Evaluation of Chicken Infectious Anemia Virus and Associated Risk Factors with Disease and Production Losses in Broilers

Author(s): Lynn T. Hagood, Tamara F. Kelly, James C. Wright and Frederic J. Hoerr Reviewed work(s): Source: Avian Diseases, Vol. 44, No. 4 (Oct. - Dec., 2000), pp. 803-808 Published by: American Association of Avian Pathologists Stable URL: [Link] . Accessed: 13/07/2012 07:17
Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . [Link]

.
JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact support@[Link].

American Association of Avian Pathologists is collaborating with JSTOR to digitize, preserve and extend access to Avian Diseases.

[Link]

AVIAN DISEASES 44:803-808,

2000

Evaluation of Chicken Infectious Anemia Virus and Associated Risk Factors with Disease and Production Losses in Broilers
Lynn T. Hagood,A Tamara F. Kelly,BJames C. Wright,C and Frederic J. HoerrAC
ACharles S. Roberts Veterinary Diagnostic Laboratory, P.O. Box 2209, Auburn, AL 36831-2209 BAlabama Veterinary Diagnostic Laboratory, 501 Usury Avenue, Boaz, AL 35957 CDepartment of Pathobiology, College of Veterinary Medicine, Auburn University, Auburn, AL 36849-5519 Received 17 December 1999

SUMMARY. A case-control study was performed to determine the significance of chicken infectious anemia virus (CIAV) as a risk factor associated with secondary disease in commercial broilers and to identify the significance of production losses associated with CIAV. The study also examined the relationship between bursal and thymic atrophy and the presence of CIAV. Cases were defined as submissions to the Alabama Veterinary Diagnostic Laboratories with a history of clinical disease and with a diagnosis of coccidiosis, gangrenous dermatitis, or respiratory disease. Controls were selected from submissions with neither a history of disease nor evidence of disease on necropsy. CIAV was detected in fresh tissues by polymerase chain reaction. Both thymic atrophy and the detection of CIAV were significantly associated with a disease case (P < 0.05). Bursal atrophy was a significant risk factor associated with the detection of CIAV in a submission (P < 0.05). Whereas CIAV was associated with disease cases that showed production losses in both percentage of livability and percentage of condemnations (P < 0.05), detection of CIAV alone was not associated with detectable losses in production or flock performance. RESUMEN. Evaluaci6n del virus de la anemia infecciosa aviar y factores de riesgo asociados con la enfermedad y con las perdidas en producci6n en pollos de engorde. Se realiz6 un estudio controlado de caso para determinar la importancia del virus de la anemia infecciosa aviar como factor de riesgo asociado con enfermedades secundarias y con las perdidas en produccion en pollos de engorde comerciales. El estudio tambien examin6 la relaci6n de la atrofia de la bolsa y el timo con la presencia del virus de la anemia infecciosa aviar. Los casos fueron recibidos en el Laboratorio de Diagn6stico Veterinario de Alabama con una historia de enfermedad clinica y con diagn6stico de coccidiosis, dermatitis gangrenosa 6 enfermedad respiratoria. Los controles fueron seleccionados de los casos recibidos que no tenian historia de enfermedad o que no presentaban ninguna evidencia de enfermedad a la necropsia. El virus de la anemia infecciosa aviar fue detectado en tejidos frescos mediante la reacci6n en cadena por la polimerasa. Tanto la atrofia del timo como la detecci6n del virus de la anemia infecciosa aviar estuvieron asociados significantemente (P < 0.05) con un caso de enfermedad. La atrofia de la bolsa fue un factor de riesgo significante (P < 0.05) asociado con la detecci6n del virus de la anemia infecciosa aviar en un caso recibido. Mientras que el virus de la anemia infecciosa aviar estuvo asociado con los casos de enfermedad que mostraron perdidas en producci6n tanto en los porcentajes de viabilidad como en los porcentajes de descartes (P < 0.05), la deteccion del virus de la anemia infecciosa aviar por si sola no estuvo asociada con perdidas detectables en la producci6n o con el rendimiento de la parvada. Key words: chicken infectious anemia, thymic atrophy, bursal atrophy, thymus, bursa of Fabricius Abbreviations: AVDL = Alabama Veterinary Diagnostic Laboratory; CI = confidence interval; CIAV = chicken infectious anemia virus; OR = Odds ratio; PCR = polymerase chain reaction

