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Effect of Selection for Increased Body Weight in Turkeys on Lymphoid Organ Weights, Phagocytosis, and Antibody Responses to Fowl Cholera and Newcastle Disease-Inactivated Vaccines1
BREEDING AND GENETICS Effect of Selection for Increased Body Weight in Turkeys on Lymphoid Organ Weights, Phagocytosis, and Antibody Responses to Fowl Cholera and Newcastle Disease-Inactivated Vaccines1 Z. Li,* K. E. Nestor,*,2 Y. M. Saif,† J. W. Anderson,* and R. A. Patterson* *Department of Animal Sciences; and †Food Animal Health Research Program, The Ohio State University, Wooster, Ohio 44691 relative weight of spleen, and ratio of spleen to bursa of Fabricius weight (P < 0.01) but had a lower relative weight of bursa of Fabricius at 9 wk of age. However, there were no line differences in the antibody responses to Newcastle disease virus or P. multocida vaccines at 1, 2, 3, 4, 5, or 12 wk after vaccination. Based on the present results, it is suggested that long-term selection for increased 16-wk BW might have resulted in changes in the immune system, as indicated by changes in the relative weights of the spleen and bursa of Fabricius and phagocytic activity. The decreased phagocytic activity in the F line may be partially responsible for increased susceptibility to specific diseases in this line.
(Key words: turkey, growth selection, antibody response, organ weight, phagocytosis) 2001 Poultry Science 80:689–694
than corresponding lines selected for low antibody response. However, Biozzi et al. (1975, 1979a) reported that a line of mice selected for low antibody response to several antigens was more resistant to challenge by some infectious agents. Previous reports showed that a turkey line (F), selected for increased 16-wk BW and exhibiting an increase of about 75% in the 16-wk BW of male turkeys in comparison to its randombred control line (RBC2) (Nestor et al., 1996b), was more susceptible than the RBC2 line to erysipelas, P. multocida, and Newcastle disease virus (NDV) (Saif et al., 1984; Sacco et al., 1991; Tsai et al., 1992; Nestor et al., 1996b, 1999). However, the F-line turkeys had higher anti-NDV titers than the RBC2 line at 3 wk following primary and secondary immunizations (Sacco et al., 1994). Line differences were inconsistent for anti-P. multocida titers at 3 wk following the primary vaccination when the antibody was detected with ELISA during a 2yr experiment (Sacco et al., 1994). The F line had a higher serum IgM, but not IgG, concentration than the RBC2
INTRODUCTION Individuals depend on the harmony of phagocytosis and cell-mediated and humoral immunities to develop resistance to infectious diseases. These three facets of the immune system are interactive but are under separate genetic control in mice (Biozzi et al., 1979b, 1982). Phagocytosis is important in general disease resistance (Lamont, 1986). Selection for antibody response to one nonreplicating antigen in chicken lines resulted in enhanced responses to other antigens and, therefore, might have improved general disease resistance (Gross et al., 1980; Siegel and Gross, 1980; Cheng and Lamont, 1988; Heller et al., 1992). In addition, chickens selected for high antibody response to Pasteurella multocida (Hofacre et al., 1986) or Escherichia coli (Pitcovski et al., 1987; Leitner et al., 1992) vaccines were more resistant to challenge with these organisms
2001 Poultry Science Association, Inc. Received for publication December 9, 1999. Accepted for publication January 15, 2001. 1 Salaries and research support were provided by state and federal funds appropriated to the Ohio Agricultural Research and Development Center, The Ohio State University. 2 To whom correspondence should be addressed: [email protected].
Abbreviation Key: CCA = carbon clearance assay; F = subline of RBC2 selected long-term for increased 16 wk BW; NDV = Newcastle disease virus; OD = optical density; PV = postvaccination; RBC2 = randombred control line.
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ABSTRACT The influence of selection was studied for increased 16-wk BW in turkeys on in vivo phagocytic activity, antibody responses to vaccines, and weight of the spleen and bursa of Fabricius. A line (F) of turkeys selected long term for increased 16-wk BW and its corresponding randombred control (RBC2) were compared. Phagocytic activity was evaluated by the carbon clearance assay. Antibody responses to inactivated Newcastle disease virus and Pasteurella multocida vaccines were examined by ELISA. Body weight and relative weights of spleen and bursa of Fabricius of the two lines were also compared. The F line had lower phagocytic activity than the RBC2 line (P < 0.05). In addition, the F line had greater BW,
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MATERIALS AND METHODS Turkeys and Management Two lines (RBC2 and F) of turkeys were used in the present study. Line RBC2 was a randombred control initiated in 1966 (Nestor, 1977a), whereas Line F, a subline of RBC2, was selected over 33 generations for increased 16-wk BW (Nestor, 1977b, 1984; Nestor et al., 1996a). The breeder flocks that produced the poults used were vaccinated with an attenuated NDV vaccine via eye drops, in September, then with an inactivated NDV vaccine subcutaneously in November, and with an avian encephalomyelitis vaccine subcutaneously in October but were not vaccinated for P. multocida. The poults were grown intermingled, sexes separate, in confinement. The birds were provided water and a multiple-ration system, ad libitum, with declining protein (Naber and Touchburn, 1970).
Vaccination and Antibody Response Ten males and ten females from each line were used for each vaccine. Poults were vaccinated subcutaneously at 6 wk of age (in April) with an inactivated NDV vaccine3 or P. multocida bacterin.3 Individual blood samples were collected prior to vaccination (0 wk) and at 1, 2, 3, 4, 5, and 12 wk postvaccination (PV). Sera were separated and stored frozen at −20 C until analysis. Serum samples were assayed simultaneously for antibody levels to P. multocida and NDV by using commercial ELISA test kits4 as instructed. Optical density (OD) values were read at 630 nm by an EIA microplate reader.5 Antibody levels were expressed as the ratio of sample to positive controls as follows: (sample OD mean − negative control OD mean)/ (positive control OD mean − negative control OD mean). Throughout this manuscript, the antibody ratio will be referred to as titer.
3
Maine Biological Laboratories, Waterville, ME 04903. IDEXX Corp., Portland, ME 04104. 5 Bio-Rad Laboratory, Richmond, CA 94801. 6 Anthes Universal Ltd., Brampton, ONT L6W 3K8. 4
Carbon Clearance Assay Six male and six female 6-wk-old poults from each line were used in the carbon clearance assay (CCA). The CCA was used to estimate the in vivo phagocytic activity based on methods described elsewhere (Glick et al., 1964; Lamont, 1986; Heller et al., 1992). Briefly, the supernatant fraction of India ink (Pelikan 518.21A 862)6 was obtained through centrifugation (300 × g for 30 min), and 1.5 mL/ kg BW was injected into the brachial vein. Blood (100 µL) was taken from the opposite wing before injection (0 min) and at 3, 6, and 15 min after the carbon injection and then was transferred immediately into 2.0 mL of 1.0% sodium citrate. After centrifugation (50 × g for 4 min), the relative amount of carbon particles remaining in the supernatant was spectrophotometrically measured by absorbance at a wavelength of 675 nm with the samples at 0 min as zero values.
