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This article was published in 1987
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Clover Associated Photosensitisation

S.J. WHITTAKER, Veterinary Inspector, Narrandera

During the Spring of 1985 severe and extensive photosensitive effects were observed in a number of Riverina sheep flocks that had been grazing heavy stands of a clover, known as Shaftal clover, that had been recently introduced and promoted to local, irrigated, rice farms as an alternative winter pasture to sub clover.

In a number of cases secondary dermatophilosis was found to be an important complication to the primary photosensitisation problem.

A small number of affected lambs were also noted as displaying a most peculiar sudden and intermittent dipping and lowering of the lower back and hindquarters.

SHAFTAL CLOVER. (Trifolium resupinatum). - Also known as Persian clover, Shaftal is an erect growing, annual clover which has been offered to Riverina rice farmers as an alternative to sub clovers for use in short rotations between rice crops.

It can also be used as a suitable replacement for oats to provide autumn/winter feed, and can be cut for high quality hay.

Shaftal's main advantages over sub clovers are that it is:

1. More resistant to waterlogging.

2. More resistant to root rot.

3. Gives higher winter feed production than sub clover, which when coupled with a longer growing season can extend feed availability to spring - ideal for finishing lambs.

4. It is also quite frost and drought tolerant.

Unfortunately however, Shaftal clover also has a few drawbacks, viz.: susceptibility to rust problems, and poor seed regenerative ability (it has no hard seed like sub clover) which results in the need to resow each year.

The other dark cloud on the horizon for Shaftal clover would seem to be the potential to cause photosensitisation problems in grazing sheep.

CASE HISTORIES.

CASE ONE. Approximately 75% ex 370, 3 mth. old X/B lambs and 25% ex 500 mixed age Corriedale and Crossbred ewes which were grazing irrigated Shaftal clover, were found to be showing clinical signs typical of a primary form of photosensitisation.

GRAZING HISTORY - The 500 ewes had been turned onto what the District Agronomist had described as 'the best pure stand of Shaftal in the district' just prior to the commencement of lambing. The ewes were carrying 8 months wool at the time and had grazed a sub clover and rye paddock during the previous month.

CLINICAL HISTORY - Approximately 20% ex 370 lambs showed signs of severe photosensitive damage viz.: swollen, oedematous and drooping ears - many of which subsequently sloughed off; hard and thickened facial skin; inflamed eyelids which were often adhered together by serous exudate; inflamed and thickened skin along the backline which was usually accompanied by wool loss, and in many cases, evidence of secondary bacterial infection under older scabby lesions along the backline, was obvious. Of these more severely affected lambs approximately 20-25 either died or were destroyed - mainly those with extensive secondary dermatophilosis, many of which had become flyblown.

A further 50% of the lambs showed a range of photosensitive symptoms, down to those with only slightly swollen ears.

At no stage of the investigation was jaundice ever observed as a clinical feature of this condition, and apart from those lambs which succumbed to secondary bacterial infections and flystrike, very little to no weight loss was noticed amongst the affected group.

The majority of affected lambs however, experienced only very limited wool regrowth along the damaged backline area, and this fact coupled with the absence of ears in most cases, made for a particularly peculiar looking beast which attracted some discrimination at the market place, despite the majority being in good to prime condition.

In an interesting clinical aside to the skin problems some 9-10 lambs developed a most peculiar intermittent hindlimb and lumbar paresis. The syndrome was most evident as affected lambs commenced to rise and/or move away, and involved a sudden dipping movement of the lower back and similarly sudden lowering of the hindquarters. The hind limb weakness appeared symmetrical and there was no apparent ataxia. In each instance where a lamb so affected was able to be examined both prior evidence of photosensitisation and current dermatophilosis were consistent findings.

Of the 500 ewes some 25% showed generally less severe signs of photosensitisation than those seen in the lambs. Symptoms were mainly confined to the face and ears with swollen ears the most common finding - only 10-12 ewes experienced actual sloughing of the ears. As expected with ewes in near full wool no photosensitive effects were observed along the backline and interestingly no ewes were found to be affected by dermatophilosis. No deaths occurred amongst the ewe flock and none were seen to exhibit any symptoms of the posterior paresis syndrome which was observed in some of the affected lambs.

