Swayback (Enzootic Ataxia) in Alberta Lambs

G. A. Chalmers

ABSTRACT Swayback (enzootic ataxia), a disease not previously described in Canada, occurred in newborn lambs in Alberta in 1972. Of 100 lambs born in one flock, over 60 succumbed in the enzootic. The diagnosis was based on the presence of a) gross cavitations and gelatinous lesions of the cerebral white matter in 16 of 24 (66.67%) lambs examined, b) central chromatolysis and hyalinization of neurons of the red and vestibular nuclei and reticular formation and of the lateral and ventral horns of the spinal cord, c) myelin deficiencies of the dorsolateral and sulcomarginal funiculi of the spinal cord and d) low hepatic and serum copper levels in affected lambs and low serum copper levels in the ewes. The feeding of sugar beet-(beta saccharifera) top silage to the ewes during pregnancy, lambing and lactation, and its relationship to the enzootic is discussed.

des neurones des noyaux rouge et vestibulaire, de la formation reticulee et des cornes laterales et ventrales de la moelle epiniere, c) la demy& linisation au sein des faisceaux dorso-lateral et sulco-marginal de la moelle epiniere, et d) une faible teneur en cuivre du foie et du serum des agneaux, ainsi que du serum des brebis. L'auteur commente l'alimentation des brebis a 1'ensilage de collets de betteraves sucrieres (Beta saccharifera), durant la gestation, lors de I'agnelage et de I'allaitement, ainsi que la relation entre cette pratique et l'enzootie qu'il rapporte.

INTRODUCTION
Historically, swayback has been associated with a conditioned copper deficiency (1, 6, 26) and is well known in the United Kingdom (1. 12, 26) although somewhat similar syndromes have been reported from several countries (29). The disease has been recorded also in goats (8, 19, 32) and in red deer (30, 42). Characteristically the condition in newborn lambs is acute, with early onset, a short fatal course and gross cavitations or gelatinous lesions of the cerebral white matter (2, 7, 28). Some investigators suggest that a syndrome of cerebral edema and cerebellar herniation (36, 37, 38) represents acute delayed swayback and is the most common fatal consequence of hypocuprosis in lambs (36). Activity of the copper bearing enzyme cytochrome oxidase is known to be reduced in the brains of swayback-affected lambs (3, 21); the most severe reduction of this enzyme occurs in groups of neurons which

RESUME
En 1972, I'ataxie enzootique ("swayback"), une maladie non encore decrite au Canada, a sevi chez des agneaux nouveau-nes, en Alberta. Au del'a de 60 des 100 agneaux nes dans un troupeau, succomberent 'a cette enzootie. Le diagnostic de la maladie s'appuyait sur: a) la presence de cavites macroscopiques et de lesions gelatineuses, au sein de la substance blanche des hemispheres cerebraux, chez 16 (66.67%) des 24 sujets examines, b) la chromatolyse centrale et la degenerescence hyaline

*Provincial Veterinary

Diagnostic Laboratory, Alberta Department of Agriculture, P.O. Box 177, Lethbridge, Alberta T1J 3Y5. Submitted May 4, 1973.

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show morphological evidence of the disease (3, 14, 22). In addition, since a depression of phospholipid synthesis occurs in copper deficient rats (15, 16), a similar situation may exist in lambs with swayback (20, 22). Because cytochrome oxidase is important in oxidative metabolism and in the synthesis of high energy compounds necessary in lipid synthesis, a deficiency of this enzyme could limit such synthesis, thus inducing lesions in the white matter of the cerebrum and spinal cord. The indications are therefore, that lesions in the white matter in swayback are unlikely to be due principally to degeneration, but rather to faulty myelination (7, 20), the abnormal products of which might subsequently degenerate (20). Additional support for such an hypothesis has been provided by the concept of biphasic myelination in the perinatal sheep (33). Enzootic ataxia, in contrast to swayback, has been associated with an uncomplicated copper deficiency, especially in Australia (2, 9, 28). In addition, the ewes have a hypochromic, macrocytic anemia (28), as well as stringy wool (28), diarrhea and a loss of condition (9). Although the acute disease with cerebral cavitation occurs, such is not the usual expression of enzootic ataxia. Instead, lambs are affected usually between three to six weeks and up to four months of age (9, 28). Those with ataxia of long duration tend to be anemic, are stunted and have fragile bones (28). In some instances, the expressions "swayback" and "enzootic ataxia" are used interchangeably (11, 17, 27) perhaps reflecting regional or traditional preferences in terminology. To complicate matters further, it has been suggested that some cases of swayback may have been due to a simple copper deficiency, when the effects of soil contamination of herbage samples were eliminated (2, 7). As well, the first description of enzootic ataxia in the United States suggested that interference from molybdenum may have been responsible for the ataxia observed (27). Syndromes of central nervous disorders clinically similar to swayback have been reported previously in neonatal lambs from western Canada. These included: a condition characterized by incoordination and paralysis in newborn lambs of the Corriedale breed (34), and subsequently identified as inherited cortical cerebellar atrophy (daft lamb disease) (23, 24) ; cerebellar ataxia in lambs born to ewes which had

