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Development of the chicken as a model for prenatal stress¹2^,

Department of Animal Science, Iowa State University, Ames 50011

³ Correspondence:
219 Poultry Science Building (phone: (765) 496-7750; fax: (765) 496-1993; E-mail:
layd{at}purdue.edu).

	Abstract

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Exposing a pregnant mammal to stressors causes behavioral and physiological alterations in her offspring ("prenatal stress"); however, elucidation of the underlying mechanism is hindered by an inability to control maternal compounds that may affect the fetus. We designed this experiment to determine if the autonomously developing chicken embryo could be developed as a model for prenatal stress. On d 16 of incubation, eggs were treated with: 1) 60 ng corticosterone (CORT), 2) elevated incubation temperature (40.6°C) for 24 h (HEAT), or 3) no treatment (Control). Chicks from all three treatments hatched at similar weights; however, HEAT chicks weighed less by 100 d of age and remained lighter until the end of the study (P < 0.05). At 8 d post-beak trimming, adrenal gland weight was not different (P > 0.20) among treatments, basal plasma corticosterone concentrations tended (P < 0.06) to be greater for CORT chicks than either the Control or HEAT chicks, and CORT chicks were heavier than HEAT chicks (P < 0.005) but not Control chicks (P > 0.20). At 11-wk, HEAT birds had heavier adrenal glands than did Control birds (P < 0.01). At 16 wk of age, Control cocks performed more (P < 0.01) pecking aggression than either HEAT or CORT cocks, whereas CORT cocks were chased more often and chased another cock less often than either HEAT or Control cocks (P < 0.01). Treatments did not alter the behavior of the hens (P > 0.10). Administration of corticosterone during incubation replicated some, but not all, of the effects seen in prenatal stress in mammals.

Key Words: Behavior • Chickens • Corticosterone • Prenatal Period • Stress

	Introduction

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Prenatal stress, the stress imposed upon a fetus when its dam is stressed, seems to be a universal challenge in mammals. Cattle (Lay et al., 1997a,b), swine (Lay, 1999; Haussmann et al., 2000), rodents, and humans (see Weinstock, 1997 for review) are altered by prenatal stress, which can be deleterious to their subsequent responses to stress. Typical (see Weinstock, 1997 for review) effects of prenatal stress are: elevation of glucocorticoids, increased emotionality, increased hypothalamic-hypophyseal-adrenal responsiveness, increased number of glucocorticoid receptors in the hypothalamus and hippocampus, delays in early motor development, greater hypothalamic ß-endorphin, feminization of males, and masculinization of females. Prenatal stress has the potential to cause grave consequences to production agriculture and animal well-being.

Research on prenatal stress began as early as the mid-1950’s (e.g., Levine and Mullins, 1958), yet little is known about the causative mechanism. Researchers (e.g., Barbazanges et al., 1996) have suggested that prenatal stress is caused by maternal cortisol interacting with the fetal hypothalamic-hypophyseal-adrenal axis. Other researchers (e.g., Keshet and Weinstock, 1995) believe that prenatal stress is caused by maternal endorphin release affecting the development of the fetus. Difficulty in determining the exact mechanism is due in part to the relative inaccessibility of the mammalian fetus to well-controlled experimental manipulations.

Epple et al. (1997) recently suggested that the embryonic chicken is susceptible to stress, and thus we question the singularity of the dam’s role in prenatal stress. We hypothesized that prehatching stress in chickens would cause deleterious effects similar to those of prenatal stress observed in mammals. To test this hypothesis, we attempted to induce prehatching stress in the developing chicken embryo by increasing the temperature of incubation or administration of corticosterone (CORT).

	Materials and Methods

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All procedures involving animals were approved by the Iowa State University Committee on Animal Care (Protocol 3-9-4157-1-G). Eggs were collected from the Iowa State University layer hen flock. The parental stock for these hens was originally derived from Hyline (Perry, IA) and subsequently selected in a closed flock at Iowa State University. Hens were artificially inseminated and eggs were collected for 10 d. The eggs (n = 378, 315 +20% extra to account for infertile/nonhatching eggs) were assigned randomly to one of three treatments (n = 126 per treatment) on d 16 of incubation (incubation in the chicken is normally 21 d): 1) administration of 60 ng/embryo of corticosterone (the predominant glucocorticoid in chickens; Sui et al., 1997; CORT); 2) increased incubation temperature (from 37.5 to 40.6°C; Thomspon et al., 1976; HEAT); or 3) incubation under normal farm conditions (Control). Because this was a preliminary experiment on the effects of prenatal stress in chickens, both the dosage of corticosterone and the time of delivery were derived through estimations based on the physiological constraints of the chicken. The increase in incubation temperature was derived from studies that measured hatchability and found that embryonic mortality was increased significantly above 40.6°C (Thompson et al., 1976). Because no previous studies have investigated prenatal stress in chickens, the day of incubation at which treatments should be applied also was unknown. Embryonic chickens were treated on d 16 of incubation because this is the age at which concentrations of corticosterone normally plateau after a sharp rise between d 14 and 16 (Scott et al., 1981). We chose this time to administer our treatments, hypothesizing that if the chick hypothalamic-hypophyseal-adrenal axis was susceptible to alteration, it would be at the time of the natural increase in endogenous corticosterone.

