Corneal diseases are common in horses and may lead to blindness.1 Horses with infectious ulcerative keratitis and stromal abscesses, for example, present frequently to veterinarians for intensive therapy to prevent vision and globe loss.1–4 Infectious ulcerative keratitis and stromal abscesses in horses are most commonly treated with a combination of medical and surgical therapies.1,4,5 Surgical intervention is typically warranted when there is disease progression despite medical treatment or when the lesion is deep and threatening perforation.1,4 However, because of disease-related corneal opacity, it may be difficult to accurately determine the depth of the lesion and the severity of inflammation in the cornea and inside of the eye, both of which may be important parameters to determine the extent and progression of the disease and if surgical intervention is indicated.6,7
Advanced imaging of the cornea and anterior segment of the eye in horses may provide additional information to assist in treatment decisions, beyond what is provided by ocular examination alone.6–9 Anterior segment optical coherence tomography (OCT) imaging was recently described in horses with corneal disease.9 In this study, light penetration was impaired, especially in the central aspect of opaque corneal lesions, which compromised the quality and diagnostic utility of the OCT images. High-frequency ultrasound is a practical advanced imaging technique that can be used to evaluate the cornea as well as the presence of cells, hyphema, fibrin, or exudate in the anterior segment of the eye.7 High-frequency ultrasound tissue penetration is 5 to 10 mm making this tool ideal for anterior segment examination of the eye.7,10–13 Specifically, high-frequency ultrasound biomicroscopy (UBM) allows for noninvasive visualization of tissue at resolutions of 20 to 80 μm, similar to a low-power histologic view.6–8,10,14 Unlike slit lamp biomicroscopy and OCT, UBM can be useful when ocular structures are obscured by opacities in the cornea or anterior segment of the eye.6,10
Ultrasound biomicroscopy of corneal disease may be important for determining treatment options, surgical planning, and prognosis.8 Its clinical use has included visualization of neoplasia, inflammatory lesions, intraocular trauma, intraocular lens placement, iridocorneal angle, glaucomatous changes, uveal cysts, and other corneal diseases.8,10,14–16 Reports of use in equine patients are currently limited to corneal thickness and anterior chamber depth measurements in normal equine patients.13,17 Thus, correlation of UBM findings, such as corneal thickness, depth of lesion, Descemet membrane disruption (DMD), or aqueous humor cellular infiltrate, to disease outcome and prognosis may provide clinicians with additional information to help guide treatment decisions in horses with corneal disease. Therefore, the purpose of this study was to evaluate UBM parameters of equine corneal disease and determine if they have a predictive value for treatment and prognosis.
Methods
This is a retrospective study. Records from horses with infectious ulcerative keratitis or stromal abscesses that presented for evaluation at the North Carolina State University College of Veterinary Medicine Equine Ophthalmology Service between 2019 and 2023 were evaluated. Stromal abscesses were defined as a focal yellow-to-white opacity located in the corneal stroma with an intact corneal epithelial surface. The corneal epithelial surface was not intact in infectious ulcerative keratitis. Inclusion criteria included a complete ophthalmic examination, with slit-lamp biomicroscopy (SL-17; KOWA), intraocular pressure measurements (TONO-PEN AVIA VET; Reichert Technologies), indirect ophthalmoscopy following pupillary dilation with 1% tropicamide ophthalmic solution (Akorn Inc), and UBM imaging. Collected case information included date of presentation, signalment, eye affected, ophthalmic exam abnormalities, aqueous flare score, aqueous cell score, size of the lesion (largest diameter) on ophthalmic exam, clinical diagnosis, date UBM was performed, corneal cytology results, aerobic (5% blood; Remel; Columbia) and fungal (Sabouraud dextrose agar with chloramphenicol; Hardy Ox) culture results, topical eye medications and oral medications administered at the time of UBM imaging, type of surgery performed, histopathology, and outcome (healed or enucleation).
