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Avian Pathology
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Naturallyoccurring adenovirusassociated gastrointestinal lesions in Coturnix (Coturnix coturnix) quail

S. S. Tsai , T. C. Chang , G. N. Chang , R. S. Chern , M. S. Chien & C. Itakura
a c a a a a b

Laboratory of Comparative Pathology, Department of Veterinary Medicine , National Pingtung University of Science and Technology , Taiwan
b c

Department of Veterinary Medicine , National Chung Hsing University , Taiwan

The Institute of Physical and Chemical Research (Riken) , Hirosawa 21, WakoShi, Saitama, 35101, Japan Published online: 12 Nov 2007.

To cite this article: S. S. Tsai , T. C. Chang , G. N. Chang , R. S. Chern , M. S. Chien & C. Itakura (1998) Naturallyoccurring adenovirusassociated gastrointestinal lesions in Coturnix (Coturnix coturnix) quail, Avian Pathology, 27:6, 641-643 To link to this article: http://dx.doi.org/10.1080/03079459808419396

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Avian Pathology (1998) 27, 641-643

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Naturally-occurring adenovirus-associated gastrointestinal lesions in Coturnix (Coturnix coturnix) quail

S. S. Tsai1*, T. C. Chang1, G. N. Chang1, R. S. Chern1, M. S. Chien2 & C. Itakura3
1

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Laboratory of Comparative Pathology, Department of Veterinary Medicine, National Pingtung University of Science and Technology, and 2Department of Veterinary Medicine, National Chung Hsing University, Taiwan, and 3The Institute of Physical and Chemical Research (Riken) Hirosawa 2-1, Wako-Shi, Saitama, 351-01, Japan

Farm-reared Coturnix quail less than 3 weeks old showed depression, ruffled feathers, diarrhoea and high mortality. Histological examination revealed basophilic intranuclear inclusion bodies mainly in the digestive tract, and rarely in the liver, kidney, nasal epithelium, conjunctiva and columnar epithelial cells within the mucosa of the bursa of Fabricius. The inclusions were more numerous in the caeca than in the small intestine. Ultrastructurally, they contained many adenovirus-like particles approximately 60 nm in diameter. This is the first evidence of adenoviral inclusions in the glandular epithelium of the gizzard, conjunctiva, plical epithelium of bursa of Fabricius, and mucosal epithelium of small and large intestines in Coturnix quail. Numerous adenoviruses have been isolated from many avian species (McFerran & Adair, 1977). In quail, adenoviruses induce quail bronchitis (Olsen, 1950) and inclusion body hepatitis (Jack et al, 1987). Both diseases cause high mortality in bobwhite quail less than 3 weeks of age. Further study indicates that they are an identical entity with different manifestations (Jack & Reed, 1990a). Although inclusion body ventriculitis due to adenovirus infection has been reported in chickens and captive bobwhite quail (Goodwin, 1993) and an adenovirus, serotype TR-59, has been isolated from the caeca of wild bobwhite quail with hepatic inclusion bodies (King et al, 1981), there is no report concerning the pathological lesion in the digestive tract of Coturnix quail. Recently, we found some interesting lesions associated with adenovirus infection in the digestive tract, bursa of Fabricius (BF) and conjunctiva of Coturnix quail. Eighteen quail were randomly collected from three quail farms (Table 1). The main signs included ruffled feathers, depression and diarrhoea without apparent respiratory disorders. The mor*To whom correspondence should be addressed. Received 11 June 1997. Accepted 19 March 1998. 0307-9457/98/060641-03 1998 Houghton Trust Ltd

tality increased markedly from 3 days old. The disease lasted more than 3 weeks with mortality ranging from 24 to 30%. Portions of brain, eye, nose, trachea, lung, airsacs, digestive tract, thymus, spleen, BF, gonads, skin, muscle, bone and heart were sampled for histopathological examination. These were fixed in 10% buffered formalin, embedded in paraffin, sectioned and stained with haematoxylin and eosin (H&E). All the quail collected from three farms had similar histopathological alterations. The typical lesion was the presence of small or large basophilic intranuclear inclusion bodies (INI) in the affected cells. The small one was rarely found and showed both Cowdry A and B types. The large one was very common, belonged to B type and was more than 10 times the size of the normal nuclei of the original cells. The INI were found mainly in the digestive tract (Table 2) and rarely in the other organs examined. Their incidence was more frequent (18/18) in the caeca (Figure 1) than in the duodenum (6/18) and

