Journal

of Wildlife

Diseases,

27(4),
Disease

1991,

Wildlife

pp. 706-709 Association 1991

Nasitrema sp.-associated (Stenella coeruleoalba)

Thomas J. OShea, Bruce L Homer,2

Encephalitis in a Striped Dolphin Stranded in the Gulf of Mexico

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 trematodes (Nasitrema sp.) and trematode eggs. Numerous specimens of Nasitrerna
sp.

nificant trematode atodes ygoid had tachment sitrema The in 10% coronal multiple larly sinus

gross findings infection. We (Nasitrema and sp.) 71 in the erosions

were counted in the left.

related to 43 tremright The with A single trachea. ptermucosa atNa-

multiple

associated

also

were

present
association sela was

in the
with observed

pterygoid

sinuses.

Pneumonia

in

a heavy growth of Vibrio damalso. This report confirms the occurrence of Nasitrema sp. -associated encephalitis in striped dolphins and in small cetaceans
from

of the sp. was brain neutral was

trematodes. noted in the removed buffered

and formalin.

immersed Serial revealed irreguof ne-

Key
tis,

the Gulf words:

of Mexico. Brain, case

sp., pathology,

sections of the fixed brain 0.5 to 2.0 cm diameter, shaped brown cavitated areas

Nasitrema leoalba, striped

dolphin,

history, encephaliStenella coeruVibrio. by parasitic

Brain

lesions

produced

trematodes of the genus Nasitrema have been implicated as a cause of death in single strandings of small cetaceans along the Pacific al., 1977; et al., sitrerna been coast Dailey Lewis for 1986; confirmed of North and and America Walker, Berry, encephalitis (Parker 1978; 1988). has Cowan Nanot et

crosis in the right and left dorsal to midthalamic regions and parietal cortices (Fig. 1). Cavitated areas contained several 0.5 x 0.25 cm flattened fragments of trematodes dorsal (weight ple and moderate identified thalamus 1.8 kg) tan with ulcerative Other lesions fixed as Nasitrema also contained streaks. and Lungs were reddened gastritis organs at gross in 10% cut mottled was sp. The left dark brown, were red, surfaces. present had parasitic necropsy. neutral bufin paraffin, thin with hematoxwith light microbrain. large borof were were significant meaty purA

interlacing

sp. -associated

nella

coeruleoalba)

in marine mammals ico. In this report

sions associated

striped dolphins (Steand is not well known from the Gulf of Mexwe implicate brain leNasitrerna death Florida. was found
sp. as a

in the pylorus. or incidental Tissues were fered formalin, sectioned at ylin scopic Areas cystic dered with and microscopy.

with in the

embedded 6 &m, stained and The most examined

major

factor

of a striped dead

dolat

eosin,

phin from northwestern An immature female Panama City Beach

(30#{176}10SON, but 1988. Time little decarcass to the Veterinary 32610, kg. sig706

lesions were of cavitated foci fewer of by diffuse and

present in the brain contained necrosis

85#{176}4905W)on 8 November since death was unknown, composition kept under

versity

liquefactive infiltrates scattered

of macrophages clusters multinucleated cells sp.

was evident. The ice during transport Florida (Gainesville, College of Florida

was
Uni-

hemosiderophages,

lymphocytes

of

Medicine USA), about Total

giant cells (Figs. 2,3). Many glial present. Sections of Nasitrema characterized mental lum, an oral by a thin tegument spine-covered sucker, and areas, absence an

where 24 hr length

a necropsy was conducted later. Weight was 53.5 was 173 cm. The most

with segacetabuof a coe-

SHORT

COMMUNICATIONS

707

FIGURE

1.

Irregular

cavitated

area

(arrow)

in

the

FIGURE

right ventricle on the

specimen.

dorsal bottom

thalamus is below right this

of area

a striped in the

dolphin. figure. Formalin-fixed The

Lateral crevice gross

striped
trematode. due and to

2. dolphin
The infiltrates

Section brain
surrounding of numbers

through a cavitated area containing a Nasitrerna

neuropil and cells. of glial is hypercellular lymphocytes, H&E. macrophages

of a
sp.

is an artifact.

