Toxoplasmosis in Atlantic Bottle-Nosed Dolphins (Tursiops truncatus) Author(s): W. Inskeep, II, C. H. Gardiner, R. K. Harris, J. P. Dubey, and R. T. Goldston Source: Journal of Wildlife Diseases, 26(3):377-382. Published By: Wildlife Disease Association URL: http://www.bioone.org/doi/full/10.7589/0090-3558-26.3.377

BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder.

BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research.

Journal

Toxoplasmosis

in Atlantic

(Tursiops

truncatus)

W. Inskeep

II,’ C. H. Gardiner,’

Pathology, Livestock Beltsville,

R. K. Harris,’

A female

(Tursiops

found

Atlantic

on

USA.

Necropsv

Picnic

Despite

Island therapy

revealed

severe

lymphadenopathv

in

her

the

in

were

Tampa

Bay,

the animals pneumonia

died. and

mother

and

the

calf,

ulcers

croscopv

and

The

eastern

of

recent

seacoast

This is the

known.

in

1

necro-

and

the

beachings

of

North

America

first

report

of

relaun-

words: Pneumonia, adrenalitis, cardiac Toxoplasma gondii, Atlantic bottledolphin, Tursiops truncatus, case report.

Infection asite many

caused

by

the

Toxoplasma gondii species of homeotherm

protozoan is

cluding Members

humans (Dubey and Beattie, of the carnivore family

are the though known, cluded.

only known definitive a variety of intermediate marine mammals are The prevalence of this

protozoan known, plasmosis richardii),

in but

marine

previous in a harbor a California

reports

include

36

the

1988,

calf

was

tissues

not

from to

found these

at two

the Departat the Armed (AFIP) for his-

topathologica! evaluation (AFIP Accession Numbers 2153586 and 2153868) Following fixation in 10% neutral buffered formalin, tissue specimens obtained

1988). Felidae

is

she died was given fluids and

Forces Institute of Pathology (Washington, D.C. 20306, USA)

in in-

hosts. Alhosts are rarely inubiquitous

mammals

dolphin

but died within severe pneumonia

dolphins were submitted ment of Veterinary Pathology

par-

common animals,

of

In January

necrosis, nosed

bottle-nosed

replacer revealed

The thymus necropsy.

toxoplasmosis

cetaceans.

Key

377-382

and lymphadenopathy in mother and calf, gastric ulcers and infection with the stomach digenean Braunina cordiformis in the mother, and a large, pale liver in the calf.

along are

Atlantic

artificial milk hr. Necropsy

was

mvonecrosis in necrosis in both

infection

dolphin

pp.

Department of Veterinary Diseases Laboratory, of Agriculture, BARCE, 33702, USA

a multivitamin injection; however, in approximately 48 hr. The calf pyrantel pamoate, penicillin, oral

tis-

gondii

pneumonia,

arid cardiac with lymphoid source

to the

in

Toxoplasma

interstitial

adrenalitis, mother and

dolphins. tionship the

immunohistochemistry

animals. with

associated

tizing

by

both

of

1990,

and her calf were found in December 1987 beached on Picnic Island in Tampa Bay, Florida (27#{176}57’N and 82#{176}27’W). The adult was given squid and fluids orally and was treated with penicillin, dexamethasone and

and infection with the stomach digenean Braunina cordiforniis in the mother, and a large, pale liver in the calf. Toxoplasma gondii was identified by light and electron migastric

the

and R. T. Goldston,3

A female

dol-

calf

26(3),

Diseases,

Dolphins

J. P. Dubey,2

bottle-nosed

and

truncatus)

beached

Florida,

sues

Wildlife

Armed Forces Institute of Pathology, Washington, D.C. 20306, USA; 2Zoonotic and Poultry Sciences Institute, Agricultural Research Service, U.S. Department Maryland 20705, USA; Animal Hospital of St. Petersburg, St. Petersburg, Florida

ABSTRACT:

phin

Bottle-Nosed

of

at necropsy by routine

were trimmed and paraffin technique

processed and sec-

tioned at S m. Sections were stained with hematoxylin and eosin for light microscopic examination. For transmission electron microscopy, selected tissues were deparaffinized, hydrated and post fixed in 1%

untoxo-

seal (Phoca vitulina sea lion (Zalophus

californianus), a West Indian manatee (Trichechus manatus) and a Northern fur seal (Callorhinus ursinus) (Van Pelt and Dieterich, 1973; Migaki et a!., 1977; Buergelt, 1983; Holshuh et al., 1985). The purpose of this report is to describe the findings in two cases of toxoplasmosis in Atlantic bottle-nosed dolphins (Tursiops

osmium tetroxide; dehydrated, cleared embedded in epoxy resin. One micron tions were cut and stained in toluidine O for preliminary light microscopic

truncatus).

interstitial

amination. were cut and In

377

lead the

and

Thin sections stained with

citrate. adult

female

pneumonia

there with

(80 to uranyl was alveolar

and secblue ex-

90 nm) acetate a diffuse ede-

378

JOURNAL

OF WILDLIFE

DISEASES,

ma and fibrinous exudation were several groups of zoites

in

and/or phages (Figs.

