ENVIRONMENT AND HEALTH

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1 ENVIRONMENT AND HEALTH Infection and Immunity in Broiler Chicken Breeders Vaccinated with a Temperature-Sensitive Mutant of Mycoplasma gallisepticum and Impact on Performance of Offspring E. K. Barbour,*,1 S. K. Hamadeh,* and A. Eid *Department of Animal Science, Faculty of Agricultural and Food Sciences, American University of Beirut, 850 3rd Avenue, New York, New York 10022; and Poultry Research Department, Hawa Companies, Safra, Lebanon ABSTRACT A comparison of infection and immunity son with nonvaccinated, MG-infected flocks at 15, 20, 23, to Mycoplasma gallisepticum (MG) in broiler chicken breeders vaccinated with a temperature-sensitive mutant of MG versus nonvaccinated chickens, and the impact on the performance of their offspring was conducted. Infection and immunity in breeders were assessed by culture and enzyme-linked immunoassay, respectively. However, performance in their offspring was assessed by studying MG infection in embryos, occurrence of infection titers to MG in relation to mortality, and feed conversion in the broilers. Five out of 10 broiler chicken breeder flocks raised on the same multiple-age farm with a long history of mycoplasmosis were vaccinated intraocularly once with a temperature-sensitive MG mutant vaccine (ts-11 ) at an average age of 7.5 wk; another five breeder flocks were left as unvaccinated controls exposed to field MG. The average recoveries of ts-11 organisms from tracheas and infraorbital sinuses of 41-wk-old vaccinates were 88 and 84%, respectively. No field MG organisms were recovered from vaccinates between 15 and 41 wk of age. The recovery of field MG organisms from tracheas and sinuses of nonvaccinated chickens increased to an average of 100% at 41 wk of age. A significant decrease (P < 0.05) in the average percentage of MG-seroconverted breeders occurred in ts-11 -vaccinated flocks in compari- 29, 32, 36, and 41 wk of age. The average infection prevalence by MG in the vitelline membrane of 7-d-old embryos produced by the five unvaccinated breeder flocks peaked at 79% when their respective hatching eggs were collected at 36 wk of breeder s age. Embryos of ts-11 -vaccinated flocks had zero prevalence of MG infection at all times between 29 and 57 wk of breeder s age. Seroconversion to MG (average of 17.7%) at 42 d of age was only present in sera of 10 offspring broiler flocks of the nonvaccinated breeders. However, a lack of seroconversion to MG occurred in 10, 42-d-old offspring broiler flocks of the five ts-11 -vaccinated breeder flocks. This lack was associated with a lower, better average feedconversion ratio (2.05) (P < 0.05) and a lower average mortality percentage (5.3%) (P < 0.05) in comparison with those obtained in the offspring of the five unvaccinated, MG-infected breeder flocks. The results indicate that vaccination of broiler chicken breeders with a temperature-sensitive mutant of MG prevented infection by field MG in tracheas and infraorbital sinuses of these breeders and in the vitelline membranes of their embryos. In addition, the broiler offspring of the vaccinated breeders had a better production performance. (Key words: broiler breeders, Mycoplasma gallisepticum, temperature-sensitive mutant vaccine, offspring performance) 2000 Poultry Science 79: INTRODUCTION Transovarian transmission of field virulent Mycoplasma gallisepticum (MG) strains from infected breeders to their offspring is well documented (Russell and Cottew, 1972; Ley and Yoder, 1997; Barbour et al., 1998). The preferred method for control of MG infection in poultry is by its eradication from breeder flocks. However, eradication is Received for publication January 10, Accepted for publication May 24, To whom correspondence should be addressed: ebø1@aub.edu.lb. 2 Developed in Australia and marketed by Select Laboratories, Inc., Gainesville, GA impractical in multiple-age poultry production farms once field MG organisms are introduced (Kleven et al., 1984). The live MG vaccine strain most commonly used in the United States is the F-strain. However, it is virulent when introduced to young chickens (Rodriguez and Kleven, 1980). Other MG strains (such as ts-11,2 ) are safe when applied to multiple-age commercial layers (Withear et al., 1990; Evans and Hafez, 1992). However, there are no reports evaluating infection and immunity in broiler chicken breeders vaccinated with a temperature-sensitive Abbreviation Key: MG = Mycoplasma gallisepticum; TS = temperature sensitive. 1730

