Phalaris is a valuable perennial grass species in Australian grazing systems. It sporadically causes poisoning which can result in significant losses for producers. Seven species of Phalaris are recognized in Australia. Phalaris aquatica is the most prominent species grown in Australia and most commonly associated with poisoning events (Alden et al, 2014). Phalaris toxicity is estimated to cost Australian producers approximately $1.7 million annually with the average farmer experiencing an outbreak between one in four and one in twenty years (Sackett et al, 2006).
Phalaris is responsible for three apparently unrelated syndromes of toxicity: phalaris “staggers” which has been reported to affect sheep, cattle and kangaroos, and two forms of phalaris “sudden death” which have been reported to affect sheep, cattle, alpacas (anecdotal evidence only in alpacas) and horses (Bourke and Carrigan 1992; Bourke et al, 2003; Bourke et al, 2005; Finnie et al, 2011; McKenzie, 2012). The two forms of phalaris sudden death are described as the cardiac form of sudden death and a nervous form of sudden death (Bourke and Carrigan, 1992).
The nervous form of phalaris sudden death is known as phalaris “polioencephalomalacia (PE)-like sudden death” (Bourke et al, 2005) and resembles ammonia toxicity (Bourke et al, 2005; Windsor, 2016). This article will discuss a case of phalaris “PE-like sudden death” in a mob of lambs.
In late April 2015 a producer in Lyndhurst contacted the District Veterinarian as 35 of a mob of 4000 first cross lambs had died overnight and a number appeared unwell. The property is a mixed grazing and cropping enterprise. The mob had been moved into a new paddock the previous evening from a paddock with minimal feed. They appeared normal when being moved.
The mob was purchased in October 2014, shorn and given one dose of a multivalent clostridial vaccine (Ultravac® 5 in 1 Vaccine, Zoetis) and drenched (drench not specified). The second dose of vaccine was administered approximately four weeks after the first dose. The lambs were approximately 8 months old. They were not being fed supplementary rations.
There was no history of problems in the paddock. No toxic plants had been identified and none were seen on a paddock inspection. The water source, being a clean trough, was determined to be adequate. The pasture was predominantly (95%) Phalaris aquatica, cultivar unknown, with a small amount of sub clover (Trifolium subterraneum). The pasture had not been fertilised in the past three years. The paddock grazed prior to this was cocksfoot (Dactylis glomerata), ryegrass (Lolium perenne) and sub clover that had been grazed bare. No toxic plants were identified. The same water source (scheme water) was used in the troughs in both paddocks.
The paddock adjacent to where the sheep had died had been treated with metaldehyde snail and slug lentils overnight (Delicia® Sluggoff Lentils®, 30mg/kg Metaldehyde, Animal Control Technologies, Australia – see figure 1). Some of the lentils were believed to have contaminated the paddock, considering the spreader used disperses pellets over approximately a 3m range.
Two affected lambs examined presented similarly. They were both in lateral recumbency with muscle fasciculation, nystagmus and frothing at the mouth. They displayed hyperaesthesia with intermittent paddling of limbs, tetanic convulsions and opisthotonus. There was no menace reflex identified. They had pyrexia at 420C, tachycardia - heart rates between 140-150bpm, tachypnoea – respiratory rates between 50 -60bpm. Their mucous membranes were pink and the capillary refill time was normal (<1 seconds) in both.
One live affected lamb was mobile and appeared to be ataxic. The manager noted that some lambs had run into fences and appeared blind and ataxic before becoming recumbent.
Two more lambs died later that day, but no further deaths were reported thereafter. The lambs had been moved to a yard and given hay after the deaths were discovered in the morning.
The two recumbent lambs were euthanised. On post-mortem there were no significant gross abnormalities. Dipstix (Multistix®, Siemens) urinalysis was within normal limits. No molluscicide lentils were found in the gastrointestinal tract.
The following samples were collected during the post-mortem:
One set of samples was submitted for testing with the following tests requested: Complete blood count and biochemistry including ammonia levels, nitrate and nitrate levels, histopathology of liver, kidney and brain and faecal worm egg count and typing.