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S. S. Tsai et al. Table 1. Outbreaks of adenoviral infection in Coturnix quail Farm No. placed No. died Mortality (%) Signs Duration of disease (days) Sampling time (days old) 10,000 3000 30 Stunting, emaciation, depression, diarrhoea >24 24&40 5000 1200 24 Ruffled feathers, depression, diarrhoea >24 12 5000 1500 30 Diarrhoea, depression >23 23

Table 2. Distribution of adenoviral intranuclear inclusion bodies seen histologically in the gastrointestinal tract of Conturnix: quail Incidence of intranuclear inclusions in Farm Duodenum 44% (4/9)a 0% (0/4) 40% (2/5) Ileum-jejunum 44% (4/9) 25% (1/4) 60% (3/5) Caeca 100% (9/9) 100% (4/4) 100% (5/5) Gizzard 22% (2/9) 0% (0/4) 0% (0/5)

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A B C
a

Number positive/number examined.

the remaining small intestine (8/18). With reference to the INI distribution, they were more numerous in the posterior portion of the caeca, than in the anterior part. Associated change was infiltration of mononuclear cells, mainly of lymphocytes and plasma cells in the lamina propria. Two birds (quail 3 and 6) from farm A had basophilic INI in the glandular epithelium of the gizzard. Quail 6 had large inclusions similar to those seen in the intestine, and quail 3 had small inclusions of Cowdry types A and B. Some epithelia containing INI were desquamated and embedded into the koilin layer which showed various degrees of erosion, accompanied by moderate infiltration of lymphocytes and plasma cells in the

lamina propria. Out of 18 birds, only two (quails 17 and 18) from farm C had INI in both the digestive tract and other organs. Large basophilic INI were detected in the renal tubules of the medullary region of quail 17. Multifocal necroses with INI formation were found in the liver of quail 18, which also contained similar inclusions in the nasal mucosal epithelium of the respiratory region, conjunctiva and in the plical epithelium of the BF. There were no remarkable tissue reactions in situ. Ultrastructurally, INI contained individual and crystalline arrays of 60 nm virus particles that expanded the nuclear membrane and marginated the chromatin (Figure 2). Virus morphology was suggestive of an adenovirus. Based on the histological examination of the

Figure 1. Many large basophilic intranuclear inclusion bodies completely filling the enlarged nuclei of crypt cells in the caecum. H & E stain, Bar = 30 pm.

Figure 2. Electron micrograph of an intranuclear inclusion body in the caecum containing many adenoviral particles arranged in paracrystalline arrays. Bar = 500 nm.

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gastrointestinal tract, concurrent infections were found, including cryptosporidiosis in 11/18 quail, tapeworm (3/18) and candidiasis (1/18). Cryptosporidiosis has been responsible for causing high mortality in young quail with signs of diarrhoea (Hoerr et al., 1986). Dual infections of adenovirus and Cryptosporidium spp. were very common in this study. Previous reports indicate that adenoviral INI are found only in the respiratory epithelium, hepatic cells and gizzard of bobwhite quail in field cases (Olsen, 1950; Jack et al, 1987; Goodwin, 1993). However, experimental studies in bobwhite quail reveal that large basophilic INI are detected in the trachea! and bronchial epithelium, hepatocytes and biliary epithelium, and BF epithelium (Jack & Reed, 1990b). The present studies on field cases indicated that adenoviral inclusions were found mainly in the digestive tract. All quail examined had adenoviral inclusions in the intestine and only one showed evidence of systemic infection. This was the first evidence that adenovirus had an ability to induce INI in the digestive tract of Coturnix quail, involving the gizzard, small intestine and caeca. Necrotizing pancreatitis and gizzard erosion have been reported in chickens associated with adenovirus infection in which large basophilic INI were seen in the necrotic pancreatic acinar cells and necrotic epithelial cell of the gizzard (Tanimura et al, 1993). In the present study, the affected quail had basophilic INI in the glandular epithelium of the gizzard without any associated changes in the pancreas. Although the inclusions consisted of large or small type, under the electron microscope, they contained similar viral particles to those of adenovirus. Adenovirus infection has been reported in Coturnix quail layers with signs of respiratory distress and soft-shelled and depigmented eggs (May, 1979). The virus was identified as fowl adenovirus serotype 1. Although adenoviral INI were also detected in adult quail in this study, the high mortality were found only in quail less than three weeks of age. The pathogenicity of adenovirus in Coturnix quail requires further study. References
Goodwin, M.A. (1993). Adenovirus inclusion body ventriculitis in chickens and captive bobwhite quail. Avian Diseases, 37, 568-571. Hoerr, F.J., Current, W.L. & Haynes, T.B. (1986). Fatal cryptosporidiosis in quail. Avian Diseases, 30, 421-425. Jack, S.W. & Reed, W.M. (1990a). Pathology of experimentally induced quail bronchitis. Avian Diseases, 34, 44-51. Jack, S.W. & Reed, W.M. (1990b). Further characterization of an avian adenovirus associated with inclusion body hepatitis in bobwhite quails. Avian Diseases, 34, 526-530. Jack, S.W., Reed, W.M. & Bryan, T.A. (1987). Inclusion body hepatitis in bobwhite quail. Avian Diseases, 31, 662-665. King, D.J., Pursglove, S.R. Jr & Davidson, W.R. (1981). Adenovirus