LABORATORY FINDINGS:

POST-MORTEM - apart from the obvious external findings previously described post-mortem failed to reveal any gross pathological changes of any significance. Superficial lymph nodes were obviously enlarged but no hepatic abnormalities were evident.

HISTOPATHOLOGY (lamb with severe photosensitisation and secondary skin infection).

Liver - mild non suppurative cholangiohepatitis.

Kidney - fine, brown pigment granules in tubular epithelial cells.

Skin - coagulative necrosis and haemorrhage in dermis with evidence of an earlier severe non suppurative dermatitis. Dermatophilus organisms were present in the epithelium. Also an extensive chronic, active inflammation in the underlying hypodermis and muscle layer.

BIOCHEMISTRY - serum enzyme levels on sera taken from 4 similarly affected lambs was as follows:

γ G.T. - 17 to 37 U/L.

S.G.O.T. - 25 to 61 U/L.

Two lambs affected with the 'posterior paresis syndrome' were also forwarded to the R.V.L. for observation and further examination.

Neither lamb showed any change in the neuromuscular signs previously described, during 2 weeks of observation, and as both lambs were suffering increasingly from dermatophilosis and body strike problems one lamb was treated with 'Streptopen' (dihydrostreptomycin and procaine penicillin) and an appropriate insecticide and the other was euthanased.

Histopathology of the skin, liver and kidney on this second lamb was as described earlier. In addition examination was also carried out on the following lines:

Brain and Cord - N.S.F.

Sciatic and femoral nerves - N.S.F.

Muscles - semimembranosus - focal fibre degeneration and macrophage infiltration.

Muscles - quadriceps - as above and focal fibre eosinophilia.

Muscles - sublumbar m.m.'s - hyaline degeneration affecting up to 20% of muscle fibres (depending on the muscle).

Following treatment the remaining lamb recovered fully with no further occurrence of the paresis syndrome!

CASE TWO.

Approximately 50% ex 160, 4-5 mth. old Crossbred lambs and 20% ex 400 first cross ewes showed variable signs of photosensitisation following introduction to the same paddock of Shaftal clover that those ewes and lambs in Case One had grazed upon.

GRAZING HISTORY - Despite warnings to the contrary, the owner of the sheep in Case Two, being desperate for agistment, moved 290 4-5 mth. old lambs and the 400 ewes onto the same paddock of Shaftal clover that was associated with the problems mentioned in Case One. The paddock concerned still provided abundant grazing from Shaftal clover and the agisted sheep moved into this paddock immediately those referred to in Case One had been removed.

CLINICAL HISTORY - early signs of photosensitisation viz.: swollen and drooping ears, were observed within 4 days of introduction to the Shaftal clover paddock. As an increasing number of both lambs and ewes were obviously becoming affected the sheep were removed from the Shaftal clover paddock, some 10 days after their introduction, and 130 lambs immediately drafted off and sold.

No indication of the incidence of photosensitisation amongst those lambs which were sold after the initial draft could be accurately ascertained.

Following removal from the Shaftal clover paddock, the whole range of photosensitive signs recorded in Case One, became increasingly apparent - particularly amongst the remaining lambs.

LAMBS - approximately 50% ex 160 remaining lambs showed some evidence of photosensitive injury, and while signs were more frequently confined to the face and ears (again ear sloughing was a common feature) approximately 208 ex affected lambs also suffered damage to the backline. These latter cases were characterised by an initial parting of the wool along the midline of the back. Closer examination of these cases revealed erythema and reddening of the skin along the backline which progressed to variable thickening, hardening and scarring of the skin in this area.

An associated loss of wool also occurred over the affected area of the back and wool regrowth in this area, particularly in the more severely scarred cases, was only very limited.

Unlike Case One secondary bacterial infections, including dermatophilosis were not commonly noticed.

Neither were any lambs (or ewes) seen to be affected by the 'posterior paresis' syndrome recorded on Case One.

Again jaundice was not noted as a clinical feature and general body condition of the lambs remained relatively unaffected throughout.

EWES - carrying 7-8 mths. wool at the time of introduction to the Shaftal clover.

Approximately 20% ex 400 ewes showed basically only moderate to mild signs of photosensitisation. Only 2-3 ewes were severely enough affected to have suffered ear sloughing and no backline lesions, nor deaths were recorded amongst the ewe flock.

CASE THREE.

