This case report describes a disease investigation of sudden death in 83 of 738 composite ewes that gained access to pig’s ear (Cotyledon orbiculata) in an unoccupied house garden. Pig’s ear (or round-leafed navel-wort) is a commonly cultivated South African succulent plant known to contain the cumulative cardiac glycoside, bufadienolide.1,2 This plant causes a well-known neurotoxicosis in South Africa1, and poisonings due to bufadienolide-containing plants are considered the most important plant-associated poisoning of livestock in South Africa.2 In Australia, C. orbiculata is a plant that is commonly found in household gardens, but no confirmed poisonings have been reported.1
In November 2019, a sheep producer in the Riverina reported a significant number of deaths in a flock of 738 composite ewes. The deaths started on 30 October 2019 with 56 found dead around or near water sources, or under shade. A further eight were found dead on 1 November, and two on the 3 November. The ewes had been grazing a barley cereal crop and were supplementary fed straw and wheaten hay. Five days prior to the deaths occurring, the producer removed the ewes from an unoccupied house yard, that they had broken into two days previously. The producer reported that he did not initially notice any clinical signs in the affected ewes prior to death.
A farm visit was performed on 4 November 2019 to necropsy one clinically affected ewe. The ewe was in sternal recumbency, alert and responsive but unable to rise. The ewe was in good body condition and significant bilateral distention of the abdomen was observed. There was also small amounts black tarry diarrhoea present around the anus and on the ground surrounding the ewe. Blood was collected from the ewe prior to euthanasia and necropsy.
On necropsy the most significant finding was multifocal mucosal haemorrhage of the abomasum (Figure 1) and intestines. The entire abomasum was severely erythematous with petechiation and/or ecchymoses observed along the abomasal folds. The intestinal contents were blood stained and the intestinal mucosa was moderately erythematous. The rumen was largely distended and filled with a significant amount of water and normal ruminal contents, which likely caused the abdominal distention seen on clinical exam. No other abnormalities were detected.
An inspection of the unoccupied house yard revealed scattered rubbish including old toys, garden equipment, drums, water pumps, tanks, paint, wood, and glass. The predominant plant in the yard was a succulent, subsequently provisionally identified by the previous owner as pig’s ear (Cotyledon orbiculata). Identification of this plant was difficult at the time of the visit as no leaves remained on the wooden stems but the lack of foliage suggested that these plants had been heavily grazed by the ewes.
Samples from the necropsy were collected and sent to Laboratory Services at Elizabeth Macarthur Agriculture Institute (EMAI).
The blood lead level and the arsenic level of the fresh kidney returned normal values (Table 1).
Table 1: Blood lead and kidney arsenic results.
|Sample||Normal reference value|
|Blood Pb level (umol/L)||< 0.1||< 0.24|
|Kidney arsenic level (mg/kg wet wt.)||< 0.5||< 1.0|
The serum biochemistry profile (Table 2) revealed elevations in GGT, AST, CK, urea, creatinine, protein, albumin, beta-hydroxybutyrate, magnesium, haptoglobin and serum haemoglobin. The haematology profile (Table 3) revealed elevations in PCV, RBC, HB, and MCH, as well as a low level of lymphocytes. The findings in the biochemistry and haematology profiles were consistent with dehydration, recumbency, decreased feed intake and inflammation. The azotaemia seen on the biochemistry profile could also suggest dehydration, however the urea was markedly high suggesting a possible renal cause or possible contribution by upper gastrointestinal bleeding.
Table 2: Serum biochemistry profile
|Sample||Normal reference values|
|GGT (u/L)||108||0 - 55|
|GLDH (u/L)||17||0 - 30|
|AST (u/L)||267||0 - 130|
|BIL (umol/L)||2.3||0 - 6.8|
|CK (u/L)||1519||0 - 300|
|UREA (mmol/L)||112||2.9 - 7.1|
|CREAT (umol/L)||521||0 - 265|
|PHOS (mmol/L)||2.04||1.13 - 2.58|
|UREA/CREA||0.21||0 - 0.07|
|PROTEIN (g/L)||85.2||55 - 80|
|ALBUMIN (g/L)||32.2||26 - 36|
|GLOB (g/L)||49||30 - 57|
|ALB/GLOB||0.7||0.5 - 1.1|
|BHB (mmol/L)||1.23||0 - 0.8|
|Ca (mmol/L)||2.72||2.12 - 2.87|
|Mg (mmol/L)||2.0||0.74 - 1.44|
|Hapto (g/L)||2.74||0 - 0.3|
|Serum HB (g/dL)||1.03||0 - 0.2|
Table 3: Haematology profile
|Sample||Normal reference values|
|PCV (%)||57||27 - 45|
|RBC (10^12/L)||15.98||9 - 15|
|HB (g/dL)||20.2||8 - 6|
|MCV (fL)||36||28 - 40|
|MCHC (g/dL)||35||31 - 38|
|MCH (pg)||13||8 - 12|
|WBC (10^9/L)||4.6||4 - 12|
|Band N. (10^9/L)||0||0 - 0.5|
|Neutro. (10^9/L)||2.94||0.7 - 6.0|
|Lympho. (10^9/L)||1.56||2 - 9|
|Mono. (10^9/L)||0.09||0 - 0.75|
|Eosino. (10^9/L)||0||0 - 1|
|Baso. (10^9/L)||0||0 - 0.3|
Histology of the gastrointestinal organs revealed acute, moderate mucosal haemorrhage of the abomasum; mild to moderate, multifocal, lymphoplasmacytic intestinal enteritis with cryptitis; and mild, acute multifocal mucosal haemorrhage with mild cryptitis of the ileum/caecum. Histology of the heart revealed mild to moderate, multifocal, subacute myocardial degeneration and necrosis with fibroplasia.
