Veterinary Immunology and Immunopathology, 30 ( 1991 ) 45-50
45
Elsevier Science Publishers B.V., Amsterdam
Immunosuppression induced by infectious bursal disease virus Y.M. Saif Food Animal Health Research Program, Ohio Agricultural Research and Development Center, The Ohio State University, Wooster, OH 44691, USA
ABSTRACT Saif, Y.M., 1991. Immunosuppression induced by infectious bursal disease virus. Vet. Immunol. Immunopathol., 30: 45-50. Immunosuppression caused by infectious bursal disease virus (IBDV) is of major interest because of the widespread occurrence of the infection in commercial chickens. Infection with IBDV at an early age significantly compromises the humoral and local immune responses of chickens. The cellular immune response is also compromised by apparently to a lesser extent and for a short period. The immunosuppression seems to be a result of direct effect (lysis) of B cells or their precursors. Other mechanisms of immunosuppression have been suggested, notably the development of suppressor cells. ABBREVIATIONS BF, bursa of Fabricius; IBDV, infectious bursal disease virus.
INTRODUCTION
Infectious bursal disease virus (IBDV) is a double-stranded RNA virus that has a bisegmented genome; it belongs to the family Birnaviridae. It causes an acute, highly contagious and immunosuppressive disease in chickens designated infectious bursal disease (IBD). The virus is stable in the environment of poultry and the infection is widespread worldwide. Two serotypes of the virus designated l and 2 and several subtypes of serotype 1 are recognized. Both serotypes infect chickens and turkeys but the disease is recognized only in chickens. The effect of the virus on lymphoid tissue was one of the early observations in naturally infected chickens. The immunosuppressive effect of the virus in chickens exposed to the virus at a young age was reported early (Allan et al., 1972). The disease has a short incubation period and high morbidity. Birds 0165-2427/91/$03.50
© 1991 Elsevier Science Publishers B.V. All rights reserved.
46
Y.M. SAIF
less than 3 weeks of age usually do not exhibit clinical signs but are immunosuppressed whereas birds between 3 and 6 weeks of age are considered most susceptible to the clinical disease. Clinical signs are not specific but gross and microscopic lesions are characteristic. Lymphoid cells and macrophages in the intestine are infected following ingestion of the virus and these cells carry the virus to the bursa of Fabricius (BF) (Muller et al., 1979). The prominent lesions are in the BF which undergoes an increase in size owing to inflammatory changes followed by atrophy. Some of the recent field isolates (referred to as variants) do not induce inflammation hence, mainly atrophy is detected. Atrophy is caused by destruction of lymphocytes. Similar but less pronounced lesions are detected in the spleen, thymus, cecal tonsils and harderian gland. INTERACTIONS OF IBDV INFECTION WITH OTHER INFECTIONS
Infection with IBDV was reported to affect the course of a variety of bacterial, protozoal and viral diseases of chickens. The effect of the infection on the antibody response to Newcastle disease virus was one of the earliest observed immunosuppressive effects of the infection (Allan et al., 1972; Faragher et al., 1974). Later, suppression of response to other vaccines was reported (Hirai et al., 1974 ). In further studies, it was demonstrated that chicks infected early in life with IBDV have increased susceptibility to a variety of viral diseases including: inclusion body hepatitis (Fadley et al., 1976), Marek's disease (Cho 1970; Sharma, 1984), infectious bronchitis (Pejkovski et al., 1979 ), infectious laryngotracheitis (Rosenberger and Gelb, 1978 ), chicken anemia (Yuasa et al., 1980) and reoviruses (Moradian et al., 1990). Infection with IBDV was also reported to increase susceptibility to Salmonella typhimurium, Escherichia coli (Wyeth, 1975 ), Staphylococcus aureus ( Santivatr et al., 1981 ) and coccidial infections (Anderson et al., 1977; Onaga et al., 1989). The immunosuppressive effects of IBDV are dependent on the strain of the virus (Sharma et al., 1989a; Craft et al., 1990; Mazariegos et al., 1990; Higashihara et al., 1991 ). H U M OR AL AND CELLULAR MANIFESTATIONS OF THE INFECTION
As mentioned earlier, the age at which infection occurs is important in determining whether immunosuppression follows the infection and the degree of immunosuppression. Infection in the first 2 weeks of life was reported to be more immunosuppressive than infection at a later age and both the primary and secondary immune responses were adversely affected (Faragher et al., 1974). Infection at 1 day of age resulted in severe deficiency of serum immunoglobulin (Ig) G and only a monomeric IgM was produced (Ivanyi,
