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Israel Journal of Veterinary Medicine Vol. 68 (4) December 2013Ozmen, O.
218
INTRODUCTION
Macrorhabdus ornithogaster was previously referred to as
Megabacteria and was once considered to be a bacterium,
however, research has conrmed that it is a yeast organism
containing a eukaryotic nucleus (1). M. ornithogaster colo-
nizes the proventriculi and ventriculi of birds (2). is or-
ganism causes a chronic wasting disease, characterized by
emaciation, weakness, high rates of morbidity and low rates
of mortality, and has been described in canaries and budgeri-
gars. Vomiting of slimy material due to acute hemorrhagic
gastritis occurs in advanced stages of the disease in budgeri-
gars (3, 4). e known host range of the organism includes
several species of poultry, other captive bird species belonging
to several orders, including psittacine and passerine cage and
aviary birds, and some free-living bird species (5).
M. ornithogaster is an anamorphic ascomycetous yeast
e Pathology of Macrorhabdus ornithogaster and Eimeria dunsingi
(Farr, 1960) Infections in Budgerigars (Melopsittacus undulatus)
Ozmen, O.,
1
* Aydogan, A.,
1
Haligur, M.,
1
Adanir, R.,
2
Kose, O.
2
and Sahinduran, S.
3
1
University of Mehmet Akif Ersoy, Faculty of Veterinary Medicine, Department of Pathology, Istiklal Yerleskesi , 15030,
Burdur, Turkey,
2
University of Mehmet Akif Ersoy, Faculty of Veterinary Medicine, Department of Parasitology, Istiklal Yerleskesi, 15030,
Burdur, Turkey.
3
University of Mehmet Akif Ersoy, Faculty of Veterinary Medicine, Department of Internal Medicine, Istiklal Yerleskesi,
15030, Burdur, Turkey.
*Corresponding Author: Dr.Ozlem Ozmen, University of Mehmet Akif Ersoy, Faculty of Veterinary Medicine Department of Pathology, Istiklal Yerleskesi,
15030, Burdur, Turkey, Tel: +90 248 2132170. Email: ozlemozmen@mehmetakif.edu.tr.
ABSTRACT
e aim of this study was to describe the pathological ndings in budgerigars simultaneously infected
under eld conditions with coccidiosis and megabacteriosis. Severe diarrhea and vomiting were observed in
a budgerigar ock. Aected birds showed inappetence and loss of condition, with a ock mortality rate of
30%. At necropsy, the proventriculi and ventriculi were swollen and hyperemic, and viscous mucus and blood
adhered to the mucosa. Cytological examination of Giemsa stained proventricular and ventricular tissue
revealed clusters of yeast. Microscopically, mild to severe inammatory reactions, ulcers and hemorrhage
were observed in the proventriculi. Numerous large, rod shaped Macrorhabdus ornithogaster organisms had
colonized the proventriculi, ventriculi and gut. e bright pink organism was easily detected in periodic acid
Schi stained sections. On microscopic examination of the feces, numerous Eimeria oocysts were observed.
Histopathological examination of the gut revealed numerous coccidial organisms in epithelial cells. Eimeria
dunsingi (Farr, 1960) was identied in the gut contents of the birds, based on morphological characteristics.
Surviving birds were treated with amphotericin-B for megabacteriosis and with toltrazuril for coccidiosis,
after which the mortalities ceased. ese results demonstrated that simultaneous natural infections under
eld conditions can cause severe, gross histopathological lesions and high rates of mortality in birds. At the
same time, this is the rst report of M. ornithogaster infection in budgerigars in Turkey.
Keywords: Macrorhabdus ornithogaster, Eimeria dunsingi (Farr, 1960), megabacteriosis, budgerigar,
pathology, coccidiosis, treatment.
Israel Journal of Veterinary Medicine Vol. 68 (4) December 2013
219
Megabacteriosis and Coccidiosis in Budgerigars
that is the only known member of its genus (6). e organ-
ism is relatively large (20-70 µm long and 1-5 µm wide), rod-
shaped to lamentous, and stains positive with Gram and
periodic acid-Schi (PAS) stains (7). Hematoxylin and eosin
staining reveals a histological appearance of the organism
in infected birds of a typical “haystack” appearance in situ.