Although no obvious lead or arsenic sources were identified in the house yard, it was considered important to rule out lead and arsenic toxicity as the mass mortality followed access to a yard containing rubbish. It was also imperative to rule out these potential diagnoses from a chemical residue and food biosecurity perspective.
A sample of the plant (Figure 2) from the house yard was collected at a later date when the foliage had regrown and was sent to the Australian Institute of Botanical Science to confirm the identification of the plant and subsequent diagnosis of sudden death in this case. The plant sample was identified as possibly C. orbiculata. However, the distinguishing features of C. orbiculata, such as reddish to pale leaf margins and leaves covered in a white powdery bloom, were not seen as the sample began to decay slightly during shipping to the laboratory.
C. orbiculata is a common garden plant that is known to contain cardiac glycosides. Cardiac glycosides can occur in plants as either cardenolides or bufadienolides, the latter of which is presumed to be found in C. orbiculata.1
Cardiac glycosides generally affect the heart, but the gastrointestinal tract, lungs, and kidneys can also be affected, either directly from the toxic principle or as a result of damage to the heart. Cardiac glycosides are inhibitors of the sodium-potassium ATPase pump, which is responsible for maintaining membrane ion concentrations and the membrane potential for cardiac muscle fibres.2 In acute poisoning, death usually occurs within a few hours of ingesting the plant2, and in most cases, heart failure is the underlying cause of death.1 Some cases, however, may live a few days and have scattered foci of myocardial necrosis.2 In these cases diagnosis is usually based on access to the plant, the observed clinical syndrome and the presence of recognisable plant parts in the ingesta.2 Clinical signs of cardiac glycoside toxicity are often delayed and include diarrhoea usually containing blood, cardiac rhythm and rate disturbances, abdominal pain, dyspnoea, neuromuscular signs, and sudden death.1,2
Plants that contain cardiac glycosides of either the cardenolide or bufadienolide types have a worldwide distribution. Common plants known to contain cardiac glycosides include Nerium oleander (oleander), Cascabela thevetia (yellow oleander), Digitalis purpurea (foxglove), Bryophyllum spp.(mother of millions).1 While there are reports of cardiac glycoside toxicity in livestock associated with the consumption of either oleander3 or mother of millions,4,5,7 there have been no confirmed poisoning cases in Australia associated with C. orbiculata and the degree of danger due to toxicity is reported as low.1 Despite this reporting, given the grazing of pig’s ear plant, the necropsy/laboratory findings seen in this case, and the exclusion of lead and arsenic toxicity as differential diagnoses, the sudden death reported in this case is suspected to have been due to cardiac glycoside toxicity.
Treatment for cardiac glycoside toxicity is generally targeted at preventing further absorption via oral administration of activated charcoal, rehydration and electrolyte replacement therapy, and arrhythmic drugs such as atropine to support the heart.1 Treatment efficacy, however, has been reported to be poorly defined and is often variable.6 Early therapeutic invention is critical for a positive outcome and therapeutic measures for the treatment of cardiac glycoside toxicity are costly in regard to both materials and time, in most cases making treatment only practicable in humans or valuable animals.1 Furthermore, in most cases, the stress of yarding stock for treatment for cardiac glycoside toxicity can result in a greater number of deaths due to stress-induced cardiac arrest.7
Treatment was not provided in this case and management was aimed at rest and limiting stress to the flock in an effort to prevent further deaths. It has been anecdotally reported in cases of cardiac glycoside toxicity due to ingestion of mother of millions (Kalanchoe delagoensis) that deaths can occur for up to around three weeks following ingestion of the toxic plant.7 In this instance, the producer reported that the deaths stopped around three to four weeks following removal of the ewes from the house yard and access to the pig’s ear.
Thank you to the Laboratory Services team at EMAI and The Australian Institute of Botanical Science for their work and assistance with this case.