IMMUNOSUPPRESSION BY INFECTIOUS BURSAL DISEASEVIRUS
47
1975; Ivanyi and Morris, 1976). The level of IgG was reported to vary depending on the age at the time of infection (Ivanyi and Morris, 1976; Hirai et al., 1979). The adverse effect on antibody (Ig) response is probably to a large extent a result of the effect on the bursa-derived lymphocytes (B-cells) in both the BF and in the blood. It was shown that the number of peripheral blood B cells was reduced but the thymus-derived lymphocytes (T cells ) were not significantly affected (Hirai et al., 1979; Sivanandan and Maheswaran, 1980a). Cells expressing IgM have been shown to be the particular targets for IBDV (Hirai and Calnek, 1979; Nakai and Hirai, 1981 ). The virus seems to have a predilection for actively proliferating cells (Muller, 1986 ) such as the immature or precursor B cells as compared with mature B cells (Sivanandan and Maheswaran, 1980b). There is evidence that the local immune system is also adversely affected by IBDV infection. A significant reduction in plasma cells in the harderian gland of chicks infected with IBDV at 1-5 days of age (Pejkovski et al., 1979; Dohms et al., 1981, 1988) and in turkey poults (Nusbaum et al, 1988) was reported. Adverse effects of infection on cell-mediated immune responses were reported but appear to be less severe and of lower magnitude when compared with the effect on antibody response. Prolonged skin graft rejection was reported in one study (Panigrahy et al., 1977 ) but this was not corroborated in other studies (Giambrone et al., 1977; Hudson et al., 1975 ). Furthermore no effect on tuberculin-delayed hypersensitivity was detected. On the other hand, in vitro studies have been useful in shedding light on the effect of IBDV infection on cell-mediated immune responses. Mitogen stimulation of peripheral blood lymphocytes from IBDV infected chickens was shown to be transiently depressed (Confer et al., 1981 ). Suppression of the cell-mediated immunity response was detected by a lymphoblast transformation assay and reached a maximum at 6 weeks post-infection (Sivanandan and Maheswaran, 1981 ). Suppression of the T-cell response of infected turkey poults was also reported (Nusbaum et al., 1988). No consistent effect on natural killer cell activity was detected (Sharma and Lee, 1984 ). MECHANISMS OF IMMUNOSUPPRESSION
Reduction in the number of lymphocytes particularly B cells and their actively dividing precursors in the BF is probably the most important cause of immunosuppression. The reduction in numbers is a result of lysis of the cells. It was speculated that suppression of B-cell function might be caused by other factors such as damage to helper T cells or other cells that might be involved in generating the immune responses (Sharma et al., 1989b). Stimulation of suppressor cells was another suggested possible mechanism (Sharma et al., 1989b ). Chickens infected with IBDV had suppressor cells in
48
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their spleens which caused in vitro mitogenic hyporesponsiveness to concanavalin A. These cells prevented normal spleen cells from responding to the mitogen and this effect was m e d i a t e d by a soluble factor (Sharma and Fredericksen, 1987 ). In summary, immunosuppression caused by IBDV is of major interest because of the widespread occurrence of the infection in commercial chickens. Infection with IBDV at an early age significantly compromises the humoral and local i m m u n e responses o f chickens. The cellular i m m u n e response is also c o m p r o m i s e d but apparently to a lesser extent and for a short period. The i m m u n o s u p p r e s s i o n seems to be the result of a direct effect (lysis) of B cells or their precursors. Other mechanisms of immunosuppression have been suggested, notably the development o f suppressor cells. There are a variety o f questions concerning immunosuppression caused by IBDV that need to be answered. These include: the persistence of i m m u n o suppression in the absence o f the virus, the ability o f the chicken to produce high levels of antibodies against the virus when response to other antigens is suppressed, the persistence o f antibodies to the virus for extended periods whereas the virus is detected only for a few days and finally the effect o f the infection on different sets o f lymphocytes and lymphokines. ACKNOWLEDGEMENTS Salaries and research support provided by state and federal funds appropriated to the Ohio Agricultural Research and Development Center, The Ohio State University. This investigation was supported in part by special grant 84-CRSR-2-2427, Science and Education Administration, U.S. D e p a r t m e n t o f Agriculture.
