group at 35°C increased linearly (Table 3). In the control group at 35°C (Table 3), the increased concentration of plasma HCO₃^– was associated with an increased concentration of plasma Cl^– at d 14, consistent with an earlier result of Yen et al. (1981). In contrast, the mild metabolic acidosis in the GC group can be attributed to the increased concentration of plasma Cl^–, which was associated with a decrease in the concentration of plasma HCO₃^– at d 14 (Table 3). This is consistent with the apparent increases in renal HCO₃^– absorption and excretion of acid equivalents (Tucker et al., 1988). As noted by Coppock et al. (1982), the concentration of plasma Cl^– reflects the balance between dietary Cl^– ingestion and renal/fecal Cl^– excretion, and therefore the greater (P < 0.05) concentration of plasma Cl^– for the GC group (Tables 2 and 3) is consistent with increased dietary inclusion of ADF16, which was particularly high in Cl^– (Table 1).

By the end of the trial (d 17), there was a tendency (P = 0.06) for HS to reduce DMI (Table 3). Depression of voluntary feed intake in ruminants due to HS has been reported in previous studies (Fuquay, 1981; Collier et al., 1982; McGuire et al., 1989; Sanchez et al., 1994; Srikandakumar et al., 2003), and probably represents one protective mechanism or adaptive behavior by which animals reduce heat load. Since heat increments from voluntary activity, rumen fermentation, feed digestion, and nutrient absorption and metabolism are reduced when feed intake is less, then not as much heat needs to be dissipated by the animals. It is also possible that the increased respiration rates observed in the HS lambs forced the lambs to consume less feed.

Rumen Tissue Histology
Rumen tissue histology is presented in Table 4. Ruminal ventral sac papillae count in the GC lambs under HS were fewer but longer (P < 0.05) than those of the control lambs (Figure 1). This is the first report of a response of rumen morphology to GC under HS. The rumen epithelium is responsible for several physiologically important functions, including nutrient absorption and transport, short-chain fatty acid metabolism, and protection (Gálfi et al., 1991). Earlier work has shown that high grain concentrate diets markedly increase the number and size of ruminal papillae in cows (Dirksen et al., 1984). Lane and Jesse (1997) reported that infusing 50% of the lamb’s estimated net energy requirement in the form of short chain fatty acids at physiological concentrations resulted in increases in papillae length. However, the underlying mechanisms of the dietary energy-dependent physiologic, biochemical, and histological alterations of the rumen epithelium are not known. More recent work has suggested that the intake of high levels of protein and carbohydrate increased papillary size and density via butyrate and propionate regulation of IGF-I production (Shen et al., 2004). There is a need for further research to better understand the factors affecting rumen development and alteration.

View larger version (72K): [in this window] [in a new window]   Figure 1. Morphology of ruminal ventral sac papillae in the grain challenge lambs under heat stress (grain challenge) vs. the control lambs.

	IMPLICATIONS

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	Footnotes

 
¹ The authors would like to thank the staff of the Ponsonby Research Station, University of Guelph, for their technical assistance. We also would like to acknowledge the continued support received from the Ontario Ministry of Agriculture and Food and the Natural Sciences and Engineering Research Council of Canada (BWM).

² Corresponding author: bmcbride{at}uoguelph.ca

Received for publication May 30, 2005. Accepted for publication September 27, 2005.

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