803

804

L. T. Hagood et al.

Chicken infectious anemia is a viral disease of chickens characterized by aplastic anemia, generalized lymphoid atrophy, and immunosuppression (3). The virus plays a role in several disease syndromes with the outcome of infection often complicated by secondary viral, bacterial, or fungal infections. Uncomplicated infection with chicken infectious anemia virus (CIAV) may result in transient poor performance and slightly increased mortality (3). Whether alone or in combination with other agents, CIAV is important because of its potential for inducing immunosuppression (11). Circumstantial evidence indicates that poor performance of commercial broiler chickens occurs after subclinical infection with CIAV, but this has not been confirmed (6,9). Although the only specific sign of infection with CIAV is anemia, gross lesions occur in lymphoid tissue and bone marrow and are most pronounced 12-16 days after infection (14,19). CIAV exerts a destructive effect on primary and secondary lymphoid tissue and specifically suppresses the population of CD4+ and CD8+ T lymphocytes in the thymus (5). CIAV infection remains subclinical in most broiler flocks because of the presence of maternal antibodies (2,17). As maternal antibody levels decline, chickens can become infected with CIAV (8). Chicks bursectomized during embryonic development are at increased risk from infection with CIAV (7,16). The risk of infection is also increased through the immunosuppressive effects of Marek's disease and infectious bursal disease (1,10). The purpose of this study was to determine the significance of CIAV as a risk factor associated with other (secondary) disease in commercial broilers and to identify the significance of production losses associated with CIAV. The association between necropsy findings of bursal and thymic atrophy and the presence of CIAV or other (secondary) disease was also examined. This retrospective case-control study involved an investigation of diagnostic submissions from commercial broiler flocks to the Alabama Veterinary Diagnostic Laboratories (AVDL) and the performance records of those flocks. MATERIALSAND METHODS Submissions to the laboratory. This study involved necropsy submissions of broilers from single

production houses to the AVDL from January 1,

1997, to December 31, 1997. For some submissions,

submitted birds represented entire [Link] birds an

per flock were submitted for necropsy from clinically

normal flocks as part of a coccidia monitoring program (control group). On average, 10 birds per flock

were submitted for necropsy from clinicallydiseased

flocks. These submissions represent standard laboratory practice for the coccidia control monitoring program and diagnostic case submissions. All submissions (cases and controls) were tested for the presence of CIAV by polymerase chain reaction (PCR) amplification of viral DNA extracted from homogenized spleen, thymus, or bone marrow and electrophoresis of amplicon in 2% agarose gel (15). Initially, all three tissues were tested, but because of the agreement of PCR results between the different tissues, subsequent cases were tested with spleen only. Age of the flock at submission was also recorded. In an effort to maintain balance and uniformity between cases and controls, only three production companies were involved in this study. Bursa of Fabricius and thymus Histopathology. lobes from submissions were routinely processed for histopathology and evaluated for lymphocytic depletion. Similar tissues were processed from each submission and scored for lymphocytic depletion as 1, normal; 2, mild; 3, moderate; and 4, severe. The most severe lesion score was recorded for each flock. Lesion scores of 3 or greater were regarded as histopathologic evidence of bursal or thymic atrophy. Selection of cases. Case criteria were defined as submissions for complete necropsy and ancillary testing that included one of the following findings: coccidiosis, gangrenous dermatitis, or respiratory disease (tracheitis). Presence of one of these findings was used as an indication of disease. Selection of controls. Controls were defined as submissions to the laboratory that had been selected from clinically normal broiler flocks for examination as part of a coccidia control monitoring program. Controls had no history of disease and no overt evidence of disease (coccidiosis, gangrenous dermatitis, or respiratory disease) on necropsy. Risk factors. The following relationships were evaluated to determine potential risk factors associated with detection of CIAV or a disease case (coccidiosis, gangrenous dermatitis, respiratory disease). 1) Presence of CIAV as determined by PCR was evaluated as a risk factor for disease. 2) The presence of bursal or thymic atrophy indicated by a lesion score of 3 or greater on histopathologic examination was evaluated as a risk factor for the presence of CIAV or disease. Performance data. Once case and control flocks were identified, production and processing information for each flock was reviewed from records within a company production complex for determination of