REFERENCES Allan, W.H., Faragher, J.T. and Cullen, G.A., 1972. Immunosuppressionby the infectious bursal agent in chickens immunized against Newcastle disease. Vet. Rec., 90:511-512. Anderson, W.I., Reid, W.M., Lukert, P.D. and Fletcher, O.J., 1977. Influenceof infectious bursal disease on the development of immunity to Eimeria tenella. Avian Dis., 21:637-641. Cho, B.R., 1970. Experimental dual infections of chickens with infectious bursal and Marek's disease agents. I. Preliminary observation on the effect of infectiousbursal agent on Marek's disease. Avian Dis., 14: 665-675. Confer, A.W., Springer, W.T., Shane, S.M. and Conovan, J.F., 1981. Sequential mitogen stimulation of peripheral blood lymphocytesfrom chickens inoculated with infectiousbursal diseases virus. Am. J. Vet. Res., 42:2109-2113. Craft, D.W., Brown, J. and Lukert, P.D., 1990. Effect of standard and variant strains of infectious bursal disease virus on infections of chickens. Am. J. Vet. Res., 51:1192-1197. Dohms, J.E., Lee, K.P. and Rosenberger, J.K., 1981. Plasma cell changes in the gland of harder followinginfectious bursal disease virus infection of the chicken. Avian Dis., 25: 683-695.
IMMUNOSUPPRESSIONBYINFECTIOUSBURSALDISEASEVIRUS
49
Dohms, J.E., Lee, K.P., Rosenberger, J.K. and Metz, A.L., 1988. Plasma cell quantitation in the gland of Harder during infectious bursal disease virus infection of 3-week-old broiler chickens. Avian Dis., 32:624-631. Fadley, A.M., Winterfield, R.W. and Olander, H.J., 1976. Role of the bursa of Fabricius in the pathogenicity of inclusion body hepatitis and infectious bursal disease virus. Avian Dis., 20: 467-477. Faragher, J.T., Allan, W.H. and Wyeth, C.J., 1974. Immunosuppressive effect of infectious bursal agent on vaccination against Newcastle disease. Vet. Rec., 95: 385-388. Giambrone, J.J., Donahoe, J.P., Dawe, D.L. and Eidson, C.S., 1977. Specific suppression of the bursa-dependent immune system of chicks with infectious bursal disease virus. Am. J. Vet. Res., 38:581-583. Higashihara, M., Saijo, K., Fujisaki, Y. and Matumoto, M., 1991. Immunosuppressive effect of infectious bursal disease virus strains of variable virulence for chickens. Vet. Microbiol., 26: 241-248. Hirai, K. and Calnek, B.W., 1979. In vitro replication of infectious bursal disease virus in established lymphoid cell lines and chicken B lymphocytes. Infect. Immun., 25: 964-970. Hirai, K., Shimakura, S., Kawamoto, E., Taguchi, F., Kim, S.T., Change, C.N. and Iritani, Y., 1974. The immunodepressive effect of infectious bursal disease virus in chickens. Avian Dis., 18: 50-57. Hirai, K., Kunihiro, K. and Shimakura, S., 1979. Characterization of immunosuppression in chickens by infectious bursal disease virus. Avian Dis., 23: 950-965. Hudson, L., Pattison, H. and Thantrey, N., 1975. Specific B lymphocyte suppression by infectious bursal agent (Gumboro disease virus) in chickens. Eur. J. Immunol., 5: 675-679. Ivanyi, J., 1975. Immunodeficiency in the chicken. II. Production of monomeric IgM following testosterone treatment of infection with Gumboro disease. Immunology, 28:1015-1021. Ivanyi, J. and Morris, R., 1976. Immunodeficiency