Avian Pathology ( 2002 ) 31, 133– 140
Histopathological and ultrastructural changes associated with herpesvirus infection in waterfowl Francisco J. Salguero, Pedro J. S´anchez-Cord´on, Alejandro N´unez ˜ & Jos´e C. G´omez-Villamandos* Departamento de Anatom´õ a Patol´ogica Comparada, Edificio de Sanidad Animal, Campus Universitario de Rabanales, 14014, C´ordoba, Spain
Duck virus enteritis is an acute contagious viral disease affecting birds of the order Anseriformes ( ducks, geese and swans). The disease agent is a member of the Herpesviridae family ( Anatidae herpes virus 1). A group of Anseriformes waterfowl from a Nature Reserve and Centre for the Recovery of Endangered Species in Spain suffered an outbreak of the disease, affecting adults, young and newborns. Other non-Anseriformes waterfowl such as coots, from the family Rallidae, order Gruiformes, were also affected. Histopathological and ultrastructural findings confirmed the viral infection. The present study provides evidence that birds different from the order Anseriformes can be affected, suggesting that the virus has the ability to infest other non-Anseriformes waterfows.
Introduction Duck virus enteritis ( DVE) is an acute contagious viral disease affecting birds of the order Anseriformes ( ducks, geese and swans) ( Davison et al., 1993 ). In ducks, the disease is caused by the Anatidae herpesvirus 1 ( Kaleta, 1990; Foulon, 1992 ), a member of the Herpesviridae family included in the subfamily a-Herpesvirinae ( Breese & Dardiri, 1968). The disease appears in waterfowl of all ages. Several studies indicate that survivors may be carriers of the virus for up to 4 years ( Burgess et al., 1979 ). Cases of the disease were recorded in domestic ducks in Holland by Baduet ( 1923 ), as early as 1923. Although it was initially thought that the disease was caused by a strain of fowl plague virus found in ducks ( Baudet, 1923; DeZeeuw, 1930), later it was discovered to be a new viral disease and was given the name duck plague ( Bos, 1942; Jansen & Kunst, 1949). The disease was subsequentl y called DVE due to the severe enteritis that accompanies it ( Leibovitz, 1968) . The disease has been reported on commercial duck farms and in a wide range of waterfowl on farms, and in the wild in
Great Britain, Europe, India, China and North America ( Devos et al., 1964; Jansen, 1968; Hanson & Willis, 1976; Montali et al., 1976; Gough & Alexander, 1990). The first indication of an outbreak of DVE affecting domestic ducks is usually a sudden high mortality rate in the group. Often the birds die without any outward clinical signs and corpses are found floating on the surface of the water ( Montali et al., 1976 ). A reduction in clutch size and prolapses of the male phallus may occur. The clinical course of the disease is accompanied by other signs such as photophobia with partially closed eyelids, loss of appetite, extreme thirst, ataxia, drooping plumage, nasal discharge, soiled vents and watery diarrhoea. When the animals are moved they suffer from tremors of head, neck and body ( Davison et al., 1993; Sandhu & Leibovitz, 1997 ). The principle lesions are characterized by vascular damage, haemorrhages in tissues, eruptions in the digestive mucosa ( Proctor, 1975), lesions in the lymphoid organs and degenerative changes in the parenchymatous organs ( Montali et al., 1976; Davison et al., 1993; Sandhu & Leibovitz, 1997 ).
