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Effects of Escherichia coli Challenge and Transport Stress on Hematology and Serum Chemistry Values of Three Genetic Lines of Turkeys¹

G. R. Huff^*,2, W. E. Huff^*, N. C. Rath^*, N. B. Anthony and K. E. Nestor

^* US Department of Agriculture, Agricultural Research Service, Poultry Production and Product Safety Research Unit, Fayetteville, AR 72701; Department of Poultry Science, University of Arkansas, Fayetteville 72701; and Department of Animal Science, The Ohio State University, Ohio Agricultural Research and Development Center, Wooster 44691

² Corresponding author: grhuff{at}uark.edu

	ABSTRACT

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Three lines of turkeys were compared for response to an Escherichia coli challenge followed by transport stress (transport). The turkey lines were a slow-growing line selected for increased egg production (egg line), a fast-growing line selected for increased 16-wk BW (F line), and a commercial line (Comm line). Birds were challenged at 14 wk of age with an air sac injection of 5,000 to 10,000 cfu of E. coli. At 8 d postchallenge, birds were subjected to a transport stress procedure that included 12 h of holding time in a transport vehicle. The following morning all birds (n = 10 to 19 birds/line) were bled. Whole blood was analyzed using the Cell-Dyn 3500 blood analysis system (Abbott Diagnostics), and serum chemistry was measured using the Express Plus analyzer (Ciba-Corning Diagnostics Corp.). Transport significantly decreased the levels of hematocrit, hemoglobin, mean cell volume, mean corpuscular hemoglobin, glucose, triglycerides, cholesterol, phosphorus, iron, albumin, and alkaline phosphatase (AP) and increased the levels of uric acid, blood urea nitrogen, alanine aminotransferase, aspartate aminotransferase, and creatine kinase. Line differences were variable, but the levels of both iron and AP were least in the fastest-growing Comm line birds and greatest in the slowest-growing egg-line birds with intermediate values in the F line. Iron and AP were also the only parameters influenced by sex, with males having greater levels of both compared with females. The creatine kinase levels were more than 6-fold greater in transported Comm line birds, and iron levels of transported Comm males were 3-fold less than controls. Previously, the growth rate of these lines was positively correlated with increased heterophil to lymphocyte ratios and susceptibility to colibacillosis. The differences seen in the Comm line for these commonly measured blood parameters suggest that they may be useful for profiling flocks to determine their response to transport stress and feed withdrawal.

Key Words: turkey • transport stress • creatine kinase • iron • Escherichia coli

	INTRODUCTION

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Stress can be described as any change in the environment that elicits a reaction of the hypothalamic-pituitary-adrenal axis (the fight or flight response) and the resulting endocrine, immune, and behavioral changes that accompany this response. The stress response has strong individual variation, and the genes responsible for these differences are being investigated (Redei, 2008). There are many environmental, social, and management stressors that can produce a stress response during poultry production (Gross and Siegel, 1988; Siegel, 1995). Those of importance in the later stages can include temperature extremes, ammonia, dust, endotoxin, disease, overcrowding and social hierarchy, lighting schedules, management failures to provide feed or water, wet litter, moving birds in a multi-house growout system, and finally catching and transportation to the processing plant. In addition, the growth rate of highly productive modern strains has been associated with the development of undesirable metabolic changes (Scheele, 1997).

Modern turkey production has benefited from the intensive selection of strains that profitably produce either meat or eggs and correlated responses in stress-related behaviors have been observed. Relative to egg strains, meat strains that have been selected for fast growth have been described as docile with excessive appetites, decreased motor ability, and poor immunoresponsiveness (Siegel, 1989). The association between fast growth and decreased disease resistance of turkeys has come primarily through the study of 4 closed genetic turkey lines developed at the Ohio Agricultural Research and Development Center (OARDC) at The Ohio State University. These lines include a randombred control line (RBC1) and its subline (egg-line) selected exclusively for increased egg production over a 250-d period and another randombred control (RBC2) and its subline selected for increased 16-wk BW (F-line; Anthony et al., 1991; Nestor et al., 2000; Emmerson et al., 2002). Differences in behavior, stress response, and disease susceptibility have been previously reported between the OARDC egg line and the F line as well as between both of these and an even faster growing commercial line. The fast-growing lines had greater airsacculitis scores, mortality incidence, and heterophil/lymphocyte ratios (H/L) when challenged with Escherichia coli and subjected to transport stress (Huff et al., 2005, 2006, 2007).

