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Canine viral enteritis. Recent developments
Abstract
Two apparently novel viral gastroenteritides of dogs were recognized in 1978: one caused by a parvo-like virus (CPV) and one by a corona-like virus (CCV). A rotavirus has also been tentatively associated with neonatal pup enteritis. Canine viral enteritis is characterized by a sudden onset of vomiting and diarrhea, rapid spread and high morbidity. Treatment is only supportive but must be initiated promptly. Infected animals should be isolated immediately; the extremely contagious nature of these diseases makes them difficult to contain. Feces from infected dogs appear to be the primary means of transmission. Sodium hypochlorite solutions (eg, Clorox) are recommended for disinfection. The development of effective vaccines is an immediate and pressing problem.
... El desarrollo de la enfermedad con un curso más prolongado muestra una intensificación de las lesiones a nivel intestinal donde el virus permanece durante un tiempo mayor (8,28,29), interviniendo como factor previo importante la variabilidad de la flora bacteriana (18) , y el posterior efecto citopático a nivel de las vellosidades, lo que permitiría el desarrollo patogénico secundario de gérmenes y toxinas (3,14), como efecto de superposición al proceso vírico, relacionados morfológicamente con la manifestación de fenómenos de trombosis vacular y un infiltrado mayor en neutrófilos. Igualmente, los fenómenos de malabsorción, desarrollados desde las lesiones entéricas primarias (18), son factores también a tener en cuenta en el curso de la enfermedad. ...
... La llegada del virus a la mucosa intestinal, bien a través de linfoblastos recirculantes (8,28,29) y/o difusión a través de las placas de Peyer adyacentes (7,8), con el desarrollo de lesiones a estos niveles, guarda relación con la aparición de anticuerpos neutralizantes en sangre (21) y con el tipo de infiltrado que aparece tanto en los animales inoculados experimentalmente (21) como en la enfermedad natural (9,27). Así, la constante presencia de eosinófilos en este proceso podría explicarse como el resultado de una acción antiparasitaria (15), si bien el hecho de que animales no parasitados y en inoculaciones experimentales (21) estén presentes, hace pensar que los eosinófilos puedan cumplir otra función igualmente de tipo defensivo (32, 36). ...
... Canine parvovirus (CPV) affects domestic and wild animals (Pollock and Carmichael, 1979). Among wild species, concern about CPV has centered on the wolf (Canis lupus), an animal on the US Endangered Species List (Mech and Goyal, 2011). ...
... Among wild species, concern about CPV has centered on the wolf (Canis lupus), an animal on the US Endangered Species List (Mech and Goyal, 2011). An important unanswered question about CPV in wolves involves contagion via feces (Pollock and Carmichael, 1979). Wolves regularly smell other wolves' feces and practice coprophagy. ...
Using real-time PCR, we tested 15 wolf (Canis lupus) feces from the Superior National Forest (SNF), Minnesota, USA, and 191 from Yellowstone National Park (YNP), USA, collected during summer and 13 during winter for canine parvovirus (CPV)-2 DNA. We also tested 20 dog feces for CPV-2 DNA. The PCR assay was 100% sensitive and specific with a minimum detection threshold of 10(4) 50% tissue culture infective dose. Virus was detected in two winter specimens but none of the summer specimens. We suggest applying the technique more broadly especially with winter feces.
... Nowadays, it is extremely unusual to see a case in most developed, temperate countries. Similarly, when canine parvoviral enteritis first appeared in the late 1970s it caused severe disease and death in both puppies and adult dogs (Pollock and Carmichael 1979). Nowadays, parvoviral enteritis is seen much less frequently, and then almost invariably in young dogs that have been incompletely vaccinated. ...
... CCoV is known to have spread worldwide, with the virus detected or isolated in Europe, U.S.A., Asia and Australia (Appel, 1987;Bandai et al., 1999;Carmichael and Binn, 1981;Naylor et al., 2001;Pollock and Carmichael, 1979). In Greece, CCoV detection was reported for the first time in 2010, and it was associated with a severe outbreak of enteritis in young dogs in a municipal kennel (Ntafis et al., 2010). ...