Relative Weight of Spleen and Bursa of Fabricius Twenty-seven, 9-wk-old turkeys from each line were used. Turkeys were weighed, euthanatized by CO2 asphyxiation, and necropsied. The weights of spleen and bursa of Fabricius were recorded, and the relative weights of spleen and bursa of Fabricius and the ratio of spleen weight to bursa weight were compared between the two lines.
Statistical Analysis The effects of line and sex on antibody titers, carbon clearance, and organ weights were analyzed by an ANOVA using the general linear model procedure of SAS software (SAS Institute, 1988). Pearson correlation coefficients were used to analyze the relationship between the antibody ratios at different points in time and BW at 8, 16, and 20 wk. A difference with a probability of P ≤ 0.05 was considered to be statistically significant.
RESULTS There were no significant effects of line or sex on the antibody titers in response to NDV vaccine, except at 12 wk after vaccination (Figure 1). At this time, females had higher antibody titers than males in the RBC2 line and than all birds in the F line (P < 0.05) (data not shown). The Pearson correlation coefficients were generally negative between anti-NDV titers and BW, except at 2 wk PV. There were significant (P < 0.05) correlation coefficients between antibody titers at 5 wk PV and BW at 20 wk (−0.354) and between antibody titers at 12 wk PV and BW at 16 wk (−0.400) or at 20 wk (−0.421) (Table 1). Neither line nor sex affected the antibody titers in the response to P. multocida vaccine (Figure 2). The Pearson correlation coefficients were generally positive between anti-P. multocida titers and BW, except at 12 wk PV (Table 1). There were significant (P < 0.05) correlation coefficients
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line at 6 wk of age (Li et al., 2000b). The RBC2 line had a greater response of peripheral blood mononuclear cells to concanavalin A, but not to phytohemagglutinin M, than the F line (Li et al., 1999a). Polymorphism of the CD8α molecule was more frequent in the F line than in the RBC2 line (Li et al., 1999b). The F line had a larger CD4+CD8− T cell subpopulation than the RBC2 line (Li et al., 2000c). In order to determine the effects of long-term selection for increased BW in turkeys on other aspects of the immune system, lymphoid organ weights, antibody responses to NDV and P. multocida vaccines at various points in time, and phagocytic activity in the two lines were compared in the present study.
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between antibody titers at 3 wk PV and BW at 16 wk (0.357) and at 20 wk (0.421) of age. There was large variation in individual antibody titers within lines. There was no sex difference in carbon clearance as measured at an OD of 675 nm. However, more carbon particles (P < 0.05) remained in the blood of the F-line turkeys than in the RBC2 turkeys at 3 and 6 min (P < 0.05) and at 15 min (P < 0.01) postinjection with India ink (Figure 3), indicating that the F-line poults cleared carbon particles from the circulation system at a slower rate than the RBC2-line birds. Therefore, the in vivo phagocytic activity in the F line was lower than in the RBC2 line. Body weight at 9 wk of age was greater in the F line than in the RBC2 line (P < 0.01) with a significant sex effect as expected (Table 2). Male poults were heavier than female counterparts in both lines (P < 0.001). There were line, but no sex, differences in the relative weight of spleen and bursa of Fabricius as well as the ratio of
FIGURE 2. Antibody titers (ratios) detected with ELISA at different times after vaccination with Pasteurella multocida bacterin vaccine in the F and RBC2 lines of turkeys. RBC2 = randombred control population; F = subline of RBC2 selected for increased 16-wk BW. Values are least squares means with the SE bars. Antibody ratio is expressed in following equation: [sample optical density (OD) mean − negative control OD mean]/(positive control OD mean − negative control OD mean).
spleen to bursa weight (P < 0.01). Compared with the RBC2 line, the F line had a higher relative spleen weight and spleen to bursa weight ratio but had a lower relative weight of the bursa.
DISCUSSION In the present study, line differences in antibody titers between the F and RBC2 lines were not observed at several points in time after vaccination with NDV and P. multocida vaccines in the thirty-third generation of selection in the F line, which was inconsistent with the results of Sacco et al. (1994). Sacco et al. (1994) reported that the F line in the twenty-sixth generation had higher antibody titers than the RBC2 line at 3 wk after vaccination with NDV vaccine. The inconsistency between the two studies might have resulted from differences in the method of antibody detection, sample number, expression of results,
TABLE 1. Pearson correlation coefficients between antibody ratios of turkeys in response to Pasteurella multocida (PM) and Newcastle disease virus (NDV) vaccines measured at different points in time postvaccination and BW at 8, 16, and 20 wk1 Vaccine group NDV
PM
Antibody ratio BW
PV0
PV1
PV2
PV3
PV4
PV5
PV12
8 16 20 8 16 20
−0.287 −0.328 −0.333 0.123 0.023 0.067
0.139 0.034 0.002 0.172 0.132 0.002
−0.061 −0.038 −0.006 0.086 0.092 0.178*
−0.078 −0.032 −0.028 0.130 0.357* 0.421*
−0.174 −0.176 −0.150 0.161 0.230 0.215
−0.264 −0.299 −0.354* 0.200 0.196 0.226
−0.338 −0.400* −0.421* −0.138 −0.139 −0.198
wk wk wk wk wk wk
1 Turkeys were vaccinated with inactivated PM or NDV vaccines at 6 wk of age. PV0, PV1, PV2, PV3, PV4, PV5, and PV12 represent antibody ratios measured prior to vaccination, and at 1, 2, 3, 4, 5, and 12 wk postvaccination, respectively. *P < 0.05.
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FIGURE 1. Antibody titers (ratios) detected with ELISA at different times after vaccination with inactivated Newcastle disease virus vaccine in the F and RBC2 lines of turkeys. RBC2 = randombred control population; F = subline of F selected for increased 16-wk BW. Values are least squares means with the SE bars. Antibody ratio is expressed in following equation: (sample optical density (OD) mean − negative control OD mean)/(positive control OD mean − negative control OD mean).