The stress of catching and transportation is perhaps the most severe environmental change experienced by turkeys and usually includes feed withdrawal because this practice is known to improve food safety by decreasing fecal contamination. A more subtle stressor, that affects birds throughout their lifespan, is respiratory exposure to fecal pathogens and their endotoxins in the litter. Systemic infection with E. coli, or colibacillosis, is a chronic stressor of poultry (Butler et al., 1977) and is also exacerbated by stress. Colibacillosis is one of the most important diseases of poultry production and is the leading cause of condemnation (Barnes et al., 2003). The behavioral and physiological response of chickens to lipopolysaccharide endotoxin has been shown to have a heritable component in challenges of genetically distinct chicken lines (Cheng et al., 2004). Exposure to E. coli and its lipopolysaccharide endotoxin results in a stress response that increases the H/L, an important indicator of stress in birds (Gross and Siegel, 1983). This response has recently been compared in chickens to that induced by dietary corticosterone and was found to have different effects on the ultra-structural morphology of heterophils and lymphocytes (Shini et al., 2008a) as well as on biological responses including metabolic, growth, and immune activities (Shini et al., 2008b).

The objective of the present study was to analyze the hematological and clinical chemistry profiles resulting from an E. coli challenge followed by transport stress in turkeys with different genetic backgrounds to determine changes in serum hematology and biochemical parameters that may be useful for profiling the level of stress in commercial turkey production.

	MATERIALS AND METHODS

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Three genetic lines of turkeys were compared for their hematological and clinical chemistry responses to transport stress and E. coli challenge. The turkey lines were the egg line, the F line, and a commercial line (Comm). The birds from the egg and F lines were the progeny of a hatch of eggs obtained from the OARDC, Wooster, Ohio. The hatch consisted of 66 egg-line birds and 42 F-line birds of mixed sex. Fifty Comm poults of mixed sex were obtained from a commercial turkey hatchery at 1 d of age and were transported to housing facilities and set in pens on the same day as the closed lines. All turkeys were reared in floor pens on pine shavings, given ad libitum access to a standard corn and soybean turkey ration meeting or exceeding the NRC recommended allowances (National Research Council, 1994), and were kept under incandescent lighting on a light schedule consisting of 23L:1D. For the first 2 wk the birds were brooded under heat lamps in a single pen for each line. At 2 wk of age they were separated into 12 pens in a 3 line x 2 treatment design with 2 replicate floor pens for each line x treatment group. Five or 6 birds were placed into each of the control pens and 7 to 10 birds were placed into each of the challenge pens where they were maintained until 13 wk of age. All animal research procedures were evaluated and approved by the Institutional Animal Care and Use Committee of the University of Arkansas.

E. coli Challenge

At 14 wk of age challenged birds were inoculated in the left cranial-thoracic air-sac with sterile tryptose phosphate broth (TPB) containing approximately 5,000 to 10,000 cfu of a nonmotile strain of E. coli serotype O2, which had originally been isolated from chickens with colisepticemia. The inoculum was prepared by adding 2 loopfulls of an overnight culture on blood agar to 100 mL of TPB and incubating for 2.5 h in a 37°C shaking water bath. The culture was held overnight at 4°C while a standard plate count was made. Ten-fold dilutions were then made in TPB based on the standard plate count.

Transport Stress

Eight days after the bacterial challenge, all challenged birds were subjected to the following transport stress procedure which included a total of 12 h of holding time in the transport vehicle without feed or water. Birds were loaded into an open-fenced trailer covered with a tarp. The egg-line birds were separated from the other 2 lines by a fence to protect them from the larger birds. The temperature ranged from 18 to 21°C, and there was a slight drizzle. The birds were driven around the University farm facilities for 3 h with occasional stops. They were then driven to the University Pilot Processing Plant, where the transport vehicle was parked in a covered holding area. After a total of 12 h from time of loading, birds were returned to their original pens where they had access to feed and water. These birds that were both challenged with E. coli and then later subjected to transport stress will be referred to as transport.

