Drought-breaking rain received by the Coonamble district in autumn 2020 saw abundant growth of the plant small-flowered mallow or marshmallow (Malva parviflora) and many subsequent cases of staggers in sheep flocks. Despite the condition being described in the literature as far back as the late 1800s, relatively little is known about its toxic principles or mode of action.
Local Land Services investigated fourteen cases of marshmallow staggers from June to October 2020 in the Coonamble district, with many more cases assumed by farmers to be marshmallow-related and not investigated by a veterinarian. The last time marshmallow staggers were seen on this scale in the Coonamble district were anecdotally reported to be during the 1970s. This paper aims to describe a selection of case presentations including contributing causative factors and outcomes.
On 1st June, a property in the Coonamble district was visited to look at lambs that were trembling and lying down in sternal recumbency when the mob of 1000 mixed age Merino ewes with four- to nine-week-old first-cross lambs at foot were brought in for lamb marking. Ten lambs were observed to be affected, while their mothers were clinically normal.
The lambs that were examined in the yards were bright and alert but had generalised muscle fasciculations and preferred to lie down rather than stand (see Video 1). Their temperatures were normal and their mucous membranes were pink. The farmer noted that the clinical signs had improved when the sheep were held in the yards on some hay for a period of time.
None of the lambs died, and as they seemed to be improving no lambs were necropsied.
An inspection of the paddock the sheep had come from found very few pasture species with small-flowered mallow as the dominant species. The owner had put grain feeders out into the paddock as he realised that the pasture was inadequate for lactating ewe nutrition.
Based on the clinical signs and the paddock inspection, other differentials such as hypocalcaemia, Mycoplasma ovis (M. ovis) infection (weaner anaemia) and border disease were excluded and a provisional diagnosis of marshmallow staggers made.
The owner continued lamb marking (using rubber rings) and afterwards moved the mob to a cereal crop. He walked most of the mob but had to pick up the worst affected lambs in a trailer. The mob was provided with hay and lime / salt in tubs. None of the lambs died and all were reported to be clinically normal two weeks later.
On 27th July, a property was visited to look at a mob of 540 single Merino ewes with lambs at foot that were mustered the evening before for lamb marking and mulesing. They were clinically normal during the 4km walk to the yards. They were held overnight in yards that were heavily dominated by Malva parviflora.
The lambs were bright and alert and had generalized muscle fasciculations. They had a 'tucked up' appearance and lay down in preference to standing. Their temperatures were normal, their mucous membranes pink and lung sounds normal. The ewes were clinically normal.
A post-mortem of one of the lambs was performed. The lamb was estimated to be eight weeks old and its abomasum was full of milk. The rumen was full of green plant material. The heart, spleen and liver were grossly normal. There was some cranioventral consolidation of the lungs, but this finding was presumed to be inhalational when exsanguinated. The hindlimb and forelimb muscles were grossly pale orange. There was some red-brown streaks through the cortex and medulla of the kidney.
Laboratory testing of the samples submitted showed mildly elevated CK of 361U/L (0-300U/L), normal AST, normal GSH PX (glutathione peroxidase) on both blood and liver, and normal Haptoglobin. The M. ovis PCR test was negative. Heart histology showed myocardial necrosis (subacute, multifocal, mild).
A diagnosis of marshmallow staggers was made based on the clinical signs of the lambs with clinically normal ewes, the history of being locked in an area heavily dominated by Malva parviflora for 12 hours prior, the exclusion of other differentials and the heart histology.
Lamb marking was attempted that day on 100 lambs, but was abandoned because many of the lambs lay down, with the mob put out into a nearby paddock. None of the lambs died and they recovered over the next week. They were returned to the yards (which were then free of Malva parviflora) and marked two weeks later with no further clinical signs.
In August, the local private practitioner visited a farm near Carinda to look at a mob of 240 maiden 1.5-year-old Merino ewes after the owner noticed a few animals dropping into sternal recumbency when mustered. They were grazing a paddock where Malva parviflora was prevalent, especially under trees and in areas where the sheep camp, although there was other pasture available in the paddock.
One of the sheep that the owner had put aside to look at had recovered and was ambulatory by the time the veterinarian visited. Blood was taken from this animal. The other sheep was still in sternal recumbency, was bright and alert with a temperature of 38.9°C and was condition score 3.5. A post-mortem was conducted. The only gross findings were that the urine was port wine coloured and the cortico-medullary junction of the kidney had red streaks throughout.
Laboratory testing showed extremely high CK in both animals with readings of 535,579 and 617,053 (0-300U/L). Haptoglobin was also extremely elevated at 1.41 and 0.69 (0-0.3g/L). Histology revealed myonecrosis (acute monophasic, multifocal, severe) in the skeletal muscle and myocarditis (necrotizing, granulomatous, chronic, focal, severe) in the heart muscle.
The laboratory noted that gross examination of the fixed skeletal muscle showed a marked longitudinal linear streaky pale pattern, suggestive of necrosis and this observation was confirmed by the histological changes (see Figure 1). The myonecrosis is consistent with a toxic myopathy, possible causes include Malva parviflora, Ixiolaena brevicompta (billy buttons), inonophore toxicosis or selenium toxicosis.
