• View in gallery
    Figure 1—

    Representative photograph (A) and SD-OCT image (B) of an eye of a Kemp's ridley sea turtle (Lepidochelys kempii) that had a substantial corneal scar. A—The scar appears as a well-delineated focal white lesion that extends horizontally across the axial cornea (arrow). B—The lesion (arrow) disrupts the architecture of the corneal stromal and alters the epithelial and stromal thicknesses.

  • View in gallery
    Figure 2—

    Representative photograph (A) and SD-OCT image (B) of an eye from a healthy rehabilitated juvenile Kemp's ridley sea turtle. a = ET. b = ST. c = TCT. d = ACD. IR = Iris. L = Lens.

  • View in gallery
    Figure 3—

    Representative photograph (A) and SD-OCT image (B) of an eye from a healthy rehabilitated juvenile Kemp's ridley sea turtle that has iridescent cells in the cornea. The iridescent cells appear to shine (arrow) grossly (A) and as focal hyperintense spots (arrow) on the SD-OCT image (B).

  • View in gallery
    Figure 4—

    Representative photographs (A and B) and SD-OCT image (C) of an eye from a healthy rehabilitated juvenile Kemp's ridley sea turtle that has corneal lesions consistent with Florida keratopathy. Grossly, the lesions appear as dull, tanto-gray, round, focal corneal opacities (arrows; A and B). The lesions appear as hyperintense, well-delineated, intraepithelial lesions (arrows) on the SD-OCT image (C). This turtle also has a small cluster of iridescent cells (asterisk) present in the dorsomedial aspect of the cornea (A and B).

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  • 29. Collin SP, Collin HB. A comparative SEM study of the vertebrate corneal epithelium. Cornea 2000; 19:218230.

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  • 37. Chittick B, Harms C. Intraocular pressure of juvenile loggerhead sea turtles (Caretta caretta. Vet Rec 2001; 149:587589.

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  • 39. Delgado C, Mans C, McLellan GL, et al. Evaluation of rebound tonometry in red-eared slider turtles (Trachemys scripta elegans. Vet Ophthalmol 2014; 17:261267.

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Ophthalmic variables in rehabilitated juvenile Kemp's ridley sea turtles (Lepidochelys kempii)

Kara R. GornikDepartment of Clinical Sciences, Cummings School of Veterinary Medicine, Tufts University, North Grafton, MA 01536.

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Christopher G. PirieDepartment of Clinical Sciences, Cummings School of Veterinary Medicine, Tufts University, North Grafton, MA 01536.

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Ruth M. MarrionInTown Veterinary Group, Bulger Veterinary Hospital, 247 Chickering Rd, North Andover, MA 01845.

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Julika N. WocialNew England Aquarium, 1 Central Wharf, Boston, MA 02110.

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Charles J. InnisNew England Aquarium, 1 Central Wharf, Boston, MA 02110.

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Abstract

OBJECTIVE

To determine central corneal thickness (total corneal thickness [TCT], epithelial thickness [ET], and stromal thickness [ST]), anterior chamber depth (ACD), and intraocular pressure (IOP) in Kemp's ridley sea turtles (Lepidochelys kempii).

DESIGN

Prospective cross-sectional study.

ANIMALS

25 healthy rehabilitated juvenile Kemp's ridley sea turtles.

PROCEDURES

Body weight and straight-line standard carapace length (SCL) were recorded. All turtles underwent a complete anterior segment ophthalmic examination. Central TCT, ET, ST, and ACD were determined by use of a spectral-domain optical coherence tomography device. Intraocular pressure was determined with a rebound tonometer; the horse setting was used to measure IOP in all 25 turtles, and the undefined setting was also used to measure IOP in 20 turtles. For each variable, 3 measurements were obtained bilaterally. The mean was calculated for each eye and used for analysis purposes.

