Field Evaluation of Maternal Antibody Transfer to a Group of Pathogens in Meat-Type Chickens

S. Gharaibeh,*1 K. Mahmoud, and M. Al-Natour*

*Faculty of Veterinary Medicine, and Faculty of Agriculture, Jordan University of Science and Technology, Irbid 22110, Jordan ABSTRACT This study was conducted to evaluate the rate of antibody transfer on a ock basis from hens to their day-old chicks in meat-type chickens raised in a commercial setting. Fifteen randomly selected hens from a commercial broiler-breeder ock were bled at 37, 40, and 45 wk of age. At day of bleeding, the collected eggs were identied and tracked through hatching where 30 hatchlings were randomly sampled and bled from the jugular vein. Antibodies against 10 different pathogens were quantied from the collected serum samples, and the percentage of maternal antibodies transfer was calculated from the chick antibody titer divided by the hen antibody titer. The results showed a signicant variation in the rate of antibody transfer among the pathogens tested for. The transfer percentages were 4.3, 19.5, 25.5, 38.6, 73.6, 6.9, 32.4, 22.4, 29.2, and 32.8 for avian encephalomyelitis virus, avian inuenza virus, chicken anemia virus, infectious bronchitis virus, infectious bursal disease virus, laryngotracheitis virus, Mycoplasma gallisepticum, Mycoplasma synoviae, Newcastle disease virus, and reovirus, respectively. The results of this work may be used in commercial farms to predict the antibody titer in dayold chicks as a function of their dams antibody titers.

Key words: maternal antibody, transfer rate, chicken 2008 Poultry Science 87:15501555 doi:10.3382/ps.2008-00119

INTRODUCTION
Newly hatched chicks are vulnerable to many pathogens because they lack a fully developed immune system. Vertical transmission of maternal antibodies from hens to chicks against certain pathogens provides a crucial mean of protection up to a certain age. Also, the level of these inherited antibodies is of a major importance when serology for disease diagnosis is considered (Sharma, 2003). More than 3 decades ago, different modes of maternal antibodies transmission have been proposed by Rose et al. (1974). It is believed that yolk and oviductal secretions are the main paths of maternal immunoglobulin transfer from hens to their hatched chicks. The transfer of hens circulating antigen-specic antibodies to yolk and hence to the embryos and then to chicks circulation via receptors on the yolk sac membrane was well characterized by several researchers (Kramer and Cho, 1970; Kowalczyk et al., 1985; Tressler and Roth, 1987; West et al., 2004). Kimijima et al. (1990) reported that antibodies secreted in the oviduct are produced from glandular cells of the oviduct, but later it

2008 Poultry Science Association Inc. Received March 19, 2008. Accepted April 16, 2008. 1 Corresponding author: saadgh@just.edu.jo

was proven to be secreted from plasma cell-like cells in the stroma (Zheng et al., 2000). The uptake of antibodies into the circulation of the embryo from egg contents occurs at a low rate, and then increases dramatically a few days before hatch (Kowalczyk et al., 1985). Maternal transfer of antibodies against certain pathogens plays a signicant role in protection of chicks against these pathogens before the development of active immunity (Heller et al., 1990; Mondal and Naqi, 2001; Ahmad and Akhter, 2003). Chicks vaccinated while having high levels of maternal antibodies resulted in vaccine failure, due to neutralization of the live vaccine and level of maternal antibodies plays a role in determining the level of response in chicks to early vaccination (Mondal and Naqi, 2001; Al-Natour et al., 2004). For example, pathogenic Mycoplasma gallisepticum (MG) is transmitted into hatching eggs, but maternal antibodies prevent or reduce embryo mortality by reducing the replication of MG inoculated into yolk sac (Levisohn et al., 1985). Recently, Hamal et al. (2006) reported that IgY, total or antigen-specic, in the hens plasma or eggs was found to be a direct indicator of maternal antibody transfer to the chicks circulation, with an expected percentage of transfer of approximately 30%. They also reported discrepancies in meat lines of chickens with reference to anti-Newcastle disease virus (NDV) and anti-infectious bronchitis virus (IBV) antibody levels in hens plasma,

