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CASE REPORT
An outbreak of primary photosensitisation in lambs secondary to
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consumption of Biserrula pelecinus (biserrula)
AE Kessell,a* GE Ladmorea and JC Quinna,b
Case report An outbreak of photosensitisation affecting
approximately 25% of a flock of 120 meat lambs that was graz-
ing a monoculture of the pasture legume Biserrula pelecinus
var. Casbah (biserrula) was investigated. Blood samples were
taken from sheep with moderate to severe clinical signs, and
from apparently normal animals, for a complete blood count
and biochemistry; 5 affected animals were subjected to a full
necropsy. Histopathological investigation showed lesions con-
sistent with photosensitisation of the exposed unpigmented
skin of the face and ears. No histopathological or clinical patho-
logical abnormalities suggestive of a hepatopathy were detected
in any of the cases, indicating that the lesions observed in this
flock were caused by a primary photosensitising agent present
in B. pelecinus.
Conclusion This is the first confirmation that photosensitisation
caused by ingestion of biserrula is caused by a primary
photosensitising agent.
Keywords Biserrula pelecinus; dermatitis; legumes; photosensitisation,
sheep
Abbreviations AST, aspartate aminotransferase; CK, creatine;
GLDH, glutamate dehydrogenase; GT, gamma-glutamyl transpeptidase;
PS, photosensitivity; SD, sorbitol dehydrogenase
Aust Vet J 2015;93;174–178 doi: 10.1111/avj.12318
B
iserrula pelecinus is a semi-erect, self-regenerating annual le-
gume originating from the southern Mediterranean.1 Its desir-
able characteristics include high seed production, adaptation
to a broad range of soil types, a deep root system and grazing toler-
ance, and these result in a highly productive pasture that is more
drought resistant and shows greater self-regeneration compared with
other pasture legumes.1–4 Biserrula was first developed for agricul-
tural use in Western Australia during the 1990s and varieties have
since been introduced into a number of areas of New South Wales.
Anecdotal evidence suggests that Biserrula sp., especially the ‘Casbah’
variety, has been positively received by the Australian farming
community.4–6
*Corresponding author.
a
School of Animal and Veterinary Sciences, Charles Sturt University, Nathan Cobb
Drive, Wagga Wagga, New South Wales, Australia; allan.kessell@gribbles.com.au
b
Graham Centre for Agricultural Innovation, (NSW Department of Primary Industries
and Charles Sturt University), Wagga Wagga, New South Wales, Australia
174 Australian Veterinary Journal Volume 93, No 5, May 2015
Since commercialisation of the first cultivar of Casbah in 1997, a
small but growing number of cases of photosensitivity (PS) have
anecdotally been noted in ewes and lambs grazing biserrula-
dominant pastures in spring, although the overall incidence remains
unclear.4,5,7 However, this photosensitisation has not been reported
in the scientific literature and its type or pathogenesis has not been in-
vestigated. We report an outbreak of PS in lambs on a pasture of pure
B. pelecinus var. Casbah, and record the clinicopathological and
histopathological changes that confirm a type I PS.
Case report
The disease outbreak occurred in early September 2013 on a farm
near Mirrool in the Riverina district of New South Wales in a flock
of 120 20-week-old South African Merino × Dorset lambs, born in
March/April 2013. The animals had been grazed on mixed pastures,
including B. pelecinus var. Casbar (Figure 1) from weaning, and were
moved to a monoculture pasture of B. pelecinus var. Casbah (approx-
imately 99%) 2 weeks prior to the outbreak. They were then observed
every 2–3 days, with the first clinical signs being noted after 7 days on
the pure biserrula pasture. Clinical signs included swelling (oedema)
and drooping of the ears, accompanied by a patchy alopecia in sun-
exposed skin of the face and ears in approximately 25% of the flock.
The most severely affected sheep showed variably extensive scab-
bing on the sun-exposed unpigmented skin of the ear. A total of
10 of the most severely affected animals, and 5 showing no clinical
signs (classified as ‘subclinical’), were separated from the flock for
further investigation.
Blood was collected from the jugular vein of each of the 15 clini-
cally and subclinically affected lambs and EDTA-preserved blood
and serum samples were placed on ice and transported to the lab-
oratory for a complete blood count and serum biochemical analysis
within 4 h of collection. In addition, 5 animals showing clinical
signs were transported to the Veterinary Diagnostic Laboratory at
Charles Sturt University, where they were euthanased by intra-
venous barbiturate injection for necropsy. A comprehensive range
of tissues from each animal was fixed in 10% buffered formal saline
for histological processing and examination.
Postmortem and laboratory findings
Results of the complete blood count and serum biochemistry are
shown in Table 1. Values for electrolytes, and the whole blood count
differential (data not shown) were all within normal reference
ranges, and there were no apparent difference in values recorded
from affected and unaffected animals.
© 2015 Australian Veterinary Association
 PRODUCTION ANIMALS

on the skin of the sun-exposed dorsal ear that consisted of exten-

sive crusting and ulceration. In some animals complete loss of a

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variable portion of the distal pinna was observed (Figure 2). All
other organ systems appeared normal.

