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Poult Sci 2008. 87:2647-2652. doi:10.3382/ps.2007-00462
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PHYSIOLOGY, ENDOCRINOLOGY, AND REPRODUCTION

Effects of Age and Strain on Yolk Sac Utilization and Leptin Levels in Newly Hatched Broilers1

J. X. Huang*,{dagger},{ddagger}, X. G. Luo*,{dagger},2, L. Lu*,{dagger} and B. Liu*,{dagger}

* Mineral Nutrition Research Division, Institute of Animal Sciences, Chinese Academy of Agricultural Sciences, Beijing 100094, China; {dagger} State Key Laboratory of Animal Nutrition, Beijing 100094, China; and {ddagger} Chongqing Academy of Animal Sciences, Chongqing 402460, China

2 Corresponding author: wlysz{at}263.net


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The dynamics of yolk sac utilization and changes of leptin levels in serum, hypothalamus, and yolk sac with age were investigated in Beijing-You (BY) and Arbor Acres (AA) male broilers during 11 d after hatch. The growth rate and feed intake of BY broilers were lower (P < 0.0001) than those of AA broilers, but the dynamics of the weights and total energy contents of yolk sacs were similar between both strains and decreased exponentially with age. Leptin levels in yolk sacs of both broiler strains increased with age during 3 d posthatching. Compared with those of AA broilers, leptin levels in yolk sacs of BY broilers were greater (P ≤ 0.0413) on d 0 and 3. There was no change in serum leptin levels in BY broilers, whereas in AA broilers, serum leptin levels on d 1 and 3 were greater (P ≤ 0.0306) than that on d 0 and then decreased with age. Compared with AA broilers, BY broilers showed lower (P ≤ 0.0254) levels of serum leptin on d 1 and 3. Hypothalamic leptin levels of both strains decreased with age except AA broilers on d 0. Hypothalamic neuropeptide Y (NPY) levels of BY and AA broilers increased with age until d 7 and then decreased. There were no differences in hypothalamic leptin and NPY levels between both strains during 11 d after hatch. Correlation analysis showed that average daily feed intake had a negative correlation with serum and hypothalamic leptin and positive correlation with hypothalamic NPY. Our results indicated that the dynamics of yolk sac utilization were similar between BY and AA broilers and decreased exponentially with age. The developmental changes of leptin and NPY in serum and hypothalamus with age varied in parameter and strain, and both signal molecules might be involved in the early programming of feed intake in chickens, but the mechanisms need further studies.

Key Words: yolk sac • feed intake • leptin • neuropeptide Y • broiler


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Leptin, the product of the ob gene, is a 16-kDa hormone that has been shown to play a key role in regulating feed intake and energy homeostasis in mammals (Friedman and Halaas, 1998). Leptin mediated its central effect through specific receptors located in the hypothalamus. Leptin receptors have been located on neurons producing neuropeptide Y (NPY), and when activated by leptin binding, it is hypothesized to function in part by downregulating the production of hypothalamic NPY (orexigenic effector) to inhibit ingestive behavior (Schwartz et al., 1998). Leptin and its receptor have also been cloned in chickens (Taouis et al., 1998; Horev et al., 2000). Unlike in mammals, chicken leptin is expressed in the liver besides adipose tissue, which is likely related to the primary role of the liver in avian lipid metabolism (Taouis et al., 1998; Ashwell et al., 1999). Several studies have showed that exogenous administration of leptin decreased feed intake in chicks, which is similar as described in mammals, but the an-orexigenic effect within chicken hypothalamus was mediated via selective neuropeptides, such as NPY and orexin (Denbow et al., 2000; Dridi et al., 2005).

