J. Anim. Sci. 2003. 81:784-790
© 2003 American Society of Animal Science
Erythropoiesis regulation during the development of ascites syndrome in broiler chickens: A possible role of corticosterone1
D. Luger*,
D. Shinder*,
D. Wolfenson
and
S. Yahav*,2
* Institute of Animal Science, ARO, the Volcani Center, Bet Dagan 50250, Israel and
and
Department of Animal Science, Faculty of Agricultural, Food and Environmental Quality Sciences, the Hebrew University of Jerusalem, Rehovot 76100, Israel
2 Correspondence:
Dept. of Poultry Sciences, P.O. Box 6 (phone: 972-8-9484415; fax: 972-8-9475075; E-mail:
yahavs{at}agri.huji.ac.il).
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Abstract
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The ascites syndrome in broiler chickens is attributed to metabolic burdening, which results from intensive genetic selection for rapid growth coupled with exposure to extreme environmental conditions, such as low ambient temperature. These conditions impose on the broilers difficulties in fulfilling tissue demands for oxygen, and the birds exhibit a decrease in blood oxygen saturation and high hematocrit values. It is unknown whether the increase in hematocrit results from alteration in erythropoiesis or from fluid exudation out of the blood system to the abdominal cavity. The present study was conducted to examine the association between abnormal stress response and erythropoiesis process in ascitic broilers. Ascitic chickens revealed a uniquely continuous stress response: expressing an increase (P 
0.05) in plasma corticosterone concentration 2 to 3 wk before death. At 5 wk of age, ascitic broilers exhibited an increase (P < 0.05) in hematocrit, blood cell count, and packed cells and blood volumes, with no significant change in plasma volume. These results confirm an accelerated erythropoiesis process in ascitic birds. Increased blood cell production in ascitic birds was matched by an increase (P < 0.05) in the proportion of immature red blood cells (23%) in comparison with broilers that remained healthy (7%), and by decreased (P < 0.05) hemoglobin content relative to red blood cells. We conclude that continually increased corticosterone concentrations, as an inducer of erythropoiesis proliferation and differentiation arrest, in ascitic chickens, resulted in increased production of red blood cells (partially immature) with decreased hemoglobin content; this decrease in hemoglobin might have contributed to enhanced development of hypoxemia and to aggravation of the syndrome.
Key Words: Ascites • Corticosterone • Erythropoiesis • Hemoglobin
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Introduction
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Recent decades have seen significant progress in the genetic selection of broiler chickens for rapid growth in a relatively short period. This, coupled with inadequate development of major systems, resulted in impaired ability to regulate the energy balance under extreme conditions, such as low ambient temperature (Ta) or high altitude (Julian, 1993; Wideman, 2000). These environmental conditions trigger the development of ascites syndrome, which is characterized mainly by hypoxemia, increased workload of the cardiopulmonary system, central venous congestion, fluid exudation (mainly into the peritoneal cavity), and finally death (Julian, 1993; Maxwell et al., 1995; Olkowski and Classen, 1998). The hypoxemia coincides with diminished oxygen saturation in the blood (Julian and Mirsalimi, 1992; Wideman et al., 1998a) although hematocrit increases significantly (Shlosberg et al., 1996; Luger et al., 2001). Elevation in hematocrit can be caused by diminished plasma volume or enhanced erythropoiesis (Maxwell et al., 1990; Yahav et al., 1997).
The development of mature peripheral red blood cells from pluripotent stem cells in the bone marrow is a complex process, regulated by several hormones (erythropoietin, corticosterone, and triiodothyronine) and growth factors (von Lindern et al., 1999; Wessely et al., 1999). The glucocorticoid hormone is a key regulator for self renewal of erythroid progenitors (Wessely et al., 1997; Bauer et al., 1999), whereas triiodothyronine (T3) mainly controls the cell differentiation pathway, with strong hemoglobin accumulation (Bauer et al., 1998). In ascitic broilers, both thyroxin (T4) and T3 declined with the development of the syndrome (Luger et al., 2001). However, the response pattern of corticosterone is not yet known. The present study was conducted to examine the association between abnormal stress response expressed by the secretion of the hormone corticosterone and its impact on erythropoiesis process in ascitic broilers.