in the chicken. IV. An immunological study of infectious bursal disease. Clin. Exp. Immunol., 23:154-165. Mazariegos, L.A., Lukert, P.D. and Brown J., 1990. Pathogenicity and immunosuppressive properties of infectious bursal disease "intermediate" strains. Avian Dis., 34: 203-208. Moradian, A., Thorsen, J. and Julian, R.J., 1990. Single and combined infections of specificpathogen-free chickens with infectious bursal disease virus and an intestinal isolate of reovirus. Avian Dis., 34: 63-72. Muller, H., 1986. Replication of infectious bursal disease virus in lymphoid cell. Arch. Virol., 87: 191-203. Muller, R., Kauffer, I., Reinacher, M. and Weiss, E., 1979. Immunofluorescent studies of early virus propagation after oral infection with infectious bursal disease virus (IBDV). Zentralbl. Veterinaermed. Reihe B., 26: 345-352. Nakai, T. and Hirai, K., 1981. In vitro infection of fractionated chicken lymphocytes by infectious bursal disease virus. Avian Dis., 25: 831-838. Nusbaum, K.E., Lukert, P.D. and Fletcher, O.J., 1988. Experimental infection of one-day-old poults with turkey isolates of infectious bursal disease virus. Avian Pathol., 17:51-62. Onaga, H., Togo, M., Otaki, Y. and Tajima, M., 1989. Influence of live virus vaccination against infectious bursal disease on coccidial infection in chickens. Jap. J. Vet. Sci., 51" 463-465. Panigrahy, B., Misra, L.K., Naqi, S.A. and Hall, C.F., 1977. Prolongation of skin allograft survival in chickens with infectious bursal disease. Poult. Sci., 56:1745. Pejkovski, C., Davelaar, F.G. and Kouwenhoven, B., 1979. Immunosuppressive effect of infectious bursal disease virus on vaccination against infectious bronchitis. Avian Pathol., 8" 95106. Rosenberger, J.K, and Gelb, Jr., J., 1978. Response to several avian respiratory viruses as affected by infectious bursal disease virus. Avian Dis., 22: 95-105. Santivatr, D., Maheswaran, S.K., Newman, J.A. and Pomeroy, B.S., 1981. Effect of infectious
50
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bursal disease virus infection on the phagocytosis of Staphylococcus aureus by mononuclear phagocytic cells of susceptible and resistant strains of chickens. Avian Dis., 25: 303- 311. Sharma, J.M., 1984. Effect of infectious bursal disease virus on protection against Marek's disease by turkey herpes virus vaccine. Avian Dis., 28: 629-640. Sharma, J.M. and Fredericksen, T.L., 1987. Mechanism of T cell immunodepression by infectious bursal disease virus of chickens. In: Avian Immunology. Alan R. Liss, New York, pp. 283-294. Sharma, J.M. and Lee, L.F., 1984. Effect of infectious bursal disease virus on natural killer cell activity and mitogenic response of chicken lymphoid cells: Role of adherent cells in cellular immune suppression. Infect. Immun., 42: 747-754. Sharma, J.M., Dohms, J.E. and Metz, A.L., 1989a. Comparative pathogenesis ofserotype 1 and variant serotype 1 isolates of infectious bursal disease virus and the effect of those viruses on humoral and cellular immune competence of specific pathogen free on chickens: Avian Dis., 33:112-124. Sharma, J.M., Dupuy, J.M. and Lamontagne, L., 1989b. Immunosuppression by avian infectious bursal disease virus and mouse hepatitis virus in virus. In: Induced Immunosuppression. Plenum Press, New York, NY, pp. 201-216. Sivanandan, V. and Maheswaran, S.K., 1980a. Immune profile of infectious bursal disease. 