isolation and serology from wild bobwhite quails. Avian Diseases, 25, 678-682. May, C.L. (1979). Adult Coturnix quail bronchitis. Avian Diseases, 24, 520-526. McFerran, J.B. & Adair, B.M. (1977). Avian adenovirusesa review. Avian Pathology, 6, 189-217. Olsen, N.D. (1950). A respiratory disease (bronchitis) of quail caused by a virus. Proceeding of 54th Annual Meeting, US Livestock Sanitary Association, pp. 1971-1974. Tanimura, N., Nakamura, K., Imai, K., Maeda, M., Gobo, T., Nitta, S., Ishihara, T. & Amano, H. (1993). Necrotizing pancreatitis and gizzard erosion associated with adenovirus infection in chickens. Avian Diseases, 37, 606-611.

RSUM Lsions gastro-intestinales associes un cas spontan d'adnovirose chez la caille des bls (Coturnix coturnix) Des cailles d'levage, ges de moins de trois semaines, ont montr de l'abattement, des plumes bouriffes, de la diarrhe et une forte mortalit. Un examen histologique a rvl la prsence de corps d'inclusion intranuclaires basophiles, principalement au niveau du tractus digestif et rarement au niveau du foie, des reins, de l'pithlium nasal, de la conjonctive et des cellules pithliales de la muqueuse de la bourse de Fabricius. Les inclusions ont t plus nombreuses dans les caeca que dans l'intestin grle. Au microscope lectronique, il a t observ de nombreuses particules virales 'adnolike' d'environ 60 nm de diamtre. C'est la premire mise en vidence d'inclusions dues un adnovirus dans l'pithlium glandulaire du gsier, au niveau de la conjonctive, de l'pithlium pliss de la bourse de Fabricius, et de l'pithlium de la muqueuse de l'intestin chez la caille des bls.

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ZUSAMMENFASSUNG Natrlich vorkommende Adenovirus-assoziierte gastrointestinale Lsionen bei Wachteln (Coturnix coturnix) In einer Farm aufgezogene, weniger als 3 Wochen alte Wachteln zeigten Schwche, gestrubtes Gefieder, Durchfall und eine hohe Mortalitt. Histologische Untersuchungen ergaben das Vorliegen basophiler intranuklerer Einschlukrperchen hauptschlich im Verdauungstrakt und selten in der Leber, der Niere, dem Nasenepithel, der Konjunktiva und in Zylinderepithelzellen in der Mukosa der Bursa Fabricii. Die Einschlsse waren in den Blinddrmen zahlreicher als im Dnndarm. Ultrastrukturell enthielten sie viele adenovirusartige Partikeln mit einem Durchmesser von etwa 60 nm. Dies ist der erste Nachweis von Adenovirus-Einschlssen im Drsenepithel des Muskelmagens, der Konjunktiva, des Faltenepithels der Bursa Fabricii und im Schleimhautepithel von Dnn- und Dickdrmen bei Wachteln.

RESUMEN Lesiones gastrointestinales asociadas a una infeccion por adenovirus en codornices (Coturnix coturnix) Codornices de granja de menos de 3 semanas de edad presentaban abatinmiento, erizamiento de plumas, diarrea y una mortalidad elevada. El estudio histolgico evidenci la presencia de cuerpos de inclusin intranucleares basfilos, principalmente localizados en el tracto digestivo y ocasionalmente en: hgado, rin, epitelio nasal, conjuntiva y celulas epiteliales cilindricas de la mucosa de la bolsa de Fabricio. Las inclusiones eran ms numerosas en el ciego que en intestino delgado. Ultraestructuralmente presentaban mltiples partculas vricas compatibles con adenovirus, de un diametro aproximado de 60 nm. Se trata de la primera descripcin de inclusiones por adenovirus en epitelio glandular de molleja, conjuntiva, epitelio de bolsa de Fabricio y epitelio de la mucosa del intestino delgado y grueso en codornices.