Ultrasound biomicroscopy
Ultrasound biomicroscopy was performed on all horses as previously described.6,7,13,17 Imaging was performed using a 70-mHz linear transducer (VevoMD; UHF70; VisualSonics) under arterial settings. Before UBM imaging, horses were tranquilized intravenously with detomidine HCl (0.01 to 0.02 mg/kg, 10 mg/mL; Orion), and a palpebral nerve block was performed (1 mL lidocaine HCl; Covetris). The eyelids were manually retracted and topical anesthesia (0.5% proparacaine hydrochloride ophthalmic solution USP; ALCON Laboratories Inc) was applied to the cornea. Artificial tear gel (Optixcare; CLC MEDICA) was used as the coupling agent on the ultrasound probe. Transcorneal ultrasonography was performed with the position of the probe perpendicular (with the probe oriented horizontally and then vertically) to the cornea. The frequency for all images collected was set at 29 to 71 MHz with a focus of 2.9 mm and a depth of 6.5 mm.
Three representative UBM images of the corneal lesion were collected for each horse. A representative image included corneal epithelium, corneal stroma, Descemet membrane, corneal endothelium, corneal lesion, and appropriate visualization of the anterior chamber. For each image, corneal thickness, depth of lesion, presence of DMD, and aqueous humor cell count (AHCC) were examined. The DMD was defined as the inability to visualize the Descemet membrane, a distinct hyperechogenic line in the posterior cornea, in the affected area. Corneal thickness was measured with the ultrasound’s instrumental internal caliper from the external aspect of the corneal epithelium to the inner aspect of the Descemet/endothelial layer. A measurement was performed per each representative image, and 3 measurements were averaged. The depth of the corneal lesion was graded as superficial (< 50% depth) or deep (> 50% depth).
Ultrasound biomicroscopy AHCC with ImageJ analysis
To determine AHCC on UBM images, ImageJ win-64 (Fiji; ImageJ 1.53 t, Java 1.8.0; National Institute of Health) was used. The first step was to convert the RGB image captured by UBM into an 8-bit format (Image → Type → 8 bit). A rectangular box with a width of 3.50 pixels and a height of 1.50 pixels was placed over the region of interest within the anterior chamber (Figures 1–3). The region of interest was defined as the area with the most visible aqueous humor cells devoid of noise artifacts. The image was then cropped to the region of interest, and the threshold (Image Adjust → Threshold) was adjusted to remove noise and brighten the cells. The image was then made binary to separate the cells from the background (Process → Binary → Make Binary), and the cell color was changed from white to black on a white background (Process → Binary → Convert to Mask). Cells that were clumped together were split using the watershed tool (Process → Binary → Watershed), and the cell count was calculated (Analyze → Analyze Particles). The AHCC was repeated for 3 representative images, and the average was calculated.
Superficial and deep corneal lesions on ultrasound biomicroscopy (UBM). A—A 13-year-old Oldenburg mare was diagnosed with superficial ulcerative fungal keratitis in the right eye. On UBM, the lesion was superficial (< 50%) with a mean aqueous humor cell count of 17.0 cells in the region of interest. B—A 17-year-old Warmblood gelding was diagnosed with superficial ulcerative fungal keratitis in the left eye. On UBM, the lesion was deep (> 50%) with a mean aqueous humor cell count of 47.0 cells in the region of interest. On the UBM images, the corneal epithelium (red arrow), Descemet membrane (white arrow), corneal lesion (yellow star), and region of interest (white box) are labeled.
Citation: Journal of the American Veterinary Medical Association 262, S2; 10.2460/javma.24.02.0097
Intact and Descemet membrane disruption on ultrasound biomicroscopy (UBM). A—15-year-old Quarter Horse gelding was diagnosed with a superficial stromal abscess in the right eye. On UBM, the Descemet membrane was intact, and the mean aqueous humor cell count was 10.0 cells in the region of interest. B—A 27-year-old Arabian mare was diagnosed with a deep stromal abscess in the right eye. On UBM, there was a break in the Descemet membrane (blue arrow), and the mean aqueous humor cell count was 11.0 cells in the region of interest. On the UBM images, the corneal epithelium (red arrow), Descemet membrane (white arrow), corneal lesion (yellow star), and region of interest (white box) are labeled.