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FIELD EVALUATION OF MATERNAL ANTIBODY TRANSFER

Table 1. Vaccination program of the broiler-breeder ock Age 1d 7d 7d 9d 12 d 15 d 19 d 14 d 27 d 40 d 8 wk 8 wk 8 wk 9 wk 10 wk 11 wk 12 wk 18 wk 18 wk 30 wk 40 wk Vaccine IBV + NDV IBV + NDV AIV H9N2 IBDV Coccidia Reovirus IBDV IBV+NDV IBDV NDV Lasota LTV IBV 4/91 Salmonella NDV Lasota MG F-strain Reovirus AEV IBDV+IBV+NDV AIV H9N2 IBV+NDV IBV+NDV Type, method L, Spray K, Subcutaneous K, Subcutaneous injection L, Drinking water L, Drinking water L, Intramuscular injection L, Drinking water L, Spray L, Drinking water L, Spray L, Eye drop L, Eye drop K, Subcutaneous injection L, Spray L, Spray K, Intramuscular injection L, Drinking water K, Intramuscular injection K, Subcutaneous injection L, Spray L, Spray
1

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Company Fatro, Italy Fatro, Italy Merial, France Fatro, Italy Biopharm, Czech Republic Fatro, Italy Fatro, Italy Intervet, the Netherlands Fatro, Italy Fatro, Italy Fatro, Italy Intervet, Netherlands Intervet, Netherlands Fatro, Italy Schering-Plough, United States Fatro, Italy Fatro, Italy Fatro, Italy Merial, France Fatro, Italy Fatro, Italy

1 AEV = avian encephalomyelitis virus; AIV = avian inuenza virus; d = day; IBV = infectious bronchitis virus; IBDV = infectious bursal disease virus; K = killed; L = live; LTV = laryngotracheitis virus; MG = Mycoplasma gallisepticum; NDV = Newcastle disease virus.

egg yolks, and in chicks plasma. The susceptibility for many poultry diseases was shown to be partly inuenced by breed (Bumstead et al., 1991). Abdel-Moneim and Abdel-Gawad (2006) detailed variation in 4 native and crossbred chicken lines in the responsiveness to infectious bursal disease virus (IBDV) and in the amounts of inherited maternally derived antibodies in both yolk and day-old chicks. Using the dams titer to predict the day-old chicks titer against certain pathogens would be valuable to poultry clinicians in the eld. This study is unique because it was conducted on a ock basis to predict the antibodies titer in day-old chicks as a function of their parent-ock titer and not individual parent-hen titer. This study also compares the rates of antibody transfer between 10 different pathogens. In contrast to previously reported records of transfer efciency in an experimental setting, the data of the herein work were collected from a heterogeneous environment of a commercial broiler-breeder farm and hatchery as well.

access to water with 16.50 h of daily illumination. The ock was visited at 37, 40, and 45 wk of age, and 15 randomly selected hens were bled from the wing vein at each visit. The ocks collected eggs on each day of visitation were identied and tracked through hatching. In reference to each day of visitation, 30 hatchlings were randomly sampled and bled from the jugular vein at the day of hatch. These 30 hatchlings are not necessarily the progeny of the exact 15 hens that were bled.

Serological Analysis
Serum was separated from blood samples by centrifugation at 15,000 g for 3 min and stored at 80C until the day of analysis. Commercial ELISA kits (Synbiotics Co., San Diego, CA) with the same batch numbers for each pathogen were used to test for presence of antibodies (IgG) against avian encephalomyelitis virus (AEV), avian inuenza virus (AIV), chicken anemia virus (CAV), IBV, IBDV, laryngotracheitis virus (LTV), MG, Mycoplasma synoviae (MS), and reovirus. The ELISA kits were used according to the manufacturers protocol using an automated microplate reader (ELx800, BIO-TEK Instruments Inc., Winooski, VT). The antibody titer in each individual sample was quantied using the software provided by the manufacturer. The geometric mean titer (GMT) for each group of serum samples was also calculated using the same software. All serum samples were read against positive and negative control antisera provided by the kit and used in each run. Hemagglutination inhibition (HI) test using procedure was used to quantify antibodies against NDV (Thayer and Beard, 1998). The serum samples in the HI test were run on a 2-fold serial dilution, and the GMT was calculated