been fed silage made from the vines of canning peas (Pisumn sativcum) (44); and congenital trembling in newborn lambs, associated with demyelination of the central nervous system and suggestive of hypomyelinogenesis congenita (13). This paper describes another neonatal ataxia which occurred in Alberta lambs in 1972. This condition, which differed markedly from those described previously, was grossly and histologically indistinguishable from swayback (enzootic ataxia), a disease not previously documented in Canada.

MATERIALS AND METHODS

A total of 24 lambs was available for necropsy. These included a majority of clinically affected lambs, a few stillborn animals and two lambs which had continued to exhibit clinical signs to nine months of age. The brains of 18 and the spinal cords of 13 of these lambs were removed and fixed in 10% neutral buffered formalin. Following fixation, two to three millimeter transverse sections of brain were cut at the following levels: the occipital lobes of the cerebral hemispheres, oculomotor nerve roots, pons, medulla oblongata at the obex, and spinal cord at various levels of the cervical and lumbar enlargements. A sagittal section through the vermis of the cerebellum was included also. Tissues wsere processed in ethyl alcohol, xylene and paraffin, embedded in paraffin and cut at six microns. Stains included hematoxylin and eosin (H&E), luxol fast blue (LFB), luxol fast blue-periodic acid-Schiff-hematoxylin (LFB-PAS-H) and in selected cases, von Kossa's and Perl's methods for calcium carbonate and iron, respectively. Blood samples for bluetongue serolory and copper determinations were collected by jugular venipuncture into plain Vacutainerl tubes from nine randomly selected post parturient ewes, most of which had lost lambs in the enzootic. Samples of liver and blood for copper analyses were collected at necropsy from six clinically affected lambs. Bluetongue serology was performed using the modified direct complement-fixation test (10). Serum and hepatic copper
'Becton, Dickinson & Co., Canada Ltd., Mississauga,
Ontario.

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values were obtained by atomic absorption spectrophotometry, employing a procedure described in "Clinical Applications of Atomic Absorption and Emission Spectroscopy

RESU LTS
FLOCK HISTORY

The flack, which consisted of 90 ewes of mixed breeding ranging in age from two to ten years had originated on the premises about 20 years previously. During the summer of 1971, the ewes had access to a tame grass pasture; however, at the onset of the breeding season in early November, the flock was removed from this pasture
2The Instrumentation Laboratory, Inc., Clinical Atomic Absorption Research and Development Laboratory, 1970, 113 Hartwell, Lexington, Mass.

Fig. 2. Transverse section of the brain of a five day old lamb affected with swayback, revealing the marked cavitation of the subcortical white matter. Note the dilated lateral ventricles.

Fig. 1. Brain of a newborn lamb affected with swayback. Note the collapse of the cerebral hemispheres.

Formalin-fixed specimen.

and hand feeding was begun. Initially, the ration consisted of third cut alfalfa hay, silage made from the tops of sugar beets (Beta saccharifera), cobalt iodized block salt and a free choice commercial minFral mix. The sugar beet-top silage, which the owner had never fed to his sheep previously, was provided virtually ad libitum throughout breeding, pregnancy, lambing and early lactation, and comprised most of the roughage available during these periods. Beginning about one month before, and continuing throughout lambing and lactation, each ewe received up to one and one half pounds of whole oats daily, as well as a small amount of first cut alfalfa hay. Lambing began in early April 1972, as expected. Of the 90 ewes, 70 subsequently produced 100 lambs, of which over 60 died in utero, shortly after birth or within the next three weeks. Most lambs were clinically affected at birth. There were no signs of unthriftiness, diarrhea, anemia or alterations of wool fibers in the ewes. Clinically, many lambs were totally recumbent and were able only to raise their heads when stimulated, while fewer animals were ambulatory but dull or mildly to severely ataxic. The major clinical signs in affected lambs were prostration, headshaking, trembling and ataxia, the latter often accompanied by swaying of the hind quarters and followed by posterior collapse. In a few cases, lambs in which clinical signs were either absent or very mild at birth, began within several days to reveal evidence of marked ataxia, swaying of the hind quarters and recumbency. Conversely,

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closer inspection, a lacy meshwork of interconnecting trabeculae of residual fibers (Fig. 3). The least severe lesions were confined to the subcortical white matter near the tips of the gyri and consisted of either tiny, focal gelatinous softenings or similar macrocavitations which were occasionnally collapsed and slit-like. Lesions were bilaterally symmetrical and evident usually as a continuum from the frontal to the occipital lobes. Gross lesions were not observed in the cerebellum, mid brain or spinal cord.
Fig. 3. Transverse section of the brain of a newborn lamb affected with swayback. Note the lacy meshwork of residual white matter of the cerebral cortex and the dilated lateral ventricles.

