Veterinary Ophthalmology (2007) 10, 5, 285–288 Blackwell Publishing Inc Severe, unilateral, unresponsive keratoconjunctivitis sicca in 16 juvenile Yorkshire Terriers
Héctor Daniel Herrera,* Nathalie Weichsler,* José Rodríguez Gómez† and José Antonio García de Jalón‡*Ophthalmology Unit, Veterinary Medicine Teaching Hospital, School of Veterinary Sciences, University of Buenos Aires, Argentina, †Surgery and ‡Pathology Units, School of Veterinary, University of Zaragoza, SpainAbstract Objective To present ophthalmic findings, clinical data, and treatment outcomes of 16
juvenile Yorkshire Terriers with severe unilateral keratoconjunctivitis sicca. Results Each of the 16 dogs exhibited extreme unilateral dryness associated with
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blepharospasm, mucoid discharge, and corneal vascularization. Ages of affected dogs at presentation ranged from 5 months to 4 years. Mean Schirmer tear test (STT) result for affected eyes was 1 mm/min. Topical application of 0.2% cyclosporine to the affected eye was not associated with improvement in STT values in any dog. Clinical signs subjectively improved with topical application of 20% chondroitin sulfate ophthalmic solution in some dogs, and transposition of the parotid duct was performed in three dogs. Histopathologic examination in one dog failed to show evidence of orbital lacrimal gland tissue. Clinical signs, age of presentation, disease severity, and lack of response to treatment are consistent with breed-related unilateral aplasia or hypoplasia of the lacrimal gland. Conclusion Lacrimal gland aplasia or hypoplasia should be considered in young dogs with severe unilateral ocular dryness, especially female Yorkshire Terriers. Key Words: congenital alacrima, developmental defect, KCS, keratoconjunctivitis sicca, Yorkshire Terrier
White Terriers, and female dogs were also more affected
INTRODUCTION
than male dogs in other clinical trials.1,9–11
Canine keratoconjunctivitis sicca (KCS) is a common ocular
Little information exists regarding congenital alacrima.
disease characterized by a variable diminution of the
In particular, predisposed breeds, clinical signs associated
aqueous layer of the precorneal tear film, and resulting in
with this syndrome and treatment and prognosis of affected
desiccation and inflammation of the conjunctiva and cornea.1–3
dogs are poorly described. The purpose of this paper was to
While ocular pain, conjunctivitis, corneal melanosis, and
describe clinical findings and treatment outcomes for 16
corneal vascularization may be present depending on the
juvenile Yorkshire Terriers with severe unilateral kerato-
stage of the disease, the main clinical sign is the presence of
conjunctivitis sicca suggestive of congenital alacrima.
mucoid ocular discharge. For this reason, KCS may be mis-diagnosed as bacterial conjunctivitis.1,2
CASE HISTORIES
In dogs, KCS is commonly characterized as an immune-
mediated disorder, occasionally associated with systemic
Sixteen Yorkshire Terriers were presented to the Ophthalmo-
autoimmune conditions.1–3 Other causes of KCS include
logy Unit of the School of Veterinary Sciences (University
infectious disease, such as distemper, toxicity due to sulfona-
of Buenos Aires) and the Surgery Unit of the School of
mides or other drugs, surgical removal of the gland of the
Veterinary (University of Zaragoza) between August 1999
third eyelid, facial trauma, and congenital alacrima.1–8
and February 2004. Each patient had a chronic history of
Breed and sex predisposition to KCS have been pro-
severe, unilateral blepharospasm and variable amounts of
posed.1–3,5,9,10 The English Bulldog, Lhasa Apso, Shih Tzu,
mucoid discharge from and over the surface of the affected
West Highland White Terrier and Cocker Spaniel are
eye (Figs. 1–3). Twelve affected dogs were female and four
recognized worldwide as predisposed breeds.1,3 A female
were male. Chi-square analysis of this gender distribution
predisposition to KCS was reported in West Highland
suggested female dogs were significantly more frequently
2007 American College of Veterinary Ophthalmologists
286 E T A L . Figure 1. Right eye of a 2-year-old, female Yorkshire Terrier with unilateral and severe keratoconjunctivitis sicca (STT 0 mm/min) and associated blepharospasm, blepharitis, copious mucoid discharge, and superficial corneal vascularization. Figure 2. Left eye of a 2-year-old, female Yorkshire Terrier with unilateral keratoconjunctivitis sicca (STT 4 mm/min) of 3 months duration. Blepharospasm, blepharitis, mucoid discharge, and superficial corneal vascularization can be observed. Figure 3. Left eye of an 11-month-old, male Yorkshire Terrier with unilateral and severe keratoconjunctivitis sicca (STT 0 mm/min) and associated blepharospasm and mild mucoid discharge.