2 MYCOPLASMA GALLISEPTICUM VACCINE IN BREEDERS 1731 mutant of MG, the impact on MG-transmission to their embryos, and the feed-conversion ratios and mortality of their broiler offspring. The objectives of this study were to assess breeders immunity, survival of temperature-sensitive mutants of MG in their tracheas and sinuses, and protection against field MG infection in broiler chicken breeders and their embryos after vaccination with a temperature-sensitive mutant vaccine (ts-11 ). The impact of this approach on the feed-conversion ratios and mortality of their broiler offspring flocks was also examined in this study. MATERIALS AND METHODS Breeders and ts-11 Vaccination Each of 10 broiler chicken breeder flocks of approximately 20,000 birds was distributed at 1 d of age into two buildings of three floor pens each. The breeders were imported at 1 d of age from Europe or the USA, and certified as free of MG and Mycoplasma synoviae. The breeder flocks were reared on the same multiple-age farm with a long history of mycoplasmosis. All breeder flocks raised in the last 15 yr on the same multiple-age farm were confirmed by culture and serology as MG-positive. The minimum and maximum distances between breederflock locations were approximately 2 and 5 km, respectively. Five out of the 10 broiler breeder flocks were vaccinated intraocularly once with ts-11 vaccine at an average age of 7.5 wk, and according to the manufacturer s instructions. The other five breeder flocks were left unvaccinated. The 10 broiler chicken breeder flocks were all free of MG infection at around 7.5 wk of age (vaccination time), as revealed by tracheal swab cultures following the procedure described below. Survival of ts-11 and Field MG Organisms Cotton swab samples were collected from tracheas and infraorbital sinuses of 20 randomly chosen birds of each breeder flock at each of seven ages (15, 20, 23, 29, 32, 36, and 41 wk). Each individual swab was cultured in 5 ml of Frey s broth medium (Frey et al., 1968). The broth culture was mixed gently, divided into equal portions, and kept in two separate sterile tubes. One portion was incubated at 40 C for 7 d for isolation of temperatureinsensitive field MG strains, and the other portion of the culture medium was incubated at 30 C for 11 d for isolation of temperature-sensitive ts-11 organisms. Broth-culture media incubated at 40 C were passed onto Frey s agar medium and left for 7 d at 40 C, whereas brothculture media incubated at 30 C were passed similarly, but were incubated for 11 d at 30 C. Field MG colonies had a fried-egg morphology, whereas ts-11 mutant colonies 3 SPAFAS Inc., a division of Wilmington Partners L.P., Preston, Connecticut, KPL, Gaithersburg, MD appeared punctiform, raised, and undulate. Two MG colonies with such described morphology were selected from each culture on the agar and passed separately into 5 ml of Frey s broth medium for purification. The 40 and 30 C cultures were left at their respective temperatures until fermentation was observed, and then were centrifuged at 3,000 rpm for 20 min; the supernatant was discarded, and the pellets were washed twice with sterile physiological saline. The washed pellet was reconstituted with 50 µl of sterile saline. Ten microliters of the reconstituted pellet were separately reacted with an equal volume of positive and negative serum for MG 3. The reaction was performed following a slide-agglutination procedure recommended by SPAFAS. 3 Confirmation of the differential identity of ts-11 organisms and field MG was based on its ability to grow at specific temperatures, matching the previously described colonial morphologies and agglutination results. MG Seroconversion in Breeders Blood was collected by a 20-gauge needle and a syringe from the individual brachial vein of 30 randomly chosen birds of each breeder flock, at ages of 1 d and 15, 20, 23, 29, 32, 36, and 41 wk. Seroconversion to MG-positive birds was determined by a commercial ELISA-MG antibody test kit. 4 Infection Prevalence in Embryos Thirty 7-d-old embryos were collected from each breeder flock at each of seven different breeder ages (29, 32, 36, 41, 46, 51, and 57 wk). The embryos were tested for field MG infection by culturing the individual vitelline membranes (1 1 cm) in 5 ml of Frey s broth medium at 40 C. The isolation and identification of field MG isolates were performed as previously described. Broiler-Offspring Performance Twenty broiler offspring flocks (two from each of the 10 breeder flocks) were assessed for their performance. The size of each broiler-offspring flock was 5,000 birds. The twenty broiler-offspring flocks were hatched from eggs collected from the 10 breeder flocks at an age of 36 wk. Blood was collected by a 20-gauge needle and syringe from individual brachial veins of 30 randomly chosen birds of each of the 20 broiler-offspring flocks, at ages of 1, 14, and 42 d. The seroprevalence to MG-positive birds was determined by using a commercial ELISA-MG antibody test kit. 4 Seroprevalence at 1dofagereflected the maternal antibodies to MG, whereas that at 14 and 42 d of age reflected the decline in maternal immunity and appearance of field MG infection, respectively (Barbour et al., 1998). At 42 d of age (market age), cumulative percentage mortality and the feed conversion of each broiler flock were determined.

