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ENVIRONMENT, WELL-BEING, AND BEHAVIOR |
* Adaptation Physiology Group, Wageningen Institute of Animal Sciences, Wageningen University, P.O. Box 338, 6700 AH Wageningen, the Netherlands; and Laboratory of Livestock Physiology and Immunology, Department of Biosystems, Catholic University Leuven, Kasteelpark Arenberg 30, 3001 Leuven, Belgium
1 Corresponding author: henk.parmentier{at}wur.nl
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Key Words: corticosterone • glucose • heat stress • lipopolysaccharide • 3,5,3'-triiodothyronine
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Lipopolysaccharide (LPS) is often used as a model antigen to study the susceptibility of the animal to (nonspecific components of microbiological) pathogens. Lipopolysaccharide is an acute inflammatory stimulus, and challenge with LPS stimulates the synthesis and release of glucocorticoids, inducing a rapid, short-lived increase in plasma corticosterone levels (Sternberg, 2006). Furthermore, LPS administration causes a temporary reduction in feed intake (Star et al., 2008), and, as for heat stress, this might have influence on physiological and metabolic processes, reflected by changes in endocrine and oxidative stress parameters. Although the effects of LPS administration on physiological responses such as fever, body temperature, and BW gain has received considerable attention, the effect on endocrine and oxidative stress responses is hardly described.
Understanding the interaction between heat stress and microbial challenge is important because 1) both are common in poultry farming and can occur together and 2) the 2 stressors represent 2 physiological drives that utilize some common effectors but induce opposite responses (Blatteis, 2000). Studies on the response to infection (as induced by LPS) during heat exposure are lacking in poultry.
In the present study, effects of single or combined environmental stressors on endocrine and oxidative stress responses were investigated in 4 layer lines. Exposure to a high temperature (climatic stress) for 23 d and single administration of the model antigen LPS (hygienic stress) were used as environmental stressors. According to Blatteis (2000), we hypothesized that chickens are able to cope with single environmental stressors but that problems in coping ability occur when chickens are exposed to combined environmental stressors. To evaluate the coping ability of the different layer lines, the effects of climatic and hygienic stress on performance and physiological responses were investigated. The current paper will focus on effects of single or combined exposure to high temperature and LPS administration on physiological (endocrine and oxidative stress) responses in 4 layer lines. Endocrine and oxidative stress responses were studied in the form of levels of corticosterone, T3, glucose, UA, and TBARS. In an accompanying paper (Star et al., 2008), effects of exposure to climatic and hygienic stress on performance of these layer lines is reported.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Four purebred layer lines from Hendrix Genetics (Boxmeer, the Netherlands) were used: 3 White Leghorn lines (WA, WB, and WF) and 1 Rhode Island Red line (B1). These lines were characterized for low or high survival rate and low or high natural humoral immune competence as determined in a previous study (Star et al., 2007a). Line WA and WF were characterized for high survival rate and, respectively, a low and high natural humoral immune competence, whereas line WB and B1 were characterized for low survival rate and, respectively, a low and high natural humoral immune competence.
At 22 wk of age, 80 hens per line (320 in total) were transported from a housing facility of Hendrix Genetics to 2 identical climate respiration chambers of Wageningen University. In each climate chamber, 40 hens per line were individually housed in battery cages (45 cm height x 40 cm depth x 24 cm width). The lines were randomly divided over the cages. Hens were fed a standard commercial phase 1 diet (159 g/kg of crude protein, 39 g/kg of crude fiber, and 11.8 MJ of ME/kg). Hens had free access to feed and water. At 22 wk of age, hens were kept at a 13L:11D light scheme. In each of the following 2 wk, the light period was increased by 1 h. At the start of the experimental period (at 24 wk of age), hens were kept at a 15L:9D light scheme until the end of the experimental period (27 wk of age). Hens received routine vaccinations to Marek’s disease (d 1), Newcastle disease (wk 2, 6, 12, 15), infectious bronchitis (d 1, wk 2, 10, 12, 15), infectious bursal disease (wk 3, 15), fowl pox (wk 15), and avian encephalomyelitis (wk 15). Beak trimming was not performed.
