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The Effect of Nonventilation During Early Incubation on the Embryonic Development of Chicks of Two Commercial Broiler Strains Differing in Ascites Susceptibility

L. De Smit^*,1, V. Bruggeman^*, M. Debonne^*, J. K. Tona^*,, B. Kamers^*, N. Everaert^*, A. Witters^*, O. Onagbesan^*, L. Arckens, J. De Baerdemaeker and E. Decuypere^*

^* Lab of Physiology of Domestic Animals, Katholieke Universiteit Leuven, Kasteelpark Arenberg 30, 3000 Leuven, Belgium; Department of Animal Production, School of Agriculture, University of Lome 1515, Togo; Lab of Neuroplasticity and Neuroproteomics, Katholieke Universiteit Leuven, Naamsestraat 59, 3000 Leuven, Belgium; and Lab of AgroMachinery and Processing, Katholieke Universiteit Leuven, Kasteelpark Arenberg 30, 3000 Leuven, Belgium

¹ Corresponding author: Lieve.desmit{at}biw.kuleuven.be

	ABSTRACT

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Despite thorough selection during the last decade, the incidence of ascites is still high in modern broiler strains. Although ascites occurs mostly at the end of the rearing period, there are indications that the etiology of this problem may have started during embryonic development. Recent studies have shown that the post-hatch performance of the broiler chick might be influenced by changing the environmental conditions in the incubator during embryonic development. This study investigated the effect of increasing incubator CO₂ concentration up to 0.7%, by nonventilation during the first 10 d of incubation, on the embryonic development of 2 commercial broiler strains (Cobb and SAS) differing in their susceptibility for ascites syndrome. The Cobb strain is suspected to be less susceptible than the SAS strain. Overall, the chick embryos of the Cobb strain had a faster development than those of the SAS strain as expressed by their higher BW from embryonic day (ED)10 until ED18. Nonventilation stimulated embryonic development resulting in higher embryonic BW, early hatch, and narrower spread of hatch in both strains. In the SAS strain, nonventilation improved hatchability by more than 10%. Gas composition of the air cell in the egg of the nonventilation groups (both Cobb and SAS) had higher partial pressure of CO₂ and lower partial pressure of O₂ from ED11 until ED14 compared with the ventilation groups. During the entire incubation period, partial pressure of CO₂ was higher in eggs of the Cobb strain compared with the SAS strain. Plasma triiodothyronine, thyroxine, and corticosterone levels were different at the end of the incubation period and during hatching due to nonventilation at the beginning of incubation. It is concluded that nonventilation during the first 10 d of incubation had a stimulatory effect on embryonic development of the 2 broiler strains with no effect of heart weights but with effects on hormone levels, air cell pressures, and hatching parameters.

Key Words: ascites • broiler • embryonic development • incubation

	INTRODUCTION

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Modern commercial broilers are the result of intensive and focused selection over many years. They are highly efficient and grow fast (Havenstein et al., 2003). This long-term selection for production traits has also led to higher incidence of ascites syndrome with negative effect on production and animal welfare. This metabolic disease results from an imbalance between the high oxygen requirement necessary to satisfy the metabolic demands of their rapid growth rates and the insufficient oxygen supply due to the proportionally underdeveloped cardiovascular and pulmonary system (Decuypere et al., 2000; Julian, 2000). To prevent ascites syndrome in commercial broiler flocks, special attention must be paid to the proper management of these highly productive animals. This includes restricting food intake during the early growth period and the imposition of optimal temperature and lighting schedules (Decuypere et al., 2000). Despite all these precautionary measures, ascites is still 1 of the major causes of economic loss in broiler industry (Maxwell and Robertson, 1998; Kinung’hi et al., 2004). The peak mortality due to ascites occurs at the end of the growth period, but it is thought that the etiology of this disease might have existed at embryonic development (Coleman and Coleman, 1991).

