Abstract
Objective
To investigate the incidence of corneal ulceration (CU) and establish risk factors for dogs referred to an academic referral hospital in Ontario, Canada.
Animals
Dogs (N = 1101).
Procedure
Type of CU, number of CU diagnoses, breed, skull conformation, weight, sex, neuter status, age, and comorbidities were analyzed for simple CU, spontaneous chronic corneal epithelial defects (SCCEDs), and complex CU. Complex ulcers were subdivided into deep, presence of keratomalacia, descemetoceles, and corneal lacerations and foreign bodies (CLFB).
Results
The inclusion criteria were met by 347 dogs and 754 served as a control population of non-corneal ulceration (NCU) cases. Complex ulcers predominated (n = 134; 38.5%), including deep (n = 41; 11.8%), with keratomalacia (n = 20; 5.7%), descemetocele (n = 59; 17.0%), and CLFB (n = 14; 4.0%). Shih tzus were most predominant for every ulcer type, except for boxers for SCCEDs. Brachycephalic breeds have 2.757 greater odds (P < 0.0001) of presenting for CU, and 2.695 greater odds (P < 0.0001) of having a complex CU. Each 1 kg decrease in body weight increased odds of CU diagnosis by 1.3%. Yearly increase in age augmented the odds of CU diagnosis by 8.9% (P < 0.0001); older dogs were more likely to have SCCEDs (P = 0.0040) and keratomalacia (P = 0.0257). Comorbidities increased odds of repeat CU diagnosis (P = 0.0024). Dogs with diabetes mellitus (P = 0.0318) had higher odds of SCCEDs.
Conclusion
Skull conformation, age, body weight, and comorbidities were identified risk factors for CU.
Clinical relevance
Knowledge of risk factors will help veterinarians triage at risk demographics.
Résumé
Évaluation du type d’ulcère cornéen, de la conformation du crâne et autres facteurs de risque chez le chien : une étude rétrospective de 347 cas
Objectif
Étudier l’incidence d’ulcération de la cornée (UC) et établir les facteurs de risque pour les chiens référés à un hôpital universitaire de référence en Ontario, Canada.
Animaux
Chiens (N = 1101).
Procédure
Le type d’UC, le nombre de diagnostics d’UC, la race, la conformation du crâne, le poids, le sexe, le statut de stérilisation, l’âge et les comorbidités ont été analysés pour les UC simples, les défauts épithéliaux cornéens chroniques spontanés (SCCEDs) et les UC complexes. Les ulcères complexes ont été subdivisés en profonds, présence de kératomalacie, descémétocèles et lacérations cornéennes et corps étrangers (CLFB).
Résultats
Les critères d’inclusion ont été remplis par 347 chiens et 754 ont servi de population témoin de cas d’ulcération non-cornéenne (UNC). Les ulcères complexes prédominaient (n = 134; 38,5 %), y compris profonds (n = 41; 11,8 %), avec kératomalacie (n = 20; 5,7 %), descémétocèles (n = 59; 17,0 %) et CLFB (n = 14; 4,0 %). Les shih tzus étaient les plus prédominants pour chaque type d’ulcère, à l’exception des boxers pour les SCCEDs. Les races brachycéphales ont 2,757 chances plus élevées (P < 0,0001) de présenter un UC et 2,695 chances plus élevées (P < 0,0001) d’avoir un UC complexe. Chaque diminution de 1 kg du poids corporel augmentait les risques de diagnostic de UC de 1,3 %. L’augmentation annuelle de l’âge augmentait les chances de diagnostic d’UC de 8,9 % (P < 0,0001); les chiens plus âgés étaient plus susceptibles d’avoir des SCCEDs (P = 0,0040) et une kératomalacie (P = 0,0257). Les comorbidités ont augmenté les chances de répéter le diagnostic d’UC (P = 0,0024). Les chiens atteints de diabète mellitus (P = 0,0318) avaient un risque plus élevé de SCCEDs.
Conclusion
La conformation du crâne, l’âge, le poids corporel et les comorbidités ont été identifiés comme facteurs de risque d’UC.
Pertinence clinique
La connaissance des facteurs de risque aidera les vétérinaires à trier les cas à risque selon les données démographiques.
(Traduit par Dr Serge Messier)
Introduction
Corneal ulceration (CU) is a prevalent condition in dogs, being diagnosed in 0.8% of all dogs examined by first opinion veterinarians (1) and 8.04 to 16.1% of cases referred to Board-certified veterinary ophthalmologists (2,3). These ulcers can range in depth from superficial absence of corneal epithelium to absence of corneal stroma resulting in exposure of the Descemet’s membrane (descemetocele). Microbial colonization of the ulceration can occur, leading to liquefaction of the stroma, commonly referred to as keratomalacia or melting. Corneal ulcers may be acute or chronic in nature and 3 categories of canine CU have been described. Simple CU are defined as superficial (denuded corneal epithelium) with an acute history and no apparent infection. Most simple ulcers heal within 7 d with the administration of topical antimicrobials to prevent secondary infection (4). Spontaneous chronic corneal epithelial defects (SCCEDs), also known as indolent ulcers, boxer ulcers, or recurrent/refractory ulcers, are diagnosed as a non-infected superficial CU with a lip of non-adherent corneal epithelium and a fluorescein stain halo effect. This type of ulcer responds to corneal debridement and keratotomy and/or diamond burr debridement within 14 d (5–9). Complex or complicated CU comprise the third and a large clinical category of ulcers with stromal loss ranging from 1% stromal loss to descemetoceles (100% stromal loss). These ulcers often persist longer than 7 d, likely have infection present, and may exhibit keratomalacia or corneal rupture. This last category requires intensive medical therapy, often with concurrent surgical intervention, to preserve the integrity of the globe (4,10).