affected than were male dogs (P = 0.05). No dogs were
the STT in the affected eye was 0 mm/min. Results of the
neutered and a familial relationship between the dogs was
STT in the unaffected eye ranged from 11 to 17 mm/min
known for only two dogs, which were mother and daughter.
(mean ± SD, 14 ± 2; median, 15). IOP was normal in all dogs.
The dogs ranged in age from 5 months to 4 years (mean ±
Affected eyes had blepharitis, mild conjunctival hyperemia,
standard deviation (SD): 2.1 ± 1.4 years; median: 2 years).
and variable degrees of superficial corneal vascularization
Duration of clinical signs before presentation ranged from 3
with a dry appearance to the ocular surface. Corneal melanosis
to 24 (mean ± SD: 9.1 ± 6.9; median: 6) months. All dogs
was not observed in any dog. The rest of the anterior segment
had been treated with various topical ophthalmic antibiotics
examination and the fundic examination revealed no
by the referring veterinarians, without resolution of clinical
abnormalities in any dog. Signs of cranial nerve dysfunction
signs. None of the dogs had been treated with sulfonamides
were not observed in any dog and no other relevant clinical
or had undergone surgery involving the third eyelid gland. A
signs were detected during the general physical examination.
history of trauma or infectious disease could not be obtained
Eleven dogs were initially treated with 0.2% cyclosporine
ophthalmic ointment (Optimmune, Schering Plough,
Thorough ophthalmic examination including the Schirmer
Buenos Aires, Argentina and Zaragoza, Spain) three times
tear test (STT) (Schering Plough Animal Heath Co., Kenil-
daily for 30 days. A mild reduction in the amount of mucoid
worth, NJ, USA), measurement of intraocular pressure
discharge and blepharospasm was observed in these eyes;
(IOP) using applanation tonometry (Tonopen, Mentor,
however, none of the treated eyes showed improvement
Norwell, MA, USA), application of fluorescein stain, slit-
in their STT values at revisit examinations during this time.
lamp biomicroscopy (Kowa SL-14, Kowa, Tokyo, Japan),
In fact, STT results declined by a further 3 mm/min and
and direct and indirect ophthalmoscopy was performed
4 mm/min, respectively, in the two dogs receiving this
in all dogs. Results of the STT in the affected eye ranged
treatment. The remaining five dogs that did not receive
from 0 to 7 mm/min (mean ± SD, 1 ± 2; median, 0). In 11 dogs,
cyclosporine, along with those three in which cyclosporine
2007 American College of Veterinary Ophthalmologists, Veterinary Ophthalmology, 10, 285–288
287
was unsuccessful, were treated twice daily with 20% chon-droitin sulfate ophthalmic solution (Tears, Labyes, BuenosAires, Argentina). All eyes receiving 20% chondroitin sulfateophthalmic solution showed subjective improvement inocular comfort as evidenced by reduced blepharospasm.
Open (lateral approach) parotid duct transposition (PDT)
was performed in three dogs, and a good result was obtainedin two. Excessive salivary secretion and facial dermatitisoccurred in the third. A nylon ligature was performedaround the duct to decrease salivary secretion in this dog.