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or changes in the F line from the twenty-sixth to thirtythird generation of selection. Sacco et al. (1994) detected the antibody in several hundred turkeys with avidinbiotin-based ELISA and expressed the results as mean loge titer. The Pearson correlation coefficients were generally positive between anti-P. multocida titers and BW except at 12 wk PV but were negative between anti-NDV titers and BW except at 2 wk PV. The present results suggest variation in the host’s antibody response to different types of antigens. The spleen and bursa are the important lymphoid organs involved in the development and differentiation of T or B lymphocytes (Eerola et al., 1987; Toivanen et al., 1987). The smaller bursa of Fabricius weight and higher ratio of spleen to bursa weight in the F line may reflect the effect of growth selection on the lymphoid tissues, and these changes in weight possibly resulted in some changes in the lymphocyte subpopulations. In chickens, Muir and Jaap (1967) reported that bursa of Fabricius
TABLE 2. Total body weight and relative weight of the spleen and bursa of Fabricius in the RBC2 and F lines (least squares mean ± SEM)1 Line
Sex
No.
F
Male Female Mean Male Female Mean
14 13 27 15 12 27
BW
Spleen
(kg)
RBC2
5.55 4.46 5.00 2.67 2.13 2.40
Bursa
Spleen:bursa ratio
(% BW) ± ± ± ± ± ±
0.07*** 0.10 0.06A 0.08*** 0.08 0.06B
1.28 1.27 1.27 1.11 1.12 1.11
± ± ± ± ± ±
0.05 0.07 0.04A 0.06 0.06 0.04B
0.89 0.99 0.94 1.09 1.19 1.14
± ± ± ± ± ±
0.05 0.07 0.04B 0.06 0.06 0.04A
1.53 1.31 1.42 1.08 0.96 1.02
± ± ± ± ± ±
0.08 0.12 0.07A 0.09 0.09 0.06B
Line means within columns with no common superscript differ (P < 0.01). Line RBC2 = a randombred control line; Line F = a subline of RBC2 selected for increased 16-wk BW. All poults were 9-wk-old. ***Sexes within lines differ (P < 0.001). A,B 1
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FIGURE 3. Optical density (OD), at 675 nm, of the supernatant fraction from blood samples collected from F and RBC2 line turkeys at 3, 6, and 15 min after injection with India ink (1.5 mL/kg BW). RBC2 = randombred control population; F = subline of RBC2 selected for increased 16 wk BW. Values are the least squares means with the SE bars. *P < 0.05; **P < 0.01.
weight at hatching was negatively associated with posthatching BW. A similar relationship was observed for turkeys in the present study. Bursa of Fabrcius size may not necessarily be associated with antibody titers. Yamamoto and Glick (1982) found that a chicken line selected for small bursa size had higher total and 2-mercaptoethanol-resistant antibody titers in the primary response to SRBC and also had higher total antibody titers in the secondary response compared to the counterparts in the line selected for large bursa size. Ubosi et al. (1985) observed that a chicken line selected for high response to SRBC had a larger bursa size than the line selected for low response. The F line had significantly lower phagocytic activity than the RBC2 line. The function of phagocytosis is mainly performed by macrophages that digest and process the antigens and then present the antigens associated with MHC molecules to T lymphocytes (Lamont, 1986). Neutrophils (heterophils in poultry) are also active phagocytic cells, and eosinophils play a major phagocytic role in the defense against parasitic organisms (Kuby, 1994). Thrombocytes have even been reported to be phagocytic (Glick et al., 1964). Therefore, phagocytosis is a first-line barrier of defense against pathogens and may not be proportional to the level of humoral immune response. Biozzi et al. (1979a) observed higher macrophage activity in a mouse line with lower antibody response. A similar finding was also obtained by Kreukniet et al. (1994), who observed that the phagocytic activity was not correlated with the antibody response in their chicken lines. The F line had a higher antibody response to SRBC (Li et al., 2000a) and higher serum IgM concentration than the RBC2 line (Li et al., 2000b). However, the F line was more susceptible to certain specific infectious diseases (Saif et al., 1984; Sacco et al., 1991; Tsai et al., 1992; Nestor et al., 1996 b,c). Published results and those in the present study suggest that the level of humoral immune response may not account for the increased susceptibility to specific diseases in the F line. Other aspects of the immune system, such as decreased phagocytosis or cellular immune response, may offer a possible explanation for the decreased disease resistance in the F line. In addition, the F line had a lower mitogenic response to concanavalin A and
INFLUENCE OF BODY WEIGHT SELECTION ON THE IMMUNE SYSTEM
ACKNOWLEDGMENTS The authors thank British United Turkeys of America, Lewisberg, WV 14901, and Hybrid Turkeys Inc., Suite C, Kitchner, Ontario, Canada N2K 3S2, for financial support.
REFERENCES Bacon, W. L., K. E. Nestor, D. A. Emmerson, R. Vasilatos-Younken, and D. W. Long, 1991. Circulating IGF-I in plasma of growing male and female turkeys of medium and heavy weight lines. Dom. Anim. Endocrinol. 10:267–277. Bacon, W. L., R. Vasilatos-Younken, K. E. Nestor, B. J. Anderson, and D. W. Long, 1989. Pulsatile patterns of plasma growth hormone in turkeys: effects of growth rate, age, and sex. Gen. Comp. Endocrinol. 75:417–426. Badolato, R., H. M. Bond, G. Valerio, A. Petrella, G. Morrone, M. J. Waters, S. Venuta, and A. Tenore, 1994. Differential expression of surface membrane growth hormone receptor on human peripheral blood lymphocytes detected by dual fluorochrome flow cytometry. J. Clin. Endocrinol. Metab. 79:984–990. Biozzi, G., D. Mouton, A. M. Heumann, and Y. Bouthillier, 1982. Genetic regulation of immunoresponsiveness in relation to resistance against infectious disease. Proc. 2nd World Congress on Genetics Applied to Livestock Production, Madrid, Spain V:150–163. Biozzi, G., D. Mouton, A. M. Heumann, Y. Bouthillier, C. Stiffel, and J. C. Mevel, 1979a. Genetic analysis of antibody responsiveness to sheep erythrocytes in crosses between lines of mice selected for high and low antibody synthesis. Immunology 3:427–438. Biozzi, G., D. Mouton, O. A. Sant’Anna, H. C. Passous, M. Gennari, M. H. Reis, V. C. A. Ferreira, A. M. Heumann, Y. Bouthillier, O. M. Ibanez, and C. Stiffel, 1979b. Genetics of immunoresponsiveness of natural antigens in the mouse. Curr. Top. Microbiol. Immunol. 85:31–98. Biozzi, G., C. Stiffel, D. Moulton, and Y. Bouthillier, 1975. Selection of lines of mice with high and low antibody responses to complex immunogens. Pages 179–228 in: Immunogenetics and Immunodeficiency. B. Becacerraf, ed. University Park Press, Baltimore, MD. Cheng, S., and S. J. Lamont, 1988. Genetic analysis of immunecompetence measures in a White Leghorn chicken line. Poultry Sci. 67:989–995.