Corneal ulcers can occur due to various etiologies (4,11–13). Trauma has been linked to simple ulcers and an initial inciting trauma is also often reported for SCCEDs (4,5). Boxer breed predisposition has been associated with SCCEDs, with a specific genetic defect being recently identified (14). Other potential contributing factors for SCCEDS include histological abnormalities in the corneal endothelial basement membrane or anterior stroma, and abnormal corneal innervation (5,7,9,15,16). Complex CU can be a direct result of trauma, or secondary to complications of normal corneal wound healing, such as anatomical abnormalities, previous treatment with corticosteroids, pre-existing ocular surface disease, or bacterial infection (1,4,17,18). Infection with Pseudomonas aeruginosa and β-hemolytic Streptococcus spp. have been associated with keratomalacia in previous studies (17,19).
Early diagnosis and proper management of CU is important to prevent progression to more complex types of ulcers, which may lead to increased or prolonged ocular pain and possibly corneal perforation and/or blindness. Numerous studies have documented that brachycephalic breeds are at a significantly higher risk of developing CU compared to non-brachycephalic breeds (1,3,18,20–25). This is in part the result of selective breeding for exaggerated morphological features such as prominent eyes, visible sclera, and nasal folds, which leads to a genetic predisposition to ocular pathologies such as medial entropion, cilia abnormalities, and tear film disorders (21,23). Furthermore, corneal innervation is significantly reduced in brachycephalics, which contributes to the development of CU (due to reduced corneal protective mechanisms). This also impairs healing capacity (1,2,18,25–27). An association between complex ulcers and keratomalacia is also seen with brachycephalic breeds, especially the shih tzu (17,19,28).
The prevalence of CU according to depth of corneal involvement in relation to specific clinical factors, such as breed, gender and age, or breed, age, and ocular comorbidities has been investigated (25,29). However, no studies to date have broadly evaluated the different types of CU by complexity and incidence as related to complete signalment (breed, skull conformation, weight, sex, neuter status, and age) in addition to concurrent ocular and systemic disease. This information could be used by veterinarians to modify treatment decisions and monitoring strategies for dogs at higher risk of CU.
The objectives of this retrospective study were to establish the demographics and potential risk factors of dogs diagnosed with 1 of 3 types of CU (simple, SCCEDs, and complex) by a Board-certified veterinary ophthalmologist at a referral hospital in central Canada. The working hypotheses were that brachycephalic breeds and dogs with underlying ocular disease would be overrepresented, particularly for complex CU.
Materials and methods
Database
Dogs diagnosed with an ocular disease by a Board-certified veterinary ophthalmologist at the Ontario Veterinary College Health Sciences Center (OVCHSC) over a 10-year period were identified, and their medical records were reviewed. Corneal ulceration cases were excluded when the diagnosis was not made or confirmed by the Ophthalmology Service. A control population of dogs brought to the OVCHSC Ophthalmology Service for initial diagnosis of non-corneal ulcerative (NCU) ophthalmic disease during the same time was also evaluated.
Each CU was categorized as follows:
simple (denuded corneal epithelium and no evidence of infection);
SCCEDs (denuded corneal epithelium with accompanying loose corneal epithelium or fluorescein stain halo); and
complex CU.
Complex CU were further subdivided into deep (extending to the stroma at any depth), presence of keratomalacia (visible melting), descemetocele (extending to the Descemet’s membrane) with or without corneal rupture, and corneal lacerations and foreign bodies (CLFB). Cases that progressed from one category of ulcer to another while under the care of a Board-certified ophthalmologist were recorded as the most severe type of CU diagnosed. For each dog, every newly diagnosed CU was recorded as a separate diagnosis but repeat diagnoses of the same ulcer during rechecks (whether healing or unchanged) were excluded. The data from the initial visit were used for dogs that were brought to the hospital with a new CU on more than one occasion and the number of repeat ulcers was recorded. During this initial visit, if bilateral corneal disease was identified, the dog was categorized by using the eye with the most severe form of corneal disease (e.g., SCCED over simple; complex over SCCED; keratomalacia over deep; and descemetoceles or CLFB over keratomalacia). For the NCU population, data from their first diagnosis made by the Board-certified veterinary ophthalmologist within the study period were used for analysis. Recheck examinations were excluded.
Additional data collected from the medical records included the affected eye, breed, skull conformation, weight, sex, neuter status, and age. For the CU population, the total number of CU diagnoses and concurrent ocular and systemic comorbidities were also recorded. Breed was recorded based on medical record information and each dog’s photograph. When non-purebred dogs were encountered, they were listed in the breed category they most resembled (e.g., German shepherd cross or mix was categorized as German shepherd). When the breed was unclear, dogs were categorized as an unidentified mixed-breed. Classification of skull conformation was based on both the reported breed and medical record photographs. When a discrepancy occurred between recorded breed and the photograph, skull conformation was assigned based on the photograph. If a photograph was not available, skull conformation was assigned in accordance with breed classification in previously published literature (21,25,27,30). Weight was recorded in kg and 3 weight categories were established: small breeds were ≤ 10 kg, medium breeds were 10.1 to 30 kg, and large breeds were > 30 kg. Age was categorized by years and months and recorded in decimal form. A comorbidity was defined as an underlying medical condition and was classified as any ocular or systemic disease that was identified in the dog’s medical records prior to admission or diagnosed during the initial examination. Comorbidities were recorded as none, ocular, systemic, or both ocular and systemic.
Statistics
Commercially available software (2013. SAS/STAT 9.4; SAS Institute, Cary, North Carolina, USA) was used for statistical analysis. To determine risk factors for developing a CU and the type of CU, parameters of interest (breed, skull conformation, weight, sex, intact status, age, and comorbidities) were modelled with univariate exact conditional logistic regression. To investigate whether the shih tzu breed was more at risk than other breeds when controlled for skull conformation, weight, sex, intact status, age, and comorbidities, a multivariate model was run. Odds ratios and P-values were reported for all analyses. Significance was set at P < 0.05.