Chickeninfectiousanemiaand broilerproduction Table 1. Detection of CIAV with disease case, bursal atrophy,or thymic atrophy. CIAV
positiveA

805

Table 2. Presence of thymic and bursal atrophy in disease and control cases. Bursal Thymic atrophyA atrophyA PrePresent Absent sent Absent Disease casesB Nondisease controls 39 28 21 35 56 51 4 12

CIAV
negativeA

Disease casesB 49 11 Nondisease controls 32 31 48 19 Thymic atrophy presentc 24 32 Thymic atrophy absentc Bursalatrophy presentc 76 31 4 Bursalatrophy absentc 12 detection by PCR. ACIAV BCoccidiosis,gangrenousdermatitis,or respiratory disease. evaluation. CHistopathologic performancedata. Percentageof livability,feed conversion, condemnations at processing, and production cost (cost per pound) were used as indicatorsof production loss and were evaluated for associations with the presenceof CIAV,thymic atrophy,and disease cases (coccidiosis,gangrenousdermatitis,and respiratory disease). To establish equivalencybetween flocks, feed conversionwas adjustedfor differencesin bird weight of an individual flock from the mean weight of all [Link] conversionratioswere adjusted 0.1 for each 0.6-pound difference in bird weight for the flock from the mean weight of all submissions. Statistical analysis. An odds ratio (OR) was used to estimatethe relativeriskfor an associationbetween the presence of a risk factor and disease. An odds ratio is defined as the odds that a case is exposed divided by the odds that a control is exposed. Individual risk factorswere evaluatedwith a 95% confidence interval (CI) on the odds ratio and the Yates corrected chi-square test (12,20). Risk factors were consideredsignificantif the CI did not cross 1.0 and P ' 0.05. Odds ratios were determined with EpiInfo statisticalsoftware(Epi-Info 6.0, 1994, Centers for Disease Control, Atlanta, GA). A Student'st-test (20) was used to analyzecontinuous variablesto determine the effect of the presence of CIAV, thymic atrophy, and disease on performance criteria (percentage of livability, adjusted feed conversion, condemnations, and cost of production). RESULTS Detection of CIAV. A total of 123 submissions to the Alabama Veterinary Diagnostic Laboratories were evaluated in the study. Of these, 60 submissions (48.8%) were considered disease cases and 63 (51.2%) were used as controls. CIAV was detected by PCR in 80 (65.0%) of the 123 submissions. The PCR re-