* To whom correspondence should be addressed Tel +34-957-218162 Fax +34-957-218847 E mail:
[email protected] s Received: 5 June 2001. Accepted 14 October 2001 ISSN 0307-9457 ( print)/ISSN 1465-3338 ( online)/02/020133-0 8 DOI: 10.1080/03079450120118612
© 2002 Houghton Trust Ltd
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F.J. Salguero et al. Table 1. Gross lesion in waterfowl affected by DVE
Coots
Adult female mallard
Chicks from the clutch
Adult male mallards
Young male mallards
Lung Hyperemia Haemorrhages
NLb NL
NL NL
NL NL
2/6 2/6
1/2 1/2
Liver Haemorrhages Degeneration Necrosis
2/2a 2/2 2/2
1/1 1/1 1/1
2/2 2/2 2/2
6/6 6/6 6/6
2/2 2/2 2/2
Kidney Haemorrhages
2/2
1/1
2/2
6/6
2/2
Pancreas Haemorrhages
2/2
1/1
2/2
6/6
2/2
Esophagus Diphtheritic membranes
NL
NL
NL
2/6
1/2
Intestine Haemorrhages Haemorrhagic enteritis Diphtheritic membranes
2/2 1/2 1/2
1/1 1/1 NL
2/2 NL NL
6/6 2/6 2/6
2/2 2/2 NL
Cloaca Diphtheritic membranes
NL
NL
NL
2/6
NL
Bursa Diphtheritic membranes
NL
NL
NL
1/6
1/2
Organs
a
Data presented as affected animals/total animals; b NL, no lesions.
Materials and Methods The birds studied were sent from the Nature Reserve and Center for the Recovery of Endangered Species in the province of Seville ( Spain). During the month of May, there was a sudden increase in the disease rate ( 80%) and mortality ( 60%) in a group of 115 waterfowl. All animals had been previously vaccinated against Newcastle’s disease. The species affected were mallards ( Anas platyrhyncho s ) of different ages and greylag geese ( Anser anser ) belonging to the family Anatide, order Anseriformes. Common coots ( Fulica atra ) and crested coots ( Fulica cristata ) belonging to the family Rallidae order Gruiformes, were also affected. Thirteen of the affected birds were sent for necropsy to the Department of Comparative Pathology of the School of Veterinary Medicine at the University of Cordoba. These included an adult female mallard, two 2-day-old chicks from its clutch, six adult male mallards, two young male mallards and two coots. During necropsy and following an examination of the lesions, samples of the spleen, bursa of Fabricius, kidney, ureter, esophagus , ventriculus, proventriculus, small intestine, large intestine, caecum, cloaca, liver, lung, trachea and pancreas were taken for other studies. Tissues were fixed in 10% formalin solution. Samples for microscopic examination were routinely processed, embedded, sectioned and stained with haematoxylin and eosin. For ultrastructural examination, part of the samples was processed routinely, post-fixed in osmium tetroxide and embedded in Epon 812. Then, 1 mm-thick sections were stained with toluidine blue, and 50 nm slices were stained using lead citrate and uranyl acetate for subsequent examination with a Philips CM-10 transmission electron microscope ( Meg´õ as & Renau, 1998). Samples for bacteriological study were taken from the same organs as used for histological and ultrastructural study.
