A Review of Proventricular Dilatation Syndrome

Association of Avian Veterinarians
A Review of Proventricular Dilatation Syndrome
Author(s): Christopher R-Gregory, Kenneth S. Latimer, Frank D. Niagro, Branson W. Ritchie,
Raymond P. Campagnoil, Terry M. Norton, Rita McManamon, Cheryl B. Greenacre
Source: Journal of the Association of Avian Veterinarians, Vol. 8, No. 2 (1994), pp. 69-75
Published by: Association of Avian Veterinarians
Stable URL: http://www.jstor.org/stable/27671120
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of
Journal
A REVIEW OF PROVENTRICULAR
SYNDROME
Christopher R Gregory, DVM'5"
S Latimer, DVM, PhD*
Kenneth
PhD**
Frank D Niagro,
Branson W Ritchie, DVM,
PhD***
P Campagnoli,
MS*
Raymond
M
DVM****
Norton,
Terry
Rita
DVM*****
McManamon,
Cheryl
B Greenacre,
DVM***
syndrome
drome,
ent
the
disease
or
syndrome,
to
hy
of macaws
dilatation dis
ease.1,5,7"17
features
pathologic
neuropathic
myenteric
ventricular
of Veterinary
""Department
Pathology
of Medical
**Department
Microbiology
of Small Animal
***Department
Medicine
of
Medicine,
Veterinary
College
of Georgia,
University
Athens, GA 30602
Park
****Riverbanks
Zoological
500 Wildlife
Parkway
SC 29210
Columbia,
*****Zoo
800 Cherokee
Atlanta,
Atlanta
SE
Avenue,
GA 30315
tis,
and
Various
of
the
gastric dilatation
ganglioneuritis,
myositis,
infiltrative
case
the
have
reflected
the
disease,
including
of psittaciformes,
and
proventricular
psittacine
splanchnic
have
reports
phoplasmacytic
and peripheral
proventriculus
cluding
names
other
Still
encephalomyeli
in both central
inflammation
nervous tissues, especially of the
and other digestive
organs in
crop,
and
ventriculus,
small
intes
of sequelae
tine. Additionally,
the possibility
such as
other than proventricular
dilatation,
nervous
serositis and central
system (CNS) in
volvement without
gastric neuropathy, has been
Myocarditis
reported.1,14,15
served.1,2,4,5,7,10,14,15,17,19,20
also
has
been
the
Furthermore,
ob
syn
drome has been observed in psittaciformes other
than those in the family Psittacidae
(Table 1).
To
date,
the
nomenclature
does
not
Journal of the Association
until
accu
nomencla
to
to
refer
this
dilatation
proventricular
of
syn
review
this
SPECIES AND SIGNALMENT
Proventricular
dilatation syndrome has
been reported in more than 50 species of
of the
Psittaciformes,
including members
cockatoos
and
families Cacatuidae
(ie,
and
Psittacidae
lovebirds,
(ie,
cockatiels)
macaws,
parrots,
Amazon
Pacific,
South
parakeets,
conures).
Afro-Asian
have
species
characteristic
with
are
species
par
Ameri
been
lesions.1,3,4,6,7"
affected
commonly
(eg, blue and gold macaws, A ra ararauna;
African
grey
Psittacus
parrots,
erithacus),
but this may
reflect a population
rather than a species predisposition
dilatation
proventricular
lesions
gestive
two
in
have
Canada
bias
to
syndrome.
also been
geese
(Branta
Sug
reported
canaden
sis).17Other nonpsittacine birds may prove
to be susceptible as improved diagnostic
tests
A
gests
neuropathy.4,5,7,18
demonstrated
lym
current
the
for the purpose
a cause is found.
appar
dilatation
pertrophy,
proventricular
or psittacines,
and proventricular
drome
of
continue
will
as
disease
and
used
proventricular
we
can,
the syndrome including proventricular
dilatation
dilatation,
syndrome,
proventricular
dilatation
psittacine
syndrome,
proventricular
wasting
limitations
described
26
Some
describe
psittacine
the
ture,
gastric
other
psittacines
were
terms
correct
most
of this syndrome, based on
designation
be lym
findings, would
histopathologic
and en
ganglioneuritis
phoplasmacytic
we
Although
recognize
cephalomyelitis.