2,

present

the

ach; and lymphoid of both lymph

and gondii

spaces was

with

as-

degeneration; of the stom-

within glomeruli (Fig. 5). A mild depletion was present in sections lymph node and spleen. In one

were

numerous

T.

identified

and

gondii

within

of a megakaryocyte glands

macro-

cells,

m yonecrosis and tunica muscularis

node

zoites

and

myocardial

which

fibrocytes

cells,

within alveolar septa 3, 4). Toxoplasma within

sociated within

septal

muscle

the

(Fig.

lymph

6).

nodes

areas of coagulative ous tachyzoites and

tachycytoplasm

The

had

adrenal

multifocal

necrosis with numera few tissue cysts (Figs.

8, 10, 11, 12). There were areas of fibrosis within the myocardium and areas of hemorrhage and edema within lymph nodes and the spleen. 7,

Additional

lesions

not

related

to the

associated

necrotizing gastritis; mural stomach abscess

with

a superficial

(2) a chronic intracontaining adult di-

geneans with eggs identified as Pholeter gastrophilus (Fig. 9); and (3) within the dermis and subcutis, a multifocal necrotizing vasculitis with associated dermatitis and panniculitis. tozoans were and 13,

Numerous found within

without 14). In the

there lymphoid nodes

associated calf,

was and

inflammation

which

diffuse, depletion the

ciliated the skin,

was

also

(Figs. a female,

mild-to-moderate in multiple

spleen.

The

prowith

lymph

lymph nodes

was

foamy fatty the

macrophages. There change of hepatocytes,

cause

at necropsy, and tubular epithelial Transmission performed on adult. Within

of the

vacuolar cells. electron the the

pale

liver

change microscopy

was

gland of

of the adrenal

adrenal cytoplasm

noid,

numerous

tries,

a nucleus

micronemes,

granules gland

(Figs. 11, 12). Sections from the cow were also

and

a

a few few

Cats

and

other

Felidae

are

the

only

known definitive hosts for T. gondii. Intermediate hosts may be infected by (1) ingestion of sporulated oocysts, (2) ingestion of infected tissue or body fluids or (3) congenitally via the placenta. The exact source

of

the

organism

phins is unknown, the sand and coastal

in

these

two

dol-

but we speculate that water could easily be

contaminated with feline feces containing oocysts of T. gondii. In addition, flood water spillage and sewage could also serve as a source Although in the

of infection the survivability

ocean

is not

for

known,

these of the

dolphins. organism

oocysts

survive

freezing and are

and drying for several months, resistant to numerous disinfectants

(Dubey

and

Beattie,

1988).

Considering

lymph node sinuses there were occasional multinucleate giant cells and a mixed population of gram-negative bacilli. There was a diffuse subacute interstitial pneumonia with a multifocal necrogranulomatous

fish, reptiles and intermediate/transport only

bronchitis

the

bacilli

of adrenal evaluated

using a peroxidase-antiperoxidase technique and confirmed the diagnosis of toxoplasmosis (Uggla et a!., 1987) A pictoral illustration is not included herein because of the lack of contrast with the black and white photograph.

durability, survival and transmission gondii in an aquatic environment considered as a possibility. Moreover,

gram-negative

rhop-

amylopectin

had multifocal areas of necrosis with a few T. gondii tachyzoites at the interface with viable lymphoid cells. In addition, within

with

noted of renal

cortical cells parasitophorous vacuoles contamed numerous tachyzoites and a tissue cyst of T. gondii (Fig. 10). Endodyogeny was present, and the organisms had a co-

T.

gondii infection were (1) intraluminal gastric adult digeneans identified as Braunina cordiformis

1990

within large was a diffuse

(Fig. 1). There gondii tachy-

T.

pneumocytes, smooth

VOL. 26, NO. 3, JULY

etary 1984).

fish

are

common

may hosts;

known

component Transplacental most

amphibians to of

be

serve however,

a common

dolphins infections

causes

its of T. must be birds, as di-

(Greene, are one

of clinical

toxo-

of

SHORT

-

.-

-..