Birds must undergo a posthatch transition period while moving from yolk sac dependence to utilization of exogenous feed. Many studies have depicted the time course of yolk sac utilization and its correlations to growth during the neonatal periods (Murakami et al., 1992; Noy and Sklan, 1999), but how the nutrient utilization of yolk sacs is regulated and how the appetite regulatory system is programmed at this stage remain unknown. Some studies have depicted the developmental changes of leptin and NPY during the embryonic and postnatal period in other animal species (Grove and Smith, 2003; McMillen et al., 2005), but there is a paucity of data in chicks. Genetic selection has introduced a wide variation in growth potential among different strains of broilers. Among the consequences of such selection is a major change in the regulation of feed intake and energy homeostasis (Cassy et al., 2004). Modern commercial broilers are prone to obesity resulting from hyperphagia when given free access to feed. However, the cause of the changes of regulating feed intake among different strains remains an enigma. Beijing-You (BY) broilers are a strain of Chinese local broilers with a slower growth rate compared with Arbor Acres (AA) broilers. Therefore, the present experiment was conducted to investigate the dynamics of yolk sac utilization and changes of leptin levels in serum, hypothalamus and yolk sacs, and hypothalamic NPY levels with age in male BY and AA broilers during 11 d after hatch.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
All procedures were approved by the Animal Care and Welfare Committee of the Chinese Academy of Agricultural Sciences. This experiment was conducted with 2 strains of commercial male broilers, namely commercial BY and AA broilers (feather-sexable yield). Two strains of fertilized eggs were obtained from the Institute of Animal Sciences in the Chinese Academy of Agricultural Sciences and local AA broiler hatchery, respectively. The breeders of 2 strains were 33 to 35 wk old, and the egg weights of BY and AA chicks were about 44 to 50 and 58 to 64 g, respectively. One thousand five hundred eggs of each strain were incubated under standard conditions (75% humidity at 37°C). To ensure that all the experimental broilers were out within a single hour, the hatching incubator was monitored at hourly intervals. During peak hatching, over 60% of the broilers emerged within the same hour, and from these broilers, 276 male broilers from each strain were subsequently selected. According to similar cage weight, 276 birds of each strain were randomly allocated to 12 electrically heated, thermostatically controlled cages with each of 23 birds, and broilers of each strain were replicated 6 times with 2 adjacent cages as 1 replicate. Immediately after they were allotted, 36 birds of each strain were selected for kill without access to feed and water, and the day was recorded as d 0 of the experiment. The remaining birds were given free access to feed and water (11 to 12 h after hatch) and were exposed to continuous lighting. The basal corn-soybean meal diet was formulated to meet nutrient requirements for broilers (Table 1Go). At 1, 3, 5, 7, 9, and 11 d of age posthatch, feed consumption and body weight were recorded for the whole group of birds per cage, and then average daily feed intake (ADFI) and weight gain per chicken per replicate were calculated. Relative daily weight gain was expressed as a percentage of average daily weight gain relative to body weight.


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  		Table 1. Composition of the basal diet
 
Sample Collections and Preparation

At 0, 1, 3, 5, 7, 9, and 11 d of age posthatch, 6 broilers from each replicate were selected according to the average body weight of the birds per cage, weighed individually, and killed by cervical dislocation. Except at d 0 killing, the birds were fasted for 2 h before being killed. The residual yolk sacs in the abdomen were excised and immediately weighed. Then, yolk sacs were frozen at –20°C for leptin and energy analysis. After killing, the hypothalamus was quickly dissected. Rostral and caudal hypothalamic boundaries corresponded to the optic chiasma and mamillary bodies, respectively. Relative yolk sac weight was expressed as a percentage of the absolute yolk sac weight (AYW) relative to body weight.

Sample Assays

Energy content of yolk sac was determined with a Parr 1281 bomb calorimeter (Parr Instrument Co., Moline, IL). Serum glucose was measured by the glucose oxidase method (Beckman analyzer II, Beckman, Fullerton, CA). Serum leptin concentration was determined with multispecies leptin RIA kits from Linco Inc. (St. Charles, MO; Dridi et al., 2000). The sensitivity was 1.0 ng/mL, and the intra- and interassay coefficients of variation were below 10%. Leptin was extracted from the yolk sac and hypothalamus by using an extraction buffer (1% Triton X-100, 0.3 M NaCl, 1 mM EDTA, 0.05 M Tris, pH 7.4) with complete protease inhibitor cocktail (1 tablet/10 mL, Boehringer Mannheim, Indianapolis, IN; Barr et al., 1997). Leptin levels in the extracts were determined according to the method for serum hormone assays. For NPY assays, hypothalamic samples were homogenized by an electric homogenizer in 1 M acetic acid. After centrifugation, aliquots of supernatants were stored at –80°C until use. Hypothalamic NPY level was determined by RIA kits following the instructions of the manufacturer (Phoenix Pharmaceuticals, Belmont, CA), with intra- and interassay coefficients of variation below 10%. Protein concentration in the extract was measured by the method of Bradford (1976).

