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A retrospective study of spinal cord lesions in goats was conducted to identify the range of lesions and diseases recognized and to make recommendations regarding the best tissues to examine and tests to conduct in order to maximize the likelihood of arriving at a definitive etiologic diagnosis in goats with clinical signs referable to the spinal cord. Twenty-seven goats with a spinal cord lesion were identified. The most common lesion recognized, in 13 of 27 goats, was degenerative myelopathy. Eight goats with degenerative myelopathy were diagnosed with copper deficiency. Non-suppurative inflammation due to caprine arthritis encephalitis virus, necrosis due to parasite larvae migration, and neoplasia were each diagnosed 3 times. Based on these findings, it is recommended that, in addition to careful handling and histologic examination of the spinal cord, samples of other tissues, including the brain, liver, and serum, be collected for ancillary testing if warranted.
Étude rétrospective des lésions de la moelle épinière chez les chèvres soumises à trois laboratoires de diagnostic vétérinaire. Une étude rétrospective des lésions de la moelle épinière chez les chèvres a été réalisée pour identifier l’ampleur des types de lésions et des maladies reconnues et pour présenter des recommandations concernant les meilleurs tissus à examiner et les tests à réaliser afin de maximiser la probabilité d’arriver à un diagnostic étiologique définitif chez les chèvres avec des signes cliniques pouvant se rapporter à la moelle épinière. Vingt-sept chèvres avec une lésion à la moelle épinière ont été identifiées. La lésion la plus couramment reconnue, chez 13 des 27 chèvres, était la myélopathie dégénérative. Huit chèvres atteintes de la myélopathie dégénérative ont été diagnostiquées avec une carence en cuivre. Une inflammation non suppurative causée par le virus de l’arthrite encéphalite caprine, une nécrose attribuable à la migration des larves de parasites et la néoplasie ont chacune été diagnostiquées trois fois. En se fondant sur ces résultats, on recommande que, en plus d’une manipulation soigneuse et d’un examen histologique de la moelle osseuse, des échantillons d’autres tissus, incluant le cerveau, le foie et le sérum, soient prélevés pour des tests auxiliaires au besoin.
(Traduit par Isabelle Vallières)
According to the Food and Agriculture Organization of the United Nations, approximately 0.3% of the goats in the world are located in North America (cited in 1). This relatively low proportion may help to explain why goat diseases and caprine practice do not receive the same attention as diseases of other animal species and other types of practice, respectively, in North American veterinary curricula and literature. Further, Lincicome (cited in 1) found that only 5% of goats submitted to diagnostic laboratories in North America had neurologic disease. For these reasons, a retrospective study of spinal cord lesions in goats was conducted to identify the range of lesions and diseases recognized and to make recommendations regarding the best tissues to examine and tests to conduct in order to maximize the likelihood of arriving at a definitive etiologic diagnosis in goats with clinical signs referable to the spinal cord.
A computer-assisted search of the records of 3 veterinary diagnostic laboratories — the Oregon State University Veterinary Diagnostic Laboratory in Corvallis, Oregon (OSU); Prairie Diagnostic Services, Inc., in both Regina, Saskatchewan, and the University of Saskatchewan in Saskatoon, Saskatchewan (PDS); and the University of Minnesota Veterinary Diagnostic Laboratory in St. Paul, Minnesota (UMN) — was conducted to identify the diagnostic reports of goats older than 1 wk of age, that had been diagnosed with lesions of the spinal cord during the 10-year period between January 2001 and December 2010, inclusive. Each diagnostic report was retrieved and reviewed. Those cases in which there was an unequivocal lesion in the spinal cord were selected for further review. For each record, the year and month of submission; the age, gender, and breed of the goat; the morphologic changes in the spinal cord and final diagnosis; and the results of ancillary tests were summarized. Goats that were older than 1 wk of age, but less than a full month of age, were classified as 0.5 months of age.
Twenty-seven goats with a spinal cord lesion were identified. Of the 27 goats, 7 were examined at OSU, 3 were examined at PDS, and 17 were examined at UMN. Except for the year 2010, at least 1 goat was examined during each calendar year of the study. Therefore, a mean of 3 goats/year were examined between 2001 and 2009, inclusive. No more than 6 goats were examined in any 1 year. The age for 26 of the goats was known and ranged from 0.5 to 84 mo with a mean of 15.5 mo. One goat was described as being an adult. The 27 goats included 13 females, 6 males, and 2 castrated males. For 6 goats, the gender was not recorded. Seven of the goats were Boer, 5 were Saanen, and there were either 2 or 3 of each of Alpine, Nigerian Dwarf, Nubian, and Pygmy goats. Two other goats were described as cross-breeds and the breed was not recorded for 2 goats. There was no apparent association between the season of the year and any specific diagnosis. With 1 exception, there was also no apparent association between the breed of goat and any specific diagnosis. The 1 exception was a congenital, and possibly familial, neuronal anomaly diagnosed in Boer goats in Oregon.