HISTOPATHOLOGY

two newborn ambulatory lambs which wrere depressed and unable to raise their heads above the level of the vertebral border of the scapula, were able to do so normally within a few days of birth and subsequently continued to gain well. Two other lambs which exhibited a stiff, unsteady gait, swaying of the hind quarters and collapse, signs which were evident particularly during periods of excitement, survived to nine months of age before being killed for necropsy. Despite severe incapacitation, most lambs would nurse if assisted. Single lambs as well as one or both twins were affected. The remaining 40 lambs, which included some survivors of the ataxia, continued to gain well and were eventually sold at auction. GRCSS PATHOLOGY

Gross lesions were observed in the cerebral hemispheres of 16 of 24 (66.67%) lambs examined. These lesions, like the clinical signs, revealed gradations of severity and were grouped, for convenience, into three categories. In the most severe cases, which included one of the nine month old survivors, the exposed gyri were taut, fluid-filled and ballooned against the cranial vault, rupturing and collapsing readily during removal (Fig. 1). The escaping fluid was clear and serous, resembling normal cerebrospinal fluid. Transverse sections of these cerebral hemispheres revealed an almost complete absence of white matter, with a thin, one to two millimeter layer of cortex overlying the resulting marked cavitation (Fig. 2). In brains with less severe lesions, the subcortical white matter was gelatinous and translucent, revealing on

Brain Stem and Spinal Cord - Lesions were seen most frequently in neurons of the red and vestibular nuclei and the reticular formation (Fig. 4). Frequently, neurons of the red nucleus revealed a sequential progression of degenerative changes characterized by vacuolation, central chromatolysis, peripheral migration of the nucleus, swelling of the cell body, and hyalinization (Fig. 4 )). Similar lesions were observed less frequently in the pontine, facial and olivary nuclei and occasionally, vacuolated neurons were noted in the oculomotor, trigeminal, lateral cuneate and hypoglossal nuclei. Neuronal lesions similar to those described for nuclei of the brain stem were observed in the lateral and ventral gray horns of the spinal cord in both the cervical and lumbar enlargements. Lesions of the white matter in the spinal cord were best appreciated using the LFBPAS-H technique, which demonstrated areas deficient of myelin in the dorsolateral and sulcomarginal funiculi.

Fig. 4. Red nucleus of a swayback-affected lamb. Note the neuronal vacuolation, central chromatolysis, peripheral nuclear migration, and swelling and hyalinization of neurons. Two normal neurons are evident. LFB. X150.

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TABLE 1. Serum and Hepatic Copper Levels in Lambs and Ewes

tive. Results of the serum and hepatic copper determinations are given in Table I.

Animal Number Lambs I1..............

1)
............

Copper Serum Liver (uLg/100 ml) (ppm, DM)a

21.1 28.1 43.5 13.6 57.5 11.1

3.. 4..
5.. 6..
1
2 .. Ewes
.
.

18.17 17.30 76.68

20.66 8.96

DISCUSSION
Although the history of silage feeding followed by incoordination in newborn lambs suggested the syndrome of cerebellar ataxia reported previously in Alberta (44), there were fundamental differences in the two enzootics. In the present case, lambs were affected, for the most part at birth, whereas in the earlier account clinical signs became evident only after the lambs had ingested milk from ewes fed peavine silage (44). Secondly, in the absence of parental serum titres to bluetongue virus the finding of gross cavitations and gelatinous lesions of the cerebral white matter, suggested that the condition was swayback. Further confirmation of this diagnosis was provided by observations of neuronal lesions of the brain stem and spinal cord, as well as deficiencies of myelin in the white matter of the spinal cord. In combination with low hepatic and serum copper levels in affected lambs and low serum copper levels in ewes in the flock (Table I), such lesions fulfilled previously published criteria for a diagnosis of swayback (2, 7). Although hepatic and serum copper levels of ewes and affected lambs were relatively higher than those published by other investigators, most copper values recorded in this enzootic were below the levels of 80 ppm (dry matter) for liver and 60 ,ug/100 ml for blood, cited as tentative criteria of a low copper status (7). Gross lesions of the cerebral white matter of lambs have tended to be associated chiefly with swayback, although gelatinous lesions have been observed in experimental Border disease (5). In recent years, somewhat similar malformations of the cerebral hemispheres of lambs have been associated with the field (12, 40) and experimental uses (31, 35, 45) of bluetongue vaccine, and with naturally-occurring bluetongue infections (12, 18, 39). Such lesions in lambs, therefore, are not pathognomonic for swayback, and further procedures, including serology, chemical analyses of blood and tissues for copper levels, and histopathology are required in the differential diag115

........