History, signalment, clinical signs, age of presentation,
disease severity, and lack of response to medical treatmentsuggested that these dogs had breed-related unilateralaplasia or hypoplasia of the lacrimal gland. Based on thispresumptive diagnosis, biopsy of the lacrimal glands of theaffected eye was proposed in seven dogs but no owner con-sented to this. However, a 5-year-old, female dog, which hadundergone PDT, experienced acute spinal cord compressiondue to intervertebral disk protrusion and underwent reductionsurgery 2 years after the original ophthalmic diagnosis. Thisdog was subsequently euthanized owing to neurologic disease,and a tissue sample was collected from the site of the orbitallacrimal gland, fixed in paraformaldehyde and routinelyprocessed for histologic examination. Light microscopicexamination of a hematoxylin and eosin-stained section of
Figure 4. Photomicrograph of a tissue sample obtained from the
this tissue revealed absence of acini and ducts consistent with
dorsolateral orbit of a 5-year-old, female Yorkshire Terrier with
aplasia. A few lobules of sebaceous glands were observed
keratoconjunctivitis sicca and suspected congenital alacrima. Note the
(Fig. 4). Biopsy of the third eyelid lacrimal gland was not
absence of acini, ducts, inflammatory cells, or fibrosis consistent with
aplasia of the lacrimal gland. Vacuolated cells (arrows) represent
During the 4.5-year study period, only one other dog with
history, signalment, clinical signs, and response to therapysuggestive of congenital alacrima was presented to theauthors. This was a 1-year-old, female Chihuahua. This dog
well described.1,3,5 Aguirre et al. reported three cases of con-
was treated with 20% chondroitin sulfate ophthalmic solu-
genital KCS in a series of 71 dogs affected with dry eye.5
tion and showed a similar response to the Yorkshire Terriers
Although these authors described congenital KCS as more
common in miniature or small-breed dogs, there was no fulldescription of the clinical characteristics of these three dogs. In the current report, all but one of the affected dogs in a
DISCUSSION
4.5-year period were Yorkshire Terriers, suggesting that
Keratoconjunctivitis sicca is a common condition in dogs.
Yorkshire Terriers are predisposed to this syndrome. A sex
One of the most common causes of this syndrome is
predisposition for KCS has been suggested by some
immune-mediated destruction of the lacrimal glands, which
authors,1,3 and in other studies female were more commonly
tends to occur in adult dogs, is typically bilateral, and has an
affected than male dogs.10,11 In the study presented here,
insidious onset until aqueous deficiency is severe enough to
female (n = 12) were presented three times more commonly
produce signs of ocular surface dryness. The Yorkshire Terrier
than male dogs (n = 4) and this difference bordered on
is not a breed usually affected by the immune-mediated form
of KCS.1 The dogs in this study were all affected with severe
Congenital aplasia or hypoplasia of the lacrimal gland
clinical signs at an early age. Besides immune-mediated
should be considered when a young dog of a small breed is
dacryoadenitis, KCS may be caused by toxicity associated
presented with signs attributable to severe, unilateral reduc-
with sulfonamides,5,6 infectious disease, such as canine
tion in the aqueous layer of the precorneal tear film. This
distemper virus,4 facial and trigeminal nerve disorders,8 and
diagnosis is supported by a lack of history suggestive of
surgical excision of the third eyelid gland.7 Evidence of these
trauma, infectious disease, toxicity, or previous surgery of
causes was not found in any patient presented in the current
the third eyelid. All of the dogs presented here met these
criteria. Although confirmation of the diagnosis by biopsy of
Congenital alacrima, caused by aplasia or hypoplasia of
the lacrimal glands was not possible in most dogs in the pre-
the lacrimal gland, has been frequently mentioned but not
sent series because of lack of owner consent, histopathologic
2007 American College of Veterinary Ophthalmologists, Veterinary Ophthalmology, 10, 285–288 288 E T A L .
examination performed in one dog was consistent with
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2007 American College of Veterinary Ophthalmologists, Veterinary Ophthalmology, 10, 285–288
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