Application of Treatments
Administration of 60 ng corticosterone (Sigma Chemical, St. Louis, MO) to each developing embryo in the CORT treatment was accomplished by applying 7.5 µL of 5% ethanol solution containing 80 µg/mL corticosterone (600 ng corticosterone applied, Sigma Chemical Co., St. Louis, MO) onto the egg on d 16 of incubation. Preliminary research conducted in our laboratory (unpublished data) found that approximately 10% [³H]-corticosterone dissolved in a 5% ethanol solution crossed through the egg shell and into the conceptus compartment. The HEAT treatment was accomplished by increasing the temperature of the incubator (Jamesway, Jamesway Incubator Co., Cambridge, Ontario, Canada) to 40.6°C (while maintaining a constant humidity) at 0600 on d 16 of incubation, and returning the temperature to 37.5°C 24 h later. All eggs were incubated in the same incubator except for the 24 h that the HEAT chicks were incubated at the elevated temperature in an identical incubator adjacent to the incubator containing all the other eggs.

Data Collection
On d 18 of incubation, 45 eggs (n = 15 per treatment) were selected randomly and opened. It was noted if the embryo was viable, and if so, it was immediately euthanitized. At this time, the weight of the embryo, yolk, and whole egg contents was recorded. Collection of data on this day of incubation allowed us to determine any early effects that treatments may have had on the developing embryo. The remainder of the eggs for each treatment group was allowed to hatch, and the chicks were raised together using normal farm management procedures with the exception that the chicks were not beak-trimmed unless they were participants in the beak-trimming stress test at 14 d of age. On d 21 (expected day of hatching), all hatched chicks were weighed and permanently identified with a stamped metal wing band. Chicks were moved to the rearing pen (4.6 x 13.7 m) and housed as a single group. At approximately 15 wk of age, significant male-female agonistic behavior was noted in the group; therefore, the majority of the cocks was separated from the hens and placed in a separate, adjacent pen (4.6 x 4.6 m) for the duration of the study. Three cocks, one from each treatment, were left housed with the hens.

At 7 d of age, 30 chicks per treatment were subjected to an isolation test. The isolation test consisted of placing a lone chick into an 50-cm diameter circle constructed of single-faced corrugated paper (commonly used as a temporary barrier in chick housing) for a 5-min duration. Latency to move and to defecate and vocalization rate were recorded. A second isolation test was performed on a different group of 30 chicks (n = 10 per treatment) at 9 d of age, for a 10-min duration.

At 14 d of age, a jugular blood sample (1 mL) was obtained from a separate group of chicks (n = 30 per treatment) that were weighed and beak-trimmed (using a standard poultry cauterizing beak trimmer). Jugular blood samples (1 mL) were collected every other day for 8 d (half the birds from each treatment bled on alternating days; all birds bled on d 1 and d 8 following beak trimming). The chicks used in the beak-trimming stress test were sacrificed on d 8 after beak trimming, weighed, and the adrenal glands and gonads collected and weighed.

At 11 wk of age, 20 birds per treatment were subjected to a handling test to assess their responses to stress. Birds were isolated from the flock, 1 mL of jugular blood was collected via venipuncture to determine basal corticosterone, and then they were handled. The handling simply consisted of holding the bird upside down by the legs and gently shaking it back and forth for 1 min. After the 1-min of handling, each bird was placed into a wire cage (38 x 51 cm floor, 36 cm height) by itself. Blood was collected, via jugular venipuncture, at 15, 45, 75, 105, and 135 min with respect to the initiation of handling for the determination of plasma corticosterone as a response to the stressor. Following the blood sampling at 135 min, birds were sacrificed, weighed, and the adrenal glands and gonads were collected and weighed.