Significant histopathological lesions were confined to the sun-

Figure 1. Pure pasture of Biserrula pelecinus var. Casbah.
Gross necropsy findings in the clinically affected lambs were con-
fined to the conjunctiva and pigmented skin of the face and ears,
although one lamb had an area of wool loss in the skin of the
dorsal lumbar midline and one lamb had a focal 1-cm area of ul-
ceration and bleeding in the skin of the upper eyelid, which was
suggestive of self-trauma. All clinically affected animals showed
moderate bilateral reddening of the conjunctiva and variable
epiphora, and some animals also showed mild swelling and
crusting of the hairless anterior midline portion of the muzzle.
All animals showed variable, and sometimes marked, changes
exposed unpigmented skin of the face and ears. There was a
variably severe necrotising, crusting and pustular dermatitis,
sometimes accompanied by re-epithelisation (Figures 3, 4). In
all animals the unpigmented skin of the face contained scattered
small intracornual accumulations of degenerate neutrophils, ac-
companied by a mild perivascular lymphoid infiltrate in the
superficial dermis. In the unpigmented sun-exposed skin of the
external pinna there were variably severe changes. Mildly affected
skin contained scattered intracornual pustules. These alternated
with areas in which the skin surface was variably covered by a
crust consisting of serum and neutrophils, which was either
sitting on top of, or within, the cornified epidermal layer. In more
severely affected areas there was a variable coagulative necrosis of
the epidermis and apical dermis. Necrosis often extended into the
apical one-third of the hair follicles, and was accompanied by a
similar necrosis within adnexal dermal elements, and sometimes
partial extrusion of hypereosinophilic necrotic sebaceous glands
into the follicular lumen. In the most severely affected areas, shed
necrotic epidermis and superficial dermis combined with the sero-
neutrophilic crust to form a variably thick ‘shed’ layer on top of
the dermis (Figure 4). In most animals there was a mild superficial
dermal fibroplasia, and in some, the beginnings of surface re-
epithelisation was evident.

Table 1. CBC and selected biochemical values from subclinical (sheep 1–5) and clinically affected sheep (sheep 6–15). Sheep 11–15 were necropsied

Sheep no. PCV WBC Fib TP ALB Glob BR GLDH GGT AST CK Urea Creat USG

1 0.36 6.3 4 71 40 31 3 31 44 149 714 5.7 57 ND

2 0.37 6.8 7 68 42 26 3 10 55 146 561 4.9 68 ND
3 0.39 8.7 8 74 41 33 4 6 62 149 933 7.5 65 ND
4 0.39 5.5 6 70 39 31 3 37 46 141 548 6.2 65 ND
5 0.37 7.7 9 72 37 35 3 10 58 117 1428 4.9 63 ND
6 0.34 6.4 3 68 39 29 2 10 54 119 546 5.9 52 ND
7 0.34 7.3 8 70 42 28 3 5 91 103 385 6.1 58 ND
8 0.37 8.2 9 74 40 34 3 14 63 149 1397 6.6 55 ND
9 0.36 5.1 5 73 39 34 2 14 70 163 10,007 5.2 52 ND
10 0.37 6.4 6 68 39 29 3 31 54 139 992 5.3 51 ND
11 0.38 6.1 8 70 38 32 2 28 58 201 10,489 3.7 41 1.022
12 0.34 7.8 5 71 34 37 3 68 59 112 269 6 43 1.044
13 0.35 6.4 3 73 38 35 2 8 51 129 394 5.2 46 1.04
13 0.3 6.6 8 58 18 40 3 3 68 341 574 5 50 1.014
15 0.32 8.3 3 67 38 29 2 38 77 141 589 7.3 48 1.026

Reference range 0.29–0.40 4.1–13.0 3–8 60–82 29–41 30–42 <3 μ 0–33 47–95 59–130 0–1194 5.0–11.4 44–72
L/L x 109/L g/L g/L g/L g/L mol/L U/L U/L U/L U/L mmol/L μmol/L

ALB, albumen; AST, aspartate transaminase; CK, creatine kinase; Creat, creatinine; Fib, fibrinogen; GGT, γ-glutamyltransferase; GLDH, gluta-
mate dehydrogenase; Glob, globulin; ND, not done; PCV, packed cell volume; TP, total protein; USG, urine specific gravity; WBC, white blood
cell count. Values in bold are outside the normal reference range.

