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Poult Sci 2008. 87:1550-1555. doi:10.3382/ps.2008-00119
© 2008 Poultry Science Association
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IMMUNOLOGY, HEALTH AND DISEASE

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

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

* Faculty of Veterinary Medicine, and {dagger} Faculty of Agriculture, Jordan University of Science and Technology, Irbid 22110, Jordan

1 Corresponding author: saadgh{at}just.edu.jo


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
This study was conducted to evaluate the rate of antibody transfer on a flock 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 flock were bled at 37, 40, and 45 wk of age. At day of bleeding, the collected eggs were identified and tracked through hatching where 30 hatchlings were randomly sampled and bled from the jugular vein. Antibodies against 10 different pathogens were quantified 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 significant 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 influenza 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 day-old chicks as a function of their dams’ antibody titers.

Key Words: maternal antibody • transfer rate • chicken


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
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 hen’s circulating antigen-specific antibodies to yolk and hence to the embryo’s and then to chick’s 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 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 significant 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-specific, 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, egg yolks, and in chicks’ plasma. The susceptibility for many poultry diseases was shown to be partly influenced 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 dam’s titer to predict the day-old chick’s titer against certain pathogens would be valuable to poultry clinicians in the field. This study is unique because it was conducted on a flock basis to predict the antibodies titer in day-old chicks as a function of their parent-flock 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 efficiency 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.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 REFERENCES
 
Birds, Husbandry, and Sampling

A commercial meat-type broiler-breeder flock (Lohman) located in northern part of Jordan at 32° N and 35° E was assigned for the study. The flock was housed in naturally ventilated open-sided house according to the specification of the supplying company and vaccinated against all the common pathogens in the region as detailed in Table 1Go. At the peak of production period and thereafter, each hen was allowed 165 g of corn-soy-based diet (2,900 kcal/kg; 16% CP; 5% CF) and free access to water with 16.50 h of daily illumination. The flock 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 flock’s collected eggs on each day of visitation were identified 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.


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  		Table 1. Vaccination program of the broiler-breeder flock1
 
Serological Analysis

Serum was separated from blood samples by centrifugation at 15,000 x g for 3 min and stored at –80°C 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 influenza 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 manufacturer’s protocol using an automated microplate reader (ELx800, BIO-TEK Instruments Inc., Winooski, VT). The antibody titer in each individual sample was quantified 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 β 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 (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 hen’s GMT for the same pathogen and multiplying this value by 100 for each visitation.

Statistical Analysis

Collected data from this field 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 Fisher’s protected least significant difference. Data were reported as meaò SEM, and the differences were considered significant at P ≤ 0.05.


   RESULTS AND DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
REFERENCES
 
The positive and negative control antisera against the agents gave ELISA results within the reference range specified 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 2Go 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 day-old hatchlings except for IBDV (Table 2Go). 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 filed 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%.


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  		Table 2. Antibody geometric mean titers1 in hens and their corresponding chicks at 3 different time points against a group of different pathogens
 
Table 3Go 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 significantly 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 3Go. 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 3Go.


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  		Table 3. Transfer percentage1 of antibodies against a group of pathogens from hens to chicks at three different time points
 
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 3Go). 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 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 insignificant 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 significantly from AIV, LTV, and AEV. However, it was not significantly 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 flocks generated from this breeder flock 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 field 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 flocks generated from this breeder flock 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 field exposure. An earlier study indicated equal transfer rates for MG and MS antibodies from breeders to the embryonic fluids 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 field 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 1Go). The transfer rate of antibodies from serum to yolk after experimental 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 flock after vaccination, we aim for a good GMT and low CV below 40%. Flocks that show CV over 60% usually indicate a deficiency in the vaccine application technique. In this study, the CV for each agent within the flock is not shown. However, the CV of the GMT in the 3 visits for each agent is listed in Table 2Go and for the transfer percentages in Table 3Go. The CV of the hens for the all agents was below 40%, which indicates a consistent flock 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 field 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 flock 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.

Received for publication March 19, 2008. Accepted for publication April 16, 2008.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
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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 fluid of chicken embryos. Avian Pathol. 34:463–472.[CrossRef][Web of Science][Medline]

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