Behavioral observations were conducted on both cocks and hens at approximately 21 wk of age. Each chicken was marked on the back with an identifying color (yellow, blue, or black) to indicate treatment. Trained observers, blind to the treatment-color association, were stationed within the pen for 10 min to record: chasing, pecking, crowing (cocks), agonistic encounters, feather eating, and dust bathing. Observations were repeated such that all birds were observed on three separate occasions on each of five alternating days. It is unlikely that the chickens responded to the color markings as previous researchers who also used color on the birds’ wings and backs did not find any behavior modification due to the added color (Shea et al., 1991).

At 26 wk of age, 18 hens (n = 6 per treatment) had a blood sample collected from the external jugular vein to assess basal corticosterone concentrations. After blood collection, the chickens were sacrificed, weighed, and the adrenal glands and gonads were collected and weighed. To assess reproductive function of each hen, the number of follicles, size of the largest follicle, number of previous ovulations (determined by counting post-ovulatory follicles), pubic width, and pubic length were recorded.

Corticosterone Assay
Plasma corticosterone concentrations were determined in duplicate using a commercially- available double antibody RIA kit (DPC, Los Angeles, CA). Cross-reactivity of the corticosterone antiserum was as follows: 11-deoxycorticosterone, 1.58%, progesterone, cortisol, aldosterone, testosterone, 18-hydroxydeoxy-corticosterone, 17-hydroxy-progesterone, DHEA, and estradiol, <0.42% (analyses by DPC). The kits were used according to the specifications of the manufacturer. Precision and accuracy of the assay were evaluated in triplicate using chicken plasma pools containing approximately 50 and 5 ng/mL of corticosterone, resulting in a mean intraassay CV of 6.9% and an interassay CV of 14.3%. The lowest detectable concentration of corticosterone was approximately 1 ng/mL.

Statistical Analysis
All means are presented as mean ± SEM. All data were analyzed with chicken as the experimental unit (because treatments were applied during incubation), and tests were done to assess the feasibility of normality using the univariate procedure of SAS (SAS Institute Inc., Cary, NC). Normal data were analyzed using the GLM procedure of SAS, and non-normal data were analyzed using Wilcoxon-Mann-Whitney ranked sum test of SAS. Body weights, organ weights, rate of gain, and concentrations of corticosterone were examined using the GLM procedure and accounting for repeated measures, with treatment, sex, treatment by sex, and treatment nested within chicken included in the model. Behavioral data were analyzed using the Wilcoxon-Mann-Whitney test.

	Results

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All 45 eggs that were opened on d 18 of incubation contained viable embryos. No differences were found among treatments for whole egg, embryo, or yolk weights (pooled mean ± SEM; 35.4 ± 0.63, 19.52 ± 0.51, or 10.92 ± 0.33 g, respectively; P > 0.20).

Of all the eggs incubated to 21 d, 11 Control, 8 HEAT, and 15 CORT did not hatch by d 21 of incubation (corresponding to 91, 94, and 88% hatching rates, respectively; P > 0.10), and were discarded. Treatments did not affect hatch weight (30.75 ± 0.25 g; P > 0.10) or sex ratio (51.3% hens vs 48.7% cocks, P > 0.44). However, by 100 d of age, HEAT chicks weighed less than either Control or CORT chicks, and this difference was maintained until birds were slaughtered at 130 d of age (P < 0.05, Figure 1).

View larger version (15K): [in this window] [in a new window]   Figure 1. Body weight of chicks from hatch to 130 d of age. By 100 d of age, elevated incubation temperature (40.6°C) for 24 h (HEAT) chicks weighed less than either control or corticosterone (CORT) chicks (P < 0.05). Control = no treatment.

View larger version (26K): [in this window] [in a new window]   Figure 2. Mean frequency of behavior during 10-min observations of cocks at 21 wk of age. Observations were repeated such that all birds were observed on three separate occasions on each of five alternating days. "Was Pecked" indicated when a cock was the recipient of a peck (aggressive action) from another cock and "Pecked Another" indicates when a cock was the individual that performed the pecking action. Bars within a behavioral category with different superscripts differ (P < 0.01). CORT = corticosterone; Control = no treatment; HEAT = elevated incubation temperature (40.6°C) for 24 h.

View larger version (33K): [in this window] [in a new window]   Figure 3. Mean frequency of behavior during 10-min observations of cocks at 21 wk of age. Observations were repeated such that all birds were observed on three separate occasions on each of five alternating days. "Was Chased" indicated when a cock was the recipient of chasing (aggressive action) from another cock and "Chased Another" indicates when a cock was the individual that performed the chasing action. Bars within a behavioral category with different superscripts differ (P < 0.01). CORT = corticosterone; Control = no treatment; HEAT = elevated incubation temperature (40.6°C) for 24 h.

