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Poult Sci 2006. 85:1520-1528
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ENVIRONMENT, WELL-BEING, AND BEHAVIOR

Responses of Thyroid Hormones of Market-Size Broilers to Thermoneutral Constant and Warm Cyclic Temperatures

X. Tao*,1, Z. Y. Zhang{dagger}, H. Dong*, H. Zhang{dagger} and H. Xin{ddagger}

* Institute of Agricultural Environment & Sustainable Development, {dagger} National Key Laboratory of Animal Nutrition, Chinese Academy of Agricultural Sciences, 2 Yuan Ming Yuan West Road, Beijing 100094, China; and {ddagger} Department of Agricultural and Biosystems Engineering, 3204 National Swine Research and Information Center, Iowa State University, Ames 50011-3310

1 Corresponding author: taoxp{at}cjac.org.cn


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
This study characterizes the responses, particularly diurnal variations, of thyroid hormones (TH) [3,5,3'-triiodothyronine (T3), thyroxine (T4), and T3:T4 ratio (T3/T4)] of Arbor Acres broilers to constant thermoneutral (TN) or warm cyclic (WC) temperatures. There existed distinct circadian variations—2 peaks in TH under the TN and WC conditions. The 2 peaks of T3, T4, and T3/T4 of the broilers occurred, respectively, at 0 and 16 h, 8 and 16 h, and 0 and 12 h under the TN condition; but at 0 and 12 h, 0 and 8 h, and 4 and 12 h under the WC conditions. During a 5-d heat exposure (HE) to the WC regimens, T3 and T4 showed continual decrease. The daily mean of T3 declined significantly (P < 0.05) on the first day of HE, whereas significant decrease of T4 (P < 0.05) occurred on the second day of HE. There was no significant change in daily mean of T3/T4 during the same HE period. Hence, results of the study indicate that T3 provides a better heat stress indicator than T4. The nature of circadian variations in TH makes it necessary to collect blood samples more than once a day, e.g., 6 times at 0, 4, 8, 12, 16, and 20 h, to ensure full evaluation of hormonal responses of market-size broilers undergoing thermal challenges.

Key Words: diurnal variation • broiler • thyroid hormone • heat stress • thermoneutral


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The major hormone product of thyroid gland, thyroxine (T4), is considered to be a prohormone of the more biologically active 3,5,3'-triiodothyronine (T3). The T3 is converted from 5'-monodeiodination (the outer ring) of T4 by type I iodothyronine deiodinase in the liver and kidney, or by type II deiodinase in the brain, pituitary gland, and brown adipose tissues (He et al., 2000). The T3 and T4 play important roles in regulating metabolism and thermogenesis of chickens.

The biological half-life of T3 and T4 in chickens has been reported to be approximately 3 h (Singh et al., 1967; May et al., 1973), which is much shorter than that in mammalian species (Lister et al., 1985). The shorter half-life of thyroid hormones (TH) in birds leads to measurable circadian fluctuations in thyroid function (Sadovsky and Bensadoun, 1971; Newcomer, 1974; Klandorf et al., 1978; Du et al., 1995), albeit the reported results were inconsistent among studies. Previous studies have examined the impact of various factors on T3 and T4 levels and patterns poultry, including species (Scanes et al., 1983; Gonzales et al., 1999), age (Newcomer, 1978; Decuypere and Buyse, 1988; Renden et al., 1994), energy intake and dietary composition (Lauterio and Scanes, 1987; Buyse et al., 1992; He et al., 2000), feeding regimen (Decuypere and Kühn, 1984; Bartov et al., 1988; McMurtry et al., 1988; Rosebrough and McMurtry, 2000), photoperiod (Newcomer, 1974; Klandorf et al., 1978), and ambient temperature (Bobek et al., 1980; Bowen and Washburn, 1985; May et al., 1986; Sinurat et al., 1987; Brigmon et al., 1992; Geraert et al., 1996, Yahav et al., 1996).