Coccidiosis is a disease that infects all avian species, in-
cluding psittacine birds. e disease can cause hemorrhagic
diarrhea, depression, emaciation, weight loss and sometimes
death (8-11). Coccidial infections in psittacine birds may be
asymptomatic or associated with diarrheal syndromes (some-
times with blood in the droppings), emaciation, general ill
health, and systemic disease (8). Coccidial species causing
infections in aviary birds include Eimeria dunsingi (Farr,
1960), E. haematodi, Isospora psittaculae, I. serini and I. laca-
zei (12-14).
M. ornithogaster has a worldwide distribution and a wide
range of host birds, including psittacines, passerines, ratites
and poultry species (15). ere has been one report on M.
ornithogaster in laying hens, (16) however, there have been
no reports concerning M. ornithogaster infection in budgeri-
gars in Turkey. Coccidiosis is a protozoan disease and can
cause high mortality in all avian species (17). Budgerigar
breeding is rapidly becoming more popular in Turkey and
the knowledge about diseases of this species is drawing
attention. Both megabacteriosis and coccidiosis are com-
mon diseases in budgerigars but there have been no re-
ports on pathological ndings in natural and simultaneous
infections.
e aim of this study was to describe the pathological
ndings in simultaneous infections with M. ornithogaster and
E. dunsingi (Farr, 1960) in budgerigars, as well as the treat-
ment and prophylaxis of these diseases. is is the rst report
of dual infection in budgerigar in Turkey.
MATERIALS AND METHODS
Deaths occurred in a colony of birds that were transported
from a hatchery 650 km away from the aviary. Seventy-ve
birds in the ock of about 250 budgerigars died, and 38
of these were presented to the Department of Pathology
University of Mehmet Akif Ersoy, for diagnosis during
the preceding three days. Eighteen of the 38 birds were
infected with both megabacteria and coccidial organisms.
Severe hemorrhagic diarrhea, depression and death were
the most common clinical symptoms. Feces usually ad-
hered around the anus (Figure 1). At necropsy, hemor-
rhages at the proventriculus and gut were observed in birds.
Coccidiosis was diagnosed in 12 birds while eight birds
were diagnosed with megabacteriosis alone. Direct mi-
croscopy of fresh impression smears of ventricular or pro-
ventricular mucosa was prepared on glass slides, unstained
and Giemsa stained preparations were examined micro-
scopically to diagnose M. ornithogaster infection. All fe-
cal impression smears without staining were examined for
any microorganism and then Fulleborn’s otation method
used for initial diagnosis of coccidiosis. A 2.5% solution of
potassium dichromate was added to feces containing the
oocysts and homogenized. e mixture was ltered and
stored in a petri dish at room temperature for sporulation.
Identication of oocysts was based on their morphological
characteristics (9, 11, 17).
For histopathological examination, tissues were xed in
10% buered formalin, processed routinely and stained with
hematoxylin and eosin (H&E). Samples from proventriculi,
ventriculi, and the gut were also stained with PAS to identify
M. ornithogaster.
e severity of gut lesions was assessed by scoring hem-
orrhages and inammatory reactions in birds with single or
dual infections. Each criterion was graded on a scale of 0 to
4 as follows: 0= no lesion, 1= focal slight, 2= focal severe, 3=
diuse slight and 4= diuse severe. Data from each animal
was analyzed statistically. One-way analysis of variance was
used to detect any dierences between the single and dual
infection groups. e non-parametric Duncan multiple com-
Figure 1: Feces around the anus, diarrhea in three budgerigars which
died from combined infection coccidiosis and megabacteriosis.
Research Articles
Israel Journal of Veterinary Medicine Vol. 68 (4) December 2013Ozmen, O.