Following selection for fast and efficient growth, the vision on adequately incubating the eggs of these commercial broilers has evolved during the last decade. Until some years ago, a large part of commercial incubations was done using the multistage system; today the incubation of broiler eggs has become a highly controlled process during which temperature, humidity, oxygen, and CO₂ concentrations create the optimal environment for embryonic development. Our recent studies have focused on the CO₂ concentration in the incubator. The composition of the ambient gaseous environment in the incubator plays an important role during embryonic development, and by manipulating the incubation conditions, we have been able to influence the developmental trajectories of the chick embryo. In these studies (De Smit et al., 2006; Tona et al., 2007), we showed that increased CO₂ concentrations in the incubator by nonventilation during the first 10 d of incubation increased the performance of the chick embryo and even had beneficial effects on post-hatch growth.

Besides the environmental incubation conditions, the genetic background of the chick also influences the embryonic developmental pathway. Chickens selected for various posthatch characteristics differ also in their embryonic developmental trajectories (Clum et al., 1995). Studies comparing broilers from lines differing in ascites susceptibility (Dewil et al., 1996; Buys et al., 1998; De Smit et al., 2005) showed that these chicks differed in embryonic characteristics. Chicks of ascites-sensitive lines hatched later, had lower thyroid hormone concentrations, and lower partial pressure of CO₂ (pCO₂) and higher partial pressure of O₂ (pO₂) in the air cell during the late stages of embryonic development. In a previous study (De Smit et al., 2006), we showed that embryonic BW, hatching time, and gas composition of the air cell were influenced by incubating the eggs under nonventilated conditions during the first 10 d of incubation. The aim of this current study was to investigate the responses of the chick embryos of 2 commercial broiler lines, varying in ascites susceptibility and posthatch growth pattern, to nonventilation during the first 10 d of incubation.

	MATERIALS AND METHODS

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Broilers

Broilers of 2 genetic stocks, which are assumed to differ in ascites susceptibility, were used. The SAS (sire line ascites-sensitive)-Hybro strain is a pure broiler sire line, fast feathering, and selected for high breast muscle weight and low feed conversion. This strain was characterized in previous studies by De Smit et al. (2005) and Tona et al. (2005). Broilers from the SAS strain are highly susceptible for ascites syndrome. The second group of broilers is the commercially available Cobb broilers, which are suspected to be less susceptible to ascites than those of the SAS strain.

Experimental Design

Two thousand four hundred broiler eggs from the 2 commercial strains [1,200 Cobb eggs collected from 39-wk-old broiler breeders (Belgabroed, Hoogstraten, Belgium) and 1,200 SAS-Hybro eggs collected from 43-wk-old broiler breeders (Boxmeer, the Netherlands)] were incubated in 2 different incubation rounds. Half of the eggs (600) from each strain were incubated in a nonventilated incubator [nonventilated (NV) group] during the first 10 d of embryonic development. This allowed the CO₂ level in the incubator to rise from 0.05% at the beginning of incubation to 0.7% at embryonic day (ED)10. The other half of the eggs were incubated in a standard ventilated incubator [ventilated (V) group]. The CO₂ concentration in this incubator remained constantly below 0.1%. The CO₂ concentration and humidity in both incubators were constantly monitored using a computerized system with a CO₂ sensor (Vaisala GMM221, Waarloos, Belgium; Figure 1). The humidity in both incubators (PasReform, Zeddam, the Netherlands) was matched based on wet bulb temperature to prevent differences in egg weight loss. At ED10, the eggs of the different groups were randomly mixed and divided over the 2 incubators that were used in this experiment. Incubation was continued as a ventilated incubation in both incubators. Other incubation conditions were the same for both incubators during the entire incubation process. The specific dry bulb temperature was 37.6°C, and the wet bulb temperature was 29°C; the eggs were turned once every hour at an angle of 90°. This research protocol was approved by the Ethical Commission for Experimental Use of Animals of the Katholieke Universiteit Leuven.

View larger version (9K): [in this window] [in a new window]   Figure 1. Evolution of the CO2 concentration in the ventilated and nonventilated incubator during the first 10 d of incubation.

From ED10 until hatch, 15 eggs per group were used to determine the yolk-free embryonic BW and the heart weight. From these measurements, the relative heart to BW was determined as the ratio of the heart weight to the yolk-free embryonic BW x 100.

At d 18 of incubation, all eggs were candled, and those with evidence of a living embryo were placed in hatching baskets. From 456 to 504 h, hatching eggs were checked individually every 2 h for internal pipping (IP), external pipping (EP), and hatching. The time interval between EP-IP, hatch-IP, and hatch-EP was calculated. Hatching percentage was calculated as hatched chicks to fertile eggs.