Results
Between May 16, 2011 and June 15, 2021, 1101 dogs received an initial diagnosis of an ophthalmic disease by a Board-certified ophthalmologist at the OVCHSC Ophthalmology Service. Of these, 347 dogs were diagnosed with CU (study population), and the remaining 754 dogs were deemed NCU cases (control population). The types of CU diagnosed were: simple (n = 125; 36%), SCCEDs (n = 88; 25.4%), and complex (n = 134; 38.6%). Complex CU included deep (n = 41; 11.8%), with keratomalacia (n = 20; 5.8%), descemetocele (n = 59; 17%), and CLFB (n = 14; 4%). Forty-nine dogs (14.1%) were presented with bilateral CU at the initial visit, whereas the remaining 298 dogs (85.9%) had only 1 eye affected. Of the 298 dogs with unilateral CU on initial presentation, 146 (49%) were right eye and 152 (51%) were left eye. Most dogs (n = 303; 87.3%) only received a diagnosis of CU once during the study period, whereas 29 (8.4%) visited a second time for a separate CU, 10 (2.9%) visited 3 times, 3 (0.9%) visited 4 times, and 2 (0.6%) received 5 separate diagnoses of CU during this time. Of the 44 dogs which received multiple diagnoses of CU over the study period, 70.5% had at least one subsequent CU diagnosed in the contralateral eye, whereas 29.5% of dogs had all subsequent CU diagnoses in the same eye as at their initial presentation.
The CU and NCU populations were comprised of 72 breeds and 91 breeds, respectively (including unidentified mixed-breed dogs) (Table 1). The 5 most common breeds for each CU type are represented in Table 2. The shih tzu breed was significantly associated with an increased overall risk of CU compared with the NCU population (P < 0.0002) (Table 1). This breed (P < 0.0001) and pugs (P = 0.0088) also had a higher risk of having a complex CU (Table 2). In addition, shih tzus were overrepresented for keratomalacia (P = 0.0338). Bichon frises (P = 0.0123) and Yorkshire terriers (P = 0.0424) were over-represented in simple ulcers. Boxers were significantly predisposed to SCCEDs (P < 0.0001), along with golden retrievers (P = 0.00898) (Table 2).
Table 1.
Overall demographic data of the 1101 dogs presenting to the Ontario Veterinary College Health Sciences Centre Ophthalmology Service for an initial diagnosis between 2011 and 2021.
| Clinical variable | Category | Number of CUa cases (%) | Number of NCUb Cases (%) | Total number in study population (%) | Odds ratio for CUa | 95% CI | P-value |
|---|---|---|---|---|---|---|---|
| Five most common breeds of CU and NCU populations | Shih tzu | 59 (17) | 68 (9) | 127 (11.5) | 2.065 | 1.393 to 3.057 | 0.0002 |
| Boston terrier | 20 (5.8) | 18 (2.4) | 38 (3.5) | 2.499 | 1.237 to 5.083 | 0.0053 | |
| Mixed breed | 19 (5.5) | 12 (1.6) | 31 (2.8) | 3.577 | 1.627 to 8.181 | 0.0005 | |
| Pug | 18 (5.2) | 34 (4.5) | 52 (4.7) | 1.091 | 0.563 to 2.041 | 0.8775 | |
| English bulldog | 17 (4.9) | 35 (4.6) | 52 (4.7) | 1.058 | 0.548 to 1.973 | 0.8788 | |
| Golden retriever | 14 (4) | 53 (7) | 67 (6.1) | 0.556 | 0.281 to 1.035 | 0.0576 | |
| Labrador retriever | 14 (4) | 49 (6.5) | 63 (5.7) | 0.605 | 0.304 to 1.133 | 0.1240 | |
| Cocker spaniel | 4 (1.2) | 47 (6.2) | 51 (4.6) | 0.176 | 2.057 to 21.940 | < 0.0001 | |
| Skull conformation | Brachycephalic | 179 (51.6) | 210 (27.9) | 389 (35.3) | 2.757 | 2.1 to 3.625 | < 0.0001 |
| Mesaticephalic | 136 (39.2) | 433 (57.4) | 569 (51.7) | 0.589 | 0.375 to 0.902 | 0.0120 | |
| Dolichocephalic | 32 (9.2) | 111 (14.7) | 143 (13) | 0.478 | 0.365 to 0.624 | < 0.0001 | |
| Size | Small | 149 (46.9) | 264 (38.3) | 413 (37.5) | 1.372 | 1.049 to 1.794 | 0.0192 |
| Medium | 110 (34.6) | 277 (40.1) | 387 (35.1) | 0.804 | 0.607 to 1.062 | 0.1183 | |
| Large | 59 (18.6) | 149 (21.6) | 208 (18.9) | 0.825 | 0.581 to 1.161 | 0.2825 | |
| Sex | Female | 142 (40.9) | 338 (44.8) | 480 (43.6) | 0.853 | 0.899 to 1.531 | 0.2505 |
| Male | 205 (59.1) | 416 (55.2) | 621 (56.4) | 1.172 | 0.899 to 1.531 | 0.2505 | |
| Neutered status | Intact (female and male) | 48 (13.8) | 112 (14.9) | 160 (14.5) | 0.920 | 0.746 to 1.601 | 0.7130 |
| Mean age (range) in years | 8.0 (0.2 to 17.4) | 6.6 (0.3 to 17.9) | 7.0 (0.2 to 17.9) | ||||
| Mean weight (range) in kg | 16.8 (1.0 to 69.0) | 19.2 (1.2 to 76.0) | 18.5 (1 to 76) |
CU — Corneal ulceration.
NCU — Non-corneal ulceration.
Table 2.
Five most common breeds representing each CU type (simple, SCCED and complex) diagnosed at the Ontario Veterinary College Health Sciences Centre Ophthalmology Service between 2011 and 2021.