220
parison method was used to assess the statistical signicance
of dierences. Statistical analyses were performed using the
SPSS 13.0 program (SPSS Inc., Chicago, IL). A P value <
0.05 was considered as statistically signicant.
Surviving birds were treated with amphotericin-
B (Fungizone, Bristol-Myers Squibb Inc, Istanbul-
Turkey) and toltrazuril (Baycox, Bayer- Istanbul-Turkey).
Amphotericin-B was administered twice a day (0.15-0.30
mL/bird) over 30 days to treat megabacteriosis, and toltra-
zuril (1.5 mL per liter of drinking water) was administered
3 days to treat coccidiosis. In addition, 0.1% apple vinegar
(Baktat Elma Sirkesi- Bursa- Turkey) in the drinking water
was administered during 10 days with one-week intervals
three times, totally 30 days.
RESULTS
At necropsy, atrophy of the pectoral muscle was most com-
monly observed in dead birds aected by megabacterio-
sis. ickening of the proventricular and ventricular walls,
covering of the proventricular mucosa by thick white mu-
cus, ulceration and hemorrhage of the proventricular and
ventricular mucosa, loosening of the koilin layer and hem-
orrhage into the lumen of these organs were commonly
observed (Figure 2). In addition marked hemorrhage in
the small intestinal wall and into the lumen were also ob-
served. e most severe histopathological lesions were seen
in the proventriculus and, in some cases the ventriculus,
including penetration of organisms into the lumen of the
supercial proventricular crypts and occasionally to deep-
er parts of the glands. Inammatory reactions were also
noted. On microscopic examination of impression smears,
long, rod-shaped organisms were observed even at
×
40
magnication. ese microorganisms were lamentous
and non-branching. e morphology, staining character-
istics, and tissue localization of the microorganisms were
consistent with previous descriptions of M. ornithogaster.
Organisms close to and inltrating the epithelium were
in parallel aggregations, whereas their orientation in the
mucin layer was less organized. e characteristics of the
disease and the shape of the organisms in the ulcerated
gastric mucosa suggested a diagnosis of M. ornithogaster
infection.
At necropsy of the birds that suered from coccidiosis,
small hemorrhagic areas and blood were observed in the
small intestine (Figure 3). On microscopic examination of
the gut contents of these birds, numerous Eimeria oocysts
were seen. Histopathology of the guts of these birds revealed
numerous Eimeria organisms, with desquamation and in-
ammation of the gut wall.
e owner stated that after transport of the birds from
the hatchery to the aviary the budgerigars gradually became
emaciated and mortality increased. Birds presented with di-
arrhea and accumulation of dried feces around the cloaca,
which in some individuals formed a packed obstruction or
plug. At necropsy of the dead birds, atrophy of the pectoral
muscles was observed, with hemorrhage of the proventricu-
lar mucosa adjoining the transition to the gizzard. Blood was
also seen in the intestinal lumen. Examination of impression
smear without staining of the gut contents revealed numer-
Figure 3: Hemorrhagic areas in gut in a budgerigar, died from
combined infection.
Figure 2: ickening of the proventricular walls (arrow) and
hemorrhage of the proventricular mucosa (arrow head).
Research Articles
Israel Journal of Veterinary Medicine Vol. 68 (4) December 2013
221
Megabacteriosis and Coccidiosis in Budgerigars
Figure 4: A: Numerous M. ornithogaster organisms (arrows) in Giemsa stained proventricular tissue from a budgerigar.
B: Clusters of M. ornithogaster (arrows) in the lumen of the proventriculus. Hematoxylin and eosin stain.
C: M. ornithogaster organisms show brilliant pink coloration on periodic acid-Schi stained sections.
D: Simultaneous identication of M. ornithogaster (arrow heads) and E. dunsingi (Farr, 1960) organisms (arrows) in a budgerigar
gut. Hematoxylin and eosin stain.
E: An E. dunsingi (Farr, 1960) oocyst as observed on microscopic examination of feces.
F: Sporulated oocyst of E. dunsingi (Farr, 1960).