and
syn
le
proventricular
The
syndrome.
rots,
fading
in
general
rise
gave
and
syndrome,
it became
When
occurred
more
macaws,
cause,
wasting
macaw
wasting
of macaws.57
that
than
unknown
dilatation
of
spectrum
in birds with
sions found
dilatation
Proventricular
syndrome was first
in
1970s.15
late
the
Initially, the disease
reported
seemed to be limited to macaws. This fact, in
distension
8(2):69-75
Veterinarians
of Avian
entire
the
reflect
rately
is charac
terized by involvement of central and peripheral
nervous tissues with lymphoplasmacytic inflamma
tory infiltrates. A causative agent has not been
dilatation syndrome, al
found for proventricular
have been observed in
inclusions
virus-like
though
some affected tissues. Suspicion of proventricular
on history, clinical
dilatation
syndrome is based
evidence
and
of proventricular
signs,
radiographie
diagnosis
enlargement or dysfunction. Definitive
dilatation
syndrome requires
of proventricular
demonstration
of characteristic lymphoplasmacytic
within
nerves, ganglia, and neuropil.
infiltrates
an
with
conjunction
macaw
terms
to
the
Veterinarians
DILATATION
SUMMARY
dilatation
Proventricular
of Avian
the Association
? 1994 Association
are
developed.
review
a
that
of available
literature
of
preponderance
adults
sug
over
juveniles (3:1) is affected with proven
tricular dilatation
syndrome. Both sexes
are
equally
a
In
affected.
retrospective
study of 10,640 pet, exotic, and wild
over a 10-year period,
birds necropsied
127 (1.2%) had diagnostic histopathologic
consistent
lesions
with
proventricular
dilatation syndrome.20 Of these 127, birds
to
of known age ranged from 10 weeks
17 years (mean age, 3.8 years; median
age,
two
years).
was
Gender
determined
in 89 of these, with a ratio of 35 males
to 54 females (0.6:l).20 At the University
in a retrospective study of 35
of Georgia,
birds with
proventricular
of Avian Veterinarians VOL
8 NO
dilatation
2, 1994
syn
69
A REVIEW OF
PROVENTRICULAR
DILATATION SYNDROME
drome, the ratio of adults to juveniles (3.6:1) and
males to females (1.2:1) approximates
that reported
in the literature.3
CLINICAL SIGNS
The most common clinical signs of proventricu
lar dilatation
include depression, weight
syndrome
loss (with or without
poorer appetite), constant or
intermittent r?gurgitation, and passage of undigested
or
seeds in the feces indicating a malabsorptive
disorder.1'5"12'14'151719,28
maldigestive
muscle
paction,7,12
ment,6
atrophy,7,1014
weakness,12,14,28
lethargy,11,14,15,17
im
Proventricular
abdominal
enlarge
polyuria,9,10
have
diarrhea,9,15 scant feces,9 and hypotension14
also been reported.
CNS
Concomitant
include ataxia,
signs may
abnormal head movements,
seizures, and proprio
or motor
ceptive
deficits.1,6,8,10,14,15,19,28
Some
affected
birds
exhibit only CNS
signs.1,14,15Of 221 birds
described in the literature as having proventricular
89 had histologie
dilatation
lesions in
syndrome,
the proventriculus.
Of these 89, 77 (86.5%) showed
one or more of the four most
common
clinical
signs.
proventriculus.
CLINICAL PATHOLOGY
Clinical
laboratory
inconsistent.
findings
in affected birds are
Hypoproteinemia,9,10,18,19
hypoglycemia,9
and
anemia9,10,1718
have
been
or bacterial opportunistic
infec
reported. Mycotic
in affected birds and may compli
tion is common
the
laboratory
findings.1,2,9,10,12,1417
1, 2a,
and
2b).1,9,10,12,14,23 Ultrasonic
of
pectoral
the
muscle
esophagus,1,6
or
ventriculus,7,10,12
atrophy,7,10,14
proventriculus,1,6,7,10"
small
intestine10,14,18
and
are
The proventriculus may appear thin-walled
none
and friable (Figs 3a, and 3b).6,9,11,15
However,
of the aforementioned
radio
physical,
laboratory,
for
graphic, or gross changes are pathognomonic
dilatation
Microbial
and
proventricular
syndrome.