RESULTS

The mean ± SD body weight and SCL were 3.85 ± 1.05 kg (8.47 ± 2.31 lb) and 29 ± 3 cm, respectively. The mean ± SD TCT, ET, ST, and ACD were 288 ± 23 μm, 100 ± 6 μm, 190 ± 19 μm, and 581 ± 128 μm, respectively. Mean ± SD IOP was 6.5 ± 1.0 mm Hg when measured with the horse setting and 3.8 ± 1.1 mm Hg when measured with the undefined setting.

CONCLUSIONS AND CLINICAL RELEVANCE

Results provided preliminary reference ranges for objective assessment of ophthalmic variables in healthy juvenile Kemp's ridley sea turtles.

Abstract

OBJECTIVE

To determine central corneal thickness (total corneal thickness [TCT], epithelial thickness [ET], and stromal thickness [ST]), anterior chamber depth (ACD), and intraocular pressure (IOP) in Kemp's ridley sea turtles (Lepidochelys kempii).

DESIGN

Prospective cross-sectional study.

ANIMALS

25 healthy rehabilitated juvenile Kemp's ridley sea turtles.

PROCEDURES

Body weight and straight-line standard carapace length (SCL) were recorded. All turtles underwent a complete anterior segment ophthalmic examination. Central TCT, ET, ST, and ACD were determined by use of a spectral-domain optical coherence tomography device. Intraocular pressure was determined with a rebound tonometer; the horse setting was used to measure IOP in all 25 turtles, and the undefined setting was also used to measure IOP in 20 turtles. For each variable, 3 measurements were obtained bilaterally. The mean was calculated for each eye and used for analysis purposes.

RESULTS

The mean ± SD body weight and SCL were 3.85 ± 1.05 kg (8.47 ± 2.31 lb) and 29 ± 3 cm, respectively. The mean ± SD TCT, ET, ST, and ACD were 288 ± 23 μm, 100 ± 6 μm, 190 ± 19 μm, and 581 ± 128 μm, respectively. Mean ± SD IOP was 6.5 ± 1.0 mm Hg when measured with the horse setting and 3.8 ± 1.1 mm Hg when measured with the undefined setting.

CONCLUSIONS AND CLINICAL RELEVANCE

Results provided preliminary reference ranges for objective assessment of ophthalmic variables in healthy juvenile Kemp's ridley sea turtles.

The Kemp's ridley sea turtle (Lepidochelys kempii) is the most endangered species of sea turtles, with a worldwide population of < 10,000 adult females.1 The majority of adult Kemp's ridley sea turtles reside in the Gulf of Mexico, although juveniles are commonly found along the northeastern coast of the United States throughout the summer months.1 When temperatures begin to decline in autumn, most of the juvenile turtles migrate to warmer waters; however, some fail to migrate south, which puts them at risk of becoming cold-stunned when local water temperatures fall below 10°C (50°F).2 Cold-stunned turtles are often found stranded on the beaches of Cape Cod, Mass, between October and December and are taken to rehabilitation centers for treatment.2 Cold-stunned turtles often have multiple physiologic derangements including metabolic and respiratory acidosis, electrolyte imbalances, dehydration, and impaired renal function,3,4 and many have concurrent lesions of varying severity in the respiratory, digestive, integumentary, nervous, skeletal, and urinary systems.5,6

Occasionally, rehabilitated cold-stunned sea turtles develop ocular disease.5 Chelonians, in general, are at risk of developing keratopathies, uveitis, and cataracts subsequent to exposure to freezing temperatures.7 One of the most common ocular abnormalities in sea turtles is corneal fibropapillomatosis, which is thought to be caused by a virus in the alphaherpesvirus family.8 Focal, necrotizing lesions with infiltration of heterophils and bacteria have been identified in the cornea, sclera, conjunctiva, and eyelids of several Kemp's ridley sea turtles during necropsy.5

To our knowledge, reference values for corneal thickness and ACD have not been reported for live sea turtles. Knowledge of the anatomic structure of the cornea and anterior chamber will aid clinicians in identifying ocular abnormalities in stranded sea turtles. Reference values have also not been reported for IOP in Kemp's ridley sea turtles, and determination of IOP in clinically normal turtles will help clinicians diagnose uveitis or glaucoma in that species. The purpose of the study reported here was to determine the central corneal thickness including the TCT, ET, ST, and ACD and the IOP in rehabilitated juvenile Kemp's ridley sea turtles.

