Introduction

Onion (Allium cepa) toxicosis in animals is characterized by haemolytic anaemia accompanied by the formation of Heinz bodies in erythrocytes (Desnoyers 2000) and has been reported in cattle (Hutchison 1977; Verhoeff et al. 1985; Carbery 1999; Rae 1999; Van Der Kolk 2000), horses (Thorp and Harshfielf 1939), dogs (Stallbaumer 1981; Solter and Scott 1987) and cats (Kobayashi 1981). It is generally accepted that sheep and goats are more resistant to onion toxicosis than other domestic animals (Thrall 2004).

The toxic components in all type of onions are aliphatic sulfides, specifically allyl and propyl di-, tri-, and tetrasulfides, with the allyl compounds being more potent than the propyl. The toxin reduces the activity of glucose-6-phosphate dehydrogenase in red blood cells; thereby interfering with regeneration of reduced glutathione needed to prevent oxidative denaturation of haemoglobin (Thrall 2004). Denaturated haemoglobin, when developed, precipitates on the surface of red blood cells (named Heinz bodies) and triggers intra- and extravascular haemolysis (Lincoln et al. 1992).

Case report

In early January 2005, 2 pregnant ewes of local breed from a flock of 70 ewes and 50 young lambs in Mashhad suburb showed signs of illness such as weakness and poor appetite. The two animals were routinely treated by a local veterinarian and died without any improvement. At post mortem examination of one of the ewes, there was onion odour detected in the forestomach contents. The kidneys were larger than normal size and of a dark-brown colour with obvious distinction between medulla and cortex. Tissue samples from liver and kidneys were taken and processed for routine histopathology.

The history showed that the flock has grazed daily on onion leaves from December 1, 2004 and were fed at night with a ration containing barley, sugar beat pulp and wheat straw. It was also noted that, within the last 10 days, four ewes had aborted near-term foetuses. Examination of the flock revealed more cases with signs of depression, weakness and moderately pale mucous membranes. Body temperatures were normal but heart and respiratory rates were elevated. There was strong onion smell in the breath of these animals. Blood samples were taken from 12 ewes, into EDTA containing tubes, and haematology revealed low levels of PCV, haemoglobin and erythrocyte numbers, mild leukocytosis and different degrees of basophilic stippling and polychromasia (Table 1). The PCV range was 17–26.8%. Vital staining of blood smears revealed Heinz bodies in erythrocytes of all samples with reticulocytosis present in some (Fig. 1).

Table 1 Results of Haematological examination of 12 ewes intoxicated with onion (Mean ± SD)
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Fig. 1
figure 1

Blood smear of an onion-intoxicated ewe showing widespread Heinz bodies in erythrocytes (Vital staining-1,000×)

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Histopathological examination of haematoxylin and eosin-stained tissue sections of kidneys revealed extensive tubular necrosis with accumulation of yellowish-brown haemosiderin pigment in the epithelial cells of renal tubules and intratubular eosinophilic casts of haemoglobin. There was hyperaemia, centrilobular hepatocellular necrosis, bile duct hyperplasia and mild infiltration of mononuclear inflammatory cells in the liver.

Diagnosis of onion toxicosis was made based on history and Heinz body detection in erythrocytes. Onion grazing was discontinued and the animals were treated with haematinics. Fifty days after discontinuing of onion feeding no death or abortion was reported in the flock.

Discussion

Although the feeding of domestic onion appears to be safe in sheep, the present report shows that unlimited access to onion feed leads to considerable haematological pathology. Ewes that had fed on onion for 1 month showed approximately 25% reduction in PCV in comparison to normal values. This is in agreement with the results of experimental feeding of onions to sheep (Kirk and Buugin 1979). However, in contrast to the reports of Kirk and Buugin (1979), we observed clinical signs of weakness, depression and poor appetite in intoxicated animals leading to death in two animals and abortion in a significant proportion of the flock. Histopathology of one ewe also revealed lesions related to haemolytic crisis due to onion consumption. The stress of pregnancy and cold-windy weather may exacerbated the toxic effects of onion.

Among domestic animals, cattle are more susceptible than dogs, horses, sheep and goats to onion toxicosis. However cats are more susceptible to develop Heinz body than other species so that onions that are cooked, raw or dehydrated can be toxic and result in haemolytic crisis. Dogs appear to vary considerably in susceptibility to onion toxicosis and the severity of anaemia varies from one individual to the next (Desnoyers 2000). The sensitivity of different animals to onion intoxication depends on the amounts of the erythrocytic pentose phosphate pathway-limiting enzyme, glucose-6-phosphate dehydrogenase (Kramer 2000). Glucose-6-phosphate dehydrogenase provides the reducing power that converts oxidized glutathion to reduced glutathion. Without reduced glutathion, hydrogen peroxide accumulates and causes oxidation of the sulfydryl groups of the globin chains, leading to the formation of precipitates—Heinz bodies. The erythrocytes that contain Heinz bodies are removed from the circulation by the reticulo-endothelial system or possibly by lysis within the circulation, leading to anaemia (Simmons 2001).

Ingestion of Brassica species by bovine and red maple (Acer rubrum) by equine can also result in Heinz body formation and haemolytic anaemia. Plants from Brassica species are rich in s-methylcystein sulfoxide, which is converted to dimethyl disulfide, a toxic compound for erythrocytes, by ruminal microorganisms. The toxin present in the leaves of red maple is unknown and causes rapid depletion of reduced glutathion in erythrocytes (Desnoyers 2000).

Experimental feeding of onion in calves has shown that 25% onion diet on the basis of dry matter (DM) is probably approaching the toxic threshold for onion consumption in cattle (Lincoln et al. 1992). Sheep can also be maintained on diets up to 50% (DM) of onion bulbs with no clinical abnormalities or detrimental effects on growth (Fredrickson et al.1995). However, when onion is considered for feeding, it is necessary to mix it in a balanced ration and animals should not be allowed free access to onion, as they may eat them preferentially (Lincoln et al. 1992).

Onion crops are grown commercially in Mashhad suburb, and during late autumn when fresh pasture is not available for sheep, onion fields are used for grazing before the harvesting of the onion bulbs. In such conditions, unlimited access of sheep to onion leaves over an extended period will not be safe and clinical and subclinical anaemia could be expected.