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Materials and Methods
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Experimental Design
The ascites syndrome was induced in broiler chickens by exposing them to low Ta and by supplying a pellet-form diet. Male chicks (Cobb) were raised in battery brooders and in cages (up to 3 and up to 7 wk of age, respectively) in a temperature-controlled room (±1.0°C) under continuous fluorescent illumination. At 1 d of age, 200 chicks were sorted into 20 groups of 10 birds according to BW. Birds of extreme weights, among a population of approximately 250 birds, were discarded. The experiment comprised two treatments: a) control, four replicates of 10 birds and b) induced ascites treatment, 16 replicates of 10 birds. Broilers in the control treatment were raised under regular conditions from 1 to 28 d of age (32 to 26°C, respectively) (Yahav et al., 1996) and were then exposed to a constant 22.0°C until 49 d of age. Chickens that were exposed to ascites-inducing conditions were raised under standard conditions during the first week of age, and then, at the ages of 7, 14, and 21 d, Ta was reduced to 26.0, 20.0, and 15.0°C, respectively. The lowest Ta was then maintained until the end of the experiment (49 d of age). Water and feed were provided ad libitum. Feed in pellet form was designed according to NRC (1994) specifications. The local animal welfare committee approved the experimental procedures.
At weekly intervals, blood samples were drawn on an individual basis. Whole blood samples were taken from the brachial vein; part of the sample was stored at 4°C pending hematocrit and hemoglobin analysis, while the other part was centrifuged and the plasma stored at -20°C pending further analysis.
At the age of 5 wk (the age at which a peak in the syndrome was demonstrated previously; Luger et al., 2001), 30 individuals were chosen; 10 were chosen randomly from the control group and 20 from the induced-ascites group (10 healthy—broilers that were exposed to low Ta and did not develop ascites—with low hematocrit levels, and 10 with ascites symptoms including high hematocrit levels). Plasma volume (PV), packed cell volume (PCV), blood cell counts, and hemoglobin concentrations were analyzed. These individuals were then killed by cervical dislocation. Heart muscle was removed immediately and the severity of the syndrome was evaluated in terms of the ratio of right ventricle weight to total ventricle weight, according to Roush and Wideman (2000) and Wideman (2000).
Plasma Corticosterone Concentration.
Corticosterone concentration was measured in ascitic chickens (according to the age of mortality) as well as in healthy and control ones. Measurement was performed by RIA with the ImmuChem double antibody kit (ICN Biomedical, Inc., Costa Mesa, CA), according to Darras et al. (1996).
Hematocrit and Hemoglobin Analysis and Blood Cell Counts.
Blood for hematocrit measurements was drawn into heparinized microcapillary tubes and centrifuged in a Hettich microliter centrifuge (Tuttlingen, Germany) for 7 min. Hemoglobin concentration was analyzed colorimetrically with a Sigma diagnostic kit (No. 525, catalog No. E9133, Sigma Chemical Co., St. Louis, MO), according to the manufacturer’s instructions. Blood cells were counted with a Coulter counter (model ZM, Coulter Electronics, Luton, U.K.) after dilution of whole blood (10 -L) by a factor of 10-4.
Erythrocytes Differential Count.
Blood smears from ascitic and nonascitic chickens were stained by the May Grünwald Gimza method (Robertson and Maxwell, 1990). Immature erythrocytes, which resembled polychromatic erythrocytes, were recognized by their large rounded shapes and lightly stained nuclei (Delcuve and Davie, 1989; Chen et al., 1996). Immature and mature erythrocytes were counted in a total of 10 slides, each divided into six different regions.
Plasma, Whole Blood and Packed Cell Volume.