1. Effect of infectious bursal disease virus on peripheral blood T and B lymphocytes in chickens. Avian Dis., 24:715-725. Sivanandan, B. and Maheswaran, S.K., 1980b. Immune profile of infectious bursal disease (IBD). II. Effect of IBD virus on pokeweed-mitogen-stimulated peripheral blood lymphocytes of chickens. Avian Dis., 24: 734-743. Sivanandan, V. and Maheswaran, S.K., 1981. Immune profile of infectious bursal disease. III. Effect of infectious bursal disease virus on the lymphocyte responses to phytomitogens and on mixed lymphocyte reaction of chickens. Avian Dis., 25:112-120. Wyeth, P.J., 1975. Effect of infectious bursal disease on the response of chickens to Styphirnurium and E.Coli infections. Vet. Rec. 96: 238-243. Yuasa, N., Taniguchi, T., Noguchi, T. and Yoshida, I., 1980. Effect of infectious bursal disease virus infection on incidence of anemia by chicken anemia agent. Avian.Dis., 24: 202-209.
45
Elsevier Science Publishers B.V., Amsterdam
Immunosuppression induced by infectious bursal disease virus Y.M. Saif Food Animal Health Research Program, Ohio Agricultural Research and Development Center, The Ohio State University, Wooster, OH 44691, USA
ABSTRACT Saif, Y.M., 1991. Immunosuppression induced by infectious bursal disease virus. Vet. Immunol. Immunopathol., 30: 45-50. Immunosuppression caused by infectious bursal disease virus (IBDV) is of major interest because of the widespread occurrence of the infection in commercial chickens. Infection with IBDV at an early age significantly compromises the humoral and local immune responses of chickens. The cellular immune response is also compromised by apparently to a lesser extent and for a short period. The immunosuppression seems to be a result of direct effect (lysis) of B cells or their precursors. Other mechanisms of immunosuppression have been suggested, notably the development of suppressor cells. ABBREVIATIONS BF, bursa of Fabricius; IBDV, infectious bursal disease virus.
INTRODUCTION
Infectious bursal disease virus (IBDV) is a double-stranded RNA virus that has a bisegmented genome; it belongs to the family Birnaviridae. It causes an acute, highly contagious and immunosuppressive disease in chickens designated infectious bursal disease (IBD). The virus is stable in the environment of poultry and the infection is widespread worldwide. Two serotypes of the virus designated l and 2 and several subtypes of serotype 1 are recognized. Both serotypes infect chickens and turkeys but the disease is recognized only in chickens. The effect of the virus on lymphoid tissue was one of the early observations in naturally infected chickens. The immunosuppressive effect of the virus in chickens exposed to the virus at a young age was reported early (Allan et al., 1972). The disease has a short incubation period and high morbidity. Birds 0165-2427/91/$03.50
© 1991 Elsevier Science Publishers B.V. All rights reserved.