Blood and Gas Sampling

From ED10 until hatch, 15 eggs per group were used daily for gas pressure measurements and to collect blood samples. Gas pressure was measured directly in the air cell of the eggs by means of a blood gas analyzer (Type 1610; Instrumentation Laboratories, Zaventem, Belgium) for the measurement of pCO₂ and pO₂. This was done by drilling a small hole in the shell just above the air cell with an 18-gauge needle. The needle of the blood gas analyzer was immediately inserted through the hole into the air cell, and the gas was analyzed. This method for measuring gas partial pressures in the air cell has previously been described by Dewil et al. (1996), Buys et al. (1998), and Tona et al.(2003).

Blood Parameters

From ED10 until hatch, blood samples were also collected from the same embryos that were used for gas pressure measurements. From ED10 until ED17, blood samples were taken from the chorioallantoic artery. From ED18 until hatch, blood sampling was done by cardiac puncture. Two hours after IP was observed, blood samples were collected from chicks. At EP and hatch, blood samples were taken directly after these events. Blood samples were collected into heparinized tubes. Blood samples were centrifuged, and plasma was collected and stored at –20°C until the determination of triiodothyronine (T₃), thyroxine (T₄), and corticosterone levels. All samples were run in the same assay to avoid interassay variability.

The T₃ and T₄ concentrations were measured in plasma samples by RIA as described previously (Huybrechts et al., 1989; Darras et al., 1992). Antisera and T₃ and T₄ standards were purchased from Byk-Belga (Brussels, Belgium). Intraassay CV were 3.54 and 3.5% for T₃ and T₄, respectively. Corticosterone concentration in plasma samples were measured using a commercially available double-antibody RIA kit from IDS Ltd. (Boldon, UK) as described by Decuypere et al. (1983) and Meeuwis et al. (1989). Intraassay CV was 1.76%.

Statistical Analyses

The data were processed with the statistical software package SAS version 8.2 (SAS Institute Inc., Cary, NY). All values are expressed as mean ± SEM. A GLM was used to analyze incubation duration, embryonic heart weight and BW, gas pressure in the air cell, and plasma T₃, T₄, and corticosterone levels in relation to strain and incubation conditions. When the means of the general model were statistically different, then these means were further compared using Tukey’s test. Significance was based on P < 0.05. The model was:

where Y_ijk = incubation duration, embryonic heart weight, embryonic BW, gas pressure in the air cell, or plasma T₃, T₄, and corticosterone levels of egg k from incubator ventilation i and broiler strain j according to incubation stage; µ = the overall mean; _i = the main effect of incubator ventilation I; _j = the main effect of broiler strain; ()_ij = the interaction between incubator ventilation and broiler strain; and e_ijk = the random error term.

Data of hatching percentage were analyzed using a logistic regression model. The goodness of fit was estimated with the Homer-Lemshow goodness of fit test.

	RESULTS

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Egg and Embryo Weight

At setting, the average egg weight of the Cobb strain was higher than that of the SAS strain (P = 0.0124). Within each strain, egg weights did not differ between the ventilated and the nonventilated incubation group. At setting, the weights of the ventilated and nonventilated Cobb eggs were 68.03 ± 0.24 g and 67.81 ± 0.25 g, respectively. For the SAS strain, the average weights were 67.63 ± 0.29 g for the ventilated and 66.92 ± 0.25 g for the nonventilated eggs.

From ED10 until IP, the chick embryos of the Cobb strain had a higher embryonic BW than those of the SAS line (P < 0.0001; Table 1). From ED10 until ED18, a higher average BW (P < 0.0001) was observed for the chicks of the nonventilated incubation compared with those of the ventilated incubation. At hatch, no differences in BW were observed between the groups (Table 1). The small differences in egg weights between the Cobb and SAS strains had no significant influence on the difference in BW (data not presented). Relative heart weights did not differ between the chick embryos of the ventilated and the nonventilated incubation, but overall, the chick embryos of the Cobb strain had lower (P < 0.0001) relative heart weight than the SAS embryos (Table 2).