Citation: Journal of the American Veterinary Medical Association 262, S2; 10.2460/javma.24.02.0097
Low and high aqueous humor cell count (AHCC) on ultrasound biomicroscopy (UBM). A—A 6-year-old Thoroughbred gelding was diagnosed with superficial ulcerative fungal keratitis in the left eye. On UBM, the mean AHCC was 3.0 cells in the region of interest. B—A 21-year-old Arabian gelding was diagnosed with a deep stromal abscess in the left eye. On UBM, the mean AHCC was greater than 300 cells in the region of interest. On the UBM images, the corneal epithelium (red arrow), Descemet membrane (white arrow), corneal lesion (yellow star), and region of interest (white box) are labeled.
Citation: Journal of the American Veterinary Medical Association 262, S2; 10.2460/javma.24.02.0097
Statistical analysis
One-way ANOVA was used to compare mean UBM AHCC with other UBM parameters (ie, depth of lesion and DMD) and clinical findings (ie, infection type, clinical diagnosis, treatments, and outcome). Pairwise analysis with a t test or pooled t test was used for multiple comparisons. Regression and bivariant fit of mean UBM AHCC by the size of the lesion (mm), aqueous flare, and aqueous cells on the ophthalmic exam and average corneal thickness (mm) were compared. Finally, the Fisher exact test was used to compare both DMD and outcome, depth of lesion and outcome, clinical diagnosis and outcome, and infection type and outcome. Differences were considered significant at P ≤ .05, and all probabilities and results were calculated using computerized statistical software (JMP Pro, v. 15.0; SAS). Data are presented as mean ± SD. Comparisons are outlined (Supplementary Tables S1 and S2).
Results
Case information and outcomes
There were 46 horses included in the study (28 geldings, 18 mares) with a clinical diagnosis of either infectious ulcerative keratitis (n = 25/46) or stromal abscess (21/46). There were 23 right and 23 left eyes. The mean age of the horses was 16.3 ± 6.3 years. The breed of horse varied from the Quarter Horse (n = 7), Paint (6), Thoroughbred (5), unspecified Warmblood (4), Oldenburg (3), Tennessee Walking (3), Arabian (3), Spotted Saddle (2), Pony (2), unknown breed (2), and 1 each of Irish Sport Horse, Haflinger, Percheron, Morgan, German Riding, Hackney, Holsteiner, Saddlebred, and Appaloosa.
On ophthalmic examination, clinical scores for aqueous flare and aqueous cells were performed by a clinician in 96% of horses (n = 44/46). The remaining 2 horses had severe corneal edema that prevented visualization into the anterior chamber. Clinical scores for aqueous flare were scored as a 0 (n = 10/44), 0.5 (4/44), 1 (15/44), 2 (10/44), 3 (5/44), or a 4 (0/44). The same scale was used for scoring aqueous cells as a 0 (n = 23/44), 0.5 (3/44), 1 (7/44), 2 (9/44), 3 (1/44), or a 4 (1/44).
Samples for cytology, culture, or histopathology were taken in 82.6% of horses (n = 38/46). Infectious agents were identified in 76.3% of cases (n = 29/38): 10.3% were bacterial (3/29), 69.0% were fungal (20/29), and 20.7% were a combination of bacterial and fungal organisms (6/29). There was a range of bacterial (ie, Streptococcus equi zooepidemicus, Moraxella osloensis, Staphylococcus epidermidis) and fungal (Fusarium spp, Aspergillus spp, and Trichophyton spp) species isolated on culture. Eight stromal abscess cases were not sampled and did not have surgical corneal samples submitted for histopathology (n = 8/46).
Topical eye and oral medications administered at the time of UBM were prescribed by a referring veterinarian or an in-hospital clinician depending on the date of imaging. These medications included a range of topical antibiotics (n = 44/46; 0.3% ofloxacin, 3.3% cefazolin, 0.5% moxifloxacin, 0.3% tobramycin, oxytetracycline, neomycin and polymyxin b sulfates and bacitracin zinc, chloramphenicol, and unknown), topical antifungals (31/46; 1% voriconazole miconazole and 1% luliconazole), topical anti-inflammatories (5/46; 0.1% diclofenac, 0.09% bromfenac, 0.03% flurbiprofen, 1% prednisolone acetate, and unknown), a topical mydriatic agent (28/46; 1% atropine sulfate), topical autologous serum (6/46), 1% EDTA (1/46), oral NSAIDs (36/46; flunixin meglumine and phenylbutazone), oral antifungals (2/26; fluconazole), oral gastrointestinal protectants (19/46; omeprazole), and oral antibiotics (4/46; trimethoprim sulfamethoxazole). A few horses were presented with no oral (n = 6/46) or topical eye medications (5/46) at the time of UBM.
