Content uploaded by Ellis Greiner
Author content
All content in this area was uploaded by Ellis Greiner
Content may be subject to copyright.
706
Journal of Wildlife Diseases, 27(4), 1991, pp. 706-709
©Wildlife Disease Association 1991
Nasitrema sp.-associated Encephalitis in a Striped Dolphin
(Stenella coeruleoalba) Stranded in the Gulf of Mexico
Thomas J. O’Shea,’ Bruce L Homer,2 Ellis C. Greiner,3 and A. William Layton,2 ‘U.S. Fish and Wildlife Service,
National Ecology Research Center, Gainesville Field Station, 412 NE 16th Ave., Gainesville, Rorida, 32601,
USA; 2Department of Comparative and Experimental Pathology, College of Veterinary Medicine, Box J-145 JHMHC,
University of Rorida, Gainesville, Rorida 32610, USA; 3Department of Infectious Diseases, College of Veterinary
Medicine, Box J-137 JHMHC, University of Florida, Gainesville, Ronda 32610, USA
ABSTRACT: An immature female striped dol-
phin (Stenella coeruleoalba) found dead on a
northwestern Florida beach in 1988 exhibited
severe inflammation bilaterally in the dorsal and
mid-thalamus in association with adult trema-
todes (Nasitrema sp.) and trematode eggs. Nu-
merous specimens of Nasitrerna sp. also were
present in the pterygoid sinuses. Pneumonia in
association with a heavy growth of Vibrio dam-
sela was observed also. This report confirms the
occurrence of Nasitrema sp. -associated enceph-
alitis in striped dolphins and in small cetaceans
from the Gulf of Mexico.
Key words: Brain, case history, encephali-
tis, Nasitrema sp., pathology, Stenella coeru-
leoalba, striped dolphin, Vibrio.
Brain lesions produced by parasitic
trematodes of the genus Nasitrema have
been implicated as a cause of death in sin-
gle strandings of small cetaceans along the
Pacific coast of North America (Parker et
al., 1977; Dailey and Walker, 1978; Cowan
et al., 1986; Lewis and Berry, 1988). Na-
sitrerna sp. -associated encephalitis has not
been confirmed for striped dolphins (Ste-
nella coeruleoalba) and is not well known
in marine mammals from the Gulf of Mex-
ico. In this report we implicate brain le-
sions associated with Nasitrerna sp. as a
major factor in the death of a striped dol-
phin from northwestern Florida.
An immature female was found dead at
Panama City Beach (30#{176}10’SO”N,
85#{176}49’05”W)on 8 November 1988. Time
since death was unknown, but little de-
composition was evident. The carcass was
kept under ice during transport to the Uni-
versity of Florida College of Veterinary
Medicine (Gainesville, Florida 32610,
USA), where a necropsy was conducted
about 24 hr later. Weight was 53.5 kg.
Total length was 173 cm. The most sig-
nificant gross findings were related to
trematode infection. We counted 43 trem-
atodes (Nasitrema sp.) in the right pter-
ygoid sinus and 71 in the left. The mucosa
had multiple erosions associated with at-
tachment of the trematodes. A single Na-
sitrema sp. was noted in the trachea.
The brain was removed and immersed
in 10% neutral buffered formalin. Serial
coronal sections of the fixed brain revealed
multiple 0.5 to 2.0 cm diameter, irregu-
larly shaped brown cavitated areas of ne-
crosis in the right and left dorsal to mid-
thalamic regions and parietal cortices (Fig.
1). Cavitated areas contained several 0.5
x0.25 cm flattened fragments of trema-
todes identified as Nasitrema sp. The left
dorsal thalamus also contained dark brown,
interlacing streaks. Lungs were meaty
(weight 1.8 kg) and were mottled red, pur-
ple and tan with reddened cut surfaces. A
moderate ulcerative gastritis was present
in the pylorus. Other organs had parasitic
or incidental lesions at gross necropsy.
Tissues were fixed in 10% neutral buf-
fered formalin, embedded in paraffin, thin
sectioned at 6 &m, stained with hematox-
ylin and eosin, and examined with light
microscopy. The most significant micro-
scopic lesions were present in the brain.
Areas of cavitated brain contained large
cystic foci of liquefactive necrosis bor-
dered by diffuse infiltrates of macrophages
with fewer hemosiderophages, clusters of
lymphocytes and scattered multinucleated
giant cells (Figs. 2,3). Many glial cells were
present. Sections of Nasitrema sp. were
characterized by a thin tegument with seg-
mental spine-covered areas, an acetabu-
lum, an oral sucker, and absence of a coe-
FIGURE 1. Irregular cavitated area (arrow) in the
right dorsal thalamus of a striped dolphin. Lateral
ventricle is below this area in the figure. The crevice
on the bottom right is an artifact. Formalin-fixed gross
specimen.