During the second half of incubation, from ED10 until IP, the gas pressure in the air cell was measured daily (Table 3). The pCO₂ increased and the pO₂ decreased in all groups toward the end of incubation (P < 0.0001). From ED11 until ED14, the pCO₂ was higher in the eggs of the NV group compared with that of the V group. During the entire incubation period, pCO₂ was higher in the eggs of the Cobb strain compared with the SAS strain. The pO₂ was significantly lower in the air cell of the eggs from the NV groups compared with the V group from ED11 until ED14. From ED12 until ED18, a lower pO₂ was measured in the air cell of the eggs of the Cobb strain compared with those of the SAS strain.

Overall hatchability was lower in the SAS strain than in the Cobb strain (P < 0.0001). No significant difference was observed between ventilated and nonventilated incubation, but the nonventilated incubation conditions improved the hatchability in the SAS strain (P = 0.0237). Hatch of fertile eggs was more than 11% higher in the SAS-NV group (88.00%) compared with the SAS-V group (76.84%; Figure 2).

View larger version (12K): [in this window] [in a new window]   Figure 2. Hatchability (%) of chicks from the Cobb and SAS strains according to nonventilated (NV) and ventilated (V) incubation during the first 10 d of incubation. Data sharing no common letter are significantly different (P < 0.05).

View larger version (19K): [in this window] [in a new window]   Figure 3. Spread of hatch of the chicks of the nonventilated (NV) and the ventilated (V) group of the Cobb and the SAS strain.

Table 6 shows the plasma T₃ and T₄ from ED17 until hatch. There was a significant effect of age (P < 0.0001) and strain (P < 0.0012) on the plasma T₃ concentration. The chicks of the Cobb strain had higher plasma T₃ levels than those of the SAS strain. There was no overall significant effect of incubation ventilation on the T₃ concentration, but at IP, the chicks of the NV group showed a trend toward higher plasma T₃ level than the V group. At hatch, there was an interaction between strain and incubation (P = 0.0070). Plasma T₄ levels were significantly different between strains (P < 0.0001) and ages (P < 0.0001). Chicks of the Cobb strain had higher plasma T₄ levels than those of the SAS strain. Incubation ventilation had no significant effect on plasma T₄ levels. The levels of corticosterone (Figure 4) were significantly influenced by strain (P < 0.0001), incubation ventilation (P < 0.0001), and embryonic age (P < 0.0001). Chick embryos from the Cobb strain had higher plasma corticosterone levels than the embryos from the SAS strain. Nonventilation at the beginning of incubation resulted in higher levels of corticosterone. Corticosterone levels increased sharply from ED11 to ED17 of the normal V incubation followed by a slow rise until IP or hatch. The NV incubation shifted the end point of this early sharp rise in corticosterone forwards to ED15 in Cobb and SAS. Additionally, the maximal level of corticosterone was lower in the NV group of the Cobb compared with V group of the Cobb, whereas this was not affected in the SAS strain.

View larger version (30K): [in this window] [in a new window]   Figure 4. Plasma corticosterone levels (ng/mL) during embryonic development (n = 15). NV = nonventilated; V = ventilated.

	DISCUSSION

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Differences in partial pressures of CO₂ and O₂ in the air cell were most probably the result of the higher metabolic rate of the NV compared with the V chicks. The higher air cell gas values in the Cobb compared with the SAS also point to a higher metabolic rate culminating in a higher BW and an overall faster development. Visschedijk (1968) showed that a higher pCO₂ at IP was also a stimulus for hatching. This was confirmed in the current study by the earlier hatching of the Cobb compared with the SAS chicks.