Materials and Methods

Animals

Medical management and rehabilitation of sea turtles were conducted with authorization of the US Fish and Wildlife Service (Permit #TE-697823) and the US National Marine Fisheries Service. The study reported here was approved by the New England Aquarium Animal Care and Use Committee and conformed to the guidelines established by the Association for Research in Vision and Ophthalmology's statement for the use of animals in vision research.

Twenty-five rescued Kemp's ridley sea turtles that were housed at a rehabilitation center managed by the New England Aquarium were enrolled in the study. The turtles had been found stranded on beaches in Cape Cod, Mass, 4 to 5 months prior to examination and were medically managed as previously described.9 At the time of study enrollment, all turtles were examined by a board-certified reptile specialist (CJI) and determined to be systemically healthy on the basis of results of serial physical examinations, hematologic and plasma biochemical analyses, and radiographic assessments. Immediately prior to ophthalmic examination, body weight and SCL were obtained for each turtle. Room temperature and tank temperature were recorded and standardized throughout the study.

Ophthalmic examination

Prior to study enrollment, all turtles underwent an ophthalmic examination that included a complete assessment of the anterior segment by a board-certified veterinary ophthalmologist (RMM) and an ophthalmology resident (KRG). Only turtles that did not have any substantial anterior segment abnormalities were enrolled in the study. Turtles with substantial corneal changes (eg, scarring) or evidence of active anterior uveitis were excluded from the study.

Optical coherence tomography

Tomographic measurements were obtained with each turtle positioned in sternal recumbency and restrained by gentle manual restraint on an examination table. In general, most turtles remained immobile while the tomographic measurements were obtained; however, some had brief intermittent periods of activity. During those periods of activity, an investigator placed a hand under the jaw of the turtle to help calm it and stabilize the head for the measurement acquisition. For each turtle, corneal thickness and ACD scans were obtained from each eye 3 times by a board-certified ophthalmologist (CGP), who used a 6-mm pachymetry protocol with an SD-OCT machinea that had a supplemental cornea-anterior module attachment. All scans were obtained by aligning the aiming circle at the center of the pupil and keeping the SD-OCT device perpendicular to the axial corneal surface. The central corneal thickness was recorded from the center circle (radius, 1 mm) of the pachymetry image and was automatically calculated by the pachymetry software from eight 1,024-A radial scans that each had a length 6 mm.

The SD-OCT machine automatically assigns an internal quality control score to each corneal scan. To maximize signal strength and subsequently optimize quality control, only scans with a quality control score ≥ 27 and that were free of motion artifact were used for measurement acquisition. Corneal dimensions were manually generated by use of the caliper function associated with the SD-OCT machine by 1 ophthalmologist (CGP). Dimensions recorded included TCT, ET, ST, and ACD. Additionally, the width and depth of corneal changes consistent with Florida keratopathy were manually measured when present.

IOP

Intraocular pressure measurements were obtained from the axial cornea by use of a rebound tonometer.b The horse setting of the tonometer was used to measure the IOP in all 25 turtles, and the undefined setting was used to also measure IOP in 20 of those turtles. For each eye, the tonometer was held in a horizontal position with the tip of the probe approximately 5 to 6 mm from the cornea. All IOP measurements were obtained by the same investigator (KRG). For each calibration setting, 3 measurements were recorded for each eye, and the mean was calculated and used for analysis. Only IOP measurements with a deviation < 2.5 mm Hg (as indicated by the absence of a bar or the presence of a bar in the lowest position) were deemed acceptable for analysis.

