Download Diseases of Marine Mammals April 9, 2001 Robert B. Moeller, Jr

Diseases of Marine Mammals
April 9, 2001
Robert B. Moeller, Jr. D.V.M.
California Animal Health and Food Safety Laboratory System
University of California
Tulare, California 93274
[email protected]
559-688-7543
The author of this lecture wishes to thank Drs. Migaki, Sweeney, Keyes, Walker, Montali, Magee,
Albert, Stroud, McNeil, Hammond, Barr, Gage, Wilson, Britt, Domingo, Haines, Garner, Gulland,
Wada, Lapointe, and Martineau for supplying photographs of the various diseases of marine mammals to
the Registry of Veterinary Pathology.
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Viral Diseases
1.
Pox Virus
A. Dolphin Pox
Dolphin pox is also known as "tattoo." Clinically, this disease is characterized by prominent welldelineated lines of hyperpigmentation of the epidermis with various design patterns. These design
patterns have been described as targets, circles, and pinhole lesions. The lesions are usually smooth and
flat, but may be raised. They are primarily located on the dorsal body, flippers, dorsal fins, and fluke.
Although this virus does not appear to cause serious illness in cetaceans, the development of these
lesions usually coincides with periods of poor health and stress.
Histologically, the lesion consists of ballooning (hydropic) degeneration of the deep layers of the
stratum intermedium. Irregularly shaped or round variably size intracytoplasmic inclusions are present
in the cells undergoing ballooning degeneration. The stratum externum may become thickened.
Minimal inflammation is observed; this maybe the reason for persistence of the lesion. The cause of the
hyperpigmentation is unknown, but there are various theories on this process. One theory is that
stimulation of the dermal melanocytes by the viral infection causes hyperpigmentation of the dermis and
epidermis. Another theory postulates that damage to the stratum externum and intermedium leads to
filling in of these defects with debris and bacteria which then causes the discoloration of the epidermis.
This is an unusual pox lesion since it is not a proliferative lesion. The virus persists for long
periods of time in the epidermis and slowly spreads on the affected animal. Affected animals appear to
not develop antibodies to the virus; however, once antibodies develop to the pox virus, the lesion
regresses with the affected skin becoming raised and bleached. The effected skin then undergoes
necrosis and sloughing. Scraping the lesion has been known to cause regression. If lesions are biopsied,
the pox lesion may regress in a zonal pattern around the biopsy site.
B. Seal Pox
Seal pox is a parapoxvirus that is known to affect numerous species of pinnipeds. An orthopox
has also been isolated from a grey seal, (Halichoerus grypus). The disease is most prevalent in
California sea lions, South American sea lions and harbor seals. Cutaneous spread of this disease is
mostly by head and neck rubbing, a common social behavior of sea lions and other pinniped. This viral
disease is rarely fatal, but can cause a high morbidity. Infected animals may demonstrate clinical disease
for up to 15 weeks.
Seal pox is a proliferative lesion characterized by the formation of numerous 2 to 3 cm cutaneous
nodules. These nodules eventually ulcerate and are slow to heal. Areas of alopecia develop over the
healed areas. The lesions are most numerous over the head and neck but can occur anywhere on the
body.
Microscopically, the lesion is characterized by ballooning degeneration of the stratum spinosum
with pustule formation. Affected cells have one or two eosinophilic intracytoplasmic inclusions 2 to 15u
in diameter. The affected epidermis is acanthotic with orthokeratotic and parakeratotic hyperkeratosis.
Inflammation can be prominent, especially during regression of the lesion.
The histologic features of pox virus in South American sea lions are unique with a downward
proliferation of the epidermis with ulceration and pustule formation. In affected epithelial cells, only
one large eosinophilic or basophilic intracytoplasmic inclusion body is observed. These inclusions are
usually surrounded by a thin halo and the nucleus is compressed. These lesions can occasionally
resemble the human disease molluscum contagiosum.
2.
San Miguel Sea Lion Virus
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San Miguel sea lion virus (SMSV) is caused by a calicivirus. This calicivirus is believed to be the
viral agent responsible for vesicular exanthema of swine. Most viral strains of San Miguel sea lion virus
are antigenically related to vesicular exanthema of swine. The disease occurs in sea lions and seals. It is
characterized by the formation of vesicles on the flippers. These vesicles usually rupture and form
prominent slow healing ulcers. This virus has also been implicated in causing ulcerative lesions on the
lips, nose, chin, and gums. Microscopically, the lesion consists of spongiosis of the stratum spinosum,
which later progresses to subcorneal vesicle formation. Intracytoplasmic or intranuclear inclusions are
not present.
Several serotypes of San Miguel sea lion virus have been isolated from aborting sea lions and
aborted fetuses. These serotypes of San Miguel sea lion virus are indistinguishable from serotypes of
vesicular exanthema virus that cause abortions in swine. The relationship of San Miguel sea lion virus
infection and abortions in affected marine mammals is suspected but not proven. The virus has been
isolated from the opal-eye fish (Girella nigricans) which is believed to function as a reservoir for the
spread of this disease. This fish is known to develop an active infection with viral replication in the
spleen. The fish remains infected for about 31 days. Clinical disease has not been observed in infected
fish.
A similar calicivirus has been isolated from Atlantic bottlenosed dolphins. These animals are
presented with vesicular skin lesions that are eroded and leave shallow ulcers. It was felt that this virus
is infective for both sea lions and dolphins.
3.
Sea Lion Hepatitis Virus
Sea lion hepatitis virus is caused by an adenovirus. This virus is not highly virulent. Only a few
animals demonstrate clinical disease, however, serological surveys demonstrate that large numbers of
animals are exposed to the virus. Sea lions, seriously affected by this agent, usually die acutely with little
clinical evidence of infection. At necropsy these animals are usually presented with icterus,
splenomegaly, mesenteric lymphadenopathy, and discoloration of the liver. Microscopically, the liver
lesion consists of random areas of coagulative and lytic necrosis of hepatocytes. In many cases, the
necrosis is most severe in the centrolobular region of hepatic lobules. Large pale eosinophilic to dark
basophilic intranuclear inclusions are present in hepatocytes and occasionally in Kupffer cells. The
inflammatory response is usually minimal, with a few macrophages, lymphocytes, and neutrophils at the
periphery of the necrotic lesion.
4.
Influenza Virus
The influenza virus observed in seals has been identified as an influenza A virus (Type
A/Seal/MA/1/80, Type A/Seal/MA/133/82, Type A/Seal/MA/3807/91, Type A/Seal/MA/3810/91,
Type A/seal/M/3911/92) and influenza B virus (Type B/seal/netherlands/1). Most influenza A viruses
have been identified as an H3 influenza viruses. This subtype of virus is most frequently detected in
birds, pigs, horses, and humans. It is felt that the viruses infecting seals are most closely related to H3
avian influenza viruses. Some feel that seals, like swine, may play a role in genetic reassortment of these
influenza viruses, thus causing a potential for interspecies transmission. It should also be noted that
several influenza A viruses have been also identified in sick long-finned pilot whales. It is unclear as to
the seriousness of these viruses in cetaceans.
These viruses have been associated with high mortality in harbor seals. This virus causes serious
respiratory distress in affected seals. Affected animals are usually presented weak and have serious
respiratory difficulties. A white mucinous to bloody discharge is observed in the trachea and bronchi.
Pulmonary, mediastinal, and subcutaneous emphysema are commonly observed. Microscopically, there
is a severe interstitial and hemorrhagic bronchopneumonia with hemorrhage in alveoli and prominent
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necrosis of bronchioles and bronchi. Mycoplasma (Mycoplasma phocidae) and other bacteria have been
isolated from affected animals. It is felt that there is a synergic effect between the virus and bacterial
agents since seals experimentally challenged with only the virus develop a mild respiratory disease.
In one outbreak (A/seal/mass/1/80, an H7N7 virus), personnel working with sick seals developed a
severe conjunctivitis which lasted 3 to 4 days. Virus was cultured from affected individuals. A type B
influenza found in the Netherlands is similar to the human type B influenza that circulated in humans in
1995 and 1996. Seals after 1995 had a 2% incidence of this virus and may have the potential of
infecting people.
5.
Phocine morbillivirus (Phocine distemper virus, PDV-1, PDV-2)
Several disease outbreaks that killed thousands of seals in Northern Europe and Lake Biakal in
Siberia have been attributed to a morbillivirus. The morbillivirus affecting harbor seals (Phoca vitulina)
and grey seals (Halichoerus grypus) in Northern Europe and North America is caused by the
morbillivirus, phocine distemper virus-1 (PDV-1). This virus is similar to, yet antigenically distinct,
from canine distemper virus. Differences in DNA sequencing between PDV-1 and canine distemper are
of such great magnitude that they need to be considered separate species. Serologic studies have
demonstrated that harbor seals (Phoca groelandica), hooded seals (Cystophora cristata) and ringed seals
(Phoca hispida) have an immune response by viral neutralization to PDV-1. The morbillivirus, phocid
distemper virus-2 (PDV-2), isolated from Siberian seals (Phoca siberica) in Lake Baikal is closely
related to a field strain of canine distemper virus found in Germany. Seals can also be susceptible to
canine distemper virus. A mass die off of Caspian seals (Phoca caspica) in the Caspian Sea (Spring
2000) has been attributed to a canine distemper virus. Canine distemper virus has also been implicated
in the die off of crab-eating seals (Lobodon carcinophagus) in Antarctica (in 1955).. A morbillivirus
isolated form sick Mediterranean monk seals (Monachus monachus) most closely resembles those
morbilliviruses identified in cetaceans. Atlantic walruses have had neutralizing antibodies to phocine
distemper virus but have not had clinical disease.
Clinically, affected seals are very weak and have severe respiratory distress. A mucopurulent to
serous oculonasal discharge is often observed. Many animals developed subcutaneous emphysema
primarily around the neck and thorax. On necropsy, these animals have edematous lungs with sharply
demarcated areas of red consolidation. Emphysema involving the interlobular septa and pleura of the
caudal lung lobes is present. Many animals developed emphysema of the mediastinum, neck, fascia, and
subcutis. Congestion and a thick mucopurulent exudate are observed in the upper respiratory tract.
Pulmonary lymph nodes are edematous. Hydropericardium, hydrothorax, and hepatic congestion are
common. Histologically, the lung lesion consists of a bronchointerstitial pneumonia with syncytial cells
and type II pneumocyte proliferation. Eosinophilic intracytoplasmic inclusions are present in bronchial
epithelium and syncytial cells. The brain has a nonsuppurative (lymphocytic) encephalitis characterized
by necrosis of neurons (primarily in the cerebral cortex), nonsuppurative perivascular cuffs, and gliosis.
Many affected neurons contain intranuclear and intracytoplasmic inclusions. Demyelination of the
subependymal white matter is also observed. Prominent depletion and necrosis of lymphocytes in
lymphoid tissues is present. Some seals develop a necrotizing nonsuppurative myocarditis. Like canine
distemper, intranuclear and intracytoplasmic inclusions are observed in the gastric mucosa and
transitional epithelium of the urinary bladder and renal pelvis.
6.
Morbillivirus in Cetaceans
A morbillivirus causing similar lesions to those observed in the phocine morbillivirus has also
been observed in cetaceans. This viral infection was first identified in harbor porpoises (Phocoena
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phocoena) from the Irish Sea during the 1988 European phocine morbillivirus outbreak. This virus has
killed numerous striped dolphins (Stenella coeruleoalba) along the Spanish Mediterranean coast, has
been identified in outbreaks affecting bottlenosed dolphins along the Eastern Atlantic and Gulf Coast of
the United States and has been identified in sick common dolphins (Delphinus delphis ponticus) on the
northern shores of the Black Sea. Pilot whales (Globicephala sp.) are also infected with this or a similar
morbillivirus. Morbilliviral infection has also been noted in the lymph nodes of a stranded fin whale
(Balaenoptera physalus). (Syncytial cells in the lymph node stain positive for morbillivirus and electron
microscopy identification of viral nucleocapsid material compatible with morbillivirus.) The viruses
affecting harbor porpoises and striped dolphins are closely related, but antigenically distinct. These
viruses are antigenically distinct from phocine morbillivirus and other mammalian morbilliviruses.
However, the cetacean morbilliviruses appear to be related to the ruminant morbillivirus peste-des-petits
ruminants. Serologic evidence of morbillivirus infection has been identified in numerous odontocete
cetaceans in the western Atlantic and may have a potential impact on these species. Affected cetaceans
develop similar pulmonary and central nervous system lesions that are observed in affected seals.
Grossly, these animals develop a severe pneumonia with multiple foci of atelectasis and consolidation.
Lung associated lymph nodes are often enlarged and edematous. Histologically, there is a
bronchointerstitial pneumonia characterized by necrosis of bronchial and bronchiolar epithelium with a
prominent mucopurulent exudate. Acidophilic intracytoplasmic inclusions are observed frequently
(occasionally intranuclear inclusions are also observed). Type II pneumocyte hyperplasia and prominent
mononuclear inflammation is observed in alveoli. Syncytia are observed in both the alveoli and
bronchiolar epithelium. A non-suppurative meningoencephalitis is observed in most affected animals.