Warm cyclic (WC) temperatures are frequently encountered during summer production. Previous studies have shown heat-induced decreases in TH of poultry (Williamson et al., 1985; Sinurat et al., 1987; Brigmon et al., 1992; Geraert et al., 1996, Yahav et al., 1996), but they could not completely discern the impact of heat stress because of the nature of daily variations in TH. Information on diurnal variations in TH of chickens at high temperatures and thermoneutral (TN) condition is lacking, making the heat stress assessment difficult.

The objectives of this study were to 1) characterize the daily variations of T3, T4, and T3:T4 ratio (T3/T4) of market-size broilers under TN condition; 2) delineate responses of TH of market-size broilers to warm cyclic temperatures as encountered during summer production in China; and 3) evaluate the adequacy of blood sampling protocols as practiced under constant TN condition for hormonal assessment of thermal stress of birds under warm cyclic temperature conditions.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Experimental Birds and Management
Four hundred 1-d-old mixed-sex Arbor Acres broiler chicks were obtained from a commercial hatchery (Beijing Huad Broiler Co., China) and reared at the Animal Nutrition Laboratory of the Ministry of Agriculture, Beijing, China. The chicks were raised in environmentally controlled battery brooders. At 4 wk of age the birds were transferred to wire mesh cages, where they had free access to feed and water via trough feeders and trough-type drinkers. At 58 d of age, 270 healthy broilers of uniform weight were selected and randomly allotted to 3 environmental chambers (3.4-m length x 2.8-m width x 2.2-m height), 90 birds (sex balanced) per chamber. Inside the environmental chambers, the birds were housed in two 4-tier wire cages (1.0-m length x 1.0-m width). The test began following a 3-d acclimation at the TN condition in the environmental chambers, i.e., when the birds were 61 d of age (body mass of 2,631 ± 64 g). During the testing period, the broilers were fed 2 times per day (8 and 20 h, after blood sampling) and had free access to water and continuous (24 h/d) incandescent lighting.

Environmental Conditions
Air temperature and RH inside the chambers were controlled by a computer-based environmental control system. Two different environmental conditions were provided successively to the birds. Namely, during the first 2 d into the test, the birds were provided with a TN constant condition of 22°C dry-bulb temperature and 40% RH. From d 3 to 8, the birds were challenged for 5 d with 1 of the 3 WC temperatures that simulated the summer climates of Harbin—northern China (Trt 1), Wuhan—central China (Trt 2), and Guangzhou—southern China (Trt 3). The temperature set points for each WC regimen were based on the respective weather data of 10 hottest days for the cities during the period from 1991 to 2001 (Lu, 1987), obtained from China Meteorological Administration. The set point temperatures corresponding to blood sample times in the 3 treatments are shown in Table 1Go. To highlight the effects of air temperatures on serum TH of the broilers, a constant RH set point of 40% was used in the 3 chambers.


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  		Table 1. Air temperature set points (°C) at the sampling moments for the 3 warm cyclic (WC) temperature regimens1
 
A programmable, battery-powered RH and temperature data logger (HOBO Pro H8 series, Onset Computer Corporation, Bourne, MA) was used to record temperature and RH in each chamber at 15-min intervals. Temperature-humidity index (THI) values, calculated from the recorded temperature and RH data, were used in the analysis. The THI equation had the form of THI = 0.81 tdb + 0.19 twb that had been developed for 42- to 48-d-old Arbor Acres broilers (Tao, 2003).

Blood Collection and Analysis
Blood samples (4 mL each) were collected from a wing vein using a 1-time-use syringe by a skilled avian physiologist, 6 times per d at 0, 4, 8, 12, 16 and 20 h, respectively. At each sampling time, 5 birds or experimental units (3 males and 2 females or 2 males and 3 females) in each chamber or regimen were bled. The samples were placed in polycarbonate tubes and centrifuged at 3,000 rpm under constant temperature of 4°C for 10 min (Hitachi Refrigerated Centrifuge, model Himac CR20B, Hitachi Ltd, Japan), and the serum was stored at –20°C until hormone analysis was performed.

The birds were handled with care and the blood drawn within 2 min to minimize artifact on hormone responses due to handling. Some birds were sampled more than once with sampling intervals no less than 3 d. The T3 and T4 concentrations were determined by double-antibody RIA using commercially available RIA kits (China Institute of Atomic Energy, Beijing, China).