46
Y.M. SAIF
less than 3 weeks of age usually do not exhibit clinical signs but are immunosuppressed whereas birds between 3 and 6 weeks of age are considered most susceptible to the clinical disease. Clinical signs are not specific but gross and microscopic lesions are characteristic. Lymphoid cells and macrophages in the intestine are infected following ingestion of the virus and these cells carry the virus to the bursa of Fabricius (BF) (Muller et al., 1979). The prominent lesions are in the BF which undergoes an increase in size owing to inflammatory changes followed by atrophy. Some of the recent field isolates (referred to as variants) do not induce inflammation hence, mainly atrophy is detected. Atrophy is caused by destruction of lymphocytes. Similar but less pronounced lesions are detected in the spleen, thymus, cecal tonsils and harderian gland. INTERACTIONS OF IBDV INFECTION WITH OTHER INFECTIONS
Infection with IBDV was reported to affect the course of a variety of bacterial, protozoal and viral diseases of chickens. The effect of the infection on the antibody response to Newcastle disease virus was one of the earliest observed immunosuppressive effects of the infection (Allan et al., 1972; Faragher et al., 1974). Later, suppression of response to other vaccines was reported (Hirai et al., 1974 ). In further studies, it was demonstrated that chicks infected early in life with IBDV have increased susceptibility to a variety of viral diseases including: inclusion body hepatitis (Fadley et al., 1976), Marek's disease (Cho 1970; Sharma, 1984), infectious bronchitis (Pejkovski et al., 1979 ), infectious laryngotracheitis (Rosenberger and Gelb, 1978 ), chicken anemia (Yuasa et al., 1980) and reoviruses (Moradian et al., 1990). Infection with IBDV was also reported to increase susceptibility to Salmonella typhimurium, Escherichia coli (Wyeth, 1975 ), Staphylococcus aureus ( Santivatr et al., 1981 ) and coccidial infections (Anderson et al., 1977; Onaga et al., 1989). The immunosuppressive effects of IBDV are dependent on the strain of the virus (Sharma et al., 1989a; Craft et al., 1990; Mazariegos et al., 1990; Higashihara et al., 1991 ). H U M OR AL AND CELLULAR MANIFESTATIONS OF THE INFECTION
As mentioned earlier, the age at which infection occurs is important in determining whether immunosuppression follows the infection and the degree of immunosuppression. Infection in the first 2 weeks of life was reported to be more immunosuppressive than infection at a later age and both the primary and secondary immune responses were adversely affected (Faragher et al., 1974). Infection at 1 day of age resulted in severe deficiency of serum immunoglobulin (Ig) G and only a monomeric IgM was produced (Ivanyi,
IMMUNOSUPPRESSION BY INFECTIOUS BURSAL DISEASEVIRUS
47
1975; Ivanyi and Morris, 1976). The level of IgG was reported to vary depending on the age at the time of infection (Ivanyi and Morris, 1976; Hirai et al., 1979). The adverse effect on antibody (Ig) response is probably to a large extent a result of the effect on the bursa-derived lymphocytes (B-cells) in both the BF and in the blood. It was shown that the number of peripheral blood B cells was reduced but the thymus-derived lymphocytes (T cells ) were not significantly affected (Hirai et al., 1979; Sivanandan and Maheswaran, 1980a). Cells expressing IgM have been shown to be the particular targets for IBDV (Hirai and Calnek, 1979; Nakai and Hirai, 1981 ). The virus seems to have a predilection for actively proliferating cells (Muller, 1986 ) such as the immature or precursor B cells as compared with mature B cells (Sivanandan and Maheswaran, 1980b). There is evidence that the local immune system is also adversely affected by IBDV infection. A significant reduction in plasma cells in the harderian gland of chicks infected with IBDV at 1-5 days of age (Pejkovski et al., 1979; Dohms et al., 1981, 1988) and in turkey poults (Nusbaum et al, 1988) was reported. Adverse effects of infection on cell-mediated immune responses were reported but appear to be less severe and of lower magnitude when compared with the effect on antibody response. Prolonged skin graft rejection was reported in one study (Panigrahy et al., 1977 ) but this was not corroborated in other studies (Giambrone et