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DOI: 10.1111/j.1365-3164.2009.00795.

Cutaneous periocular Habronema infection in a


dromedary camel (Camelus dromedarius)

Debbie A. Myers*, Chris D. Smith*, Ellis C. leesei, causes parasitism of the conjunctival sac and is
Greiner*, Ellen Wiedner†, Jeffrey Abbott*, seen in Africa, Russia and India. The parasite is not very
Rosanna Marsella* and Catherine Nunnery* common in the camel population, and does not cause
clinically significant disease.1
*University of Florida, College of Veterinary Medicine, Veterinary Habronema and Draschia are genera of nematodes in
Medical Teaching Hospital, PO Box 100101, Gainesville, the order Spirurida. Habronema spp. and Draschia spp.
FL 32610-0101, USA occur worldwide, and in the United States are found most

Ringling Brothers and Barnum & Bailey Center for Elephant Conser- commonly in the southeast.2 The organisms primarily
vation, Polk City, FL 33868, USA
affect equids including horses, donkeys, mules, and
Correspondence: Debbie A. Myers, University of Florida, Gainesville,
zebras, and cutaneous habronemiasis has also been iden-
FL 32610-0101, USA. E-mail: dmyersvet@yahoo.com
Sources of Funding tified in dogs.3 No species of Habronema or Draschia
This study is self-funded. have ever been documented to parasitize either new or
Conflict of Interest old world camelids.
None declared. Habronema spp. have an indirect lifecycle. The spirurid
larvae L1s hatch from eggs during passage through the
Abstract stomach of infected horses or other equids. After being
excreted in the manure, they are ingested by the interme-
A 6-year-old castrated dromedary camel (Camelus diate hosts, which are maggots of houseflies and stable
dromedarius) presented with a non-healing, severely flies. The larvae then develop concurrently with their fly
pruritic, ulcerative fibrotic plaque located at the hosts. After 2 weeks, the flies mature and carry the lar-
medial canthus. Histological examination of surgical vae – now infective L3s – to open wounds on horses or
biopsies identified degenerating nematode larvae other equids. At this point, the affected animal either
within eosinophilic granulomas. Treatment involved ingests the larvae, or develops cutaneous habronemiasis
repeated debridement of the lesion, injectable iver- (also called ‘summer sores’). In the stomach, adult
mectin and anti-inflammatory therapies, and inject- worms can cause gastritis, gastric ulceration, and colic
able and topical antibiotics. A specially constructed and some infected individuals may not develop skin
mask with goggles to prevent the camel from contin- lesions, but will present with poor hair coat, ill thrift, and
uing to self-traumatize the eye and lesion was indigestion.4
also placed. Full recovery occurred approximately Cutaneous lesions are typically non-healing and pruritic,
1 month after diagnosis. Because of the location of and are characterized by granulation tissue containing
the lesion, time of year, the gross and microscopic numerous eosinophils. In equids, common sites for infec-
characteristics of the lesion, the presence of a likely tion are the limbs, ventral aspect of the abdomen, pre-
nematode larva and the response to treatment, a puce, external genitalia in males, ocular and periocular
diagnosis of cutaneous habronemiasis was made. areas and commissure of the lips. When the L3 larvae are
Accepted 27 March 2009 deposited near the eyes, inflammation, excess lacrima-
tion, photophobia, oedema, and conjunctivitis often
ensue. Periocular habronemiasis is well documented
in horses.5–8 Diagnosis by faecal examination is often
unsuccessful because the thin-walled eggs and delicate
larva can be easily overlooked. Cutaneous habronemiasis,
Introduction
however, can generally be diagnosed by identification of
Several cutaneous parasites occur in camels including larvae in skin biopsies or scrapings.
three species of Onchocerca: Onchocerca fasciata, This case report describes a dromedary camel with clin-
O. gutturosa and O. armillatta. Ochocerca gutturosa and ical and histopathological findings compatible with cuta-
O. armillata are both accidental and rare parasites and the neous habronemiasis.
infection is usually aborted and unable to develop to
patency.1 Onchocerca fasciata is a specific and prevalent
parasite of camelids with 26% of camels infected in Saudi
Case report
Arabia. The disease is characterized by the presence of A privately owned 6-year-old, 600 kg, castrated drome-
asymptomatic nodules in the subcutaneous tissues of dary camel (Camelus dromedarius) presented for evalua-
the head and neck regions and is less common in the fas- tion in June of 2007 for severe periocular swelling,
cia of the nuchal ligament. The camel eye worm, Thelazia blepharospasm, and a purulent lesion at the medial

ª 2010 The Authors. Journal compilation ª 2010 ESVD and ACVD, Veterinary Dermatology, 21, 527–530. 527
Myers et al.