This involves primarily the cerebral grey matter with occasional eosinophilic intranuclear inclusions
present. Necrosis of the bile duct epithelium and transitional epithelium of the urinary bladder with
occasional eosinophilic intracytoplasmic inclusions is also observed. The lymph nodes have prominent
lymphoid depletion with scattered multinucleated syncytial cells present throughout the lymph node.
Multinucleated syncytial cells and inflammation have been observed in the mammary gland. All
affected areas demonstrate intense immunohistochemical staining for morbillivirus. Many affected
dolphins also have serious secondary systemic infections of toxoplasmosis, aspergillosis and other fungi.
It is interesting to note that the Florida manatee (Trichechus manatus latirostris) has seroconverted
by virus neutralization to dolphin morbillivirus. To date no clinical disease has been reported in these
animals.
7. Seal Herpesvirus
Several herpesviruses have been isolated from harbor seals and a California sea lion. Two distinct
types have been isolated from affected animals, these have been identified as phocid herpesvirus type 1
and type 2 (PHV-1and PHV-2). PHV-1 is characterized as a member of the alpha-herpesvirus
subfamily and closely related to canid and felid herpesvirus. PHV-2 has been classified as a gammaherpesvirus. Numerous pinniped species have antibodies to PHV-1 and PHV-2 (Ringed seals, spotted
seals, harbor seals, bearded seals, ribbon seals, Steller sea lions, Northern fur seals and walrus). Most
animals with seroconversion to these viruses do not demonstrate clinical disease.
PHV-1 affects mostly young harbor seals. This virus has been shown to cause a serious systemic
infection. Affected animals demonstrated an acute pneumonia, necrotizing hepatitis and necrotizing
adrenalitis. Occasionally, a non-suppurative encephalitis is observed with rare neuronal necrosis. The
pneumonia is characterized as a diffuse interstitial pneumonia with multifocal fibrinous exudation and
emphysema. Within the liver and adrenal gland, there is multifocal necrosis of the hepatic and
adrenocortical parenchyma with a minimal mononuclear cell infiltrate. Acidophilic intranuclear
inclusion bodies are observed in the areas of necrosis. Electron microscopy demonstrates unenveloped
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hexagonal viral particles 90 to 100 nm with a central dense core and cytoplasmic enveloped particles
150-160 nm in diameter. The nature of this virus and its potential to cause disease in wild and captive
populations of seals is still unknown. This virus has been inoculated in young seals with only minimal
upper respiratory signs (nasal discharge). Phocine herpesvirus, like most mammalian herpesviruses, is
most often fatal in the young and seriously stressed animal. Most sick animals also have concurrent
bacterial or protozoal infections that may mask the herpes viral infection. Like most herpesviruses, this
herpesvirus probably expresses itself in times of stress, as either subclinical oral or genital lesions.
The phocine herpesvirus-2 was isolated from a California sea lion with a severe bacterial
pneumonia, free ranging harbor seals and from seals with abortions during the early epizootic of
morbillivirus infection in Northern Europe. The importance of this virus in the pathogenesis of this
pneumonia is unknown. (A non-oncogenic retrovirus was also isolated from the skin of this affected sea
lion). This virus is highly cell associated and causes little or no disease in pinnipeds.
A gamma herpesvirus has been identified in a metastatic carcinoma of the lower genital tract from
California sea lions. This virus is associated with the neoplastic cells. The association of the virus with
the development of neoplasia of the vagina and cervix is unknown.
8.
Herpesvirus in Beluga Whales (Delphinapterus leucas)
A herpesvirus has been observed to cause a focal dermatitis in beluga whales. These epidermal
lesions consisted of random variably sized multiple discrete raised pale grey areas which eventually
ulcerate and are slow to heal. Histologically the epithelial lesion involved the superficial epidermis with
the epithelial cells undergoing intercellular edema, necrosis and microvesicle formation. The infected
epithelial cells contained prominent eosinophilic intranuclear inclusion bodies.
9.
Herpesvirus of Sea Otters (Enhydra lutris)
A herpesvirus has been implicated in causing extensive oral lesions in sea otters. Clinically these
lesions consist of variably sized irregular white plaques and/or deep often bilaterally symmetrical ulcers.
These lesions are commonly found mostly on the gingiva and under the tongue. In severely affected
animals, the ulcers tend to coalesce to cover extensive areas of the buccal, labial, gingival and glossal
mucosa. Infected animals rarely show a reluctance to eat, even with extensive oral lesions.
Histologically, the lesions reveal extensive chronic ulcers with associated mixed bacterial colonies and
separate foci of epithelial necrosis and intracellular edema. Numerous eosinophilic intranuclear
inclusion bodies are observed in the degenerating and necrotic cells.
10. Herpesvirus of Bottlenosed dolphins
A disseminated herpes viral infection was identified in an immature female bottlenosed dolphin.
On necropsy, the animal had an enlarged thymus, pericardial hemorrhage and hydrothorax.
Histologically there was a necrotizing interstitial pneumonia, lymphocytic myocarditis, splenic and
lymphoid necrosis, and a necrotizing adrenalitis. Intranuclear inclusions are observed in numerous cells
of the thymus, spleen, adrenal gland, heart, lungs, and glomeruli. Sequencing of DNA products
indicates this virus is an alpha herpesvirus.
11.
Hepatitis B-Like Infection in Dolphins
A hepatitis B-like infection has been identified in a Pacific white-sided dolphin (Lagenorhynchus
obliquidens). This animal developed cyclic periods of inactivity, anorexia, and icterus. Blood values
demonstrated a leukocytosis with neutrophilia, lymphopenia, and eosinopenia. Biochemical values
showed markedly elevated alanine transaminase (ALT), aspartate transaminase (AST), gamma
glutamyltransferase (GGT), lactic acid dehydrogenase, total bilirubin, direct bilirubin and indirect
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bilirubin. These findings suggested a chronic active hepatitis. Supportive measures were instituted and
the dolphin eventually recovered. Serum from the animal was found to be positive for antihepatitis B
virus core (anti-HBc) activity, hepatitis B virus DNA (HBV-DNA) and hepatitis B surface antibodies
(Anti-HBs). Other cetaceans and humans who had contact with this animal were examined for hepatitis
B antigens. One killer whale was positive while all other cetaceans and humans were negative.
12. Papillomas in cetaceans
Papillomas have been reported on the skin, penis, genital slit, vagina, tongue, pharynx, and first
gastric compartment of cetaceans. Although a papillomavirus has not always been implicated as the
cause of these lesions, they should be suspected. In the beluga whale , the gastric papillomas identified
in the first gastric compartment are white (like the surrounding normal mucosa), well defined, exophytic
masses with a central wart like core composed of small filamentous papillae. Histologically, the
papilloma develop into an exophytic cup shaped mass with marked epithelial proliferation supported by
a thin fibrovascular proliferation forming numerous arborizing projections from the submucosa. The
proliferating epithelium consists of a flattened basal cell layer 3 to 15 cells thick with a mature
epithelium overlying the basal cells. Scattered amongst the hyperplastic epithelium, individual and
small groups of epithelial cells undergo hydropic degeneration (cells become swollen and globular with
a pale granular cytoplasm). Ultrastructurally, the cells undergoing hydropic degeneration with
aggregates of small 40 nm hexagonal viral particles observed in the cytoplasm. These viral particles are
consistent with papillomavirus. It is unclear if any of these papillomas cause physical problems with the
affected animals. Papillomas on the penis are usually raised plaques on the mucosal surface. Like man,
papillomavirus may infect the cervical mucosa and might cause neoplasia from this region.
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Bacterial Diseases
Bacterial diseases are the leading cause of death in marine mammals. These organisms are usually
observed as opportunistic invaders in conjunction with parasitic, viral or traumatic injuries. The
inhibition of bacteria in the marine mammal's environment is one of the most important factors in
maintaining marine mammal health in captivity.
One must remember that these animals are mammals and therefore are affected by the same
bacteria as their terrestrial counterparts. This discussion will focus only on bacteria that have gained
notoriety as pathogens in the marine mammal.
1.
Erysipelothrix rhusiopathiae
Erysipelothrix rhusiopathiae is a small pleomorphic gram positive rod. This bacteria causes two
distinct forms of disease in dolphins: a dermatological disease and a septicemic disease. The
dermatological disease is characterized by dermal infarction that results in sloughing of the epidermis.
Occasionally micro-infarcts result in the characteristic rhomboid areas of cutaneous necrosis. If
untreated, these animals will usually die. The septicemic disease is usually peracute, with the animal
found moribund or dead. At necropsy, affected animals may demonstrate multifocal areas of necrosis
and inflammation involving numerous organs. Culturing the agent (a small pleomorphic gram positive
bacilli) from affected tissues and blood (lymph nodes, kidney, liver, heart, blood) is the only way of
identifying this organism as the agent responsible for the septicemia. A killed bacterin is available for
vaccination. This vaccine has produced excellent results in controlling the disease, however, the vaccine
is known to cause anaphylactic reactions in some cetaceans. It is important to remember that Erysipelas
is commonly found in fish; ingestion may be the route of infection in cetaceans.
2.
Pseudomonas Infection
Various species of Pseudomonas (gram negative bacilli) have been incriminated in causing
bacterial disease in both pinnipeds and cetaceans. It is felt that this organism is an opportunistic
pathogen which colonizes wounds and can lead to septicemia. Pseudomonas aeruginosa has caused
bronchopneumonia and multiple large cutaneous ulcers in Atlantic bottlenosed dolphins. The bacteria
are known to progress deep into the cutaneous tissue, causing serious damage to the animal. Many times
pseudomonas septicemia causes a characteristic proliferation of gram negative bacilli into the wall of
affected blood vessels. If affected animals develop a septicemia, cutaneous lesions similar to those
observed with erysipelas may develop. Thus, culturing the lesions is the only method of determining
which organism is responsible for the animals illness.
Pseudomonas pseudomallei is a pathogen found in Southeast Asia. The organism is a water
contaminant and is thought to gain entrance into the animal through cutaneous wounds. A septicemia
soon follows which may result in death. Animals often die peracutely with no clinical signs. Grossly
and histologically, lesions are characterized by multifocal areas of necrosis and inflammation involving
many organs (lungs, liver, spleen, kidneys, and lymph nodes). This agent is infectious to man and may
be transmitted via cuts or abrasions as well as by aerosol transmission.
3. Edwardsiella
Edwardsiella species are gram negative bacilli that are common inhabitants of water. These
bacteria are noted to cause bacterial septicemia in fish. This organism can be a pathogen in both
pinnipeds and cetaceans. Affected animals present with a serious necrotizing enterocolitis and/or
septicemia. Animals with septicemia can develop a severe embolic interstitial or bronchointerstitial
pneumonia, a necrotizing hepatitis and a necrotizing splenitis. Animals with an intestinal lesion develop
a necrotizing and hemorrhagic enteritis/colitis similar to that found in salmonella infections. Isolation of
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Edwardsiella from the lungs and liver are usually suggestive of a septicemia. Animals that develop this
disease are usually debilitated or stressed and probably get these organisms from ingestion of
contaminated fish.
4. Salmonella
Salmonella are gram negative, non-lactose fermenting bacilli. Salmonella infections have been
observed in both cetaceans and pinnipeds. Salmonella typhimurium, S. enteritidis and S. newport are
the most prevalent salmonella that cause disease. Other Salmonella species have been isolated from
marine mammals without apparent disease. These bacteria are of particular concern for animals housed
in rehabilitation centers. Thus, recently stranded animals should be quarantined and monitored for
salmonella prior to placing with other animals. Salmonella infections usually occur in animals that are
debilitated and/or stressed. Animals present with a hemorrhagic diarrhea and/or septicemia. Animals
with the hemorrhagic diarrhea usually have a necrotizing enterocolitis. Culturing the feces is
recommended for isolation of the organism. Animals that develop a septicemia can die acutely with no
clinical signs. On necropsy, the animal may have a bronchopneumonia and/or a diffuse embolic
interstitial pneumonia. A necrotizing hepatitis and splenitis are common; meningoencephalitis may
occur. Isolation of the organism from the lungs and liver are usually consistent with a septicemia.