© 2015 Australian Veterinary Association Australian Veterinary Journal Volume 93, No 5, May 2015 175
 PRODUCTION ANIMALS
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Figure 2. Lesions in the sun-exposed skin of the pinnae in 4 of the affected
lambs. Lambs A and B show severe crusting and desquamation; in lamb C
there is a more chronic lesion as crusts have lifted from the underlying
healing skin. Note the healed pinnae in lamb D, although the apical tip
has been lost.
Figure 3. Low-power light microscopic view of the pinna of lamb 11. A thick
crust (arrow) is sitting on top of the sun-exposed skin on the dorsal surface
of the pinna. The skin on the non-sun-exposed ventral surface is unaffected.
Note also some epithelialisation of the epidermis under the crust (H&E, x400).
Histological changes found in other tissues of both affected and sub-
clinical animals consisted of small numbers of nematodes consistent
with Ostertagia sp. within the abomasum; small numbers of coccidial
oocysts within the small intestine; small to moderate numbers of
sarcocysts scattered throughout heart and skeletal muscle; and mild,
multifocal periportal lymphocytic infiltrations in the livers. These
were all considered background lesions in lambs of this age.
176 Australian Veterinary Journal Volume 93, No 5, May 2015
Figure 4. High-power light microscopic view of the epidermal crust,
consisting of serum with large numbers of neutrophils. The adnexal ele-
ments of sebaceous glands (smaller arrows) and follicular structures (larger
arrows) within the crust are indicative of coagulative necrosis of the dermis
(H&E, x400).
Discussion
Photosensitisation in animals is defined as a severe dermatitis that re-
sults from a heightened reactivity of skin cells and associated dermal
tissues upon their exposure to long-wavelength ultraviolet light, fol-
lowing ingestion or contact with compounds that are UV or light re-
active.8–10 Following activation, these compounds initiate production
of reactive oxygen species, resulting in an oxidative stress response in
the cell, leading to degeneration and cell death.9,11,12 Typically, in the
skin this results in coagulative necrosis of epidermis, apical follicular
epithelium, adnexal elements and the superficial dermis, followed by
neutrophilic inflammation and secondary bacterial infection. Al-
though these changes may be similar to those seen in chemical or
thermal burns, in photosensitivity they are restricted to unpigmented,
poorly haired, sun-exposed areas of skin.12
There are three categories of PS: types I, II and III. Type I PS is
commonly termed ‘primary’ photosensitivity, and manifests after
the ingestion or cutaneous absorption of exogenous pre-formed pho-
todynamic agents, usually of plant origin. Type II PS is a rare congen-
ital photosensitivity secondary to abnormal porphyrin metabolism;
type III PS is commonly referred to as a ‘secondary’ or ‘hepatogenous’
PS.12
Phylloerythrin is a metabolite of chlorophyll formed by the microbial
digestion of plant material in the intestines. Like chlorophyll, it is able
to be activated by light and type III PS results when the liver fails to
absorb, metabolise and excrete phylloerythrin into bile, resulting in
its systemic deposition in tissues, including skin.9,13–15 Toxic plants
and mycotoxins that cause severe widespread liver damage account
for most cases of type III PS, and it is primarily seen in herbivores,
and is the most common type of PS seen in veterinary medicine.
Regardless of the aetiology and/or the photodynamic agent involved,
the clinical signs of photosensitisation are similar. The presence of the
skin pigment melanin blocks ultraviolet light penetration through the
© 2015 Australian Veterinary Association