| CUa type | Top 5 represented breeds | Number of dogs each breed (%) | Total number of dogs with CUa type | Odds ratio | 95% CI | P-value |
|---|---|---|---|---|---|---|
| Simple | Shih tzu | 12 (9.6) | 125 | 0.396 | 0.183 to 0.800 | 0.0070 |
| Bichon frise | 9 (7.2) | 125 | 5.635 | 1.372 to 32.977 | 0.0123 | |
| Mixed breed | 9 (7.2) | 125 | 1.642 | 0.573 to 4.641 | 0.3289 | |
| Yorkshire terrier | 9 (7.2) | 125 | 3.355 | 0.983 to 13.050 | 0.0424 | |
| Labrador retriever | 8 (6.4) | 125 | 2.455 | 0.727 to 8.802 | 0.1521 | |
| SCCEDsb | Boxer | 14 (15.9) | 88 | 24.046 | 5.340 to 222.743 | < 0.0001 |
| Golden retriever | 8 (9.1) | 88 | 4.195 | 1.235 to 15.137 | 0.0098 | |
| Shih tzu | 8 (9.1) | 88 | 0.409 | 0.160 to 0.919 | 0.0317 | |
| Boston terrierc | 6 (6.8) | 88 | 1.280 | 0.390 to 3.688 | 0.7918 | |
| Complex | Shih tzu | 39 (29.1) | 134 | 3.945 | 2.113 to 7.559 | < 0.0001 |
| Pug | 12 (9) | 134 | 4.075 | 1.298 to 15.127 | 0.0088 | |
| Boston terrier | 10 (7.5) | 134 | 1.635 | 0.592 to 4.515 | 0.3451 | |
| English bulldog | 6 (4.5) | 134 | 0.861 | 0.255 to 2.615 | 0.8062 | |
| Mixed breed | 5 (3.7) | 134 | 0.552 | 0.152 to 1.671 | 0.3353 | |
| Complex — Deep | Shih tzu | 6 (14.6) | 41 | 0.314 | 0.098 to 0.862 | 0.0209 |
| Boston terrier | 4 (9.8) | 41 | 1.467 | 0.141 to 8.233 | 0.6445 | |
| Pug | 4 (9.8) | 41 | 1.147 | 0.238 to 4.612 | 1.0000 | |
| Mixed breed | 3 (7.3) | 41 | 3.553 | 0.391 to 44.129 | 0.3227 | |
| Maltese terrier | 3 (7.3) | 41 | 7.144 | 0.554 to 385.309 | 0.0851 | |
| Complex — Keratomalacia | Shih tzu | 10 (50) | 20 | 2.904 | 0.977 to 8.678 | 0.0338 |
| Boston terrierd | 2 (10) | 20 | 1.467 | 0.141 to 8.233 | 0.6445 | |
| Complex — Descemetocele | Shih tzu | 21 (35.6) | 59 | 1.743 | 0.771 to 3.979 | 0.1804 |
| Pug | 7 (11.9) | 59 | 1.876 | 0.482 to 7.941 | 0.366 | |
| Boston terrier | 4 (6.8) | 59 | 0.837 | 0.165 to 3.734 | 1.0000 | |
| English bulldog | 3 (5.1) | 59 | 1.283 | 0.165 to 9.952 | 1.0000 | |
| Chihuahua | 2 (3.4) | 59 | 1.278 | 0.090 to 18.134 | 1.0000 | |
| Complex — CLFBc | Shih tzu | 2 (14.3) | 14 | 0.376 | 0.039 to 1.820 | 0.2340 |
| Miniature schnauzere | 2 (14.3) | 14 | 9.502 | 0.637 to 142.145 | 0.0541 |
CU — Corneal ulceration.
SCCEDs — Spontaneous chronic corneal epithelial defects.
CLFB — Corneal laceration and foreign bodies.
English bulldog and mixed breed dogs tied with 5 cases each.
Bichon frise, chihuahua, French bulldog, Italian greyhound, Manchester terrier, miniature pinscher, Yorkshire terrier, and mixed breed dogs tied with 1 case each.
Border collie, French bulldog, German shepherd, German short-haired pointer, golden retriever, Labrador retriever, Lhasa apso, pug, Rottweiler, and mixed breed dogs tied with 1 case each.
Brachycephalic skull conformation significantly increased the odds of CU (P < 0.0001) and was the most common skull type among all dogs with CU (Table 1). In comparison, the NCU population was predominantly mesaticephalic (Table 1). The association between CU type and skull conformation was also significantly different, with brachycephalics being over-represented for complex ulcers (P < 0.0001), in particular descemetoceles (P = 0.0055) (Table 3). Mesaticephalics were significantly more likely to have a simple ulcer (P = 0.0014) or a CLFB (P = 0.0115) (Table 3). Dolichocephalics were predisposed to bilateral CU (P = 0.0257), whereas brachycephalics were at a reduced risk (P = 0.0487) (Table 3). Skull conformation did not significantly increase the probability of repeat CU during the study period.
Table 3.
Relationship between skull conformation and CU type, odds of bilateral ulceration or repeat CU diagnosis for the 347 dogs diagnosed with a CU at the Ontario Veterinary College Health Sciences Centre Ophthalmology Service between 2011 and 2021.