:

-

.#{149}

,

‘

:

..

i”e

379

..

_,

.

COMMUNICATIONS

;,#{149}:#{231} ‘

#{149} ‘....‘.“

.....“-.

‘I#{149}#{149}i”

-

““I” p

.

.,

...

#{149}..

‘

#{149}..?

p’#{149}

5,

J

.:

--:‘

.#{149}

-‘k.i

-

-

FIGURE

Fici.

RF;

Atlantic

=

RE

=

Ficu H&E. FIGi.

H&E.

2.

Tachyzoites

3.

interstitial of

dolphin.

pneumonia Toxoplasma

H&E.

Bar

in an

Atlantic

bottle-nosed

in

alveolar

septal

gondii =

dolphin. fibrocyte

H&E.

or

smooth

Bar

=

muscle

tim.

70

cell

of

an

7 m.

Tachvzoites

of

Toxoplasma

gondii

in pneumocyte

of an

Atlantic

bottle-nosed

dolphin.

H&E.

Tachvzoites

of

Toxoplasma

gondii

in pneumocyte

of an

Atlantic

bottle-nosed

dolphin.

H&E.

Tachyzoites

of

Toxoplasma

gondii

in a cardiac

of Toxoplasma

gondii

10 zm.

FIGURE Bar

Fibrinous

bottle-nosed

FIG Bar

1.

4.

10 sm. iii.:

Bar ni;

Bar

5. =

6. =

myocyte

of an

Atlantic

bottle-nosed

dolphin.

Atlantic

bottle-nosed

dolphin.

15 sm. Tachyzoites 15

m.

in

a

megakaryocyte

of

an

380

JOURNAL

OF WILDLIFE

..‘,

-.

DISEASES,

.

#{149}

I.

“I

I

,

#

VOL. 26, NO. 3, JULY

#{149}1

.,‘

...

1990

S

I I

)

‘

.r.#{149}.

,

,

..s4

,.#{149}

,.,.

‘..

Sc

#{149}1

-

#{149}‘‘

J

.3

S

S #{149}:.

“#{149}S

p Is

‘1 S.

.,

,5

-*%4#{149},.

4i

-..

.

.

‘

.

#{149}

“

#{149}‘,

0

#{149}#{149}#{149} #{149}‘#{149}#{149}#{149} #{149}

“I,,.

#{149} ,,,.#{149}t

#{149}-

I

.

‘ #{149}

4I

I’

#{149}‘..‘

...l

‘*#{149}

‘

#{149},

.

I”

.,...

#{149}.:‘

#{149}‘

‘,‘.:

‘%:#{149}.‘

Is

#{149}

#{149}

.,,;

,..

‘“

r#{149}

I.,

‘a

.,.

‘yI,,,,l,

,

..s.

.,

S

#{149}:.

#{149}#{149}:, #{149}#{149}S.

I

-

-

.

-

.

-

5’ .-.‘

ii

7.

FIGURE

of

Fic HE.

R1

8. =

Fic

ni;

‘I’ransmission

Fict conoid

ru;

Fici of

Ri;

Bar

Atlantic =

of Toxoplasma

Trematode

eggs

tachyzoites

bottle-nosed

dolphin.

Note

tachyzoites

and

tissue

cysts

15 pm.

gondii

A young

Toxoplasma

bradyzoites

11.

an Atlantic

in the

micrograph.

Brady

zoites

micronemes

12.

within

in adrenal

a chronic

of Toxoplasma

electron

(t’),

in an

I1&E.

cortical

cells

of an

Atlantic

bottle-nosed

dolphin.

pm.

10. The

(arrows).

Tachyzoites 20

9.

Note ni;

adrenalitis

gondii

Bar

dolphin. Fici dolphin.

cell

Necrotizing

Toxoplasma

(iii),

Toxoplasma

bottle-nosed

of the 3.5

=

of Toxoplasma

dolphin.

abscess

cyst

in

of

(arrows).

adrenal

dividing

cortical and

an

H&E.

cell

of

contain

Atlantic Bar

an

=

bottle-nosed 15 pm.

Atlantic

relatively

bottle-nosed

organelles.

fewer

pm.

in adrenal

granules undergoing

stomach

macrophages

cyst are

gondii

amvlopectin gondii

within

tissue

gondu

center Bar

intramural

gondii

(a).

endodyogeny.

Transmission

cortical

Transmission electron

cell

in an

electron

Atlantic

bottle-nosed

micrograph.