parasitic infections, gastrointestinal obstructions, neo
toxin
trauma, malassimilation
disorders,
plasms,
ingestion, or malnutrition may cause similar changes
70
VOL
8 NO
2, 1994 Journal of the Association
of Avian Veterinarians
tissues
finitive
remains
diagnostic
the
most
de
finding.2
HISTOPATHOLOGY
lymphoplasmacytic
gan
antemortem
However,
glioneuritis.2
common.
a. Gregory CR, Latimer KS, Ritchie BW, et al. Unpublished data. College of
Veterinary Medicine, University of Georgia, 1992-1994.
nervous
demonstrating
NECROPSY
Emaciation,1,11,15
considered.5,10'12,19
and
exami
be used to demonstrate
dilatation
the
of
impaction
proventriculus.8
Endoscopie
amination may
show impaction,
ulc?ration,
dilatation of the proventriculus.10
nation may
dilatation
12,1445,17,19
be
and
ex
Survey and contrast radiography are useful diag
in birds with proventricular
nostic techniques
dila
tation syndrome.4,9 Distension
of the proventriculus
and long transit time of barium are common find
(Figs
also
of characteristic
histopatho
in central and peripheral
lesions
logic
A presumptive diagnosis of proven
tricular dilatation
is often
syndrome
based on history,
clinical signs, and
evidence of proventricu
radiographie
lar dilatation or dysfunction. Antemor
tem
or
bippsy of the ventriculus20,23
evaluation
of
postmortem
histologie
the proventriculus
and ventriculus can
be used to confirm
the diagnosis by
ANCILLARY DIAGNOSTIC
FINDINGS
ings
must
and
Presence
heterophilia,1,9,14,17,19
cate
1. Ventral/ dorsal survey radio
di
graph of a bird with proventricular
latation syndrome. Notice the silhouette
on the right, representing the distended
Figure
techniques are invasive and potentially
fatal in sick birds. Also, small biopsy
affected
specimens may not contain
nerve
and
be
may
plexuses
nondiagnostic.23 Exarnination of affected
tissues by light microscopy
reveals
in
infiltrates
both
lymphoplasmacytic
central and peripheral nervous tissues.
Most commonly
affected are the my
enteric
laris
4b)
plexuses
of
the
tunica
in the proventriculus
and
muscu
(Figs 4a,
ventriculus.1,2,4-7,911,14,15,17,19,29
In
filtrates also may be observed in plex
uses of the crop, duodenum
(Fig 4c),
and esophagus. Conduction
fibers in
the heart also may be involved
(Fig
u.4,5,7,10,14,15,17,19
4d)
perivascular
infil
trates may be seen in affected organs.
or perivascular
cellular infil
Neural
trates may
extend
into surrounding
tissue layers. In the brain and spinal
cord,
lymphoplasmacytic
encephalitis
(Fig 4e) and myelitis may be present
with
concomitant
cuff
perivascular
?np. 1,2,4-7,9-11,14,15,17,18,22
Figure 2a and b (following). Ventral/
dorsal contrast radiographs of a bird
with proventricular dilatation syndrome
after oral administration
of barium.
In a study of 421 psittaciforme
birds submitted
16 (3.8%) had proventricular
for necropsy,
dilata
tion.11 Of these 16 birds, four had lymphoplasma
In another
cytic infiltrates in the proventriculus.
seven
of
birds
with
proven
study
psittaciforme
A REVIEW OF
PROVENTRICULAR
DILATATION SYNDROME
all seven had lym
syndrome,
in
infiltrates
the
and
phoplasmacytic
proventriculus
In
five had similar infiltrates in the ventriculus.7
seven
all
had
infil
addition,
lymphoplasmacytic
trates in the pons, medulla,
and midbrain,
three
had infiltrates in the cerebrum, and one had infil
trates in the cerebellum. Two birds had cardiac
lesions consisting of focal lymphocytic myocardi
tis and fibrosis. Of the 221 birds in the literature
described as having proventricular
dilatation
syn
tricular
dilatation
confirmation
of the dis
drome, 89 had histologie
ease. Of these 89 birds, all had lymphoplasmacytic
infiltrates in the proventriculus,
80 (89.9%) had
67
and
dilatation,
proventricular
(75.3%) had lym
phoplasmacytic
in the brain. Of
infiltrates and perivascular cuffing
the 35 birds studied at the Univer
3a and b (below). Necropsy
dilatation syndrome.