Statistical Analysis
All results were subjected to standard 1-way ANOVA, and significant differences were examined by 2-tailed t-tests. The relationship between TH levels and the environmental parameters was developed using regression analysis. All analyses were performed using the software of Statistical Package for the Social Sciences (SPSS Inc. Release 10.0, Chicago, IL). Means were considered significantly different at P < 0.05.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Effect of Gender on Thyroid Hormone Levels
Daily blood samples collected from the 5 sampled birds per treatment or regimen were equal by gender. The thyroid hormone (TH) values were analyzed for significant differences between the male and female birds. The results indicated that although the mean values of T3, T4, and T3/T4 somewhat differed between the genders, the differences were not significant (Table 2Go). Therefore, TH values of the male and female broilers at each sampling time were pooled in the subsequent analyses.


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  		Table 2. Effect of broiler gender on serum levels of 3,5,3'-triiodothyronine (T3), thyroxine (T4), and T3/T4 during exposure to thermoneutral (TN) and warm cyclic temperatures1
 
Effect of Repeated Blood Sampling on TH
Throughout the test period, some broilers were sampled more than once; the time interval of 2 adjacent samplings was at least 3 d. Some birds were sampled twice, i.e., on d 1 and again on d 4, whereas a few birds were sampled 3 times, i.e., on d 1, 4, and 7. The effect of repeated sampling for a given HE day on the TH levels was analyzed. The results showed that repeated sampling had no significant effects on the TH responses (P = 0.12 to 0.79, Table 3Go).


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  		Table 3. Effect of repeated sampling on serum levels of 3,5,3'-triiodothyronine (T3), thyroxine (T4), and T3:T4 ratio (T3/T4) in broilers for a given heat exposure (HE) day1
 
Effect of Heat Exposure on TH Concentrations
The T3 and T4 levels of the broilers at each sampling time and their means for the entire test period are summarized in Table 4Go. When the birds were kept at the TN condition of 22.9 ± 1.2°C and RH of 39 ± 7% during the first 2 d into the test, the daily means of T3 and T4 were 1.95 ± 0.50 and 20.82 ± 1.77 nmol/L for d 1, and 1.79 ± 0.42 and 21.52 ± 1.81 nmol/L for d 2, respectively. There was no significant difference between the 2 d. The TH concentration ranged from 1.2 to 2.7 nmol/L for T3 and 17.4 to 24.6 nmol/L for T4. The means of T3 and T4 concentrations over the 2 d were used as the baseline for assessing the impact of the subsequent heat exposure (HE) to WC temperatures.


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  		Table 4. Summary of 3,5,3'-triiodothyronine (T3) and thyroxine (T4) concentrations of market-size broilers at various sampling times of the day under thermoneutral (TN) constant and warm cyclic (WC) temperatures1
 
There were no significant differences in daily means of T3, T4, or T3/T4 among the 3 WC temperature treatments. The pooled daily means of T3 concentration over the treatments were, respectively, 1.35 ± 0.50, 1.14 ± 0.28, 1.06 ± 0.47, 1.07 ± 0.42, and 1.00 ± 0.38 nmol/L for HE d 1, 2, 3, 4, and 5. The corresponding T4 concentrations were 19.21 ± 3.88, 15.22 ± 2.64, 14.06 ± 3.10, 12.57 ± 3.36, and 11.53 ± 3.59 nmol/L, respectively. The resultant T3/T4 ratios were 0.071 ± 0.026, 0.077 ± 0.020, 0.075 ± 0.026, 0.087 ± 0.029, and 0.085 ± 0.013, respectively. Daily means of Ts and T4 decreased with HE time and fell by 45.9% (T3) and 45.6% (T4) on the last day of HE compared with their respective TN baseline.

To further examine the TH changes over the course of HE, daily means of T3, T4, and T3/T4 for all the treatments during the 5-d HE were compared progressively, and the results are shown in Table 5Go. The mean T3 declined significantly (P < 0.05) on d 1 of HE. Another significant decline (P < 0.05) of T3 occurred on d 3 using the HE d 1 value as the base. The response of T4 lagged behind that of T3. The first significant decrease (P < 0.05) of T4 from its TN baseline occurred on d 2 of HE. The T4 continued to decrease with time of HE, and the second significant decline (P < 0.05) from the d 2 value occurred on d 4 of HE. Changes in T3/T4 were relatively milder. It declined on the first 3 d of HE, then returned almost to the baseline value.