increased

lom (Fig. indistinct

of

2). Most (because

internal structures of necrosis) and

were much

the tegument was covered by macrophages and multinucleated giant cells. There were also numerous oval or triangular eggs (60 to 80 sm the long axis) with an tile, approximately slightly
3). A

necropsy. Recovery and identification of the microorganism followed standardized laboratory protocol. The lung sample was minced, and planted on a Columbia at agar (colistin

plate

with

5%

sheep a Columbia agar plate

blood,

MacConkey sheep

6 to 8 m birefringent
single

wide brown
was

refracwall
some-

plate, and nalidixic acid) After

CNA with 5% pewere that the Gramrod. using

golden
operculum

blood.

a 24-hr

incubation plates

( Fig.
times

identified. distorted within had

Most and

eggs many

were were

fractured partially giant cells.

nod at 35 C with 5% evaluated and it was only growth was negative, Further non-enteric, identification

CO2, the determined

and/or
encompassed

an oxidase-positive, slightly curved was pursued

by multinucleated and Scarred

Capillaries
plastic

walls.
proliferations

the lesion were hyperdegenerate (basophilic) areas of brain contained of fibrous astrocytes. The contained
numbers

surrounding
merous vacuoles,

parenchyma
increased

nuof

an API rapid This system fermentative menters not teriaceae, such

NFT identification system. is designed to classify nonorganisms and some ferbelonging to the Enterobacas the vibrios. Nasitrema in association been reported
sp. or

glial cells, and Other ations

pterygoid significant

scattered a chronic

swollen

axons. alter-

microscopic

The presence of adult Nasitrerna sp.-like eggs lesions common Pacific rhynchus in the brain has

with for

included

hyperplastic

sinusitis associated with trematode eggs in the underlying stroma, as described in the brain. The lungs had a subacute, moderate, m ultifocal

bronchointer(not distinct
pancreatitis

dolphins (Del phinus delphis), white-sided dolphins (Lagenoobliquidens), Dalls porpoises (Phocoenoides dalli), and northern right (Lissodelphis coast of borealis), all North America

stitial tified,

pneumonia. Trematode but morphologically

idenfrom

whale dolphins from the Pacific

Nasitrerna sp.)-associated periportal hepatitis were Bacteriological studies

present yielded

and also. heavy

(Parker et al., 1977; Dailey and Walker, 1978; Cowan et al., 1986; Lewis and Berry, 1988). Forrester (1991) reviewed four unpublished University case of reports Florida from the College files of The of Veteri-

growth of a pure isolate of Vibrio damsela from a section of lung obtained aseptically

708

JOURNAL

OF W1LDLIFE

DISEASES,

VOL. 27, NO 4, OCTOBER

1991

FIGURE macrophages,

3.

Fractured lymphocytes,

and

distorted multinucleated

triangular giant cells

and

oval (arrows),

trematode and

eggs increased

surrounded numbers of

by

infiltrates

of

glial

cells

within

a striped

dolphin

brain.

Part

of a

Nasitrema

can

be seen

adjacent

to this area.

H&E.

nary

Medicine

which

also

indicate from were

the enceph-

ocof on

both similar

Nasitrema

sp.

and

Campula

sp.

are

currence

of trematode-associated

alitis in small cetaceans Mexico. These reports

the Gulf based

morphologically, and trematodes have been found of cetaceans only Nasitrema

when adult in the brains sp. has been

strandings of one striped dolphin, one rough-toothed dolphin (Steno bredanensis), and two pantropical spotted dolphins (Stenella between Florida striped thology attenuata). 1980 and beaches dolphin
was

Strandings occurred 1985 on northwestern 150 km the of the 1988 Associated pacase reported

identified (Parker et al., 1977; Howard et al., 1983). Nasitrerna sp. -associated lesions have been suggested to be a cause of strandings and the
ways

within

deaths Pacific been

of some small coast. However, clear in the whether brain to death or other also

cetaceans it has the from events debilitated

from not althe

stranding. similar to

trematode some secweakened to Both

infection animal, ondary

above. Numerous trematode eggs were noted, but only one intact adult was observed microscopically. It appeared morphologically similar to Nasitrerna, but its identification was not confirmed (Forrester, 1991). Encephalitis
sp.

leading cause,

the animals and allowed the parasites invade the brain (Cowan et al., 1986). scenarios are possible, and generalizations beyond each specific case are inapproprireside Cowan ate. Nasitrema sp. normally air sinuses of small cetaceans. (1986) suggested that aberrant of Nasitrerna occurs directly sinus-inner ear complex to space and that this migration

associated in

with small

Cam
sp. eggs
1972;

pula
was in

cetaceans,

has been reported but the diagnosis of based on the morphology the brain and (Ridgway Ridgway, that

Cam
of

pula
the

in the et al.