Statistical analysis

Outcomes analyzed included body weight, SCL, TCT, ET, ST, ACD, and IOP. For each ophthalmic measurement, the mean was calculated for each eye. Because of the small study population, nonparametric analyses were used for analysis whenever possible. Wilcoxon rank sum tests and Kruskal-Wallis tests were performed to determine whether any of the outcomes varied significantly between the right and left eyes. The results of those tests indicated that there was no significant difference between the right and left eyes for any measurement; therefore, the data for the right and left eyes were pooled, and the mean for each measurement was calculated. The respective correlations between ocular measurements (TCT, ET, ST, ACD, and IOP) and SCL and body weight were assessed by means of nonparametric Spearman correlation coefficients.

A 2-way ANOVA was used to evaluate the difference in IOP measurements obtained by the 2 calibration settings for the rebound tonometer. In that model, the dependent variable was IOP, and calibration setting (horse or undefined) and eye (right or left) were the predictor variables.

Preliminary reference ranges for TCT, ET, ST, ACD, and IOP as measured by use of the horse setting (IOPhorse) were determined as described10 by use of a robust method, which has been validated for use with small sample sizes. The preliminary reference range for IOP as measured by use of the undefined setting (IOPundefined) was determined as described10 by a nonparametric method because the sample size (n = 20) was smaller than that (25) for the other variables. All analyses were performed with statistical software,c and values of P ≤ 0.05 were considered significant.

Results

Turtles

Throughout the study, tank temperature ranged from 24.3 to 24.6°C (75.7 to 76.3°F), and room temperature ranged from 21.0 to 22.3°C (69.8 to 72.2°F). Twenty-eight turtles were initially evaluated for study enrollment. Three turtles were excluded from the study because they had substantial corneal changes (eg, scarring; Figure 1) or evidence of active anterior uveitis. Thus, only 25 turtles were enrolled in the study, and those turtles had a mean ± SD body weight of 3.85 ± 1.05 kg (8.47 ± 2.31 lb) and SCL of 29 ± 3 cm. None of the turtles examined had evidence of corneal fibropapillomatosis.

Figure 1—
Figure 1—

Representative photograph (A) and SD-OCT image (B) of an eye of a Kemp's ridley sea turtle (Lepidochelys kempii) that had a substantial corneal scar. A—The scar appears as a well-delineated focal white lesion that extends horizontally across the axial cornea (arrow). B—The lesion (arrow) disrupts the architecture of the corneal stromal and alters the epithelial and stromal thicknesses.

Citation: Journal of the American Veterinary Medical Association 248, 6; 10.2460/javma.248.6.673

Ophthalmic variables

On ophthalmic examination, the anterior segment was considered clinically normal for 38 of 50 eyes (17 of 25 turtles) on the basis of uniformity in the corneal contour, profile, and thickness as well as absence of corneal opacification and intraocular inflammation (ie, flare; Figure 2). Nineteen of 50 eyes (12 of 25 turtles) had iridescent cells within the cornea or on the anterior lens capsule (Figure 3), and those iridescent cells were considered a normal variation. Corneal changes that did not affect the central corneal thickness measurements were present in 12 of 50 eyes (8 of 25 turtles) and included minor paraxial corneal scarring and lesions consistent with Florida keratopathy (Figure 4). Three eyes (2 turtles) had lesions consistent with Florida keratopathy with a mean ± SD depth of 56 ± 13 μm and width of 380 ± 251 μm. All of those lesions were confined to the corneal epithelium as determined on the basis of SD-OCT imaging.

Figure 2—
Figure 2—

Representative photograph (A) and SD-OCT image (B) of an eye from a healthy rehabilitated juvenile Kemp's ridley sea turtle. a = ET. b = ST. c = TCT. d = ACD. IR = Iris. L = Lens.