MATERIALS AND METHODS Birds, Husbandry, and Sampling

A commercial meat-type broiler-breeder ock (Lohman) located in northern part of Jordan at 32 N and 35 E was assigned for the study. The ock was housed in naturally ventilated open-sided house according to the specication of the supplying company and vaccinated against all the common pathogens in the region as detailed in Table 1. At the peak of production period and thereafter, each hen was allowed 165 g of corn-soybased diet (2,900 kcal/kg; 16% CP; 5% CF) and free

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1

GHARAIBEH ET AL.
Table 2. Antibody geometric mean titers in hens and their corresponding chicks at 3 different time points against a group of different pathogens Time 1 Disease2 AEV AIV CAV IBV IBDV LTV MG MS NDV Reo
1 2

2 Chicks 40 199 2,944 10,042 20,920 122 1,839 1,258 65 1,057 Hens 3,839 1,910 9,283 19,472 35,012 3,146 3,165 4,881 372 2,761 Chicks 405 668 1,985 6,706 21,104 209 1,134 828 58 790 Hens 6,572 1,853 7,921 18,189 35,179 2,875 3,408 3,887 280 2,739

3 Chicks 123 202 1,692 5,981 27,073 211 693 504 124 1,101

CV3 (%) Hens 31.8 9.7 7.9 6.5 18.2 27.4 19.0 18.9 23.8 15.6 Chicks 101 75.7 29.7 28.6 15.2 28.1 47.3 43.8 44.0 17.1

Hens 7,481 1,586 8,742 20,716 25,072 1,798 4,483 3,371 234 3,566

Measured by ELISA for all agents except for NDV measured by HI (see Materials and Methods section). AEV = avian encephalomyelitis virus; AIV = avian inuenza virus; CAV = chicken anemia virus; IBV = infectious bronchitis virus; IBDV = infectious bursal disease virus; LTV = laryngotracheitis virus; MG = Mycoplasma gallisepticum; MS = Mycoplasma synoviae; NDV = Newcastle disease virus; Reo = reovirus. 3 Coefcient of variation ([standard deviation/average] 100%).

(Villegas, 1998). Appropriate controls for the HI test (positive antiserum control, negative antiserum control, antigen control, and erythrocyte control) were included in each run. The percentage of maternal antibody transfer from hens to their day-old hatchling chicks was calculated by dividing chicks GMT for each pathogen by their hens GMT for the same pathogen and multiplying this value by 100 for each visitation.

Statistical Analysis
Collected data from this eld study were subjected to ANOVA as a completely randomized design to determine the differences among percentage of maternal antibody transfer for the examined diseases. The statistical analysis was achieved using the general linear model procedure of SAS (SAS Institute, 1996). Hens and chicks serum GMT level in each visitation was considered as the experimental unit. Transfer percentages among diseases were separated using Fishers protected least signicant difference. Data were reported as mean SEM, and the differences were considered signicant at P 0.05.