Due to the prevalence of the plant and the history of other cases across the district, a diagnosis of marshmallow staggers was made.
One hundred and forty crossbred mixed-sex lambs with an average weight of 55kg were trucked from a property north of Coonamble to the Dubbo saleyards in mid-September.
Upon unloading, the sheep were noticed to tremble and were keen to lie down. They were put up for sale but due to the clinical signs were rejected by the buyer and instead put into a pen and fed hay. Approximately ten died. After a week on hay in the pen, the sheep were trucked back to the property of origin. Approximately ten more died during this trip and five were found to be down and trembling upon arrival home.
Lamb One was examined in sternal recumbency. It could stand but had generalized muscle fasciculations and was ataxic and knuckling on its hind legs. It walked a few steps but preferred to lie down in sternal recumbency with its legs tucked under itself. Video 2 is from another case, but shows the clinical signs seen in adult sheep. Mucous membranes were pink, heart rate slightly elevated, temperature normal, and lung sounds normal. This sheep was given 300ml of Minbal 4-in-1 (ca gluconate 27.5g/L, magnesium hypophosphite, hypophosphite 12.2g/L, glucose 182g/L) solution subcutaneously but did not respond.
Lamb Two had died just prior to the visit. The only abnormality seen grossly on post-mortem was pale orange muscle bellies in the hind legs.
Laboratory testing of post-mortem samples found aqueous humour calcium to be normal 1.52mmol/L (>1.4mmol/L), aqueous humour negative for nitrates (performed in the field) and myositis (lympohistocytic, multifocal, mild with myocyte degeneration) in both the skeletal and heart muscle examined. These lesions are consistent with Malva parviflora toxicity.
A mob of 1000 mixed-sex weaner merino lambs from near Warren were marked in August 2020. There were 60 shaking lambs that lay down at lamb marking, with clinically normal ewes. The owner sought veterinary advice via phone at this time and a provisional diagnosis of marshmallow staggers was made. The lambs recovered post-marking.
These lambs were weaned in late September and were put onto 17 hectares of wheat crop that ran down to a creek. The sheep were not receiving any mineral supplementation. Malva parviflora was present along the creek under the trees. The plants were dry, but it appeared that the seeds had been stripped off the stalks by the sheep.
In mid-October, they were moved into another pasture paddock with a good species variety including a scattering of Malva parviflora. When moved, some lambs were seen to shake, then lay in sternal recumbency. Thirteen died or were euthanased by the overseer. A veterinary visit occurred at this time, but no diagnosis was reached. Heart, liver, kidney and gastrointestinal tract histology were all unremarkable and calcium levels were normal.
In late October, on a Friday, the lambs were again mustered a short distance for shearing. Approximately 60 went down upon mustering and many had to be carried to the yards. On Saturday there was a cold change and heavy rainstorm. Approximately 40 lambs died in the yards.
A veterinary visit on Monday morning found a number of lambs in sternal recumbency in the yards with generalized muscle fasciculations. The lambs could stand, but when they walked had a “humped” appearance and were ataxic and knuckling in the hind limbs. Mucous membranes were pink, temperatures of two lambs were both 40°C and lung sounds were clear. There was no response to administration of Minbal 4 in 1 (ca gluconate 27.5g/L, magnesium hypophosphite, hypophosphite 12.2g/L, glucose 182g/L) subcutaneously.
Three lambs were necropsied. There were no gross abnormalities on post-mortem. Aqueous humour was negative for nitrates on dipstick performed in the field.
Laboratory examination of the tissues submitted revealed elevated CK 1556U/L (0-300) and cardiomyopathy (monophasic, subacute, multifocal, mild to moderate with myocyte loss, regeneration and repair). The laboratory commented that the heart lesions were most likely due to toxic insult from toxic plants such as Malva parviflora or Ixiolaena brevicompta, plants containing cardiac glycosides, or ionophores and that the lesions were in the regenerative / repair phase. They were an estimated 7-10 days old.
A diagnosis of marshmallow staggers was made based on these findings. Shearing continued at a slow and gentle pace and the lambs were put into a paddock with less Malva parviflora. The remainder recovered.
Malva parviflora (commonly called marshmallow or small-flowered mallow) is an annual weed in Australia. It is thought to have been introduced intentionally as a garden plant sometime prior to 1845 as it was cultivated in Europe as a salad vegetable (Dalby, 1968). Stanley (1895) noted that the plant was present on the Hunter and Richmond Rivers since around 1880. By 1922, it was noted by Dodd and Henry that there was "luxuriant growth" following rain in the Gwydir, Peel and Namoi river areas. It is reported in the literature to grow to 60cm high, however under the right conditions, such as those experienced at Coonamble in 2020, it grows to over two metres in height. It produces very small white to pink flowers in early spring that develop into fruitlets or seeds which appear as small green buttons, and as the warmer weather progresses these become black, wrinkled and ribbed at the edges. These seeds seem to be appetising to sheep and are commonly associated with staggers in many of the cases seen. In many cases of staggers the marshmallow was dry stalks, but the sheep had stripped the stalks bare of the seeds.