Statistical Analysis

Statistical analyses of the data were performed by ANOVA (1-way ANOVA and Duncan’s multiple range test), Student’s t-test, and regression analysis using the SAS 6.03 statistical software (SAS Institute, 1989). Statements of significance were based on P < 0.05.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
There were significant differences (P < 0.0001) in initial body weight and early growth performance between BY and AA broilers. On d 0 posthatching, average body weight of AA broilers (38.9 ± 0.23 g) was greater (P < 0.0001) than that of BY broilers (29.5 ± 0.28 g). The AA broilers grew faster, at least partially due to their greater feed intake. During 11 d posthatching, ADFI and relative daily weight gain of AA broilers were greater (P ≤ 0.0004) than those of BY broilers of the same age (Figure 1Go and 2Go).


Figure 1
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  		Figure 1. Average daily feed intake (ADFI) as a function of age in newly hatched Beijing-You (BY) and Arbor Acres (AA) broilers. Equations are as follows: BY broiler: y = 1.65x + 3.54 (R2 = 0.982, P = 0.0001); AA broiler: y = 3.62x + 1.78 (R2 = 0.997, P < 0.0001), where y = ADFI (g) and x = days after hatch.

 

Figure 2
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  		Figure 2. Relative daily weight gains in newly hatched Beijing-You (BY) and Arbor Acres (AA) broilers.

 
Yolk sac utilization was almost completed before 7 d posthatching (Figure 3AGo). On d 0 posthatching, the AYW of BY broilers were significantly lower (about 34%) than those of AA broilers, but this difference between strains decreased gradually with age. A similar phenomenon was observed in total energy content of fresh yolk sac (Figure 4Go). The AYW and total energy contents of yolk sacs of BY and AA broilers decreased exponentially with age. Changes of the relative yolk sac weight of 2 broiler strains with age were similar to those of the AYW, but the differences between strains disappeared (Figure 3BGo).


Figure 3
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  		Figure 3. (A) Absolute and (B) relative weights of yolk sacs as a function of age in newly hatched Beijing-You (BY) and Arbor Acres (AA) broilers. Equations are as follows: BY broiler: y1 = 3.105e–0.407x (R2 = 0.977, P < 0.0001); y2 = 10.142e–0.547x (R2 = 0.988, P < 0.0001); AA broiler: y1 = 4.516e–0.344x (R2 = 0.934, P = 0.0004); y2 = 11.447e–0.525x (R2 = 0.970, P < 0.0001), where y1 = absolute weight of yolk sac (g); y2 = relative weight of yolk sac (%); and x = days after hatch.

 

Figure 4
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  		Figure 4. Total energy contents of yolk sacs as a function of age in newly hatched Beijing-You (BY) and Arbor Acres (AA) broilers. Equations are follows: BY broiler: y = 35.570e–0.505x (R2 = 0.959, P = 0.0035); AA broiler: y = 57.343e–0.433x (R2 = 0.991, P = 0.0004), where y = total energy contents of yolk sac (kJ) and x = days after hatch.

 
Serum glucose in BY broilers stayed at a low level during 3 d after hatch, increased significantly on d 5, and then decreased (Figure 5AGo). But, no difference was observed in serum glucose of AA broilers during 11 d after hatch. Compared with AA broilers, BY broilers showed significantly greater levels of serum glucose only on d 5 (P = 0.0157). There was no change in serum leptin levels in BY broilers (Figure 5BGo), whereas in AA broilers, serum leptin levels on d 1 and 3 were greater than those on d 0 (P ≤ 0.0306) and then decreased with age. Compared with BY broilers, AA broilers showed greater levels of serum leptin on d 1 and 3 (P ≤ 0.0254). Hypothalamic leptin levels in BY broilers gradually decreased with age during the postnatal period, whereas in AA broilers, hypothalamic leptin level on d 1 was greater than that on d 0 (P = 0.0017) and then decreased with age (Figure 6AGo). Changes of hypothalamic NPY levels with age were similar between both strains, with an increase with age until d 7 followed by a decrease (Figure 6BGo). There were no differences in hypothalamic leptin and NPY levels between both strains during 11 d after hatch. Correlation analysis showed that serum and hypothalamic leptin of both strains had a negative relation with ADFI, whereas hypothalamic NPY had a positive relation with ADFI (Table 2Go).