5. Leptospirosis
Leptospirosis, primarily caused by Leptospira pomona is known to cause abortions and renal
disease in California sea lions and Northern fur seals. L. grippotyphosa, L. icterohemorrhagiae, and L.
bratislava have been identified serologically, however, this may be due to antigen cross reactivity of L
pomona with these leptospira. This disease is believed to be endemic in rookeries in California and is
most prevalent in the autumn affecting predominately subadult and young adult males. Animals are
usually depressed, anoretic, pyrexic, and reluctant to move due to posterior limb paresis. Other lesions
include icterus, oral ulcerations and excessive thirst. Clinically most animals have a leukocytosis and
elevated creatinine, phosphorus and BUN levels, which indicate renal disease. Grossly, the kidneys are
swollen. On cut surfaces the renal cortex and medulla are pale with loss of differentiation. Hemorrhage
at the corticomedullary junction and subcapsular region is commonly observed in the kidney. In some
animals the liver is swollen and friable. Histologically, a lymphoplasmacytic interstitial nephritis with
tubular necrosis is present with the spirochete present in the renal tubular epithelium and free in the
lumina. In newborn and aborted fetuses, the disease is characterized by subcutaneous hemorrhage and
hemorrhage into the anterior chamber of the eye (The disease “Red Eye”). This disease may have
zoonotic significance since affected sea lions have demonstrated that they may shed the bacteria in the
urine for up to 154 days. In the live animal, rising titers or titers above 1:3200 are considered to be
infected with leptospirosis.
5. Dermatophilus congolensis
Dermatophilus congolensis is a disfiguring cutaneous disease affecting pinnipeds (South American
sea lion). This disease is characterized by a scruffy pustular or exudative dermatitis involving the entire
body. These lesions are elevated above the skin, forming very prominent scabs. Mortality is low, but
morbidity is high.
Histologic examination of the epidermis demonstrates the characteristic multiple layers of
coagulative necrosis of the epidermis with a peripheral line of degenerating neutrophils separating each
necrotic layer. Numerous gram positive cocci that form the characteristic parallel rows are observed in
the necrotic debris.
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6. Mycobacteriosis
Several species of Mycobacteria have been isolated from seals (M. tuberculosis complex (M.
bovis, M. fortuitum, M. chelonei), a California sea lion (M. smegmatis), and several manatee (M.
chelonei and M. marinum). These infections have been presented as either nonhealing chronic
cutaneous lesions, generalized infections with caseonecrotic granulomas in various organs and lymph
nodes or pulmonary infections with granulomas present. Numerous acid-fast bacteria are observed in
the cutaneous lesions. Microorganisms may be more difficult to find in granulomas caused by M.
tuberculosis complex (M. bovis). Since several of these species of Mycobacteria are found in the soil
and water, persistent nonhealing cutaneous lesions should be cultured for Mycobacterium. All these
organisms have a zoonotic potential, care should be taken when treating and handling these wounds.
7. Staphylococcus sp.
Staphylococcus aureus has been implicated as one of the causes of pneumonia in dolphins
maintained in captivity. Staphylococcus has also been isolated from septicemia which have lead to
embolic nephritis and cerebral abscesses as well as cutaneous lesions. S. aureus is a part of the normal
flora of the blow hole of many normal dolphins. However, some investigators feel that if it is present in
the upper respiratory tract, it should be considered a potential pathogen. Staphylococcus delphini has
been isolated from a purulent dermatitis in dolphins. In seals, staphylococcus has been identified in
animals with cutaneous abscesses or pneumonia.
8. Clostridial disease
Clostridium perfringens has been reported to cause enterotoxemia in young pinnipeds, gas
producing myositis in dolphins and cutaneous abscesses in fur seals. The necrotizing myositis observed
in dolphins and the subcutaneous abscesses in pinnipeds has been attributed to injection site
contamination. Since Clostridium perfringens and other clostridial organisms are normal inhabitants of
the gut and common in dead animals, it is best to do impression smears from the lesion (gut or muscle)
on clean glass slides for bacterial evaluation.
9. Klebsiella
Klebsiella (Gram negative bacilli) has seen associated with pneumonia in marine mammals. As
usual, bacterial cultures are necessary to differentiate this organism from other bacterial infections.
10. Nocardia
Nocardia asteroides has been isolated from numerous cetaceans. This organism has been
associated with necrotizing and pyogranulomatous lymphadenitis, pleuritis, encephalitis and mastitis.
The organism is a thin filamentous gram positive organism which can be acid fast.
11. Brucella
Brucella has been identified in several species of cetaceans (Atlantic white-sided dolphins,
Lagenorhynchus acutus; striped dolphins, Stenella caeruleoalba; and bottlenosed dolphin, Tursiops
truncatus), pinnipeds ( hooded seal, Cystophora cristata; grey seal, Halichoerus grypus; Pacific harbor
seals, Phoca vitulina richardsi; ringed seals) and a European otter (Lutra lutra). These organisms have
been cultured from the placenta and aborted fetus of a bottlenosed dolphin (Tursiops truncatus) and from
lesions in the subcutis (sub-blubber abscesses), lymph nodes, liver, spleen, epididymis, bones and lungs
from other affected animals. The placenta developed a necrotizing placentitis with gram negative
coccobacilli within the trophoblast. Lesions in lymph nodes, liver and lungs are characterized by a
multifocal granulomatous inflammation. Biotyping of the bacteria indicates that these bacteria are
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closely related to Brucella abortus or Brucella melitensis. However, it is felt that these may represent a
new species of brucella with several different biovars. (Some have suggested that the brucella organism
identified in the bottlenosed dolphin be called Brucella delphini.) It is currently unclear as to what
impact this organism has on marine mammals. However, antibodies to Brucella species are widely
distributed among many different marine mammals in the north Atlantic. Brucella organisms have been
identifies in Parafilaroides sp. of lungworms. Brucella organisms have been observed in the uterus and
intestines of this lungworm. The importance of this lungworm in the transmission of brucella to animals
is unknown. These parasites may represent an important transport host for the dissemination of this
bacteria in the wild.
11. Streptococcus
Streptococcus spp. have been isolated from seals with pneumonia and septicemia and cetaceans
with septicemia, metritis, pneumonia and skin lesions. These are primarily beta-hemolytic streptococcal
species (Gram positive diplococci). Most are normal inhabitants of the skin and upper respiratory tract.
A beta-hemolytic streptococcus, Streptococcus phocae, was isolated from many of the seals that died of
pneumonia during the phocine morbillivirus outbreak in the North Atlantic. Most animals present
themselves clinically with dyspnea, coughing and a nasal discharge. Pathological examination
demonstrated a severe pneumonia with areas of consolidation of the lungs, purulent exudate in the
bronchi and bronchioles, interlobular edema and emphysema. Rarely do streptococcal organisms cause a
primary infection. These organisms usually are associated with viral infections.
12.
Coxiella burnetii
Coxiella burnetii has been identified in the placenta of an aborted Pacific harbor seal (Phoca
vitulina richardsi). This full term fetus was born alive (but euthanized) from a seal that had an
encephalitis caused by Sarcocystis neurona-like protozoan. The placental trophoblasts were distended
with large spherical aggregates of dense basophilic granular material. The cytoplasmic aggregates
stained pink on Gram stain and pale pink with a Gimenez stain for rickettsia. There was marked
necrosis and drop off of trophoblasts and abundant eosinophilic cellular debris on the chorioallantoic
membrane just adjacent to the placental labyrinth. Multifocal hemorrhage was noted in the
chorioallantoic connective tissue, but no inflammation as noted. Organisms stained positive for Coxiella
burnetii using anti-Coxiella burnetii antibody. No fetal lesions were observed. It is unknown how
common placental infections with C. burnetii are in seals. The source of the infection is unknown, but
like most terrestrial mammals, infection may occur with or without abortions. Handlers of placental
tissues and/or newborn pups should take precautions because of the potential zoonotic concerns that are
known to exist with this organism.
11
Mycotic Diseases
Numerous mycotic diseases have been reported in pinnipeds and cetaceans. Most have been single
reportable cases; only several fungal organisms have been associated with outbreaks of disease.
Since fungal organisms are usually opportunistic or secondary invaders; these organisms pose a serious
health risk to the animal that is immunocompromised. Animals that are malnourished, have preexisting
viral or bacterial diseases, have undergone prolonged drug (antibiotic) therapy, or immunosuppressed
due to stress are predisposed to get these infections.
1. Candidiasis
Candida albicans is the most common species of Candida to cause clinical disease in stressed
pinnipeds and cetaceans. Infected animals usually develop cutaneous and/or intestinal infections with
lesions occurring primarily at mucocutaneous junctions, blowhole and vagina. Disseminated candidiasis
has been reported in the killer whale and other cetaceans. It is felt that most marine mammals can be
infected by Candida. Infections are usually observed in animals that are severely stressed and/or under
prolonged antibiotic therapy. These lesions appear as white or yellow creamy plaques. In internal
organs, prominent focal areas of necrosis are visible. Histologically large colonies of septate hyphae,
pseudohyphae (3-7 microns wide) and blastospores (3 to 5 microns diameter) are observed in the
necrotic lesions. The finding of Candida in the esophagus or vagina is very common and may be
identified histologically as an incidental finding. However, when the organism invades healthy tissue,
the fungus is considered pathogenic.
2. Loboa loboi
Lobomycosis is a fungal disease that affects the skin of the Atlantic bottlenosed dolphin and man.
Grossly, these lesions are located anywhere on the animal's body (head, fin and flukes are the most
common sites) and are white, multiple and nodular. These lesions have a cobble stone appearance on the
skin. Histologically, there is a superficial granulomatous dermatitis involving the papillary dermis. This
granulomatous dermatitis is composed almost entirely of macrophages and multinucleated giant cells
containing numerous round yeast forms (5-10 microns in diameter) connected to each other and forming
long chains. Some yeast forms contain a 1 to 2 micron central body. Larger yeast forms may have a
rough and spiny surface. The epidermis over these areas of inflammation is acanthotic with downward
growth of the rete pegs. Clinically the animals are not seriously affected by the growth of the organisms;
however, if these become large, the animal may become debilitated and die (usually due to secondary
bacterial infections). Treatment has not proven successful, however, removal of the affected area has
shown positive results.
3. Fusarium
Outbreaks of Fusarium-induced dermatitis has been observed in a group of captive California sea
lions, grey seals, harbor seals, Atlantic white sided dolphins and a pygmy sperm whale. The lesions
consisted of papules and nodules on the face, trunk, flippers and the caudal portions of the body.
Histologically, there is hyperplasia of the follicular and epidermal epithelium with associated chronic
active inflammation and numerous fungal hyphae (Septate branching hyphae, 2 to 5 microns in width
with parallel sides). In marine mammals, Fusarium spp. are most likely opportunistic invaders of the
skin. Animals that are immunocompromised due to stress or illness may be most susceptible. Damage
to the integument due to excessive chlorination of the water and high fluctuating pool temperatures may
also play an important role in this disease. Treatment of the animals with ketoconazole caused the
dermatitis to resolve in 3 to 4 weeks.
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4. Aspergillus and Zygomycetes Infections:
Aspergillus and Zygomycetes infections cause serious disease in individual animals. As with
infection with Candida, the affected animals are usually stressed and/or under prolonged antibiotic
therapy. Infection can involve focal areas, usually the esophagus or lungs; however, systemic spread of
the fungus is common. Lesions involving the esophagus and trachea usually appear as ulcers with
yellow to cream colored plaques over the affected area. Systemic spread leads to necrosis of multiple
tissues with liver and kidney commonly involved. Diagnosis is by observing the characteristic hypha
(Aspergillus: long branched septate hyphae, 3-4 microns wide with parallel walls. Zygomycetes: long
non-septate non-parallel walled hyphae with irregular branching).
5. Dermatophytosis: Microsporum and Trichophyton spp.
Cutaneous infections with Microsporum canis and Trichophyton spp. have been reported in both
cetaceans and pinnipeds. Microsporum canis has been isolated from harbor seals and Trichophyton spp.
in Northern fur seals (Callorhinus ursinus), Steller sea lions (Eumetopias jubatus) and bottlenosed
dolphins (Tursiops truncatus). Infections in the seals is characterized by round depilated areas, 2 to 3 cm
in diameter on the face and back. These depilated areas spread over the entire body. Histologically there
is epidermal hyperplasia with hyperkeratosis, parakeratosis, necrosis and microvesiculation and
microabscess formation. Numerous neutrophils are present in the affected epidermis. Numerous
branched septate hyphae 2-7 microns in diameter are observed in the parakeratotic and necrotic regions.
6. Coccidioides immitis
Coccidioides immitis has been identified as an endemic disease in the California sea lion
(Zalophus californianus) and an isolated case in the California sea otter (Enhydra lutris) and bottlenosed
dolphin (Tursiops truncatus gilli). This organism appears to be endemic in animals that inhabit the
southern and central part of their range from Baja California, Mexico in the south to Monterey County,
California in the north. Coccidioides immitis is an infectious agent to numerous animal species and is a
serious health risk to man (Valley Fever) when living in endemic areas. Endemic areas are Arizona,
Southern and Central California, Mexico, New Mexico, Nevada, Utah and Texas. This organism
probably infects sea lions, like most animals, as a mild respiratory disease. Recovery usually occurs after
a short illness. Some animals develop a serious disseminated disease. Sick animals usually beach and
are presented ill. Gross necropsy findings are focal to disseminated granulomas involving the lungs,
liver, pancreas, numerous lymph nodes (retropharyngeal, submandibular, mesenteric, and
tracheobronchial lymph nodes) and occasionally a purulent pleuritis and peritonitis. Histologically the
affected organs develop pyogranulomatous inflammation with variable numbers of multinucleated giant
cells and large round double contoured wall spherules, 10-70 micron in diameter. Filling the spherules
are numerous small 2-5 micron endospores. Animals are most likely infected by the inhalation of
spores. Coccidioides immitis is also known to survive in sea water for several weeks. It is unknown if
sea water could be a means of infecting animals.