3 1732 BARBOUR ET AL. Statistics s were allocated to vaccination treatments or kept as nonvaccinated controls according to a complete randomized design within time. Percentages were compared between treatments using χ 2 (MSTAT Statistical Computing Program). 5 Comparison of means of feed conversion in offspring flocks, produced by differently treated breeder flocks, was analyzed by ANOVA for complete randomized design (MSTAT). RESULTS AND DISCUSSION Survival of ts-11 and Field MG Organisms The percentage recovery of ts-11 organisms in tracheas and infraorbital sinuses of vaccinated breeders decreased between 15 and 41 wk of age (Figure 1). However, the recovery of field MG organisms in unvaccinated flocks increased in both tracheas and infraorbital sinuses during the same period. Attempts to isolate field MG organisms from tracheas and sinuses of ts-11 -vaccinated breeders and to isolate ts-11 organisms from the same organs of unvaccinated breeders were not successful. The ts-11 organisms seem to have lower survival capacity in tracheas and infraorbital sinuses in comparison with field MG organisms. However, the survival of ts-11 in breeders tracheas (mean of 88%) at 41 wk of age (about 33.5 wk postvaccination) was much higher than in previous documentation (Abd-El-Motelib and Kleven, 1993), in which the survival of ts-11 organisms at 90 d postvaccination occurred only in two out of five chickens (40%). The density of breeders in the field per unit area and the nature of the intensive management applied in this study are most likely different than the isolation rooms provided for the five birds in the described experiment (Abd- El-Motelib and Kleven, 1993), which could have led to a difference in the survival of ts-11 organisms in the tracheas of chickens. Attempts to recover field MG organisms from infraorbital sinuses and tracheas of ts-11 vaccinated breeders and ts-11 organisms from the same organs of unvaccinated breeders were negative (Figure 1), which is in agreement with previous works reporting the failure to isolate challenge organisms of MG (S6) from chickens vaccinated with a temperature-sensitive MG (Lam et al., 1983; Karaca and Lam, 1987), and the inability of ts-11 organisms to cause horizontal infection in sentinel birds housed in adjoining pens (Ley et al., 1996). MG Seroconversion in Breeders All sera collected from the 10 breeder flocks at 1 d of age were negative for MG antibodies, a reflection of the absence of MG infection in their grandparents. The average percentage seroconversion to MG-positive birds was always lower between 15 and 41 wk of age in ts-11-5 Michigan State University, East Lansing, MI FIGURE 1. Mean percentage recovery ± SE of ts-11 organisms from tracheas and infraorbital sinuses of five vaccinated breeder flocks, and of field Mycoplasma gallisepticum (MG) from tracheas and infraorbital sinuses of five unvaccinated breeder flocks, at seven different ages, in weeks. vaccinated than in the nonvaccinated, MG-infected breeder flocks (P < 0.05) (Table 1). The fact that the mean percentage seroconversion to MG-positive birds was always significantly lower (P < 0.05) between 15 and 41 wk of age in ts-11 -vaccinated than in nonvaccinated, MGinfected breeder flocks (Table 1) is most likely due to the milder postvaccination reaction induced by ts-11 in comparison with field MG organisms. This result is in agreement with previous works confirming the mild reaction in ts-11 -vaccinated chickens (Abd-El-Motelib and Kleven, 1993), its safe nature (Withear et al., 1990), and the resulting lower serological response (Abd-El-Motelib and Kleven, 1993). Infection Prevalence of MG in Embryos The mean infection prevalence of field MG organisms in the vitelline membrane of 7-d-embryos of the five un-