Eerola, E., T. Veromaa, and P. Toivanen, 1987. Special features in the structural organization of the avian lymphoid system. Pages 9–22 in: Avian Immunology: Basis and Practice. A. Toivanen and P. Toivanen, ed. CRC Press, Inc., Boca Raton, FL. Glick, B., K. Sato, and F. Cohenour, 1964. Comparison of the phagocytic ability of normal and bursectomized birds. J. Reticuloendothel. Soc. 1:442–449. Gross, W. G., P. B. Siegel, R. W. Hall, C. H. Domermuth, and R. T. Dubois, 1980. Production and persistence of antibodies in chickens to sheep erythrocytes. 2. Resistance to infectious diseases. Poultry Sci. 59:205–210. Heller, E. D., G. Leitner, A. Friedman, Z. Uni, M. Gutman, and A. Cahaner, 1992. Immunological parameters in meat-type chicken lines divergently selected by antibody response to Escherichia coli vaccination. Vet. Immunol. Immunopathol. 34:159–172. Hofacre, C., J. R. Glisson, and S. H. Kleven, 1986. Comparison of vaccination protocols of broiler breeder hens for Pasteurella multocida utilizing enzyme-linked immunosorbent assay and virulent challenge. Avian Dis. 31:260–263. Kozak, R. W., J. F. Haskell, L. A. Greenstein, M. M. Rechler, T. A. Maldmann, and S. P. Nissley, 1987. Type I and II insulinlike growth factor receptors on human phytohemagglutininactivated T lymphocytes. Cell Immunol. 109:318–331. Kreukniet, M. B., M.G.B. Nieuwland, and A. J. van der Zijpp, 1994. Phagocytic activity of two lines of chickens divergently selected for antibody production. Vet. Immunol. Immunopathol. 44:377–387. Kuby, J., 1994. Immunology. 2nd ed. W. H. Freeman and Company, New York, NY. Lamont, S. J., 1986. Genetic association of reticuloendothelial activity in chickens. Proc. 3rd World Congress on Genet. Applied to Livestock Production. Agricultural Communications, University of Nebraska, Lincoln, NE XI:643–647. Leitner, G., Z. Uni, A. Gahaner, M. Gutman, and E. D. Heller, 1992. Replicated divergent selection of broiler chickens for high or low early antibody response to Escherichia coli vaccination. Poultry Sci. 71:27–37. Li, Z., K. E. Nestor, Y. M. Saif, and J. W. Anderson, 2000a. Antibody responses to sheep red blood cell and Brucella abortus antigens in a turkey line selected for increased body weight and its randombred control. Poultry Sci. 79:804–809. Li, Z., K. E. Nestor, Y. M. Saif, J. W. Anderson, and R. A. Patterson, 2000b. Serum immunoglobulin G and M concentrations did not appear to be associated with resistance to Pasteurella multocida in a large-bodied turkey line and a randombred control population. Poultry Sci. 79:163–166. Li, Z., K. E. Nestor, Y. M. Saif, W. L. Bacon, and J. W. Anderson, 1999a. Effect of selection for increased body weight on mitogenic response in turkeys. Poultry Sci. 78:1532–1535. Li, Z., K. E. Nestor, Y. M. Saif, Z. Fan, M. Luhtala, and O. Vainio, 1999b. Cross-reactive anti-chicken CD4 and CD8 monoclonal antibodies suggest polymorphism of the turkey CD8α molecule. Poultry Sci. 78:1526–1531. Li, Z., K. E. Nestor, Y. M. Saif, and M. Luhtala, 2000c. Flow cytometric analysis of T lymphocyte subpopulations in largebodied turkey lines and a randombred control population. Poultry Sci. 79:219–223. Muir, F. V., and R. G. Jaap, 1967. A negative genetic correlation between bursa weight at hatching and post-hatching body growth of chickens. Poultry Sci. 46:1483–1488. Naber, E. C., and S. P. Touchburn, 1970. Ohio poultry rations. Ohio Cooperative Extension Service Bulletin 343. The Ohio State University, Columbus, OH. Nestor, K. E., 1977a. The stability of two randombred control populations of turkeys. Poultry Sci. 56:54–57. Nestor, K. E., 1977b. Genetics of growth and reproduction in the turkey. 5. Selection for increased body weight alone and in combination with increased egg production. Poultry Sci. 56:337–347.
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a higher frequency of CD8α polymorphism (Li et al., 1999a,b). Selection for increased 16-wk BW has resulted in changes in production of some hormones involved in growth, such as growth hormone and insulin-like growth factor-I (Vasilatos-Younken et al., 1988; Bacon et al., 1989, 1991), and might also have caused changes in receptors for these hormones that might affect immune response and disease resistance. In humans, the receptors for growth hormone, insulin-like growth factor-I, and somatostatin have been found to be expressed on lymphocytes and monocytes (Kozak et al., 1987; Tapson et al., 1988; Roldan et al., 1989; Sreedharan et al., 1989; Stuart et al., 1991; Badolato et al., 1994). In summary, the F-line turkeys were heavier and had higher relative spleen weight and ratio of spleen to bursa of Fabricius weight, but had lower relative bursa weight. The F-line birds had lower in vivo phagocytic activity than the RBC2 line as evaluated by the CCA. There were no line differences in the antibody responses to the NDV and P. multocida vaccines.
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LI ET AL. SAS Institute, 1988. SAS威/STAT User’s Guide. SAS Institute Inc., Cary, NC. Siegel, P. B., and W. B. Gross, 1980. Production and persistence of antibodies in chickens to sheep erythrocytes. I. Directional selection. Poultry Sci. 59:1–5. Sreedharan, S. P., K. T. Kodama, K. E. Peterson, and E. J. Goetzl, 1989. Distinct subsets of somatostatin receptors on cultured human lymphocytes. J. Biol. Chem. 264:949–952. Stuart, C. A., R. T. Meehan, L. S. Neale, N. M. Cintron, and R. W. Furlanetto, 1991. Insulin-like growth factor-I binds selectively to human peripheral blood monocytes and Blymphocytes. J. Clin. Endocrinol. Metab. 72:1117–1122. Tapson, V. F., M. Boni-Schnetzler, P. F. Pilch, D. M. Center, and J. S. Berman, 1988. Structural and functional characterization of the human T lymphocyte receptor for insulin-like growth factor-I in vitro. J. Clin. Invest. 82:950–957. Toivanen, P., A. Naukkarinen, and O. Vainio, 1987. What is the function of bursa of Faricius? Pages 79–100 in: Avian Immunology: Basis and Practice. A. Toivanen and P. Toivanen, ed. CRC Press, Inc., Boca Raton, FL. Tsai, H. J., Y. M. Saif, K. E. Nestor, D. A. Emmerson, and R. A. Patterson, 1992. Genetic variation in resistance of turkeys to experimental infection with Newcastle disease virus. Avian Dis. 36:561–565. Ubosi, C. O., W. B. Gross, and P. Siegel, 1985. Divergent selection of chickens for antibody production to sheep erythrocytes: Age effects in parental lines and their crosses. Avian Dis. 29:150–158. Vasilatos-Younken, R., W. L. Bacon, and K. E. Nestor, 1988. Relationship of plasma growth hormone to growth within and between turkey lines selected for differential growth rates. Poultry Sci. 67:826–834. Yamamoto, Y., and B. Glick, 1982. A comparison of the immune response between two lines of chickens selected for differences in the weight of the bursa of Fabricius. Poultry Sci. 61:2129–2132.