canthus of the right eye. The camel was otherwise systems. Blood samples were taken for haematology and
healthy, was pastured in southern Florida where it was serum biochemistry. Serum biochemistry was within
born and had never travelled outside the state. The camel normal limits. The complete blood count showed
was wormed monthly with an unknown amount of oral leukocytosis (23 920 ⁄ lL; reference 10 200–21 500 ⁄ lL),
equine formulation ivermectin paste. The animal had eosinophilia (1310 ⁄ lL; reference 200–1200 ⁄ lL), and
been seen previously by a veterinarian for a periocular neutrophilia (19 000 ⁄ lL; reference 3780–17 400 ⁄ lL).9,10
lesion of 2 weeks duration. A biopsy of the lesion taken Faeces were collected and rare trichostrongyle ova were
by the veterinarian showed multiple granulomas, areas of identified by faecal flotation.
patchy ulceration, and proliferative granulation tissue with An ophthalmologic examination showed mild conjuncti-
moderate eosinophilic inflammation extending from the vitis. Gram stain of the purulent exudate covering the
dermis to the subcutaneous muscle. A few coccoid lesion showed many Gram-positive and a few Gram-neg-
bacteria were seen, but no other aetiologic agent could ative rod bacteria. Samples of the exudate were also sub-
be identified. At that time, the veterinarian treated the mitted for aerobic, anaerobic, and fungal cultures.
camel with a single subcutaneous dose of ivermectin Aerobic culture, yielded scant to moderate growth of a
(0.2 mg ⁄ kg; Ivomec, Merial Limited, Duluth, GA, USA). mixed bacterial flora. No anaerobic organisms were iden-
A topical insecticide and long-acting steroid were also tified on culture and no fungal organisms were identified
administered. from fresh biopsy tissue. Fresh skin tissue was also sent
The camel did not improve after treatment and was to the University of Georgia for polymerase chain reaction
referred 2 weeks later to the University of Florida, Col- (PCR) testing for specific fungal organisms (i.e. Aspergil-
lege of Veterinary Medicine for further evaluation. On pre- lus spp., Candida albicans, Fusarium spp., Cryptococcus
sentation, there was a 1.5 · 4 cm fibrotic ulceration neoformans) and the results were also negative.
extending ventral and rostral from the medial canthus of After local anaesthesia with 2% lidocaine administrated
the right eye. The lesion was mildly proliferative with a subcutaneously as a ring block, three 5 mm punch biop-
raised rim suggestive of granulation tissue and was par- sies of the lesion were taken, placed in 10% buffered for-
tially covered by a haemorrhagic crust (Figure 1). The ani- malin, and submitted for histopathology. Histologically,
mal was observed rubbing and scratching the lesion the lesion consisted of broad ulcerations covered by mod-
repeatedly. erate to extensive granulation tissue and serocellular
For all diagnostic and therapeutic procedures, the crusts composed predominantly of degenerating eosin-
camel was sedated with xylazine (0.25 mg ⁄ kg) (Anased; ophils. The granulation tissue was infiltrated by numerous
Lloyd Incorporated, Shenandoah, IA, USA) and butor- eosinophils and fewer mast cells. Occasional small aggre-
phanol (0.1 mg ⁄ kg) (Torbugesic; Fort Dodge Animal gates of coccoid bacteria were scattered on the ulcerated
Health, Fort Dodge, IA, USA) intramuscularly and surface and trapped within the crusts. Multifocal eosino-
reversed with atipamezole intramuscularly (0.005 mg ⁄ kg) philic granulomas were distributed in the mid to deep der-
(Antisedan; ZooPharm, Fort Collins, CO, USA). mis often underlying the granulation tissue (Figure 2). The
On initial physical examination, no abnormalities were inflammatory infiltrate was centred on ovoid cross sec-
seen with the exception of the integument and ocular tions of larvae with a cuticle and lack of internal structures
(Figure 3). The larvae ranged in size from 45 to 52 lm in
diameter. This size and the presence of a cuticle sug-
gested nematode larvae. Calcareus corpuscles seen with
cestode larvae were not present. Chitin seen with arthro-
pods was not noted histologically. The round body in

Figure 1. A dromedary camel (Camelus dromedarius) with a


1.5 · 4 cm fibrotic and ulcerated lesion extending ventral and rostral Figure 2. Photomicrograph of dromedary camel (Camelus dromeda-
from the medial canthus of the right eye is shown. The lesion was rius) skin. Note the broad ulceration, cellular crust, granulation tissue,
mildly proliferative with a raised rim, suggestive of granulation tissue, and eosinophilic granulomas in the underlying dermis. Haematoxylin
and was partially covered by a haemorrhagic crust. and eosin.