Scott et al. (1981) reported that plasma corticosterone levels start to increase from ED10 and that after ED14 there was a sharp rise until ED16. Around ED15, the adeno-hypophyseal-adrenal axis is established, and from this point onwards, the production of corticosterone is regulated by feedback mechanisms. The results of our experiment are in agreement with those of Kalliecharan and Hall (1974) and Scott et al. (1981). The plasma corticosterone levels increased until ED17, after which they became stable until hatch. The NV chicks of the Cobb strain reached stable plasma corticosterone concentrations earlier (around ED15) than those of the V group (around ED17). Moreover, in the days before they reached this plateau, the chicks of the NV group had higher corticosterone levels than those of the V group. This can possibly be explained by the overall faster embryonic development of the chick embryos of the NV group, whereas the increase in plasma corticosterone level until ED16 might depend on the number of secretory cells in the adrenal cortex, which exponentially increases around ED13 and ED14 (Girouard and Hall, 1973). Blacker et al. (2004) measured higher levels of surfactant lipids in chick embryos incubated under conditions of hypoxia compared with control chicks, and this was accompanied with an earlier pipping in 29.5% of these hypoxic chicks. Early elevated levels of corticosterone are the likely cause of these changes in the surfactant lipid concentrations (Hylka and Doneen, 1983). A faster development of the surfactant system results in a faster maturation of the lungs, and the latter might explain the differences in hatching time. Indeed, plasma corticosterone concentrations started to increase earlier in Cobb embryos compared with the SAS embryos and in the NV embryos compared with the embryos of the V group. The same difference was found in pipping and hatching time; the NV chicks hatched earlier than the V chicks, and the chicks of the Cobb strain were faster than those of the SAS strain. The latter is in agreement with earlier studies that have shown that chicks from ascites-sensitive strains hatch later compared with ascites-resistant strains (Dewil et al., 1996; Buys et al., 1998; Tona et al., 2005).

Concomitantly with the higher corticosterone levels, the chicks from the Cobb strain also had higher plasma T₃ and T₄ levels compared with the SAS strain during the last days of their incubation period. Longer incubation periods have been related to depressed embryonic thyroid function (McNabb et al., 1989; Christensen et al., 2002). Dewil et al. (1996) found that chicks of ascites-resistant lines hatched early compared with ascites-sensitive lines and linked this to higher embryonic thyroid activity. In all groups, T₃ increased sharply at IP, a period of transition from chorioallantoic to pulmonary respiration. At IP, there was a trend for higher T₃ concentrations in the chicks of the NV group compared with the V group. These results are similar to previous findings of Buys et al. (1998), who reported increased plasma T₃ in embryos incubated under increased CO₂ concentrations. This increase in T₃ could also be due to higher corticosterone levels that act as a stimulator of the thyroid metabolism (Decuypere et al., 1983; De Groef et al., 2006). Plasma T₄ concentrations increased during the final days of incubation, reaching their maximum at IP for the SAS- and the Cobb-NV group and at hatch for the Cobb-V group. The interval between IP (the start of pulmonary respiration) and hatching is thyroxin-dependent (Decuypere et al., 1991); thus, the shorter interval between IP and hatch for the chicks of the Cobb-NV group compared with the other groups might be explained by their higher plasma thyroxin concentrations until the moment of IP.

Hatchability was improved in the group of the SAS strain incubated under nonventilated conditions. The lower hatching percentage of the SAS-V group was mainly due to more of late deads (after ED18) or chicks that did not finish their hatching and got stuck at the phase of internal or external pipping. This enhanced hatchability due to nonventilation in the beginning of incubation for groups with a low control hatchability was also reported by others (Hogg, 1997; De Smit et al., 2006; Tona et al., 2007).

From this study, we can conclude that nonventilation during the first 10 d of incubation resulting in increased levels of CO₂ in the incubator has a stimulatory effect on embryonic development in the 2 broiler strains differing in their susceptibility for ascites syndrome. The timing and the time intervals of the hatching process were changed and could be brought into relation with the changes in air cell gasses and hormones. Hatchability was improved in the SAS strain and was due to the higher levels of CO₂ in the incubator. Further research will be necessary to reveal the effect of nonventilation during incubation on the prevalence of ascites syndrome during the posthatch growing period.

	ACKNOWLEDGMENTS

 
We thank G. Nackaerts and I. Vaesen (Faculty of Bioscience Engineering, Katholieke Universiteit Leuven) for their skilled technical assistance. Lieve De Smit was supported by the Fund for Scientific Research Flanders (FWO-Vlaanderen, Brussels, Belgium; G0286.04). K. Tona was granted a fellowship from the Vlir (Vlaamse Universitaire Raad, Brussels, Belgium). V. Bruggeman is a postdoctoral fellow from the FWO-Vlaanderen.

Received for publication August 1, 2007. Accepted for publication November 18, 2007.

