Glaucoma is a group of progressive ocular diseases that cause irreversible blindness, resulting from apoptosis of retinal ganglion cells and degeneration of the optic nerve head in animals (8,11). Among the factors associated with glaucoma development, the elevation of the intraocular pressure (IOP) is a strong risk factor in all veterinary species (9,12). Glaucoma can be classified as congenital, primary, or secondary based on the probable cause. Primary glaucoma is attributed to an IOP elevation due to the compromise of aqueous humor outflow through the iridocorneal angle (ICA) and ciliary cleft (CC) without clinically concurrent ocular diseases (11,12). Although primary glaucoma presents as a unilateral condition clinically, it is understood as a bilateral condition in many canine breeds (11). Primary glaucoma can be subdivided into two categories based on gonioscopic morphology of the ICA: open-, closed/narrowed-angle glaucoma (9,11). Primary angle-closure glaucoma (PACG) is the most common form of inherited canine glaucoma (15). In secondary glaucoma, elevation of IOP is initiated by antecedent or concurrent ocular diseases (12).

Regardless of primary or secondary glaucomas, clinicians need to assess the condition of the ICA and CC systematically with gonioscopy and high-resolution ultrasound (HRUS) (1,2). The former can visualize only the most anterior opening of the CC together with the pectinate ligament, namely the ICA, while the latter allows an evaluation of the trabecular meshwork within the CC including ICA (1,3,5,6). The advanced imaging technologies, HRUS, provides detailed cross-sectional views of the eye using a high frequency ranging from 20 to 40 MHz (2). Therefore, HRUS with tissue penetration of approximately 30 mm or less is particularly useful for examining the delicate anterior segment of the eye, such as cornea, anterior chamber, ICA and CC (7,12). Overall, HRUS enhances gonioscopic examinations by providing important information on the entire length of the CC and its structures along with ICA in the clinical management of canine glaucoma (3,10,11). Therefore, the purpose of the study is to report the diagnosis and management for PACG with gonioscopy and HRUS in a Maltipoo dog.

A two-year-old spayed female Maltipoo dog was presented with a two-month duration of glaucoma OD, which had been medically managed with topical antiglaucoma agents. On the first presentation, the menace response and dazzle reflex were absent OD, but present OS. Slit-lamp biomicroscopy (HS-7000^®; Huvitz Co., Ltd., Korea) OD revealed buphthalmia, mild corneal edema, and conjunctival and episcleral hyperemia along with posterior polar lens opacity (Fig. 1). No remarkable abnormalities were noted in the anterior segments OS. Fluorescein staining for corneal ulcerations was negative in both eyes. The IOPs measured by rebound tonometry (TONOVet Plus^®; Icare/Tiolat, Finland) were 70 mmHg OD and 30 mmHg OS. Binocular indirect ophthalmoscopy (Vantage Plus^®; Keeler Instruments Inc., USA) OD showed moderate cupping of the optic nerve head and mild retinal vascular attenuation in conjunction with retinal hyperreflectivity at the superior tapetal area (Fig. 2). In order to reduce the IOP, 20% mannitol (Choongwae 20% mannitol Inj, JW Pharmaceutical Co. LTD, Gwacheon-si, Gyeonggi-do, Korea, 1 g/Kg) was injected intravenously for 20 min and recorded 17 mmHg OD and 15 mmHg OS of IOPs. The ICA viewed by gonioscopy (Koeppe large diagnostic lens; Ocular Instruments Inc., USA) was completely closed by solid sheets of iris-like tissue with a few of flows holes in all four quadrants OD (Fig. 3A). Some abnormally broader and thicker pectinate ligament fibers with normal width of the ICA OS were identified around circumference (Fig. 3B). High-resolution ultrasonography with high-frequency small-footprint linear array transducer of 22 MHz frequency (LOGIQ^TM e; General Electric Healthcare, USA) showed the CC totally collapsed OD (Fig. 4A). This was characterized by a lack of hypoechoic space between the inner and outer leaves of the ciliary body and complete contact of the peripheral iris with the limbal cornea area. Although gonioscopy was relatively normal, HRUS demonstrated similar abnormal findings OS only with a small hypoechoic space within the CC compared to OD (Fig. 4B). Based on the clinical and HRUS findings, a diagnosis of late and early stage of PACG was made in OD and OS, respectively. The owners elected the medial therapy for the glaucoma from a variety of surgical options and medical management.

Figure 1. Clinical appearance of anterior ocular surface viewed by direct diffuse illumination of slit lamp biomicroscopy in both eyes (A, right eye with chronic glaucoma, B, left eye with early glaucoma). (A) Note moderate pupil dilation, larger globe size than that of the left eye, and lens opacity. (B) There are no remarkable abnormalities noted in the anterior segments.

Figure 2. Fundus photographs of both eyes (A, right eye with chronic glaucoma, B, left eye with early glaucoma). (A) There is moderate retinal hyperreflectivity at the superior tapetal area and moderate optic disc cupping with mild retinal vascular attenuation. (B) There are no abnormalities noted in the fundus.

Figure 3. Gonioscopic appearance of both eyes (A, right eye with chronic glaucoma, B, left eye with early glaucoma). (A) Note the iridocorneal angle completely collapsed by solid sheets with some flow holes (arrow). (B) Note some abnormally broader base and thickened pectinate ligament fibers (arrow).