Bleeding

The morning after transport stress, 69 surviving birds were weighed and bled by venipuncture and blood was delivered to glass serum-collecting tubes without coagulant and EDTA-coated tubes. All treated birds and untreated control birds were bled at the same time, which was 12 h after the end of the transport period and 9 d after challenge with E. coli. Total red blood cell counts (RBC), hemoglobin concentration (HGB), hematocrit (HCT), mean cell volume (MCV), mean corpuscular hemoglobin (MCH), and mean corpuscular hemoglobin concentration (MCHC) were measured in whole blood using a Cell-Dyn 3500 blood analysis system (Abbott Diagnostics, Abbott Park, IL), which employs both electronic impedance and laser light scattering and has been standardized for analysis of turkey blood. All samples were analyzed within 2 h of collection.

Before serum was collected, blood samples were held at room temperature for 4 h and were then refrigerated overnight. Serum samples were frozen at µ20°C, and all samples were thawed and assayed at the same time. Clinical chemistry analysis of serum levels of calcium, phosphorus, total protein, albumin, glucose, triglycerides, cholesterol, uric acid, blood urea nitrogen (BUN), iron, and the enzyme activities of alkaline phosphatase (AP), alanine aminotransferase (ALT), aspartate aminotransferase (AST), and creatine kinase (CK) were measured using the Express Plus (Ciba-Corning Diagnostics Corp., Medfield, MA) automated clinical chemistry analyzer according to the manufacturer’s directions. The assays have been previously validated for use with poultry serum samples. At 15 wk and 4 d of age birds were weighed, sexed, and necropsied as described previously (Huff et al., 2006).

Statistics

Pen means were analyzed as a 3 x 2 x 2 factorial arrangement (line x treatment x sex) using the general linear models procedure of SAS software, and main effect means were separated using Duncan’s multiple range test (SAS Institute Inc., 2004). When there were no interactive effects due to sex, data were analyzed as a 3 x 2 factorial arrangement (line x treatment). When treatment and line interactions were significant, treatment means within line and line means within treatment were separated using the least squares means procedure of SAS software. A P-value of less than 0.05 was considered significant unless otherwise stated.

	RESULTS

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Determination of sex at necropsy revealed that blood samples from male and female birds, respectively, in each line were as follows: egg line, 10/12; F line, 10/9; Comm line 15/13. There were no significant differences between the sexes for any of the values presented in Tables 1, 2, or 3, so male and female values were combined. The main effect mean (MEM) for treatment was significant for HCT, HGB, MCV, and MCH, which were all decreased by transport (Table 1). The MEM for line was significant for MCV and MCH with the egg line having lower MCV levels compared with the other 2 lines and the F line having greater MCH levels than the 2 other lines. There were no significant treatment x line interactions for the values in Table 1.

Treatment significantly affected MEM for serum levels of uric acid, BUN, albumin, ALT, AST, and CK (Table 3). Transport increased uric acid, BUN, ALT, AST, and CK and decreased albumin. The MEM differences for line were significant for uric acid, albumin, and CK (Table 3). Uric acid levels were lower in the Comm line as compared with both other lines. Albumin was greater in the egg line as compared with the Comm line, and CK was greater in the egg line as compared with the F line. There were significant treatment x line interactions for uric acid, albumin, and AST.

Sex significantly affected MEM for both iron and AP levels with females having lower levels than males (Table 4). The MEM for treatment and line were also significant for iron and AP. Transport decreased iron and AP compared with the control. The Comm line had lower iron levels as compared with both other lines. The egg line had the greatest levels of AP, whereas the Comm line had the least level and the F line was intermediate. There were significant treatment x line interactions for iron and AP levels.

	DISCUSSION

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The parameter most highly affected by transport stress in this study was CK, which was increased 6-fold on average, and in the egg line was increased 19-fold. Creatine kinase is an indicator of muscle growth (Hagiwara et al., 1989) and damage (Hochleithner, 1994), and CK activity in turkeys has been reported as being extremely sensitive to physical stress and exercise (Hochleithner, 1994). Creatine kinase activity has been reported to increase dramatically from d 3 to wk 20 in a fast-growing turkey line (Szabó et al., 2005) and to be greater in fast-growing turkey lines as compared with slower growing lines (Wilson et al., 1990; Kowalski et al., 2002). In the present study, control birds from the 2 fast growing lines had numerically greater CK values compared with the egg line, but whereas transport had a highly significant effect on all 3 lines, the slow-growing egg line had the greatest increase as a result of transport.

