Primary photosensitisation occurs in sheep following the direct ingestion or absorption of a photodynamic agent.1 A range of plants that have been implicated including Hypericum perforatum (St John's wort) and Polygonum fagopyrum (buckwheat).1,2 More recent studies have also reported that Biserrula pelecinus (biserrula) can cause primary photosensitisation in sheep.3,4
From December 2019 to February 2020, five properties in the NSW Central Tablelands Local Land Services region reported photosensitisation in young sheep grazing dryland lucerne (Medicago sativa).
Lucerne is a perennial pasture legume that is commonly used in NSW for year-round grazing of livestock in addition to being cut for hay.5 The exact role that lucerne plays in the occurrence of photosensitisation has remained unclear despite several reported cases implicating the legume in the development of the disease.2,6
During the summer of 2019-2020, we received reports of acute onset of facial lesions and swellings in sheep from five separate properties in the Central Tablelands of NSW.
All affected flocks were crossbred or British breed weaned lambs. Flock 1 were Border Leicesters, Flock 2 were first-cross wethers, Flock 3 were composites and Flocks 4 and 5 were second cross lambs. Mob sizes ranged from 43 to 325 head, with one property having two mobs affected, whilst the remaining four properties only had one mob affected. The flock prevalence ranged from 12% (Flock 5) to 100% (Flock 4).
All affected flocks had been grazing dryland lucerne prior to the onset of clinical signs. The lucerne crops ranged from immature to six-year-old plants, with some mobs grazing short lush crops, whilst others had been eating dry, drought-affected lucerne. Flock 3 was grazing a native grass pasture; however, some sheep had inadvertently gained access to a neighbouring lucerne paddock. The pastures grazed by Flock 4 contained both Panicum effusum (hairy panic) and Chondrilla juncea (skeleton weed) in addition to lucerne. They were also being supplementary fed oaten hay that was also fed to other, unaffected mobs on the property.
The onset of facial lesions varied between the different affected mobs on each property, with three mobs affected within 3-5 days of being moved into the lucerne paddocks. Conversely, on Properties 4 and 5, affected mobs had been grazing dry lucerne for 4-6 weeks prior to the onset of clinical signs. Both properties received rain in the leadup to the development of facial lesions.
Sheep from properties 1, 3, 4, and 5 were examined. All affected sheep displayed similar clinical signs, despite the differences in breed and geographical location. Affected sheep had mild to marked swelling of the face, especially around eyes, nose, ears and submandibular regions. More severely affected sheep had ulcerative, crusting lesions on the ears. In some cases, these lesions produced a yellow exudate. All sheep that were examined were bright and alert, with no signs of systemic illness or evidence of jaundice.
In some cases, the lucerne paddocks were inspected for aphids and in some cases the owners were asked if they were aware of aphid infestations on their lucerne crops. There was no evidence of aphid infestation.
Despite the high prevalence of disease in some flocks, no deaths were reported.
Blood samples were collected for biochemistry to assist in determining the nature and prognosis of the photosensitisation.
On four properties (Flocks 1, 3, 4 and 5), 2-4 clinically affected sheep were blood sampled. Sheep from Flock 1 had biochemical evidence of hepatocellular (elevated GLDH levels) and biliary damage (elevated GGT levels). There was little to no evidence of hepatocellular or biliary damage in Flocks 3-5 (Table 1).
|Flock||Samples||GGT range and mean||GGT Normal U/L||GLDH range and mean||GLDH Normal U/L||AST range and mean||AST Normal U/L||Bilirubin range and mean||Bilirubin Normal umol/L|
|1||2||61-76 (68.5)||0-55||24-78 (51)||0-30||103-111 (107)||0-130||2.8-3.3 (3.05)||0.0-6.8|
|3||4||35-60 (45.5)||20-52||2.3-4.5 (4.0)||<20||109-176 (150)||60-280||3.0-5.0 (4.0)||1.71-8.55|
|4||3||30-59 (40)||0-55||4-13 (7)||0-30||78-107 (94)||0-130||4.2-5.6 (4.0)||0.0-6.8|
|5||3||19-45 (28)||20-52||2.4-7.6 (4.1)||<20||116-140 (124)||60-280||3.0-4.0 (3.3)||1.71-8.55|
Following examination and sample collection, sheep that were still grazing lucerne paddocks were moved to alternate, more shaded pastures or sheds.
All properties reported that lesions resolved in the days to weeks following removal from lucerne, with most affected sheep making a full recovery.
To distinguish between primary or secondary photosensitisation, biochemical blood analysis was performed on a sample of affected sheep in four of the five affected flocks. The sheep from Flock 2 were not examined or blood tested, the observations being collected by phone from the experienced stock owner.
In sheep, GGT and GLDH are sensitive markers for cholestasis and hepatocellular damage, respectively.8,9 Therefore the mild to moderate elevations in both GGT and GLDH indicate hepatocellular injury and cholestasis in Flock 1 (Table 1). This result was unexpected given that the sheep examined in this flock were bright and alert, with pink (and not icteric) mucus membranes and only mildly swollen ears.8 The sheep from this mob had no known access to potentially hepatotoxic plants unlike sheep from Flocks 3 and 4 that could potentially have grazed hepatotoxic plants.
There were no significantly elevated liver or biliary parameters in samples collected from Flocks 3,4 and 5. The similar clinical presentation of all five flocks suggest that photosensitisation associated with grazing lucerne is more common amongst juvenile sheep, regardless of breed or sex. However, these cases occurred towards the end of a prolonged drought when grazing lucerne would most likely be used to grow young sheep.
Several other studies have evaluated the role lucerne plays in the development of photosensitisation in sheep. One study found that the presence of Coccinella septempunctata (seven-spot ladybird) larvae on lucerne can contribute to the development of primary sensitisation. Another study that evaluated the onset of photosensitisation in sheep grazing biserrula found that no photosensitisation occurred in the sheep grazing a mixed lucerne pasture.3 A study investigating cases of secondary photosensitisation in juvenile sheep found that the sheep were grazing a pasture of lucerne with marked infiltration of heliotrope. Sheep were removed from pasture until the heliotrope had perished. The sheep were returned to the lucerne pasture with no further cases of photosensitisation, suggesting that lucerne was unlikely to be the main cause of the photosensitisation, but may play a role when a hepatotoxic plant is cograzed.14
Cattle have also been found to be susceptible to both primary and secondary photosensitisation, associated with flood-affected, mouldy or even high-quality lucerne hay and silage.12,13
Photosensitisation is usually rare, sporadic and reversible in sheep grazing lucerne so preventative measures are usually not undertaken. Intermittent grazing of both hay and alternate pastures may be warranted in some situations.14
This study supports the view that lucerne can cause primary rather than secondary photosensitisation in sheep. While sheep in Flock 1 had biochemical evidence of mild hepatocellular and biliary damage, none of the sheep in the study were dull or icteric and no deaths were reported. This is contrary to our observations on sheep suffering from secondary photosensitisation after grazing weeds such as Panicum spp and Tribulus terrestris. In addition to swollen faces and ears, these sheep are usually dull, listless, markedly icteric and a proportion may die.