The owner in this instance reported that following the introduction to a pure stand of Shaftal clover, approximately 10% of 450, 3-4 mth. old X/B lambs were found to be similarly affected to those lambs in the previous cases.

He reported seeing swollen, droopy ears within a few days of introduction to the paddock, closely followed by 'sunburning' along the backline and wool loss from the back about 14 days post introduction. These sheep were removed from the paddock at this stage and when examined some two months later, ear sloughing and nil to variable regrowth, as described in previous cases with backline damage, were the only symptoms of earlier problems still in evidence.

Again no loss of condition or signs of 'posterior paresis' were reported.

The owner also recalled 2-3 ex 600 ewes which had grazed the same paddock, as having swollen, droopy ears, but no other problems were noted.

OTHER CASES.

A number of other similar instances of photosensitisation amongst sheep grazing Shaftal clover were either reported and/or investigated during the Spring of 1985.

In most cases the incidence was less than 5% of the mob and in many only 3-4 affected lambs were involved.

These affected lambs became a local talking point and were well known as 'the sheep without ears', but apart from being the source of some owner embarrassment as the butt of saleyard jokes, and considerable buyer resistance, most affected lambs appeared to suffer very little loss of condition and proved to be cheap mutton for the local butchers.

SHAFTAL CLOVER GRAZING TRIAL.

Clinical examination of sheep which had suffered from photosensitisation whilst grazing Shaftal clover, along with random enzymology and histopathology from affected cases had all indicated the photosensitive damage to be of the primary form.

In order to more closely observe the development of photosensitive signs and effects and to monitor for any evidence of liver damage amongst lambs grazing Shaftal clover, a small trial was conducted.

METHOD:

In late Winter, 1986, 500 first cross woolly ewes and 500, 2-3, mth. old fat lambs were introduced to an irrigated paddock of Shaftal clover and sub clover.

Sheep were monitored over a two month period at approximately two weekly intervals for any sign of photosensitisation and ten lambs which were randomly selected and permanently identified were bled for serum enzymology at each of these fortnightly inspections.

RESULTS:

No signs of photosensitisation were seen at any stage of the trial.

A survey of enzymology results giving mean results for the ten lambs sampled, and standard deviations, in units/litre is as follows:

Date 26.7.86 7.8.86 20.8.86 18.9.86
Gamma glutathione transaminase 30.3 ± 6.2 30.7 ± 6.0 26.4 ± 3.5 27.0 ± 3.3
S.G.O.T. 38.1 ± 12.3 35.9 ± 5.0 43.1 ± 6.3 43.0 ± 7.8

COMMENT:

No significant change in serum enzyme levels was observed.

DISCUSSION.

The aetiology of photosensitisation is rather complex.

The primary form of photosensitisation due to the ingestion of exogenous photodynamic agents usually occurs when the plant is in the lush green stage and is growing rapidly. Stock are affected within 4 + days of going onto the pasture and new cases cease to appear soon after the animals are removed. It most cases the plant responsible must be eaten in large amounts and will therefore usually be found to be dominant inhabitant of the pasture. Plants which contain photosensitising substances include St. John's wort (Hypericum perforatum), wild carrot (Cynopterus watsoni), buckwheat (Polygonum fagopyrum) and the aphids which infest trefoil (Medicago denticulata).

The hepatogenous form of photosensitisation which results from the abnormal tissue accumulation of otherwise normal metabolic products, because of faulty excretion through the liver, has been recorded as being associated with many plants and weeds including Panicum spp., Caltrops (Tribulus terrestris), Lantana camara, Lupins and heliotrope.

Photosensitive dermatitis has also been observed in association with the ingestion of other plants such as Brassica spp., kale, lucerne,etc., where the aetiology viz. primary or hepatogenous, has not been definitely ascertained.

Many clinical cases of severe photosensitive dermatitis have also been observed in both cattle and sheep simply grazing green pasture, without the cause being identified.

Although primary photosensitisation whilst grazing any form of clover is a relatively uncommon occurrence, it would seem reasonable to assume from the cases encountered during the Spring of 1985, that Shaftal clover was at least responsible for the photosensitive affects seen about the head and face of those sheep grazing upon it. The agisted sheep mentioned in Case Two, which were forced onto the Shaftal clover and developed photosensitive symptoms within four days of introduction to the paddock, provides sound, almost trial-like evidence for assuming this point of view.