13
Protozoal Diseases
1. Sarcocystis sp.
Sarcocystis species have been reported in numerous pinnipeds and cetaceans and the sea otter.
These species of sarcocystis are S. balaenopteralis in a whale (Balaenoptera borealis), S. neurona in a sea
otter and harbor seal, and several unnamed species of Sarcocystis in a sperm whale (Physeter catodon),
Northern fur seal (Callorhinus ursinus), striped dolphin (Stenella caeruleoalba) and ringed seals (Phoca
hispida). These protozoal organisms appear to be incidental findings in these animals. Little is known
about their life cycle. A necrotizing hepatitis characterized by multifocal areas of necrosis has been
observed in a captive sea lion. This organism appears to be similar to Sarcocystis canis. It is not known
whether this organism is normally found in this animal. In a captive sea otter, encephalomyelitis (most
severe in the cauda equina region) has been observed caused by Sarcocystis neurona-like organisms.
The source of the infection was not known.
2. Toxoplasma gondii
Toxoplasma gondii has been observed in several species of marine mammals including: the
California sea lion, Northern fur seal, harbor seal, manatee, Atlantic bottlenosed dolphin (Tursiops
truncatus), and Spinner dolphin. These animals have demonstrated a disseminated infection with
necrosis of numerous organs containing toxoplasma tachyzoites. It is felt that these animals probably
were immunocompromised leading to infection. Transplacental transmission is unknown but probably
can occur.
3. Ciliated Protozoa of Dolphins
A ciliated protozoa (Kyaroikes cetarius, possible) has been identified in necrotic cutaneous lesions
in Atlantic bottlenosed dolphins, spotted dolphins (Stenella attenuata), common dolphins, pygmy sperm
whales, Frazer’s dolphins, and killer whales. These lesions are usually a pyogranulomatous dermatitis
and cellulitis with large ciliate protozoa scattered amongst the necrotic debris. These ciliated protozoa
are large (up to 60-100 microns in diameter with a large 20 micron nucleus). These organisms have also
been associated with pneumonia and lymphadenitis. These protozoa may be opportunistic invaders since
these protozoa are commonly found in and around the blowhole of dolphins (50% of wild dolphins)
without any inflammation or disease.
4. Giardiasis
Giardia sp. oocyst have been identified in fecal samples from ringed seals (Phoca hispida), harp
seals (Phoca groenlandica), grey seals (Halichoerus grypus), and harbor seals in the arctic, subarctic and
eastern regions of Canada. Infected animals have not demonstrated illness. The zoonotic potential of
infected seals to act as reservoirs for human infection is unknown. To date, feces from beluga whales
and northern bottlenosed whales (Hyperoodon ampullatus) were negative for Giardia sp. cysts.
14
External Parasites
1. Lice
Lice are a common finding on pinnipeds. Only anopluran (sucking) lice have been found on these
animals. Antarctophthirius microchir is a common louse noted on sea lion pups. These insects cause
alopecia in infected animals. These organisms are believed to be the intermediate host for the filarid
nematodes of pinnipeds; however, this has not been proven.
Cetaceans are also known to harbor lice. Several species of lice have been isolated from the skin
of these animals. Clinical disease has not been associated with these organisms.
2. Mites
Demodex zalophi has been observed in California sea lions. These animals develop alopecia and
thickening of the skin over the genitalia, flippers and ventral body. The mites live in hair follicles and
are diagnosed by skin scrapings.
Sea otters have also been observed to have demodex mites. These mites are observed in hair
follicles around the face. No serious dermatologic conditions have been observed in these animals.
Demodex mites only cause a mild follicular ectasia and minimal associated folliculitis.
3. Barnacles
Barnacles are common on certain cetaceans. These can be either sessile or pedunculated. They do
not cause damage to the skin of affected animals.
15
Internal Parasites of Pinnipeds
Respiratory System
(1) Lung mites:
Lung mites are common parasites of the nasal passages, trachea, bronchi, and bronchioles. Both
seals and sea lions are affected. The most common mites observed are Orthohalarachne diminuata and
Orthohalarachne attenuata. O. diminuata inhabits the airways of the lung, and O. attenuata are found in
the nasopharynx. The nasal mite, Halarachne miroungae has been observed in sea otters. Grossly these
mites are seen as small white specks on the mucosa of the respiratory tract (O. attenuata, .5 to 5 mm; O.
diminuata, .6 to .8 mm). Clinically, these mites do not cause any serious problems, however, they might
cause copious amounts of mucus in the upper respiratory tract and nose, nasal discharge, dyspnea, and
coughing.
(2) Lungworms
(a) Parafilaroides decorus is the most common lungworm of young (1-2-year-old)
California sea lions. The intermediate host for this metastrongylid is the opal eye fish (Girella
nigricans). After ingestion of the fish and release of the larvae into the gastrointestinal tract, the larvae
migrate to the lungs (alveoli), where maturation occurs. Females release larvae in the alveoli; larvae
then migrate up the respiratory airways, are swallowed, and are then discharged with the feces.
Histologically, uncomplicated infections result in goblet cell hyperplasia of the bronchiolar epithelium in
which mucoid obstruction is observed. A suppurative or granulomatous bronchopneumonia is observed
if a secondary bacterial infection occurs. Grossly, these lungs have a patchy, or mottled, appearance of
red and grey hepatization. Other Parafilaroides species have been noted in the lungs of other species of
pinnipeds. Parafilaroides lungworms have been identified with brucella bacteria present in their uterus
and gut. These lungworms may cause brucellosis infection in pinnipeds.
(b) Otostrongylus circumlitus is another large Metastrongylid nematode that inhabits the
primary and secondary bronchi of harbor seals and northern elephant seals. This parasite causes
prominent bronchiectasis. Bronchiectatic abscesses containing these parasites are occasionally observed.
Histologically, the bronchi and bronchioles have marked goblet cell hyperplasia of the peribronchiolar
glands; mucus plugs fill the dilated bronchioles. As with most lungworms, a verminous pneumonia may
develop as a result of secondary bacterial infection.
Digestive tract
(1) Stomach worms
Contracaecum and Anisakis are the most common nematode stomach worms of both pinnipeds
and cetaceans. These parasites cause ulceration of the gastric mucosa and submucosa during migration.
Occasionally Anisakine parasites may induce nodules in the gastric mucosa and submucosa. On
histologic examination, parasites are found in the ulcerated regions. In cetaceans (odontocete), these
parasites are located in the first and third chamber of the stomach. These parasites are usually incidental
findings; however, they have been noted to cause hemorrhage and melena in both pinnipeds and
porpoises. The life cycle is not fully understood; it is felt that a crustacean is the first intermediate host
and a fish (many different species) is the second intermediate host. (The Pacific herring is the second
intermediate host for Anisakis spp.)
(2) Hookworms (Uncinaria lucasi and Uncinaria hamiltoni)
16
Hookworms are common in sea lions and the Northern fur seal. Uncinaria lucasi is the most
pathologic hookworm for Northern fur seal pups. Young fur seals and sea lions become infected during
ingestion of the mother's milk. The parasites become adults within several weeks and cause severe
hemorrhage into the intestines, which results in anemia. Surviving pups usually shed the parasites after
three months. Surviving animals later become reinfected with the third-stage larvae by larval
penetration of the skin or by ingestion of the larvae. These larvae migrate to the blubber of the ventral
abdomen or mammary glands, where they remain dormant until they are shed in the females milk.
(3) Liver Flukes
Zalophotrema hepaticum is the liver fluke of sea lions. This fluke causes little damage and is
found in the common bile duct, intrahepatic bile duct, and gallbladder. Occasionally these flukes will
cause cystic cavitation in the hepatic parenchyma.
In sea otters, (also bearded seals) the gallbladder fluke, Orthosplanchnus fraterculus, causes cystic
hyperplasia of the gallbladder mucosa. It also is believed to be responsible for causing a chronic
fibrosing cholecystitis which is sometimes characterized by nodular thickening of the periductal and
gallbladder connective tissue. This parasite does not appear to adversely affect the host.
These flukes are very small, 1-3 mm in length. The eggs are the characteristic yellow color of fluke eggs
and triangular in appearance.
(4) Acanthocephalids
Acanthocephalids are common intestinal parasites in pinnipeds and sea otters. These parasites are
primarily of the genus Corynosoma. Acanthocephalids are observed usually as incidental findings in the
colon and small intestine (ileum and jejunum). These parasites bury their heads deep into the mucosa
and submucosa. In pinnipeds they rarely cause problems. However, in sea otters they are known to
burrow through the intestinal wall and cause a life threatening peritonitis. Three other species of
Acanthocephalids also occasionally infect sea otters, Falsifilicollis altmani, F. kenti, and F. major.
Cardiovascular system
Heartworms
Heartworm disease in pinnipeds is caused by both Dirofilaria immitis and Dipetalonema
spirocauda. D. spirocauda is the most common heartworm found in most feral pinnipeds (primarily
harbor seals). The life cycle is unknown, but the louse is suspected to be the intermediate host. These
parasites are observed in the right ventricle and pulmonary arteries. Severe infection causes dilatation of
the right ventricle and myocardial hypertrophy. Microscopically, the pulmonary arteries and arterioles
have prominent intimal proliferation. Secondary chronic passive congestion may be observed in
severely affected animals.
Dirofilaria immitis is occasionally observed in captive pinnipeds. These parasites live in the same
location and cause the same problems as D. spirocauda. The identification of microfilaria is helpful in
separating D. immitis from D. spirocauda. The microfilaria of D. immitis are usually larger (300 x 5
microns) than D. spirocauda (225 x 4 microns). However, microfilaria from D. spirocauda cannot be
differentiated morphologically from the common nonpathogenic subcutaneous filariid Dipetalonema
odendhali.
Dipetalonema odendhali is often found in the subcutaneous tissue, in the intermuscular fascia,
beneath the parietal peritoneum, free in the abdominal and thoracic cavities, and in the pericardial sac.
17
Internal Parasites of Cetaceans
Respiratory tract
(1) Nasitrema sp.
Nasitrema flukes are common flukes located in the head sinuses of many porpoises, dolphins, and
toothed whales. These flukes range in size from 9-12 mm (Nasitrema stenosomum) to 28-35 mm
(Nasitrema gondo). This parasite is normally found in the submucosal glands of these sinuses.
Occasionally this fluke is observed in the middle ear. This parasite rarely causes problems; however,
these flukes will occasionally migrate to the brain and cause serious central nervous system damage.
Lesions caused by this fluke usually contain numerous small yellow triangulated fluke eggs (60 to 80
microns on the long axis with a single operculum). Numerous strandings have been associated with
parasitic migration of this parasite into the brain. The life cycle is unknown.
(2) Hunterotrema caballeroi
This is a rather large fluke (up to 25 cm long) observed in the Amazon River dolphin. This
parasite causes a mild to moderate mucoid exudate in the bronchi of these animals. However, it has
been incriminated in bronchial obstruction, bronchiectasis, and atelectasis.
(3) Stenurus sp.
This is another common nematode (metastrongyle) located in the pulmonary parenchyma of the
harbor porpoise and dall porpoise. These parasites usually cause subpleural nodules, which are filled
with the parasites. This parasite has been known to migrate and fill the tympanic bullae. These parasites
have been incriminated in dolphin strandings when the parasites have been observed in the tympanic
bullae.
(4) Halocercus sp.
The nematode Halocercus is a lungworm (Metastrongyle) that affects dolphins and porpoises.
These parasites inhabit the small bronchi and bronchioles. Heavily infected animals may develop a
neutrophilic and eosinophilic bronchopneumonia. These parasites form granulomas within the
bronchioles, which become encapsulated and calcify. The bronchopneumonia is often accompanied by
hypertrophy of the smooth muscles of the terminal bronchioles. The life cycle of this lungworm is
unknown, but believed to be direct. Infections of young dolphins with these parasites also suggests
transplacental transmission of the parasite.
(5) Crassicauda sp.
These nematodes are commonly found in the pterygoid air sinus and are associated with erosions
of the pterygoid bone. Migration of this organism to the brain or tympanic bulla can lead to CNS lesions
and strandings of affected animals. Crassicauda sp. have been found in the mammary gland, air sinuses,
blubber and muscle.
Digestive Tract
(1) Braunina cordiformis
This fluke is usually observed in the second chamber of the stomach of Atlantic bottlenosed
dolphins. It causes minimal damage and irritation to the gastric mucosa. The fluke, when attached to the
gastric mucosa, has a characteristic urn shaped appearance (5 mm x 5mm) in the lumen of the stomach.