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Nestor, K. E., 1984. Genetics of growth and reproduction in the turkey. 9. Long-term selection for increased 16-week body weight. Poultry Sci. 63:2114–2122. Nestor, K. E., D. O. Noble, J. Zhu, and Y. Moritsu, 1996a. Direct and correlated responses to long-term selection for increased body weight and egg production in turkeys. Poultry Sci. 75:1180–1191. Nestor, K. E., Y. M. Saif, J. W. Anderson, R. A. Patterson, and Z. Li, 1999. Variation in resistance to Pasteurella multocida among turkey lines. Poultry Sci. 78:1377–1379. Nestor, K. E., Y. M. Saif, J. Zhu, and D. O. Noble, 1996b. Research Note: Influence of growth selection in turkeys on resistance to Pasteurella multocida. Poultry Sci. 75:1161–1163. Nestor, K. E., Y. M. Saif, J. Zhu, D. O. Noble, and R. A. Patterson, 1996c. The influence of major histocompatibility complex genotypes on resistance to Pasteurella multocida and Newcastle disease virus in turkeys. Poultry Sci. 75:29–33. Pitcovski, J, D. E. Heller, A. Cahaner, and B. A. Peleg, 1987. Selection for early responsiveness of chickens to Escherichia coli and Newcastle disease virus. Poultry Sci. 66:1276–1282. Roldan, A., E. Charreau, R. Schillaci, E. M. Eugui, and A. C. Allison, 1989. Insulin-like growth factor-I increases the mitogenic response of human peripheral blood lymphocytes to phytohemagglutinin. Immunol. Lett. 20:5–8. Sacco, R. E., K. E. Nestor, Y. M. Saif, H. J. Tsai, and R. A. Patterson, 1994. Effect of genetic selection for increased body weight and sex of poults on antibody response of turkeys to Newcastle disease virus and Pasteurella multocida vaccines. Avian Dis. 38:33–36. Sacco, R. E., Y. M. Saif, K. E. Nestor, N. B. Anthony, D. A. Emmerson, and R. N. Dearth, 1991. Genetic variation in resistance of turkeys to experimental challenge with Pasteurella multocida. Avian Dis. 35:950–954. Saif, Y. M., K. E. Nestor, R. N. Dearth, and P. A. Renner, 1984. Case report—Possible genetic variation in resistance of turkeys to erysipelas and fowl cholera. Avian Dis. 28:770–773.
(Key words: turkey, growth selection, antibody response, organ weight, phagocytosis) 2001 Poultry Science 80:689–694
than corresponding lines selected for low antibody response. However, Biozzi et al. (1975, 1979a) reported that a line of mice selected for low antibody response to several antigens was more resistant to challenge by some infectious agents. Previous reports showed that a turkey line (F), selected for increased 16-wk BW and exhibiting an increase of about 75% in the 16-wk BW of male turkeys in comparison to its randombred control line (RBC2) (Nestor et al., 1996b), was more susceptible than the RBC2 line to erysipelas, P. multocida, and Newcastle disease virus (NDV) (Saif et al., 1984; Sacco et al., 1991; Tsai et al., 1992; Nestor et al., 1996b, 1999). However, the F-line turkeys had higher anti-NDV titers than the RBC2 line at 3 wk following primary and secondary immunizations (Sacco et al., 1994). Line differences were inconsistent for anti-P. multocida titers at 3 wk following the primary vaccination when the antibody was detected with ELISA during a 2yr experiment (Sacco et al., 1994). The F line had a higher serum IgM, but not IgG, concentration than the RBC2
INTRODUCTION Individuals depend on the harmony of phagocytosis and cell-mediated and humoral immunities to develop resistance to infectious diseases. These three facets of the immune system are interactive but are under separate genetic control in mice (Biozzi et al., 1979b, 1982). Phagocytosis is important in general disease resistance (Lamont, 1986). Selection for antibody response to one nonreplicating antigen in chicken lines resulted in enhanced responses to other antigens and, therefore, might have improved general disease resistance (Gross et al., 1980; Siegel and Gross, 1980; Cheng and Lamont, 1988; Heller et al., 1992). In addition, chickens selected for high antibody response to Pasteurella multocida (Hofacre et al., 1986) or Escherichia coli (Pitcovski et al., 1987; Leitner et al., 1992) vaccines were more resistant to challenge with these organisms
2001 Poultry Science Association, Inc. Received for publication December 9, 1999. Accepted for publication January 15, 2001. 1 Salaries and research support were provided by state and federal funds appropriated to the Ohio Agricultural Research and Development Center, The Ohio State University. 2 To whom correspondence should be addressed: [email protected].
Abbreviation Key: CCA = carbon clearance assay; F = subline of RBC2 selected long-term for increased 16 wk BW; NDV = Newcastle disease virus; OD = optical density; PV = postvaccination; RBC2 = randombred control line.
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ABSTRACT The influence of selection was studied for increased 16-wk BW in turkeys on in vivo phagocytic activity, antibody responses to vaccines, and weight of the spleen and bursa of Fabricius. A line (F) of turkeys selected long term for increased 16-wk BW and its corresponding randombred control (RBC2) were compared. Phagocytic activity was evaluated by the carbon clearance assay. Antibody responses to inactivated Newcastle disease virus and Pasteurella multocida vaccines were examined by ELISA. Body weight and relative weights of spleen and bursa of Fabricius of the two lines were also compared. The F line had lower phagocytic activity than the RBC2 line (P < 0.05). In addition, the F line had greater BW,
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MATERIALS AND METHODS Turkeys and Management Two lines (RBC2 and F) of turkeys were used in the present study. Line RBC2 was a randombred control initiated in 1966 (Nestor, 1977a), whereas Line F, a subline of RBC2, was selected over 33 generations for increased 16-wk BW (Nestor, 1977b, 1984; Nestor et al., 1996a). The breeder flocks that produced the poults used were vaccinated with an attenuated NDV vaccine via eye drops, in September, then with an inactivated NDV vaccine subcutaneously in November, and with an avian encephalomyelitis vaccine subcutaneously in October but were not vaccinated for P. multocida. The poults were grown intermingled, sexes separate, in confinement. The birds were provided water and a multiple-ration system, ad libitum, with declining protein (Naber and Touchburn, 1970).