In all cases investigated during Spring '85, affected sheep had grazed very pure stands of Shaftal clover, and there was very little else by way of weeds and/or other plants which the stock could have eaten. Neither had problem paddocks been sprayed with any unusual pesticides or herbicides.

As all recorded cases occurred on rice farms where there was inevitably few to no trees in the paddocks concerned, shade seeking behaviour by affected sheep was not possible and this could have been a contributing factor to the very early appearance of clinical signs.

It would seem the type of photosensitivity observed in sheep grazing Shaftal clover, whilst most likely to be of the primary form, must remain of uncertain aetiology.

However, on no occasion was jaundice ever observed as a clinical feature in photosensitisation affected sheep; nor did serum enzyme levels used to indicate liver damage reach levels which would have been consistent with significant hepatocellular dysfunction or cholestasis; nor did liver histopathology indicate any such similar problem.

As regards the backline lesions seen in many affected sheep it is difficult to rationalise the role that Shaftal clover has played. In some cases it would seem that skin damaged by the photosensitive effects of grazing Shaftal, has succumbed to secondary invasion by Dermatophilus congolensis, whilst in others the simple physical wetting effect of lush pasture may have created conditions ideally suited to the development of a primary dermatophilosis.

In a similar incident, Allworth et al. record the occurrence of dermatophilosis and some photosensitive lesions amongst 5 month old lambs that had been grazing Brassica crops (rape) during a particularly wet N.Z. summer.

Allworth et al. concluded that wetness (rainfall per se) was not the only factor involved in the dermatophilosis outbreaks that they investigated, as on each farm where the dermatophilosis problem occurred, lambs which were managed similarly to the affected mobs, but were not placed on Brassica spp. crops, were not affected by dermatophilosis.

They postulated that the influence of the Brassica spp. crops on the occurrence of dermatophilosis could be explained by one of two means. Firstly that 'rape scald' may have predisposed the sheep to dermatophilosis. 'Rape scald' is a photosensitisation of uncertain aetiology which results in inflammation and necrotising skin lesions, and ear sloughing was observed amongst dermatophilosis affected sheep on at least one ex four farms involved.

Secondly, the crop may have maintained a high moisture level and in tall, lush crops such as rape and Shaftal clover, this may have resulted in prolonged wetting and maceration of the lambs' skin.

In the same investigation Allworth et al. also report on seeing a sudden crouching movement in a small proportion of dermatophilosis affected lambs. The movement was involuntary and from all descriptions identical to that seen amongst the lambs grazing Shaftal clover.

It is also interesting and perhaps significant that one such affected lamb that had grazed Shaftal, when treated with Streptopen for dermatophilosis completely recovered from the 'posterior paresis' syndrome.

As to the explanation for this peculiar paresis, Allworth et al. came to a similar conclusion, in that they also believed sensory nerve endings in the lumbar region of some affected lambs, were being excessively stimulated by an inflamed and thickened epidermis, which resulted in the involuntary crouching movements seen during the course of both investigations.

In conclusion the photosensitive/dermatophilosis effects associated with grazing Shaftal clover during the Spring of 1985 modified both agronomic recommendations and farmer acceptance of this clover as a pasture species to such an extent, that the management of the trial to monitor these effects in 1986, could at best be conducted on a pasture where Shaftal clover provided only 50% of the available grazing.

Where offered as mixed and balanced pasture none of the photosensitive effects listed in this paper have been recorded in sheep grazing Shaftal clover.

ACKNOWLEDGEMENTS.

I would like to thank Mr. Richard Whittington of the Regional Veterinary Laboratory at Wagga for his assistance in the investigation of this condition.

REFERENCES.

  1. Allworth, West & Bruere - Ovine Dermatophilosis in young sheep associated with the grazing of Brassica spp. crops'. N.Z. Vet. Journal 33 : 210 - 212
  2. Blood & Henderson - 'Veterinary Medicine' - Third Edit. 244 - 246 & 413 - 415
  3. Edwards, J. - Dispelling some myths about 'Dermo'. Journal of Agriculture, W.A. No. 2 : 62 - 64
  4. Hungerford, T.G. - 'Diseases of Livestock'. Eighth Edit. 72 - 82
  5. Reed, K. - Persian Clover in Victoria. Field Day Notes
  6. Hedditch, M. - Shaftal Clover. Field Day Notes

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