18
(2) Pholeter gastrophilus
Pholeter gastrophilus is another fluke observed in the second chamber of the stomach of dolphins.
This parasite buries deep in the submucosa, forming prominent small black cavitary nodules that can be
identified on palpation. The mucosa usually remains intact over these parasitic nodules. The nodules
have abundant fibrous connective tissue surrounding the parasite with a variable granulomatous and
eosinophilic inflammatory reaction. These flukes have prominent cuticular spines on the tegument and
yellow, single operculated eggs.
(3) Cyclorchis campula (Also Campula pilliata & C. oblonga)
This is a trematode that primarily inhabits the bile and pancreatic ducts of cetaceans. This parasite
causes extensive irritation of the ducts, with hyperplasia of the ductal epithelium and fibroplasia
developing around the ducts. This chronic irritation may progress to a chronic fibrosing hepatitis and
pancreatitis. Numerous parasites are found in the large dilated pancreatic ducts; the smaller ducts are
usually sclerotic. The fluke has numerous prominent tegumental spines. This parasite, like Nasatrema,
have characteristic small yellow triangular eggs.
19
Miscellaneous Diseases
1. Freshwater and Cetaceans
Cetaceans that are not maintained in ocean sea water (3.4% salt) can develop skin and corneal
lesions. These lesions usually develop in animals that have been maintained for a week or longer in
water containing less than 1% salt. These lesions are characterized by areas of ulceration and necrosis of
the epidermis and corneal opacity. Histologically, the lesion is characterized by ballooning degeneration
of the stratum externum (parakeratotic layer). Later the entire thickness of the epidermis becomes
necrotic and/or ulcerated. If these animals are placed back into normal sea water, recovery usually
occurs.
2. Pinniped Hyponatremia
This is a problem observed primarily in seals. This disorder is characterized by a decline (either
sudden or gradual) in blood sodium levels and is observed primarily in animals held in fresh water. It is
brought on by various stresses or disease (i.e., Vitamin E deficiency). Clinically, affected animals
demonstrate one or more of the following signs: lethargy, ataxia, head and body shaking, convulsions,
and sudden death. Diagnosis is confirmed by finding blood sodium levels between 120 and 147 mEq/L
(normal, 150 to 160 mEq/L). Salt administration is the treatment of choice in affected animals.
3. Thiamine Deficiency
Thiamine deficiency has been observed in both pinnipeds and cetaceans. This deficiency is
associated with the ingestion of thiaminase-containing fish (herring, smelt, capelin). Clinically, these
animals develop anorexia, irregular breathing, and unresponsiveness to touch, noise, and light
stimulation. Untreated animals develop central nervous system signs (tremors and spasms, capable of
leading to death). It does not appear that any consistent histologic lesions are associated with thiamine
deficiency in these animals. It has been reported that affected sea lions had a dilated left ventricle and
myelin sheath degeneration of the peripheral and vagus nerves. Treatment and prevention are by the use
of thiamine supplements in the diet.
4. Vitamin E Deficiency
Vitamin E deficiency develops in marine mammals that are fed improperly stored fish that are high
in unsaturated fatty acids. This deficiency is felt to cause both muscle degeneration and steatitis. Seals
are the marine mammal most commonly affected. Affected animals are usually anorectic, reluctant to
move, and have an arched posture. Histologically, the muscles are undergoing degeneration and
necrosis. Steatitis has been observed in California sea lions and Amazon River dolphins. These animals
developed a fatal condition characterized by weakness and generalized subcutaneous nodules of fat
necrosis. Vitamin E supplements aid in the prevention of the disease and should be established on the
basis of fat content of the fish, storage, and method of preparation and feeding. Since the viscera of fish
contain more vitamin E than the flesh, it is preferable to feed whole fish instead of eviscerated fish. It is
important to remember that pinnipeds suffering from vitamin E deficiency are more likely to develop
hyponatremia. Treatment of choice for seals with hyponatremia is vitamin E supplementation and the
addition of salt to the diet.
5. Capture Myopathy
20
Exertional rhabdomyolysis has been noted in captive marine mammals during capture, restraint,
and transportation. These animals develop skeletal muscle degeneration and necrosis. It is felt that low
or deficient levels of vitamin E may play an important role in the development of this condition.
6. Scombroid Poisoning
Scombroid poisoning is a condition in man and marine mammals associated with the ingestion of
poorly preserved scombroid fish (tuna and mackerel). Clinically, affected animals develop nonspecific
signs (inappetence, debilitation, irritable behavior, gastric ulcers, and pulmonary edema), which
disappear on change of diet. Animals that have ingested this poorly preserved fish usually recover. One
should always use caution when feeding scombroid fish. Ensure that these fish have been stored frozen
for less than four months.
7. Microphthalmia and Freshwater Dolphins
Many species of freshwater dolphin (particularly the Ganges River dolphin) have microphthalmia
and apparent blindness. This is a normal finding in these animals. Histologically, these eyes have a
minimal slit-like opening between the eyelids and a microphthalmic eyeball. The eye is nonfunctional
and has a thick cornea, iris, ciliary body, retina, and optic nerve.
8. Disaccharide Intolerance in Pinnipeds
Pinnipeds have no tolerance for dietary disaccharides, including both lactose and sucrose. If
abandoned pups are fed formula high in sugars, diarrhea develops; as the intolerance progresses, a
dermatitis develops and death follows. It appears that pinniped milk does not contain lactose or any
other carbohydrate. These animals lack enzymes in the intestine to properly degrade these sugars.
Formulas composed of fish or marine products containing a high fat content and only simple sugars
should be used when feeding abandoned pups.
9. Cutaneous Gout
The Amazon dolphin (Inia geoffrensis) has higher serum uric acid levels than other cetaceans (10
mg/dl, which is approximately 10 times higher than that reported for other cetaceans). One Amazon
dolphin developed near the base of the flippers an ulcerative dermatitis that was characterized by a
granulomatous inflammatory reaction associated with numerous urate crystals in the tissue. The animal
was treated with allopurinol over a 6 month period. The treatment decreased the animal's serum uric
acid concentration and healed the lesions.
10. Heat Prostration
Since cetaceans have a thick layer of blubber surrounding their body, dissipation of heat can be a
serious problem in stranded animals. Stranded animals need to be kept shaded, cool and moist at all
times. Ideally they should be kept out of the sun to prevent sunburn. Once an animal is stranded and left
out of water in the sun, its body temperature greatly increases causing serious problems for the animal.
Animals that die of heat prostration usually demonstrate diffuse edema and congestion of the lungs.
11. Sunburn in Cetaceans
Cetaceans need to have their skin protected from the direct affects of the sun. Animals that are
either out of the water due to stranding or for physical examination need to be monitored to protect them
from the sun. Sun screens (zinc oxide) can be useful in protecting these animals. Animals that are
sunburned have ballooning degeneration of the epidermis which, in severe cases, can ultimately lead to
necrosis of the epidermis.
21
12. Sea Otter Hemorrhagic Gastroenteritis
The cause of sea otter hemorrhagic gastroenteritis is unknown. This disease is usually observed in
severely stressed or debilitated animals. Affected animals develop a severe bloody diarrhea and are
usually depressed and anoretic. Most affected animals usually die.
At necropsy the only lesion observed is blood in the entire intestinal tract extending from the
duodenum to the rectum. Histologically, there is little damage to the intestinal mucosa: prominent
pooling of blood in the mucosa and submucosa is often observed. Isolation of bacteria from the lesion
have failed to identify a specific bacterial agent. The pathogenesis of this lesion is unclear. It is felt that
the gastrointestinal tract may act as a shock organ with pooling of blood into the intestinal mucosa and
diapedesis of blood into the intestinal lumen.
13. Nephrolithiasis in Pinnipeds
The finding of kidney stones in seals is a common finding. These stones appear to be incidental
findings in many seals and are considered of little pathologic significance.
14. Trauma
Trauma due to shark bites, whale bites, or man-made actions such as shooting or boat strikes can
be observed in all marine mammals. Shark bites are often characterized by parallel rake or bite marks on
the body.
15. Cardiomyopathy in Pygmy and Dwarf Sperm Whales
A cardiomyopathy involving the right ventricle has been observed in pygmy (Kogia breviceps) and
dwarf (Kogia simus) sperm whales. This lesion has been observed primarily in adult animals. Grossly,
the right ventricle is enlarged and flabby. Histologically there is moderate to focally extensive
myocardial fibrosis involving the right ventricle and ventricular septa. Myofiber degeneration
characterized by hyaline change and loss of striations is frequently associated with the fibrosis.
Occasionally remaining myofibers demonstrate crisscrossing or whirling patterns, and myofiber
hypertrophy with enlarged nuclei and nucleoli and sarcoplasmic lipofuscinosis. No changes were
observed in the coronary arteries, endocardium, pericardium or aorta. Most livers have centrolobular
hepatocellular loss and/or necrosis suggestive of right side heart failure. The cause of this lesion is
unknown.
16. Vaginal calculi in Dolphins
Vaginal calculi have been observed in the common, Pacific white-sided and spotted dolphins.
These calculi become very large, exhibit concentric crystallized layers and contain calcium phosphate
compounds. These calculi are found associated with the cervix, pseudocervix, and vagina. Most calculi
contain fetal bones which suggests that parts of the fetal skeleton become entrapped in this location and
crystallize.
17. Northern Elephant Seal Skin Disease (NESSD)
Northern elephant seal skin disease (NESSD) is a skin condition of unknown etiology involving
young seals less than 2 years of age. The skin lesions are characterized by variably sized areas of
alopecia and hyperpigmentation with variably sized areas of epidermal ulceration and necrosis.
Microscopically the lesions are characterized by an ulcerative dermatitis with marked hyperkeratosis of
the epidermis and follicular epithelium, acanthosis and sebaceous gland metaplasia and atrophy. Some
follicular dilatation with prominent amounts of keratin within the dilated follicle has also been observed.
22
Secondary suppurative inflammation due to bacterial infections are common. Diseased seals have
depressed thyroxine, triodothyroxine, retinol, serum iron, albumen, calcium and cholesterol levels.
Alanine aminotransferase, aspartate aminotransferase, lactate dehydrogenase, gamma glutamyl
transpeptidase, BUN, and uric acid were elevated. Diseased seals are usually smaller in size (15%
smaller) than non-affected animals. Affected animals have elevated serum polychlorinated biphenyl
(PCB) and p,p’ dichloro-diphenyl-dichloroethane (p.p’DDE; a metabolite of DDT) levels. Lesions
observed in affected animals are similar to those observed in PCB toxicosis.
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21)
22)
23)
24)
Viral Diseases
Barr B: Herpes-like viral dermatitis in a Beluga whale (Delphinapterus leucas). J. Wild Disease,
25(4): 608, 1989.
Barret T: Dolphin and porpoise morbillivirus are genetically distinct from phocine distemper
virus. Virology, 193:1010-1012, 1993.
Barret T: Morbilliviruses in aquatic mammals: Report on round table discussion. Vet
Microbiology. 44(2-4):261-265, 1995.
Barret T: Morbillivirus infections with special emphasis on morbilliviruses of carnivores. Vet
Microbiology 69(1-2):3-13, 1999.
Bergman A: Pathological findings indicative of distemper in European seals. Vet Microbiology,
23:331-341, 1990.
Birkun A: Epizootic of morbilliviral disease in common dolphins (Delphinus delphis ponticus)
from the Black Sea. Vet Record 144(4):85-92, 1999.
Blanchard T: Disseminated herpesviral infection in a bottlenosed dolphin. American College of
Veterinary Pathologist 49th Annual meeting, St. Louis, MO. 35:(5):435, 1998.
Blixenkrone-Moller M: Infection studies in mink with seal-derived morbillivirus. Arch. Virol.
106:165-170, 1989.
Borst GHA: An outbreak of a herpesvirus infection in harbor seals (Phoca vitulina). J Wild Dis
22(1):1, 1986.
Bossart GD: Hepatitis B-like infection in a Pacific white-sided dolphin (Lagenorhynchus
obliquidens). JAVMA, 196(1): p. 127, 1990.
Bossart GD: Acute necrotizing enteritis associated with suspected coronavirus infections in three
harbor seals. J Zoo and Wild Med. 21(1):84, 1990.
Bostock CJ: Characterization of the European seal morbillivirus. Vet. Micro. 23:351-360, 1990.
Britt JO: Acute viral hepatitis in California sea lion. JAVMA, 175:921, 1979.
Callon RJ: The appearance of H3 influenza viruses in seals. Journal of General Virology,
76:199-203, 1995.
Daoust PY: Phocine distemper in a harp seal (Phoca groenlandica) from the Gulf if St.
Lawrence, Canada. J Wildl Dis 29(1):114-117, 1993.
Daoust PY: Herpesvirus in botryomycotic lesions from a harp seal (Phoca groenlandica). Vet
Path. 31(3):385-387, 1994.