Figure 5
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  		Figure 5. Changes of (A) serum glucose and (B) leptin levels in Beijing-You (BY) and Arbor Acres (AA) broilers with age during 11 d after hatch. Means with different letters (capital letters for BY broilers and lowercase letters for AA broilers) differ significantly among ages but in the same line (P < 0.05). An asterisk indicates significant differences between lines at the same age (P < 0.05); n = 6.

 

Figure 6
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  		Figure 6. Changes of (A) hypothalamic leptin and (B) neuropeptide Y (NPY) levels in Beijing-You (BY) and Arbor Acres (AA) broilers with age during 11 d after hatch. Means with different letters (capital letters for BY broilers and lowercase letters for AA broilers) differ significantly among ages but in the same line (P < 0.05). An asterisk indicates significant differences between lines at the same age (P < 0.05); n = 6.

 

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  		Table 2. Correlation analysis between average daily feed intake (ADFI) and serum and hypothalamic leptin and hypothalamic neuropeptide Y (NPY) of Beijing-You (BY) and Arbor Acres (AA) broilers
 
Leptin levels in yolk sacs were determined only during the first 3 d posthatching in the present experiment, due to the sample amount. During the first 3 d post-hatching, leptin levels in yolk sacs of both BY and AA broilers on d 3 were greater (P ≤ 0.0038) than those on d 0 and 1, but there was no difference (P ≥ 0.7337) between 0 and 1 d (Figure 7Go). Compared with those of AA broilers, leptin levels were greater in yolk sacs of BY broilers at the same age, and there were significant differences (P ≤ 0.0413) on d 0 and 3.


Figure 7
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  		Figure 7. Leptin levels of yolk sacs in Beijing-You (BY) and Arbor Acres (AA) broilers at different ages. Means with different letters (capital letters for BY broilers and lowercase letters for AA broilers) differ significantly among ages but in the same line (P < 0.05). An asterisk indicates a significant difference (P < 0.05) between BY and AA broilers at a given age; n = 6.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
In the present experiment, growth performance between the 2 strains during the postnatal period significantly differed, whereas the similar dynamics of growth and yolk sac utilization were observed in BY and AA broilers. The weights and total energy contents of yolk sacs of both strains declined exponentially with age, which agreed with the previous results (Murakami et al., 1992; Noy and Sklan, 1999). It is well known that yolk sac is vital to the early growth of newly hatched chicks; however, the mechanisms regulating the nutrient utilization of yolk sacs remain an enigma. Leptin has been shown to regulate energy metabolism in rodents (Halaas et al., 1995; Pelleymounter et al., 1995). Leptin injections increased energy expenditure and decreased fat mass, without affecting lean body mass (Halaas et al., 1995; Pelleymounter et al., 1995), and leptin could increase muscle fatty acid oxidation and decrease esterification into muscle triacylglycerol, both in vivo and in vitro (Muoio et al., 1997; Shimabukuro et al., 1997). Furthermore, leptin mRNA expression was also found in the yolk sac membrane of chick embryos at 17 d of age besides hepatic and adipose tissue (Ashwell et al., 1999). The present experiment also showed that leptin immunoactivity was present in the yolk sacs of newly hatched broilers, and its levels varied with age and strain. This suggests that leptin might be involved in the regulation of yolk sac utilization, but further studies are needed to elucidate the mechanisms.

As a hormonal sensing mechanism for fat deposition and energy homeostasis, leptin plasma levels increased with age in hens with a maximum level in adult hens at the first egg, which was also correlated with the developed adiposity at this stage (Dridi et al., 2000). But, this phenomenon did not occur in neonatal and young chicks. Plasma concentrations of leptin in Ross broilers did not change significantly during the first 35 d of life despite dramatic changes in body weight (Cassy et al., 2004). The present results also showed that serum leptin levels of BY broilers had no statistic differences during 11 d after hatch, whereas serum leptin levels of AA broilers on d 1 and 3 were significantly greater than that on other days. This suggests that the differences in the timing and magnitude of the neonatal peak in blood leptin were associated with strain and age of the bird.