| Skull conformation | Ulcer type, affected eye and number of diagnoses | Number of CUa cases (%) | Total number of each CUa type | Odds ratio | 95% CI | P-value |
|---|---|---|---|---|---|---|
| Brachycephalic | Simple | 45 (36) | 125 | 0.371 | 0.228 to 0.596 | < 0.0001 |
| SCCEDsb | 45 (51.1) | 88 | 0.976 | 0.585 to 1.632 | 1.0000 | |
| Complex | 89 (66.4) | 134 | 2.695 | 1.684 to 4.354 | < 0.0001 | |
| Deep | 23 (56.1) | 41 | 0.525 | 0.229 to 1.209 | 0.1134 | |
| Keratomalacia | 14 (70) | 20 | 1.212 | 0.398 to 4.158 | 0.8019 | |
| Descemetocele | 47 (80.0) | 59 | 3.052 | 1.330 to 7.375 | 0.0055 | |
| CLFBc | 5 (35.7) | 14 | 0.241 | 0.059 to 0.866 | 0.0156 | |
| Bilateral ulcer | 22 (44.9) | 49 | 0.478 | 0.208 to 1.050 | 0.3559 | |
| > 1 Ulcer diagnosis | 23 (52.3) | 44 | 1.032 | 0.487 to 1.918 | 1.0000 | |
| Mesaticephalic | Simple | 63 (50.4) | 125 | 2.069 | 1.291 to 3.329 | 0.0014 |
| SCCEDsb | 37 (42) | 88 | 1.172 | 0.693 to 1.970 | 0.5302 | |
| Complex | 36 (26.9) | 134 | 0.416 | 0.252 to 0.678 | 0.0002 | |
| Deep | 16 (39) | 41 | 2.320 | 0.965 to 5.572 | 0.0557 | |
| Keratomalacia | 3 (15) | 20 | 0.435 | 0.077 to 1.655 | 0.2761 | |
| Descemetocele | 9 (15.3) | 59 | 0.323 | 0.120 to 0.797 | 0.0102 | |
| CLFBc | 8 (57.1) | 14 | 4.322 | 1.201 to 16.512 | 0.0115 | |
| Bilateral ulcer | 19 (38.8) | 49 | 1.252 | 0.569 to 2.712 | 0.5810 | |
| > 1 Ulcer diagnosis | 15 (34.1) | 44 | 0.779 | 0.635 to 2.692 | 0.5113 | |
| Dolichocephalic | Simple | 17 (13.6) | 125 | 2.167 | 0.976 to 4.860 | 0.0516 |
| SCCEDsb | 6 (6.8) | 88 | 0.656 | 0.213 to 1.708 | 0.4052 | |
| Complex | 9 (6.7) | 134 | 0.596 | 0.235 to 1.390 | 0.2538 | |
| Deep | 2 (4.9) | 41 | 0.632 | 0.061 to 3.526 | 0.7215 | |
| Keratomalacia | 3 (15) | 20 | 3.139 | 0.465 to 16.463 | 0.1325 | |
| Descemetocele | 3 (5.1) | 59 | 0.618 | 0.096 to 3.051 | 0.7307 | |
| CLFBc | 1 (7.1) | 14 | 1.076 | 0.023 to 9.211 | 1.0000 | |
| Bilateral ulcer | 8 (16.3) | 49 | 2.974 | 0.993 to 7.952 | 0.0257 | |
| > 1 Ulcer diagnosis | 6 (13.6) | 44 | 1.678 | 0.220 to 1.884 | 0.4011 |
CU — Corneal ulceration.
SCCEDs — Spontaneous chronic corneal epithelial defects.
CLFB — Corneal laceration and foreign bodies.
Dogs with CU ranged in size from 1.0 to 69 kg (mean: 16.8 kg), compared to the NCU population mean of 19.2 kg (Table 1). Body weight was significantly different when comparing the CU and NCU populations, with 1.3% increased odds of CU diagnosis for every 1 kg decrease in body weight (P = 0.01). Within the CU population, small dogs predominated (46.9%). Small dogs were also associated with increased odds of CU compared to the NCU group (P = 0.0192) (Table 1). In addition, small dogs were significantly predisposed to complex CU (P = 0.0037), particularly keratomalacic CU (P = 0.0052). Large dogs were significantly predisposed to SCCEDs (P = 0.0096) and CLFB (P = 0.0069) (Table 4).
Table 4.
Comparison of CU type by weight category, gender, and neuter status for the 347 dogs diagnosed with a CU by the Ontario Veterinary College Health Sciences Centre Ophthalmology Service between 2011 and 2021.
| Clinical variable | CUa type | Number of CUa cases by type (%) | Total number of CUa type with clinical variable recorded | Odds ratio | 95% CI | P-value |
|---|---|---|---|---|---|---|
| Small dogsb | Simple | 53 (46.1) | 115 | 0.966 | 0.605 to 1.540 | 0.9104 |
| SCCEDsc | 25 (30.9) | 81 | 0.433 | 0.245 to 0.748 | 0.0017 | |
| Complex | 71 (58.2) | 122 | 1.947 | 1.228 to 3.099 | 0.0037 | |
| Deep | 22 (59.5) | 37 | 1.039 | 0.467 to 2.326 | 1.0000 | |
| Keratomalacia | 17 (89.5) | 19 | 6.710 | 1.493 to 62.363 | 0.0052 | |
| Descemetocele | 27 (50.9) | 53 | 0.637 | 0.296 to 1.361 | 0.2154 | |
| CLFBf | 5 (38.5) | 13 | 0.457 | 1.113 to 1.626 | 0.2577 | |
| Medium dogsd | Simple | 40 (34.8) | 115 | 1.022 | 0.619 to 1.676 | 1.0000 |
| SCCEDsc | 33 (40.7) | 81 | 1.417 | 0.823 to 2.420 | 0.1865 | |
| Complex | 37 (30.3) | 122 | 0.732 | 0.442 to 1.202 | 0.2360 | |
| Deep | 12 (32.4) | 37 | 1.125 | 0.451 to 2.708 | 0.8349 | |
| Keratomalacia | 1 (5.3) | 19 | 0.253 | 0.027 to 1.150 | 0.0620 | |
| Descemetocele | 20 (37.7) | 53 | 1.742 | 0.760 to 4.037 | 0.1752 | |
| CLFBf | 3 (23.1) | 13 | 0.692 | 0.117 to 2.843 | 0.7569 | |
| Large dogse | Simple | 22 (19.1) | 115 | 1.068 | 0.567 to 1.973 | 0.8819 |
| SCCEDsc | 23 (28.4) | 81 | 2.186 | 1.150 to 4.104 | 0.0096 | |
| Complex | 14 (11.5) | 122 | 0.437 | 0.211 to 0.854 | 0.0122 | |
| Deep | 3 (8.1) | 37 | 0.591 | 0.100 to 2.415 | 0.5497 | |
| Keratomalacia | 0 (0) | 19 | 0.261* | 0 to 1.299 | 0.1282 | |
| Descemetocele | 6 (11.3) | 53 | 0.948 | 0.255 to 3.338 | 1.0000 | |
| CLFBf | 5 (38.5) | 13 | 6.686 | 1.450 to 28.769 | 0.0069 | |
| Female | Simple | 52 (41.6) | 125 | 1.045 | 0.652 to 1.669 | 0.9355 |
| SCCEDsc | 35 (39.8) | 88 | 0.938 | 0.553 to 1.578 | 0.9009 | |
| Complex | 55 (41) | 134 | 1.008 | 0.634 to 1.601 | 1.0000 | |
| Deep | 19 (46.3) | 41 | 1.364 | 0.606 to 3.061 | 0.4491 | |
| Keratomalacia | 6 (30) | 20 | 0.571 | 0.167 to 1.723 | 0.3308 | |
| Descemetocele | 25 (42.4) | 59 | 1.102 | 0.520 to 2.333 | 0.8601 | |
| CLFBf | 5 (35.7) | 14 | 0.779 | 0.193 to 2.777 | 0.7787 | |
| Intact | Simple | 17 (13.6) | 125 | 0.970 | 0.480 to 1.905 | 1.0000 |
| SCCEDsc | 9 (10.2) | 88 | 0.643 | 0.262 to 1.429 | 0.3403 | |
| Complex | 22 (16.4) | 134 | 1.411 | 0.725 to 2.729 | 0.3434 | |
| Deep | 6 (14.6) | 41 | 0.826 | 0.243 to 2.465 | 0.8044 | |
| Keratomalacia | 0 (0) | 20 | 0.152* | 0 to 0.735 | 0.0436 | |
| Descemetocele | 9 (15.3) | 59 | 0.859 | 0.298 to 2.380 | 0.8172 | |
| CLFBf | 7 (50) | 14 | 6.844 | 1.782 to 26.645 | 0.0021 |
CU — Corneal ulceration.