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  		Table 5. Comparison of daily means of serum levels of 3,5,3'-triiodothyronine (T3), thyroxine (T4), and T3:T4 ratio (T3/T4) of broilers exposed to thermoneutral constant or warm cyclic temperatures1
 
To delineate the quantitative relationship of TH with environmental temperature and HE, the profiles of T3 and T4 reduction ({Delta}T3 and {Delta}T4) along with the THI increment from TN ({Delta}THI) are shown in Figure 1Go. The {Delta}T3 and {Delta}T4 showed negative relations with {Delta}THI except for the last day of HE, possibly a result of acclimation to the HE. Regression analysis of the {Delta}T3 and {Delta}T4 vs. {Delta}THI and HE time ({Theta}, h) revealed the following functional relations:


Figure 1
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  		Figure 1. The profiles of 3,5,3'-triiodothyronine (T3) and thyroxine (T4) reductions ({Delta}T3 and {Delta}T4) changed with the temperature-humidity index (THI) increment from thermoneutral (TN) baselines on: heat exposure d 1 (A), heat exposure d 2 (B), heat exposure d 3 (C), heat exposure d 4 (D), heat exposure d 5 (E), and heat exposure d 1 to 5 (F).

 

Formula 1([1])


Formula 2([2])

Circadian Variations of TH under TN Condition
The circadian variations of the broiler TH under TN condition are depicted by the means of T3, T4, and T3/T4 at each sampling time during the first and second day of TN exposure (Figure 2Go). The T3, T4, and T3/T4 all exhibited 2 daily peaks. Specifically, T3 peaked at 0 and 16 h; both were significantly greater than the valley values at 8 and 20 h (P < 0.05). The highest T3 value at 0 h was 1.9 times the lowest value at 8 h. In comparison, T4 peaked at 8 and 16 h and reached the lowest value at 12 h. However, no significant difference was observed in T4 between any 2 sampling times of the day. The T3/T4 fluctuated differently compared with T3 and T4.


Figure 2
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  		Figure 2. The profiles of daily variations of 3,5,3'-triiodothyronine (T3), thyroxine (T4), and T3/T4 in market-size broilers under thermoneutral (TN) constant conditions.

 
In light of the circadian variations in TH under the TN condition, a randomly sampled, instantaneous value during the day may not provide good information on the physiological status of the birds. In fact, it may even lead to wrong conclusion when/if the blood samples were collected near the peak or valley time. It is therefore suggested that blood samples be collected 6 times throughout the day, as practiced in the current study for measurement of TH levels. If fewer samples have to be collected, they should be done at least 1 h outside the peak or valley time.

Circadian Variations of TH under WC Temperatures
The T3, T4, and T3/T4 for each WC regimen exhibited similar circadian variations during the 5-d HE. Samples of temporal profiles of TH on the first day of HE are shown in Figure 3Go. The T3, T4, and T3/T4 exhibited 2 peaks, but the diurnal rhythms were different from each other and also different from their counterpart under TN condition. The T3 peaked at 0 and 12 h and reached valley values at 8 and 16 h. Significant differences were observed between the peaks and valleys only on the first day of HE. The T4 showed 2 peaks at 0 and 8 h and 2 valleys at 4 and 16 h. The T3/T4 showed peaks at 4 and 12 h and valleys at 8 and 20 h. The similarity shared by T3 and T4 variations was that both reached the minimum at 16 h and the maximum at 0 h. The minimum T3 and T4 values were 61 and 83% of the corresponding maximum values, respectively. Because of the differences in T3 and T4 diurnal variations, the diurnal pattern of T3/T4 followed neither.


Figure 3
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  		Figure 3. The profiles of diurnal variations of 3,5,3'-triiodothyronine (T3) and thyroxine (T4) on the first day into the warm cyclic temperatures simulating the summer climates of A: Harbin—northern China (treatment 1), B: Wuhan—central China (treatment 2), and C: Guangzhou—southern China (treatment 3) and the diurnal variations of T3:T4 ratio (T3/T4) under the 3 warm cyclic temperatures (D).