... Rotavirus has been occasionally observed in stools of dogs with diarrhoea (Pollock and Carmichael, 1979 ;Eugster and Sidwa, 1979 ;England and Poston, 1980;Eugster and Sneed, 1980;McNulty, Curran, McFerran and Collins, 1980;Dagenais, Calberg-Bacq, Schwers and Pastoret, 1980a;Osterhaus, Drost, Wirahadiredja and van den Ingh, 1980;Fulton, Johnson, Pearson and Woode, 1981). ...
Ten young dogs were experimentally infected twice with different isolates of bovine rotavirus and 2 uninfected dogs were kept in contact with them. None of the animals developed diarrhoea, but all of them excreted rotavirus in their faeces over a period of up to 10 days after each inoculation, as shown by counterimmunoelectro-osmophoresis and virus isolation. Dogs may thus play a role in the epizootiology of rotavirus diarrhoea in calves. Seroconversion occurred in 6 of the 10 infected dogs but in neither of the 2 contact controls.
Fecal samples from both diarrheic (n=25) and non-diarrheic (n=8) dogs of both sexes, with varying ages and breeds, were examined by electronic microscopy (EM) in order to determine candidate viral pathogens which would be associated with gastroenteritis, particularly the canine gastroenteritis complex, in an attempt to correlate viral etiology and clinical and vaccination history. In addition to EM, 71 stool samples were tested by ELISA to detect either rotavirus or adenovirus antigens. Viral particles could be visualized by EM in 25 (75.8%) of the 33 samples. Type-I virus-like structures and parvoviruses were frequently detected, accounting for 44% and 36% of the virus-positive preparations. Bloody diarrhea was noted in 90.9% of dogs that were excreting viral particles.
Immunohistochemical and histological investigations on antigen distribution in Parvovirus-infected dogs and cats
In organs known as replication sites of parvovirus and additionally in stratified squamous epithelia from different regions of 35 dogs with letal parvovirus enteritis and 19 cats with letal panleukopenia the distribution of antigen and the prevalence of histologic lesions were studied by immunofluorescence and histologic techniques. The findings showed no striking differences between dogs and cats.
Antigen was found in the epithelia of the dorsal side of the tongue (96.3 %), pharynx (81.0 %), esophagus (50.0 %), ventral side of the tongue (20.4 %) and planum nasale (5.6 %). The epithelia of the skin and the mucous membranes of the male and female genital organs never contained antigen. Moreover antigen was detected in the mucosa of the small intestine (85.2 %), bone marrow (81.6 %), spleen (79.6%), thymus (66.7%), mesenteric lymph nodes (60.4%), tonsilla palatina (58.5%), smooth muscle cells of the tunica muscularis of the small intestine (9.3 %) and myocardium (1.9%).
The histologic lesions found in intestinal mucosa, lymphatic tissues, bone marrow and myocardium are in accordance with literature. The tunica musculatis of the small intestine and the epithelium of tongue, pharynx and esophagus contained intranuclear inclusion bodies, the epithelium of tongue and pharynx showed necroses additionally.
Tongue- and esophagus-erosions as well as ***ulcers reported mainly in panleukopenia according to our results may be explained as a sequel of parvovirus infection of the epithelia of these organs. The prevalence of antigen and intranuclear inclusion bodies in the myocardium and smooth muscle cells of the small intestine — tissues with low or no mitotic activity, — allows to question the postulate of the parvoviruses' exclusive affinity to rapidly dividing cells.
Von 35 Hunden mit Parvovirusenteritis und 19 Katzen mit Panleukopenie wurden post mortem die Organe, welche schon seit längerem als Replikationsorte der Parvoviren bekannt sind und zusätzlich geschichtete Plattenepithelien verschiedener Körperregionen mittels direkter Immunfluoreszenz und histologisch untersucht. Die Befunde ließen bei Hund und Katze keine gravierenden Unterschiede erkennen.