Citation: Journal of the American Veterinary Medical Association 248, 6; 10.2460/javma.248.6.673

Figure 3—
Figure 3—

Representative photograph (A) and SD-OCT image (B) of an eye from a healthy rehabilitated juvenile Kemp's ridley sea turtle that has iridescent cells in the cornea. The iridescent cells appear to shine (arrow) grossly (A) and as focal hyperintense spots (arrow) on the SD-OCT image (B).

Citation: Journal of the American Veterinary Medical Association 248, 6; 10.2460/javma.248.6.673

Figure 4—
Figure 4—

Representative photographs (A and B) and SD-OCT image (C) of an eye from a healthy rehabilitated juvenile Kemp's ridley sea turtle that has corneal lesions consistent with Florida keratopathy. Grossly, the lesions appear as dull, tanto-gray, round, focal corneal opacities (arrows; A and B). The lesions appear as hyperintense, well-delineated, intraepithelial lesions (arrows) on the SD-OCT image (C). This turtle also has a small cluster of iridescent cells (asterisk) present in the dorsomedial aspect of the cornea (A and B).

Citation: Journal of the American Veterinary Medical Association 248, 6; 10.2460/javma.248.6.673

Results of the Wilcoxon rank sum analysis and Kruskal-Wallis test indicated that TCT (P = 0.76), ET (P = 0.80), ST (P = 0.55), ACD (P = 0.24), IOPhorse (P = 0.51), and IOPundefined (P = 0.40) did not differ significantly between the right and left eyes. Additionally, the generated box plots suggested that all variables had excellent correlation between the right and left eyes. Therefore, the data for the right and left eyes were combined, and the means were calculated and used for subsequent analyses. The mean ± SD and preliminary reference ranges for those variables were summarized (Table 1).

Table 1—

Mean ± SD and preliminary reference ranges for select ophthalmic variables determined on the basis of measurements obtained from 25 healthy, rehabilitated juvenile Kemp's ridley sea turtles (Lepidochelys kempii).

VariableMean ± SDReference range
TCT (µm)288 ± 23243.5–340.3
ET (µm)100 ± 685.6-II2.I
ST (pm)190 ± 19153.8–229.6
ACD (pm)581 ± 128416.5–788.1
IOPhorse (mm Hg)6.5 ± 1.05.0–9.0
IOPundefined (mm Hg)3.8 ± 1.1I.9–6.5

IOPhorse = IOP as determined by a rebound tonometer and use of the horse calibration setting. IOPundefined = IOP as determined by a rebound tonometer and use of the undefined calibration setting.

Results of the nonparametric correlation analyses indicated that TCT, ET, and ST were significantly and positively correlated with both body weight and SCL (Table 2). Anterior chamber depth and IOP were not significantly correlated with body weight or SCL.

Table 2—

Spearman correlation coefficients for correlations between select ophthalmic variables and body weight and SCL for 25 healthy rehabilitated juvenile Kemp's ridley sea turtles.

VariableBody weightSCL
TCT (pm)0.627*0.709*
ET (pm)0.350*0.373*
ST (pm)0.569*0.661*
ACD (pm)0.069–0.001
IOPhorse (mm Hg)–0.008–0.140
IOPundefined (mm Hg)0.2470.103

P ≤ 0.05.

See Table 1 for remainder of key.

The IOPhorse was consistently greater than the IOPundefined by a mean of 2.7 mm Hg. That difference was significant (P < 0.001).