Figure 4. High-resolution ultrasound examination of both eyes (A, right eye with chronic glaucoma, B, left eye with early glaucoma). (A) The ciliary cleft was totally closed between the inner and outer leaves of the ciliary body shown as relatively hyperechoic complex (arrow). (B) The ciliary cleft was narrowed and shown as a small hypoechoic cleft between leaves of the ciliary body (arrow).

Medical management OD was prescribed as 0.005% latanoprost (Xalatan^®; Pfizer Inc., USA, q 12 h), 2% dorzolamide HCl/0.5% timolol malate (Cospot^®; Santen Pharmaceutical Co. LTD, Japan, q 8 h), and 0.03% flubiprofen sodium hydrate (Flubiprofen^®; Bausch & Lomb Incorporated, USA. q 24 h) OD. During three months of treatment, documented IOP elevations occurred three times, convincing the owner to elect ocular evisceration with implantation of an intrascleral prosthesis to salvage the globe OD. IOP of the OS was maintained within the normal range of less than 20 mmHg with medical management of 2% dorzolamide HCl/0.5% timolol malate and 0.03% flubiprofen sodium hydrate until the time of surgery for OD. There were no changes in ICA or CC during the follow-up time.

The case report describes PACG OD and early diagnosis of glaucoma OS through evaluation of ICA and CC using gonioscopy and HRUS in a Maltipoo dog. On the examination of OS, there were no clinical signs of glaucoma, and even abnormalities of ICA identified by gonioscopic examinations. Canine glaucoma is mostly associated with IOP elevation because of obstruction of the ICA and CC, which is the main drainage of aqueous humor in the dog (12). Therefore, it is crucial to evaluate the ICA and entire CC objectively with gonioscopy and HRUS in order to categorizes the type of glaucoma, such as primary (i.e., pectinate ligament dysplasia) or secondary glaucoma (1,4,5,11).

Previous studies proposed gonioscopic grading systems for assessing the ICA in dogs based on the length, morphology, and abnormal percentage of pectinate ligaments (5,13,14). In addition to these criteria, the European College of Veterinary Ophthalmologists (ECVO) recommended stricter guidelines that merged the angle width into the pectinate ligament dysplasia as a marker for the PACG and classified the pectinate ligament as follows: fibrae latae, lamina, and occlusio (11). The dogs can still be considered unaffected in case of the fibrae latae affected with 50% or less of the pectinate ligament circumference (12).

In this case report, the ICA OD was covered with solid sheets of iris-like tissue with multiple flow holes consistent with occlusio recommended by the ECVO (Fig. 3A). The gonioscopic appearance OS appeared to be unaffected even with the characteristics of mild fibrae latae (12). The findings of both eyes allowed us to consider the OD primary open angle glaucoma, because it is well known to evaluate the ICA of the fellow, unaffected eye for classifying the type of glaucoma in one eye (11,12). Given that the IOP OS was above the normal upper limits, however, this observation is likely associated with early signs of glaucoma. Accordingly, further diagnostic evaluation of ICA and CC using HRUS was performed to differentiate early glaucoma from the false elevation of IOP in OS and to determine PACG OD (7,9,10).

The HRUS has been widely applied to explore subtle changes in eyes prior to the onset of clinical signs of glaucoma in a clinical setting, typically with just topical anesthetic, avoiding anesthesia or sedation (2,7). It is a very useful imaging modality to assess the ocular anterior segment, including the structural abnormalities of the deeper CC and ICA, thereby providing more accurate differentiation of the type of glaucoma. Generally, the HRUS imaging of the CC is clinically interpreted as open (divergence of the outer and inner walls of the ciliary body with wide spaces within the CC), narrowed (parallel outer and inner walls of the ciliary body with lessened CC area than the normal), or closed (completely collapsed CC without any substantial width) (4). Overall, these previous studies suggested that a collapsed CC identified by HRUS was more likely to be a predisposing factor for glaucoma development in dogs (4,7).

In this case report, the HRUS showed the CC of OD completely collapsed based on the full apposition of the outer and inner walls of the CC shown as a hyperechoic complex, creating an indiscernible CC (Fig. 4A). While the CC of OS was long and parallel with relatively hypoechoic tissue within the cleft (Fig. 4B). Considering HRUS images of both eyes, these structural changes in CC of OS could contribute to mild IOP elevation and could be considered a characteristic precursor to glaucoma development. Based on the HRUS images of OS obtained in the report, it appeared reasonable to diagnose OD as PACG.

In this case report, HRUS and gonioscopy examinations were performed to confirm the prognostic symptoms in OS without any clinical sings of glaucoma but OD diagnosed with glaucoma. Both narrowed CCs and mild abnormalities in the pectinate ligament with normal width of ICA were observed in OS by HRUS and gonioscopy, respectively. The results played an essential role in determining PACG in OU and managing early glaucoma of OS in this dog. Therefore, comprehensive evaluation of the CC and its contents using HRUS may be a more instrumental predictor of glaucoma than assessment of the ICA with gonioscopy.

The authors have no conflicting interests.