Vaccination and Antibody Response Ten males and ten females from each line were used for each vaccine. Poults were vaccinated subcutaneously at 6 wk of age (in April) with an inactivated NDV vaccine3 or P. multocida bacterin.3 Individual blood samples were collected prior to vaccination (0 wk) and at 1, 2, 3, 4, 5, and 12 wk postvaccination (PV). Sera were separated and stored frozen at −20 C until analysis. Serum samples were assayed simultaneously for antibody levels to P. multocida and NDV by using commercial ELISA test kits4 as instructed. Optical density (OD) values were read at 630 nm by an EIA microplate reader.5 Antibody levels were expressed as the ratio of sample to positive controls as follows: (sample OD mean − negative control OD mean)/ (positive control OD mean − negative control OD mean). Throughout this manuscript, the antibody ratio will be referred to as titer.
3
Maine Biological Laboratories, Waterville, ME 04903. IDEXX Corp., Portland, ME 04104. 5 Bio-Rad Laboratory, Richmond, CA 94801. 6 Anthes Universal Ltd., Brampton, ONT L6W 3K8. 4
Carbon Clearance Assay Six male and six female 6-wk-old poults from each line were used in the carbon clearance assay (CCA). The CCA was used to estimate the in vivo phagocytic activity based on methods described elsewhere (Glick et al., 1964; Lamont, 1986; Heller et al., 1992). Briefly, the supernatant fraction of India ink (Pelikan 518.21A 862)6 was obtained through centrifugation (300 × g for 30 min), and 1.5 mL/ kg BW was injected into the brachial vein. Blood (100 µL) was taken from the opposite wing before injection (0 min) and at 3, 6, and 15 min after the carbon injection and then was transferred immediately into 2.0 mL of 1.0% sodium citrate. After centrifugation (50 × g for 4 min), the relative amount of carbon particles remaining in the supernatant was spectrophotometrically measured by absorbance at a wavelength of 675 nm with the samples at 0 min as zero values.
Relative Weight of Spleen and Bursa of Fabricius Twenty-seven, 9-wk-old turkeys from each line were used. Turkeys were weighed, euthanatized by CO2 asphyxiation, and necropsied. The weights of spleen and bursa of Fabricius were recorded, and the relative weights of spleen and bursa of Fabricius and the ratio of spleen weight to bursa weight were compared between the two lines.
Statistical Analysis The effects of line and sex on antibody titers, carbon clearance, and organ weights were analyzed by an ANOVA using the general linear model procedure of SAS software (SAS Institute, 1988). Pearson correlation coefficients were used to analyze the relationship between the antibody ratios at different points in time and BW at 8, 16, and 20 wk. A difference with a probability of P ≤ 0.05 was considered to be statistically significant.
RESULTS There were no significant effects of line or sex on the antibody titers in response to NDV vaccine, except at 12 wk after vaccination (Figure 1). At this time, females had higher antibody titers than males in the RBC2 line and than all birds in the F line (P < 0.05) (data not shown). The Pearson correlation coefficients were generally negative between anti-NDV titers and BW, except at 2 wk PV. There were significant (P < 0.05) correlation coefficients between antibody titers at 5 wk PV and BW at 20 wk (−0.354) and between antibody titers at 12 wk PV and BW at 16 wk (−0.400) or at 20 wk (−0.421) (Table 1). Neither line nor sex affected the antibody titers in the response to P. multocida vaccine (Figure 2). The Pearson correlation coefficients were generally positive between anti-P. multocida titers and BW, except at 12 wk PV (Table 1). There were significant (P < 0.05) correlation coefficients
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line at 6 wk of age (Li et al., 2000b). The RBC2 line had a greater response of peripheral blood mononuclear cells to concanavalin A, but not to phytohemagglutinin M, than the F line (Li et al., 1999a). Polymorphism of the CD8α molecule was more frequent in the F line than in the RBC2 line (Li et al., 1999b). The F line had a larger CD4+CD8− T cell subpopulation than the RBC2 line (Li et al., 2000c). In order to determine the effects of long-term selection for increased BW in turkeys on other aspects of the immune system, lymphoid organ weights, antibody responses to NDV and P. multocida vaccines at various points in time, and phagocytic activity in the two lines were compared in the present study.
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between antibody titers at 3 wk PV and BW at 16 wk (0.357) and at 20 wk (0.421) of age. There was large variation in individual antibody titers within lines. There was no sex difference in carbon clearance as measured at an OD of 675 nm. However, more carbon particles (P < 0.05) remained in the blood of the F-line turkeys than in the RBC2 turkeys at 3 and 6 min (P < 0.05) and at 15 min (P < 0.01) postinjection with India ink (Figure 3), indicating that the F-line poults cleared carbon particles from the circulation system at a slower rate than the RBC2-line birds. Therefore, the in vivo phagocytic activity in the F line was lower than in the RBC2 line. Body weight at 9 wk of age was greater in the F line than in the RBC2 line (P < 0.01) with a significant sex effect as expected (Table 2). Male poults were heavier than female counterparts in both lines (P < 0.001). There were line, but no sex, differences in the relative weight of spleen and bursa of Fabricius as well as the ratio of
FIGURE 2. Antibody titers (ratios) detected with ELISA at different times after vaccination with Pasteurella multocida bacterin vaccine in the F and RBC2 lines of turkeys. RBC2 = randombred control population; F = subline of RBC2 selected for increased 16-wk BW. Values are least squares means with the SE bars. Antibody ratio is expressed in following equation: [sample optical density (OD) mean − negative control OD mean]/(positive control OD mean − negative control OD mean).
spleen to bursa weight (P < 0.01). Compared with the RBC2 line, the F line had a higher relative spleen weight and spleen to bursa weight ratio but had a lower relative weight of the bursa.
DISCUSSION In the present study, line differences in antibody titers between the F and RBC2 lines were not observed at several points in time after vaccination with NDV and P. multocida vaccines in the thirty-third generation of selection in the F line, which was inconsistent with the results of Sacco et al. (1994). Sacco et al. (1994) reported that the F line in the twenty-sixth generation had higher antibody titers than the RBC2 line at 3 wk after vaccination with NDV vaccine. The inconsistency between the two studies might have resulted from differences in the method of antibody detection, sample number, expression of results,
TABLE 1. Pearson correlation coefficients between antibody ratios of turkeys in response to Pasteurella multocida (PM) and Newcastle disease virus (NDV) vaccines measured at different points in time postvaccination and BW at 8, 16, and 20 wk1 Vaccine group NDV
PM
Antibody ratio BW
PV0
PV1
PV2
PV3
PV4
PV5
PV12
8 16 20 8 16 20
−0.287 −0.328 −0.333 0.123 0.023 0.067
0.139 0.034 0.002 0.172 0.132 0.002
−0.061 −0.038 −0.006 0.086 0.092 0.178*
−0.078 −0.032 −0.028 0.130 0.357* 0.421*
−0.174 −0.176 −0.150 0.161 0.230 0.215
−0.264 −0.299 −0.354* 0.200 0.196 0.226
−0.338 −0.400* −0.421* −0.138 −0.139 −0.198
wk wk wk wk wk wk
1 Turkeys were vaccinated with inactivated PM or NDV vaccines at 6 wk of age. PV0, PV1, PV2, PV3, PV4, PV5, and PV12 represent antibody ratios measured prior to vaccination, and at 1, 2, 3, 4, 5, and 12 wk postvaccination, respectively. *P < 0.05.