RESULTS AND DISCUSSION

The positive and negative control antisera against the agents gave ELISA results within the reference range specied by the individual kit manufacturer. Also, the NDV HI test positive and negative control antisera gave the expected results and titers. In addition, the HI test antigen and erythrocyte controls behaved within the normal range. Table 2 summarizes the GMT in hens and their corresponding chicks sampled at 37, 42, and 45 wk of age. The

CV of GMT in hens mostly showed lower values when compared with those assayed from their respective dayold hatchlings except for IBDV (Table 2). The CV of hens titers averaged 17.9% across all pathogens examined in the herein study over the 3 sampling periods, whereas chicks CV averaged 43%. The AEV titers reported the highest CV in hens and chicks, 31.8 and 101%, respectively. The IBV reported the lowest CV (6.5%) in hens, whereas IBDV registered the lowest CV in chicks (15.2%). From our led experience and the results of this study, it appears that the commercial ELISA kits used will result in a large discrepancy when the titer is very low as evident with chicks AEV GMT of 40, 405, and 123 for the 3 time points with a CV of 101%. However, the readings are more consistent when titer is higher as evident with chicks IBDV GMT of 20,920, 21,104, and 27,073 for the 3 time points with a CV of 15.2%. Table 3 describes the percentages of transfer over the 3 visitation periods. The IBDV registered the highest (P < 0.05) percentage of transfer (73.6%) among all the pathogens tested for. The lowest (P < 0.05) percentage of transfer was claimed by AEV with an average of 4.3%, which was not signicantly different from LTV and AIV values of 6.9 and 19.5%, respectively. Statistically, the other 6 pathogens demonstrated comparable transfer percentages as shown in Table 3. The CV of the transfer percentages varied across the examined pathogens. The AEV demonstrated the highest variation with a CV of 125.5%, and LTV had the lowest CV value (5%) as mentioned in Table 3. There were considerable variations among the transfer rate of maternal antibodies against the different pathogens and ranged from 4.3% for AEV to 73.6% for IBDV (Table 3). The IBDV had the highest (P < 0.05) transfer rate of 73.6% among all the pathogens tested for. The IBDV targets the lymphoid cells in the chicken

FIELD EVALUATION OF MATERNAL ANTIBODY TRANSFER

Table 3. Transfer percentage of antibodies against a group of pathogens from hens to chicks at three different time points Time Disease AEV AIV CAV IBV IBDV LTV MG MS NDV Reo
2 1

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1% 0.5 12.5 33.7 48.5 83.4 6.8 41 37.3 27.8 29.6

2% 10.6 35 21.4 34.4 60.3 6.6 35.8 17 15.6 28.6

3% 1.9 10.9 21.4 32.9 77 7.3 20.3 13 44.3 40.2

Mean transfer (%) 4.3e 19.5cde 25.5bc 38.6b 73.6a 6.9de 32.4bc 22.4bcd 29.2bc 32.8bc

CV%3 125.5 69 27.8 22.2 16.2 5 33.3 58.2 49.3 19.5

ae Means not sharing a common superscript differ signicantly (P < 0.05). 1 Transfer percentage = (geometric mean titer in chicks/geometric mean titer in breeders) 100%. 2 AEV = avian encephalomyelitis virus; AIV = avian inuenza virus; CAV = chicken anemia virus; IBV = infectious bronchitis virus; IBDV = infectious bursal disease virus; LTV = laryngotracheitis virus; MG = Mycoplasma gallisepticum; MS = Mycoplasma synoviae; NDV = Newcastle disease virus; Reo = reovirus. 3 Coefcient of variation [(standard deviation/average) 100%].

body including the circulating lymphocytes and especially B lymphocytes in the bursa (Burkhardt and Muller, 1987), which are responsible for the development of the humoral antibody response. After development of the reproductive tract of the hens, some of these lymphocytes localize in the lamina propria of the oviduct and in the stroma of the ovary. Antibodies produced locally in these organs usually constitute an insignicant proportion of the transferred antibody to the eggs compared with the circulating antibodies in the blood (Sharma, 2003). The IBDV targets B lymphocytes (Burkhardt and Muller, 1987); it is believed that this is why IBDV had the highest rate of transfer compared with the other pathogens tested for in this study. In previous studies, IBDV antibodies transfer rate was 45% in layers (Fahey et al., 1987) and ranged from 30 to 53% in native Egyptian chickens (Abdel-Moneim and Abdel-Gawad, 2006). This high transfer rate should be taken into account when vaccinating the hatching chicks because chicks with high maternal antibodies against IBDV showed no active immune response to vaccination at early ages (Naqi et al., 1983). The IBV had the second highest transfer rate (38.6%) after IBDV and differed signicantly from AIV, LTV, and AEV. However, it was not signicantly higher than reovirus, MG, NDV, CAV, and MS. There are several serotypes of IBV that infect the reproductive system of chickens (Cavanagh and Naqi, 2003) that might result in activation of the mucosal immunity in the reproductive tract causing direct secretion of IBV antibodies into the egg similar to the mechanism mentioned above for IBDV. Similar rates of transfer of IBV antibodies were 35.5 and 40.7% in 2 different lines of chickens (Hamal et al., 2006).