Degenerative myelopathy was the most common spinal cord lesion and was diagnosed in 13 of the 27 goats (Table 1). The lesions featured variable combinations of necrosis and chromatolysis of neurons, evidence of Wallerian degeneration of axons, and decreased amounts of myelin. Eight of these goats had symmetrical lesions that were restricted to, or heavily concentrated on, the white matter of the ventral funiculi and motor neurons of the ventral horns. Three of these animals were examined at OSU; 2 animals, from different farms, were examined at PDS; and 3 animals were examined at UMN. The nature and distribution of the spinal cord lesions in these 8 goats were suggestive of those associated with copper deficiency. Six of these 8 goats had their hepatic copper concentrations determined and were found to be below the reference interval of 25 to 150 ppm (2) in every case. The range of these 6 concentrations was 1.7 to 12.7 ppm with a mean concentration of 5.4 ppm. For 1 of the other 2 goats, a 3-month-old, the dam had been diagnosed with low serum copper concentrations. Copper analysis was not performed in 1 goat.
Of the remaining 5 goats with degenerative myelopathy, 2 had marked vertebral malformations that created foci of stenosis with compression of the spinal cord. Histologically, the lesions in the spinal cord were spatially associated with the malformed vertebrae. One of the affected animals was examined at OSU and the other at UMN. No underlying cause for the degenerative myelopathy was determined for the remaining 3 goats, which were all examined at UMN. Each of these goats had symmetrical white matter lesions of the spinal cord that included dilation of myelin sheaths and either swollen axons or so-called digestion chambers, i.e., aggregations of axon fragments, degenerated myelin debris, and macrophages. However, unlike goats with copper deficiency myelopathy, there were no lesions in the spinal cord neurons, or lesions of any kind in the brain. Of these 3 animals, the 24-month-old had a hepatic copper concentration of 67.9 ppm; the 42-month-old had a hepatic copper concentration of 1.5 ppm; and the 4-month-old did not have its hepatic copper concentration determined.
The other 14 goats in this study were diagnosed with a variety of spinal cord disorders that included primarily inflammation (n = 4), primarily necrosis (n = 4), congenital neuronal anomalies (n = 3) and neoplasia (n = 3) (Table 1). The 4 goats with an inflammatory lesion had extensive, moderate to severe, infiltration of lymphocytes, plasma cells, and macrophages into the meninges and perivascular spaces of the white matter of the spinal cord that was associated with necrosis and the presence of gitter cells. The animals involved were all examined at UMN, young, and of different breeds. In 3 of the 4 cases, caprine arthritis encephalitis (CAE) virus was detected within the spinal cord lesions by means of immunohistochemistry. In the fourth case, involving an 8-month-old Saanen goat, an enzyme-linked immunosorbent assay (ELISA) did not detect evidence of CAE virus infection in serum that had been collected 1 mo prior to postmortem examination, and immunohistochemical testing did not detect CAE antigen in the brain.
Randomly located foci of necrosis, axonal swelling, and myelin sheath dilation, accompanied by a relatively mild degree of inflammation and gliosis, were identified in 4 goats, all of which were examined at UMN. In 3 of these goats, the predominant inflammatory cells included eosinophils, lymphocytes and plasma cells. Examination of multiple sections of brain and spinal cord revealed nematode larvae in 2 of these 3 animals. In each case, there was speculation that the parasite involved was Parelaphostrongylus tenuis, but the identity of the parasite was not confirmed. The fourth goat, a 3-month-old, male, Saanen, had a history of being ill shortly after birth and never being normal. Prior to being euthanized, the goat was described as having a hunched back and then unable to stand. The postmortem examination revealed foci of chronic and active inflammation with fibrosis; vasculitis with thrombosis; and necrosis in several organs and tissues including the umbilicus, brain stem, and multiple segments of spinal cord. The predominant lesion in the spinal cord was necrosis, which was presumed to be secondary to a vascular lesion and ischemia. Arcanobacterium pyogenes was isolated from multiple tissues.