4 MYCOPLASMA GALLISEPTICUM VACCINE IN BREEDERS 1733 TABLE 1. Percentage of seroconversion to Mycoplasma gallisepticum (MG)-positive birds at different time intervals in ts-11 -vaccinated and unvaccinated, MG-infected broiler chicken breeder flocks Percentage 2 of MG-seropositive birds at different ages ts-11 Item vaccination 1 15 wk 20 wk 23 wk 29 wk 32 wk 36 wk 41 wk 1 Yes Yes Yes Yes Yes Mean 11.3 b 47.3 b 70.7 b 67.3 b 71.4 b 83.3 b 84.0 b 6 No No No No No Mean 54.0 a 68.0 a 88.0 a 98.0 a a a a χ 2 (1 df) P <0.05 <0.05 <0.05 <0.05 <0.05 <0.05 <0.05 a,b Means in a column followed by different superscripts are significantly different (P < 0.05). 1 ts-11 vaccination was done at an average age of 7.5 wk and according to manufacturer s instructions. All breeder flocks had a zero percent MG-seropositiveness at 1 d of age. 2 Percentage of 30 serum samples collected per flock at each age between 15 and 41 wk. vaccinated breeder flocks peaked to 79.3% when their respective hatching eggs were collected at 36 wk of breeders age (Table 2). However, this mean infection prevalence declined to a minimum of 6.7% when the embryos hatching eggs were collected at 57 wk of breeders age. In addition, the 7-d-old embryos of ts-11 -vaccinated flocks had a zero prevalence of MG when their respective hatching eggs were collected at seven different times between 29 and 57 wk of breeder s age. This prevalence is significantly less than that obtained in embryos of hatching eggs collected from unvaccinated breeders at the same seven ages (P < 0.05). The high protection against field MG infection in tracheas and sinuses of breeders by ts-11 vaccination was associated with a complete protection against egg transmission, as shown in the absence of MG infection in the vitelline membrane of 7-d-old embryos when their respective hatching eggs were collected between 29 and 57 wk of breeders age (Table 2). Protection studies against MG egg transmission in Leghorn pullets by live strains other than ts-11 organisms have been reported before (Glisson and Kleven, 1984). The use of the F-strain resulted in a significant reduction of MG egg transmission, reaching a minimal infection of 1.8% during Week 25 postchallenge with a field R-strain of MG (Glisson and Kleven, 1984). In this study, the nonvaccinated breeders resulted in embryos highly infected with MG when their hatching eggs were collected at 36 wk of breeders age (Table 2). It is worth mentioning that at this age, TABLE 2. Percentage recovery of field Mycoplasma gallisepticum (MG) organisms from the vitelline membrane of 7-d-old embryos 1 of respective hatching eggs collected at different ages of ts-11 -vaccinated and unvaccinated, MG-infected broiler chicken breeder flocks Percentage recovery of field MG from 7-d-old embryos of hatching eggs collected at different ages of breeders ts-11 Item vaccination 2 29 wk 32 wk 36 wk 41 wk 46 wk 51 wk 57 wk 1 Yes Yes Yes Yes Yes Mean 0.0 b 0.0 b 0.0 b 0.0 b 0.0 b 0.0 b 0.0 b 1 No No No No No Mean 21.3 a 59.3 a 79.3 a 67.3 a 17.3 a 10.7 a 6.7 a χ 2 (1 df) P <0.05 <0.05 <0.05 <0.05 <0.05 <0.05 <0.05 a,b Means in a column followed by different superscripts are significantly different (P < 0.05). 1 Thirty vitelline membranes of 30 individual embryos were cultured per flock and at each age shown above. 2 ts-11 vaccination was done at an average age of 7.5 wk and according to manufacturer s instructions.