Small dogs — ≤ 10 kg body weight.
SCCEDs — Spontaneous chronic corneal epithelial defects.
Medium dogs — 10.1 to 30 kg body weight.
Large dogs — > 30 kg body weight.
CLFB — Corneal laceration and foreign bodies.
Indicates a median unbiased estimate and a one-sided P-value due to small sample size.
No significant relationship was determined between the proportion of females to males, and proportion of intact dogs when comparing the CU and NCU populations (Table 1). Intact dogs were more likely to have CLFB (P = 0.0021) (Table 4). Each additional year of age increased the odds of CU by 8.9%, in comparison to the NCU population (95% CI: 1.054 to 1.124, P < 0.0001). When comparing age by CU type, older dogs were more likely to be diagnosed with SCCEDs (OR: 1.098; 95% CI: 0.855 to 0.971, P = 0.0040) and keratomalacia (OR: 1.139, 95% CI: 0.783 to 0.984, P = 0.0257), whereas younger dogs were more likely to have a CLFB (OR: 0.727; 95% CI: 0.607 to 0.869, P = 0.0005).
Dogs with no comorbidities (P < 0.0001), and those with ocular comorbidities (P = 0.0021), were at increased odds of diagnosis with a complex CU, compared to simple ulcers or SCCEDs (Table 5). Ocular comorbidities recorded included keratoconjunctivitis sicca (KCS), eyelid abnormalities, diseases of the nictitating membrane, cilia abnormalities, corneal degeneration and dystrophy, and blindness (Table 5). Concurrent systemic diseases reported included hypothyroidism, hyperadrenocorticism, diabetes mellitus (DM), and neurological conditions (Table 5). Dogs with a concurrent systemic disease or both ocular and systemic disease were not significantly predisposed to any CU type (Table 5). Diabetes mellitus was associated with an increased odds of diagnosis with SCCEDs (OR: 3.559, 95% CI: 0.053 to 0.942, P = 0.0318). Entropion was also statistically significant in regard to odds of SCCEDs diagnosis (OR: 7.246, 95% CI: 0.003 to 0.888, P = 0.0345); however, this finding is likely not clinically significant as only one dog diagnosed with a SCCED also had entropion, and in this case the entropion did not correlate with the location of the CU. Dogs with entropion had an increased odds of diagnosis with complex CU (OR: 4.016, 95% CI: 0.046 to 0.877, P = 0.0199). No other significant associations were identified for individual comorbidities. Dogs diagnosed with a comorbidity were at increased odds of repeat CU during the study period (OR: 5.225, 95% CI: 1.598 to 27.080, P = 0.0024); however, comorbidities were not associated with bilateral CU (P = 0.0745). Small dogs with a comorbidity of any type, were at 9.022 greater odds (95% CI: 1.225 to 403.979, P = 0.0230) of being diagnosed with keratomalacia.
Table 5.
Distribution of corneal ulceration type of the 347 dogs presenting to Ontario Veterinary College for the first time between 2011 and 2021 by comorbidities.
| Comorbidity type | Ulcer type | Number of CUa cases in category (%) | Total number of CUa type | Odds ratio | 95% CI | P-value |
|---|---|---|---|---|---|---|
| No comorbidity | Simple | 12 (9.6) | 125 | 0.209 | 0.098 to 0.411 | < 0.0001 |
| SCCEDsb | 25 (28.4) | 88 | 1.260 | 0.698 to 2.234 | 0.4767 | |
| Complex | 50 (37.3) | 134 | 2.822 | 1.669 to 4.811 | < 0.0001 | |
| Deep | 10 (24.4) | 41 | 0.430 | 0.168 to 1.031 | 0.0524 | |
| Keratomalacia | 6 (30) | 20 | 0.684 | 0.200 to 2.070 | 0.6175 | |
| Descemetocele | 21 (35.6) | 59 | 0.877 | 0.405 to 1.882 | 0.7235 | |
| CLFBc | 13 (92.9) | 14 | 28.494 | 4.010 to > 999.999 | < 0.0001 | |
| Ocular comorbidityd | Simple | 81 (64.8) | 125 | 0.371 | 0.229 to 0.598 | < 0.0001 |
| SCCEDsb | 38 (43.2) | 88 | 1.388 | 0.830 to 2.334 | 0.2173 | |
| Complex | 51 (38.1) | 134 | 1.992 | 1.256 to 3.179 | 0.0021 | |
| Deep | 19 (46.3) | 41 | 1.640 | 0.725 to 3.709 | 0.2467 | |
| Keratomalacia | 5 (25) | 20 | 1.573 | 0.520 to 5.374 | 0.4611 | |
| Descemetocele | 26 (44.1) | 59 | 0.675 | 0.315 to 1.440 | 0.2886 | |
| CLFBc | 1 (7.1) | 14 | 0.109 | 0.002 to 0.770 | 0.0170 | |
| Systemic comorbiditye | Simple | 3 (2.4) | 125 | 2.319 | 0.609 to 13.054 | 0.2725 |
| SCCEDsb | 6 (6.8) | 88 | 0.493 | 0.151 to 1.737 | 0.2230 | |
| Complex | 6 (4.5) | 134 | 0.941 | 0.291 to 3.294 | 1.0000 | |
| Deep | 1 (2.4) | 41 | 2.261 | 0.242 to 110.141 | 0.6665 | |
| Keratomalacia | 1 (5) | 20 | 0.872 | 0.090 to 43.365 | 1.0000 | |
| Descemetocele | 4 (6.8) | 59 | 0.379 | 0.033 to 2.756 | 0.4045 | |
| CLFBc | 0 (0) | 14 | 0.973* | 0.173 to infinity | 0.6283 | |
| Ocular and systemic comorbidity | Simple | 29 (23.2) | 125 | 0.866 | 0.496 to 1.527 | 0.6838 |
| SCCEDsb | 19 (21.6) | 88 | 1.002 | 0.541 to 1.915 | 1.0000 | |
| Complex | 27 (20.1) | 134 | 1.152 | 0.659 to 2.045 | 0.6881 | |
| Deep | 11 (26.8) | 41 | 0.569 | 0.218 to 1.523 | 0.2437 | |
| Keratomalacia | 8 (40) | 20 | 0.303 | 0.098 to 0.977 | 0.0301 | |
| Descemetocele | 8 (13.6) | 59 | 2.151 | 0.813 to 6.197 | 0.1284 | |
| CLFBc | 0 (0) | 14 | 5.576* | 1.134 to infinity | 0.0719 |
CU — Corneal ulceration.