	Discussion

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Incubation of eggs at 40.6°C for 24 h did not decrease hatchability when compared with controls. This is in agreement with previous work, suggesting that even 48 h of incubation at 40.6°C beginning on d 16 of incubation was not detrimental to the developing embryo (Thompson et al., 1976). Thompson et al. (1976) suggested that heat-stressed embryos were generally weaker (based on number of cull chicks) but only for those birds thermally stressed at temperatures >40.6°C. Incubation for up to 48 h at 40.6°C had no apparent impact on chick viability. Interestingly, Thompson et al. (1976) reported that the low-viability chicks hatching from heat-stressed eggs weighed as much as 4 g more than controls. We did not find a similar increase in hatchling weight in our study, but the increase in weight found by Thompson et al. (1976) was attributed to embryos in the largest eggs preferentially surviving, rather than a growth-promoting effect of heat stress, although specific data were not presented. In those birds that were beak-trimmed, HEAT-treated birds weighed less than CORT-treated birds 8 d after beak trimming. Furthermore, by 100 d of age, birds exposed to an elevated temperature on d 16 of incubation weighed less than Control and CORT birds. These data lead us to suggest that even a short-term (i.e., 24-h) heat stress during early development, insufficient to cause significant mortality, can have important long-term ramifications on the physiology of the animal.

Incubation of eggs at normal temperature (i.e., 37.5°C) with application of 60 ng of corticosterone to the embryo (via 600-ng application to the shell) did not decrease hatchability when compared with controls. This is not surprising, based on previous reports of glucocorticoid administration to chicken embryos (Karnofsky et al., 1951; Sames and Leathem, 1951; Evans, 1953). Indeed, Karnofsky et al. (1951) reported that a 2-mg dosage of cortisone acetate was required to be lethal to 50% of the treated eggs. In a number of studies on the effects of embryonic administration of glucocorticoids to chickens, either BW near normal hatching time (Karnofsky et al., 1951; Sames and Leathem, 1951; Evans, 1953) or at hatching (Scott et al., 1981) was reduced by the glucocorticoid treatment. We did not observe a reduction in hatchling weight in the present study, but the dosage of glucocorticoid (60 ng per embryo) is more than five orders of magnitude lower than the dosages (0.5 to 1 mg per embryo) used in studies reporting growth retardation (Karnofsky et al., 1951; Evans, 1953; Scott et al., 1981). Additionally, we observed no difference in growth rate or mature weight in birds exposed to elevated corticosterone during incubation, leading us to suggest that the dosage of corticosterone employed was low enough to establish effects on the hypothalamic-hypophyseal-adrenal axis without markedly affecting the growth axis (hypothalamic-hypophyseal-liver axis).

As our goal was to attempt to modify the programming of the hypothalamic-hypophyseal-adrenal axis, timing of the treatment was critical. Work in other species (rat, mouse, and lamb, reviewed by Gluckman, 1985) supports the suggestion that the hypothalamic axes are susceptible to modification by endogenous hormones at times when peripheral hormone increases during embryonic development. In a model proposed by Gluckman (1985), endocrine control between the central and peripheral nervous systems is affected by pulsatile release of hypothalamic hormones during fetal development. These hormones act on the hypophysis to produce an associated peripheral hormone effect, which then negatively feeds back on the hypothalamus to create a "set point" in organ development. Theoretically, the mechanism of this set point is created by increasing or decreasing the number of responsive cells in the organ, the number of receptors on the cells, and(or) the ability of the cell to produce the specified hormone. If the developing fetus is exposed to "stress" hormones during development, then its hypothalamic-hypophyseal-adrenal axis could be permanently altered by such a mechanism (Henry et al., 1994). In addition to the work of Scott et al. (1981) cited earlier, evidence exists suggesting that d 16 of incubation is a time of increased activity, if not activation, of the hypothalamic-hypophyseal-adrenal axis (Pedernera, 1971; Girouard and Hall, 1973; Wise and Frye, 1975). Indeed, Woods et al. (1971) showed that embryos hypophysectomized at 33 to 38 h of incubation exhibited a slowly increasing concentration of chorioallantoic corticosteroids from d 10.5 to 13.5 of incubation, similar to that exhibited by intact embryos. However, allantoic fluid concentrations of corticosteroids increased dramatically beginning on d 14.5 in both intact and hypophysectomized embryos with the increase significantly reduced in the hypophysectomized embryo through d 17.5 of incubation (Woods et al., 1971). Additionally, in a separate group of hypophysectomized embryos, ACTH administration did not alter concentrations of corticosteroid from those found in vehicle-treated controls on d 16.5 of incubation; however, ACTH administration did increase allantoic corticosteroid concentrations nearly two-fold on d 17.5 of incubation. Wise and Frye (1975) demonstrated that embryos on d 16 of incubation, but not on d 14 of incubation were able to respond to the stress of a broken shank bone with an increase in corticosterone. Of note, the embryonic chick adrenal gland in culture appears to be able to respond to increasing dosages of ACTH by d 8 of incubation (Pedernera, 1971). Furthermore, application of 100 µL of Ringers solution caused significant alterations in allantoic AA concentrations in embryos on d 13 of incubation; however, there was no change in allantoic concentrations of glucose, and corticosteroids were not measured (Hohlwerg et al., 1999). These data support the concept that adrenal gland growth and development occur in the chicken embryo during development, but that final maturation and/or normal levels of allantoic corticosteroids require hypophyseal ACTH and the underlying feedback mechanism is likely subject to alteration.