B
A
C
D
E
F
Research Articles
Israel Journal of Veterinary Medicine Vol. 68 (4) December 2013Ozmen, O.
222
ous coccidial organisms, together with very large rod-shaped
organisms. ese organisms were also observed on Giemsa
stained impression smears (Fig. 4A).
In 18 birds, M. ornithogaster organisms were observed
in the proventriculus, ventriculus and gut, together with
coccidial organisms in the small intestine. At necropsy of
these birds both proventricular-ventricular and gut lesions,
as well as inammation were observed. Younger birds, es-
pecially, died from the diseases, and death usually occurred
suddenly in simultaneously aected birds. Atrophy of the
pectoral muscle was not severe in these cases. Microscopic
examination revealed more severe hemorrhage and inl-
trations in birds with dual infections and this was statisti-
cally signicant (p<0.01) (Table 1). On histopathological
examination of the mucosa of the gizzard, massive clumps
of rod shaped organisms attached to the epithelium were vi-
sualized (Figures 4B, 4C), and these clumps were observed
throughout the proventriculus, ventriculus and gut. In some
of the birds, the organisms penetrated deeply between mu-
cosal folds and were occasionally detected in submucosal
glands (Figure 4D). Numerous coccidial organisms were
observed in the epithelial cells of the gut. Inammatory
reactions were observed in almost all organs of the gastro-
intestinal tract.
Oocysts collected from infected birds sporulated within
one week when stored at room temperature. e oocysts were
distinctly ovoid and colorless to pale blue. ey measured 25
to 35 µm (mean 29.91 µm, SD 3.34 µm)
×
22.5 to 27.5 µm
(mean 24.37 µm, SD 1.88 µm). e oocysts lacked a collar,
micropyle and polar cap but possessed a single eccentrically
located polar granule (Figure 4E). e oocysts were bound by
a smooth bilayered wall. e outer layer was colorless or light
brown and the inner layer was colorless or blue. Sporulated
oocysts contained four ovoid to pyriform sporocysts mea-
suring 12.5 to 15 µm
×
7.5 to 10 µm in diameter (Figure
4F). e sporocysts contained a prominent anterior steida
body and a large posterior residuum consisting of numerous
granules in a compact mass. e sporocysts contained two
elongate sporozoites arranged head-to-tail. e sporozoite
nuclei were located centrally next to a single large refrac-
tile granule. Based on these morphological data, only one
Eimeria spp. had infected the birds and this was the highly
pathogenic Eimeria dunsingi (Farr, 1960). e other visceral
organs were normal in appearance. ere was no mortality
after treatment of the ock.
DISCUSSION
M. ornithogaster “megabacteriosis” has been diagnosed in
many species and results in a varied spectrum of clinical
symptoms and pathologies. In some species (chickens, tur-
keys, guinea fowls) the disease has been characterized clini-
cally by emaciation, prostration, loss of appetite, cachexia and
death, with a typically chronic course. A more acute disease
was observed in nches and budgerigars (18). In budgerigars
in this study suering from megabacteriosis the symptoms
included emaciation, diarrhea, and hemorrhage of the pro-
ventriculus. e presence of characteristic large, rod-shaped
organisms supported the diagnosis (19-21).
Coccidiosis is a common disease in budgerigars and can
result in death. In this study, megabacteriosis and coccid-
iosis were found to occur concurrently. Clinical signs and
pathological ndings related to the gastrointestinal system,
and mortality was 30%. Diarrhea was more frequent than
vomiting, and coccidiosis lesions were more marked than
megabacteriosis lesions.
Postmortem ndings included proventriculitis and pro-
ventricular dilatation. Gram-positive, PAS-positive, aci-
dophilic (on Giemsa staining), rod-shaped bacteria were
identied histologically, especially in the area between the
proventriculus and the ventriculus. A diagnosis may be made
by cytological demonstration of organisms in proventricular
washings (22). In the present study, the diagnosis was made
by cytological and histological conrmation of megabacte-
riosis, and by histological and parasitological conrmation
of coccidiosis. PAS staining was performed to support the
diagnosis of megabacteriosis. e clinical and pathological
ndings were in agreement with previous studies however
due to the coccidiosis co-infection the pathology was more
severe and mortality was higher.