evaluation. AHistopathologic BCoccidiosis,gangrenousdermatitis,or respiratory disease. suits indicated the presence of CIAV in 49 (81.7%) of the disease cases. Association of CIAV with disease. CIAV was a significant risk factor for a disease case (OR = 4.60, 95% CI = 1.89-11.38, P = 0.0003; Table 1). Association of thymic atrophy with CIAV and disease. Thymic atrophy was present in 48 (60.0%) of the submissions positive for CIAV but was not considered a significant risk factor associated with the detection of virus (OR = 1.89, 95% CI = 0.84-4.30, P = 0.1363; Table 1). Thymic atrophy was present in 39 (65.0%) of the disease cases. Thymic atrophy was determined to be a significant risk factor associated with a disease case (OR = 2.32, 95% CI = 1.06-5.14, P = 0.035; Table 2). Association of bursal atrophy with CIAV and disease. Bursal atrophy was present in 76 (95.0%) of the submissions positive for CIAV and was considered a significant risk factor associated with the detection of virus (OR = 7.35, 95% CI = 1.98-29.60, P = 0.0009; Table 1). Bursal atrophy was present in 56 (93.3%) of diseased cases but was not a significant risk factor associated with disease (OR = 3.29, 95% CI = 0.90-13.03, P = 0.076; Table 2). Association of CIAV and performance. The performance of flocks associated with detection of CIAV in a submission is listed in Table 3. Although mean percentage of livability was 1.52% lower (P = 0.06) and mean percentage of condemnations was 0.63% higher (P = 0.171) in flocks with CIAV, the associations were not considered significant by a one-tailed t-test. The detection of CIAV in a submission was not associated with a change in adjusted feed conversion (P = 0.374) or cost of produc-

806

L. T. Hagood et al.

Table 3. Association of CIAV with performance. CIAV positiveA Mean percentageof livability (?SD) Adjusted feed conversion (+SD) Mean percentageof condemnations (+SD) Averagecost per pound (cents) (+SD) ACIAV detection by PCR. 90.24 2.18 3.81 19.77 (+4.81) (+0.16) (?3.57) (+1.66) CIAV negativeA 91.76 2.19 3.18 19.54 (?5.57) (+0.12) (?3.23) (+1.19)

tion (P = 0.211) of the flock compared with flocks negative for CIAV (Table 3). formance.

DISCUSSION This study of field cases and diagnostic submissions in commercial broilers supports experimental findings associated with CIAV infection in chickens. Detection of CIAV increased in cases diagnosed with coccidiosis, gangrenous dermatitis, or respiratory disease (disease cases). This supports the hypothesis that CIAV infection plays a role in disease syndromes complicated by other viral, bacterial, or fungal infections. The association found between thymic atrophy, a characteristic lesion of CIAV infection, and diseased cases may further support this hypothesis. On the other hand, a relationship was not detected between the lesion of thymic atrophy and detection of CIAV in this study. Although other agents may cause thymic atrophy, this finding could also be explained by persistence of thymic lesions beyond presence of CIAV in tissues. Although CIAV may be present in rectal contents for up to 49 days (18), virally infected cells are usually not detected from the proventriculus, duodenum, kidney, or lung beyond 22 days after infection (13). However, the histopathologic lesion of the thymus does not return to normal until 32-36 days after infection (3). Although the authors have not determined the duration of viral detection in the spleen after infection with CIAV, the presence of thymic atrophy could persist beyond clearance and detection of the virus.

Association of thymic atrophy and per-

The histopathologic presence of thymic atrophy in a submission was not associated with a significant change in mean percentage of livability (P = 0.197), adjusted feed conversion (P = 0.167), mean percentage of condemnations (P = 0.22), or cost of production (P = 0.305) in the flock compared with flocks without thymic atrophy (Table 4).

Association of disease and performance.

Cases of disease were significantly associated with performance and production losses in the flock. Mean percentage of livability was 4.43% lower (P = 0.0000003) and mean percentage of condemnations was 2.10% higher (P = 0.0006) in disease cases than controls. The cost of production for the flock was 0.74 of a cent per pound more (P = 0.007) in disease cases than controls. The difference in adjusted feed conversion between disease cases and controls was not significant (P = 0.26; Table 5).

Age of flock at submission. The mean age

(+SD) of the flock at submission was 29.7 (+8.4) days for flocks negative for CIAV compared with a mean age of 37.2 (?8.4) days for CIAV-positive flocks (7.5 days difference, P = 0.000008). The mean age (+SD) of the flock at submission was 38.1 (?8.2) days for disease cases and 31.2 (?8.8) days for survey controls (6.9 days difference, P = 0.00002).