De Guise S: Gastric papilloma in eight St. Lawrence Beluga whales (Delphinapterus leucas). J
Vet Diag Invest 6:385-388, 1994.
Dierauf L.A.: Viral hepatitis (Adenovirus) in a California sea lion, JAVMA, 179: 1194, 1981.
Di Guardo G: Post mortem investigations on cetaceans found stranded on the coast of Italy
between 1990-1993. Vet Record 136(17):439-442, 1995.
Duigan PJ: Phocine distemper in harbor seals (Phoca vitulina) from Long Island, New York. J
Wildl Dis 29(3):465-469, 1993.
Duigan PJ: Epizootiology of morbillivirus infection in North American harbor seals (Phoca
vitulina) and grey seals (Halichoerus grypus). J Wildl Dis 31(4):491-501, 1995.
Duigan PJ: Morbillivirus infection in cetaceans of the western Atlantic. Vet Microbiolog. 44(23):241-249, 1995.
Domingo M: Pathologic and immunocytochemical studies of morbillivirus infection in Striped
Dolphins (Stenella coeruleoalba). Vet Path. 29:1-10, 1992.
Duignan PJ: Morbillivirus infection in two species of Pilot Whales (Globicephala sp.) From the
Western Atlantic. Mar Mammal Sci. 11:150-162, 1995.
24
25)
26)
27)
28)
29)
30)
31)
32)
33)
34)
35)
36)
37)
38)
39)
40)
41)
42)
43)
44)
45)
46)
47)
48)
49)
50)
51)
52)
Duignan P: Epizoology of Morbillivirus infection in Harp, Hooded and Ringed seals from the
Canadian Arctic and Western Atlantic. J Wild Dis 33(1):7-19,1997.
Duignan P: Morbillivirus infection in two species of pilot whale (Globicephela sp.) from the
Western Atlantic. Marine Mammal Sci. 11(2):150-162, 1995.
Duignan P: Morbillivirus infection in manatees. Marine Mammal Sci. 11(4):441-451, 1995.
Fowler ME: Zoo and Wild Animal Medicine, W. B. Saunders Co., Philadelphia, PA, 1986.
Frey HR: Herpesvirus in harbor seals (Phoca vitulina), isolation, partial characterization and
distribution. J Vet Med 36:699, 1989.
Gage LJ: Clinical signs of San Miguel seal lion virus in debilitated California sea lions. J Zoo
and Wild Med 21(1):79, 1990.
Gaskell R: Herpesvirus of carnivores. Vet Microbiology 69:73-88, 1999.
Geraci JR: Dolphin Pox: A skin disease of cetaceans. Can J Comp Med. 43: 399, 1979.
Geraci JR: Mass mortality of harbor seals: Pneumonia associated with influenza virus. Science.
215:1129, 1982.
Gulland FMD: Herpes virus infection in stranded Pacific harbor seals of coastal California. J
Wild Dis 33(3):450-458, 1997.
Hall AJ: Morbilliviruses in Marine Mammals. Trends Microbiology, 3(1):4-9, 1995.
Harder T.: Morbillivirus infections of seals during the 1988 epidemic in the Bay of Heligoland.
J. Vet. Med. 37: 644-650, 1990.
Harder T: Characterization of Phocid Herpesvirus 1 and 2 as Putative Alpha and Gammaherpesvirus of North American and European Pinnipeds. J Gen Viol 77(1):27-35, 1996.
Hicks SD: Seal pox in captive grey seals and their handlers, J Wild Dis, 23:1, 1987.
Horvat B: Herpesvirus in harbor seals (Phoca vitulina): Transmission in homologous Host. J Vet
Med 36:715, 1989.
Howard EB: Pathology of Marine Mammal Diseases, CRC Press, Boca Raton, FL, 1983.
Jauniaux T: Lesions of morbillivirus infection in a fin whale (Balaenoptera physalus) stranded
along the Belgian coast. Vet Record 143(15):423-424, 1998.
Kennedy S: A review of the 1988 European seal morbillivirus epizootic. Vet Record, 127:563567, 1990.
Kennedy S: Histopathologic and immunocytochemical studies of distemper in harbor porpoises.
Vet Path, 28:1-7, 1991.
Kennedy S: Histopathology and immunocytochemical studies of distemper in seals. Vet Path
26:97-103, 1989.
Kennedy S: Viral distemper now found in porpoises. Nature, 336:21, 1988.
Kennedy S: Mass die off of Caspian seals caused by a canine distemper virus. Emerging
Infectious Diseases. 6:637-639, 2000.
Kennedy-Stoskopf S: Isolation of a retrovirus and a herpesvirus from a captive California sea lion.
J Wild Dis 22:156, 1986.
Lapointe JM: Placentitis due to Coxiella burnetii in a Pacific harbor seal (Phoca vitulina
richardsi). J Vet Diag Invest 11:541-543, 1999.
Lambertsen RH: Genital papillomatosis in sperm whale bulls. J Wild Dis. 23:361, 1987.
Liess B: Morbillivirus infection among seals (Phoca vitulina) during the 1988 epidemic in the Bay
of Heligoland. J Vet Med 36:709, 1989.
Kennedy S: Morbillivirus infection in aquatic mammals. J Comp Path 119:201-225, 1998.
Lipscomb TP: Morbilliviral disease in Atlantic bottlenosed dolphins (Tursiops truncatus)
in the 1987-1988 Epizootic. J Wildl Dis 30:567-571, 1994.
25
53)
54)
55)
56)
57)
58)
59)
60)
61)
62)
63)
64)
65)
66)
67)
68)
69)
70)
71)
72)
73)
74)
75)
Lipscomb TP: Morbillivirus epizootic in bottlenosed dolphins of the Gulf of Mexico. J Vet Diag
Invest. 8:283-290, 1996.
Lipscomb T.P: Morbilliviral disease in an Atlantic bottlenosed dolphin (Tursiops truncatus) in the
Atlantic and Gulf of Mexico epizootics by PCR based assay. J Wildl Dis. 31: 410-415,1995.
Lipscomb TP. Metastatic carcinoma of California sea lions: Evidence of genital origin and
association with a gamma-herpesvirus infection. American College of Veterinary Pathologist 49th
Annual meeting. 1998, Vet Path 35(5):421,1998.
Martineau D.: Pathology of stranded Beluga whales from the St. Lawrence estuary, Quebec,
Canada. J. Comp. Path. 98: 287, 1988.
Migaki G.: Selected dermatoses of marine mammals. Clinics in Dermatology 5: 155, 1987.
Momaev L.V.: Characterization of morbillivirus isolation from Lake Baikal seals (Phoca sibirica).
Vet Microbiology. 44(2-4):251-259, 1995.
Neill J.D.: Development of PCR primers for specific amplification of two distinct regions of the
genomes of San Miguel sea lion and Vesicular Exanthema of swine viruses. Mol and Cell Probes.
9:33-38,1995.
Nettleton P.F.: Isolation of a Parapox from a grey seal (Halichoerus grypus). Vet record.
137(22):562-564, 1995.
Nielsen O.: A morbillivirus antibody survey of Atlantic walrus, narwal, and beluga in Canada.
Journal Wildlife Diseases 36(3):508-517, 2000.
Orlich M.: Trypsin resistant protease activation mutants of an influenza virus. J General Virology.
76: 625-633, 1995.
Osterhaus A.D.M.E.: Mass mortality in seals caused by a newly discovered virus-like
morbillivirus. Vet. Micro. 23: 343-350, 1990.
Osterhaus A.D.M.E.: The isolation and partial characterization of a highly pathogenic herpesvirus
from the harbor seal (Phoca vitulina). Arch of Viol. 86: 239, 1985.
Osterhaus A.D.M.E.: Isolation of a parapoxvirus from pox-like lesions in grey seals. Vet Record.
Page 601-602, Dec 17 1994.
Osterhaus A.D.M.E.: Isolation of an Orthopox virus from pox -like lesions of a grey seal. Vet
Record. 127: 191-192, 1990.
Osterhaus A.D.M.E.: Morbillivirus infections of aquatic mammals: Newly identified members of
the genus. Vet Microbiology. 44(2-4): 219-227, 1995.
Osterhaus A.D.M.E.: Influenza B virus in seals. Science 288:1051-1053, (May 12), 2000.
Sawyer J.C.: Vesicular exanthema of swine and San Miguel sea lion virus. JAVMA, 169; 707,
1976.
Scheiblauer H.: Pathogenicity of Influenza A/Seal/Mass/1/80 virus mutants for mammalian
species. Arch Viol. 140(2):341-348, 1995.
Seal B.S.: Analysis of serologic relationship among SMSV and VESV isolates. Application of
Western blot assays for detection of antibodies in swine sera to these virus types. J. Vet. Diagn.
Invest. 7(2):190-195, 1995.
Skillings D.E.: First isolation of a calicivirus from the Steller sea lion (Eumetopias jubatus). J
Wild Dis. 23: 534, 1987.
Smith A.W.: Calicivirus-induced vesicular disease in cetaceans and probably interspecies
transmission. JAVMA. 183: 1223-1225, 1983.
Smith A.W.: Regression of cetacean tattoo lesions concurrent with conversion of precipitin
antibody against a poxvirus. JAVMA, 183: 1219, 1983.
Smith A.W.: Calicivirus induced vesicular disease in cetaceans and probable interspecies
transmission. JAVMA. 183: 1223, 1983.
26
76)
77)
78)
79)
80)
81)
82)
83)
84)
85)
86)
87)
88)
89)
90)
91)
92)
93)
94)
95)
96)
97)
98)
Smith A.W.: Virus and viral diseases of marine mammals. JAVMA. 175: 918, 1979.
Smith A.W.: Isolation and identification of five new serotypes of caliciviruses from marine
mammals. AJVR. 42: 693, 1981.
Smith A.W.: Caliciviruses of ocean origin: A review. J. Zoo and Wild Med. 21(1): 3, 1990.
Stack M.J.: Mixed parapox and calicivirus infections of grey seals(Halichoerus grypus) in
Cornwall. Vet. Record. 132: 163-165, 1993.
Sweeney J.C.: Common disease of pinnipeds. JAVMA. 165: 805, 1974.
Taubenberger J.K: Two morbilliviruses implicated in bottlenosed dolphins epizootics. Emerging
Infectious Diseases. 2(3): 213-216, 1996.
Webster R.G. Characterization of an influenza A virus from seals. Virology 113:712-724,1981.
Webster R.G.: Conjunctivitis in human beings cause by Influenza A virus of seals. New Journal
of Medicine 304:911,1981.
Wilson T.W.: Pox in young, captive harbor seals. JAVMA. 161: 611, 1972.
Wilson T.W.: Morphologic studies of seal pox virus. J Wild Dis. 6: 94, 1970.
Wilson T.W.: Pox in a South American sea lion. Can J Comp Med. 35: 174, 1974.
Wilson T.W.: Pox in a captive harbor seal. JAVMA. 161: 611, 1972.
Van Bressen M.F.: Morbillivirus infection in Mediterranean Striped Dolphins.(Stenella
coernulwalba). Vet Record. 12: 471-472, 1991.
Visser I.K.G.: Characterization of morbilliviruses isolated from dolphins and porpoises in
Europe. Journal of General Virology. 74: 631-641, 1993.
Visser I.K.G.: Continued presence of phocine distemper virus in the Dutch Wadden Sea seal
population. Vet. Record. 133: 320-322, 1993.
Visser I.K.G.: Prevalence of morbilliviruses among pinniped and cetacean species.
Rev Sci Tech Off. Int. Epiz. 12(1):197-202, 1993.
Van Bressem M.F.: Morbillivirus infection in Mediterranean Striped Dolphins (Stenella
caeruleoalba). Vet Record. 129: 471-472, 1991.
Van Bressem M.F.: Genital and lingual warts in small cetaceans from coastal peru. Disease of
Aquatic Organisms. 26:1-10, 1996.
Van Bressem M.F.: Genital disease in the Peruvian Dusky dolphin (Lagenorhynchus obscurus). J.
Comp Path 122:266-277, 2000.
Van Bressem M.F.: A review of virus infections of cetaceans and the potential impact of
morbilliviruses, pox viruses, and papillomaviruses on host population dynamics. Dis of Aquatic
Organisms 38:53-65, 1999.
Van de Bildt MW.: Morbilliviruses in Mediterranean monk seals. Vet Microbiology 69(1-2):1921, 1999.
Van de Bildt M.W.: Identification of morbilliviruses of probable Cetacean origin in carcasses of
Mediterranean monk seals (Monachus monachus). Vet Record (June 10, 2000)146:691-694,
2000.
Zarnke R.L.: Serologic survey for phocid herpesvirus-1 in marine mammals form Alaska and
Russia. J. Wild. Dis. 33(3)459-465, 1997.
Bacterial Diseases
1)
Baker J.R.: Pathology and bacteriology of adult male Antarctic fur seals, Arctocephelus gazella,
dying at Bird Island, South Georgia. Br. Vet. J. 145:263-275, 1989.
