Enzootic ataxia, or ‘delayed swayback’, was first reported in Australia in 1937 and is generally accepted to be associated with foeto-maternal copper deficiency. Historically it has most often occurred in areas that have naturally high levels of molybdenum in the soil (Campbell, 1983). As modern farming methods have evolved, fertiliser application, utilisation of various grazing crops such as canola and water management practices have influenced the mineral and trace element profiles in soil and pasture. As a result, now when there are suspect cases the presentation needs to be considered in combination with the particular farm’s history as cases will occur outside of areas that have naturally high levels of molybdenum in the soil.
A Boer goat stud located near Young NSW, with 600 does kidding from September to October, was visited on 28 November 2018, after the producer reported a history of ataxic kids. The first case was in 2017, with a two-month-old buck identified as having an unusual gait, which progressed over several months to sternal recumbency, culminating in death at eight months of age (Image 1).
In 2018, two two-month-old kids were identified as being ataxic and staggering, which again progressed to recumbency. They remained bright, alert and responsive and ate and drank if nursed, but failure to recover and thrive prompted the owner to euthanise one animal before calling the District Veterinarian.
These episodes of ataxia had only occurred since the goats were moved onto the current property two years ago. The does kidded in the same paddock in both 2017 and 2018, which had undergone soil testing in 2016, showing elevated levels of iron (Table 1). The does were provided with lick blocks containing iodine because the farmer was of the opinion that it may help manage chronic lameness in the flock.
|Organic Carbon %||0.87 %|
|Nitrate N mg/kg||51 mg/kg|
|Sulphate S mg/kg||8 mg/kg|
|Phosphorus (Colwell) mg/kg||38 mg/kg|
|Potassium (Colwell) mg/kg||270 mg/kg|
|Potassium (Amm-acet.) meq/100g||0.69 meq/100g|
|Calcium (Amm-acet.) meq/100g||1.76 meq/100g|
|Magnesium (Amm-accet.) meq/100g||0.38 meq/100g|
|Aluminium (KCl) meq/100g||0.31 meq/100g|
|Sodium (Amm-acet.) meq/100g||0.04 meq/100g|
|Elect. Conductivity dS/m||0.154 dS/m|
|Copper (DTPA) mg/kg||0.52 mg/kg|
|Zinc (DTPA) mg/kg||0.55 mg/kg|
|Boron (Hot Water) mg/kg||0.41 mg/kg|
|Manganese (DTPA) mg/kg||52 mg/kg|
|Iron (DTPA) mg/kg||135 mg/kg|
|Amm. Nitrogen (KCl) mg/kg||6 mg/kg|
|Cation Exch Cap meq/100 g||3.18 meq/100g|
|Calcium / Magnesium ratio||4.63|
|Potassium % of cations||21.7 %|
|Calcium % of cations||55.4 %|
|Magnesium % of cations||12 %|
|Aluminium % of cations||9.7 %|
|Sodium % of cations (ESP)||1.3 %|
|Elec. Cond. (Sat. Ext.) dS/m||1.54 dS/m|
The remaining clinically affected kid was in lateral recumbency, although bright, alert and responsive, normothermic, picking at grass and urinating and defecating normally. It struggled to remain in sternal recumbency unless assisted, was unable to stand and had slow to absent proprioception. Hind limbs appeared to be held in rigid extension for periods of time and had moderate muscular atrophy. There was a fine head tremor, most notable when held in sternal recumbency. Pupils were of equal size and neurological exam was otherwise unremarkable.
The post-mortem was unremarkable. The brain and cervical spinal cord were removed and fixed in 10% formalin for histopathology.
Biochemical and haematological abnormalities were as expected for a recumbent animal including: mild haemoconcentration (indicative of dehydration); mildly decreased creatinine (suggestive of poor muscle mass); mild hyperketonaemia (consistent with negative energy balance); mildly increased CK (consistent with myopathy); and a mild increase in GLDH (indicative of a hepatopathy).
Serum lead levels were below detectable limits and serum copper levels were within normal limits. Caprine arthritis encephalitis ELISA was negative.