FIGURE 2. Section through a cavitated area of a
striped dolphin brain containing a Nasitrerna sp.
trematode. The surrounding neuropil is hypercellular
due to infiltrates of macrophages and lymphocytes,
and increased numbers of glial cells. H&E.
SHORT COMMUNICATIONS 707
lom (Fig. 2). Most internal structures were
indistinct (because of necrosis) and much
of the tegument was covered by macro-
phages and multinucleated giant cells.
There were also numerous oval or trian-
gular eggs (60 to 80 sm the long axis) with
an approximately 6 to 8 m wide refrac-
tile, slightly birefringent golden brown wall
(Fig. 3). A single operculum was some-
times identified. Most eggs were fractured
and/or distorted and many were partially
encompassed by multinucleated giant cells.
Capillaries within the lesion were hyper-
plastic and had degenerate (basophilic)
walls. Scarred areas of brain contained
proliferations of fibrous astrocytes. The
surrounding parenchyma contained nu-
merous vacuoles, increased numbers of
glial cells, and scattered swollen axons.
Other significant microscopic alter-
ations included a chronic hyperplastic
pterygoid sinusitis associated with trema-
tode eggs in the underlying stroma, as de-
scribed in the brain. The lungs had a sub-
acute, moderate, m ultifocal bronchointer-
stitial pneumonia. Trematode (not iden-
tified, but morphologically distinct from
Nasitrerna sp.)-associated pancreatitis and
periportal hepatitis were present also.
Bacteriological studies yielded heavy
growth of a pure isolate of Vibrio damsela
from a section of lung obtained aseptically
at necropsy. Recovery and identification
of the microorganism followed standard-
ized laboratory protocol. The lung sample
was minced, and planted on a Columbia
agar plate with 5% sheep blood, a
MacConkey plate, and a Columbia CNA
(colistin nalidixic acid) agar plate with 5%
sheep blood. After a 24-hr incubation pe-
nod at 35 C with 5% CO2, the plates were
evaluated and it was determined that the
only growth was an oxidase-positive, Gram-
negative, non-enteric, slightly curved rod.
Further identification was pursued using
an API rapid NFT identification system.
This system is designed to classify non-
fermentative organisms and some fer-
menters not belonging to the Enterobac-
teriaceae, such as the vibrios.
The presence of adult Nasitrema sp. or
Nasitrerna sp.-like eggs in association with
lesions in the brain has been reported for
common dolphins (Del phinus delphis),
Pacific white-sided dolphins (Lageno-
rhynchus obliquidens), Dall’s porpoises
(Phocoenoides dalli), and northern right
whale dolphins (Lissodelphis borealis), all
from the Pacific coast of North America
(Parker et al., 1977; Dailey and Walker,
1978; Cowan et al., 1986; Lewis and Berry,
1988). Forrester (1991) reviewed four un-
published case reports from the files of The
University of Florida College of Veteri-
FIGURE 3. Fractured and distorted triangular and oval trematode eggs surrounded by infiltrates of
macrophages, lymphocytes, multinucleated giant cells (arrows), and increased numbers of glial cells within
a striped dolphin brain. Part of a Nasitrema can be seen adjacent to this area. H&E.
708 JOURNAL OF W1LDLIFE DISEASES, VOL. 27, NO 4, OCTOBER 1991
nary Medicine which also indicate the oc-
currence of trematode-associated enceph-
alitis in small cetaceans from the Gulf of
Mexico. These reports were based on
strandings of one striped dolphin, one
rough-toothed dolphin (Steno bredanen-
sis), and two pantropical spotted dolphins
(Stenella attenuata). Strandings occurred
between 1980 and 1985 on northwestern
Florida beaches within 150 km of the 1988
striped dolphin stranding. Associated pa-
thology was similar to the case reported
above. Numerous trematode eggs were
noted, but only one intact adult was ob-
served microscopically. It appeared mor-
phologically similar to Nasitrerna, but its
identification was not confirmed (Forres-
ter, 1991). Encephalitis associated with
Cam pula sp. has been reported in small
cetaceans, but the diagnosis of Cam pula
sp. was based on the morphology of the
eggs in the brain (Ridgway and Dailey,
1972; Sweeney and Ridgway, 1975). How-
ever, it is now recognized that the eggs of
both Nasitrema sp. and Campula sp. are
similar morphologically, and when adult
trematodes have been found in the brains
of cetaceans only Nasitrema sp. has been
identified (Parker et al., 1977; Howard et
al., 1983).