SCCEDs — Spontaneous chronic corneal epithelial defects.
CLFB — Corneal laceration and foreign bodies.
Ocular comorbidities included keratoconjunctivitis sicca (KCS), eyelid abnormalities, diseases of the nictitating membrane, cilia abnormalities, corneal degeneration and dystrophy and blindness.
Systemic comorbidities included hypothyroidism, hyperadrenocorticism, diabetes mellitus (DM), and neurological conditions.
Indicates a median unbiased estimate and a one-sided P-value due to small sample size.
The multivariate model revealed several significant risk factors. For the overall risk of CU, skull type and age were the only significant factors. Brachycephalics were at increased odds of CU compared to mesaticephalics (OR: 3.084, 95% CI: 2.209 to 4.306, P < 0.0001) and dolichocephalics (OR 3.514, 95% CI: 2.133 to 5.790, P < 0.0001). Yearly increase in age also augmented the risk of CU (OR: 1.114, 95% CI: 1.075 to 1.156, P < 0.0001). For the risk of different CU types, brachycephalic skull conformation was associated with reduced odds of simple CU compared to mesaticephalic (OR: 0.401, 95% CI: 0.230 to 0.701, P = 0.0030) and dolichocephalic conformation (OR: 0.357, 95% CI: 0.151 to 0.843, P = 0.0030). Increased age also significantly reduced the odds of a simple CU (OR: 0.935, 95% CI: 0.879 to 0.995, P = 0.0354). Both increase in age (OR: 1.183, 95% CI: 1.094 to 1.280, P < 0.0001) and body weight (OR: 1.045, 95% CI: 1.023 to 1.068, P < 0.0001) augmented the odds of SCCEDs. Brachycephalics were associated with increased odds of complex CU compared to mesaticephalics (OR: 2.424, 95% CI: 1.447 to 4.063, P = 0.0008). Decreasing body weight was associated with complex CU diagnosis (OR: 1.043, 95% CI: 0.939 to 0.979, P < 0.0001). The shih tzu breed was not significant in the multivariate model when comparing overall risk of CU or CU type.
Discussion
This is the first study to investigate the complexity of CU type in relation to breed, skull conformation, weight, sex, neuter status, age, and presence of comorbidities with a large sample size. Complex CU were the most common within our study population. This result is difficult to compare to the existing literature since there are no previous studies investigating CU by complexity. In the present study, a higher proportion of superficial ulcers (simple and SCCEDs combined) (61.4%) was seen compared with the studies by Iwashita et al (32.4%) and Kim et al (44%) (25,29). Furthermore, 14.1% of our population had bilateral CU, which contrasts with previously reported studies of 5.8% (1), 12.1% (2), and 53.8% (3). Most (87.4%) dogs had only one diagnosis of CU over the study period, which is consistent with a previous study (1).
The shih tzu breed was significantly overrepresented in the present study, in every category of CU, except for SCCEDs (Table 2). This result was consistent with a previous study (29) that identified the shih tzu as the most prevalent breed, and supported other studies, which reported the shih tzu as a commonly affected breed (1,18,23,25). In particular, a significant association was identified between the shih tzu breed and keratomalacia which, to the best of our knowledge, has only previously been reported as an abstract (28). This important finding can help veterinarians plan CU treatment options for this breed. However, to fully assess the significance of the shih tzu breed’s apparent predisposition to CU, analysis of other potential contributing factors including owner socioeconomic status should be evaluated. Although these data were not available in the present study, further investigation is warranted in future studies. In our study, the boxer was the most common breed in the SCCEDs category, which is consistent with previous investigations (5,6,8,15,16). In contrast, one SCCEDs study revealed the Pembroke Welsh corgi, French bulldog, and Boston terrier to be more commonly affected than boxers (25), and another study indicated that mixed-breed dogs were the most common breed (7).
Previous literature demonstrated that brachycephalic breeds are overrepresented in cases of CU (5,10,19,20,25,31,32). One study reported that brachycephalics were 20 times more likely to be affected than non-brachycephalics (21). In our study, brachycephalics were only 2.76 times (P < 0.0001) more likely to have a CU diagnosis relative to non-brachycephalic breeds; this difference in results could be due to sample size as our study had 347 dogs with CU, compared with 31 (21). Furthermore, our study demonstrates that brachycephalics are more likely to have a diagnosis of complex CU (P < 0.0001), particularly descemetoceles (P = 0.0055) (Table 3). This finding is mirrored in other studies which revealed brachycephalic breeds are overrepresented with deeper CU (25) and with full-thickness corneal defects requiring conjunctival grafts (20). In contrast, mesaticephalic breeds represented 50% of all simple CU diagnoses (P = 0.0014) (Table 3). This result is comparable to a recent study of CU depth, in which non-brachycephalic breeds were more likely to have superficial CU than brachycephalic breeds (25). A potential hypothesis for this result is that brachycephalic breeds are more likely to have progressed to a complex CU by the point of referral. Brachycephalic breeds have reduced corneal sensation compared to mesaticephalic and dolichocephalic breeds (1,21,26). This reduced corneal sensation can result in decreased corneal protective mechanisms and diminished clinical signs, which may delay referral until severe lesions are noted (2,18,21,25).