Antigen war in Zungenoberseitenepithel (96,3%), Pharynxepithel (81,0%), Ösophagusepithel (50,0%), Zungenunterseitenepithel (20,4%) und Epithel des Nasenspiegels (5,6%) nachweisbar. Epithel der äußeren Haut und der Schleimhäute männlicher und weiblicher Geschlechtsorgane war nie antigenhaltig. Außerdem fand sich Antigen in Dünndarmmukosa (85,2%), Knochenmark (81,6%), Milz (79,6 %), Thymus (66,7 %), Mesenteriallymphknoten (60,4 %) Tonsilla palatina (58,5 %), glatten Muskelfasern der Tunica muscularis des Dünndarms (9,3 %) und Myokard (1,9 %).
Die histologischen Veränderungen von Dünndarmschleimhaut, lymphatischem Gewebe, Knochenmark und Myokard waren literaturkonform. In glatten Muskelfasern der Tunica muscularis des Dünndarms und im Zungen-, Pharynx- und Ösophagusepithel wurden Kerneinschlußkörperchen (KEK), im Zungen- und Pharynxyepithel diese im Verein mit Nekrosen angetroffen.
Die vor allem bei Panleukopenie in der Literatur mehrmals erwähnten Zungen- und Ösophagus-erosionen bzw. ***ulcera finden ihre Erklärung in der gemäß der vorliegenden Untersuchung gesicherten Manifestation der Parvovirusinfektion im Epithel dieser Organe. Das Auftreten von Antigen und KEK im Myokard und in glatten Muskelfasern des Dünndarms — Geweben, die nicht zu den Wechselgeweben zählen — gibt Anlaß, den vielfach postulierten Tropismus der Parvoviren ausschließlich zu den mitosereichen Geweben in Frage zu stellen.
Zusammenfassung
Bei 17 (1,75%) von 973 Kot‐ und Darmproben enteritisch erkrankter Hunde ließ sich mittels ELISA Rotavirusantigen nachweisen, ebenso bei 2 von 30 Kontrolltieren. Beim Hund scheint das Rotavirus daher nicht die gleiche Bedeutung als typischer Enteritiserreger zu besitzen wie bei anderen Tierspezies oder beim Menschen. Der Anteil von 84% positiven Serumproben unter 300 Hunden (Nachweis von Rotavirus‐Antikörpern im ELISA) spricht andererseits für eine starke (klinisch inapparente?) Durchseuchung der Hundepopulation. Ob und in welchem Maße daran u.U. andere als originär canine Rotaviren beteiligt sind, ließ sich durch die Untersuchungen nicht klären.
Summary
Significance of rotavirus infections in dogs
Rotavirus antigen was detected by ELISA in 17 (1.75%) of 973 faecal and intestinal samples from dogs with enteritis, and in two of 30 control animals. In contrast to other species including man, rotavirus obviously is not a typical aetiological agent of enteritic diseases in the dog. On the other hand, the rate of 84% seropositive dogs (demonstration of antibodies by ELISA) speaks in favour of a widespread occurrence of rotavirus infections (possibly inapparent) also in this species. It has to be clarified whether and to what degree other than canine rotaviruses are involved.
Résumé
Signification des infections à Rotavirus chez le chien
Un antigène Rotavirus a été mis en évidence au moyen de l'ELISA dans 17 (1,75%) sur 973 échantillons de matières fécales et d'intestin de chiens souffrant d'entérite et chez 2 des 30 animaux de contrôle. Rotavirus ne semble pas avoir la même signification chez le chien que chez d'autres espèces animales ou chez l'être humain en tant qu'agent typique d'entérite. Le 84% des sérums positifs parmi 300 chiens (mise en évidence des anticorps Rotavirus avec ELISA) indique par ailleurs une forte contamination (cliniquement inapparente?) de la population canine. Les recherches n'ont pas permis d'expliquer dans quelle mesure d'autres Rotavirus que ceux d'origine canine intervenaient.