Experimental Design
After an adaptation period of 12 d (temperature maintained at 21°C), hens in the first climate chamber were exposed to acute heat stress. Within approximately 1 h, the temperature in this chamber increased from 21 to 32°C, and was maintained at 32°C during the following 23 d. In the second chamber (control), the temperature was maintained at 21°C. At d 1 after the start of heat stress, half of the hens of the heat treatment and half of the control hens were i.v. injected with 1 mg/kg of BW of Escherichia coli LPS (serotype O55:B5, Sigma Chemical Co., St. Louis, MO). The remaining hens received a placebo treatment of PBS. An overview of the experimental design is given in Table 1
. The Institutional Animal Care and Use Committee of Wageningen University approved the experimental protocol.
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Blood samples were collected from the wing vein of all 320 individual hens at d –5, 2, 8, 15, and 22 after the start of heat stress. After sampling, blood was centrifuged and plasma was stored at –20°C until further processing.
Corticosterone. Corticosterone concentration in plasma samples collected from each chicken were quantified using a sensitive and highly specific commercial RIA kit (IDS Inc., Boldon, UK). Before assay, plasma samples were heated at 80°C for 10 min to inactivate corticosterone-binding proteins. Corticosterone concentrations were expressed in nanograms per milliliter of plasma.
T3. Plasma concentration of T3 was measured by RIA according to Darras et al. (1991). Measurements were performed using a commercial available T3 antiserum (ByK-Sangtec Diagnostica GmbH, Dietzenbach, Germany) in combination with a specific tracer (Amersham International, Slough, UK). Concentrations of T3 were expressed in nanograms per milliliter of plasma.
Glucose and UA. Plasma concentrations of glucose and UA were measured by commercial colorimetric diagnostic kits (glucose: IL Test kit, No. 182508–00; UA: IL Test kit, No. 181685–00), using the Monarch 2000 Chemistry System Model 760 (Monarch Chemistry System, Instrumentation Laboratories, Zaventem, Belgium). Glucose and UA concentrations were expressed in milligrams per deciliter of plasma.
TBARS. Lipid peroxidation was measured by spectrophotometric determination of TBARS with a modified method described by Lin et al. (2004a, b). Levels of TBARS were expressed as nanomoles of malondialdehyde per milliliter of plasma.
Statistical Analysis
Differences in levels of corticosterone, T3, glucose, UA, or TBARS were analyzed by a 4-way ANOVA for the effect of line, temperature, LPS administration, time, and their interactions by repeated measurement procedure using a "hen nested within line, temperature, and LPS administration" option. Corticosterone and T3 were measured at d –5, 2, and 8 after the start of heat stress, whereas glucose, UA, and TBARS were measured at d –5, 2, 8, 15, and 22 after the start of heat stress.
Mean differences among lines and treatments were tested with Bonferroni’s test. The PROC MIXED procedure of SAS was used for statistical analysis (SAS Institute, 2004). Effects were considered significant at P < 0.05.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Main effects of exposure to heat, LPS administration, or combined exposure to heat and LPS are shown in Figure 1 and will be described first, whereas more detailed results per line are given in Table 2 and will be described after the main effects.
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The 4 layer lines differed in corticosterone level (P < 0.0001; Table 2
). Line WB had at each sample day significantly higher corticosterone levels than line B1, WA, and WF. Furthermore, there was a line x heat interaction (P < 0.05), indicating that lines differed in corticosterone levels in response to heat stress.
T3
Main effects of exposure to heat, LPS administration, or combined exposure to heat and LPS are shown in Figure 2 and will be described first, whereas more detailed results per line are given in Table 2 and will be described after the main effects.
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The 4 layer lines differed in T3 level (P < 0.0001; Table 2), in which line WA and WB had higher T3 levels than line B1 and WF. Besides, lines differed in T3 levels in response to heat stress (line x heat interaction; P < 0.05); T3 levels of line B1 were decreased by heat stress, T3 levels of line WB were increased, and T3 levels of line WA and WF were comparable to the control groups (21°C + PBS) of these lines. Furthermore, T3 levels during the complete observation period were affected by a line x LPS x time interaction (P < 0.01; Table 2).