In our study, dolichocephalic breeds were under-represented in all categories of CU. Previous investigations have not separated dolichocephalic breeds from mesaticephalics, instead comparing brachycephalic and non-brachycephalic breeds (19,21,23–25). Our study provides further insight into the relationship between skull conformation and complexity of CU. Interestingly, dolichocephalic skull conformation was associated with an increased risk of bilateral presentation. All dolichocephalic dogs with bilateral CU also had a comorbidity (75% ocular, 25% ocular and systemic), which likely accounts for this unexpected finding. Skull conformation did not predispose to having repeat visits.
The mean weight of dogs diagnosed with CU was higher than previously reported (1,21). This increase could be attributed to the higher proportion of dogs referred for SCCEDs, which are often associated with larger breeds such as boxers and retrievers (5,7,8). Smaller dogs (< 10 kg) were significantly overrepresented for complex CU, specifically with keratomalacia (P = 0.0052) (Table 4). This association between small body weight and more complex CU is a new finding, not previously reported. This may be a reflection that popular small breed dogs are brachycephalic. Furthermore, brachycephalic breeds are at an increased risk of having ocular comorbidities due to skull conformation. Of these comorbidities, our study demonstrated only an association between entropion and complex CU; however, a previous study indicated that comorbidities are all recognized risk factors for development of CU and can complicate healing of an existing CU (23).
Results of the present study show that sex was not a risk factor for CU diagnosis or specific CU type. Intact animals were not at an increased overall risk of CU; however, they were significantly more likely to be diagnosed with a CLFB (P = 0.0021) (Table 4). This result is difficult to compare, as previous literature has not studied neuter status in relation to CU complexity. Although most previous studies did not individualize each type of CU, our overall demographics for all ulcer types (40.9% females, 13.8% intact) is generally consistent with previously published data (3,12,20). Certain values did contrast with previous investigations reporting a higher proportion of males (71%) or higher proportion of intact animals (80.8 to 96%) (12,20). This may be due to our individual study population having a higher proportion of spayed or neutered animals compared to previous studies (33). This previously reported higher proportion of male and intact animals could also be affected by a smaller sample size compared with our study (8,20,22).
The average age at diagnosis for our CU population was significantly higher (8.0 y) than in many previous studies (2,3,12,20,21). One study had a similar overall mean age of 8.3 y in their referred cases and another study reported a median age of 7.2 y derived from a population of dogs seen at primary care facilities (1,25). Other studies, more specific to SCCEDs, have reported a similar mean age to our findings (7,8). The association between increased age and complex CU, was consistent with a previous study that demonstrated a significant proportion of older dogs with deeper CU (25). This finding could be linked to age-related changes in the ocular surface, including altered tear film composition and reduced lacrimal secretions (6,34,35).
As hypothesized, dogs with ocular comorbidities were significantly more likely to be diagnosed with a complex CU (Table 5). Interestingly, having no comorbidities was also significantly associated with complex CU. This finding potentially reflects that some complex CU have an acute or traumatic etiology, as opposed to CU progression due to underlying comorbidities. In addition, as we analyzed a referral population, it is possible that the keratomalacia was too advanced to identify prior ocular disease. This would potentially skew our data towards a high proportion of CU with keratomalacia with no concurrent comorbidity. Diabetes mellitus was associated with an increased odds of SCCEDs and this could be due to a reduced tear production and quality, which in turn impairs corneal wound healing (5,13). Entropion was the only individual significant ocular comorbidity, which was surprising as KCS and cilia abnormalities were expected to predispose to more severe types of CU, especially in our small brachycephalics. Although these expected individual correlations were not identified within our data, a significant finding was that small dogs with a comorbidity of any type, were at 9.022 greater odds (95% CI: 1.225 to 403.979, P = 0.0230) of a diagnosis of keratomalacia. In addition, all dogs with comorbidities were at 5.225 times increased odds (P = 0.0024) of repeat CU diagnosis during the study period. Although prior studies have reported on the percentage of dogs with repeated CU (1), this finding has not previously been correlated with comorbidities as demonstrated in our study.
A potential limitation of the present study was that the referral population may have resulted in selection bias towards dogs with more complex lesions. However, a full range of CU complexities were included in the study, and the proportion of simple CU (36%) compared to complex CU (38.6%) was very similar. Therefore, this study likely still reflects the general canine population. In addition, the study provides useful information for the general practitioner, such as highlighting that earlier referral may be warranted for small breed, aged, or brachycephalic dogs at risk of a complex CU. The retrospective nature of the study did impose reliance on the accuracy of the medical records for complete and factual information. For example, determination of skull type was based on breed and photographs rather than exact cranio-facial dimensions. The dogs were categorized based on best judgement and current literature (1,21,25,27,30); however, breeds can have variability in their skull shape (30) and this may have yielded some inconsistent data, most likely in the brachycephalic versus mesaticephalic skull shapes.
In conclusion, CU is a painful condition that threatens the globe’s integrity. Recognition of at-risk canine demographics, as well as potential contributing comorbidities, is essential to minimize complications of CU. The results of our study established that the shih tzu breed, brachycephalic dogs of all weights, small dogs, and increasing age significantly increased the odds of a diagnosis of CU; in particular complex ulcers. Ocular comorbidities were associated with an increased risk of a complex CU, and the presence of a comorbidity increased the odds of a repeat CU diagnosis. This information will help clinicians formulate treatment plans for dogs fitting these demographics. CVJ
Footnotes
Use of this article is limited to a single copy for personal study. Anyone interested in obtaining reprints should contact the CVMA office (hbroughton@cvma-acmv.org) for additional copies or permission to use this material elsewhere.
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