Creatine kinase has been suggested as a marker for the degree of stress susceptibility in pigs, with the suggestion that the stress resistance of some genetic lines is reflected by the degree of muscle cell membrane permeability (Reddy et al., 1971). Transport stress has been shown to increase CK levels in broilers (Mitchell et al., 1992; Scholtyssek and Ehinger, 1976), pigeons (Scope et al., 2002), pigs (Boss and McMurray, 1979; Yu et al., 2007), catfish (Ellsaesser and Clem, 1987), cattle (Warriss et al., 1995; Maria et al., 2004), sheep (Knowles et al., 1998), horses (Codazza and Redaelli, 1974), and wild chamois (López-Olvera et al., 2006). Creatine kinase levels were also increased by the stress of capture in ducks (Bollinger et al., 1989; Dabbert and Powell, 1993) and in wild turkeys (Nicholson et al., 2000). The findings from those studies indicate that CK increase may be a valuable marker for the degree of stress imposed by catching and transport. The changes seen in CK activity in wild turkeys after capture were correlated with mortality at 14 d postcapture, suggesting that susceptible individuals could be identified by their CK response (Nicholson et al., 2000).

Transport also increased serum levels of the enzymes ALT and AST, as well as decreased AP. Increases in ALT are nonspecific and can be due to damage of almost any tissue, whereas increases in AST are indicative of liver or muscle damage (Hochleithner, 1994). The levels of AST seen in transported birds in the present study are 2- to 5-fold greater than the reported reference values for wild turkeys of 255 to 499 IU/L (Bounous et al., 2000).

The ALT and AST have been reported to increase and AP to decrease in a commercial turkey strain with age from 3 d to 20 wk. The increases seen in ALT and AST were suggested to be indicative of intensive growth and expressed muscle hypertrophy as the result of single-sided selection for meat production and high white glycolytic muscle mass (Szabó et al., 2005).

Transport has previously been shown to increase AST levels in captured ducks (Bollinger et al., 1989; Dabbert and Powell, 1993), and in transported pigs (Yu et al., 2007) and wild chamois (López-Olvera et al., 2006). Transported wild chamois also had increased levels of ALT, which along with increases in AST, CK, and LDH have been used to determine the degree of stress in transported wild ungulates (López-Olvera et al., 2006).

In the present study uric acid levels were increased by transport, in agreement with previous reports in which transport stress was found to increase uric acid levels in 3 out of 7 broiler flocks and decrease glucose levels in 4 out of 7 flocks tested, however the mean values of these 7 flocks were not statistically different (Halliday et al., 1977). Plasma uric acid is a major antioxidant in birds and is a reliable indicator of oxidative stress and kidney tubular function (Hartman et al., 2006). However, contrary to these results, transport stress in pigeons decreased uric acid levels (Scope et al., 2002).

For most parameters the differences between lines were variable, but the levels of iron and AP were indirectly correlated with growth rate, with male Comm line birds having the lowest levels. The MEM for iron and AP were also the only parameters influenced by sex, with males having greater levels of both compared with females, and iron and AP levels were decreased by transport. The transported male Comm line iron levels were 3-fold lower than its control and were equivalent to the female Comm line levels. Previously, the growth rate of these lines was positively correlated with an increased H/L and also with increased susceptibility to colibacillosis (Huff et al., 2005, 2006).

Iron has an important role in resistance to infection because it is necessary for development and differentiation of immune cells and is involved in regulation of cell-mediated immune pathways and cytokine activity (Weiss, 2002, 2005). Chronic inflammatory disease has been shown to divert iron from the circulation to the reticuloendothelial system (Weiss, 2005) where high levels can increase susceptibility to bacterial infection (Jurado, 1997; Khan et al., 2007; Nairz et al., 2007).

The current data suggest that turkey serum enzyme levels may be useful for determining the response to stress. The highly significant increases seen in the transport birds for CK, ALT, and AST, and the decreases seen in AP and iron may be used for profiling individuals and flocks to determine their responses to transport stress and feed withdrawal and possibly more general stress responses. The determination of stress-susceptible individuals may be useful in the genetic selection of turkeys with a moderate response to the stressors of commercial turkey production.