proventricular
Figure
Figure 2a. Ten minutes after gavage, the
contrast medium
is present within
the
the
and
upper portion of
proventriculus
outlines a filling defect (food).
of a bird with
Figure 3a. The liver is reflected to show the proven
tricular dilatation seen at necropsy. Notice the undi
gested seed visible through the thin-walled proven
triculus.
movement
Figure 2b. Minimal
of the
contrast medium
is observed 2 hours
later.
Figure 3b. Organs removed from the bird in figure
3a. In addition to the changes in the proventriculus,
the duodenum
is also abnormally
large.
Journal of the Association
of Avian Veterinarians VOL
8 NO
2, 1994
71
A REVIEW OF
PROVENTRICULAR
DILATATION SYNDROME
Figures 4a-4e (below). Photomicrographs of typical histo
in birds with proventricular
dilata
pathologic findings
tion
syndrome.
sity of Georgia,
findings on gross and
examination
of tissues re
histologie
vealed that 26 had lymphoplasmacytic
infiltrates in the proventriculus,
24 had
in the ventriculus,
18 had
infiltrates
in the brain, and 22 had
infiltrates
dilatation.3
proventricular
ETIOLOGY
The cause and pathogenesis of prov
entricular dilatation
syndrome are un
known. Some findings suggest that the
disease
is infectious,1,3,23,30 and if so,
transmission
of the disease by me
chanical or insect vectors,
airborne
and fecal/oral
contact would
Figure 4a. Lymphoplasmacytic
infiltrates in the nerve
the
tunica
muscularis
plexuses of
of the proventriculus.
extend
into
the
Infiltrates
surrounding tissue. H&E;
lOOx.
and direct
transmission,
all be possible etiologic
factors.1,3 Conversely,
it is possible that
dilatation
is
proventricular
syndrome
a randomly
noninfectious
occurring
disease.
The disease may occur sporadically
or may affect several psittacine birds
a
in
over
group
a
brief
period.2,20,29
occurrence, with a higher in
cidence of disease in warmer months,
has been described.2 This may suggest
an insect vector. Proventricular
dilata
tion syndrome does not develop in all
Seasonal
suggests that
exposed birds,1,20 which
some birds have
innate resistance,
immune response,
develop a protective
or become carriers. Proventricular
di
latation
acute,
syndrome
and
acute,
ever, most
4b. Higher magnification
of the proventricular
in
4a.
Notice
infiltrate
predominance
figure
of lympho
cytes and plasma cells and absence of visible neural
tissue. H&E; 400x.
Figure
after
clinical
to
viral
tion
>***<??*
?*L V-rf*
a year
signs.1'3'1014?15'1718
infection.1,4'5'7'18,19,30
has
generally
Serum
paramyxovirus
.
^:1|?
how
stages;
die within
lesions are most con
Histopathologic
sistent with an inflammatory
response
ful.2,6,7,11,19,30
NET
birds
developing
has sub
apparently
chronic
esviruses,
Viral
been
avian
herp
and
papovaviruses,
avian encephalitis
to
titers
antibody
types1"4,6'7'
avian
isola
unsuccess
virus have been nega
tive.7,22
of light and electron mi
Results
studies vary. Viral particles
croscopy
have not been seen by some investiga
tors,7,11,12,22
whereas
others
have
ob
served virus-like
inclusion bodies
in
and CNS
particles
peripheral
sues.4'19,25
Figure 4c. Lymphoplasmacytic
of the small intestine. H&E;
72
VOL
8 NO
2, 1994 Journal of the Association
infiltrates within
lOOx.
of Avian Veterinarians
ganglia
Light
microscopy
has
and
tis
shown
intranuclear and intracytoplasmic
in
clusion bodies in the myenteric
plex
uses and celiac ganglion of some af
fected birds. A distinct halo surrounds
the intranuclear
inclusions.4
A REVIEW OF
PROVENTRICULAR
DILATATION
SYNDROME
Electron microscopy
has revealed vi
rus-like particles, approximately
100 nm
in diameter,
in the spinal cords of
some affected birds.25 Mannl
and col
describe
intranuclear
inclusion
leagues
bodies near the nucleoli and intracyto
plasmic inclusion bodies near the cell
in affected neural tissues.
membranes
Both
types of inclusion bodies had
diameters of 1.5 to 3.5 |Lim and elec
tron-dense,
irregular subunits of 15 to
50 nm in diameter.