Congenital anomalies manifesting as a reduced number, abnormal appearance, and necrosis of spinal cord neurons associated with Wallerian degeneration was described in 3 goats that either could not stand or had difficulty standing from birth. These goats were also young (Table 1) and all were female. One goat, examined at PDS, was a Nubian and 2 goats, examined at OSU, were closely related Boer goats. The neurons in the spinal cord of these Boer goats had a granular or finely vacuolated appearance when examined by routine light microscopy. Electron microscopy revealed increased numbers of mitochondria, many of which were enlarged.
A neoplasm involving the spinal cord was diagnosed in 3 goats. Two goats had lymphoma and the third goat had a primary spinal cord neoplasm diagnosed as an astrocytoma. In 1 of the goats with lymphoma, the spinal cord was the only tissue involved. The second goat had lymphoma in both the thorax and the spinal cord.
The spinal cord lesions identified in the diagnostic records reviewed for this study comprise the range of morphologic changes commonly encountered in mammalian pathology, i.e., developmental anomalies, degeneration, various types of inflammation, ischemia, other types of necrosis, and neoplasia. The most common disease diagnosed was copper deficiency myelopathy that is more commonly known as swayback and enzootic ataxia. Many regard these 2 terms as synonyms while others consider swayback to be a congenital disease and enzootic ataxia as a disease that develops after birth. Copper deficiency myelopathy in goats typically manifests as enzootic ataxia in kids by 3 mo of age, but onset of signs can be delayed to about 6 mo of age. Congenital disease, i.e., swayback, is rare in goats (1,3–5). The disease is thought to be caused by a deficient intake of copper by does during pregnancy. The deficiency is most commonly associated with a diet low in copper, but it might also be associated with a conditional or secondary copper deficiency in which excess levels of dietary molybdenum, cadmium, sulfates, or other minerals or substances impair the absorption of copper (1,3,4). While the lesions present in the spinal cord of affected kids is characteristic, demonstration of low concentrations of copper in the liver is diagnostic. There were 2 unexpected findings among the goats with copper deficiency myelopathy in this study. One was that 4 of the 8 animals were older than 3 mo and 3 of the 8 animals were 18 mo and older (Table 1). The other was that characteristic changes in the white matter were most consistently present in the ventral funiculi. While involvement of the ventral funiculi has been reported in copper deficiency myelopathy in goats, it is more typical for the white matter lesions to involve the dorsolateral aspects of the lateral funiculi.
Four goats had non-suppurative meningitis and perivascular leukomyelitis suggestive of a viral infection (5). In 3 of these 4 cases, a CAE virus infection was diagnosed. CAE virus is a lentivirus within the retrovirus family that is known to produce 5 clinical conditions in goats. The most common lesion is arthritis, but mastitis, pneumonia, leukoencephalomyelitis, and weight loss are also associated with infection. The neurologic form of the disease is slowly progressive over a number of weeks and most common in kids 4 or 6 mo of age and less (1,4). The 3 goats diagnosed with CAE virus infection were 5 mo of age or less (Table 1) and the diagnosis was made by identifying CAE virus antigens within spinal cord lesions using immunohistochemistry. CAE virus could not be detected in the fourth goat with similar spinal cord lesions. This goat was 8 mo old and this case serves as a reminder that there are other viruses that can cause nonsuppurative meningitis and myelitis in goats. Rabies, pseudorabies, border disease, Borna disease, and louping-ill have all been diagnosed in goats, although uncommonly (1,4,6). While ruminants appear to be far less susceptible to West Nile virus infection and disease than horses, West Nile virus infection should remain a differential diagnosis in goats with nonsuppurative meningoencephalomyelitis for which no other diagnosis has been confirmed.
Based on the presence of randomly located foci of spinal cord necrosis, eosinophilic inflammation, or both, nematode larvae migration was suspected in 3 goats and confirmed by the presence of the larvae in histologic sections in 2. Cerebrospinal nematodiasis has been previously described in goats (1,4,7). In North America, the condition is caused by the larvae of Parelaphostrongylus tenuis, the meningeal worm of white-tailed deer, in which it rarely causes clinical disease. In other regions of the world, cerebrospinal nematodiasis in goats has been caused by Setaria sp., Elaphostrongylus rangiferi, and Elaphostrongylus cervi. In this condition, goats are aberrant hosts that become infected after accidently ingesting the gastropod (slug or snail) intermediate host while grazing. In this study all of the goats with confirmed or suspected cerebrospinal nematodiasis were examined at UMN. The fact that P. tenuis is known to exist in the UMN area and has not been reported in the OSU and PDS areas of western North America is consistent with previous reports of cerebrospinal nematodiasis and may explain the findings of the current study. Because white-tailed deer infested with P. tenuis rarely display clinical signs, goats and other grazing animals may serve as a sentinel for the presence of this parasite where it has not been previously reported. It is therefore important to know that examination of the brain stem and spinal cord is the most useful method for diagnosing central nervous system nematodiasis in goats.