5 1734 BARBOUR ET AL. TABLE 3. Performance of broiler offspring flocks 1 hatched from eggs collected from 36-wk-old ts-11 vaccinated and unvaccinated Mycoplasma gallisepticum (MG)-infected broiler chicken breeder flocks Percentage 3 of MG-seropositive Broiler- broilers at different ages Feed ts-11 offspring % conversion vaccination 2 flock 1 d 14 d 42 d mortality ratio 1 Yes Yes Yes Yes Yes Mean 17.0 b 0.0 b 0.0 b 5.3 b 2.05 b 1 No No No No No Mean 58.7 a 0.0 b 17.7 a 10.7 a 2.44 a χ NA 4 df P <0.05 >0.05 <0.05 <0.05 <0.05 t-value NA NA NA NA a,b Means in a column followed by different superscripts are significantly different (P < 0.05). 1 Two broiler-offspring flocks per breeder flock. The size of each broiler flock is 5,000 birds. 2 ts-11 vaccination was done at an average of 7.5 wk and according to manufacturer s instructions. 3 Thirty serum samples were randomly collected from each broiler flock at each designated age, namely, 1, 14, and 42 d. 4 NA = not applicable. the breeders showed 100% infectivity with field MG in both tracheas and infraorbital sinuses (Figure 1). Hatching eggs collected from nonvaccinated, MG-infected breeders beyond 36 wk of age started to result in fewer MG-infected embryos reaching 6.7% infectivity at 57 wk of breeders age. The breeders at such an older age seem to have a higher protection against egg transmission due to early natural exposure to field MG, leading to higher immunities as birds get older. Previous workers demonstrated a marked decrease in egg transmission when older hens were infected early in life with virulent strains of MG (Olson et al., 1964; Russell and Cottew, 1972). Broiler-Offspring Performance The maternal immunity to MG in 10 offspring flocks produced from ts-11 -vaccinated breeders (Table 3) showed a lower mean seroconversion to MG at 1 d of age (17.0%) in comparison with the mean in 10-d-old offspring flocks of nonvaccinated, MG-infected breeders (58.7%) (P < 0.05); the maternal immunity decreased to a mean of zero percentage seroconversion to MG at 14 d of age in the offspring of both the ts-11 -vaccinated and the nonvaccinated, MG-infected broiler breeder flocks (P > 0.05). However, seropositivity to MG appeared again only in the offspring of nonvaccinated, MG-infected breeders, averaging 17.7% at a market age of 42 d. The lack of seropositivity to MG in 42-d-old broiler flocks of ts-11 -vaccinated breeders was associated with lower, i.e., better, mean feed conversion (2.05) (P < 0.05), and lower mean percentage mortality (5.3%) (P < 0.05) in comparison with the offspring of nonvaccinated, MG-infected breeder flocks, showing a mean feed conversion of 2.44 and a mean percentage mortality of 10.7%. The lower MG conversion in ts-11 -vaccinated breeder flocks in comparison with nonvaccinated, MG-infected breeders (Table 1) resulted in the same pattern of MG seropositivity in 1-dold offspring broilers of the respective breeders (Table 3). This seropositivity may indicate the existence of a positive relationship between the magnitude of MG conversion in breeders and the magnitude of transferable maternal antibodies to MG in their day-old offspring. This result is in agreement with the conclusions of previous reports on such relationships (King, 1987; Barbour et al., 1996). Regardless of the higher seropositivity to MG (58.7%) in 1-d-old broilers of the nonvaccinated, MGinfected breeders, such prevalence of seropositivity was not protective in preventing the appearance of an average

6 MYCOPLASMA GALLISEPTICUM VACCINE IN BREEDERS % seroconversion to MG at 42 d of age. Previous work has shown a higher transmission of MG through the egg in nonvaccinated, MG-challenged Leghorn hens in comparison with vaccinated, challenged birds (Glisson and Kleven, 1984). The failure to isolate field MG organisms from tracheas and infraorbital sinuses of ts-11 -vaccinated breeders (Figure 1) and from the vitelline membrane of their 7-dold embryos (Table 2) is most likely the reason for the absence of seroconversion to MG at the market age (42 d old) of their broiler offspring (Table 3). The absence of humoral antibody titers to MG in broilers at 42 d of age (Talkington et al., 1985) is most likely due to the absence of MG colonization