	ACKNOWLEDGMENTS

 
The authors gratefully acknowledge the excellent technical assistance of Dana Bassi, Sonia Tsai, Scott Zornes, David Horlick, and Wally McDonner (USDA-Agricultural Research Service-Poultry Production and Product Safety Research Unit, Fayetteville, AR) and Linda Stamps (University of Arkansas, Fayetteville).

	FOOTNOTES

 
¹ Mention of a trade name, proprietary product, or specific equipment does not constitute a guarantee or warranty by the USDA and does not imply its approval to the exclusion of other products that may be suitable.

Received for publication March 26, 2008. Accepted for publication June 17, 2008.

	REFERENCES

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Anthony, N. B., D. A. Emmerson, and K. E. Nestor. 1991. Genetics of growth and reproduction. 12. Results of long-term selection for increased 180-d egg production. Poult. Sci. 70:1314–1322.[Web of Science][Medline]

Barnes, H. J., J. P. Vaillancourt, and W. B. Gross. 2003. Colibacillosis. Pages 631–656 in Diseases of Poultry. 11th ed. Y. M. Saif, ed. Iowa State Press, Ames, IA.

Bollinger, T., G. Wobeser, R. G. Clark, D. J. Nieman, and J. R. Smith. 1989. Concentration of creatine kinase and aspartate aminotransferase in the blood of wild mallards following capture by three methods for banding. J. Wildl. Dis. 25:225–231.[Abstract]

Boss, B. W., and C. H. McMurray. 1979. The effect of the duration and type of stress on some serum enzyme levels in pigs. Res. Vet. Sci. 26:1–6.[Web of Science][Medline]

Bounous, D. I., and N. L. Stedman. 2000. Normal Avian Hematology: Chicken and Turkey. Pages 1147–1154 in Schalm’s Veterinary Hematology. B. F. Feldman, J. G. Zinkl, and N. C. Jain, ed. Lippincott Williams & Wilkins, Philadelphia, PA.

Bounous, D. I., R. D. Wyatt, P. S. Gibbs, J. V. Kilburn, and C.F. Quist. 2000. Normal hematologic and serum biochemical reference intervals for juvenile wild turkeys. J. Wildl. Dis. 36:393–396.[Abstract]

Butler, E. J., M. J. Curtis, and E. G. Harry. 1977. Escherichia coli endotoxin as a stressor in the domestic fowl. Res. Vet. Sci. 23:20–23.[Web of Science][Medline]

Campbell, T. W., and C. K. Ellis. 2007. Avian and Exotic Animal Hematology and Cytology. Blackwell Publishing, Ames, IA.

Cheng, H. W., R. Freire, and E. A. Pajor. 2004. Endotoxin stress responses in chickens from different genetic lines.1. Sickness, behavioral, and physical responses. Poult. Sci. 83:707–715.[Abstract/Free Full Text]

Codazza, D. G. M., and G. Redaelli. 1974. Serum enzyme changes and haematochemical levels in thoroughbreds after transport and exercise. 1974. J. S. Afr. Vet. Assoc. 45:331–333.

Dabbert, C. B., and K. C. Powell. 1993. Serum enzymes as indicators of capture myopathy in mallards (Anas platyrhynchos). J. Wildl. Dis. 29:304–309.[Abstract]

Ellsaesser, C. F., and L. W. Clem. 1987. Blood serum chemistry measurements of normal and acutely stressed channel catfish. Comp. Biochem. Physiol. 88A:589–594.[CrossRef][Medline]

Emmerson, D. A., S. G. Velleman, and K. E. Nestor. 2002. Genetics of growth and reproduction in the turkey. 15. Effects of long-term selection for increased egg production on the genetics of growth and egg production traits. Poult. Sci. 81:316–320.[Abstract/Free Full Text]

Gross, W. B., and H. S. Siegel. 1983. Evaluation of the heterophil/lymphocyte ratio as a measure of stress in chickens. Avian Dis. 27:972–979.[CrossRef][Web of Science][Medline]