 
The diurnal fluctuations of T3, T4, and T3/T4 of the broilers under the WC conditions were quite different from those under the TN condition. When TH are used as heat stress indicators of chickens, sampling time will be critical due to their circadian variation. Data from this study suggest that collection of 6 samples (once every 4 h) throughout the day would be highly desirable. If this is not possible, at least 3 samples at 12, 16, and 20 h should be considered to reasonably assess the impact of WC temperatures on the birds, as experienced in the present study.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The outcome of broiler TH being independent of bird sex as shown in the current study was in agreement with the reports of Mitchell (1988) and May (1982). However, Sadovsky and Bensadoun (1971) found that plasma iodohormone of hens was significantly higher than that of roosters. It is speculated that differences in bird’s age (10-mo-old hens or roosters vs. 2-mo-old broilers) and thus reproduction status might have contributed to the differences in the findings.

The diurnal rhythms of TH under the TN condition were partly in agreement with the studies by Du et al. (1995) and Sadovsky and Bensadoun (1971). Our finding of maximum T3 value occurring at midnight agreed with Du et al. (1995), who observed 3 peaks of T3 at 0 (highest), 8, and 16 h for adult White Leghorn roosters under natural photoperiod and cool conditions, although bird species differed between the 2 studies. The current study showed 2 peaks of T3 at 0 and 16 h and a valley (instead of another peak) at 8 h. This result differed from the report by Sadovsky and Bensadoun (1971) that showed peaks of T3 at 8 and 16 h. The different photoperiods involved might have contributed to the outcome. Photoperiods in both previous studies began at 6 h, which stimulated feed intake and in turn could have caused T3 to peak 2 h later. Such stimulating effect was presumably less under continuous lighting as used in the current study. The diurnal variations of T4 was in agreement with the observations by Sadovsky and Bensadoun (1971), with 2 peaks showing at 8 and 16 h. The T3/T4 ratio was subject to the influence of both T3 and T4. As such, variation patterns were different from those of T3 or T4.

Broilers under the WC temperatures also exhibited 2-peak circadian rhythms of TH. However, timing of the peak occurrence was somewhat different from that under the TN condition. Specifically, T3 and T4 under both the TN and WC conditions shared 1 peak time of 0 h for T3 and 8 h for T4. On the other hand, T3 and T4 peaked at 16 h under the TN condition, but both showed the daily low at 16 h, corresponding to the highest temperature of the day under the WC regimens. Clearly, environmental temperature has a major impact on the dynamics of TH.

In addition to affecting the diurnal variations, the high temperature also affected the magnitude of TH. When the broilers were exposed to the WC temperatures, daily mean of T3 dropped significantly on d 1 of HE. The response of T4 was relatively slower in that significant decline in daily mean occurred on d 2 of HE. Both T3 and T4 continued to decrease and remained at the lower levels throughout the 5-d HE period. The T3/T4 declined to some extent on the first 3 d, but no significant difference was detected. There has been extensive documentation in the literature concerning the effects of temperature on TH, but the results vary. Geraert et al. (1996) reported a significant reduction in plasma T3 concentration, whereas T4 concentration did not decrease as much or even remained unchanged under chronic HE. Rudas and Pethes (1984) found that T4 concentration was reduced after exposure to 35°C for 1 h, but T3 concentration was not changed. Sinurat et al. (1987) indicated that the plasma T3 concentration decreased, but T4 concentration increased during exposure to high temperature. The discrepancies among these research findings could have resulted from different environmental scenarios involved. Under the current study conditions, decrease in both T3 and T4 during a 5-d exposure to the WC regimens was observed. Our data thus showed that T3 seems a more responsive indicator when TH are used to assess the environment impact.

The results of this study also suggest that circadian rhythms of TH for market-size broilers under WC environmental conditions could be quite different from those under TN conditions. To ensure a good representation of the diurnal hormonal variations, 6 samples per d (once every 4 h) are highly recommended.

Received for publication August 12, 2005. Accepted for publication May 4, 2006.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
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