In order to determine plasma volume, blood samples were collected for background. Then, Evans blue (0.5 mg/kg of BW) was injected into the brachial vein and a blood sample was collected from the contralateral vein after 5 min (Yahav et al., 1997). The Evans blue concentration in the plasma samples was measured colorimetrically (at 620 nm). Blood volume was calculated according to Yahav et al. (1997).
Plasma Ingredients Analysis.
Total protein and albumin concentrations and osmolality were analyzed in the plasma and abdominal cavity fluid of ascitic broilers. Total protein and albumin concentrations were analyzed colorimetrically with Sigma diagnostic kits 541 and 631, respectively. Osmolality was analyzed by osmometer (- Osmette, Precision System Inc., Natic, MA).
Statistical Analysis.
All data (except that of corticosterone concentration, Table 2
) included three treatments (i.e., control, healthy, and ascites, and were subjected to one-way ANOVA according to Snedecor and Cochran (Snedecor and Cochran, 1989), and to Duncan’s multiple-range tests (Duncan, 1955). For corticosterone, the analysis was done for each week separately (between 2 to 7 wk of age). In this analysis, the third treatment (ascites) was separated to four groups by age of mortality (4 to 7 wk of age). The number of ascitic groups declined with age; therefore, for corticosterone, one-way ANOVA was conducted separately for each week of age. Means were considered significantly different at P 0.05.
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Table 2. Plasma corticosterone concentration (ng/mL; analyzed separately for each week) during the course of ascites syndrome development in broiler chickens, at 2 to 7 wk of age
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Results
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Ascites Characteristics
The mortality rate from ascites in the ascites induction treatment exceeded 23%. The mortality from ascites was distributed from 4 to 7 wk of age with a maximum at 5 wk (9.6%) (Data not shown). In the control birds, no incidences of mortality or ascites were observed. At the age of 5 wk, BW of the ascitic broilers was significantly lower than that of the healthy and control broilers (Table 1). In all ascitic broilers, significant hypertrophy of the right ventricle was exhibited (Table 1), which resulted in significant increases in the heart weight and the ratio of right to total ventricle weights as a percentage of BW.
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Table 1. Heart muscle and right ventricle (RV) weights as percentages of body weight, and ratio of right ventricle to total ventricles (RV:TV), of control, healthy, and ascitic broilers at 5 wk of age
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Plasma Corticosterone Concentration
Plasma corticosterone concentration did not differ among treatments at the age of 2 wk (Table 2
). Exposure to cold resulted in a significant increase in the hormone concentration (3 wk of age). At this age, broilers that died from ascites at 4 and 5 wk of age exhibited the significantly higher corticosterone concentration than the others. In the healthy birds, the hormone concentration returned to a level similar to that of the control group, whereas the ascitic chickens demonstrated significantly higher hormone concentration that remained elevated 1 to 2 wk before death.
The Association Between Plasma and Abdominal Cavity Fluid
Similar values of osmolality and of total protein and albumin concentrations were measured in the plasma and in the abdominal cavity fluid of the ascitic broilers (Table 3).
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Table 3. Total protein (g/dL), albumin (g/dL), and osmolality (mOsmol/L) in the plasma and abdominal cavity fluid of ascitic broilers at 5 wk of age
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Blood Volume Distribution, Hemoglobin, and Erythrocytes Differential Count
Plasma volume did not differ among control, healthy, and ascitic broilers (Fig. 1). However, hematocrit and PCV were significantly elevated in the ascitic birds compared with that of the healthy and control broilers (Table 4 and Figure 1, respectively), resulting in significantly higher BV in the ascitic broilers. The increase in PCV was attributed to a significant increase in the number of blood cells, which coincided with a significant increase in hemoglobin concentration (Table 4). Slides of blood smears (Figure 2) exhibited a significant increase in the number of immature red blood cells in the bloodstream of ascitic broilers (23.5%) compared with those in the healthy and control birds (7.2 and 2.3%, respectively; Figure 3). Calculation of hemoglobin content respective to red blood cell count exhibited a significant reduction of this parameter in the ascitic birds (P 0.05) in comparison to the healthy ones (Figure 4).