27
2)
3)
4)
5)
6)
7)
8)
9)
10)
11)
12)
13)
14)
15)
16)
17)
18)
19)
20)
21)
22)
23.
24)
25)
26)
27)
28)
29)
Baker J.R.: Isolation of salmonellae from seals from UK waters. Vet. Record. 136: 471-472,
1995.
Boever W.: Mycobacterium chelonei infection in a Natterer Manatee. JAVMA. 169: 927-929,
1976.
Buck J.D.: Clostridium perfringens as the cause of death of a captive Atlantic bottle-nosed
dolphin (Tursiops truncatus). J. Wild. Dis. 23: 488, 1987.
Colgrove, G.S.: Cerebral abscess associated with stranding in a dolphin. J. Wildlife Disease.
12:271-274, 1976.
Cousin D.V.: ELISA for the Detection of tuberculosis in seals. Vet Record. 121: 305, 1987.
Cousin D.V.: Tuberculosis in captive seals: Bacteriological studies on an isolate belonging to the
Mycobacterium tuberculosis complex. Res. Vet. Sci. 48:196-200, 1990.
Cousin D.V.: Tuberculosis in wild seals and characterization of the seal bacillus. Aust. Vet. J.
7:92-97, 1993.
Diamond S.S.: Fatal bronchopneumonia and dermatitis caused by Pseudomonas aeruginosa in an
Atlantic bottlenosed dolphin. JAVMA. 37(3):303-305, 1979.
Dierauf L.A.: An epizootic of Leptospirosis in California sea lions. JAVMA. 187:1145, 1985.
Enalt D.R.: Characteristics of a Brucella species from a bottlenosed dolphin (Tursiops truncatus).
J. Vet Diagn Invest. 6:448-452 , 1994.
Fowler M.E.: Zoo and Wild Animal Medicine, W.B. Saunders Company, Philadelphia, PA, 1986.
Foster G.: Isolation of Brucella species from cetaceans, seals and an otter. Vet Record.
138(24): 583-586, 1996.
Forshaw D.: Tuberculosis in a captive colony of pinnipeds. J. Wild. Dis. 27:288-295, 1991.
Garner M.M.: Evidence of Brucella infection in Parafilaroides lungworms in a Pacific harbor seal
(Phoca vitulina richardsi). J. Vet. Diagn. Invest. 9:298-303,1997.
Greenwood A. G. Clostridial myositis in marine mammals. Vet Record. July 15 1978, p54-55.
Geraci J.R.: Erysipelas in dolphins. AJVR. 27:597, 1966.
Gilmartin W.G.: Salmonella in feral pinnipeds off the Southern California coast. J. Wild. Dis.
15:511, 1979.
Gulland F.M.D.: Leptospirosis in California sea lions (Zalophus californianus) stranded along the
central California coast, 1981-1984. J. Wild. Dis. 32(4): 572-580, 1996.
Gutter A.E.: Generalized mycobacteriosis in a California sea lion (Zalophus californianus). J.
Zoo. Anim. Med. 18: 118-120. 1987.
Howard E.B.: Pathobiology of Marine Mammal Diseases. CRC Press, Boca Raton, FL, 1983.
Jahans K.L. The Characterization of Brucella strain isolated from marine mammals. Vet Micro
57:373-382, 1997.
Joseph B.E.: Valvular endocarditis in a Northern sea otter(Enhydra lutris). J. Zoo and Wild. Med.
21: 88-91, 1990.
Kettener P.S. Septic embolic nephritis in a dolphin caused by Staphylococcus aureus. Australian
Vet. Journ. 50: 123, 1974.
Keyes M.C.: Pathology of the Northern fur sea., JAVMA. 147: 1090, 1965.
Kinsel M. J. Fatal Erysipelothrix rhusiopathiae septicemia in a captive Pacific white-sided dolphin
(Larenorhyncus obliquidens) J. Zoo and Wildlife Medicine: 28(4): 493-497, 1997.
Medway W.: Some bacterial and mycotic diseases of marine mammals. JAVMA. 177:831, 1980.
Medway W.: Respiratory problem in captive small cetaceans. JAVMA. 163:571-573, 1973.
Miller WG.: Brucella induced abortions and infections in bottlenose dolphins (Tursiops truncatus).
J Zoo Wildl Medicine 30(1):100-110, 1999.
28
30)
Morales, P.: Systemic Mycobacterium marinum infection in an Amazon manatee. JAVMA.
187:1230, 1985.
31) Patterson I.A. P. Brucella infections in marine mammals from Scottish waters, 2000 Proceedings
AAZV and IAAAM Joint Conference.
32). Pier A.C. Cetacean Nocardiosis. J Wildl disease 6: 112-118, 1970.
33) Ramano M.I.: Genetic characterization of Mycobacteria from South American wild seals. Vet.
Micro. 57 (1-2): 89-98, 1995.
34) Rand C.S. Nodular suppurative cutaneous cellulitis in a Galapagos sea lion. Journal of wildlife
diseases 11: 325-329, 1975.
35) Ross H.M.: Brucella species infection in sea mammals. Vet Record. 134 (14): 359, 1994.
36) Ross H.M.: Brucella species infection in North Sea seal and cetacean populations. Vet Record.
138 (26): 647-648, 1996.
37) Siebold H.R.: Erysipelothrix septicemia in the porpoise. JAVMA. June 1, 537-539, 1956.
38) Simpson C.F.: Cutaneous lesions in a porpoise with erysipelas. JAVMA. 133: 558, 1958.
39) Smith A.W.: A preliminary report on potentially pathogenic microbiological agents recently
isolated from pinnipeds. J. Wildl. Disease 10:54-59, 1974.
40) Smith A.W.: Naturally occurring Leptospirosis in Northern Fur Seals. J. Wild. Dis. 13: 144,
1977.
41) Smith A.W.: Leptospira pomona, and reproductive failure in California sea lions. JAVMA. 165:
996, 1974.
42) Stroud R.K. Salmonella meningoencephalitis in a Northern fur seal (Callorhinus ursinus). Journal
of wildlife Diseases 16: 15-18., 1980.
43) Sweeney J.C. Survey of Diseases in free-living California sea lions. Journal of Wildlife Disease
10: 370-376, 1974.
44) Sweeny J.C.: Common diseases of pinnipeds. JAVMA. 165: 805, 1974.
45) Sweeney J.C.: Common disease of small cetaceans. JAVMA. 167:533-540, 1975.
46) Stadlander C.T.: Characterization of cytopathogenicity of aquarium seal mycoplasmas and seal
Finger Mycoplasmas by light and scanning electron microscopy. Int J Med Microbiol Viral
Parasital Infect Disease. 280 (4):458-467-1994.
47) Streitfeld M.M.: Staphylococcus aureaus infections of captive dolphins (Tursiops truncatus and
oceanarium personnel. AJVR 37 (3): 303-305, 1976.
48) Stoskopf M.K.: Tuberculosis in pinnipeds. Proc. Anim. Meet An. Assoc. Zoo Vet. P. 393, 1987.
49) Trudgett A.: Analysis of a seal and a porpoise morbillivirus using monoclonal antibodies. Vet
Record. 128:61, 1991.
50) Tryland M.: Evidence of Brucella infection in marine mammals in the North Atlantic ocean. Vet
record 144(21):588-592, 1999.
51) Varaldo, P.E.: Staphylococcus aureus NOV., a Coagulase positive species Isolated from dolphins.
International Journal of Systemic Bacteriology. 38:436-439, 1988.
52) Vedros N.: Leptospirosis epizootic among California sea lions. Science 179: 1250-1251, 1971.
53) Wells S.K.: Cutaneous mycobacteriosis in a harbor seal: Attempted treatment with hyperbaric
oxygen. J. Zoo and Wild. Med. 21(1): 73, 1990.
54) Woods, R.: Tuberculosis in a wild Australian fur seal (Arctocephalus pusillus dorifesus) from
Tasmania. J. Wildl. Dis. 31(1): 83-86, 1995.
55) Van Pelt R.W.: Staphylococcal infection and toxoplasmosis in a young harbor seal. J. Wildl. Dis.
9: 258, 1973.
29
Mycotic Diseases
1)
2.
3)
4)
5)
6)
7)
8)
9)
10)
11)
12)
13)
14)
15)
16)
17)
18)
19)
20)
21)
22)
Caldwell D.: Lobomycosis as a disease of Atlantic bottlenosed dolphins. Amer J Trop Med Hyg,
24: 105, 1975.
Cornell L.H. Coccidioidomycosis in a California sea otter (Enhydra lutris). J. Wild. Dis 15:373378, 1979.
Carrol J.M. Pulmonary aspergillosis of the bottlenosed dolphin (Tursiops truncatus). Veterinary
Clinical Pathology 2:139-140, 1968.
Dilbone R.P.: Mycosis in a manatee. JAVMA 147: 1095, 1965.
Dunn J.L.: Candidiasis in captive pinnipeds. JAVMA. 185; 1328, 1984.
Dunn J.L.: Candidiasis in captive cetacean. JAVMA. 181; 1316-1321, 1982.
Fauquier D.A. Coccidioidomycosis in free-living California sea lions (Zalophus californianus) in
central California. J. Wild. Dis. 32(4): 707-710, 1996.
Farnsworth R.J. Dermatomycosis in a harbor seal causes by Microsporum canis. Journal of Zoo
Animal Medicine 6:26-27.
Frasco, S.: Mycotic dermatitis in an Atlantic white sided dolphin, a pigmy sperm whale and
two harbor seals. JAVMA. 208 (5) 727-729, 1996.
Medway W.: Some bacterial and mycotic diseases of marine mammals. JAVMA. 177; 831, 1980.
Migaki, G.: Lobo's disease in an Atlantic bottlenosed dolphin. JAVMA. 159; 578, 1971.
Migaki G.: Pulmonary cryptococcoses in an Atlantic bottlenosed dolphin (Tursiops truncatus).
Lab Ani Sci. 28: 603-606, 1978.
Migaki G.: Sporotrichosis in a Pacific white-sided dolphin (Lagenorhynchus obliguidens).
AJVR. 39:1916-1919, 1978.
Montali R.J.: Cyclic dermatitis associated with Fusarium sp. infection in pinnipeds. JAVMA.
179: 1198, 1981.
Nakeeb S. Chronic cutaneous Candidiasis in bottle-nosed dolphins. JAVMA. 171:961-966,
1977.
Reed R.E.: Coccidioidomycosis in a California sea lion (Zalophus californianus). J Wild Dis.
12:372-375, 1976.
Reidarson T. H. Coccidioidomycosis in a bottlenosed dolphin. J Wildlife Dis. 34(3)629-631.
Sweeney J.C.: Common diseases of pinnipeds. JAVMA. 165: 805, 1974.
Sweeney J.C.: Systemic mycosis in marine mammals. JAVMA. 169:946-948, 1976.
Tanaka E.: Dermatophytosis in a Steller sea lion (Eumetopias jubatus). J Vet Med Sci. 56(3):551553, 1994.
Williamson W.M.: North American blastomycosis in a Northern sea lion. JAVMA. Nov. 15,
1959: 513-515.
Wilson T.M.: Histoplasmosis in a harp seal. JAVMA. 165: 815-817, 1974.
30
Protozoal Diseases
1)
Akao, S.: A new species of Sarcocystis parasitic in the whale (Balaenoptera borealis). J.
Protozool. 7:290-294, 1970.
2)
Bishop L.: Parasites related to lesions in a bearded seal. .J Wildl. Dis. 15: 285, 1979.
3)
Brown R.J.: Sarcocystis in the Northern fur seal. J. Wildl. Dis. 10: 53, 1974.
4)
Dailey, M.D.: Parasites and associated pathology observed in cetaceans stranded along the Oregon
coast. J. Wildl. Disease. 14:503, 1978.
5)
Hadwen S.: Cyst forming protozoa in reindeer and caribou and a Sarcosporidian parasite of the
seal (Phoca richardi). JAVMA. 61: 374-382, 1922.
6)
Buergelt C.D.: Toxoplasmic meningoencephalitis in a West Indian manatee. JAVMA. 183: 1294,
1983.
7)
Holshuh H.J.: Toxoplasmosis in a feral Northern fur seal. JAVMA. 187: 1229, 1987.
8)
Howard E.B.: Pathology of Marine Mammal Disease. CRC press, Boca Raton, Fl., 1993.
9)
Inskeep W.: Toxoplasmosis in Atlantic bottlenosed dolphins (Tursiops truncatus). J Wild
Disease. 26: 377-382, 1990.
10) Measures LN.: Giardiasis in Pinnipeds from Eastern Canada. J Wild Dis 35(4):779-782.1999.
11) Mense G.M.: Acute hepatic necrosis associated with a Sarcocystis canis like protozoa in a sea
lion. (Zalophus californianus). J. Vet Diagn Invest. In press.
12) Migaki G.: Fatal disseminated toxoplasmosis in a spinner dolphin (Stenella longirostris). Vet
Path. 27: 463-464, 1990.