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FIGURE 1. Antibody titers (ratios) detected with ELISA at different times after vaccination with inactivated Newcastle disease virus vaccine in the F and RBC2 lines of turkeys. RBC2 = randombred control population; F = subline of F selected for increased 16-wk BW. Values are least squares means with the SE bars. Antibody ratio is expressed in following equation: (sample optical density (OD) mean − negative control OD mean)/(positive control OD mean − negative control OD mean).
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or changes in the F line from the twenty-sixth to thirtythird generation of selection. Sacco et al. (1994) detected the antibody in several hundred turkeys with avidinbiotin-based ELISA and expressed the results as mean loge titer. The Pearson correlation coefficients were generally positive between anti-P. multocida titers and BW except at 12 wk PV but were negative between anti-NDV titers and BW except at 2 wk PV. The present results suggest variation in the host’s antibody response to different types of antigens. The spleen and bursa are the important lymphoid organs involved in the development and differentiation of T or B lymphocytes (Eerola et al., 1987; Toivanen et al., 1987). The smaller bursa of Fabricius weight and higher ratio of spleen to bursa weight in the F line may reflect the effect of growth selection on the lymphoid tissues, and these changes in weight possibly resulted in some changes in the lymphocyte subpopulations. In chickens, Muir and Jaap (1967) reported that bursa of Fabricius
TABLE 2. Total body weight and relative weight of the spleen and bursa of Fabricius in the RBC2 and F lines (least squares mean ± SEM)1 Line
Sex
No.
F
Male Female Mean Male Female Mean
14 13 27 15 12 27
BW
Spleen
(kg)
RBC2
5.55 4.46 5.00 2.67 2.13 2.40
Bursa
Spleen:bursa ratio
(% BW) ± ± ± ± ± ±
0.07*** 0.10 0.06A 0.08*** 0.08 0.06B
1.28 1.27 1.27 1.11 1.12 1.11
± ± ± ± ± ±
0.05 0.07 0.04A 0.06 0.06 0.04B
0.89 0.99 0.94 1.09 1.19 1.14
± ± ± ± ± ±
0.05 0.07 0.04B 0.06 0.06 0.04A
1.53 1.31 1.42 1.08 0.96 1.02
± ± ± ± ± ±
0.08 0.12 0.07A 0.09 0.09 0.06B
Line means within columns with no common superscript differ (P < 0.01). Line RBC2 = a randombred control line; Line F = a subline of RBC2 selected for increased 16-wk BW. All poults were 9-wk-old. ***Sexes within lines differ (P < 0.001). A,B 1
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FIGURE 3. Optical density (OD), at 675 nm, of the supernatant fraction from blood samples collected from F and RBC2 line turkeys at 3, 6, and 15 min after injection with India ink (1.5 mL/kg BW). RBC2 = randombred control population; F = subline of RBC2 selected for increased 16 wk BW. Values are the least squares means with the SE bars. *P < 0.05; **P < 0.01.
weight at hatching was negatively associated with posthatching BW. A similar relationship was observed for turkeys in the present study. Bursa of Fabrcius size may not necessarily be associated with antibody titers. Yamamoto and Glick (1982) found that a chicken line selected for small bursa size had higher total and 2-mercaptoethanol-resistant antibody titers in the primary response to SRBC and also had higher total antibody titers in the secondary response compared to the counterparts in the line selected for large bursa size. Ubosi et al. (1985) observed that a chicken line selected for high response to SRBC had a larger bursa size than the line selected for low response. The F line had significantly lower phagocytic activity than the RBC2 line. The function of phagocytosis is mainly performed by macrophages that digest and process the antigens and then present the antigens associated with MHC molecules to T lymphocytes (Lamont, 1986). Neutrophils (heterophils in poultry) are also active phagocytic cells, and eosinophils play a major phagocytic role in the defense against parasitic organisms (Kuby, 1994). Thrombocytes have even been reported to be phagocytic (Glick et al., 1964). Therefore, phagocytosis is a first-line barrier of defense against pathogens and may not be proportional to the level of humoral immune response. Biozzi et al. (1979a) observed higher macrophage activity in a mouse line with lower antibody response. A similar finding was also obtained by Kreukniet et al. (1994), who observed that the phagocytic activity was not correlated with the antibody response in their chicken lines. The F line had a higher antibody response to SRBC (Li et al., 2000a) and higher serum IgM concentration than the RBC2 line (Li et al., 2000b). However, the F line was more susceptible to certain specific infectious diseases (Saif et al., 1984; Sacco et al., 1991; Tsai et al., 1992; Nestor et al., 1996 b,c). Published results and those in the present study suggest that the level of humoral immune response may not account for the increased susceptibility to specific diseases in the F line. Other aspects of the immune system, such as decreased phagocytosis or cellular immune response, may offer a possible explanation for the decreased disease resistance in the F line. In addition, the F line had a lower mitogenic response to concanavalin A and
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ACKNOWLEDGMENTS The authors thank British United Turkeys of America, Lewisberg, WV 14901, and Hybrid Turkeys Inc., Suite C, Kitchner, Ontario, Canada N2K 3S2, for financial support.
