Proceeding of the Institute for Zoo and Wildlife Research, Berlin, Germany (IZN) ISSN 1431-7338
42.International Symposium on Diseases of Zoo and Wild Animals, May 04 - 08 - 2005, Prague, Czech Republic

PROVENTRICULAR DILATATION DISEASE (PDD) IN SPIX’S MACAWS
(CYANOPSITTA SPIXII)
HAMMER S1, GERLACH H2, BÜRKLE M3, SCHULZ J1

1 Al Wabra Wildlife Preservation, PO Box 44069, Doha, State of Qatar; awwp.director@alwabra.com
2 Grosshesseloher Str.23, 81479 Munich, Germany
3 Tierärztliche Praxis, Dr. Bürkle/Dr. Britsch, Am Storrenacker 1b, 76139 Karlsruhe, Germany

Extended Abstract

Summary

Proventricular dilatation disease (PDD) is still considered to be the most threatening disease amongst psittaciformes. Clinical signs can include among                         others depression, weight loss and the passage of undigested seeds in the feces. Lately, the disease seems to affect more often the central nervous                            system, ganglia of the heart and adrenal glands. Evaluation of crop biopsies for non-purulent ganglionitis is still the only way to obtain a definitive                                         antemortem diagnosis. In March 2004, at Al Wabra Wildlife Preservation in Qatar, three adult Spix’s Macaws (Cyanopsitta spixii) were diagnosed                           either suspected or proven for PDD by crop biopsies. In spite of intensive symptomatic treatments all three birds developed either gastro-intestinal                                  or central nervous disease and died eventually between April 2004 and January 2005. Additionally, serology of Paramyxovirus and histological                               findings following necropsies have been compared between the three cases.

Introduction
Proventricular Dilatation Disease (PDD) was first described in the late 1970s (GRAHAM, 1984). Until now it has been reported in more than 50                          different parrot species (GREGORY et al., 1994). Clinical signs can include depression, weight loss (with or without decreased appetite) and the                                      passage of undigested seeds (ROSSKOPF et al. 1986). Classical histological changes are an inflammatory response characterized by the                                               accumulation of lymphocytes and plasma cells in the nervous system, especially of the intrinsic nerves that supply the muscles in the proventriculus                                  and other digestive organs including the crop, ventriculus and duodenum (GERLACH, 1994). Lately, the non-purulent ganglionitis seems to affect                                    more often the central nervous system, and ganglia of the heart and adrenal glands, rather than the gastrointestinal tract (GERLACH, 1997). To date,                   evaluation of crop biopsies is still the only way to obtain a definitive antemortem diagnosis (RITCHIE et al., 2004). Crop biopsy is diagnostic in                      approximately 75% of birds with clinical PDD (GREGORY et al., 1996). Unchanged crop ganglia do not exclude an infection.

Case Reports
Clinical History
From November 2003 until March 2004, a total of 25 Spix’s Macaws (Cyanopsitta spixii) were transferred from the Philippines to Al Wabra  Wildlife Preservation in Qatar. The birds were kept in four different houses under quarantine conditions. Extensive health checks were performed      to gain status information on the physical condition of the animals. In February 2004, an adult female Spix’s Macaw (case # 1), was reported   anorexic and slightly depressed. CBC and blood biochemistry were within normal limits and no microbiologic growth occurred from swabs taken from the crop and the cloaca. Even though no indications for a disease were found, the bird kept loosing weight and had to be force fed up to             3 times daily.

Histological evaluation of a crop biopsy showed the presence of severe multi-focal lymphoplasmacytic infiltrates within ganglia, indicative for PDD.                          Shortly after that diagnosis, the female started to regurgitate and trembled a lot. Despite further symptomatic treatment she died 3 weeks afterwards,                                 2 months after the first onset of disease. On its arrival in March 2004, an adult, male Spix’s Macaw (case # 2), already looked weak with ruffled                           feathers, his body condition was only average. A crop biopsy taken immediately showed rare multifocal perivascular lymphocytes and plasma cells.                             Even though the ganglia were not involved, the bird was evaluated suspicious for PDD. The male remained under quarantine conditions and oral                                     treatment with celecoxib (10 mg/kg BW po), a cyclooxigenase-2 (COX-2) inhibitor, was started. In June 2004 he started to show CNS-signs,                                       he was not able to coordinate his feet properly anymore and was trembling a lot but his appetite and feces were normal. Another crop-biopsy, taken                               in June 2004, could not confirm the suspected diagnosis of PDD, but again the bird was considered suspicious for the disease as a proliferation of                                 glial cells was diagnosed.