in the respiratory tract (Talkington and Kleven, 1985) of offspring produced from ts-11 vaccinated breeders. This absence of seroconversion to MG in the 42-d-old broiler-offspring of ts-11 -vaccinated breeders was associated with better feed conversion and lower mortality than those observed in the offspring of nonvaccinated, MG-infected breeders. Previous works have shown the association of the control of MG infection in broilers with improvements in feed conversion and reduction in mortality rate (Ley and Yoder, 1997). In conclusion, vaccination of broiler chicken breeders with a temperature sensitive mutant of MG prevented infection by field MG in tracheas and infraorbital sinuses of these breeders and in the vitelline membranes of their embryos. In addition, the broiler offspring of the vaccinated breeders had better production performance. ACKNOWLEDGMENTS We are grateful for the grant provided by the University Research Board of the American University of Beirut and to the laboratory facilities provided bv the Private Poultry Sector of Lebanon represented by Hawa Companies at the town of Safra, Lebanon. REFERENCES Abd-El-Motelib, T. Y., and S. H. Kleven, A comparative study of Mycoplasma gallisepticum vaccines in young chickens. Avian Dis. 37: Barbour, E. K., S. Hamadeh, R. Talhouk, W. Sakr, and R. Darwish, Evaluation of an enrofloxacin-treatment program against Mycoplasma gallisepticum infection in broilers. Prev. Vet. Med. 35: Barbour, E. K., M. Kahoul, S. Hamadeh, C. Hilan, and R. Talhouk, The role of serological profiling technology in poultry breeders. Pages in: Proceedings of the 45th Western Poultry Disease Conference. Cancun, Mexico. University of California-Davis Press, Davis, CA. Evans, R. D., and Y. S. Hafez, Evaluation of a Mycoplasma gallisepticum strain exhibiting reduced virulence for prevention and control of poultry mycoplasmosis. Avian Dis. 36: Frey, M. C., R. P. Hanson, and D. P. Anderson, A medium for the isolation of avian mycoplasmosis. Am. J. Vet. Res. 29: Glisson, J. R., and S. H. Kleven, Mycoplasma gallisepticum vaccination effects on egg transmission and egg production. Avian Dis. 28: Karaca, K., and K. M. Lam, Effect of temperature-sensitive Mycoplasma gallisepticum vaccine preparations and routes of inoculation on resistance of white leghorns to challenge. Avian Dis. 30: King, D. J., Serological profiles of commercial broiler breeders and their progeny: 1. Infectious bronchitis virus. Avian Dis. 30: Kleven, S. H., J. R. Glisson, M. Y. Lin, and F. D. Talkington, Bacterins and vaccines for the control of Mycoplasma gallisepticum. Isr. J. Med. Sci. 20: Lam, K. M., W. Lin, R. Yamamoto, and T. B. Farver, Immunization of chickens with temperature-sensitive mutants of Mycoplasma gallisepticum. Avian Dis. 27: Ley, D. H., J. M. McLaren, A. M. Miles, and H. J. Barnes, Transmissibility and safety of live Mycoplasma gallisepticum vaccines. Pages in: Proceedings of the 45th Western Poultry Disease Conference. Cancun, Mexico. Ley, D. H., and H. W. Yoder, Jr., Mycoplasma gallisepticum infection. Pages in: Diseases of Poultry. 10th ed. B. W. Calnek, H. J. Barnes, C. W. Beard, L. R. McDougald, and Y. M. Saif, ed. Iowa State University Press, Ames, IA. Olson, N. O., J. O. Heishman, and C. J. Cunningham, Control of chronic respiratory disease. VI. The effect on egg transmission of early exposure of chicks to Mycoplasma gallisepticum. Avian Dis. 8: Rodriguez, R., and S. H. Kleven, Pathogenicity of two strains of Mycoplasma gallisepticum in broiler chickens. Avian Dis. 24: Russell, R. G., and G. S. Cottew, Isolation of Mycoplasma gallisepticum from embryonated chicken eggs. Aust. Vet. J. 48:425. Talkington, F. D., and S. H. Kleven, Evaluation of production against colonization of the trachea following administration of Mycoplasma gallisepticum bacterin. Avian Dis. 29: Talkington, F. D., S. H. Kleven, and J. Brown, An enzymelinked immunosorbent assay for the detection of antibodies to Mycoplasma gallisepticum in experimentally infected chickens. Avian Dis. 29: Withear, K. G., Soeripto, K. E. Harrigan, and E. Ghiocas, Safety of temperature sensitive mutant Mycoplasma gallisepticum vaccine. Aust. Vet. J. 67:

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