Discussion

Results of the present study provided preliminary reference ranges for TCT, ET, ST, ACD, and IOP for healthy rehabilitated juvenile Kemp's ridley sea turtles. Spectral-domain optical coherence tomography has been used to measure central corneal thickness in healthy dogs,11 cats,12 horses,13 and a subset of reptilian species.14 The thickness of individual corneal layers has been established by the use of SD-OCT in dogs15 and horses.16 Additionally, SD-OCT has been used to establish normative data for ACD in select ophidian, chelonian, and saurian species.14 The findings of the present study suggested that the TCT of juvenile Kemp's ridley sea turtles as measured by SD-OCT was substantially thinner than that of dogs,11 cats,12 and horses13; however, the TCT of juvenile Kemp's ridley sea turtles appeared to be thicker than that of Hermann's tortoises (Testudo hermanni), Greek tortoises (Testudo graeca), red-footed tortoises (Geochelone carbonaria), and serrated hingeback tortoises (Kinixys erosa).14

A-mode ultrasonography has been used to measure TCT in red-eared sliders (Trachemys scripta elegans)17 and an undefined species of tortoise.d The TCT of red-eared sliders as measured by A-mode ultrasonography is considerably thinner than that of the Kemp's ridley sea turtles of the present study.17 However, the mean TCT for the tortoises (242 μm)d was similar to the mean TCT for the Kemp's ridley sea turtles of the present study (288 μm).

Histologic examination of globe specimens by use of light microscopy has also been used to measure TCT in freshwater and sea turtle species. The TCT of juvenile leatherback sea turtles (Dermochelys coriacea) and green sea turtles (Chelonia mydas) was substantially thinner, whereas the TCT of adult leatherback sea turtles and green sea turtles was similar,18,19 compared with the TCT of the juvenile Kemp's ridley sea turtles of the present study.

Direct comparison of TCT as determined by SD-OCT for the Kemp's ridley sea turtles of the present study with the TCT as determined by other modalities (ie, A-mode ultrasonography and histopathology) for other sea turtle species should be interpreted cautiously. For example, the manner in which light waves (SD-OCT) and sound waves (A-mode ultrasonography) transverse the cornea might differ and thereby affect measurement of the TCT. Also, globe handling and fixation in preparation for histologic examination might alter corneal thickness.

In the present study, TCT, ET, and ST were positively correlated with both SCL and body weight. In dogs, corneal thickness increases until 100 months of age.20 To our knowledge, studies investigating corneal maturation in reptile and aquatic species have not been conducted. The observed correlation between corneal thickness and both SCL and body weight in the present study was likely associated with the varying ages of the juvenile turtles assessed.

The present study was the first to describe the presence of iridescent cells in the cornea of Kemp's ridley sea turtles. Iridescent cells have been reported in the corneas of several fish and amphibians and have been well characterized in various species of teleost fish.21–23 The location of the iridescent cells varies on the basis of taxonomic group. Iridescent cells have been described in locations throughout the corneal stroma, as a separate layer between the stroma and Descemet membrane, and within either the Descemet membrane or corneal endothelium.22,24 In many teleost fish, iridescent cells form a distinct layer between the anterior and posterior corneal stroma, which is known as the autochthonous layer.19,21,23 The proposed functions of the iridescent cells include reduction of intraocular glare to increase visual range underwater, birefringence, filtration or polarization of color, camouflage, and enhancement or suppression of reflections.22,25

Two turtles (3 eyes) in the present study had lesions consistent with Florida keratopathy. Florida keratopathy is commonly identified in the corneas of dogs and cats living in tropical and subtropical climates26 and has also been described in birds and horses.27 Ophthalmoscopically, the lesions in the Kemp's ridley sea turtles were multifocal, round-to-oval, gray-to-white, well-delineated opacities with uniform density in the anterior cornea that appeared similar to those described in dogs and cats with Florida keratopathy.26 After hatching, Kemp's ridley sea turtles migrate north from the Gulf of Mexico along the eastern coast of Florida, which makes the development of Florida keratopathy a possibility on the basis of geographic exposure. However, on the basis of SD-OCT results, the Florida keratopathy–like lesions in the Kemp's ridley sea turtles appeared to originate from within the corneal epithelium. In dogs with Florida keratopathy, lesions are generally observed throughout corneal stroma with most localized in the anterior stroma.26 To our knowledge, SD-OCT images have not been obtained from any animal with histologically confirmed Florida keratopathy; therefore, the exact characteristics of opacities as determined by SD-OCT in dogs, cats, birds, and horses remain unknown. Histologic examination would be required to confirm whether the 2 turtles of the present study did have Florida keratopathy and determine whether the corneal lesions in those turtles contained vacuoles and rod-like structures similar to those described for Florida keratopathy lesions in dogs.27