It is known that maternal antibodies play a major role in the protection of chicks against AEV (Westbury and Sinkovic, 1978). It was surprising that the transfer rate for AEV was the lowest (4.3%) and the ELISA GMT in the 3 chick groups in this study ranged from 40 to 405. This low titer appeared to be protective against the disease because none of the broiler ocks generated from this breeder ock suffered from AE, although we have serological evidence that AEV does exist in Jordan (unpublished observation). The LTV transfer rate was also very low (6.9%) and ELISA GMT in chicks was low and ranged from 122 to 211; However, the immunity against LTV is cell mediated, and maternal antibodies do not confer protection to the progeny against LTV-caused disease (Fahey et al., 1983). Maternal antibodies to CAV usually confer complete protection against the disease (Otaki et al., 1992) and the industry practice to ensure protection of chicks from CAV infection is usually done through vaccinating or exposing the breeders before lay. The breeders in this study were not vaccinated, and the titer in the breeders is a result of eld exposure to the virus. The transfer rate of CAV in this study was 25.5%, and the ELISA GMT titers in chicks ranged from 1,692 to 2,944. This titer was protective against the disease, and none of the broiler ocks generated from this breeder ock suffered from CAV. The transfer rate of reovirus in this study was 32.8%. It was reported earlier that maternal antibody against reovirus protects chicks to some degree (Van der Heide et al., 1976). The MG transfer rate (32.4%) was more than MS (22.4%). Breeders were vaccinated with live F-strain of MG but not for MS, and the titer of MS in the breeders is due to eld exposure. An earlier study indicated equal transfer rates for MG and MS antibodies from breeders to the embryonic uids of the developing embryo measured by indirect immunoperoxidase test but did not specify the rate in the serum of hatched chicks (Bencina et al., 2005). The difference in the transfer rate between the 2 organisms in this study could be due to the differences in serological tests used in this study (ELISA) and the technique used in the previous study (indirect immunoperoxidase) or due to the fact that MG titer in the breeders is a response to vaccination, whereas the MS titer is due to a eld exposure of the breeders in this study. However, it is known that maternal antibodies confer very little protection against MG challenge and cell-mediated immunity plays a more active role in protection against MG (Lin and Kleven, 1984). Newcastle disease virus antibodies had a transfer rate of 29.2% in this study; whereas in a previous study, the transfer rate of NDV antibodies was 35.5 to 40.7% in 2 different lines of chickens (Hamal et al., 2006). The AIV antibodies transfer rate in this study was 19.5% from serum of the breeders to serum of the chicks, and the titer in breeders was induced by 2 doses of killed AIV (H9N2) vaccine at 1 and 18 wk of age (Table 1). The transfer rate of antibodies from serum to yolk after ex-