Eimeria dunsingi (Farr, 1960) is a highly pathogenic
Table 1: Statistical analysis and mortality in birds with single
or dual infections.
Groups n Mortality
rate (%) Hemorrhage Inltration
Coc+ Mega 18 47 2.72±1.01
a
2.94±0.80
a
Coc 12 32 1.91±0.90
b
2.25±0.96
b
Mega 8 21 1.50±0.75
b
1.62±0.51
b
P value <0.01* <0.01*
Coc: Coccidiosis, Mega: megabacteriosis,
*Dierences between mean values for groups, as indicated by dierent
letters in the same column, are statistically signicant (P < 0.01).
Research Articles
Israel Journal of Veterinary Medicine Vol. 68 (4) December 2013
223
Megabacteriosis and Coccidiosis in Budgerigars
Eimeria species found in parrots and budgerigars. is or-
ganism localizes in the anterior part of the gut and is com-
mon throughout the world. e endogenous developmental
stages generally localize in villus epithelium, distal to the
nucleus (14). e ndings from this study were in agreement
with previous studies on the localization and morphology of
this organism. Because of the pathogenicity of the organism,
the coccidiosis lesions were more severe than those due to
megabacteriosis.
Experimental infections with pure cultures of megabac-
terium induce disease only in English standard budgerigars
and not in the common breed. ese ndings suggest that
birds vary in their susceptibility to the organism, and other
factors are involved in the pathogenesis. Spontaneous re-
covery was common in experimental cases (23). is present
study showed that simultaneous infection with M. ornitho-
gaster and E. dunsingi (Farr, 1960) can increase the sever-
ity and rate of mortality of the disease in budgerigars. e
study also indicated that when mortality in budgerigars is
high, the possibility of a coinfection should be taken into
consideration.
Domestic animals are invariably transported for a variety
of reasons, and it can cause potential stress. Transport stress
may be increases the animals’ susceptibility to diseases (24)
and increase the mortality rate (25). Birds are very sensi-
tive to change, so moving can be particularly stressful for
them (13). Transportation was considered to be a predispos-
ing factor in the occurrence of disease outbreaks in birds in
this study as there was no clinical problems observed in the
hatchery and in the remaining birds. e outbreak only oc-
curred after transportation.
e prevalence of M. ornithogaster infection is highest
in captive-bred budgerigars, parrotlets and canaries, and the
disease occurs in these birds throughout the world (19, 26,
27). To the best knowledge of the authors this is the rst
report of megabacteriosis in budgerigars in Turkey. Owners
do not generally seek veterinary or laboratory assistance and
professionals may not be aware of the occurrence of exotic
bird diseases in this country, which may explain the absence
of previous reports. is study showed that M. ornithogaster
infection may have been a problem in budgerigars.
Because the pathogenic organism is a yeast, birds with
megabacteriosis show very poor responses to antibiotics,
and antifungal drugs are most commonly recommended
(27-29). e present study conrmed the benet of treat-
ment with amphotericin-B in budgerigars with megabacte-
riosis. Megabacteriosis causes an increase in the pH of the
proventricular mucus from 2.7 to 7.0-7.3 (39, 30). Because
megabacteria thrive in an alkaline environment, an alterna-
tive treatment strategy is to increase the acidity of the pro-
ventricular uid by oral administration of apple vinegar or
grapefruit juice (13). We also found that 0.01% apple vinegar
in drinking water was eective for prophylaxis. is study
also conrmed that toltrazuril is an eective treatment for
coccidiosis. e present results showed that co-infection can
cause severe lesions and increased mortality in budgerigars.
Practitioners should consider simultaneous infection in bud-
gerigars, especially in disease outbreaks with high mortality,
and when there is no response to treatment. Prophylactic
measures against megabacteriosis, such as administration of
apple vinegar, may be advisable before birds are transported
or experience other types of stress.
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