al., 1977; Hudson et al., 1975 ). Furthermore no effect on tuberculin-delayed hypersensitivity was detected. On the other hand, in vitro studies have been useful in shedding light on the effect of IBDV infection on cell-mediated immune responses. Mitogen stimulation of peripheral blood lymphocytes from IBDV infected chickens was shown to be transiently depressed (Confer et al., 1981 ). Suppression of the cell-mediated immunity response was detected by a lymphoblast transformation assay and reached a maximum at 6 weeks post-infection (Sivanandan and Maheswaran, 1981 ). Suppression of the T-cell response of infected turkey poults was also reported (Nusbaum et al., 1988). No consistent effect on natural killer cell activity was detected (Sharma and Lee, 1984 ). MECHANISMS OF IMMUNOSUPPRESSION
Reduction in the number of lymphocytes particularly B cells and their actively dividing precursors in the BF is probably the most important cause of immunosuppression. The reduction in numbers is a result of lysis of the cells. It was speculated that suppression of B-cell function might be caused by other factors such as damage to helper T cells or other cells that might be involved in generating the immune responses (Sharma et al., 1989b). Stimulation of suppressor cells was another suggested possible mechanism (Sharma et al., 1989b ). Chickens infected with IBDV had suppressor cells in
48
Y.M. SA1F
their spleens which caused in vitro mitogenic hyporesponsiveness to concanavalin A. These cells prevented normal spleen cells from responding to the mitogen and this effect was m e d i a t e d by a soluble factor (Sharma and Fredericksen, 1987 ). In summary, immunosuppression caused by IBDV is of major interest because of the widespread occurrence of the infection in commercial chickens. Infection with IBDV at an early age significantly compromises the humoral and local i m m u n e responses o f chickens. The cellular i m m u n e response is also c o m p r o m i s e d but apparently to a lesser extent and for a short period. The i m m u n o s u p p r e s s i o n seems to be the result of a direct effect (lysis) of B cells or their precursors. Other mechanisms of immunosuppression have been suggested, notably the development o f suppressor cells. There are a variety o f questions concerning immunosuppression caused by IBDV that need to be answered. These include: the persistence of i m m u n o suppression in the absence o f the virus, the ability o f the chicken to produce high levels of antibodies against the virus when response to other antigens is suppressed, the persistence o f antibodies to the virus for extended periods whereas the virus is detected only for a few days and finally the effect o f the infection on different sets o f lymphocytes and lymphokines. ACKNOWLEDGEMENTS Salaries and research support provided by state and federal funds appropriated to the Ohio Agricultural Research and Development Center, The Ohio State University. This investigation was supported in part by special grant 84-CRSR-2-2427, Science and Education Administration, U.S. D e p a r t m e n t o f Agriculture.
REFERENCES Allan, W.H., Faragher, J.T. and Cullen, G.A., 1972. Immunosuppressionby the infectious bursal agent in chickens immunized against Newcastle disease. Vet. Rec., 90:511-512. Anderson, W.I., Reid, W.M., Lukert, P.D. and Fletcher, O.J., 1977. Influenceof infectious bursal disease on the development of immunity to Eimeria tenella. Avian Dis., 21:637-641. Cho, B.R., 1970. Experimental dual infections of chickens with infectious bursal and Marek's disease agents. I. Preliminary observation on the effect of infectiousbursal agent on Marek's disease. Avian Dis., 14: 665-675. Confer, A.W., Springer, W.T., Shane, S.M. and Conovan, J.F., 1981. Sequential mitogen stimulation of peripheral blood lymphocytesfrom chickens inoculated with infectiousbursal diseases virus. Am. J. Vet. Res., 42:2109-2113. Craft, D.W., Brown, J. and Lukert, P.D., 1990. Effect of standard and variant strains of infectious bursal disease virus on infections of chickens. Am. J. Vet. Res., 51:1192-1197. Dohms, J.E., Lee, K.P. and Rosenberger, J.K., 1981. Plasma cell changes in the gland of harder followinginfectious bursal disease virus infection of the chicken. Avian Dis., 25: 683-695.