Results Clinical findings All affected animals suffered non-specific signs, consisting of drooping plumage, closed eyelids, retracted neck, lameness, loss of appetite and watery diarrhoea. The first affected bird was a female mallard ( A. platyrhyncho s ) that died 48 h after the appearance of the first clinical signs. Within 24 h after death of the first bird, two chicks from its clutch and the young male mallards were the next birds showing signs of disease. They died 24 h after the onset of the signs. At the same time, the outbreak affected adult male mallards and one greylag geese ( A. anser; necropsy was not performed), as well as one common coot ( F. atra ) and one crested coot ( F. cristata ) that showed similar signs and died 24 h after the beginning of the clinical signs. Gross findings Necropsy revealed similar lesions in all the birds ( Table 1), although they were less severe in the older animals. Scattered whitish spots ( inconsistent and not prominent), indicative of multifocal
Herpesvirus infection in waterfowl 135 Table 2. Histopathologycal findings in waterfowl affected by DVE
Coots
Adult female mallard
Chicks from the clutch
Adult male mallards
Young male mallards
Lung Hyperemia Haemorrhages
NLb NL
NL NL
NL NL
2/6 2/6
1/2 1/2
Liver Haemorrhages Fat degeneration hepatocytes Necrotic hepatitis ICIBs
2/2a 2/2 2/2 2/2
1/1 1/1 1/1 1/1
2/2 2/2 2/2 2/2
6/6 6/6 6/6 6/6
2/2 2/2 2/2 2/2
Ureter ICIBs
NL
NL
NL
1/6
NL
Kidney Haemorrhages Nephrosis IIBs
2/2 NL NL
1/1 NL NL
2/2 NL NL
6/6 2/6 1/6
2/2 NL NL
Pancreas Necrotic pancreatitis IIBs
2/2 2/2
1/1 1/1
NL NL
2/6 2/6
2/2 2/2
Esophagus Diphteritic membranes IIBs ICIBs Cellular infiltrate
NL NL NL NL
NL NL NL NL
NL NL NL NL
2/6 2/6 1/6 2/6
1/2 1/2 NL 1/2
Intestine Haemorhagic enteritis Diphteritic membranes IIBs Cellular infiltrate
1/2 1/2 1/2 1/2
1/1 NL 1/1 1/1
NL NL NL NL
2/6 2/6 2/6 2/6
2/2 NL 2/2 2/2
Cloaca Haemorrhages Diphteritic membranes IIBs Cellular infiltrate
NL NL NL NL
NL NL NL NL
NL NL NL NL
4/6 2/6 2/69 2/6
2/2 NL NL NL
Spleen Lymphoid depletion Necrosis IIBs
2/2 2/2 2/2
1/1 1/1 1/1
NL NL NL
4/6 4/6 4/6
2/2 2/2 2/2
Bursa Lymphoid depletion Diphteritic membranes IIBs
2/2 NL NL
1/1 NL NL
NL NL NL
4/6 1/6 1/6
2/2 1/2 1/2
Organs
a
Data presented as affected animals/total animals; b NL, no lesions.
necrotic hepatitis, were present in all the birds necropsied. While some animals had only a moderate number of necrotic foci, accompanied by a slight decrease in color and consistence of the liver, indicative of liver degeneration, other animals presented numerous necrotic foci accompanied by severe hepatic degeneration, characterized by a friable consistence and yellowish color of liver.
Other lesions present in all birds were petechiae in the liver, kidney, pancreas and intestinal serosa. Haemorrhagic enteritis, characterized by a dark-red lining of blood mixed with mucus and remains of intestinal necrotic epithelium detached in the lumen, was observed in some animals ( Table 1) . Additionally, in some cases, the mucosa of the esophagus, small intestine, cloaca and bursa of Fabricius showed a diphtheritic inflammation
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F.J. Salguero et al.
Figure 1. 1a: Liver. Acidophilic ( arrowhead) and basophilic ( arrow) IIBs in hepatocytes of a young male mallard. Haematoxylin and eosin ( HE); bar, 50 mm. 1b: Esophagus. Acidopholic IIBs in glandular epithelial cells ( arrow) and acidophilic ICIBs in epithelium ( arrowhead ) of an adult male mallard. HE; bar, 50 mm. 1c: Intestine. Necrotic enteritis ( diphtheritic membrane) in a coot. HE; bar, 200 mm. 1d: Pancreas. Multifocal necrosis in a coot. HE; bar, 200 mm. 1e: Ureter. Balloon-shaped epithelial cells and moderate cellular infiltrate in an adult male mallard. HE; bar, 100 mm. 1f: Bursa of Fabricius. Severe necrosis on lymphoid follicles in an adult female mallard. Some cells show IIBs ( arrow) . HE; bar, 75 mm.