Gross, W. B., and P. B. Siegel. 1988. Environment-genetic influences on immunocompetence. J. Anim. Sci. 66:2091–2094.[Abstract/Free Full Text]

Hagiwara, Y., T. Shimo-Oka, K. Okamura, and E. Ozawa. 1989. Basis for the assay of myogenic cell growth using creatine kinase activity as an index, with special reference to measurement of power ratio of transferrins in growth promotion. Jpn. J. Pharmacol. 49:53–58.[CrossRef][Medline]

Halliday, W. G., J. G. Ross, G. Christie, and R. M. Jones. 1977. Effect of transportation on blood metabolites in broilers. Br. Poult. Sci. 18:657–659.[CrossRef][Web of Science][Medline]

Hartman, S., S. A. Taleb, T. Geng, K. Gyenai, X. Guan, and E. Smith. 2006. Comparison of plasma uric acid levels in five varieties of the domestic turkey. Poult. Sci. 85:1791–1794.[Abstract/Free Full Text]

Hochleithner, M. 1994. Biochemistries. Pages 223–244 in Avian Medicine: Principles and Application. B. W. Ritchie, G. J. Harrison, and L. R. Harrison, ed. Wingers Publishing Inc., Lake Worth, FL.

Huff, G., W. Huff, N. Rath, A. Donoghue, N. Anthony, and K. Nestor. 2007. Differential effects of sex and genetics on behavior and stress response of turkeys. Poult. Sci. 86:1294–1303.[Abstract/Free Full Text]

Huff, G. R., W. E. Huff, J. M. Balog, N. C. Rath, N. B. Anthony, and K. E. Nestor. 2005. Stress response differences and disease susceptibility reflected by heterophil to lymphocyte ratio in turkeys selected for increased body weight. Poult. Sci. 84:709–717.[Abstract/Free Full Text]

Huff, G., W. Huff, N. Rath, J. Balog, N. B. Anthony, and K. Nestor. 2006. Stress-induced colibacillosis and turkey osteomyelitis complex in turkeys selected for increased body weight. Poult. Sci. 85:266–272.[Abstract/Free Full Text]

Jurado, R. L. 1997. Iron, infections, and anemia of inflammation. Clin. Infect. Dis. 25:888–895.[Web of Science][Medline]

Khan, F. A., M. A. Fisher, and R. A. Khakoo. 2007. Association of hemochromatosis with infectious diseases: Expanding spectrum. Int. J. Infect. Dis. 11:482–487.[CrossRef][Web of Science][Medline]

Knowles, T. G., P. D. Warriss, S. N. Brown, and J. E. Edwards. 1998. Effects of stocking density on lambs being transported by road. Vet. Rec. 142:503–509.[Abstract/Free Full Text]

Kowalski, A., P. Mormede, K. Jakubowski, and M. Jedlinska-Krakowska. 2002. Comparison of susceptibility to stress in two genetic lines of turkey broilers BUT-9 and Big-6. Pol. J. Vet. Sci. 5:145–150.[Medline]

López-Olvera, J. R., I. Marco, J. Montané, and A. Lavín. 2006. Transport stress in Southern chamois (Rupicapra pyrenaica) and its modulation by acepromazine. Vet. J. 172:347–355.[CrossRef][Web of Science][Medline]

Maria, G. A., M. Villarroel, G. Chacìon, and G. Gebresenbet. 2004. Scoring system for evaluating the stress to cattle of commercial loading and unloading. Vet. Rec. 154:818–821.[Abstract/Free Full Text]

Mitchell, M. A., P. J. Kettlewell, and M. H. Maxwell. 1992. Indicators of physiological stress in broiler chickens during road transportation. Anim. Welf. 1:91–103.

Nairz, M., I. Theurl, S. Ludwiczek, M. Theurl, S. M. Mair, G. Fritsche, and G. Weiss. 2007. The co-ordinated regulation of iron homeostasis in murine macrophages limits the availability of iron for intracellular Salmonella typhimurium. Cell. Microbiol. 9:2126–2140.[CrossRef][Web of Science][Medline]

National Research Council. 1994. Nutrient Requirements of Poultry. National Academy Press, Washington, DC.