528 ª 2010 The Authors. Journal compilation ª 2010 ESVD and ACVD, Veterinary Dermatology, 21, 527–530.
Cutaneous habronemiasis in a camel

PCR has been published for the diagnosis of equine


habronemiasis and would have helped in the identification
of the larvae in this case; however, the size of the larvae
and the presence of cuticle are characteristics of
nematode parasites and the clinical presentation and
components of the inflammatory infiltrate suggested
habronemiasis.12 Moreover, other cutaneous parasitic
diseases of camelids such as Onchocerca species infec-
tions have different clinical presentation and typically do
not develop in the periocular area.1 Other gross differen-
tial diagnoses such as squamous cell carcinoma, trauma
associated with exuberant granulation tissue, microfilarial
dermatitis, bacterial and fungal granulomas, and foreign
body sequestration have histopathological findings that
are not consistent with the pathology seen in this case.
The exact pathogenesis of cutaneous habronemiasis is
Figure 3. Photomicrograph of dromedary camel (Camelus dromeda- unknown, however, a hypersensitivity reaction to the
rius) skin. Note large numbers of eosinophils centred on a cross sec-
dead or dying larvae and the marked tissue eosinophilia
tion of a nematode larva with a cuticle consistent with Habronema
spp. There is loss of detail of the larva due to significant degenera-
are presumed to be involved.2 The larvae were degener-
tion. Haematoxylin and eosin. Bar = 150 lm. ated at the time the biopsy was performed, possibly as a
result of the marked tissue eosinophilia induced by the
parasite and the ivermectin dose given previously by the
cross section was consistent with the shape seen with referring veterinarian. It is also possible that the larvae
nematodes and uncharacteristic of trematodes which are died spontaneously and the need for treatment could be
larger in size. Moreover, the eosinophilic granuloma was questioned in this case.13 However, the parasite caused a
characteristic of Habronema spp. and uncommonly, if severe periocular inflammation and the marked pruritus
ever, seen in cestode and trematode larval infections. experienced by the camel resulted in self-inflicted trauma
The location of the larvae in the deep dermis is also con- and secondary infection warranting treatment. Treatment
sistent with Habronema spp.11 for this camel was similar to that used in equine habrone-
For three consecutive days, the lesion was surgically miasis2,14 with anti-inflammatory therapies, ivermectin,
debrided and flushed with copious amounts of dilute injectable antibiotic, and topical fly repellent. In horses
povidone-iodine solution. Silver sulfadiazine cream 1% the disease is often treated with anti-inflammatories and
(Silvadene; Marion Laboratories Inc., Kansas City, MO, antibiotics for 3 weeks or longer. However, in this case
USA) and fly ointment repellent (Flys-off Ointment; the camel became aggressive after 1 week of treatment
Farnam Pet Products) were applied topically. Ceftiofur and the decision was made to discontinue treatment
sodium (2.2 mg ⁄ kg intramuscularly once daily for 7 days) because the lesion was starting to improve. A fly mask
(Naxcel; Pfizer Animal Health) was given to treat the sec- adapted to fit the camel was also necessary to prevent
ondary infection. Flunixin meglumine (1.25 mg ⁄ kg intra- additional self-trauma.
muscularly once daily for 7 days) (Banamine; Intervet This camel was wormed regularly with an oral ivermec-
Schering-Plough Animal Health), was given to reduce the tin paste which did not prevent the development of cuta-
inflammation and for analgesia. A Duoderm patch (Bristol- neous habronemiasis. This occurrence is also noted in
Myers Squibb, New York, NY, USA) was applied over the llamas, a new world camelid, where oral treatment with
eye. Duoderm dressing consists of a highly flexible poly- ivermectin paste has been shown to be ineffective at
urethane outer foam layer and an adhesive skin contact reaching adequate blood serum concentrations.15 In
layer that contains a hydrocolloid to absorb liquid and dromedaries, there are conflicting reports regarding the
wound exudate. The dressing maintains a moist environ- efficacy of both oral and parenteral ivermectin administra-
ment for optimal wound healing. Also, to prevent the tion.16 Pharmacokinetic studies of subcutaneous iver-
camel from further traumatizing the eye, an equine fly mectin in dromedary camels have shown that at the
mask was altered to fit the camel and was placed with a ruminant dose of 0.2 mg ⁄ kg, lower ivermectin plasma
plastic bowl over the eye. A single dose of ivermectin concentrations develop as compared to cows and
0.2 mg ⁄ kg was administered subcutaneously and full sheep.17 Dromedaries also have a slower rate of ivermec-
resolution of the lesion occurred within 1 month. The tin absorption compared to ruminant species.17 However,
case was then lost to follow-up. side effects have been reported in this species with
higher doses of ivermectin and repeated doses of the
drug, rather than increased amounts are probably safer in
Discussion
camelids.18
In this case, a diagnosis of granulomatous dermatitis In this camelid, the histopathological findings of multi-
associated with Habronema or Draschia larvae was estab- focal eosinophilic granulomas centred on ovoid cross sec-
lished on the basis of clinical and histopathological tions of larvae that had a cuticle and ranged in size from
findings. The microscopic features of the larvae and the 45 to 52 lm in diameter were compatible with an infec-
inflammatory response were similar to those previously tion caused by the nematode Habronema spp. or Draschi-
reported in equine cutaneous habronemiasis.4 A nested- a spp. Cutaneous habronemiasis should be considered as