Resumen
La significación de infecciones por rotavirus en el perro
En 17 (1,75%) entre 973 muestras de heces e intestinos de perros enfermos de enteritis se pudo poner en evidencia antígeno de rotavirus a igual que en 2 de 30 animales testigos, mediante el procedimiento ELISA. Por lo tanto, parece ser que en el perro no tiene la misma significación como agente etiológico típico de enteritis que en otras especies animales o en el ser humano. Por el contrario, la cuota de un 84% de muestras de suero positivas entre 300 perros (puesta en evidencia de anticuerpos de rotavirus en el ELISA) aboga a favor de una morbilidad considerable (¿clínicamente inaparente?) de la población canina. Por medio de esta pesquisa no se pudo aclarar si y en qué grado, si se presenta la ocasión, se hallan envueltos otros rotavirus que no sean los caninos originarios.
Foram analisadas 33 amostras de fezes de cães com diarréia (n=25) e sem diarréia (n=8), de variadas idades e raças, de ambos os sexos, a fim de se determinar a ocorrência de agentes virais considerados causadores da gastroenterite no cão, suas possíveis associações e a participação no complexo gastroenterite canina, buscando relacionar a etiologia viral com o histórico de vacinação, além do exame clínico dos animais. Utilizou-se microscopia eletrônica nas 33 amostras fecais e o teste ELISA em 71 amostras para detecção de antígeno de rotavírus e adenovírus. Partículas virais foram detectadas em 75,8% (25/33) do total de amostras diarréicas ou não, examinadas à microscopia eletrônica. Em 44% dos espécimes positivos para vírus (11/25), o vírus-like tipo 1 foi o mais detectado nas amostras fecais, seguido pelo parvovírus (24%). A ocorrência de diarréia com sangue esteve associada a 90,9% dos agentes detectados, variando em freqüência de 25% a 100% dos casos.
The clinical signs, hematologic changes, serum and fecal virus titers, specific antibody production and the occurrence of histologic lesions were studied in 22 nine-week-old seronegative beagle dogs inoculated by the oral and intravenous route with canine parvovirus. Approximately 30% of the dogs had clinical signs of pyrexia, depression, vomiting, and diarrhea irrespective of the route of inoculation. Events in the dogs inoculated intravenously preceded those in dogs inoculated orally by approximately two days. Only one dog died. Lymphopenia was the most consistent hematologic change. Viremia always preceded the initiation of fecal virus shedding. Viral titers in the serum and feces were significantly greater in symptomatic dogs compared to asymptomatic dogs. Termination of the plasma viremia coincided with the onset of the humoral immune response, but viremia persisted one day longer in symptomatic dogs. The severity of lymphoid tissue and intestinal infection, assessed by tissue immunofluorescence and histology, was also greater in symptomatic dogs. The severity of intestinal disease was highly correlated with the magnitude and duration of viremia.
Canine parvovirus infections were studied in 65 dogs using conventional immunofluorescence technique and with immunofluorescence technique on formalin‐fixed material. The results of the two methods were similar. The use of formalin‐fixed material for detecting parvovirus simplifies collection and storage of specimens. It also provides an opportunity to make retrospective studies and to compare consecutive sections for normal histology and immunofluorescence.
The study also demonstrated canine parvovirus infection in dogs which died from causes other than parvoviral enteritis, such as pneumonia and heptatitis.
Zusammenfassung
Parvovirus Infektion beim Hund nachgewiesen durch Immunofluoreszenz
65 Hunde wurden mittels herkömmlicher Immunofluoreszenz und einer Technik nach Formalinfixierung auf das Vorhandensein einer caninen Parvovirus‐Infektion untersucht und beide Nachweismethoden miteinander verglichen. Es zeigte sich, daß die Ergebnisse beider Untersuchungsreihen übereinstimmten.
Die Verwendung von fixiertem Material zum Nachweis von caninem Parvovirus erleichtert die Sammlung und Lagerung von Untersuchungsmaterial. Desweiteren bietet diese Technik auch Möglichkeiten, Untersuchungen rückwirkend anzustellen und eine Gefrierschnittserie mit der bisherigen histologischen und fluoreszenztechnischen Methodik zu vergleichen.
