CASE NOTES

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Sorghum-Associated neuroaxonal degeneration in dorper lambs

Megan Davies, District Veterinarian, Narrabri and Thomas Westermann, Pathology Resident, EMAI

Posted Flock & Herd December 2018

INTRODUCTION

Sorghum is one of several cultivated plants that contain cyanogenic glycosides, which undergo conversion to hydrogen cyanide (HCN) following ingestion. In acute cyanide poisoning associated with sorghum consumption, affected animals die rapidly and diagnosis is often made post-mortem. Extended periods of grazing sorghum may lead to ataxia in sheep, cattle and horses. Neurological signs of the ataxic syndrome in sheep, including weakness, ataxia, head shaking, knuckling of fetlocks, inability to rise, and opisthotonus, are associated with a distinctive histopathological change of neuroaxonal degeneration in the brain and spinal cord; pregnant ewes may produce stillborn, weak or arthrogrypotic lambs. In this report, we describe an outbreak of sorghum-associated neuroaxonal degeneration in a mob of Dorper lambs.

History

In April 2018, the District Veterinarian, Narrabri investigated the deaths of 18 eight-month-old White Dorper lambs, which had died over a period of three weeks, several weeks after commencement of grazing forage sorghum (hybrid variety “Nudam” Sudan x Sudan Grass, Nuseed Pty Ltd) in a paddock near Gunnedah in North West NSW. Several months earlier the lambs had been vaccinated with a 5-in-1 clostridial vaccine containing selenium. 

The property was drought affected. The sorghum was the only feed available to the lambs, and there were no weeds or other plant species in the crop. When introduced to the paddock, the lambs were part of a larger mob, including 300 ewes. When the sheep began grazing the sorghum, it was approximately 50cm high, but when the District Veterinarian visited the property, the few remaining stalks were 20-30cm high, with significant regrowth around the bases of the plants (Figure 1). There had been no significant rainfall, and water was from troughs containing bore water. 

Figure 1. Sorghum crop grazed by affected lambs. Photo taken one week after sheep were removed from paddock.

At routine inspection of the sheep, the producer would find a few lambs lying down, unable to get up. When lifted to a standing position, affected lambs would stagger off and re-join the mob. The producer would later find the lambs dead in the paddock – the time from when the lambs first exhibited signs to time of death is unknown. No ewes were affected.

The producer put out several large oaten hay bales to supplement the sorghum and noted that the rate of deaths seemed to slow during the time the hay was available. 

Following the 18 deaths, the producer moved the sheep from the paddock and separated the ewes from the lambs. The lambs were put into a different paddock, containing the same variety of sorghum, and were given sulphur lick blocks on the recommendation of a feed supplier. No further deaths occurred, however the producer noted that several lambs were still staggering and unstable on their feet. 

Clinical Examination

On the day of examination, only two affected 8-month-old wether lambs were identified.

Lamb 1: This lamb had been marked with stock marker two weeks earlier as it was observed to be staggering in the paddock. Video 1 shows the behaviour of this lamb when it was held in a small yard. 

Video 1. Lamb 1 observed in small yard.

This lamb was bright and alert, and was attempting to jump the fence to join the rest of the mob in the adjacent pen. It was knuckling over in all four limbs, was markedly ataxic, and fell over numerous times. It was able to stand again independently, but staggered from side to side. When it fell, it would land on its back and paddle its legs. It displayed no limb weakness, rather incoordination, with the hind limbs crossing over each other and rump swaying. The forelimbs were steadier but occasionally knuckling of the forelimbs occurred. When standing still it displayed widespread muscle tremors.

There was no distinct circling behaviour or opisthotonus observed, and the lamb appeared normal on visual examination, including menace and palpebral reflexes. Deep pain responses were also present in all four limbs. The lambs body temperature was 40.5^oC, and its heart rate and respiratory rate were not elevated. 

Lamb 2: This lamb was first detected during muster that morning, when it was observed to be running in circles, charging through the mob knocking over other sheep, and behaving in a manner that the owner described as ‘crazy’. After 15 minutes pursuit in a paddock as it ran around quickly in large circles, it was examined. Its forelimbs bore increased weight, and there was a hypermetric gait. Its body temperature was 41.1^oC, and heart rate and respiratory rate were both markedly elevated. It also had normal deep pain responses, and intact menace and palpebral responses. 