Glucose
Main effects of exposure to heat, LPS administration, or combined exposure to heat and LPS are shown in Figure 3 and will be described first, whereas more detailed results per line are given in Table 3 and will be described after the main effects.
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The 4 layer lines differed in glucose level (P < 0.01; Table 3), in which line WB and WF had higher glucose levels than line WA (line B1 was in-between). There was also a line x time interaction (P < 0.05), which suggests that lines had a different response pattern; line B1 and WB had an increased glucose level between d 2 and 8 after the start of heat stress, whereas line WA and WF had a decreased glucose level between d 2 and 8.
UA
Main effects of exposure to heat, LPS administration, or combined exposure to heat and LPS are shown in Figure 4 and will be described first, whereas more detailed results per line are given in Table 3 and will be described after the main effects.
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The 4 layer lines differed in UA level (P < 0.0001; Table 3), in which line B1 and WB had higher UA levels than line WA and WF. There was also a line x time interaction (P < 0.0001), indicating that the lines had a different response pattern; lines WA, WB, and WF had an increase in UA levels from d 2 to 15 after the start of heat stress whereafter the UA levels stabilized, whereas line B1 had an increase in UA level from d 2 to d 8 after the start of heat stress whereafter the UA levels stabilized.
TBARS
Main effects of exposure to heat, LPS administration, or combined exposure to heat and LPS are shown in Figure 5 and will be described first, whereas more detailed results per line are given in Table 3 and will be described after the main effects.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The 4 purebred lines used in the present study were characterized in a previous study (Star et al., 2007a) for high or low natural immune competence and high or low survival rate. Lines B1 and WF were selected for high natural immune competence, whereas lines WA and WB were selected for low natural immune competence. It was expected that endocrine and, to a lesser extent, oxidative stress responses would be related to natural immune competence, because immune responses are affected by the release of hormones by the hypothalamic-pituitary-adrenal axis (Mashaly et al., 1998; Sternberg, 2006). However, in the present study, natural humoral immune competence seemed not related with endocrine and oxidative stress responses to different stressors.
In the present study, the 4 layer lines differed in response patterns and in response levels. The endocrine system of line WB was most sensitive for environmental changes, based on the observed differences in levels of corticosterone and T3 between the treatment groups within this line. In addition, performance parameters (Star et al., 2008) and immune competence (Star et al., 2007b) of line WB were less affected by environmental changes. Performance parameters and immune competence of line B1 were most affected by environmental changes, and in addition, line B1 showed a low sensitive endocrine response to environmental stressors. Like Wingfield and Kitaysky (2002), who suggested that glucocorticoids function as antistress hormones, we speculate that line B1 and WB have different mechanisms to cope with stress, which is probably based on the endocrine responsiveness, and especially on the glucocorticoid hormone corticosterone, to stressors. Corticosterone, as a response upon stress, may be beneficial in the interpretation that sensitivity to this hormone enables line WB to maintain performance together with low sensitivity of immune competence, whereas the stress response of line B1 is to a lesser extent under control of corticosterone resulting in sensitivity in immune competence and inability to maintain performance.