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GHARAIBEH ET AL. Cavanagh, D., and S. A. Naqi. 2003. Infectious bronchitis. Pages 101119 in Diseases of Poultry. 11th ed. Y. M. Saif, H. J. Barnes, J. R. Glisson, A. M. Fadly, L. R. McDougald, and D. E. Swayne, ed. Iowa State Press, Ames. Fahey, K. J., T. J. Bagust, and J. J. York. 1983. Laryngotracheitis herpesvirus infection in the chicken: The role of humoral antibody in immunity to a graded challenge infection. Avian Pathol. 12:505514. Fahey, K. J., J. K. Crooks, and R. A. Fraser. 1987. Assessment by ELISA of passively acquired protection against infectious bursal disease virus in chickens. Aust. Vet. J. 64:203207. Hamal, K. R., S. C. Burgess, I. Y. Pevzner, and G. F. Erf. 2006. Maternal antibody transfer from dams to their egg yolks, egg whites, and chicks in meat lines of chickens. Poult. Sci. 85:13641372. Heller, E. D., G. Leitner, N. Drabkin, and D. Melamed. 1990. Passive immunization of chicks against Escherichia coli. Avian Pathol. 19:345354. Kimijima, T., Y. Hashimoto, H. Kitagawa, Y. Kon, and M. Sugimura. 1990. Localization of immunoglobulins in the chicken oviduct. Jpn. J. Vet. Sci. 52:299305. Kowalczyk, K., J. Daiss, J. Halpern, and T. F. Roth. 1985. Quantitation of maternal-fetal IgG transport in the chicken. Immunology 54:755762. Kramer, T. T., and H. C. Cho. 1970. Transfer of immunoglubulins and antibodies in the hens egg. Immunology 19:157 167. Levisohn, S., J. R. Glisson, and S. H. Kleven. 1985. In ovo pathogenicity of Mycoplasma gallisepticum strains in the presence and absence of maternal antibody. Avian Dis. 29:188197. Lin, M. Y., and S. H. Kleven. 1984. Transferred humoral immunity in chickens to Mycoplasma gallisepticum. Avian Dis. 28:7987. Mondal, S. P., and S. A. Naqi. 2001. Maternal antibody to infectious bronchitis virus: its role in protection against infection and development of active immunity to vaccine. Vet. Immunol. Immunopathol. 79:3140. Naqi, S. A., B. Marquez, and N. Sahin. 1983. Maternal antibody and its effect on infectious bursal disease immunization. Avian Dis. 27:623631. Otaki, Y., K. Saito, M. Tajima, and Y. Nomura. 1992. Persistence of maternal antibody to chicken anaemia agent and its effect on the susceptibility of young chickens. Avian Pathol. 21:147151. Rose, M. E., E. Orlans, and N. Buttress. 1974. Immunoglobulin classes in the hens egg: Their segregation in yolk and white. Eur. J. Immunol. 4:521523. SAS Institute. 1996. SAS/STAT Users Guide: Statistics. Version 6, 4th ed. SAS Institute, Cary, NC. Sharma, J. M. 2003. The Avian Immune System. Pages 516 in Diseases of Poultry. 11th ed. Y. M. Saif, H. J. Barnes, J. R. Glisson, A. M. Fadly, L. R. McDougald, and D. E. Swayne, ed. Iowa State Press, Ames. Thayer, S. G., and C. W. Beard. 1998. Serological Procedures. Pages 255266 in A Laboratory Manual for the Isolation and Identication of Avian Pathogens. 4th ed. D. E. Swayne, J. R. Glisson, M. W. Jackwood, J. E. Pearson, and W. M. Reed, ed. Am. Assoc. Avian Pathologists, Kennett Square, PA. Trampel, D. W., E. M. Zhou, K. J. Yoon, and K. J. Koehler. 2006. Detection of antibodies in serum and egg yolk following infection of chickens with an H6N2 avian inuenza virus. J. Vet. Diagn. Invest. 18:437442. Tressler, R. L., and T. F. Roth. 1987. IgG receptors on the embryonic chick yolk sac. J. Biol. Chem. 262:1540615412. Van der Heide, L., M. Kalbac, and W. C. Hall. 1976. Infectious tenosynovitis (viral arthritis): Inuence of maternal antibodies on the development of tenosynovitis lesions after experimental infection by day-old chickens with tenosynovitis virus. Avian Dis. 20:641648.