Intranuclear and
intracytoplasmic particles, ranging from
30 to 250 nm in diameter, also were
observed. Larger particles had a dis
tinct
envelope.4
4d. Infiltrates
involving myocardial
Figure
of lymphocytes and plasma cells
conduction fibers. H&E; lOOx.
intranuclear inclusion
Electron-dense,
bodies 50 to 200 nm in diameter have
in the columnar
also been reported
mu
of
the
epithelium
proventricular
cosa19 and intranuclear particles 70 to
80 nm in diameter in renal epithelium
of affected birds24; the latter may have
been an incidental finding to concur
rent adenovirus
infection. The possi
an
vector and the ultra
of
insect
bility
structural characteristics of proventricu
lar dilatation
suggest a to
syndrome
this
virus
group does
gavirus; however,
not characteristically
produce inclusion
in tissue sections or cell cul
bodies
ture.
cases of avian
The
first reported
viral serositis were birds from a group
of various psittacine
species from an
a
with
of
aviary
history
proventricular
dilatation syndrome. The only reported
association
between
the two diseases
this
from
originates
aviary. In these
it
is
reports,
speculated that avian viral
serositis and proventricular
dilatation
be
different
manifesta
syndrome may
tions
of
the
same
disease.26,31,32
How
ever, a direct relationship between the
two diseases has not been shown. Birds
with
lesions suggestive of avian viral
serositis
and experimentally-infected
chicks had lesions in the proventricu
that were histo
lus, heart, and CNS
to
similar
lesions
described
logically
in birds with
dilatation
proventricular
In
addition, hepatocellu
syndrome.26
lar and bursal lymphoid necrosis, epi
and serofibrinous
carditis,
splenitis,
ascites were present in psittacine birds
with avian viral serositis.26 Initial iso
lates from the birds with avian viral
4e. Perivascular
infiltrates or "cuffing" of lym
and
cells
in the brain. H&E; lOOx.
phocytes
plasma
Figure
suggested a togavirus,26 one which has been
speculated to be a member of the eastern encephalitis
virus complex.31 Demonstration
of a definitive
rela
between
dilatation
tionship
proventricular
syndrome
and avian viral serositis requires isolation or identi
fication of a togavirus in tissues of psittacine birds
affected with proventricular
dilatation
syndrome.
Past failures to isolate a causative agent of proven
tricular dilatation
syndrome may be explained
by
loss of a microorganism's
in tissue speci
viability
or absence of a
the
mens,
microorganism
during
chronic
of
the
disease.
it
has
stages
Alternatively,
been suggested that the neuropathic
lesions in birds
with proventricular
dilatation syndrome might be the
result of a viral-induced autoimmune response,20 similar
to the postinfectious
sequelae in human patients with
in
which
viral
measles,
damage induces inflammatory
of
neural
tissue.33
However,
damage
demyelination
of neural tissue, a sequela commonly
in
reported
humans with autoimmune neuritis, is not observed in
tissues from psittacine
birds affected with proven
tricular dilatation
syndrome
serositis
Journal of the Association
of Avian Veterinarians VOL
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2, 1994
73
A REVIEW OF
PROVENTRICULAR
DILATATION
SYNDROME
1. Avian
Table
species
to
reported
be
affected
Number
Cacat?a
moluccensis
Cacat?a
goffini
Cacat?a
sulphurea
Cacat?a
Cacat?a
roseicapillus
triton
galerita
Cacat?a
haematuropygia
Ara
auricollis
Ara
rubrogenys
macao
Ara
Anodorhyncus
severa
Ara
sulphur-crested
cockatoo
Moluccan
cockatoo
triton
lesser
militaris
Ara
Ara
spp.