Overall, 76.1% of horses (n = 35/46) healed their corneal lesion, either with medical (topical eye and oral medications) or a combination of medical and surgical therapy, while 23.9% of horses (11/46) were enucleated. Medical therapy was performed on all horses (n = 46/46), and 43.5% of horses (20/46) were treated medically alone without surgical intervention. Of these horses, 50.0% (10/20) were enucleated. Horses with a clinical diagnosis of ulcerative keratitis (n = 25/46) were significantly more likely to heal their corneal lesion compared to those with a stromal abscess (P = .042). Intrastromal injection of 1% voriconazole was performed in 6.5% of horses (n = 3/46). One horse received 3 injections but was unresponsive and later enucleated. The second horse underwent surgical therapy (penetrating keratoplasty with conjunctival graft) in addition to medical therapy and healed its corneal lesion. The last horse received 1 intrastromal injection of 1% voriconazole and 0.5% moxifloxacin, as well as subconjunctival 0.05% amphotericin B injections that then healed with continued medical therapy. Subconjunctival 0.05% amphotericin B injections were administered alone in 10.9% of horses (n = 5/46). Forty percent of horses healed their corneal lesion with continued medical therapy (n = 2/5). Twenty percent of horses healed their corneal lesion with surgical therapy (penetrating keratoplasty with conjunctival graft) in addition to medical therapy (n = 1/5), and the remaining 40.0% of horses were later enucleated (2/5).
Surgical procedures (other than enucleations) were performed in 56.5% of horses (n = 26/46) and included superficial keratectomy (11/26), keratectomy with conjunctival graft (5/26), and penetrating keratoplasty with conjunctival graft (10/26). Corneal lesions were healed in 96.2% (n = 25/26) of these horses, while only 1 was enucleated due to a failed keratectomy with conjunctival graft. In the healed group, 1 horse had a superficial keratectomy and then later underwent a penetrating keratoplasty with a conjunctival graft due to worsening disease. Horses that were confirmed to have a fungal infection were significantly more likely to heal their corneal lesion (P = .011), of which 95% of cases underwent surgical therapy (n = 19/20).
Size of lesion, corneal thickness, and depth of lesion
The largest diameter (mm) or size of the lesion measured on ophthalmic examination ranged from 1 to 10 mm. The mean (± SD) diameter of the corneal lesions was 6.9 ± 4.3 mm. Corneal thickness (mm) measured on UBM ranged from 0.8 and 2.9 mm. The mean (± SD) UBM corneal thickness was 1.5 ± 0.4 mm. There was no significant difference between the diameter of the lesion or corneal thickness and outcome. Horses had a deep corneal lesion on UBM in 69.6% of cases (n = 32/46), while the remaining 30.4% had a superficial corneal lesion (14/46; Figure 1). Eyes with deep corneal lesions were significantly more likely to have an outcome of enucleation compared to superficial lesions (P = .015; Supplementary Table S1). There was no significant association between the depth of the lesion and with overall diameter of the lesion or corneal thickness. Finally, there were no significant associations between the diameter of the lesion, corneal thickness, or depth of the lesion with topical eye or oral medications used before UBM.
Descemet membrane disruption
On UBM, DMD was visualized as a discontinuity of the hyper-echogenic line at the posterior cornea (Figure 2) and recognized in 39.1% of the horses (n = 18/46). Eyes with DMD were significantly more likely to have an outcome of enucleation compared to eyes without DMD (P = .032; Supplementary Table S2). Also, as expected, eyes with deep corneal lesions were significantly more likely to have DMD (P ≤ .001). There was no significant correlation between the presence of DMD and the diameter of the lesion or corneal thickness and no significant association between the presence of DMD and the use of any topical eye or oral medications before UBM.