In the present study, the level of T3, as a thermoregulatory hormone, was temporarily decreased at d 2 after the start of heat stress. A decreased T3 level after heat exposure was also found in other studies (Geraert et al., 1996; Lin et al., 2000, 2006; Uni et al., 2001; Maak et al., 2003). In the present study, heat stress increased levels of corticosterone and glucose. The metabolic effect of elevated corticosterone levels is to provide glucose by gluconeogenesis (Davis et al., 2000). Furthermore, heat stress decreased plasma UA levels, as also found by Lin et al. (2000), whereas other studies (Koelkebeck and Odom, 1995; Geraert et al., 1996; Lin et al., 2006) found no effect of heat stress on UA levels. The decrease in UA levels might be related to the weight loss of the chickens (Star et al., 2008), because there is a positive correlation between plasma UA levels and BW loss (Tsahar et al., 2006). The reduction in feed intake (Star et al., 2008) probably caused the weight loss and, related to this, the changes in UA level. Interestingly, mechanisms underlying changes in glucose and UA level are probably different between reduced feed intake due to heat stress or due to forced feed restriction. Forced feed restriction caused a decrease in glucose level (Nijdam et al., 2005) and increase in UA level (Buyse et al., 2002). The decrease in glucose level due to forced feed restriction is caused by a reduced glucose utilization and overall metabolism together with a shift from glucose to free fatty acid use (Buyse et al., 2002; Swennen et al., 2005). The increase in glucose level as a consequence of reduced feed intake due to heat stress is probably caused by a slight increase in gluconeogenesis linked with initial increased corticosterone levels, which could explain the opposite changes in glucose levels in both situations of reduced feed intake. The increase in UA level due to forced feed restriction is caused by an enhanced gluconeogenesis at the expense of body proteins (Buyse et al., 2002). The decrease in UA level as a consequence of reduced feed intake due to heat stress is probably caused by a decreased metabolic level. This could induce a protein-sparing effect (by downregulation of protein turnover) as well as glucose sparing by increased utilization of fat reserves. Therefore, this weight loss due to heat exposure could result in decreased UA levels. Furthermore, the decreased UA level and enhanced level of TBARS suggests an increased oxidative stress caused by heat stress, indicating a disturbance in the balance between the oxidation and antioxidant defense system. Although there was no replication of the heat stress environment (possible confounded results), the findings of endocrine and oxidative stress responses, as well as the findings described in the accompanying paper (Star et al., 2008), are in accordance with other studies.
The effect of microbial challenges, mimicked by LPS, on endocrine and oxidative stress responses of adult laying hens is not documented. Lipopolysaccharide administration caused an increase in T3 levels, which is probably related to the drop in egg production as described in Star et al. (2008). It has been found that T3 is associated with the reproductive state of the chicken. When there is a (fast) drop in egg production, for example during molt (Hoshino et al., 1988; Davis et al., 2000), plasma T3 levels will increase. Levels of UA were decreased by LPS administration, probably due to the reduction in feed intake, and similar as explained for the decrease of UA during heat stress. The reduction in feed intake by LPS administration, however, had no detectable effect on levels of corticosterone and TBARS. Lipopolysaccharide is an acute inflammatory stimulus, and LPS administration induces a rapid, short-lived increase in plasma corticosterone levels (Stenzel-Poore et al., 1993). In a study by Kluger et al. (1997), male rats were exposed to heat stress and were administered with LPS 24 h later. Corticosterone levels were measured, and injection of LPS led to a marked rise in plasma corticosterone at 4 h but not at 24 h postinjection. In the present study, blood samples were taken 1 d after LPS administration. The reaction of corticosterone on LPS treatment was probably more acute and took place within 1 d after treatment, which might explain why no effect of LPS on corticosterone was found. The effect of LPS administration on TBARS is, to our knowledge, not studied before. Lin et al. (2004a, b) found that levels of TBARS were elevated for chronic and acute stress effects after corticosterone administration. In the present study, however, no effect of LPS administration on level of TBARS was found.
Under the given circumstances (temperature of 21 or 32°C with or without 1 mg/kg of BW of LPS), the results of this study indicate that, based on endocrine and oxidative stress responses, hens were able to cope with single or combined heat stress and LPS administration. There were no interactions between heat stress and LPS administration, but both stressors caused a reduction in feed intake, and changes in plasma levels of the endocrine and oxidative stress parameters are partly related with the reduction in feed intake. Although line B1 showed the largest reduction in feed intake, it seems that line WB reacted in the most sensitive way to environmental changes. Neither natural humoral immune competence nor survival rate, on which bases the lines were characterized, was indicative for the stress response to different stressors. The present data suggest that heat stress and LPS administration acted like 2 independent stressors and that the 4 layer lines differed in response patterns and response levels.
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ACKNOWLEDGMENTS |
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Received for publication April 3, 2007. Accepted for publication February 21, 2008.
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