Abstract
Nasitrema spp. are common trematode parasites which normally inhabit the pterygoid sinuses and tympanic cavities of many species of
small cetaceans. However, ova and occasionally adults of these parasites have also been found damaging the 8th cranial nerve and in the brain and meninges of
several cetacean species (Table 1). It is speculated that in these cases, Nasitrema may play a significant role in the morbidity/mortality of affected
dolphins due to central nervous system dysfunction and disruption of equilibrium or acoustic abilities.
Staff at Mote Marine Laboratory's Dolphin and Whale Hospital have treated three live stranded specimens of the pygmy killer whale, Feresa
attenuata, in the past 5 years. Histological examination of brain tissue from two of the three demonstrated numerous trematode ova in the brain and meninges
of MML 9313, and the meninges of MML 9805, both consistent with Nasitrema sp.
Table 1. Species with reported cranial nerve damage/brain lesions associated with Nasitrema spp.
Species |
Common Name |
Reference |
Delphinus delphis |
Common dolphin |
Cowan et al., 1986 |
Feresa attenuata |
Pygmy killer whale |
Schwab, 1985 |
Globicephala macrorhynchus |
Short finned pilot whale |
Morimitsu et al., 1987 |
Grampus griseus |
Risso's dolphin |
Morimitsu et al., 1992 |
Lagenorhynchus obliquidens |
Pacific white-sided dolphin |
Lewis and Berry, 1988 |
Lissodelphis borealis |
Northern right whale dolphin |
Cowan et al., 1986 |
Peponocephala electra |
Melon-headed whale |
Morimitsu et al., 1986 |
Phocoenoides dalli |
Dall's porpoise |
Cowan et al., 1986 |
Pseudorca crassidens |
False killer whale |
Morimitsu et al., 1987 |
Stenella attenuata |
Pan tropical spotted dolphin |
Forrester, 1991 |
Stenella coeruleoalba |
Striped dolphin |
O'Shea et al., 1991 |
Steno bredanensis |
Rough toothed dolphin |
Forrester, 1991 |
Description of Brain Pathology
MML 9313 ("Lunar")--A 232 cm. male which stranded on 16 Nov. 1993 at
Marco Island, FL. Nasitrema-like ova were associated with focal lesions of the frontal, parietal, and occipital lobes consisting of cortical depletion,
cavitation, and liquefaction necrosis of affected regions. Lesions also involved the subarachnoid space. Parasite ova but not adults were found.
MML 9805 ("Pasco")--A male, 214 cm. in length which stranded at New
Port Richey, FL on 22 Aug 1998. The cerebrum contained subdural aggregates of trematode ova consistent with Nasitrema. The extensive lesions seen in the
previous case were not seen. No adult parasites were seen.
Diagnosis
If present in sputum, gastric, or fecal samples, Nasitrema ova are readily discernible microscopically. The operculated, golden brown
ova measure ~45 microns x ~80 microns and are triangular in cross section. In these two cases very few Nasitrema ova were seen in multiple blowhole,
gastric, and fecal samples. Therefore, relative abundance may not correlate well with severity of infection. In additional cases involving Tursiops
truncatus, blowhole exudates often have a distinctive frothy, mucoid appearance, red-brown in color. This was not observed in the cases reported here.
The premortem diagnosis of brain or auditory involvement associated with these parasites is much more difficult. Magnetic resonance imaging
(MRI) may prove fruitful if the machine can accommodate the animal and motion can be controlled. MRI was attempted with MML 9805. Head motion, however, caused
results of inadequate quality for a diagnosis.
Eosinophilia, which may indicate parasitic infestation, is often offset by stress-induced eosinopenia in stranded cetaceans. In the two cases
mentioned here absolute eosinophil counts were not elevated, ranging from 70-1400.
Therefore, the clinician may need to rely on clinical signs for a tentative diagnosis.
Clinical Signs
Head/Tail Arching (opisthotonus). While being supported in the
water, the whale would strongly dorsiflex into a "U" shape, holding its head and tail upwards for a few seconds, then relaxing to a normal posture. This behavior
may be repeated every few minutes. In cetaceans that are out of water, "arching" is generally considered a sign of severe stress, which may rapidly lead to death.
This was not the case in these two patients, both of whom exhibited this behavior repeatedly.
Head Tilt. Pasco often swam at the pool's surface with his neck
flexed upward at a slight angle.
Disorientation/Loss of Equilibrium. Pasco, when released to
evaluate his swimming ability, would often roll from one side to the other. There was no consistency to which side he would fall. There was no evidence of
pulmonary pathology to explain this behavior which apparently was due to a loss of equilibrium. It has also been reported that a stranded white-sided dolphin swam
in tight circles. This animal too was found to have Nasitrema sp ova in the brain upon postmortem examination3.
Slowed Respiratory Reflexes. The normal reflex to close the
blowhole immediately at the detection of water is of paramount importance to the survival of cetaceans, but was greatly slowed in MML 9805.
Our limited experience with this species indicates that they are voracious eaters. Even so, it is to be expected that the drive to reach
the surface to breathe will predominate over the urge to eat. However, on more than one occasion, Pasco continued to make efforts to weakly swim toward food even
though he was initiating respiration while still underwater and had to be immediately lifted to the surface.
Treatment
If parasites have reached the brain, antiparasitic therapy may be a moot point since any CNS dysfunction is likely to be permanent. However,
Nasitrema has been treated with praziquantel or bithionol. Because of the suspected CNS pathology, we chose to euthanize MML 9805.
Conclusions
CNS disorders may have many etiologies. However, parasitic migration of Nasitrema sp. should be high on the differential diagnosis
list. The CNS symptoms observed may depend on the area of the brain affected. Therefore, the clinical signs described here may not represent a complete listing.
Neural invasion by the trematode Nasitrema is an important morbidity, mortality factor in stranded cetaceans. Gross lesions may or may
not be present.
MRI may offer premortem diagnosis if the patient is a suitable candidate and of a size compatible with the machine. Body motion must be
controlled, through restraint or sedation.
Nasitrema sp. is commonly found in Tursiops truncatus, although as yet ova have not been reported from brain/nerve tissue. The
reason for this is unknown, and merits continued investigation. The life cycle of this parasite remains unknown.
Acknowledgements
We wish to thank Dr. Robin Overstreet, Gulf Coast Research Laboratory, for help with parasite identity.
References
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