Aqueous humor cell counts
UBM images were used to calculate AHCC (Figure 3). Comparisons of AHCC among UBM and clinical variables are presented (Supplementary Table S3). The AHCC ranged from 0 to 300 cells. The mean (± SD) AHCC for all cases was 56.0 ± 82.5 cells. With increasing aqueous flare and cell clinical scores, a trend toward higher AHCC measured on UBM was noted. However, statistically, there was no significant correlation between aqueous flare clinical scores and AHCC. Statistics were unable to be performed with clinical aqueous cell scores due to the low sample size for aqueous cell scores of 3 (n = 1) and 4 (1). Neither aqueous flare nor aqueous cell clinical scores had a significant correlation to the outcome (healed vs enucleation).
There was no association between the clinical diagnosis of stromal abscess or ulcerative keratitis and AHCC. There was also no association between the presence of an infection or infection type verified on cytology, culture, or histopathology (ie, bacterial or fungal) and AHCC. Horses treated with systemic antibiotics at the time of UBM had significantly lower AHCC than those compared to horses not treated with systemic antibiotics (P = .003). On the other hand, there were no significant differences in AHCC in eyes treated with or without topical antibiotics, topical antifungals, topical atropine, topical NSAIDs, topical corticosteroids, systemic antifungals, or systemic NSAIDs at the time of UBM.
Increasing diameter (size) of the lesion was significantly correlated with higher AHCC (P ≤ .001). Deep corneal lesions had significantly higher AHCC (mean ± SD; 71.6 ± 91.3 cells) compared to superficial corneal lesions (15.7 ± 28.9 cells; P = .002). There was no significant correlation between AHCC and corneal thickness or AHCC and DMD.
Eyes that underwent enucleation had a higher AHCC (82.8 ± 101.0 cells) compared to eyes that healed (47.3 ± 75.4 cells), but these differences were not significant (P = .218). Interestingly, eyes that received surgical treatment (other than enucleation) had a significantly higher AHCC than those treated medically alone (P = .013). Taken together, higher AHCC was measured in cases that needed enucleation and in eyes that received surgery.
Discussion
The results of this study suggest that UBM parameters in horses with corneal disease provide valuable clinical data to augment routine clinical examination. Not only is UBM an efficient and safe imaging modality for horses, but parameters such as size and depth of the lesion, overall corneal thickness, presence of DMD, and AHCC can be evaluated accurately and objectively on UBM images. The depth of the lesions, presence of DMD, and presence and estimates of AHCC can be determined in real-time during the UBM examination. The corneal thickness and size of the lesion can be measured on UBM imaging using instrument internal calipers. Objective quantification of AHCC is accomplished with open-access computer software (ImageJ) using the methodology described herein.
Results of this study suggest that increased AHCC correlated with advanced corneal disease, such as those corneal lesions with a larger diameter (size) and a deeper location in the cornea. Furthermore, eyes with deep corneal lesions and those with DMD, as identified on UBM, were significantly more likely to result in enucleation. Conversely, the diameter of the lesion, as determined on ophthalmic examination, and corneal thickness measured by UBM were not associated with the outcome. Together, these results support that eyes with deep corneal lesions (> 50% depth), those with DMD, and eyes with increased AHCC represent poorer prognosis. To prevent loss of the eye, aggressive therapy such as early surgical intervention is warranted in these cases. Additionally, because the central aspects of corneal lesions cannot be visualized by routine slit-lamp biomicroscopy, UBM provides more accurate and reliable information on the depth of corneal lesions and integrity of the Descemet membrane, which likely represents the area of most advanced disease.
Slit-lamp biomicroscopy clinical scoring of aqueous humor flare and cells was only weakly associated with increasing AHCC on UBM and was not associated with outcome. The aqueous flare and cell clinical scores did not follow an increasing trend with increasing grade, and cells on UBM were consistently detected in patients with an aqueous flare and cell clinical score of 0. These discrepancies are most likely from limited visualization into the anterior chamber due to corneal disease (ie, the presence of a plaque, corneal abscess, and corneal edema). Other plausible causes include the subjectivity of the clinicians and environmental lighting. Thus, similar to when assessing the lesion depth and the Descemet membrane integrity, UBM may be a more reliable tool than slit-lamp biomicroscopy when evaluating intraocular inflammation to assess disease severity and predict case outcomes.