Die Untersuchungen zeigen gleichzeitig, daß Hepatitis und Pneumonie die Todesursachen bei einer Parvovirusinfektion sein können.
Résumé
Infection à Parvovirus du chien démontrée par immunofluorescence
On a recherché une infection à Parvovirus canin chez 65 chiens au moyen de l'immunofluorescence traditionelle et avec une technique après fixation à la formaline; les deux méthodes ont été comparées. Les résultats des deux méthodes ont correspondu.
L'utilisation d'un matériel fixé pour la mise en évidence du Parvovirus canin facilite la collecte et l'entreposage du matériel d'examen. Cette technique offre également des possibilités d'effectuer des recherches rétrospectives et de comparer une sirie de coupes par congélation avec la méthode histologique et par la technique de la fluorescence utilisée jusqu'à maintenant.
Les recherches ont également montré qu'une hépatite et une pneumonie pouvaient être des causes de mort lors d'une infection â Parvovirus.
Resumen
La infección por parvovirus canino demostrada mediante inmunofluorescencia
Se examinaron 65 perros mediante la inmunofluorescencia convencional y con una técnica, tras fijación en formol, en cuanto a la presencia de una infección por parvovirus canino, comparándose entre sí ambos métodos de puesta en evidencia. Así se pudo comprobar que coincidían los resultados de ambas series de investigación.
El uso de material fijado para la puesta en evidencia de parvovirus canino simplifica la colección y el almacenamiento de material des pesquisa. Además, esta técnica ofrece también posibilidades para llevar a cabo investigaciones retroactivas y comparar una serie criotómica con la técnica histológica y fluorescente convencional.
Los estudios efectuados muestran, al mismo tiempo, que la hepatitis y la pneumonía pueden ser causas de muerte en una infección por parvovirus.
Canine rotavirus particles were visualized by direct electron microscopy in the feces from a clinically normal dog. The virus was subsequently propagated in cell cultures; it was characterized and compared with rotaviruses from other species. Replication of the virus in cell culture was found to be less dependent upon trypsin than that of human, bovine and porcine rotaviruses. Reproducible, sharp-edged plaques of various sizes were produced by the canine rotavirus in an established cell line of fetal rhesus monkey kidney, MA 104, under overlays of carboxymethyl cellulose or agarose. Intracytoplasmic inclusion bodies of different sizes and shapes were produced in infected MA 104 cells. By plaque reduction neutralization assay, a two-way antigenic relationship was found between the canine (CU-1) and simian (rhesus MMU 18006 and SA-11) rotaviruses. The canine rotavirus had a one-way antigenic relationship with feline (Taka), bovine (NCDV), and porcine (OSU) rotaviruses.
The last decade of research has resulted in an explosion of knowledge about viral gastroenteritis. Great advances have been made in delineating the causative agents, epidemiology, pathophysiology, and immunity of viral gastroenteritis. Despite the major advances reviewed here, there has been no significant change in practical diagnosis, therapy, or prevention of gastroenteritis. The diagnosis of rotavirus gastroenteritis is now possible using technology readily available in clinical laboratories and undoubtedly will be the first major advance gaining widespread use. However, at this time the diagnosis of viral gastroenteritis continues to rest on the typical clinical picture and exclusion of common bacterial pathogens. The diagnosis of all other gastroenteritis agents remains the province of the highly sophisticated research laboratory that uses electron microscopy or experimental radioimmunoassay requiring carefully defined and difficult to acquire fecal and serum samples. Therapy is still limited to nonspecific supportive measures. No intervention has significantly altered the course of illness or prevented infection. The selection of oral or intravenous replacement fluids remains a function of severity of illness and risk of complications. The high-risk patients include the elderly, debilitated, or very young, and these may require hospitalization or parenteral fluids. Development of a vaccine for rotavirus appears feasible. The limited antigenic varieties, laboratory growth in vitro, related animal viruses, and the potential for production of hybrid strains make this a fertile area of exploration. The need to protect for a relatively limited period of time (approximately six months to two years of age) enhances the likelihood of success. However, the mixed results of vaccination of calves to prevent rotavirus gastroenteritis warns of potential difficulties ahead. Many basic research advances are required before vaccines for Norwalk-like viruses can be developed. The viruses must be purified, cultivated, and the antigenic varieties delineated. Even if these formidable problems are overcome, vaccination may not be practical owing to the variety of antigenic strains and the relatively short immunity in naturally acquired infection.