IMMUNOSUPPRESSIONBYINFECTIOUSBURSALDISEASEVIRUS
49
Dohms, J.E., Lee, K.P., Rosenberger, J.K. and Metz, A.L., 1988. Plasma cell quantitation in the gland of Harder during infectious bursal disease virus infection of 3-week-old broiler chickens. Avian Dis., 32:624-631. Fadley, A.M., Winterfield, R.W. and Olander, H.J., 1976. Role of the bursa of Fabricius in the pathogenicity of inclusion body hepatitis and infectious bursal disease virus. Avian Dis., 20: 467-477. Faragher, J.T., Allan, W.H. and Wyeth, C.J., 1974. Immunosuppressive effect of infectious bursal agent on vaccination against Newcastle disease. Vet. Rec., 95: 385-388. Giambrone, J.J., Donahoe, J.P., Dawe, D.L. and Eidson, C.S., 1977. Specific suppression of the bursa-dependent immune system of chicks with infectious bursal disease virus. Am. J. Vet. Res., 38:581-583. Higashihara, M., Saijo, K., Fujisaki, Y. and Matumoto, M., 1991. Immunosuppressive effect of infectious bursal disease virus strains of variable virulence for chickens. Vet. Microbiol., 26: 241-248. Hirai, K. and Calnek, B.W., 1979. In vitro replication of infectious bursal disease virus in established lymphoid cell lines and chicken B lymphocytes. Infect. Immun., 25: 964-970. Hirai, K., Shimakura, S., Kawamoto, E., Taguchi, F., Kim, S.T., Change, C.N. and Iritani, Y., 1974. The immunodepressive effect of infectious bursal disease virus in chickens. Avian Dis., 18: 50-57. Hirai, K., Kunihiro, K. and Shimakura, S., 1979. Characterization of immunosuppression in chickens by infectious bursal disease virus. Avian Dis., 23: 950-965. Hudson, L., Pattison, H. and Thantrey, N., 1975. Specific B lymphocyte suppression by infectious bursal agent (Gumboro disease virus) in chickens. Eur. J. Immunol., 5: 675-679. Ivanyi, J., 1975. Immunodeficiency in the chicken. II. Production of monomeric IgM following testosterone treatment of infection with Gumboro disease. Immunology, 28:1015-1021. Ivanyi, J. and Morris, R., 1976. Immunodeficiency in the chicken. IV. An immunological study of infectious bursal disease. Clin. Exp. Immunol., 23:154-165. Mazariegos, L.A., Lukert, P.D. and Brown J., 1990. Pathogenicity and immunosuppressive properties of infectious bursal disease "intermediate" strains. Avian Dis., 34: 203-208. Moradian, A., Thorsen, J. and Julian, R.J., 1990. Single and combined infections of specificpathogen-free chickens with infectious bursal disease virus and an intestinal isolate of reovirus. Avian Dis., 34: 63-72. Muller, H., 1986. Replication of infectious bursal disease virus in lymphoid cell. Arch. Virol., 87: 191-203. Muller, R., Kauffer, I., Reinacher, M. and Weiss, E., 1979. Immunofluorescent studies of early virus propagation after oral infection with infectious bursal disease virus (IBDV). Zentralbl. Veterinaermed. Reihe B., 26: 345-352. Nakai, T. and Hirai, K., 1981. In vitro infection of fractionated chicken lymphocytes by infectious bursal disease virus. Avian Dis., 25: 831-838. Nusbaum, K.E., Lukert, P.D. and Fletcher, O.J., 1988. Experimental infection of one-day-old poults with turkey isolates of infectious bursal disease virus. Avian Pathol., 17:51-62. Onaga, H., Togo, M., Otaki, Y. and Tajima, M., 1989. Influence of live virus vaccination against infectious bursal disease on coccidial infection in chickens. Jap. J. Vet. Sci., 51" 463-465. Panigrahy, B., Misra, L.K., Naqi, S.A. and Hall, C.F., 1977. Prolongation of skin allograft survival in chickens with infectious bursal disease. Poult. Sci., 56:1745. Pejkovski, C., Davelaar, F.G. and Kouwenhoven, B., 1979. Immunosuppressive effect of infectious bursal disease virus on vaccination against infectious bronchitis. Avian Pathol., 8" 95106. Rosenberger, J.K, and Gelb, Jr., J., 1978. Response to several avian respiratory viruses as affected by infectious bursal disease virus. Avian Dis., 22: 95-105. Santivatr, D., Maheswaran, S.K., Newman, J.A. and Pomeroy, B.S., 1981. Effect of infectious
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