Throughout August and September 2004 different other treatments were tried without any improvement. Towards the end of September his state                                      worsened rapidly and he could not perch anymore. For animal welfare reasons the decision was taken to euthanize this Spix’s Macaw. The third                                 case, another adult male Spix’s Macaw (case # 3), was diagnosed positive for PDD as a crop biopsy, taken in March 2004, showed typical lesions                        indicative for PDD. Therefore he was put on celecoxib-treatment and remained in quarantine. For several months he looked and behaved normal.                                    A second crop-biopsy taken in September 2004 was only evaluated as a chronic/subacute ingluviitis. The observed lesions were not considered to                                 be typical for PDD, but the male remained suspicious for the disease as the proventriculus appeared enlarged on radiographs taken the same day. In                            December 2004, the bird showed for the first time a reduction in his body condition despite normal appetite. Paramyxovirus-like particles were found                              in its feces by electron microscopic examinations. Additionally he was diagnosed seropositive for avian paramyxovirus (APMV-1) and seropositive                                     for pigeon paramyxovirus (PPMV-1). At that stage, slight head tremors were noted occasionally, but within 6 weeks the symptoms became worse                              until the bird was almost unable to perch. In January 2005 he died with a weight of 185 g only.

Further Investigations
Histopathologic evaluations were done in all three Spix’s Macaws. In the first deceased female (case # 1), no inflammatory reaction was present in the                        crop, some mononuclear cellular invasions were noted in the gizzard, and a classical non-purulent ganglionitis was diagnosed in the proventriculus. In                              the cerebrum and the adrenal gland, few perivascular infiltrations with mononuclear cells were present. In case # 2, where two different crop biopsies                             did not reach a clear diagnosis of PDD, also no obvious histopathologic lesions were found in proventriculus, gizzard and pancreas. In the crop,                        perivascular infiltrations with mononuclear cells (as far as recognizable not in the ganglia) and proliferation of glia cells in few ganglia were noted. The                        adrenal gland had two little subcapsular infiltrates out of mononuclear cells.

A cerebral pseudoneuronophagia and gliosis as well as few mononuclear cells outside the vesicular wall were present; only one blood vessel seen had                               a perivascular cuffing typical for PDD. Additionally, a malacia of the substantia alba of the spinal cord and gliosis was found, and a massive nephropathy         characterised by sclerosis of the glomerula, tubulonephrosis and focal interstitial nephritis. Apparently there was a viral infection of the brain but the                         changes were not typical for PDD. Serum taken during euthanasia was sent for serologic evaluation of paramyxovirus-antibodies; the bird was                          seropositive for APMV but seronegative for PPMV. There is a high probability that the aetiologic agent of PDD is an Avian Paramyxovirus. That is why                           a specificerology is done for APMV with ELISA and Western Blot. The viral particles found in the feces were APMV; however, it seems that these                      excreted particles are not infectious (GRUND, oral information, 2005).

The histopathologic evaluation of the third Spix’s Macaw (case #3) revealed a non-purulent ganglionitis of the ventriculus, verifying the PDD infection.                           The crop, however, only showed a non-purulent perivasculitis, and in the proventriculus no obvious lesions could be found at all. In heart, adrenal gland,                 cerebrum and spinal cord no lesions indicative for a PDD infection could be found. Also, signs of a PMV infection were not present.

Discussion
To date the causative agent of PDD is still not finally identified. Even though various viruses have been found in parrots with confirmed PDD, only                           APMV could be demonstrated with some frequency in PDD positive birds (MANNL et al., 1987; GRUND et al., 1999). Tissue homogenates from                      affected birds can experimentally induce the lymphoplasmacytic ganglioneuritis that characterizes PDD. Clinical changes in those animals vary from                            central nervous  system to gastrointestinal signs. The same virus can cause different clinical signs even within the same bird species. The incubation                             period in those experimentally infected birds varied between 11 days and three months (RITCHIE et al., 2004). The crop biopsy as well as the                    histopathologic xamination of the deceased female (case #1) revealed the classical non-purulent ganglionitis, conclusive for PDD.

However, two crop biopsies and a complete histopathologic evaluation of case # 2 did not reveal the classical findings. And in case #3 the non-purulent             ganglionitis in the crop could neither be confirmed in a second biopsy nor during histopathologic postmortem evaluation, only in the gizzard a non-purulent           ganglionitis was present. The lack of any convincing findings other than a suspicion of a paramyxovirus infection should lead to a careful reevaluation of                           the case of the second Spix’s Macaw (case #2) that has been euthanized. For epidemiologic reasons this male was treated for suspected PDD                             alongside with the other birds. However, one could speculate that the underlying (chronic) nephropathy could have made the bird susceptible for clinical                            consequences of a PDD-infection. The third bird was proven positive for PDD despite an only ‘suspicious’ follow up crop biopsy; the suspicion for an                    infection with a paramyxovirus could not be confirmed.

The diversity of these three cases and the fact that the last two birds were both seropositive for APMV only recently (they had been negative in tests                           done some months earlier), suggests that a paramyxovirus helped as a trigger for the development of clinical PDD or was even the cause of the central                      nervous signs in the second parrot. A high incidence of subclinical APMV-1 infections in captive psittacine species was recently reported and is                         considered  to contribute to a chronic disease like PDD (GRUND and MOHN, 2003); clinical problems might even be aggravated by other primary                      diseases as in the second animal. Currently further investigations are ongoing within the remaining Spix’s Macaw population at AWWP, not only with                                 a major emphasis on the PDD-status but also to verify infections with APMV.

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