Herpesvirus infection in waterfowl 137 Table 3. Ultrastructural findings: presence of herpesviral particles in waterfowl affected by DVE
Organs Liver Ureter Kidney Pancreas Esophagus Intestine Cloaca Spleen Bursa a
Coots
Adult female mallard
Chick from the clutch
Adult male mallards
Young male mallards
2/2a –b – 2/2 – 1/2 – 2/2 –
1/1 – – 1/1 – 1/1 – 1/1 –
2/2 – – – – – – – –
6/6 1/6 1/6 2/6 2/6 2/6 2/6 4/6 1/6
2/2 – – 2/2 1/2 2/2 – 2/2 1/2
Data presented as affected animals/total animals; b –, absence of herpesviral particles.
accompanied by white to yellow membranes, revealing congested and ulcerated areas when removed ( Table 1) . Microscopic findings Microscopic findings are presented in Table 2. Histological examination revealed necrosis in the liver of all birds. The severity of the lesions varied among the animals. Necrotic foci of hepatocytes were surrounded by a non-severe inflammatory reaction, constituted mainly by mononuclear cells. Two types of intranuclear inclusion bodies ( IIBs) were seen in the hepatocytes ( Figure 1A), in the infiltrate cells and in the epithelial cells of the bile ducts: ( a) small acidophilic IIBs surrounded by a clear halo; and ( b) slightly basophilic IIBs occupying the entire nucleus. Different degrees of hyperemia, haemorrhages and fatty degeneration of hepatocytes ( hepatic steatosis) were also observed. In the esophagus ( Figure 1B ), scattered necrotic cells in the epithelium and in glandular structures were observed, together with the presence of diphtheritic pseudomembranes on the mucus surface, composed of abundant necrotic debris, heterophils and fibrin. These lesions were associated with the presence of IIBs in glandular epithelial cells, similar to those described in the hepatocytes. In addition, in the epithelial cells, the presence of acidophilic intracytoplasmic inclusion bodies ( ICIBs) were also observed ( Figure 1B). A cellular infiltrate composed of mononuclear cells, was found in the lamina propria. The large intestine and cloaca of some birds showed severe haemorrhages and diphtheritic pseudomembranes ( Figure 1C), similar to those described in the esophagus, and abundant IIBs in epithelial cells that in some cases showed a balloonshaped profile ( Table 2) . A mononuclear cell infiltrate was also found in the lamina propria of these tissues.
Some animals had multifocal necrosis of the pancreas ( Figure 1D). This was accompanied by a mononuclear-type infiltrate associated with the presence of IIBs in the glandular epithelium. Hyperemia, haemorrhages and nephrosis in the kidney were observed in some birds, as well as the presence of IIBs in the epithelial cells of the tubules and interstitial cells and acidophilic ICIBs in the epithelial cells of the ureter ( Figure 1E). The lesions of lymphoid organs were varied. Reactive follicles, lymphoid depletion, and necrosis and IIBs in the mononuclear cells of the spleen cords were detected in the spleen of some animals. Severe lymphoid depletion was observed in the bursa of Fabricius ( Figure 1F), associated with necrosis, that in some cases led to epithelial lesions and diphtheritic membranes. Numerous IIBs in epithelial cells, lymphoid cells and interstitial cells of the bursa were also identified. Hyperaemia and haemorrhages were occasionally observed in the lungs. Ultrastructural findings Ultrastructural study revealed herpesvirus particles and viral replication sites in all cells population s containing IIBs ( Table 3). The viral particles measured 105 to 115 nm in diameter, were hexagonal in shape and showed variable electron-densit y in the cores ( Figure 2). The virions were nonenveloped and scattered randomly in the nucleus or aligned close to the nuclear envelope. Clusters of viral particles were found in the cytoplasm as well as solitary enveloped virions measuring 200 to 250 nm in diameter ( Figure 3). These virions were found in the cytoplasmic vesicles in some cells and were observed budding through the nuclear envelope. The ICIBs were formed by clusters of virions enveloped by membranes similar to those already described.
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F.J. Salguero et al.
Figure 2. Epithelial pancreatic cell of a coot. Intranuclear viral replication site with non-electron-dense viral particles ( arrow) and particles with electron-dense nucleoid ( arrow). The cytoplasm of this cells contains numerous viral particles surrounded by a membrane. Transmission electron microscope ( arrowhead) ; bar, 250 nm.
Figure 3. Coot. Details of viral particles in the cytoplasm of an epithelial pancreatic cell. Transmission electron microscope; bar, 150 nm.