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Figure 1. Blood (BV), plasma (PV), and packed cell (PCV) volumes in control, healthy, and ascitic broilers, presented as percentages of BW. For PCV and BV, different letters and asterisks, respectively, designate significant differences (P 0.05); n = 10. For BV, SEM = 1.57; for PV, SEM = 1.35; and for PCV, SEM = 1.1.
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Table 4. Hemoglobin (g/dL) concentration, hematocrit, and blood cell counts (x 1010/mL) of ascitic, healthy, and control broilers at 5 wk of age
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Figure 2. Blood smears from ascitic and nonascitic chickens were stained by the May Grünwald Gimsa method. Immature erythrocytes were characterized by large, rounded, and lightly stained nuclei, and resembled polychromatic erythrocytes. Immature and mature erythrocytes were counted in a total of 10 slides, with six different regions in each.
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Figure 3. Percentage of immature cells in the red blood count (RBC). Immature and mature erythrocytes were counted in a total of 10 blood smear slides, with six different regions in each. Between columns, different letters designate significant differences (P 0.05).
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Figure 4. Hemoglobin content in blood cell count (1,000) of healthy and ascitic broilers, represented as variance (%) from control. Between columns, different letters designate significant differences (P 0.05).
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Discussion
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This study has demonstrated for the first time the association among abnormal stress response, disorder in the erythropoiesis process leading to the production of relatively high numbers of immature red blood cells, and the development of the ascites syndrome in fast-growing chickens. This association is explained by the central role of corticosterone in accelerating erythrocytes proliferation and impairing its differentiation. The findings in this study may provide an explanation for previous contradictory evidences of increased hematocrit on the one hand (Shlosberg et al., 1996; 1998; Luger et al., 2001) and reduced blood oxygen saturation on the other hand (Julian and Mirsalimi, 1992; Wideman et al., 1998a) in ascitic broilers.
One of the defining characteristics of ascites syndrome is the accumulation of fluid in the abdominal cavity. This has been well documented in humans with liver cirrhosis or renal failure (Henriksen et al., 1981; 2001; Hedenborg et al., 1988). In broilers, however, it is related to the increased metabolic activity needed to meet the energy demands for both maintenance and growth under relatively extreme cold conditions (Bendheim et al., 1992; Julian, 1993). In the present study, we found that in ascitic broilers, the composition of the abdominal cavity fluid was fairly similar to that of the plasma (in osmolality, total protein, and albumin concentrations), suggesting a deficiency in the selective permeability of the blood vessels. These findings resemble those in cirrhotic human patients with ascites (Parving et al., 1977a,b; Henriksen et al., 2001). The escape of plasma fluid out of the blood vessels was probably due to increased pulmonary hypertension and central venous congestion, symptoms found both in humans (Henriksen et al., 2001) and in broilers (Wideman, 2000).
Another phenomenon that is common to most ascites cases in broilers is a significant increase of hematocrit (Maxwell et al., 1990; Julian and Mirsalimi, 1992; Wideman al., 1998b). In a previous study (Luger et al., 2001), we found that hematocrit in ascitic broilers increased after exposure to cold and that the increase became significant approximately 2 wk before death.