Toxoplasma

gondii

micrograph.

Bar

Bar

within =

0.7

dolphin; =

an adrenal pm.

0.5

pm.

cortical

SHORT

FIGURE

(arrow).

13.

Necrotizing

vasculitis

in panniculus

of

an

Atlantic

bottle-nosed

COMMUNICA11ONS

dolphin;

ciliated

381

protozoan

H&E.

FIGURE

14.

Ciliated

H&E.

(arrow).

plasmosis

Bar

in

protozoan

in

dermal

connective

tissue;

large,

note

dark

macronucleus

and

cilia

15 pm.

=

many

animals

including

hu-

The

necrotizing

lesions

observed

in this

mans. This may have been the route of infection for the calf. During the extraintestinal (parenteral) stage of the T. gondii life cycle, tachyzoites multiply in nearly any type of host

case are similar to those seen in other species where target organs such as lung, lymphoid tissue and heart are affected. Although the pathological

majority lesions

cell tie,

bottle-nosed by T. gondii,

dolphins were the relationship,

resulting 1988).

in necrosis Previous

mammal toxoplasmosis presence of the parasite including: brain, spinal renal in a northern fur Indian

manatee;

(Dubey reports

and Beatof marine

document the in multiple organs cord, heart and adseal; brain in a West

heart

and

stomach

in

et

rich,

1973).

fection organism

al., In

1977;

Van

most

animals

is usually subclinical; may cause severe

lesions in immunodeficient immunocompromised The

thymus

herein fact,

was not combined

of

the

Pelt

a

Diete-

T. gondii however, symptoms

neonates

dolphin

and

fetuses or calf

inthe and

or in adults.

Martie John

Collard,

clearly

Robin-Anne

Jenkins

for

histoAtlantic caused if any, to

partment

of

C.

cephalitis the

assistance.

and The

contained herein are the authors and are official or as reflectDepartment of the Force or of the De-

Defense. LITERATURE

BUERGEI.T,

Ferris,

technical

opinions or assertions the private views of not to be construed as ing the views of the Army, Navy, or Air

reported

found at necropsy. This with the lesions found in

the lymph nodes and spleen, suggests that the calf may have been immunocompromised. In addition, there were less severe lesions of lymphoid depletion in the adult female.

significant these two

the recent dolphin beachings along the eastern seacoast of North America is unknown. We wish to express our appreciation to

California sea lion; and liver in a harbor seal (Holshuh et a!., 1985; Buergelt, 1983; Migaki

of in

D.

1983.

Toxoplasmic

in a West

American

CITED

Indian

Veterinary

meningoen-

manatee. Medical

Journal

of

Association

18.3:

1294-1296. DUBEY,

J.

P.,

AND

mosis

of animals

Raton,

Florida,

GREENE,

C.

E.,

AND

C.

P.

220 A.

1988.

BE.ATTIE.

and

man.

CRC

Press,

ToxoplasInc.,

Boca

pp. K.

PRI.;sTwooD.

1984.

Coc-

382

JOURNAL

cidial

OF WILDLIFE

infections.

In

infectious diseases (ed).

W.

F.

H.

the

dog

Saunders

J.,

pp. 826. A. E. SHERROD,

ANDREWS,

ANI)

American

VOL. 26, NO. 3. JULY

microbiology

and

cat,

C.,

J.

Toxoplasmosis

38:

A.,

AI.1.EN,

C.

northern

R.

TAYLOR,

1985.

fur seal.

Medical AND

in a California

S.

L.

Journal

Association

in fetuses

B.

ican

Toxo-

SJOLAND,

of 187:

VAN

PELT,

R.

H.

W.

CASEY.

sea

lion

1977.

(Zalophus

fetal

P.

W.,

AND

seal.

of sheep. Research

R.

A.

for

publication

17 July

48:

DIETERRH.

and

Journal

1987.

DUBEY.

toxoplasmosis of

Wildlife

9: 258-261.

Received

Veterinary

of toxoplasmosis

membranes

infection

harbor

J.

AND

of Veterinary

Staphylococcal

of

diagnosis

and

Journal

Journal

135-136.

Immunohistochemical

young F.

American

Research UGGLA,

1229-1230. MIGAKI,

californianus).

and

Philadelphia,

E. B. How.xRD.

Veterinary

1990

C. E. Greene

Company,

in a feral

plasmosis

Clinical

of the

B.

Pennsylvania, HoLsIIt’H,

DISEASES,

1989.

Amer348-351. 1973.

in a Diseases