Abstract
Hydrocephalus was diagnosed in wild red fox (Vulpes vulpes) kits in four contiguous counties in northern Virginia in 1996–1997. Hydrocephalus has not been previously reported in red fox. The distribution and similar histories of these cases suggest a common etiology. Diagnostic testing indicates a viral cause to be unlikely. Alternatively, these cases of hydrocephalus may be either genetic or environmental in origin.
Introduction
Hydrocephalus is the abnormal accumulation of cerebrospinal fluid within the ventricular system of the brain.4 Clinical signs may include enlargement of the head, prominence of the forehead, divergent strabismus, brain atrophy, seizures, and behavioral or mentation abnormalities. Hydrocephalus can be either acquired or congenital. Acquired forms can be caused by infection, trauma, or tumors. Congenital hydrocephalus can be caused by in utero viral infection, toxoplasmosis, or teratogenic drug or chemical exposure. This report describes a recent, small, localized outbreak of hydrocephalus in wild red fox kits in northern Virginia in 1996–1997.
In April 1996, a wild red fox kit found in Loudon Co., VA was brought to a wildlife rehabilitator (APH) who specializes in foxes. The fox had an enlarged head, made frequent, inappropriate vocalizations, and appeared to be blind. The fox was recognized as appearing hydrocephalic, because the rehabilitator had seen a similar previous case in 1986, which had been diagnosed at The Wildlife Center of Virginia as being hydrocephalus. The rehabilitator was presented with a second fox kit with similar clinical signs a few weeks later from Fairfax Co., VA and a third similar kit from Fauquier Co., VA in May 1996.
Methods
Diagnostics were not performed on the first two of these red fox kits. The carcass and blood samples from the third affected red fox kit were submitted for examination to the Southeastern Cooperative Wildlife Disease Study (SCWDS) at the University of Georgia College of Veterinary Medicine. This was the first case of hydrocephalus in red fox ever observed at SCWDS. Subsequently, the rehabilitator and referring veterinarian (VC) started collecting serum samples from unvaccinated, unaffected adult and juvenile red and gray foxes to use as negative controls in a serologic comparison between foxes with hydrocephalus and clinically normal foxes.
No further cases were reported until April 1997, when three more affected red fox kits were found in Fairfax Co., Prince William Co., and Loudon Co., VA. Samples from all three of these foxes were submitted to SCWDS.
Results
External examination and radiographs of the heads of the affected fox kits revealed marked enlargement and doming of the cranium. The cerebral ventricles were markedly dilatated. The cerebral hemispheres were reduced to thin shells, and the surface of the cerebellum was flattened dorsally. Histologically, the cell density of the cerebrum appeared high due to compression of the tissue.
The affected red fox kits had positive serologic titers to canine distemper virus (CDV), canine parvovirus (CPV), and canine adenovirus (CA), but negative titers to canine parainfluenza virus (CPI). Samples of brain tissue from the affected red fox kits were negative by fluorescent antibody testing for CDV, CPV, CA, and CPI.
Nine unaffected red and gray fox kits tested from the same area of Virginia had similar serologic profiles. All nine unaffected kits tested had positive titers to CDV, 8/8 tested had positive titers to CPV, 8/9 had positive titers to CA, and 9/9 had negative titers to CPI. Additionally, serum samples from seven unaffected adult red and gray foxes were analyzed. All seven adult foxes had positive titers to CPV, whereas only 3/7 had positive titers to CDV, and only 1/7 had a positive titer to CA.
Discussion
While hydrocephalus is the most common canine congenital anomaly of the nervous system,1 hydrocephalus in foxes is unreported in the literature. Hydrocephalus has been reported to be caused by canine parainfluenza virus in dogs; other viruses known to cause encephalitis in dogs include Aujeszky’s disease, canine distemper, canine herpes, infectious canine hepatitis, and rabies.1
Serologic tests have disclosed antibodies to canine parvovirus, canine adenovirus, canine coronavirus, canine herpesvirus, and canine parainfluenza virus in wild red and gray foxes.2 In gray foxes, canine distemper is the most significant mortality factor of all infectious and noninfectious disease.3
The similarity in the ages of the hydrocephalic foxes of this report (less than 3 months old) and the close geographic association, found within four adjacent counties, suggests these cases likely share a common etiology. The fox kits of this report were screened serologically for exposure to viral agents associated with encephalitis in domestic canids. Serologically, there were no differences between affected and unaffected fox kits; therefore, it is unlikely that viral exposure leading to these positive titers was the cause of the hydrocephalus. Of the viral pathogens screened for in the fox kits of this report, all were negative for canine parainfluenza virus, the only virus confirmed to cause hydrocephalus in domestic canids. The positive serologic titers in the fox kits of this report are most likely due to maternal antibodies. The negative fluorescent antibody test results indicate there was no active viral infection caused by these viruses at the time of euthanasia. Comparatively, the adult foxes examined in this report had fewer positive titers than did the fox kits, perhaps due to the waning of maternal antibodies over time. However, positive titers in some adult foxes suggest exposure as adults to these viruses without the occurrence of hydrocephalus as a consequence.
These findings suggest that a viral etiology for the hydrocephalus seen in these red fox kits is unlikely. Alternatively, the hydrocephalus seen in these foxes might have a genetic basis present in the breeding subpopulation encompassing these four adjacent counties. An environmental toxin or contaminant present within the geographic limits of these four adjacent counties represents another possible cause, with implications for the human residents of these counties, as all are well populated. The red fox kits produced in northern Virginia in 1998 will be closely watched for reoccurrence of this anomaly.
Acknowledgments
The authors would like to thank Drs. John Fischer and Michael Teglas of SCWDS for performing the post-mortem examinations on the foxes in this report.
Literature Cited
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2. Davidson, W.R., M.J. Appel, G.L. Doster, O.E.Baker, and J.F. Brown. Diseases and parasites of red foxes, gray foxes, and coyotes from commercial sources selling to fox-chasing enclosures. J. Wildl. Dis. 28:581–589.
3. Davidson, W.R., V.F. Nettles, L.E. Hayes, E.W. Howerth, and C.E. Couvillion. 1992. Diseases diagnosed in gray foxes (Urocyon cinereoargenteus) from the southeastern United States. J. Wildl. Dis. 28:28–33.
4. Simpson, S.T. 1989. Hydrocephalus. In: Kirk, R.W. Current Veterinary Therapy X. W.B. Saunders Co., Philadelphia, Pennsylvania, Pp 842–847.