13) Migaki G.: Sarcosporidiosis in a ringed seal. JAVMA. 177: 917, 1986.
14) Migaki G.: Toxoplasma in a California Sea Lion. AJVR. 38: 135, 1977.
15) Munday B.L.: Sarcocystis and related organisms in Australian wildlife. J Wild Dis. 14: 417,
1978.
16) Olson M.E. Giardiasis in ringed seals from the Western Arctic. J. Wild. Dis. 33(3): 646-648,
1997.
17) Rosonke BJ.: Encephalomyelitis associated with a Sarcocystis neurona-like organism in a sea
otter, JAVMA 215(12):1839-1842 1999.
18) Schulman FY.: Dermatitis with invasive ciliated protozoa in dolphins that died during the 19871988 Atlantic bottlenose dolphin morbilliviral epizootic. Vet Path 36:171-174,1999.
19) Van Pelt R.W.: Staphylococcal infection and toxoplasmosis in a young harbor seal. J Wild Dis.
9:258, 1973.
Parasites
1)
2)
3)
4)
Abolla E. Long term recording of gastric ulcers in cetaceans stranded on the Galician (NW Spain)
coast. Diseases of aquatic Organisms 32:71-73,1998.
Bishop L.: Parasite-related lesions in a bearded seal, Erignathus barbatus. J Wild Dis. 15:285,
1979.
Brown R.S.: Lesions associated with fatal hookworm infections in the Northern fur seal. JAVMA.
165: 804, 1974.
Conlogue G.J.: Pediculosis and severe heartworm infection in a harbor seal. Vet Med. 75:11841187, 1980.
31
5)
6)
7)
8)
9)
10)
11)
12)
13)
14)
15)
16)
17)
18)
19)
20)
21)
22)
23)
24)
25)
26)
27)
28)
29)
30)
31)
32)
Conlogue G.J.: Parasites of the Dall’s porpoise (Phocoenoides dalli). J. Wildl Dis. 21:160-166,
1985.
Dailey M.: Parasites and associated pathology observed in cetaceans stranded along the Oregon
Coast. J Wild Dis. 14: 503, 1978.
Dailey M.: Evidence of prenatal infection in the Bottlenosed dolphin (Tursiops truncatus) with the
lungworm Halocercus lagenorhynchi. J Wildl Dis. 27:164-165, 1995.
Dailey M.D.: Parasitism as a factor in single strandings of Southern California cetaceans. J
Parasitology. 64; 593, 1978.
Dailey M.D.: Disease of Mammalia: Cetacea. In Disease of Marine Mammals. Vol IV, Part 2.
O. Kinne (ed.) Biologische Anstaff Helgoland, Hamburg, Germany. 1985, p805-847.
Dunn J.L.: Dipetalonema spirocauda Infection in the Atlantic harbor seals (Phoca vitulina
concolor). J Wild Dis. 12: 531, 1976.
Eley T.J.: Dipetalonema spirocauda In Alaskan marine mammals. J Wild Dis. 17: 65, 1981.
Forrester D.J.: Heartworms in captive California sea lions. JAVMA. 163: 568, 1973.
Fowler M.E.: Zoo and Wild Animal Medicine. W.B. Saunders Company, Philadelphia, PA, 1986.
Garner M.M.: Evidence of Brucella infection in Parafilaroides lungworms in a Pacific harbor seal
(Phoca vitulina richardsi). J. Vet. Diagn. Invest. 9:298-303,1997.
Howard E.B.: Pathobiology of Marine Mammal Diseases, CRC Press Boca Raton, Florida, 1983.
Johnston D.G.: Parasitism in some marine mammals. JAVMA. 155:1064, 1969.
Keyes M.C.: Pathology of the Northern fur seal. JAVMA. 147: 1090, 1965.
Kim K.C.: Population, microhabitat preference and affect of infestation of two species of
Orthohalarachne in the Northern fur seal. J Wild Dis. 16:45,1980.
Koie M. The life cycle of Contracaecum osculatum senso stricto in view of experimental
infections. Parasitology Res. 81(6):481-489,1995.
Lewis R.J.: Brain lesions in a Pacific white-sided dolphin (Lagenorhynchus obliquidens). J. Wild
Dis. 24(3): 77, 1988.
Lyons E.: Uncinariasis in Northern fur seals and California sea lion pups from California. J. Wild
Dis. 33(4): 848-852, 1997
Medway W.: Dirofilaria immitis infection in a harbor seal. JAVMA. 167: 549, 1975.
Migaki G.: Hepatic trematodiasis in a Ganges River dolphin. JAVMA. 175: 926, 1979.
Migaki G.: Some histopathological lesions caused by helminths of marine mammals. J Wild Dis.
7: 281, 1971.
Morales G.A.: Verminous pneumonia in California sea lions. Vet Path. 7: 89, 1970.
Morimitsu T.: Mass stranding of Odontoceti caused by parasitogenic eight cranial neuropathy. J
Wild Dis. 23: 586, 1987.
Moser M.: The lungworm Halocercus spp. In cetaceans from California. J. Wildl, Dis. 29(3):507508, 1993.
Olsen S.W.: Life cycle of Uncinaria lucasi stiles, 1901 (Nematoda: Ancylostomatidae) of fur
seals, Callorhinus ursinus, on the Pribilof Islands, Alaska. J Parasitology. 51:689, 1965.
O'Shea T.J.: Nasitrema associated encephalitis in striped dolphin (Stenella caeruleoalba)
stranded in the Gulf of Mexico. J. Wild Dis. 27(4):706-709, 1991.
Parker G.A.: Cerebral trematodiasis in a dolphin. Mil Med. 142:861, 1977.
Perry M.L.: A New species of Dipetalonema from the California sea lion and a report of
microfilaria from a Stellar sea lion (Nematoda: Filarioides). J Parasito. 53:1076, 1967.
Ridgeway S.H.: Cerebral and cerebellar involvement of trematode parasites in dolphins and their
possible role in strandings. J. Wild Dis. 8:33-43, 1972.
32
33)
34)
35)
36)
37)
38)
39)
40)
Rausch R.: Studies on the helminth fauna of Alaska. XIII. Diseases in the sea otter, with special
reference to helminth parasites. Ecology. 34: 584-604, 1953.
Schryver H.F.: The stomach fluke Braunina cordiformis in the Atlantic bottlenosed dolphin.
JAVMA. 151: 884-886, 1967.
Stroud R.K.: Parasites and associated pathology observed in pinnipeds stranded along the Oregon
coast. J Wild Dis. 14: 292, 1978.
Sweeny J.C.: Common diseases of pinnipeds. JAVMA. 165: 805, 1974.
Wazura K.W.: Helminths of the beluga whale (Delphinapterus leucas) from the Mackenzie river
delta, Northwest Territories. J Wild Dis. 22: 440-442.
Wild P.W.: A report on the sea otter, Enhydra lutris, in California Department of Fish and Game.
Marine Resources Technical Report No. 20, 1974.
Woodard J.C.: Some parasitic disease of dolphins. Path Vet 6: 257, 1969.
Young P.G.: Larval nematodes from fish of the subfamily Anasakinae. J Comp Path. 79: 301,
1969.
Miscellaneous Disease
1)
2)
3)
4)
5)
6)
7)
8)
9)
10)
11)
12)
13)
14)
15)
16)
Alexander J.W.: Vertebral osteomyelitis and suspected disko-spondylitis in an Atlantic
bottlenosed dolphin (Tursiops truncatus). J Wild Disease 25: 118-121, 1989.
Baker J.R.: Pollution associated uterine lesions in grey seals from the Liverpool Bay area of the
Irish Sea. Vet Record. 125: 330, 1989.
Barnett J.E.F.: Conditions in grey seals (Halichoerus grypus) presented for rehabilitation. Vet
Record 147, 98-104, 2000.
Beckmen K.B.: Clinical and pathological characterization of Northern elephant seal skin disease.
J. Wild. Dis. 33(3): 438-449, 1997.
Bossart G.D.: Invasive gingival squamous cell carcinoma in a California sea lion (Zalophus
californianus). J Zoo and Wild Med. 21: 92-94, 1990
Bossart G.D.: Cardiomyopathy in stranded pygmy and dwarf sperm whales. JAVMA. 187:
11, 1137-1140, 1985.
Citino S.B.: Nutritional myopathy in a captive California sea lion. JAVMA. 187: 1234, 1985.
De Guise S.: Tumors in St. Lawrence beluga whales (Delphinapterus leucas). Vet. Path. 31:444449, 1994.
De Guise S.: Non-neoplastic lesions in beluga whales and other marine mammals from the St.
Lawrence estuary. J. Comp Path. 112: 257-271, 1995.
De Guise S.: Intestinal adenocarcinoma in two Beluga whales (Delphinapterus leucas). Can Vet
J. 36(9): 563-565, 1995.
De Guise S.: Pathology and toxicology of Beluga whales from the St. Lawrence estuary, Quebec,
Canada. Past, present and future. Sci. Total Environ. 154(2-3): 201-215, 1994.
De Guise S.: True hermaphroditism in a St. Lawrence Beluga whale (Delphinapterus leucas). J.
Wildl. Dis. 32(3): 548-551, 1996.
Fowler M.E.: Zoo and Wild Animal Medicine. W.B. Saunders Company, Philadelphia, PA, 1986.
Frasca S.: Acute gastric dilatation with volvulus in a Northern fur seal (Callorhinus ursinus). J.
Wildl. Dis. 32(3): 548-551, 1996.
Garman R.H.: Cutaneous gout in an Amazon dolphin. JAVMA. 1983: 1292, 1983.
Geraci J.R.: Dietary disorders in marine mammals synthesis and new finding. JAVMA. 179:
1183, 1981.
33
17)
18)
19)
20)
21)
22)
23)
24)
25)
26)
27)
28)
29)
30)
31)
32)
33)
34)
35)
36)
37)
Geraci J.R.: Experimental thiamine deficiency in captive harp seals. Can J Zool. 50: 179, 1972.
Geraci J.R.: Hyponatremia and the need for dietary salt supplementation in captive pinnipeds.
JAVMA. 161: 618, 1972.
Geraci J.R.: Thiamine deficiency in seals and recommendations for its prevention. JAVMA. 165:
801-803, 1974.
Geraci J.R.: Tumors in cetaceans: Analysis and new findings. Can J Fish Aquat Sci. 44: 12891300, 1987.
Gulland F.M.: Metastatic carcinoma of probable transitional cell origin in 66 free living California
sea lions, 1979-1994. J. Wildl. Dis. 32(2): 250-258, 1996.
Gulland F.M.: Baseline coagulation assay values for Northern Elephant seals (Mirounga
angustirostris) and disseminated intravascular coagulation in this species. J. Wildl. Dis. 32(3):
536-540, 1996.
Heidel J.R.: Intestinal volvulus in a Bowhead whale, Balaena mysticetus. J. Wildl. Dis. 30(1):
126-128, 1994.
Hirst L.W.: Pathologic findings in the anterior segment of the pinniped eye. JAVMA. 183:
1226-1231, 1983.
Howard E.B.: Pathobiology of Marine Mammal Diseases, CRC Press, Boca Raton, Florida, 1983.
Martineau D.: Pathology of stranded Beluga whales (Delphinapterus leucas) from the St.
Lawrence Estuary, Quebec, Canada. J Comp Path. 98: 287-311, 1988.
Martineau D.: Transitional cell carcinoma of the urinary bladder in a Beluga whale
(Delphinapterus leucas). Can Vet J. 26: 297-302, 1985.
Martineau D.: Pathology and toxicology of beluga whales from the St. Lawrence estuary,
Quebec, Canada, Past, present and future. Science of the Total Environment. 154: 201-215,
1994.
Migaki G.: Renal adenoma in an Atlantic bottlenosed dolphin. AJVR. 39: 1920-1921, 1978.
Miller G.J.: Ecotoxicology of petroleum hydrocarbons in the Marine environment. J Applied
Tox. 2: 88-97, 1982.
Morimitsu T. Histopathology of eighth cranial nerve of mass stranding dolphins at Gato Island.
Japan. J Wildl Dis. 28(4): 656-658, 1992.
Shlosberg A.: Lead toxicosis in a captive bottlenosed dolphin (Tursiops truncatus) consequent to
ingestion of air gun pellets. J. Wild. Dis. 33(1):135-139, 1997.
Stoskopf M.K.: Ocular anterior segment disease in Northern fur seals. JAVMA. 187: 11411145, 1985.
Stroud R.K.: Nephrolithiasis in a harbor seal. JAVMA. 175: 924-925, 1979.
Stroud R.K. Lymphosarcoma in a harbor seal. (Phoca vitulina richardii). J Wildlife Diseases
16:267-270.
White J.R.: Thiamine deficiency in an Atlantic bottlenosed dolphin on a diet of raw fish.
JAVMA. 157: 559, 1970.
Woodhouse CD: Observations of vaginal calculi in dolphins. J Wildl Dis 27(3):421-427, 1991.
34