3 4 5. 6 7 8 9

..

2.9 22.8 57.8 41.2 13.2 5..6.1 .. 7.195.7 72.8

-Farts per million. drv matter

Cerebr-um and Cerebellumn- Neurons of the cerebrum were generally unaffected. In some cases, clusters of glial cells were noted surrounding individual neurons, most of which had large vesicular nuclei. In several brains, laminar neuronal necrosis with mineralization was observed. Special stains demonstrated that the mineral deposits consisted, in part, of iron salts, but not of calcium carbonate. In those brains with large cavitations (Fig. 2), the thin cortex revealed laminated, parallel-running fibers and nuclei of glial cells, reminiscent of the compression capsule described previously (7). Examination of those cerebral hemispheres with gelatinous translucent white matter revealed a loose, thin lacy network of fibers intermixed with moderate numbers of glial cells. In some areas, these cells were suggestive of microglia, based on the appearance of dark, pyknotic nuclei and foamy, debris-laden cytoplasm. Such cells were infrequent however, and when seen, were within the microcavitations which replaced some of the groups of fibers. Lesions were not observed in the cerebellum.
SEROLOGICAL AND CHEMICAL EXAMINATIONS Examination of serum samples from nine ewes in the flock for evidence of exposure to bluetongue virus, were uniformly nega-

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nosis. In the United Kingdom, gelatinous lesions or cavitations have been seen only rarely in swayback-affected lambs over three weeks of age and never in lambs over eight weeks of age (2) ; however, cavitations have been observed in a two month old animal in California (11), and in the present case, in a nine month old survivor. The feeding of sugar beet-top silage preceding the birth of swayback-affected lambs was of interest for several reasons. Firstly, its use represented the only known major change in the nutritional management of this flock in 20 years. Secondly, it was the main source of roughage for the flock throughout pregnancy, lambing and early lactation. Finally, the presence of low serum copper levels in ewes being fed sugar beet-top silage has had an interesting precedent: a relationship between the feeding of peavine silage and low serum copper levels was noted by earlier investigators who found copper values of 40 and 12 ,ug/100 ml in the serum of ewes fed oat hay and peavine silage, respectively (44). In the context of the present case, such findings are further intriguing in view of the authors' observations of "swelling and a homogeneous appearance of a few neurons in the more distal sections of the spinal cord" (44) of several lambs. On the basis of these considerations, therefore, the feeding of large amounts of sugar beet-top silage to ewes which subsequently produced swayback-affected lambs, raises presently unanswered questions regarding its role in the pathogenesis of this enzootic. Results of investigations into this aspect of the enzootic will be reported in another communication. Despite the overlapping of the syndromes of swayback and enzootic ataxia and the concurrent semantic issues, the suggestion of Underwood (43) that " these conditions appear to be pathologically identical and the term 'enzootic neonatal ataxia' can properly be applied to them", is reasonable. Although there are diverging opinions on the relative importance of the lesions of the brain stem and cerebrum (4, 7, 25, 26, 41), those in the brain stem and spinal cord are probably "the most significant lesions observed and the only histological changes which could constitute a reliable basis for the diagnosis of swayback" (7). In support of this contention, Barlow et al (7) found that 69.5 % of their cases of swayback failed to reveal gross lesions of the cerebrum,

but that all cases showed neuronal lesions of the brain stem and spinal cord, and deficiencies of myelin in the dorsolateral and sulcomarginal funiculi of the spinal cord. Such observations agree with Australian investigations of enzootic ataxia ( 9) and provide some understanding of the basis of the ataxia encountered in these conditions.

ACKNOWLEDGMENTS
The author wishes to express his gratitude to the Animal Diseases Research Institute, Htull, Quebec for performing the bluetongue serology; to Mrs. K. I. Strausz and Dr. J. E. Roff, Provincial Analysts, for the copper analyses; to Mrs. R. Vanderzee and Mrs. V. Wong for excellent technical assistance; and to many colleagues for their valuable advice. encouragement and review of the manuscript.
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