An interesting finding was that the use of oral antibiotics at the time of UBM resulted in significantly lower AHCC (compared to horses not receiving systemic antibiotics), a result that was not observed with the use of other medications, including topical and oral anti-inflammatory drugs. This may be coincidental due to a small sample size of data analysis, but possibly the use of systemic antibiotics reduced bacteria in the uveal tract, helped stabilize the blood-ocular barrier, or had a direct anti-inflammatory effect.18–21 There were also limitations in identifying infectious agents, specifically in stromal abscess cases where cytology and culture samples were not taken, the corneal lesion was not isolated on the histopathologic section, or surgical samples were not submitted to histopathology. The oral antibiotics used in the horses of this study included trimethoprim sulfamethoxazole (n = 4), which has been shown to have an immunomodulatory effect.19,20 Although not an objective of this study, our data did not support that any specific medication was associated with outcomes, whether positive or negative. However, nearly all horses in this study were treated with similar treatment regimens before imaging, and no negative treatment control groups were examined since this was a retrospective study.
When deciding on a course of therapy there are many factors to consider other than ophthalmic examination, imaging, and other diagnostic findings, including owner financial constraints, ease of administration of medications and patient compliance, and access to an isolated stall or round pen away from other horses. The decision to enucleate in this study may not have been based solely on medical findings such as a lack of response to therapy. In addition, it is possible that the UBM findings influenced the clinician’s treatment recommendations, such as more aggressive therapy with deeper lesions and those with visibly higher inflammation inside the anterior chamber of the eye. The results of this study reinforce the importance of aggressive therapy; despite high AHCC, surgically treated eyes resulted in a high healing percentage (ie, > 96%), while those that did not receive surgery had a 50% enucleation rate. A finding of a high AHCC, in any case, suggests that surgical treatment should be considered to help prevent the loss of the eye.
Study limitations were centered on the retrospective nature of the study. This study only included corneal disease grouped as infectious ulcerative keratitis or stromal abscess and UBM images were not collected throughout treatment, which should be the emphasis of future studies to monitor the effect of therapeutics over time. Additionally, calculated AHCC within the selected region of interest could be under- or overestimated since cells within the anterior chamber may not be homogenously distributed.
Repeat UBM imaging was not evaluated and is beyond the scope of the study; however, repeated UBM over the course of treatment could assess improvement or worsening of the disease. Prospective studies are needed to assess response to therapy, such as in a horse with high AHCC on UBM, will the use of systemic antibiotics reduce the count on subsequent imaging and improve overall prognosis? Furthermore, repeat UBM imaging in future studies may determine if treatments can reduce the depth of the lesion and allow the DMD to heal. Finally, future studies comparing UBM with a laser flare cell meter or anterior segment fluorophotometry in validating AHCC in horses with corneal disease could be completed. A flare cell meter and anterior segment fluorophotometry are noninvasive and invasive methods, respectively, to assess aqueous flare and cells. While UBM overall is a superior clinical diagnostic tool as several additional clinical parameters (such as depth and presence of DMD) can be assessed, validating UBM AHCC with a flare cell meter and anterior segment fluorophotometry could be completed.
Supplementary Materials
Supplementary materials are posted online at the journal website: avmajournals.avma.org.
Acknowledgments
The authors thank the North Carolina State College of University Ophthalmology Team for their expertise and guidance and the fellow residents who helped perform imaging.
Disclosures
Dr. Gilger served as Guest Editor for this JAVMA Supplemental Issue. He declares that he had no role in the editorial direction of this manuscript. The other authors have declared no conflicting interests.
No AI-assisted technologies were used in the generation of this manuscript.
Funding
The authors have nothing to disclose.
ORCID
B. C. Gilger https://orcid.org/0000-0002-7771-9166
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