	REFERENCES

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Blacker, H. A., S. Orgeig, and C. B. Daniels. 2004. Hypoxic control of the development of the surfactant system in the chicken: Evidence for physiological heterokairy. Am. J. Physiol. Regul. Integr. Comp. Physiol. 287:403–410.

Buys, N., E. Dewil, E. Gonzales, and E. Decuypere. 1998. Different CO₂ levels during incubation interact with hatching time and ascites susceptibility in two broiler lines selected for different growth rate. Avian Pathol. 27:605–612.[Medline]

Christensen, V. L., G. S. Davis, and K. Nestor. 2002. Environmental incubation factors influence embryonic thyroid hormones. Poult. Sci. 81:442–450.[Abstract/Free Full Text]

Clum, N. J., D. K. McClearn, and G. F. Barbato. 1995. Comparative embryonic development in chickens with different patterns of postnatal growht. Growth Dev. Aging 59:129–138.[Web of Science][Medline]

Coleman, M. A., and G. E. Coleman. 1991. Ascites control through proper hatchery management. Misset World Poult. 7:33–35.

Darras, V. M., L. R. Berghman, A. Vanderpooten, and E. R. Kuhn. 1992. Growth hormone acutely decreases type III iodothyronine deiodinase in chicken liver. FEBS Lett. 310:5–8.[CrossRef][Web of Science][Medline]

Decuypere, E., J. Buyse, and N. Buys. 2000. Ascites in broiler chickens: Exogenous and endogenous structural and functional causal factors. World’s Poult. Sci. J. 56:367–377.[CrossRef][Web of Science]

Decuypere, E., E. Dewil, and E. R. Kühn. 1991. The hatching process and the role of hormones, Pages 239–256 in Avian Incubation. Butterworth & Co., London, UK.

Decuypere, E., C. G. Scanes, and E. R. Kühn. 1983. Effect of glucocorticoids on circulating concentrations of thyroxine (T₄) and triiodothyronine (T₃) and on peripheral monodeiodination in pre- and post-hatching chickens. Horm. Metab. Res. 15:233–236.[Web of Science][Medline]

De Groef, B., S. Grommen, and V. Darras. 2006. Increasing plasma thyrocine levels during late embryogenesis and hatching in the chicken are not caused by increased sensitivity of the thyrotropes to hypthalamic stimulation. J. Endocrinol. 189:271–278.[Abstract/Free Full Text]

De Smit, L., V. Bruggeman, J. K. Tona, M. Debonne, O. Onagbesan, L. Arckens, J. De Baerdemaeker, and E. Decuypere. 2006. Embryonic developmental plasticity of the chick: Increased CO(2) during early stages of incubation changes the developmental trajectories during prenatal and postnatal growth. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 145:166–175.[CrossRef][Medline]

De Smit, L., K. Tona, V. Bruggeman, O. Onagbesan, M. Hassanzadeh, L. Arckens, and E. Decuypere. 2005. Comparison of three lines of broilers differing in ascites susceptibility or growth rate. 2. Egg weight loss, gas pressures, embryonic heat production, and physiological hormone levels. Poult. Sci. 84:1446–1452.[Abstract/Free Full Text]

Dewil, E., N. Buys, G. A. A. Albers, and E. Decuypere. 1996. Different characteristics in chick embryos of two broiler lines differing in susceptibility to ascites. Br. Poult. Sci. 37:1003–1013.[CrossRef][Web of Science][Medline]

Girouard, R. J., and B. K. Hall. 1973. Pituitary-adrenal interaction and growth of the embryonic avian adrenal gland. J. Exp. Zool. 183:323–331.[CrossRef][Web of Science][Medline]

Hassanzadeh, M., H. Gilanpour, S. Charkhkar, J. Buyse, and E. Decuypere. 2005. Anatomical parameters of cardiopulmonary system in three different lines of chickens: Further evidence for involvement in ascites syndrome. Avian Pathol. 34:188–193.[CrossRef][Web of Science][Medline]

Havenstein, G. B., P. R. Ferket, and M. A. Quereshi. 2003. Growth, livability, and feed conversion of 1957 versus 2001 broilers when fed representative 1957 and 2001 broiler diets. Poult. Sci. 82:1500–1508.[Abstract/Free Full Text]

Hogg, A. 1997. Single stage incubation trails. Avian Poult. Biol. Rev. 8:168. (Abstr.)