Necropsy findings

EDTA and clotted blood samples were collected from Lambs 1 and 2, and a necropsy examination was conducted on Lamb 1 after euthanasia by captive bolt and exsanguination. Gross findings were unremarkable. The rumen was full of sorghum with no other feedstuffs identified. No gastrointestinal parasites were detected, and the bladder was empty. The rostral cerebral cortex was damaged by the captive bolt but the brain was otherwise intact. Brain, cervical spinal cord and samples of liver, spleen, kidney, heart and lung tissue were fixed in formalin solution and sent to EMAI for histopathological examination. 

Feed samples of the sorghum crop were collected at midday and submitted to the Feed Quality Service at Wagga Wagga Agricultural Institute for Prussic Acid and Nitrate testing. 

Laboratory findings

Serum biochemistry results showed mildly elevated creatinine kinase levels in both lambs – 791U/L and 511U/L, respectively (normal range 0-300U/L). All other parameters including calcium, magnesium, and liver enzymes AST and ALT, were within normal limits. Blood Vitamin A and E concentrations in both lambs were within normal limits. 

Microscopically, in grey matter of the ventral horn of the spinal cord, and various nuclei throughout the brainstem, including the ambiguous, accessory cuneate and cochlear nuclei there were small to moderate numbers of segmentally swollen axons (spheroids) (Fig 2). Also, within white matter tracts of the cerebellum, rostral brainstem, caudal brainstem and spinal cord were multiple foci of mild to moderate Wallerian degeneration (Fig 3). Histopathological findings in the basal ganglia were limited to mild scattered myelinic vacuolation in the internal capsule, and there were no changes observed in the cerebral cortex. 

These findings were consistent with a diagnosis of sorghum associated neuroaxonal degeneration.

Figure 2. Lamb 1, brain, caudal cerebellar peduncle, grey matter, with a spheroid (arrow head) adjacent to a neuron (arrow) (H&E stain, 1000x).

Figure 3. Lamb 1, cervical spinal cord, ventrolateral funiculus, white matter, with myelinomacrophages (arrow heads) within digestion chambers (Wallerian degeneration) (H&E stain, 1000x).

The qualitative Prussic (Hydrocyanide) Acid test on the feed sample provided showed a strong positive result. Unfortunately a quantitative result was not obtained. A nitrate / nitrite dipstick test on the feed sample was negative for nitrite, and positive for nitrate, with a level of 2500ppm. Levels above 1200ppm are considered potentially toxic to livestock. 

Outcome

No further deaths were noted after the lambs were moved to the new paddock. The remaining affected lamb (Lamb 2) returned to the mob and was assumed to recover, as it was not found dead. 

DISCUSSION

The histopathological diagnosis of sorghum-associated neuroaxonal degeneration in the one animal (Lamb 1) necropsied, suggests that the other 19 lambs in this mob grazing the sorghum crop and showing similar neurological signs, including the 18 that died, were affected by the same disorder. 

The mob was grazing a sorghum crop with high levels of cyanide, as well as potentially toxic levels of nitrate. Nitrate toxicosis is often associated with chocolate brown blood, while cyanide poisoning is described as causing bright red blood (Plant, 1992). Neither of these changes to blood colour was noted at necropsy of Lamb 1. Both nitrate and cyanide toxicoses can cause sudden death in ruminants, as well as excitement, generalised muscle tremor and staggering gait, followed by spasm and rapid death (Plant, 1992, McBarron, 1976).  Whilst trembling and ataxia were observed in these lambs, sudden death was not; Lamb 1 showed clinical signs for up to two weeks before it was euthanased. Consequently, acute nitrate and/or cyanide toxicosis is unlikely in this case. 

There was no history of access to any other potentially toxic feed or water sources. Metabolic disturbances (hypomagnaesaemia, selenium deficiency and vitamin A deficiency) were considered possible differential diagnoses, as causes of neurological disease in lambs (West, et al., 2009). Hypomagnesaemic sheep may show muscle tremors and severe nervous excitement. They may collapse on one side with their heads thrown back and have convulsions with severe limb paddling (West, et al., 2009). However, a diagnosis of hypomagnesaemia was discounted in this outbreak as hypomagnesaemic sheep don’t usually survive for weeks, and serum magnesium concentrations in affected Lambs 1 and 2 were within normal limits. 

Vitamin A deficiency is also not uncommon in the Narrabri district during drought conditions, and recent cases nearby involved lambs showing neurological signs including seizures and muscle tremors. Vitamin A deficiency is also reported to cause convulsions, syncope and paralysis (Radostits, et al., 2007). In this outbreak, hypovitaminosis A was ruled out by the blood test results for Lambs 1 and 2. Glutathione peroxidase levels were not measured in Lambs 1 and 2, as selenium deficiency was considered unlikely due to a history of supplementation, normal blood vitamin E concentrations and, in Lamb 1, an absence of gross evidence of skeletal muscle abnormality at necropsy (Radostits, et al., 2007).