Histopathology identified that within all sections of the cervical spinal cord, white matters tracts within the ventral and lateral funiculi had extensive, bilaterally symmetrical, moderate degenerative lesions. Swollen myelin sheaths were arranged in rows, and often contained axonal fragments and macrophages within their lumens (digestion chambers, Wallerian degeneration), or rarely round to ovoid, homogenous, eosinophilic material (spheroids) (Images 2 & 3). Within the ventral motor horn of one section, an individual neuron was enlarged with markedly swollen cytoplasm and dispersion of the Nissl bodies (central chromatolysis). There were no significant findings within examined brain sections, which included the frontal, parietal and occipital lobes of the cerebral cortex, the basal ganglia, the thalamus and the rostral brainstem.
In January 2019 pasture from the paddock that the does had grazed during gestation and kidding underwent analysis in two separate halves as the producer had managed them differently, spreading chicken manure, compost and lime on the bottom of the paddock and not the top (Table 2).
|Pasture Analysis of ‘Kidding Paddock’||Recommended Trace Element Allowances for Goats|
|Element||Bottom Half of Paddock||Top Half of Paddock||Average||Recommended dietary level|
|Aluminium||390 mg/kg||400 mg/kg||395 mg/kg|
|Arsenic||<5 mg/kg||<5 mg/kg||<5 mg/kg|
|Boron||13 mg/kg||8.1 mg/kg||10.55 mg/kg|
|Cadmium||<0.2 mg/kg||<0.2 mg/kg||<0.2 mg/kg|
|Cobalt||0.3 mg/kg||0.22mg/kg||0.26 mg/kg||0.1 mg/kg DM|
|Copper||6.6mg/kg||7.2mg/kg||6.9 mg/kg||8-10 mg/kg DM|
|Manganese||260 mg/kg||94 mg/kg||177 mg/kg||40-50 mg/kg DM|
|Molybdenum||0.45 mg/kg||0.4 mg/kg||0.425 mg/kg||0.1 mg/kg DM|
|Nickel||3.6 mg/kg||2.4 mg/kg||3 mg/kg|
|Lead||<2 mg/kg||<2 mg/kg||<2 mg/kg|
|Selenium||0.17mg/kg||0.09mg/kg||0.13 mg/kg||0.1 mg/kg DM|
|Zinc||30 mg/kg||30 mg/kg||30 mg/kg||50 mg/kg DM|
Significantly, the copper levels were mildly low and the iron levels high in comparison to goat dietary requirements and levels that influence copper absorption. The sulphur results were adequate in the bottom half of the paddock with 0.23% and slightly below requirements in the top half of the paddock with 0.19% (average of 0.21%). The copper to molybdenum ratio was 16.2:1.
Due to the narrow safety margin of copper and the risk of toxicity, and the relatively low number of ataxic animals, copper supplementation was not advised. Were there to be increased numbers of ataxic kids, copper supplementation might have been indicated, but should only be provided to pregnant does during gestation. Despite these recommendations, the producer opted to provide lick blocks containing copper, starting with twelve bucks, five of which died shortly thereafter; cause of death was not investigated, but copper toxicity was a potential cause. The producer has continued to provide lick blocks containing copper and iodine, with fewer deaths, and now plans to custom mix his own loose lick.
In Australia, secondary copper deficiency is a more common cause of enzootic ataxia than primary copper deficiency. This finding is not surprising considering Australian soils are typically not copper deficient and that differences in feed iron, molybdenum and sulphur levels can result in a fourfold variation in bioavailability of copper, and therefore their ability to provide adequate copper to ruminants (Underwood & Suttle, 1999).
Previously, much of the nutritional recommendations for goats has been extrapolated from the requirements of sheep and cattle. In 2000, Meschy reviewed the recent advances in goat nutrition studies, including microminerals such as copper. As for other ruminants, the copper requirements of goats is 8-10 mg/kg dry matter (DM) intake. However, the difference between goats and other ruminants is that hepatic storage is ten times lower in goats, leading to a higher susceptibility of newborn kids to enzootic ataxia (Meschy, 2000).