Following the beak-trimming stress, CORT birds had a tendency to have higher circulating concentrations of corticosterone than either HEAT or Control birds. Beak trimming has been shown to serve as a chronic stressor, with apparent pain perception lasting for up to 5 wk (see Gentle, 1986 for review). The apparent increased hypothalamic-hypophyseal-adrenal responsiveness (or decreased liver catabolism of corticosterone) in CORT-treated birds, similar to the increased hypothalamic-hypophyseal-adrenal responsiveness of rats born to dams restrained for the last third of gestation, would support the suggestion that elevated maternal glucocorticoid may be responsible for some of the observed alterations in the physiology of prenatally-stressed individuals. These data do not exclude a potential role of increases in maternal opioid concentrations or the concentrations of other compounds in either contributing to other alterations in the physiology of prenatally-stressed individuals, or reinforcing/providing redundant mechanisms for transducing prenatal stress. It is worthy to reiterate that the increase in incubation temperature did not result in similar alterations in postnatal physiology and behavior, supporting our suggestion that a number of different factors imposed during gestation/incubation can alter the growth, physiology, and behavior of an individual postnatally and that both the quality and the quantity of the prenatal exposure will determine the severity of the alteration.

In the present study, heat stress caused increased adrenal gland weight and impaired growth, while exogenous corticosterone tended to cause alterations of the hypothalamic-hypophyseal-adrenal axis and also caused behavioral alterations indicative of a more submissive bird, or a bird that is not at the top of the social hierarchy. These findings imply that alterations due to prenatal stress are not caused solely by exposing the developing embryo to greater concentrations of glucocorticoids and/or that components of an animal’s physiology and behavior can be altered by a variety of factors including maternal glucocorticoids, opioids, and other as yet implicated compounds as well as direct stressors. If there are indeed developmental alterations that are the result of changes in maternal physiology ("indirect stress") as well as application of stressors that alter conceptus physiology ("direct stress"), then a need may exist for elucidating generalized responses and underlying mechanisms for both types of situations.

	Implications

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As with all animals, cattle, sheep, swine, and poultry are exposed to some degree of stress during their lifetimes. Previous research in rodents, swine, and cattle indicates that stress during gestation may have profound deleterious effects on subsequent offspring. To date, the mechanism by which these alterations occur has remained elusive. However, research suggests that the chicken may be developed as a model by which the mechanism can be elucidated. Future research directed at understanding prenatal stress in cattle, sheep, and swine will allow maximization of both productivity and animal well-being.

	Footnotes

 
¹ Journal paper number J-19185 of the Iowa Agricultural and Home Economics Experiment Station, Ames, Project 3090, and supported in part by Hatch Act and State of Iowa Funds. This work was also supported in part by a Carver Trust grant.

² We would like to thank Mark F. Haussmann, Sara Hoge, George Brant, and Jenny Groeltz for their tremendous effort on this project. We would also like to provide a special "Thank You" to Alison M. Steng and P. B. Ribbon for their insightful direction in the preparation of this manuscript.

⁴ Current address: USDA-ARS Livestock Behavior Research Unit, Purdue University, West Lafayette, IN 47907.

⁵ Current address: Division of Animal and Veterinary Sciences, West Virginia University, Morgantown, WV 26506.

Received for publication August 23, 2001. Accepted for publication January 30, 2002.

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