Sorghum-associated ataxic syndromes occur in  horses, cattle and sheep, and in horses and cattle are associated with cystitis, urinary incontinence and birth of weak or malformed offspring (Bradley, et al., 1995).

In sheep, sorghum-associated ataxic syndrome manifests clinically as weakness, ataxia, head shaking, knuckling of fetlocks, inability to rise, and opisthotonus (Bradley, et al., 1995; Radostits, et al., 2007, McKenzie, 2012); urinary incontinence does not occur. Sorghum-associated ataxic syndrome has also been associated with the birth of weak or malformed offspring (ankylosis or arthrogryposis) and abortion (Cope, 2018 and Bradley, et al., 1995; Cantile and Youssef, 2016). Accordingly, the producer has been warned to closely monitor the ewe group during lambing for any abnormalities. At the time of writing, lambing of ewes exposed to the sorghum pasture on the affected property was approximately halfway complete with no abnormal lambs identified. 

The distinctive histopathological finding of neuroaxonal degeneration seen in Lamb 1 is a consistent feature of sorghum-associated ataxic syndrome in sheep. However, the moderate Wallerian degeneration detected within white matter in the cervical spinal cord of this case is not usually a feature of sorghum-associated syndrome in sheep, although it is the main change in sorghum-associated ataxia in cattle and horses (Cantile and Youssef, 2016; Bradley, et al., 1995).

Attempts to link the sorghum-associated ataxic syndrome (in sheep, cattle and horses) to cyanogenetic compounds in the plants are inconclusive, and a causal association with cyanides seems unlikely (Cantile and Youssef, 2016). A previous study that attempted to identify the specific contributory factors leading to increased toxicity of the sorghum crop responsible for the neurological syndrome suggested that there is an undefined toxic principle in the sorghum pastures associated with the lesions in the brain and spinal cord (Bradley, et al., 1995). 

The cessation of lamb deaths after the sheep were moved to another paddock, may be partly attributed to the associated feeding of oaten hay, which would have reduced the proportion of sorghum in the feed consumed by the lambs.

Affected animals that receive adequate nursing care (i.e. are able to eat and drink, and are safe from predators) are able to recover once removed from the sorghum crop causing the ataxic syndrome (Bradley, et al., 1995), however full recovery may take several months.

In future, to avoid repeated occurrences of sorghum-associated ataxic syndrome, this producer may choose to avoid grazing stressed sorghum crops or sorghum crops with new growth. The producer may also chose to supplement with sulphur – though care must be taken because of the possible risk of polioencephalomalacia (Cope, 2018).  

ACKNOWLEDGEMENT

Our thanks to Roger Cook, Veterinary Pathologist, EMAI, for his assistance with this case report. 

REFERENCES 

1. Bradley, G.A. et al., 1995. Neuroaxonal Degeneration in sheep grazing sorghum pastures. Journal of Veterinary Diagnostic Investigation, Volume 7, pp. 229-236
2. Cantile, C., Youssef, S., 2016 Jubb Kennedy Palmer’s Pathology of Domestic Animals 6th ed (Maxie, M. Grant, editor) Vol 1 : 305
3. Cope, R.B., 2018. Overview of Cyanide Posioning. MSD Veterinary Manual. www.msdvetmanual.com [Accessed 9 May 2018]
4. McBarron, E.J., 1976. Medical and Veterinary Aspects of Plant Poisons in New South Wales. Glenfield NSW: Department of Agriculture New South Wales
5. McKenzie, R., 2012. Australia's Poisonous Plants, Fungi and Cyanobacteria. A guide to Species of Medical and Veterinary Importance. Collingwood: CSIRO Publishing.
6. Nuseed PTY LTD, 2018. Nudan Forage Sorghum. http://www3.nuseed.com [Accessed 9 May 2018]
7. Plant, J., 1992. The TG Hungerford Vade Mecum Series for Domestic Animals. Series B, Number 15. Diagnosis of Diseases of Sheep. Sydney: University of Sydney Post Graduate Foundation in Veterinary Science.
8. Radostits, O.M., Gay, C.C., Hinchcliff, K. W. & Constable, P.D., 2007. Veterinary Medicine. A Textbook of the diseases of cattle, horses, sheep, pigs and goats. 10th ed. Sydney: Saunders Elsevier
9. West, D.M., Bruere, A.N. & Ridler, A.L., 2009. The Sheep. Health, Disease and Production. 3rd ed. Wellington: New Zealand Veterinary Association