Nestor, K. E., J. W. Anderson, and R. A. Patterson. 2000. Genetics of growth and reproduction in the turkey. 14. Changes in genetic parameters over thirty generations of selection for increased body weight. Poult. Sci. 79:445–452.[Abstract/Free Full Text]

Nicholson, D. S., R. L. Lochmiller, M. D. Stewart, R. E. Masters, and D. M. Leslie Jr. 2000. Risk factors associated with capture-related death in eastern wild turkey hens. J. Wildl. Dis. 36:308–315.[Abstract]

Nijdam, E., E. Delezie, E. Lambooij, M. J. Nabuurs, E. Decuypere, and J. A. Stegeman. 2005. Feed withdrawal of broilers before transport changes plasma hormone and metabolite concentration. Poult. Sci. 84:1146–1152.[Abstract/Free Full Text]

Reddy, M. V. V., L. L. Kastenschmidt, R. G. Cassens, and E. J. Briskey. 1971. Studies on stress-susceptibility: The relationship between serum enzyme changes and the degree of stress-susceptibility. Life Sci. 10:1381–1391.

Redei, E. E. 2008. Molecular genetics of the stress-responsive adrenocortical axis. Ann. Med. 40:139–148.[CrossRef][Web of Science][Medline]

SAS Institute Inc. 2004. SAS/STAT 9.1 User’s Guide, Cary, NC.

Scheele, C. W. 1997. Pathological changes in metabolism of poultry related to increasing production levels. Vet. Q. 19:127–130.[Web of Science][Medline]

Scholtyssek, S., and F. Ehinger. 1976. Effects of transportation on broilers and broiler carcasses. Arch. Geflugelkd. 40:27–35.

Scope, A., T. Filip, C. Gabler, and F. Resch. 2002. The influence of stress from transport and handling on hematologic and clinical chemistry blood parameters of racing pigeons (Columba livia domestica). Avian Dis. 46:224–229.[CrossRef][Web of Science][Medline]

Shini, S., P. Kaiser, A. Shini, and W. L. Bryden. 2008a. Differential alterations in ultrastructural morphology of chicken heterophils and lymphocytes induced by corticosterone and lipopolysacharides. Vet. Immunol. Immunopathol. 122:83–93.[CrossRef][Web of Science][Medline]

Shini, S., P. Kaiser, A. Shini, and W. L. Bryden. 2008b. Biological response of chickens (Gallus gallus domesticus) induced by corticosterone and a bacterial endotoxin. Comp. Biochem. Physiol. B 149:324–333.[CrossRef][Medline]

Siegel, H. S. 1995. Stress, strains and resistance. Br. Poult. Sci. 36:3–22.[Web of Science][Medline]

Siegel, P. B. 1989. The genetic-behavior interface and well-being of poultry. Br. Poult. Sci. 30:3–13.[CrossRef][Web of Science][Medline]

Szabó, A., M. Mézes, P. Horn, Z. Sütö, Gy. Bázár, and R. Romvári. 2005. Developmental dynamics of some blood biochemical parameters in the growing turkey (Meleagris gallopavo). Acta Vet. Hung. 53:397–409.[CrossRef][Web of Science][Medline]

Warriss, P. D., S. N. Brown, J. G. Knowles, S. C. Kestin, J. E. Edwards, S. K. Dolan, and A. J. Phillips. 1995. Effects on cattle of transport by road for up to 15 hours. Vet. Rec. 136:319–323.[Abstract]

Weiss, G. 2002. Iron and immunity: A double-edged sword. Eur. J. Clin. Invest. 32(Suppl 1):70–78.[CrossRef][Web of Science][Medline]

Weiss, G. 2005. Modification of iron regulation by the inflammatory response. Best Pract. Res. Clin. Haematol. 18:183–201.[Medline]

Wilson, B. W., P. S. Nieberg, R. J. Buhr, B. J. Kelly, and F. T. Shultz. 1990. Turkey muscle growth and focal myopathy. Poult. Sci. 69:1553–1562.[Web of Science][Medline]

Yu, H., E. D. Bao, R. Q. Zhao, and Q. X. Lv. 2007. Effect of transportation stress on heat shock protein 70 concentration and mRNA expression in heart and kidney tissues and serum enzyme activities and hormone concentrations of pigs. Am. J. Vet. Res. 68:1145–1150.[CrossRef][Web of Science][Medline]

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