One goat was diagnosed with ischemic necrosis in the spinal cord associated with neonatal sepsis. It is interesting that no cases of bacterial meningitis were diagnosed among the goats included in this study. The reason for this is not known, but it may be due to the exclusion from this study of goats that were 1 wk of age or less. It has been suggested that most cases of bacterial meningitis in neonatal farm animals develop between 2 and 7 d postpartum as a sequel to neonatal sepsis, and is facilitated by failure of passive transfer of immunity. In such circumstances, the central nervous system might be the only tissue infected and the presence of suppurative inflammation will be highly suggestive of a bacterial infection (3,5,8). However, in cases of neonatal sepsis, it is more likely that other tissues will be involved and histologic examination and bacterial culture of multiple organs or tissues will assist in making a definitive diagnosis. This was the situation in the goat reviewed in this study. Bacterial meningitis of older goats may be a sequela of a surgical procedure or may represent an extension of an infection of another tissue. Examination and bacterial culture of multiple organs or tissues will also be helpful in these situations.
Neoplasms of the spinal cord are thought to occur rarely in farm animals, including goats (3,9), and a review of the reports of goats with central nervous system (CNS) neoplasms further supports this opinion (1). Nevertheless, in the current study, 3 goats, or 11%, were found to have neoplasms involving the spinal cord. Two of these neoplasms were lymphoma, and lymphoma in this location has not been previously described in goats. What is of further interest is that in a review of lymphoma of goats, Craig et al (10) found that only 3 of 10 affected animals had enlarged superficial lymph nodes. For these reasons, and because goats with lymphoma tend to have only vague clinical signs of weight loss, anorexia, and depression, there may be little antemortem physical evidence to suggest the presence of spinal lymphoma in goats. There is no known cause of lymphoma in goats and most cases are isolated instances of so-called spontaneous development, typically in goats 2 y of age and older.
Based on the results of this study, the following recommendations are offered to owners, practicing veterinarians, and diagnostic veterinary pathologists interested in optimizing the investigation of the cause of clinical signs referable to the spinal cord in naturally dying or euthanized goats. First, the spinal cord and brain should be examined and efforts should be made to preserve the CNS at the time of examination. To facilitate the preservation of the spinal cord, 3 approaches should be considered. Ideally, the spinal cord and brain should be removed from the carcass and kept cool, not frozen if possible, and submitted to a diagnostic laboratory as quickly as possible. In situations where submission of the CNS to the diagnostic laboratory may be delayed or may result in physical damage to the spinal cord, it should be fixed in 10% neutral buffered formalin (NBF) as soon as possible. However, it is acknowledged that postmortem removal of the spinal cord and brain may be difficult and time consuming. In such situations submission of the entire carcass is a logical alternative but, again, the carcass should be kept cool and not frozen, if possible.
When the spinal cord is removed from the vertebral canal, care should be taken not to damage the spinal cord and to examine the vertebral column for any lesions that may have caused stenosis of the vertebral canal and spinal cord compression. Typically, the entire spinal cord and brain should be fixed in 10% NBF. However, consideration should be given to holding portions of the CNS frozen for possible future study such as virus isolation, bacterial culture, or the location and identification of parasites. Because the most common condition diagnosed in this study was copper deficiency myelopathy, an appropriate amount of liver should also be held frozen in the event that determination of hepatic copper concentration is warranted.
Finally, while it is becoming more common to diagnose viral infections in formalin-fixed tissues, it may be useful to collect and submit serum, prior to death or euthanasia, from the animal showing clinical signs, herd mates, or both. This serum might be useful in diagnosing exposure to, or infection by, pathogenic viruses, e.g., CAE, and might be used to assess copper status if liver is not available for analysis. Those involved in the pursuit of a diagnosis of the cause of spinal cord disease should also be aware of the potential additional fees associated with ancillary testing such as analysis for copper concentrations, immunohistochemical testing, and bacterial culture.
The authors acknowledge Dr. Marie Gramer and Mary Thurn of University of Minnesota for their editorial and technical assistance. CVJ
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