Huybrechts, L. M., R. Michielsen, V. M. Darras, F. C. Buonomo, E. R. Kuhn, and E. Decuypere. 1989. Effect of the sex-linked dwarf gene on thyrotrophic and somatotrophic axes in the chick embryo. Reprod. Nutr. Dev. 29:219–226.[CrossRef][Web of Science][Medline]

Hylka, V. W., and B. A. Doneen. 1983. Ontogeny of embryonic chicken lung: Effects of pituitary gland, corticosterone, and other hormones upon pulmonary growth and synthesis of surfactant phospholipids. Gen. Comp. Endocrinol. 52:108–120.[CrossRef][Web of Science][Medline]

Julian, R. J. 2000. Physiological, management and environmental triggers of the ascites syndrome: A review. Avian Pathol. 29:519–527.[CrossRef][Web of Science][Medline]

Kalliecharan, R., and B. K. Hall. 1974. A developmental study of the levels of progesterone, corticosterone, cortisol, and cortisone circulating in plasma of chick embryos. Gen. Comp. Endocrinol. 24:364–372.[CrossRef][Web of Science][Medline]

Kinung’hi, S. M., G. Tiahun, H. M. Hafez, M. Woldemeskel, M. Kyule, M. Grainer, and M. P. O. Baumann. 2004. Assessment of economic impact caused by poultry coccidiosis in small and large scale poultry farms in Debre Zeit, Ethiopia. Int. J. Poult. Sci. 3:715–718.

Maxwell, M. H., and G. W. Robertson. 1998. UK survey of broiler ascites and sudden death syndromes in 1993. Br. Poult. Sci. 39:203–215.[CrossRef][Web of Science][Medline]

McNabb, F. M. A., E. A. Dunnington, T. B. Freeman, and P. B. Siegel. 1989. Thyroid hormones and growth patterns of embryonic and posthatch chickens from lines selected for high and low juvenile body weight. Growth Dev. Aging 53:87–92.[Web of Science][Medline]

Meeuwis, R., R. Michielsen, E. Decuypere, and E. R. Kuhn. 1989. Thyrotropic activity of the ovine corticotropin-releasing factor in the chick embryo. Gen. Comp. Endocrinol. 76:357–363.[CrossRef][Web of Science][Medline]

Sadler, W. W., H. S. Wilgus, and E. G. Buss. 1954. Incubation factors affecting hatchability of poultry eggs. Poult. Sci. 33:1108–1115.[Web of Science]

Scott, T. R., W. A. Johnson, D. G. Satterlee, and R. P. Gildersleeve. 1981. Circulating levels of corticosterone in the serum of developing chick embryos and newly hatched chicks. Poult. Sci. 60:1314–1320.[Web of Science][Medline]

Tona, K., B. Kemps, V. Bruggeman, F. Bamelis, L. De Smit, O. Onagbesan, J. De Baerdemaeker, and E. Decuypere. 2005. Comparison of three lines of broiler breeders differing in ascites susceptibility or growth rate. 1. Relationship between acoustic resonance data and embryonic or hatching parameters. Poult. Sci. 84:1439–1445.[Abstract/Free Full Text]

Tona, J. G., R. D. Malheiros, F. R. Bamelis, C. Carheghi, V. M. B. Moraes, O. Onagbesan, E. Decuypere, and V. Bruggeman. 2003. Effects of storage time on incubation egg gas pressure, thyroid hormones and corticosterone levels in embryos and on their hatching parameters. Poult. Sci. 82:840–845.[Abstract/Free Full Text]

Tona, K., O. Onagbesan, V. Bruggeman, L. De Smit, D. Figueiredo, and E. Decuypere. 2007. Non-ventilation during early incubation in combination with dexamethasone administration during late incubation 1. Effects on physiological hormone levels, incubation duration and hatching events. Domest. Anim. Endocrinol. 33:32–46.[CrossRef][Web of Science][Medline]

Visschedijk, A. H. J. 1968. The air space and embryonic respiration. 2. The times of pipping and hatching as influenced by an artificially changed permeability of the shell over the air space. Br. Poult. Sci. 9:185–196.[CrossRef][Web of Science][Medline]

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