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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, Spain Abstract
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 Fax: +54 11 4827-4753e-mail: 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
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
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 .
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2007 American College of Veterinary Ophthalmologists, Veterinary Ophthalmology, 10, 285–288



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