These two phenomena, abdominal fluid accumulation and a sharp increase of hematocrit, raised the question of whether the increase of hematocrit was caused by a decline in plasma volume as a result of plasma leakage out of the blood vessels or by an increase in erythropoiesis as a compensatory reaction to the lack of oxygen in the tissues. As in the case of human ascitic patients (Salo et al., 1997), the ascitic broilers in the present study exhibited conservation of plasma volume similar to that of the healthy ones. However, the PCV in the ascitic broilers increased significantly, by up to 80%, as a result of a significant increase in the number of erythrocytes, which also contributed to a significant elevation in blood volume. Thus, enhanced erythropoiesis, and not plasma volume reduction, was found to be involved in the hemodynamics of the ascitic broilers. This finding could also account for the blood congestion and the increased blood viscosity (Fedde and Wideman, 1996) that contribute to the enhanced cardiac workload (Owen et al., 1995, Wideman and Tackett, 2000), blood pressure (Owen et al., 1995), and blood-flow resistance (Wideman et al., 1998a) in ascitic chickens. In these birds, the high PCV on the one hand and the significant decline in oxygen saturation in the blood on the other hand (Julian and Mirsalimi, 1992; Buys et al., 1999) raised the possibility of an impaired oxygen-carrying capacity in the blood. In the present study, the increased red blood cell count was accompanied by a significant increase in blood hemoglobin concentration, but further calculations of hemoglobin content per 1,000 red blood cells revealed a significant reduction in hemoglobin content in the ascitic broilers compared with the healthy and control broilers (Figure 4). These results suggest a possible inefficient enhancement in the erythropoiesis process.
As was previously demonstrated (Lucas and Jamroz, 1961), up to 3% of immature erythrocytes are naturally present in the chicken bloodstream. These erythrocytes are characterized by large, brightly stained nuclei. The ascites-induction conditions elicited enhanced erythropoiesis, which resulted in an increased proportion of immature erythrocytes in the bloodstream. However, whereas in the healthy broilers only a moderate proportion of immature erythrocytes was observed (7.2%), in the ascitic ones, immature erythrocytes contributed up to 23.5% to the total erythrocyte count. The significant increase in immature erythrocytes, coupled with the significant decline in hemoglobin content, may provide the explanation for the decline of oxygen saturation in the blood of ascitic broilers (Julian and Mirsalimi, 1992; Wideman and Tackett, 2000).
The differences between healthy and ascitic chickens in their production of erythrocytes in general and of immature erythrocytes in particular, suggest that the erythropoiesis regulation in the ascitic birds is defective. In the present study, the ascitic broilers underwent metabolic stress during their exposure to low Ta. Their reaction to this stress could have been exhibited in a significantly increased plasma corticosterone concentration that persisted and then increased further approximately 2 wk before death. Such a stress response might be attributed to the continuous hypoxemia. These alterations in the corticosterone concentration was linearly correlated to hematocrit (r = 0.822) and may partially account for the defective erythropoiesis regulation that led to accelerated proliferation of erythroid progenitors with impaired differentiation and resulted in the accumulation of immature erythrocytes in the bloodstream (Wessely et al., 1997; Bauer et al., 1999). Ascitic chickens also exhibited hypothyroidism (Luger et al., 2001), showing significantly lower plasma concentrations of both T4 and T3. The role of T3 as a significant controller of erythrocyte differentiation (Dinnen et al., 1994; Bauer et al., 1998), also contributed to the increase in production of immature red blood cells and to the reduction of blood hemoglobin content (Luger et al., 2002).
It may be concluded that acute cold exposure that leads to significant stress response, coupled with the failure to produce sufficient thyroid hormones, may explain the enhanced erythropoiesis, including the marked proportion of immature red blood cells that contributed to hypoxemia and to the development of the ascites syndrome.
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Implications
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These findings shed light on the significant involvement of an inefficient erythropoiesis process that contributed to aggravation of the development of ascites syndrome in broiler chickens. Results further elucidate the complexity of the syndrome that causes major economic losses in the poultry industry.
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Footnotes
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1 Contribution from the Agricultural Research Organization, the Volcani Center, Bet Dagan, Israel. No. 403/2002. This study was supported by the Egg and Poultry Board of Israel. We wish to thank M. Rusal, V. Rzepakovsky, and V. Bresler for technical assistance. 
Received for publication August 28, 2002.
Accepted for publication November 21, 2002.
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Abstract
Introduction