Circulating leptin is influenced by nutritional state, being significantly lower in the fasted state than in the fed state. This suggests that there is a compensatory mechanism of regulating feed intake (Dridi et al., 2000). In the present experiment, serum leptin levels of AA broilers on d 0 (before ingesting) were significantly lower than those on d 1 (after ingesting), which was also seen in hypothalamic leptin of AA broilers. These data suggest that leptin might be involved in the early programming of appetite regulation in the chickens, but for functionality of this factor, injection trials are needed. In addition, there was no difference in serum and hypothalamic leptin in BY broilers during the postnatal period. It is difficult to explain this phenomenon, and whether it is associated with strain or others needs further studies.

In the present experiment, hypothalamic leptin immunoactivity was determined by RIA, which has never been reported before. Only Morash et al. (1999) has reported that leptin mRNA was selectively transcribed in specific areas of rat brain using reverse transcription PCR, and leptin mRNA expression in the hypothalamus was suppressed by fasting (48 h). The present study also showed that hypothalamic leptin levels of BY and AA broilers decreased with age during the postnatal period and that serum and hypothalamic leptin had a negative correlation with ADFI, which confirms its function of decreasing feed intake (Dridi et al., 2005).

The development of the hypothalamic appetite regulatory network in rodents occurs predominantly after birth (Grove and Smith, 2003). Although NPY was present within the hypothalamic arcuate nuclei of the fetal rat from as early as 14.5 d of gestation, NPY projections between the arcuate nuclei and dorsomedial nucleus were not complete until 10 to 11 d after birth, and NPY containing projections to the paraventricular nucleus did not fully develop until around 15 to 16 d (Grove and Smith, 2003). However, in sheep and human, NPY projections were present in the fetal para-ventricular nucleus during late gestation (Warnes et al., 1998; Koutcherov et al., 2002). No data has ever been reported in chicken embryos before, but as an oviparous animal, we could speculate that the central system of regulating energy homeostasis might be present during the development of chick embryos and play an important role in the early programming of appetite in chickens. Neuropeptide Y and leptin receptor mRNA were expressed in the chicken brain at hatch (Cassy et al., 2004), and the present study also showed that NPY was highly expressed in the hypothalamus of the broilers at hatch. These data partially support the above hypothesis, but further studies in vivo are needed. In the present experiment, changes of hypothalamic NPY levels with age were similar between BY and AA broilers, with an increase with age until d 7 but then a decrease. There was a positive correlation between hypothalamic NPY and ADFI, which agreed to its function of promoting feed intake (Schwartz et al., 1998). These data suggested that NPY might be involved in the early programming of feed intake in chickens, but injection trials are needed to elucidate it.

The difference in feed intake observed between both strains could not be associated with serum and hypothalamic leptin levels and hypothalamic NPY levels, because no constant differences were observed between both strains during 11 d after hatch. Control of feed intake is complex and involves many different messengers, including central and peripheral signal molecules, and the complexity of their potential interactions has only started to be appreciated. A better understanding of the detailed mechanisms underlying the regulation of feed intake and body weight between strains is needed to develop new approaches.

In conclusion, the dynamics of yolk sac utilization in both BY and AA broilers were similar, with a decline in an exponential way with age. The developmental changes of serum and hypothalamic signal molecules with age varied in parameter and strain. Leptin and NPY might be involved in the early programming of feed intake in chickens, but the mechanisms need further studies.


   FOOTNOTES
 
1 Supported by the National Basic Research Program of China (Project No. 2004CB117501; Beijing, P. R. China), Basic Science Research Program (Project No. ywf-td-4; Beijing, P. R. China), and Chinese Academy of Agricultural Sciences Foundation for First-Place Outstanding Scientists (Chinese Academy of Agricultural Sciences, Beijing, P. R. China). Back

Received for publication November 15, 2007. Accepted for publication July 8, 2008.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
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