maracan?
military
macaw
Ara
chlor opter a
Psittacus
erithacus
Timneh
timneh
Deroptyus
accipitrinus
roratus
Eclectus
meyeri
1
1
1
56
4
4
2
parrot
parrot
pionus
pionus
thick-billed
parrot
Amazon
blue-fronted
parrot
Amazon
leucocephala
tucumana
Cuban
Amazona
ochrocephala
Amazona
albifrons
xantholora
yellow-crowned
white-fronted
parrot
Amazon
Tucuman
parrot
Amazon
parrot
Amazon
parrot
Amazon
parrot
Amazon
yellow-lored
conure
golden
Aratinga
guarouba
Aratinga
jandaya
jenday
?enday
nanday
conure
Patagonian
sun conure
Aratinga
Aratinga
auricapilla
golden-capped
conure
conure
peach-fronted
birds,
only
89 had
histologie
parrot
conure
patagonus
solstitialis
?urea
conure
confirmation
of proventricular
THERAPY AND PREVENTION
nosis
ciation,
dilatation
disturbances.4
Morbidity
had histologically
syndrome.8,9,17
placement,
8 NO
reported
confirmed
long-term
from
occurring
survivors
have
ap
not
dilatation
as fluid
such
of antiemetics
pro
prog
ema
or CNS
but mortality
proventricular
treatment
Supportive
administration
2, 1994 Journal of the Association
The
is low,
The
for
autointoxication,
infections,
100%.4,12,22
treatment
specific
syndrome.
with
death
poor,
secondary
proaches
is no
there
remains
4
parrot
parrot
Amazona
Currently,
ventricular
1
parakeet
red-lored
221
2
grey parrot
African
grey
Jardine's
vasa
these
3
macaw
autumnalis
Of
3
white-capped
blue-headed
vasa parrot
pachyrhynca
Rhynchopsitta
aestiva
Amazona
*
3
hybrid
macaw
Meyer's
menstruus
Aratinga
5
5
macaw
red-bellied
rufiventris
guliemi
Poicephalus
Pionus
senilis
Cyanoliseus
5
parrot
Senegal
hawk-headed
parrot
eclectus
parrot
senegalus
Nandayus
39
7
macaw
grey-cheeked
parakeet
African
Amazona
1
1
green-winged
Psittacus
Amazona
A mazo na
1
cockatoo
sulphur-crested
Illiger's
pyrrhopterus
spp
erithacus
Coracopsis
1
cockatoo
macaw
hyacinth
severe macaw
Ara
Pionus
2
blue and gold macaw
macaw
yellow-collared
macaw
red-fronted
scarlet macaw
noble
Poicephalus
cockatoo
lovebird
nohilis
Poicephalus
3
2
cockatoo
red-vented
sulphurea
6
4
cockatoo
rose-breasted
hyacinthinus
Poicephalus
birds
literature*
cockatoo
cockatoo
citron-crested
Ara
Brotogeris
Psittacula
of
the
cockatiel
Goffin's
sulphurea
spp
Agapornis
Ara arar auna
in
greater
umbrella
citronocristata
Cacat?a
VOL
syndrome.
name
Common
Species
hollandicus
Nymphicus
Cacat?a
galerita galerita
Cacat?a
alba
74
dilatation
proventricular
by
re
and vitamin
of Avian Veterinarians
dilatation
syndrome.
preparations, tube or handfeeding of small
portions of liquid or semisolid diets, and
antimicrobial
in
therapy for secondary
fection may extend life for a short pe
riod
of
time.1,6,9,19
Until
agent can be identified,
sures
such
avoidance
between
as
of
quarantine
or
direct
an
infectious
preventive
of
new
indirect
mea
birds,
contact
isolated groups of psittacine birds,
seem prudent.
hygiene
and appropriate
research
Acknowledgments: Dr. Gregory's
is funded in part by Zoo Atlanta
and
Park.
Additional
Riverbanks
Zoological
funding has been provided by the Bird
Clubs of Virginia,
Inc., the Association
of Avian Veterinarians,
the International
Avian
and the
Research
Foundation,
Cowan Avian Health
Foundation,
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75