REFERENCES Bacon, W. L., K. E. Nestor, D. A. Emmerson, R. Vasilatos-Younken, and D. W. Long, 1991. Circulating IGF-I in plasma of growing male and female turkeys of medium and heavy weight lines. Dom. Anim. Endocrinol. 10:267–277. Bacon, W. L., R. Vasilatos-Younken, K. E. Nestor, B. J. Anderson, and D. W. Long, 1989. Pulsatile patterns of plasma growth hormone in turkeys: effects of growth rate, age, and sex. Gen. Comp. Endocrinol. 75:417–426. Badolato, R., H. M. Bond, G. Valerio, A. Petrella, G. Morrone, M. J. Waters, S. Venuta, and A. Tenore, 1994. Differential expression of surface membrane growth hormone receptor on human peripheral blood lymphocytes detected by dual fluorochrome flow cytometry. J. Clin. Endocrinol. Metab. 79:984–990. Biozzi, G., D. Mouton, A. M. Heumann, and Y. Bouthillier, 1982. Genetic regulation of immunoresponsiveness in relation to resistance against infectious disease. Proc. 2nd World Congress on Genetics Applied to Livestock Production, Madrid, Spain V:150–163. Biozzi, G., D. Mouton, A. M. Heumann, Y. Bouthillier, C. Stiffel, and J. C. Mevel, 1979a. Genetic analysis of antibody responsiveness to sheep erythrocytes in crosses between lines of mice selected for high and low antibody synthesis. Immunology 3:427–438. Biozzi, G., D. Mouton, O. A. Sant’Anna, H. C. Passous, M. Gennari, M. H. Reis, V. C. A. Ferreira, A. M. Heumann, Y. Bouthillier, O. M. Ibanez, and C. Stiffel, 1979b. Genetics of immunoresponsiveness of natural antigens in the mouse. Curr. Top. Microbiol. Immunol. 85:31–98. Biozzi, G., C. Stiffel, D. Moulton, and Y. Bouthillier, 1975. Selection of lines of mice with high and low antibody responses to complex immunogens. Pages 179–228 in: Immunogenetics and Immunodeficiency. B. Becacerraf, ed. University Park Press, Baltimore, MD. Cheng, S., and S. J. Lamont, 1988. Genetic analysis of immunecompetence measures in a White Leghorn chicken line. Poultry Sci. 67:989–995.
Eerola, E., T. Veromaa, and P. Toivanen, 1987. Special features in the structural organization of the avian lymphoid system. Pages 9–22 in: Avian Immunology: Basis and Practice. A. Toivanen and P. Toivanen, ed. CRC Press, Inc., Boca Raton, FL. Glick, B., K. Sato, and F. Cohenour, 1964. Comparison of the phagocytic ability of normal and bursectomized birds. J. Reticuloendothel. Soc. 1:442–449. Gross, W. G., P. B. Siegel, R. W. Hall, C. H. Domermuth, and R. T. Dubois, 1980. Production and persistence of antibodies in chickens to sheep erythrocytes. 2. Resistance to infectious diseases. Poultry Sci. 59:205–210. Heller, E. D., G. Leitner, A. Friedman, Z. Uni, M. Gutman, and A. Cahaner, 1992. Immunological parameters in meat-type chicken lines divergently selected by antibody response to Escherichia coli vaccination. Vet. Immunol. Immunopathol. 34:159–172. Hofacre, C., J. R. Glisson, and S. H. Kleven, 1986. Comparison of vaccination protocols of broiler breeder hens for Pasteurella multocida utilizing enzyme-linked immunosorbent assay and virulent challenge. Avian Dis. 31:260–263. Kozak, R. W., J. F. Haskell, L. A. Greenstein, M. M. Rechler, T. A. Maldmann, and S. P. Nissley, 1987. Type I and II insulinlike growth factor receptors on human phytohemagglutininactivated T lymphocytes. Cell Immunol. 109:318–331. Kreukniet, M. B., M.G.B. Nieuwland, and A. J. van der Zijpp, 1994. Phagocytic activity of two lines of chickens divergently selected for antibody production. Vet. Immunol. Immunopathol. 44:377–387. Kuby, J., 1994. Immunology. 2nd ed. W. H. Freeman and Company, New York, NY. Lamont, S. J., 1986. Genetic association of reticuloendothelial activity in chickens. Proc. 3rd World Congress on Genet. Applied to Livestock Production. Agricultural Communications, University of Nebraska, Lincoln, NE XI:643–647. Leitner, G., Z. Uni, A. Gahaner, M. Gutman, and E. D. Heller, 1992. Replicated divergent selection of broiler chickens for high or low early antibody response to Escherichia coli vaccination. Poultry Sci. 71:27–37. Li, Z., K. E. Nestor, Y. M. Saif, and J. W. Anderson, 2000a. Antibody responses to sheep red blood cell and Brucella abortus antigens in a turkey line selected for increased body weight and its randombred control. Poultry Sci. 79:804–809. Li, Z., K. E. Nestor, Y. M. Saif, J. W. Anderson, and R. A. Patterson, 2000b. Serum immunoglobulin G and M concentrations did not appear to be associated with resistance to Pasteurella multocida in a large-bodied turkey line and a randombred control population. Poultry Sci. 79:163–166. Li, Z., K. E. Nestor, Y. M. Saif, W. L. Bacon, and J. W. Anderson, 1999a. Effect of selection for increased body weight on mitogenic response in turkeys. Poultry Sci. 78:1532–1535. Li, Z., K. E. Nestor, Y. M. Saif, Z. Fan, M. Luhtala, and O. Vainio, 1999b. Cross-reactive anti-chicken CD4 and CD8 monoclonal antibodies suggest polymorphism of the turkey CD8α molecule. Poultry Sci. 78:1526–1531. Li, Z., K. E. Nestor, Y. M. Saif, and M. Luhtala, 2000c. Flow cytometric analysis of T lymphocyte subpopulations in largebodied turkey lines and a randombred control population. Poultry Sci. 79:219–223. Muir, F. V., and R. G. Jaap, 1967. A negative genetic correlation between bursa weight at hatching and post-hatching body growth of chickens. Poultry Sci. 46:1483–1488. Naber, E. C., and S. P. Touchburn, 1970. Ohio poultry rations. Ohio Cooperative Extension Service Bulletin 343. The Ohio State University, Columbus, OH. Nestor, K. E., 1977a. The stability of two randombred control populations of turkeys. Poultry Sci. 56:54–57. Nestor, K. E., 1977b. Genetics of growth and reproduction in the turkey. 5. Selection for increased body weight alone and in combination with increased egg production. Poultry Sci. 56:337–347.
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a higher frequency of CD8α polymorphism (Li et al., 1999a,b). Selection for increased 16-wk BW has resulted in changes in production of some hormones involved in growth, such as growth hormone and insulin-like growth factor-I (Vasilatos-Younken et al., 1988; Bacon et al., 1989, 1991), and might also have caused changes in receptors for these hormones that might affect immune response and disease resistance. In humans, the receptors for growth hormone, insulin-like growth factor-I, and somatostatin have been found to be expressed on lymphocytes and monocytes (Kozak et al., 1987; Tapson et al., 1988; Roldan et al., 1989; Sreedharan et al., 1989; Stuart et al., 1991; Badolato et al., 1994). In summary, the F-line turkeys were heavier and had higher relative spleen weight and ratio of spleen to bursa of Fabricius weight, but had lower relative bursa weight. The F-line birds had lower in vivo phagocytic activity than the RBC2 line as evaluated by the CCA. There were no line differences in the antibody responses to the NDV and P. multocida vaccines.
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