ª 2010 The Authors. Journal compilation ª 2010 ESVD and ACVD, Veterinary Dermatology, 21, 527–530. 529
Myers et al.

a differential diagnosis for camels with pruritic and 9. Fowler M. Camelidae. In: Fowler ME, Miller RE, eds. Zoo and
ulcerative lesions in geographic regions where this condi- Wild Animal Medicine, 5th edn. Philadelphia: W.B. Saunders,
2003: 612–25.
tion is prevalent.
10. Teare A. International Species Information System Physiological
Data Reference Values CD-ROM. Camelus dromedarius. Apple
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Equine Parasites. Philadelphia: Lea and Febiger, 1986: 412–5. efficacy against equine gastrointestinal parasites. Veterinary
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Résumé Un dromadaire (Camelus dromedarius) stérilisé de 6 ans présentait une plaque ne cicatrisant
pas, sévèrement prurigineuse, fibrotique, ulcérative localisée au canthus médial. L’examen histologique
des biopsies a révélé la présence de larves dégénérées de nématode au sein de granulomes éosinophili-
ques. Le traitement consistait en des débridements répétés de la lésion, de l’ivermectine injectable, des
anti-inflammatoires ainsi qu’une antibiothérapie topique et injectable. Un masque spécialement fabriqué à
cet usage à l’aide de lunettes a été posé sur l’animal pour éviter l’automutilation de l’œil et de la lésion.
Une complète guérison a été observée un mois après le diagnostic. Vu la localisation, les caractéristiques
macroscopiques et microscopiques de la lésion, la période de l’année, la présence de larves de nématodes
et la réponse au traitement, un diagnostic d’habronémose cutanée a été porté.

Resumen Un dromedario castrado de seis años de edad (Camelus dromedarius) se presentó con una
placa fibrótica, muy prurı́tica, ulcerada y que no cicatrizaba, localizada en el canto medial de un ojo. El exa-
men histológico de la biopsia mostraba larvas de nematodos degeneradas dentro de granulomas eosinofı́li-
cos. El tratamiento incluyó extirpación parcial de la lesión, ivermectina inyectaba, terapia antiinflamatoria, y
antibióticos tópicos e inyectados. Se aplicó una máscara especial con gafas de protección para prevenir
que el dromedario continuara traumatizando el ojo y la zona de la lesión. Se observó una recuperación total
aproximadamente un mes tras el diagnostico. Dada la localización de la lesión, la época del año, las cara-
cterı́sticas macroscópicas e histológicas, la presencia de probables larvas de nematodo y la respuesta al
tratamiento se dio un diagnostico de habronemiasis cutánea.

Zusammenfassung Ein sechs Jahre altes Dromedar (Camelus dromedarius) wurde mit einer schlecht-
heilenden, stark juckenden, ulzerierten fibrotischen Plaque im Bereich des medialen Kanthus vorgestellt.
Bei der histologischen Untersuchung der chirurgischen Biopsien wurden degenerierte Nematodenlarven
inmitten eosinophiler Granulome identifiziert. Die Behandlung bestand aus wiederholtem Debridement der
Veränderung, injizierbarem Ivermectin und einer entzündungshemmenden Therapie, sowie injizierbaren
und topischen Antibiotika. Eine speziell konstruierte Maske mit einer Schutzbrille, um das Dromedar daran
zu hindern, das Auge und die Läsion weiterhin selbst zu traumatisieren, wurde ebenfalls verwendet. Etwa
einen Monat nach der Diagnose kam es zur vollständigen Heilung. Aufgrund der Lokalisation der Verände-
rung, der Jahreszeit, der makroskopischen und mikroskopischen Charakteristika der Läsion, des Vorkom-
mens einer vermeintlichen Nematodenlarve und des Behandlungserfolges wurde die Diagnose einer
Habronemiasis gestellt.

530 ª 2010 The Authors. Journal compilation ª 2010 ESVD and ACVD, Veterinary Dermatology, 21, 527–530.

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