No worm eggs were detected in the faecal samples.
A private laboratory was located that was able to test tissue samples for metaldehyde levels ($340 for each tissue tested). It was decided to hold this testing until the biochemistry and histopathology results had been obtained.
|WBC||4.0-12.0||10^9 /L||12.1 High|
|BAND N.||0.00-0.50||10^9 /L||0.00|
|NEUTRO.||0.70-6.00||10^9 /L||9.44 High|
Platelet clumping observed; platelets appear adequate on blood film; Haemolysis (+); positive interference in PROT-RTS assay.
The vacuolar changes in the cortical grey matter represent astrocytic oedema. Similar oedematous changes are seen in polioencephalomalacia, where they are accompanied by neuronal necrosis, whereas neurones in cases of Phalaris PE-like sudden death are largely intact. The lesions are also distinct from hepatic encephalopathy associated with more protracted hyperammonaemia of chronic hepatopathy; the underlying process here is intramyelinic oedema manifesting as variably sized often large and elongated vacuoles at the white-grey matter junction. It has to be noted that vacuolation can be a post-mortem artefact, and identification of the brain lesions of Phalaris PE-like sudden death, although variable, is most reliable in fresh brain samples.
Hyperammonaemia remains the most valuable diagnostic indicator, together with the clinical history, and exclusion of other common causes of hyperammonaemia in ruminants.
The main laboratory findings were: a marked, peracute oedema of the cerebrocortical grey matter and hyperammonaemia.
There were non-specific degenerative hepatocyte changes. In the opinion of the pathologist these changes would not cause liver failure with hyperammonaemia and are terminal changes. There was no evidence of a significant hepatopathy.
The mild decrease in calcium levels was clinically insignificant.
Samples of aqueous humour taken from two lambs were subsequently analysed for ammonia levels (they had been frozen). Both had increased ammonia levels in the aqueous humour. The reference range is 0-200umol/L and the samples were both high at 1770 umol/L and 2020 umol/L, respectively.
Further tests to determine metaldehyde and lead tissue levels were not pursued.
No treatment was given.
Differential diagnoses considered on first examination included metaldehyde toxicity, acute phalaris poisoning, polioencephalomalacia, focal symmetrical encephalomalacia, lead poisoning, hepatopathy (causing hepatic encephalopathy), calcium and or magnesium disturbances and tetanus. The first two differentials were considered most likely in light of the history. The laboratory findings did not support the other diagnoses.
The LD50 of metaldehyde in sheep is 300mg/kg. Metaldehyde is primarily a neurotoxin which can cause central nervous system depression, clonic seizures and death by respiratory failure, consistent with the signs observed in the affected lambs. The severity of signs and symptoms depends on the amount of metaldehyde ingested. Onset of signs occurs between 15 minutes and a few hours of ingestion (Gupta, 2007). The average weight of the lambs was 30-35kg. It was calculated that the lethal dose of the lentils would be 300-350mg. This made poisoning by this means appear less probable considering it was unlikely a sufficient volume of lentils was deposited in the paddock to kill 37 lambs: very few lentils were found during paddock inspection and none were found in the gastrointestinal tracts of post-mortem animals. Given this reasoning, associated cost and a plausible alternative diagnosis, tissue testing for metaldehyde was not performed.
The laboratory findings supported a diagnosis of phalaris “PE-like sudden death” specifically there was a marked, peracute oedema of the cerebrocortical grey matter and hyperammonaemia. In the absence of a significant hepatopathy and with no history of exposure to urea, the hyperammonaemia is most likely due to poisoning by phalaris. The brain lesions, although not pathognomonic, are consistent with peracute astrocytic oedema as seen in peracute ammonia toxicity and phalaris “PE- like sudden death” (Bourke et al, 2005). The brain pathology and high blood ammonia levels in lamb one and high aqueous humour ammonia levels in lamb one and two in addition to the history and clinical signs concluded with a diagnosis of phalaris “PE- like sudden death”.