Table 4. Association of thymic atrophywith performance. Thymic atrophy presentA Thymic atrophy absentA Mean percentageof livability (?SD) Adjusted feed conversion (+SD) Mean percentageof condemnations (?SD) Averagecost per pound (cents) (+SD) evaluation. AHistopathologic
90.42 (?5.04) 2.17 (?0.16) 3.81 (+3.75) 91.23 (?5.24) 2.19 (?0.20)

3.31 (+3.06)
19.77 (?1.78)

19.63 (?+1.26)

Chickeninfectiousanemiaand broilerproduction Table 5. Association of diseasewith performance. Disease caseA Mean percentageof livability (+SD) Adjusted feed conversion (+SD) Mean percentageof condemnations (?SD) Averagecost per pound (cents) (?SD) 88.46 2.19 4.64 20.08 (?5.46) (?0.18) (?4.24) (+1.31)

807

Nondisease control 92.89 2.18 2.63 19.33 (?3.75) (+0.09) (?2.14) (?1.59)

disease. ACoccidiosis, gangrenousdermatitis,or respiratory

Bursal atrophy, a lesion often associated with immunosuppression from several causes, was associated with detection of CIAV. This finding in commercial broilers is supportive of previous experimental findings that bursal atrophy is a risk factor for the development of CIAV (4,16). With the use of ancillary diagnostic and clinical data, infectious bursal disease virus has been demonstrated to be a likely cofactor associated with bursal atrophy (unpubl. information). Consideration must also be given to the potential of CIAV to induce similar changes in the bursa (3). CIAV infection results in lymphocytic depletion, although slight, in this tissue and could be a contributing factor in this finding. In this retrospective study, it was impossible to determine which finding occurred first, the bursal atrophy or presence of CIAV. In this study, significant losses in production and flock performance were associated with disease cases. The mean percentage of livability was 4.43% lower (P < 0.001) and mean percentage of condemnations was 2.10% higher (P < 0.001) in disease cases compared with controls. The total cost of production was also higher for disease cases by 0.74 of a cent per pound (P = 0.007). Because of the increased risk for disease associated with detection of CIAV, decreases in production and performance criteria of broilers infected with CIAV would be expected. However, this study found no difference in adjusted feed conversion, percentage of livability, condemnations, or cost of production between infected and noninfected broiler flocks. Regarding detection of CIAV, these results are not supportive of previous findings of poor performance of commercial broiler chickens after subclinical infection with CIAV (8). However, because of the findings that detection of CIAV and histopathologic evidence of thymic atrophy are associated with an increased risk for a diseased case, the results suggest that infection with CIAV is a contributing factor to