Astrovirus-like, coronavirus-like, and parvovirus-like particles were detected through electron microscopic (EM) examination of loose and diarrheal stools from a litter of beagle pups. Banding patterns obtained from equilibrium centrifugations in CsCl supported the EM identification. Densities associated with the identified particles were: 1.34 g/ml for astrovirus, 1.39 g/ml for "full" parvovirus and 1.24-1.26 g/ml for "typical" coronavirus. Convalescent sera from the pups aggregated these three particle types as observed by immunoelectron microscopy (IEM). Only coronavirus-like particles were later detected in formed stools from these same pups. Coronavirus and parvo-like viruses are recognized agents of canine viral enteritis, however, astrovirus has not been previously reported in dogs.
The maternal antibody (MAb) titre to canine parvovirus (CPV) was determined on consecutive serums from 39 puppies in 7 litters. Vaccination with inactivated CPV was performed at a variety of ages and the response of the puppies determined. Transfer of MAb was demonstrated in 71% (5/7) of the litters and persisted for up to 10 weeks in some litters. MAb titres of >20 precluded a vaccination response by puppies. Sixty‐ one per cent (8/13) of puppies responded to vaccination when the MAb titre was <20. However, no anamestic response occurred and in some cases a decrease in antibody titre was observed following a second vaccination. During an outbreak of canine parvovirus enteritis (CPE) in the kennel, 33 puppies developed clinical signs of enteritis. Of these puppies 85% (28) had MAb titres of <80 at the onset of clinical signs. Fifty per cent (4/8) of the puppies which responded to vaccination developed CPE, whereas 100% (5/5) of those that did not respond to vaccination developed CPE.
The results indicate that MAb may persist for up to 10 weeks and puppies with MAb in the titre range >20 to <80 do not respond to vaccination but are still susceptible to infection. It is also apparent that a significant minority of puppies with MAb <20 do not respond to vaccination.
An examination of the breeding records of the kennel for the 7 year period 1973–1981 demonstrated a sudden decrease in reproductive efficiency during and subsequent to 1978. This coincided with the recognition of cases of CPV infection in the kennel. It is suggested that further investigation is required into the possible role of CPV in reproductive failure.
The authors would like to thank H. Findlay, P. Hinchliffe, G. Griffiths and S. MacPhail for technical assistance and Dr G. Wilcox and R. Flower for helpful discussion and advice.
Five 7-week-old pups and four 4-week-old pups, all seronegative to canine parvovirus, were inoculated intravenously with 1000 haemagglutinating units of canine parvovirus originally isolated from the myocardium of a dog with naturally occurring myocarditis. After three days, pups in both litters became pyrexic, anorectic and depressed, with vomiting and diarrhoea. The 4-week-old pups were killed on day 4, and the 7-week-old pups died or were killed on day 5 post-inoculation. Histological examination showed degeneration and necrosis of intestinal crypt epithelial cells and villous atrophy. All pups had thymic atrophy caused by lymphoid depletion. Peyer's patches, mesenteric lymph node and spleen also had lymphoid depletion. Lymphoid necrosis was present occasionally in these tissues. In the bone marrow, granulocytes and granulocyte and erythroid precursors were depleted. Amphophilic intranuclear inclusion bodies were abundant in crypt epithelial nuclei, less so in myocardial nuclei. Canine parvovirus was isolated from intestinal contents, thymus, spleen, mesenteric lymph node and liver in most pups, but not from kidney or myocardium.
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