Intoxication of sheep causing “sudden death” was first described by Moore et al in 1961. This was later characterised as a cardiac dysfunction by Gallagher et al 1964. Bourke and Carrigan (1992) reviewed 20 outbreaks of sudden death in sheep between 1981 and 1991 and defined a cardiac presentation and a polioencephalomalacic presentation.
In this paper, the cardiac presentation was defined as sudden onset of collapse, respiratory distress, cyanosis, ventricular fibrillation and cardiac arrest in sheep grazing phalaris dominant pastures after they were mustered or otherwise disturbed. Mildly affected sheep may recover after a brief period of collapse and respiratory distress. Nervous signs are not seen in these cases clinically and there were no lesions on brain histopathology.
The polioencephalomalacic form was defined as dead sheep on phalaris pastures with histologically identified brain lesions. Signs in surviving sheep included: blindness, aimless wandering, head pressing, intermittent paddling, head and body tremors, teeth grinding, ear and face twitching, coma, convulsions (Bourke and Carrigan, 1992).
In cases of phalaris sudden death reported in the literature, death occurs within 12-48 hours of sheep being moved onto the phalaris pasture. In most cases the sheep are hungry when moved onto the phalaris pasture. The phalaris plants are often short, dry weather affected and freshly shooting. The polioencephalomalacic sudden death outbreaks generally occur between late autumn and early winter (Bourke & Carrigan, 1992; Bourke et al, 2003; Bourke et al, 2005, Finnie et al, 2011).
As the toxin(s) responsible for the acute poisonings have not been identified and there is no effective treatment known, prevention of such poisoning by adhering to known pasture management strategies is the only way of reducing stock losses (Alden et al, 2014; Windsor, 2016).
The impact of phalaris sudden death can be reduced if stock owners are advised not to put hungry sheep onto phalaris pastures. This applies particularly to sheep managed by rotational grazing systems, sheep held without feed for a day or more and sheep that have been transported over long distances. Rain following a period of moisture stress seems to enhance the potential toxicity of phalaris (Bourke and Carrigan, 1992). In this case, the rainfall data for the area was not unusual for the time of year (see Appendix 1).
As expressed by Windsor (2016) “it is advised that the phalaris pastures are continuously grazed or set-stocked to keep the new growth during autumn/winter to a minimum, and that hungry sheep should not be placed on previously spelled phalaris dominant pastures, especially not following periods of moisture stress or heavy frosts. From autumn through to late winter it may be wise to test the toxic potential of a paddock by placing a group of sentinel sheep onto the paddock 48 hours before the entire flock is given free access.”
A current but unproven theory is a toxin that inhibits the urea cycle resulting in acute ammonia toxicity; a high nitrogen content of the phalaris pasture would further increase its toxic effect, as would simultaneous ingestion of other feed high in nitrogen eg legumes (Windsor, 2016).
There is still much to be learnt from cases of acute phalaris poisoning, and as recommended by Bourke and Carrigan (1992), veterinarians investigating such cases are advised to: accurately record the signs displayed by any affected survivors, collect brains for histopathology, collect rumen samples, collect whole blood and aqueous humour from affected sheep and toxic pastures for cyanide and nitrate determination.
Further, it is advised that fixed liver samples are submitted in suspect cases acute phalaris sudden death to exclude hepatic failure as cause of hyperammonaemia. In live animals, serum should be taken off the clot as soon as possible to estimate ammonia levels. Aqueous humor should be removed from the eyeball as soon after death as possible and chilled for ammonia testing. Details of pasture grazed and supplementary feed should be included in the history. Histopathology is most useful on brains of euthanased or freshly dead animals, as the lesions of peracute hyperammonaemia are quite subtle, and post-mortem artefacts interfere with interpretation; however, brains from animals that have been dead for longer may still be useful for exclusion of other neurological disease e.g. polioencephalomalacia or listeriosis. In this way a greater understanding of phalaris poisoning events will be obtained.
Rainfall data for 2013 - 2015 in Lyndhurst.