epidermis to the sensitive underlying dermal layers,16 giving signifi-
cant protection from the excitation ability of the light. Thus dermal
lesions typically develop in unpigmented, lightly haired skin exposed
to sunlight.
Initial clinical signs of photosensitisation include excessive lacrima-
tion, poorly demarcated erythema and oedema of affected areas.17
Local oedema can be severe, leading to drooped pinnae, swollen eye-
lids with secondary entropian and epiphora that may progress to
blephorospasm, and oedema of the lips and muzzle. Initial signs
may include behavioural changes such as restlessness, head-shaking
and self-mutilation secondary to intense pruritus and photophobia.17
These initial observations precede fulminant stages of blisters, exuda-
tion and skin loss due to necrosis, gangrene and sloughing. Chronic
photosensitisation may result in resolution or chronic lesions such
as areas of dermal hyperpigmentation and lichenification and vari-
able loss of the distal pinnae.11
Clinical pathological changes associated with hepatogenous type III PS
reflect elevations in analytes referrable to hepatic and biliary function
and integrity. These commonly include variable, often marked increases
in hepatocellular specific enzymes (GLDH, SD), enzymes induced by
cholestasis (GGT), and other possible markers of cholestasis (e.g. biliru-
bin).9 Clinically, animals affected with type III PS are often jaundiced, in-
dicating elevations in serum bilirubin above 45 μmol/l.
Histopathological changes in the liver associated with hepatogenous PS
are well detailed in the literature, and are usually diffuse and severe, as
would be expected, but vary in type depending on the causative toxin.12
In this disease outbreak there was no significant difference in any com-
plete blood count values between clinical and subclinical animals. No
elevations in bilirubin or GGT were recorded. Two lambs (12 and 15)
showed very mild elevations in GLDH, which is considered specific for
hepatocellular necrosis in sheep, but this was not seen histologically in
any of these animals. Of the clinically affected animals, six also had mild
elevations in AST, which may be released from both damaged hepato-
cytes and muscle cells, and three of these also had elevations in the mus-
cle specific enzyme CK, suggesting muscle rather than hepatic damage.
Sections of diaphragm, heart and tongue in all necropsied animals
contained a small number of sarcocysts and a mild multifocal lympho-
cytic myositis. Additional skeletal muscle samples from the hindleg, fore-
leg and psoas muscle were examined in lamb 11 because of the marked
elevation in CK noted in the biochemical results. The only lesions found
were mild myositis associated with sarcocysts that were noted in all
necropsied lambs and this was considered a background lesion in lambs
of this age. The pattern of enzyme change was also seen in the subclinical
lambs, among which three animals showed a mild elevation in AST and
one had mild elevation in CK. These findings, along with no significant
elevation in GLDH and no histological evidence for hepatocellular
change, strongly suggest that the elevations in AST and CK in the clinical
and subclinical lambs are more consistent with muscle damage than with
hepatocellular necrosis.
Ulcerative lesions seen within the ileal mucosa of lamb 14 (strongly
suggestive of Salmonella spp. enteritis, although culture was not done)
help explain the hypoalbuminaemia seen in this lamb, which is there-
fore likely not connected to the toxicity associated with biserrula.
© 2015 Australian Veterinary Association
PRODUCTION ANIMALS
Isolated cases of PS have occurred in sheep grazing the ‘Casbah’ vari-
ety of biserrula throughout the Western Australian wheatbelt4–7 and
PRODUCTION ANIMALS
cases of biserrula PS have been noted in spring in Western Australia,
in both ewes and lambs grazing biserrula pastures.18 Observed clinical
signs and lesions on the unpigmented skin of the face, ears and tail of
the affected animals in those reports, including loss of all or parts of
the pinnae following consumption of Biserrula sp., are consistent with
PS.7,19 Anecdotal reports suggest that the plant is most toxic during
the flowering stage and has reduced or absent toxicity when dried or
ensiled.20 Anecdotal evidence also suggests there is no hepatic in-
volvement in Biserrula sp. associated PS, which if true would indicate
that this photosensitisation is type I, associated with ingestion of a
preformed plant compound, or a secondary metabolite. In support
of this hypothesis, clinical and histopathological results in this out-
break do not suggest any significant hepatopathy. Taken collectively,
these findings confirm that the photosensitivity associated with
consumption of Biserrula sp. is a type I PS.
If the photosensitising compound/s present in B. pelecinus could be
identified, selective plant breeding may be able to generate cultivars
that do not contain them, enabling safe consumption of the plant
by livestock at all stages of its growth cycle. It has also been suggested
that primary photosensitising compounds that are activated by ultra-
violet light may have potential as anticancer drugs.21,22 Further stud-
ies are required to identify the causal photosensitising compound/s
present in this important pasture legume species.
In conclusion, biserrula is a useful addition to the repertoire of self-
regenerating legumes available to farmers in the temperate regions
of southern Australia, but consumption of the plant may be associated
with a type I PS that can result in serious disease and production
losses. Close observation can detect the initial behavioural and skin
changes seen with type 1 PS and allow management strategies to pre-
vent the more severe consequences of prolonged toxic exposure. Ac-
curate identification of the toxic stage of plant growth and the
causative compound/s may allow the development of non-toxic vari-
eties and therefore encourage wider uptake of this valuable plant.
Acknowledgments
The authors thank the producer involved in this case report and the
staff of the Charles Sturt University Veterinary Diagnostic Labora-
tory. GEL was supported by a scholarship from the Australian Wool
Education Trust. AEK and JCQ are supported by Meat and Livestock
Australia.
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(Accepted for publication 2 September 2014)
© 2015 Australian Veterinary Association