Herpesvirus infection in waterfowl 139
Bacteriological study Bacterial cultures from different areas of intestine and cloaca were positive for Salmonella spp. and Escherichia coli. The rest of the studied organs were negative.
Discussion The birds examined in our study presented multifocal necrotic hepatitis and enteritis associated with the presence of intranuclear inclusion bodies. In addition, ultrastructural findings of viral particles and viral replication sites characteristic of herpesvirus were observed ( Barr et al., 1992; Sandhu & Leibovitz, 1997; Go´ mez-Villamandos et al., 1998 ). These lesions allowed us to diagnose this outbreak as an anatidae herpesvirus infection ( DVE) affecting adult, young and newborn Anseriformes waterfowl and other non-Anseriformes waterfowl such as coots. Clinically, infection by DVE may be confused with diphteroid forms of poxvirus infection, due to the presence of diphteritic yellowish lesions on the mucus membrane of the esophagus. However, in the poxvirus infection, similar lesions appear also in the mouth and trachea and produce severe respiratory signs ( Tripathy & Reed, 1997), not observed in our case. Additionally, the cytoplasmic inclusion bodies ( Bollinger bodies) and ultrastructural particles, characteristic of poxvirus infection, were not found. Chronic infection of viral diseases, complicated by secondary bacterial invaders such as Salmonella spp., could induce a diphteroid form of enteritis ( Vindevogel & Duchatel, 1997 ). In our case, the isolation of Salmonella spp. and E. coli was considered not eminent due to the presence of inclusion bodies in the epithelial cells and the peracute course of the disease. Natural susceptibility to DVE has been limited to members of the family Anatidae ( ducks, geese and swans) of the order Anseriformes ( Sandhu & Leibovitz, 1997), although it has been shown that the virus can be adapted to grow in embryonating chicken eggs ( Jansen, 1968; Sandhu & Leibovitz, 1997). Susceptibilit y of the American coot ( F. americana; family Rallidae) to herpesvirus characteristic of birds from other orders, such as the falcon herpesvirus ( Mare´ & Graham, 1976; Mozos et al., 1994 ), has also been described. However, according to the literature consulted, it would be the first time that this disease has been described in non-Anseriforme birds, specifically common coots ( F. atra ) and crested coots ( F. cristata ). Outbreaks on ducks farms are usually caused through transmission of the causal agent by wildfowl flying over the farms ( Montali et al., 1976 ). In our case, no outbreaks of the disease were reported near the reserve, in spite of the large
population of waterfowl in the area. The outbreak may have been caused by the combination of two factors: first, the presence of a non-identifie d carrier; and, second, the stress suffered by the birds as the result of vaccination and the reproductive season. The high rate of mortality affecting young and adult animals would suggest that this population was not immunized against the virus. This would explain the chance nature of the disease and its rapid progress in all the birds, especially the youngest. Other authors, however, state that adult birds rather than young tend to experience a higher mortality rate ( Sandhu & Leibovitz, 1997 ). DVE replicates in epithelial cells ( Tantaswasdi et al., 1988; Barr et al., 1992 ) and, given its alpha herpesvirus nature, produces ICIBs composed of large clusters of virions ( Kaleta, 1990; Barr et al., 1992 ). These features have also been observed in our study. Furthermore, IIBs were observed in the epithelial cells of the kidney, and ICIBs in the epithelial cells of the ureter. The fact that replication in the kidney was found in one adult bird in which the course of the disease was less marked suggests that, when the disease progresses more rapidly, the virus has time to spread to tissues where it is not frequently found. The present study provides evidence that the disease affects birds belonging to orders that are taxonomically different from the order Anseriformes. The lesions presented in coots ( order Gruiformes ) were similar to DVE lesions, suggesting that the virus can cross between different orders and families and adapted to new hosts, developing the characteristic form of the disease.
Acknowledgments The authors thank the Nature Reserve and Center for the Recovery of the Endangered Species ‘Ca˜nada de los Pa´ jaros’, Seville, Spain. They appreciate the technical assistance of the Central Service for Support for Research, University of Co´ rdoba, Spain. This paper has been supported by a grant from PAI ( Agr-137 ).