Nasitrerna sp. -associated lesions have
been suggested to be a cause of strandings
and deaths of some small cetaceans from
the Pacific coast. However, it has not al-
ways been clear whether the trematode
infection in the brain also debilitated the
animal, leading to death from some sec-
ondary cause, or other events weakened
the animals and allowed the parasites to
invade the brain (Cowan et al., 1986). Both
scenarios are possible, and generalizations
beyond each specific case are inappropri-
ate. Nasitrema sp. normally reside in the
air sinuses of small cetaceans. Cowan et al.
(1986) suggested that aberrant migration
of Nasitrerna occurs directly from the air
sinus-inner ear complex to the subdural
space and that this migration is due to
SHORT COMMUNICATiONS 709
other complicating factors that disturb the
host-parasite relationship. In contrast to
findings in stranded individuals, many
clinically normal small cetaceans taken in
fishing nets have a high prevalence of Na-
sitrerna sp. infection in the sinuses without
the presence of adults or eggs in the brain
(Dailey and Walker, 1978; Cowan et al.,
1986). In addition to encephalitis, the fe-
male striped dolphin we examined also had
a subacute pneumonia, which was less
chronic than the encephalitis, indicating
that the pneumonia developed after the
onset of encephalitis. Vibrio damsela was
the only bacterium isolated from the lung,
and we speculate that it is likely to have
been the cause of the pneumonia. This or-
ganism has apparently not been reported
previously in association with pneumonia
in striped dolphins, although other species
of Vibrio have been isolated from tissues
of four other species of cetaceans (Dailey,
1985). Vibrio damsela is a common bac-
terium in Gulf waters and its presence is
normally non-pathogenic. However, it has
also been reported to be a primary patho-
gen causing infections of wounds in bot-
tlenose dolphins, Tursiops truncatus (Fu-
jioka et al., 1988). In this particular case
severity and duration of lesions suggest that
the encephalitis resulted in debilitation of
the striped dolphin, which in turn resulted
in pneumonia, seemingly due to a Vibrio
damsela infection. Both the encephalitis
and pneumonia contributed to the cause
of death.
Personnel of the Gulf World aquarium
in Panama City notified us of the strand-
ing. J. Gore, Florida Game and Fresh Wa-
ter Fish Commission, expedited transfer
of the carcass. C. Beck and R. Bonde pro-
vided critical assistance at necropsy. R.
Appy verified the identification of Nasi-
trerna. B. Punch, University of Florida
Veterinary Medical Teaching Hospital, in-
terpreted microbiological results. D.
Forrester and C. Beck reviewed the manu-
script. The dolphin was recovered through
the Southeastern U.S. Marine Mammal
Stranding Network, under authorization
of the National Marine Fisheries Service.
LITERATURE CITED
COWAN, D. F. ,W. A. WALKER, AND R. L. BROWNELL,
JR. 1986. Pathology of small cetaceans stranded
along southern California beaches. In Research
on dolphins, M. M. Bryden and R. Harrison (eds.).
Oxford University Press, Oxford, England, pp.
323-367.
DAILEY, M. D. 1985. Diseases of Mammalia: Ce-
tacea. In Diseases of marine animals, Vol. IV,
Part 2, 0. Kinne (ed). Biologische Anstalt Hel-
goland, Hamburg, Germany, pp. 805-847.
,AND W. A. WALKER. 1978. Parasitism as
a factor (?) in single strandings of southern Cal-
ifornian cetaceans. The Journal of Parasitology
64: 593-596.
FORRESTER, D. J. 1991. Parasites and diseases of
wild mammals in Florida. University of Florida
Press, Gainesville, Florida. In press.
FUJIOKA, R. S. ,S. B. GRECO, M. B. CATES, AND J. P.
SCHROEDER. 1988. Vibrio damsela from
wounds in bottlenose dolphins Turslops trun-
catus. Diseases of Aquatic Organisms 4: 1-8.
HOWARD, E. B. ,J. 0. BRITT, AND G. MATSUMOTO.
1983. Parasitic diseases. In Pathobiology of ma-
rine mammals, Vol. 1, E. B. Howard (ed). CRC
Press, Boca Raton, Florida, pp. 119-232.
LEWIS, R. J. ,AND K. BERRY. 1988. Brain lesions in
a Pacific white-sided dolphin (Lagenorhynchus
obliquidens). Journal of Wildlife Diseases 24:577-
581.
PARKER, G. A., G. MIGAKI, AND W. A. WALKER.
1977. Cerebral trematodiasis in a dolphin. Mil-
itary Medicine 142: 861-871.
RIDGWAY, S. H., AND M. D. DAILEY. 1972. Cerebral
and cerebellar involvement of trematode para-
sites in dolphins and their possible role in strand-
ings. Journal of Wildlife Diseases 8: 33-43.
SWEENEY, J.C., AND S. H. RIDGWAY. 1975. Com-
mon diseases of small cetaceans. Journal of the
American Veterinary Medical Association 167:
533-540.
Received for publication 25 February 1991.