The range for ACD (416.5 to 788.1 μm) for the juvenile Kemp's ridley sea turtles of the present study was fairly wide and was similar to that for terrestrial chelonians,14,28 adult green sea turtles, and juvenile green, leatherback, and hawksbill sea turtles.18 However, the ACD range for the turtles of the present study was substantially lower than that (1 to 2 mm) for adult leatherback sea turtles as determined by histologic evaluation of frozen specimens.19 This discrepancy in the ACD may simply be a reflection of the larger size of adult leatherback sea turtles, compared with juvenile Kemp's ridley sea turtles.

Similar to species of birds and mammals that reside near the surface of the water, the eyes of sea turtles are emmetropic when exposed to the air but have a substantial degree of hyperopia when underwater.18 When underwater, the cornea loses its refractive power because of a minute difference between the refractive indices of the cornea and the surrounding seawater.29 To compensate for hyperopia, many fish and aquatic mammals have evolved with an ability to increase the accommodative and refractive powers of the lens,30 and most underwater animals, including sea turtles, have fairly flat corneas and spherical lenses.18,19 Aquatic chelonians have evolved with the ability to use the iris sphincter muscle to alter the anterior profile of the lens such that anterior lenticonus results, which dramatically changes the curvature and refractive ability of the lens.23,31 In several reptile and amphibian species, the eyes can compensate for hyperopia independently and the refractive states between the eyes of an individual animal may differ by as much as 6 diopters.32 Although this mechanism has not been described for Kemp's ridley sea turtles, this species likely has some combination of the compensatory mechanisms described for hyperopia, which could account for the observed variability in ACD within and between turtles of the present study.

For the turtles of the present study, the IOPhorse was consistently higher than the IOPundefined. The rebound tonometer was held at a fixed distance (5 to 6 mm) from the eye and had a small probe that was rapidly propelled electromagnetically from the instrument to contact the cornea. When the probe contacted the cornea, it rebounded back to the tonometer. The rebound tonometer calculates probe deceleration to determine IOP, which differs from indentation tonometry that uses corneal curvature to calculate IOP.33 Use of a rebound tonometer has several advantages over use of an applanation tonometer, such as topical anesthesia is not required for rebound tonometry; the rebound tonometer has a very small probe tip, which makes it more practical than applanation tonometry for measurement of IOP in animals with small eyes or eyes with substantial ocular disease; and the probe tip of the rebound tonometer is disposable and easily changed.33 The rebound tonometer is similar to the Goldmann or applanation tonometer in that the species calibration settings for the instrument are based on the mean central corneal thickness for each species.34 The rebound tonometer has 3 settings for use in veterinary patients (dog, horse, and undefined).33

Intraocular pressure in many reptile species, including multiple turtle and tortoise species, has been measured by use of both rebound and applanation tonometry, and IOP as determined by applanation tonometry appears to be consistently higher than IOP as determined by rebound tonometry.7,28,35–39 For the turtles of the present study, the ranges for IOP (IOPhorse, 5.0 to 9.0 mm Hg; IOPundefined, 1.9 to 6.5 mm Hg) were most similar to those for red-eared sliders (IOPhorse, 5 to 13 mm Hg38; IOPundefined, 2 to 9 mm Hg17,38), which were also determined by rebound tonometry. The mean IOP as determined by applanation tonometry for juvenile loggerhead sea turtles restrained in sternal recumbency (5 mm Hg)37 was also similar to the mean IOP determined by rebound tonometry for the juvenile Kemp's ridley sea turtles of the present study. Additionally, IOP was not significantly associated with carapace length for the juvenile Kemp's ridley sea turtles of the present study or red-footed tortoises of other studies.28,33,35