disease in commercial broilers. Furthermore, the study indicates significant production losses associated with disease cases. The losses from disease resulting in decreased livability and increased cost of production compounded by increases in condemnations at processing translate into substantial economic losses for companies and producers with current volumes of production. REFERENCES 1. Bulow,V. v., B. Fuchs, and R. [Link] infectious anemia caused by chicken anaemia agent (CAA). In: Acute virus infections of poultry, J. B. McFerranand M. S. McNulty, eds. MartinusNijhoff Publ. Dordrecht, The Netherlands. Pp. 203-212. 1986. 2. Bulow, V. v., R. Rudolph, and B. Fuchs. Erhohte Pathogenitatdes Erregensder aviareninfektiosen Anamie bei Huhnerkuken(CAA) bie simultaner Infektion mit dem Virus der MarekschenKrankheit (MDV), Buritisvirus(IBDV) oder Reticuloendotheliosevirus(REV). J. Vet. Med. B 33:93-116. 1986. 3. Bulow, V. v., and K. A. Schat. Chicken infectious anemia. In: Diseases of poultry, 10th ed. B. W. Calnek, H. J. Barnes, C. W. Beard, L. R. McDougald, and Y. M. Saif, eds. Iowa State University Press,Ames, IA. Pp. 739-756. 1997. 4. Hu, L. B., B. Lucio, and K. A. Schat. Abrogation of age-relatedresistanceto chicken infectious anemia by embryonal bursectomy. Avian Dis. 37: 157-169. 1993. 5. Hu, L. B., B. Lucio, and K. A. Schat. Depletion of CD4+ and CD8+ T lymphocyte subpopulations by CIA-1, a chicken infectious anemia virus. Avian Dis. 37:492-500. 1993. 6. Jorgensen,P. H., L. Otte, O. L. Nielsen, and M. [Link] of subclinicalvirus infections and other factors on broiler flock [Link]. Poult. Sci. 36:455-463. 1995. 7. Lucio, B., K. A. Schat, and H. L. Shivaprasad. Identificationof the chicken anemia agent, reproduction of the diseaseand serologicalsurveyin the United [Link] Dis. 34:146-153. 1990.

808

L. T. Hagood et al. 14. Taniguchi, T., N. Yuasa, M. Maeda, and T. Horiuchi. Hematopathologicalchanges in dead and moribund chicks induced by chicken anemia agent. Natl. Inst. Anim. Health Q. (Yatabe) 22:61-69. 1982. 15. Todd, D., R. A. Mawhinney, and M. S. McNulty. Detection and differentiation of chicken anemia virus isolates by using the polymerasechain reaction.J. Clin. Microbiol. 30:1661-1666. 1992. 16. Yuasa,N., K. Imai, and K. [Link] of chicken anaemiaagent in bursectomised chickens. Avian Pathol. 17:363-369. 1988. 17. Yuasa,N., T. Noguchi, K. Furuta,and I. Yoshida. Maternalantibody and its effect on the susceptibility of chicks to chicken anemia agent. Avian Dis. 24:197-201. 1980. 18. Yuasa, N., T. Taniguchi, T. Imada, and H. Hihara. Distribution of chicken anemia agent (CAA) and detection of neutralizingantibody in chicks experimentallyinoculatedwith CAA. Natl. Inst. Anim. Health Q. (Yatabe)23:78-81. 1983. 19. Yuasa,N., T. Taniguchi, and I. [Link] lation and some characteristics an agent inducing anemia in chicks. Avian Dis. 23:366-385. 1979. 20. Zar,J. H. Biostatisticalanalysis,2nd ed. Prentice-Hall, Inc., Englewood Cliffs, NJ. 1984.

8. McConnell, C. D. G., B. M. Adair, and M. S. McNulty. Effects of chicken anemia virus on cellmediated immune function in chickens exposed to the virus by a naturalroute. Avian Dis. 37:366-374. 1993. 9. McNulty, M. S., S. G. Mcllroy, D. W. Bruce, and D. Todd. Economic effects of subclinicalchicken anemia agent infection in [Link]. 35:263-268. 1991. 10. Rosenberger, K., and S. S. Cloud. The efJ. fects of age, route of exposure, and coinfection with infectious bursal disease virus on the pathogenicity of and transmissibility chicken anemia agent (CAA). Avian Dis. 19:753-759. 1989. 11. Rosenberger, K., and S. S. Cloud. Chicken J. anemia virus. Poult. Sci. 77:1190-1192. 1998. clinicalepidemiology: 12. Smith, R. D. Veterinary a problem-oriented approach, 2nd ed. CRC Press Inc., Boca Raton, FL. pp. 91-109. 1995. 13. Smyth, T. A., D. A. Moffett, M. S. McNulty, D. Todd, and D. P. Mackie. A sequentialhistopathologic and immunocytochemical study of chicken anemia virus infection at one day of age. Avian Dis. 37:324-338. 1993.