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Davison, S., Converse, K.A., Hamir, A.N. & Eckroade, R.J. ( 1993 ). Duck viral enteritis in Muscovy ducks in Pennsylvania. Avian Diseases, 37, 1142–1146. Devos, A., Viaene, N. & Staelens, H. ( 1964 ). Duck plague in Belgium. Vlaams Diergeneeskd Tijdschr, 33, 260– 266. DeZeeuw, F.A. ( 1930 ). Nieuwe gevallen van eendenpest en de specificiteit van het virus. Tijdschr Diergeneeskd, 57, 1095– 1098. Foulon, T. ( 1992 ). Herpesviridae: classification et structure en 1991. Comparative Immunological and Microbiological Infectious Diseases, 15, 13– 29. G´omez-Villamandos, J.C., Herv´as, J., Salguero, F.J., Quevedo, M.A., Aguilar, J.M. & Mozos, E. ( 1998 ). Haemorragic enteritis associated with herpesvirus in storks. Avian Pathology, 27, 229– 236. Gough, R.E. & Alexander, D.J. ( 1990 ). Duck virus enteritis in Great Britain, 1980 to 1989. Veterinary Record, 126, 595– 597. Hanson, J.A. & Willis, N.G. ( 1976 ). An outbreak of duck virus enteritis ( duck plague) in Alberta. Journal of Wildlife Diseases, 12, 258– 262. Jansen, J. ( 1968 ). Duck plague. Journal of American Veterinary Medicine Association, 152, 1009–1016. Jansen, J. & Kunst, H. ( 1949 ). Is duck plague related to Newcastle disease or to fowl plague? Proceedings of the XIVth International Veterinary Congress, 2, 363– 365. Kaleta, E.F. ( 1990 ). Herpesviruses of birds. A review. Avian Pathology, 19, 193– 211. Leibovitz, L. ( 1968 ). Progress report: duck plague suveillance of American Anseriformes. Bulletin Wildlife Diseases Association, 4, 87– 90. Mar´e, M.C. & Graham, D.L. ( 1976 ). Pathogenicity and host range of the falcon herpesvirus. In L.A. Page ( Ed.), Wildlife Diseases ( pp. 471– 482 ). New York: Plenum Publishing Corporation. Meg´õ as, L. & Renau, J. ( 1998 ). T´ecnicas generales. In L. Meg´õ as & J. Renau ( Eds.), Manual de T´ecnicas de Microscop´õ a Electr´onica ( in Spanish ) ( pp. 1–19). Granada: Editorial Universidad de Granada, Campus Universitario de Cartuja. Montali, R.J., Bush, M. & Greenwell, G.A. ( 1976 ). An epornitic of duck viral enteritis in a zoological park. Journal of American Veterinary Medicine Association, 169, 954– 958. Mozos, E., Herv´as, J., Moyano, T., D´õ az, J. & G´omez-Villamandos, J.C. ( 1994 ). Inclusion body disease in a peregrine falcon ( Falcon peregrinus ): histological and ultrastrultural study. Avian Diseases, 23, 175–181. Proctor, S.J. ( 1975 ). Pathogenesis of digestive tract lesions in duck plague. Veterinary Pathology, 12, 349– 361. Sandhu, T.S. & Leibovitz, L. ( 1997 ). Duck virus enteritis ( Duck plague ). In B.W. Calnek ( Ed. ), Diseases of Poultry 10th edn ( pp. 675– 683 ). Ames, IA: Iowa State University Press. Tantaswasdi, U., Wattanavijarn, W., Methiyapun, S., Kumagai, T. & Tajima, M. ( 1988 ). Light, immunofluorescent and electron microscopy of duck virus enteritis ( duck plague). Japan Journal of Veterinary Science, 50, 1150–1160. Tripathy, D.N & Reed, W.M. ( 1997 ). Pox. In B.W. Calnek ( Ed.), Diseases of Poultry 10th edn ( pp. 643– 659). Ames, IA: Iowa State University Press. Vindevogel, H. & Duchatel, J.P. ( 1997 ). Miscellaneous herpesvirus infections. In B.W. Calnek ( Ed.), Diseases of Poultry 10th edn ( pp. 757–761 ). Ames, IA: Iowa State University Press.