The IOPs measured in the Kemp's ridley sea turtles of the present study were substantially lower than the IOPs reported for several land tortoise and turtle species.7,28,35,36,38,39 There are several possible explanations for the differences in IOP among those species. The IOP was measured by use of applanation tonometry in many of those species.28,35,36 In fact, IOP was measured by rebound tonometry only in Hermann's tortoises7 and red-eared sliders.38,39 Differences in the instrumentation used and their mechanisms for indirectly determining IOP may account for those discrepancies. Alternatively, differences in IOP may reflect anatomic differences (eg, globe size or corneal thickness) between terrestrial tortoises and sea turtles. Additionally, unlike sea turtles, tortoises and many freshwater turtles can retract their heads into their shells, and the restraint required to obtain tonometric measurements in those species might have artificially increased the IOP. Direct measurement of IOP by manometry (gold standard) concurrently with tonometry is necessary to determine which method of tonometry (applanation or rebound) and which calibration setting (dog, horse, or undefined) provides the most accurate measurement of IOP in chelonians.

The present study had several limitations. Spectral-domain optical coherence tomography was the only imaging modality used to measure central corneal thickness. Measurements could have been validated by use of A-mode ultrasonography, and further normative information could have been acquired by the use of B-mode ultrasonography and histologic evaluation. Intraocular pressures were obtained by rebound tonometry by use of only the horse and undefined calibration settings. Use of the dog setting on the rebound tonometer and measurement of IOP by applanation tonometry would have provided more comprehensive data for comparison purposes. Finally, data were obtained solely from turtles that had no or only minor corneal abnormalities. Evaluation of turtles with substantial corneal scarring and evidence of anterior uveitis might have provided valuable information about corneal changes or alterations in IOP in turtles with ocular disease.

To our knowledge, the present study was the first to measure ophthalmic variables for healthy rehabilitated juvenile Kemp's ridley sea turtles. Determination of values for ophthalmic variables in clinically normal turtles is important for the establishment of baseline or reference ranges against which measurements from other turtles can be compared during hospitalization and rehabilitation. Many of the healthy juvenile Kemp's ridley sea turtles of the present study had iridescent cells in the cornea or anterior lens capsule, and 2 turtles had corneal lesions similar to those observed in dogs with Florida keratopathy.

Acknowledgments

Presented in abstract form at the 45th meeting of the American College of Veterinary Ophthalmologists, Fort Worth, Tex, October 2014.

The authors thank Bruce Barton for assistance with statistical analysis.

ABBREVIATIONS

ACD

Anterior chamber depth

ET

Corneal epithelial thickness

IOP

Intraocular pressure

SCL

Straight-line standard carapace length

SD-OCT

Spectral-domain optical coherence tomography

ST

Corneal stromal thickness

TCT

Total corneal thickness

Footnotes

a.

Optovue iVue SD-OCT, Optovue Inc, Freemont, Calif.

b.

TonoVet, Icare Finland, Vantaa, Finland.

3.

SAS, version 9.3, SAS Institute, Cary, NC.

d.

Merlini NB, Comerlato AT, Bortolini Z, et al. Schirmer tear test and central corneal thickness in the tortoise (Chelonoidis sp) (abstr), in Proceedings. 44th Annu Meet Am Coll Vet Ophthalmol 2013;25.

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Contributor Notes

Dr. Gornik's present address is Pittsburgh Veterinary Specialty and Emergency Center, 807 Camp Horne Rd, Pittsburgh, PA 15237.

Address correspondence to Dr. Pirie (chris.pirie@tufts.edu).