Staggers associated with marshmallow have been reported in NSW as far back as 1895 (Dodd & Henry, 1922). Cases have also been reported in Western Australia (Main & Butler, 2006). Despite case reports over the past 100 years, there is little published evidence of the toxic principle or mode of action. Early researchers have suggested that plant nitrate content may be a contributing factor (Stewart 1900, Webb 1952), however Dodd and Henry (1922) dismissed this theory on both clinical and physiological grounds. A feed test conducted on marshmallow in the early flowering stage that was two metres tall from Trangie in June 2020 showed the nitrate content to be 3948 mg/kg NO3 (see figure 1), which is below the toxic threshold for livestock. This finding, combined with testing for nitrates in many of the cases investigated during 2020, also indicates that nitrates are not involved in the pathogenesis of the disease. Main and Butler (2006) surmised that the toxin or toxins target the musculature rather than the central nervous system, which is consistent with our observations.
Tables 1 and 2: Feed tests from Marshmallow plants, Trangie 2020
|Neutral Detergent Fibre (NIR)||%||39|
|Acid Detergent Fibre (NIR)||%||21|
|Crude Protein (NIR)||%||33.3|
|Metabolisable Energy||MJ/kg DM||12.6|
|Water Soluble Carbohydrates||%||4.5|
|Nitrate (as NO3)||mg/kg||3948|
|# Tests were performed using ICPMS|
The symptoms of staggers produced by Malva parviflora as described by Dodd and Henry (1922) are that affected animals lag behind, move with a stiff action in the hind legs, arch the back and have the head stretched out. They rapidly become worse if travelling and eventually are unable to continue. The respiration is rapid but shallow and the pulse quick. A trembling or quivering of the muscles of the shoulders and hindquarters and sometimes of the whole body develops. Finally, the animals go down with head and legs stretched out or with the body resting on the sternum with the forelegs doubled under. If allowed to rest they will, at length, rise and walk away. If urged to move they may die.
Dodd and Henry's 1922 feeding trials found that ingestion of large quantities of Malva parviflora (0.5-6.5kg per day) and driving the sheep produced clinical disease in lambs at foot (with clinically normal ewes) in as little as five days, continuing for up to 43 days (Malva parviflora being fed during this period). They could produce clinical disease in adult dry sheep with ingestion of 2-6.4kg of Malva parviflora in as little as nine days, symptoms continuing for 23 days. The plants used in these experiments were fresh short mallow, dried mallow freshly cut, tall mallow, and from new growth to fully flowering and seeding stages. They also induced clinical disease in one sheep being fed a sole diet of 700g of Malva parviflora seeds per day after six days. As a result of these feeding trials it seems that all above-ground parts of the plant can produce myopathy, signs of which are exhibited when the sheep are exercised.
The paper postulated that the reason that suckling lambs showed symptoms while their dams remained clinically normal is that young lambs are highly susceptible to the toxin and adult sheep must ingest a much larger amount of the plant. The authors went on to say that they thought it more probable that the toxic principle can be transmitted in the milk of the ewes without these showing any symptoms of staggers.
In 1928 Marsh, Clawson and Roe could not produce staggers by feeding 5.2-5.9% of their body weight of the dried plant to sheep, but in this experiment the sheep were not exercised. This observation parallels some of the findings from the feeding experiments recorded by Dodd and Henry in 1922. As such, the disease seems to be induced by a complex interaction between the plant and exercise.
Sheep seem to recover from the staggers if removed from the plant and given other pasture or hay to eat. The recovery time varies from a few days to several weeks and seems to be longer in animals that are low in condition (Hurst 1942). Dodd and Henry (1922) proved that one attack of the disease does not confer immunity and that a move back onto Malva parviflora can induce staggers once again.
Marshmallow staggers should be considered a differential for staggers in both lambs and adult sheep when the plant is present in large quantities. In the Coonamble district this scenario does seem to happen after autumn rains, with the plant growing profusely throughout the winter months. The plant seems to flourish after drought, especially in areas where there has been a reduction in ground cover.
While the exact toxin and mode of action is still unknown, it seems to produce two clinically distinct syndromes - tremors and exercise intolerance in suckling lambs (with clinically normal dams), and ataxia and exercise intolerance in weaners or adult sheep.
Diagnosis can usually be confirmed with histology of skeletal muscle and heart muscle, with improved chances when a range of samples—for example hindlimb and forelimb muscle bellies, diaphragm and tongue, as well as multiple sections of heart muscle, from several animals—are submitted.
CK levels can be useful to support a diagnosis, however in our experience the clinical signs do not seem to parallel the elevation in CK and it can be an unreliable indicator when viewed in isolation.
I would like to thank the Central West Local Land Services District Veterinarian group who all contributed their thoughts on marshmallow staggers throughout 2020, as well as Shaun Slattery from North West Local Land Services for sharing his references, case histories and lab results.