Meat and Livestock Australia has published an extensive report reviewing copper deficiency in southern Australian sheep flocks, which investigated the productivity and economic implications of copper deficiency and recommendations for treatment and ongoing management of deficient flocks. It is suggested that fertiliser practices in modern farming have changed the mineral and trace element profiles, highlighting the importance of managing pastures on an individual basis (Dickson, 2016).
There is poor agreement within the literature regarding ovine and caprine copper requirements. Reported copper requirements in sheep are usually 7-11 mg/kg DM, but levels as low as 0.5 mg/kg DM have been suggested, perhaps not accounting for actual bioavailability (Dickson, 2016). Goats are thought to have similar requirements, 8-10 mg/kg DM (Meschy, 2000), suggesting that the analysed pasture (6.9 mg/kg DM) may have been slightly copper deficient.
Iron levels of >150 mg Fe/kg DM, as in this case (average of 375 mg/kg), can adversely affect the bioavailability of copper (Bone, 2010; Dickson, 2016). Although the exact mechanism is unknown, hypotheses include iron/sulphur/copper complexes in the rumen that are excreted or iron sulphide forming in the rumen and then binding copper in the acidic environment of the abomasum, forming copper sulphide that is also excreted (Dickson, 2016).
Sulphur acts both independently and in combination with molybdenum to antagonise copper absorption (Dickson, 2016) by forming copper monosulphide, an insoluble and therefore unavailable compound. Of the two, molybdenum rather than sulphur is the primary influencing factor (Underwood and Suttle (1999). Sulphur requirements in the goat are slightly higher than other ruminants, being 2.2 g/kg during growth and 2.6 g/kg during lactation (Meschy, 2000). In this case, the sulphur results were adequate in the bottom half of the paddock (0.23%) and slightly deficient in the top half of the paddock (0.19%), with an average of 0.21%, or 2.1 g/kg pasture.
Recommended copper to molybdenum ratios vary across literature (Dickson, 2016). A ratio of less than 5:1 is thought to be suggestive of potential copper deficiency, while a ratio of less than 2:1 is a highly suggestive. In cases such as this one where concentrations of sulphur and/or iron exceed the animals’ requirements, the most appropriate ratio of copper to molybdenum is 5:1 (Dickson, 2016). In this case the Cu:Mo ratio was 16.2:1 suggesting that molybdenum was not the cause of the secondary copper deficiency in this case.
The normal serum copper levels in the kid indicate that the copper levels in its diet were adequate, however it is not reflective of the serum copper levels of the pregnant doe in the last trimester. The histopathological changes associated with enzootic ataxia are caused by a copper deficiency during the last 2 months of gestation.
Histopathological findings were consistent with many of the features of enzootic ataxia, however there were some unobserved changes that have been described in the literature, including neuronal degenerative changes in the red, lateral vestibular and medullary reticular nuclei, and the dorsal spinocerebellar nuclei in Clarke’s column. Additionally, although the cerebellum was not histologically examined in this case, a distinctive lesion described in goat kids is cerebellar degeneration and dysplasia, characterized by necrosis and dystopia of Purkinje cells, depletion of the granule cell layer and Wallerian degeneration in white matter tracts (Cantile & Youssef, 2016).
A diagnosis of enzootic ataxia was made in this case on the basis of consistent clinical signs and histopathological findings, and was supported by pasture analysis results. Secondary copper deficiency associated with elevated iron levels, detected in the soil in 2016 and in the pasture samples in 2018, was probably the primary cause of enzootic ataxia in this case, although there may have been some component of primary copper deficiency as well. These findings highlight the importance of investigating soil and pasture mineral and trace element profiles on an individual property or paddock basis, rather than by district, given that prior to 2018 diagnoses of copper deficiency had not been made in Young for approximately 20 years. Interestingly, over the summer of 2018-2019, two more cases of copper deficiency were diagnosed in the Young area, perhaps suggesting that seasonal drought conditions may have also been an influencing factor.