perimental infection with another strain of a low pathogenic AIV (H6N2) was 66% (Trampel et al., 2006). The difference in the transfer rate between this study and the other study may be due to the fact that we tested for antibodies in the serum of the hatched chicks and not in yolk as they did, or may be due to the difference in exposure to the antigen by killed vaccine in this study or experimental infection with live virus in the other study. Within a chicken ock after vaccination, we aim for a good GMT and low CV below 40%. Flocks that show CV over 60% usually indicate a deciency in the vaccine application technique. In this study, the CV for each agent within the ock is not shown. However, the CV of the GMT in the 3 visits for each agent is listed in Table 2 and for the transfer percentages in Table 3. The CV of the hens for the all agents was below 40%, which indicates a consistent ock immunity for all agents. The CV of chicks was over 60% for AEV and AIV, and the chicks had a very low GMT for these 2 agents. This may be due to differences in the sampling of hatched chicks and inconsistent transfer rate of antibodies. The CV of the percentages of transfer is related to the variations seen among chick groups. This study is unique by presenting data for the transfer of antibodies against 10 different pathogens from broiler-breeder hens to their chicks in a eld situation and not in an experimental setting or housing. The results of this study can be used by the poultry industry where random samples from a breeder ock are selected for antibody titration and then the chicks antibody titer is extrapolated based on the hens titer. This will be a great help for broiler producers to plan their vaccination programs and as a guideline for serological titers in case diagnostic approaches are needed.

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Abdel-Moneim, A. S., and M. M. A. Abdel-Gawad. 2006. Genetic variations in maternal transfer and immune responsiveness to infectious bursal disease virus. Vet. Microbiol. 114:1624. Ahmad, Z., and S. Akhter. 2003. Role of maternal antibodies in protection against infectious bursal disease in commercial broilers. Int. J. Poult. Sci. 2:251255. Al-Natour, M. Q., L. A. Ward, Y. M. Saif, B. Stewart-Brown, and L. D. Keck. 2004. Effect of different levels of maternally derived antibodies on protection against infectious bursal disease virus. Avian Dis. 48:177182. Bencina, D., M. Narat, A. Bidovec, and O. Zorman-Rojs. 2005. Transfer of maternal immunoglobulins and antibodies to Mycoplasma gallisepticum and Mycoplasma synoviae to the allantoic and amniotic uid of chicken embryos. Avian Pathol. 34:463472. Bumstead, N., B. J. Millard, B. A. Barrow, and J. K. A. Cook. 1991. The genetic basis of disease resistance in chickens. Pages 1023 in Breeding for Disease Resistance in Farm Animals. J. B. Owan, and R. P. E. Axford, ed. CAB Int. Wallingford, UK. Burkhardt, E., and H. Muller. 1987. Susceptibility of chicken blood lymphoblasts and monocytes to infectious bursal disease virus (IBDV). Arch. Virol. 94:297303.

FIELD EVALUATION OF MATERNAL ANTIBODY TRANSFER Villegas, P. 1998. Titration of Biological Suspensions. Pages 248254 in A Laboratory Manual for the Isolation and Identication of Avian Pathogens. 4th ed. D. E. Swayne, J. R. Glisson, M. W. Jackwood, J. E. Pearson, and W. M. Reed, ed. Am. Assoc. Avian Pathologists, Kennett Square, PA. West, A. P., Jr., A. B. Herr, and P. J. Bjorkman. 2004. The chicken yolk sac IgY receptor, a functional equivalent of the mammalian MHC-related Fc receptor, is a phospholipase A2 receptor homolog. Immunity 20:601610.

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Westbury, H. A., and B. Sinkovic. 1978. The pathogenesis of infectious avian encephalomyelitis. IV. The effect of maternal antibody on the development of the disease. Aust. Vet. J. 54:8185. Zheng, W. M., J. Izaki, S. Furusawa, and Y. Yoshimura. 2000. Localization of immunoglobulin G gamma-chain mRNAexpressing cells in the oviduct of laying and diethylstilbestrol-treated immature hens. Gen. Comp. Endocrinol. 120:345352.