´ RESUM E´ L´esions histopathologiques et ultrastructurelles li´ees a` une infection a` herp`esvirus chez les palmip`edes L’ent´erite virale du canard ( DVE ) est une maladie virale tr`es contagieuse affectant les oiseaux de l’ordre des Ans´eriformes ( canards, oies et cygnes). L’agent de la maladie est un membre de la famille des Herpesviridae ( herpesvirus 1 des Anatidae). Un groupe de palmip`edes Ans´eriformes de la R´eserve Naturelle et du Centre de Soins des Esp`eces en voie d’extinction en Espagne ont pr´esent´e la maladie. Les adultes, les jeunes et les nouveau- n´es ont e´ t´e affect´es. D’autres palmip`edes n’appartenant pas aux Ans´eriformes tels les foulques de la famille des Rallidae, ordre des Gruiformes ont e´t´e e´ galement affect´es. Les observations histopathologiques et ultrastructurales ont confirm´e l’infection virale. La pr´esente e´ tude prouve que des oiseaux appartenant a` des ordres diff´erents des Ans´eriformes peuvent eˆtre infect´es, sugg´erant que le virus ait la possibilit´e d’infecter des palmip`edes nonAns´eriformes. ZUSAMMENFASSUNG Histopathologische und ultrastrukturelle Ver¨anderungen im Zusammenhang mit einer Herpesvirusinfektion bei Wassergef l¨ugel Die Entenpest ist eine akute kontagi¨ose Viruskrankheit, die V¨ogel der Ordnung Anseriformes ( Enten, G¨anse und Schw¨ane ) bef¨allt. Der Krankheitserreger ist ein Mitglied der Familie Herpesviridae ( Anatidae Herpesvirus 1). Eine Gruppe anseriformer Wasservo¨ gel aus einem Naturschutzgebiet und Zentrum f¨ur die Rettung gef¨ahrdeter Arten in Spanien erlitt einen Ausbruch der Krankheit, die Adulte, Junge und Neugeborene befiel. Andere, nicht anseriforme Wasservo¨ gel wie Bl¨assh¨uhner aus der Familie Rallidae, Ordnung Gruiformes, waren ebenfalls erkrankt. Histopathologische und ultrastrukturelle Befunde best¨atigten die Virusinfektion. Die vorliegende Studie liefert Anhaltspunkte daf¨ur, dass andere V¨ogel als solche von der Ordnung Anseriformes befallen sein ko¨ nnen, was darauf schließen l¨asst, dass das Virus die F¨ahigkeit hat, andere nicht anseriforme Wasservo¨ gel zu infizieren. RESUMEN Cambios histopatol´ogicos y ultraestructurales asociados a la infecci´on con herpesvirus en aves acu´aticas La enteritis del pato ( DVE ) es una enfermedad viral contagiosa y aguda que afecta aves del orden Anseriformes ( patos, gansos y cisnes). El agente que produce la enfermedad es un miembro de la familia Herpesviridae ( Anatidae herpes virus 1). Un grupo de aves acu´aticas anseriformes de una Reserva Natural y de un Centro para la Recuperaci o´ n de Especies en peligro de extinci´on en Espan˜ a, sufrieron una epidemia de la enfermedad que afect´o a adultos, j´ovenes y reci´en nacidos. Otras aves acu´aticas no anseriformes como las fochas, de la familia Rallidae, orden Gruiformes, tambi´en se vieron afectadas. Los hallazgos histopatol´ogicos y ultraestructurales confirmaron la infecci o´ n viral. El presente estudio proporciona datos sobre la afectaci o´ n de aves de un orden diferente al de las Anseriformes, lo cual sugiere que el virus puede infectar aves acu´aticas no anseriformes.