Sweeney it is now

and Dailey, 1975). Howthe eggs of

migration from the air the subdural is due to

ever,

recognized

SHORT

COMMUNICATiONS

709

other complicating factors host-parasite relationship.

findings in

that In

disturb contrast

the to

Veterinary terpreted Forrester

script.

Medical Teaching microbiological and The C. Beck was U.S. Marine

LITERATURE

Hospital, results. the manuthrough Mammal authorization Service.

inD.

clinically fishing sitrerna nets

sp.

stranded normal small have

infection

individuals, cetaceans prevalence sinuses

in the

many taken in of Nawithout

reviewed recovered Marine under Fisheries

CITED
AND

dolphin Network,

a high

the of the

Southeastern National

Stranding

the presence (Dailey and 1986). male

a chronic subacute

of adults Walker, dolphin

pneumonia,

or eggs in the brain 1978; Cowan et al., to encephalitis, we examined which the also fehad

In striped

addition

COWAN, JR.

D. F. , W. A.
1986.

WALKER,

R. L.
cetaceans

BROWNELL,

that
onset

the
of

than the pneumonia

encephalitis.

encephalitis, developed Vibrio isolated that from

was less indicating after the was lung, have orto This the

Pathology

of small

stranded

damsela

along southern California on dolphins, M. M. Bryden Oxford University Press,

323-367.

beaches. In Research and R. Harrison (eds.). Oxford, England, pp.

the and been

ganism

only we the

bacterium speculate cause has

in

it is likely pneumonia.

of the
association

apparently dolphins, have been

previously in striped

not been reported with pneumonia although isolated other from species tissues

DAILEY, M. D. 1985. Diseases of Mammalia: Cetacea. In Diseases of marine animals, Vol. IV, Part 2, 0. Kinne (ed). Biologische Anstalt Helgoland, Hamburg, Germany, pp. 805-847. , AND W. A. WALKER. 1978. Parasitism as a factor (?) in single strandings of southern Californian cetaceans. 1991. in Florida. Florida. M. 1988. The Journal Parasites In of and press. Parasitology diseases of Florida of

of

Vibrio

of four 1985). terium normally also been gen tlenose jioka

severity

other species of cetaceans (Dailey, Vibrio damsela is a common bacin Gulf waters and its presence is non-pathogenic. reported to be infections Tursiops In resulted dolphin, which seemingly infection. Both contributed of the City Florida Gulf Game World and this 1988). duration of dolphins, et al., and However, a primary wounds truncatus particular suggest in debilitation in turn resulted due to a Vibrio the encephalitis to the
cause

64: 593-596. FORRESTER, D. J.

wild Press,
FUJIOKA,

mammals Gainesville,

University B. CATES,

it has pathoin bot(Fucase that of

causing

of lesions

the

encephalitis

the striped in pneumonia, damsela and of death. Personnel in Panama ing. ter pneumonia

AND J. P. damsela from wounds in bottlenose dolphins Turslops truncatus. Diseases of Aquatic Organisms 4: 1-8. HOWARD, E. B. , J. 0. BRITT, AND G. MATSUMOTO. 1983. Parasitic diseases. In Pathobiology of marine 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-

R. S. , S. B. GRECO,

SCHROEDER.

Vibrio

581.
PARKER,

G.

A.,
Cerebral

G.

MIGAKI,

AND

W.

A.

WALKER.

1977.
itary RIDGWAY,

trematodiasis
AND

in a dolphin. 1972. of possible Diseases trematode role 8: 33-43. 1975. Journal

Association

Mil-

aquarium strandWaFresh

Medicine S. H.,
cerebellar
in

142: 861-871. M. D. DAILEY.

involvement and their

Cerebral parain strandComof the 167:

notified

us of the

and
sites

J.

Gore,

dolphins of
AND

Fish Commission, of the carcass. C. Beck vided Appy trerna. critical verified B. Punch, assistance the

expedited transfer and R. Bonde proat necropsy. of of NasiFlorida R.

ings.
SWEENEY,

Journal

Wildlife S. H. small

J. C.,
diseases

RIDGWAY.

mon
American 533-540.

of
Veterinary

cetaceans.
Medical

identification University

Received

for

publication

25 February

1991.