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BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. OPHTHALMIC EXAMINATION OF THE CAPTIVE WESTERN LOWLAND GORILLA (GORILLA GORILLA GORILLA) Author(s): David LiangM.D., Thomas P. AlvaradoD.V.M., Deniz OralM.D., Jose M. VargasM.D., Melissa M. DenenaM.S., and James P. McCulleyM.D. Source: Journal of Zoo and Wildlife Medicine, 36(3):430-433. 2005. Published By: American Association of Zoo Veterinarians DOI: http://dx.doi.org/10.1638/03-121.1 URL: http://www.bioone.org/doi/full/10.1638/03-121.1 BioOne (www.bioone.org ) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use . Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder.

OPHTHALMIC EXAMINATION OF THE CAPTIVE WESTERN LOWLAND GORILLA (GORILLA GORILLA GORILLA)

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BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, researchlibraries, and research funders in the common goal of maximizing access to critical research.

OPHTHALMIC EXAMINATION OF THE CAPTIVE WESTERN LOWLANDGORILLA (GORILLA GORILLA GORILLA)Author(s): David LiangM.D., Thomas P. AlvaradoD.V.M., Deniz OralM.D., Jose M. VargasM.D.,Melissa M. DenenaM.S., and James P. McCulleyM.D.Source: Journal of Zoo and Wildlife Medicine, 36(3):430-433. 2005.Published By: American Association of Zoo VeterinariansDOI: http://dx.doi.org/10.1638/03-121.1URL: http://www.bioone.org/doi/full/10.1638/03-121.1

BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, andenvironmental sciences. BioOne provides a sustainable online platform for over 170 journals and books publishedby nonprofit societies, associations, museums, institutions, and presses.

Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance ofBioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use.

Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiriesor rights and permissions requests should be directed to the individual publisher as copyright holder.

430

Journal of Zoo and Wildlife Medicine 36(3): 430–433, 2005Copyright 2005 by American Association of Zoo Veterinarians

OPHTHALMIC EXAMINATION OF THE CAPTIVE WESTERNLOWLAND GORILLA (GORILLA GORILLA GORILLA)

David Liang, M.D., Thomas P. Alvarado, D.V.M., Deniz Oral, M.D., Jose M. Vargas, M.D.,Melissa M Denena, M.S., and James P. McCulley, M.D.

Abstract: This study examined the captive western lowland gorilla (Gorilla gorilla gorilla) eye as compared andcontrasted with the human eye. Bilateral ophthalmic examinations of western lowland gorillas (n 5 5) while undergeneral anesthesia were performed opportunistically, including slit-lamp biomicroscopy, dilated fundus examination,cycloplegic retinoscopy, Schiotz tonometry, corneal diameter and thickness measurements, A-scan and B-scan ultra-sonography, keratometry, and cultures of the eyelid margins and bulbar conjunctiva. Mean spherical equivalent refrac-tive error by cycloplegic retinoscopy was 11.20 6 0.59 diopters. Mean intraocular pressure by Schiotz tonometry was12.0 6 4.3 mm Hg. Mean optic nerve head cup to disc ratio was 0.42 6 0.11. Mean horizontal corneal diameter was13.4 6 0.8 mm, and mean vertical cornea diameter was 12.7 6 0.8 mm. Mean central corneal thickness by ultrasoundpachymetry was 489 6 52 mm. Mean axial length of the eye by A-scan was 22.75 6 0.71 mm. Mean lens thicknessby A-scan was 4.23 6 0.34 mm. Mean anterior chamber depth by A-scan was 4.00 6 0.26 mm. Mean keratometryreading was 44.38 6 1.64 diopters. Eyelid margin and bulbar conjunctival cultures isolated Candida sp. (n 5 5),Staphylococcus aureus (n 5 4), Staphylococcus epidermidis (n 5 3), Staphylococcus saccharolyticus (n 5 3), andMicrococcus sp. (n 5 3). This study suggests important similarities between western lowland gorilla and human eyes.These similarities may allow diagnostics, techniques, and equipment for human eye surgery, such as those used forcataract extraction and intraocular lens implantation, to be successfully utilized for gorillas.

Key words: Comparative anatomy, eyes, gorilla, ophthalmic examination.

INTRODUCTION

The western lowland gorilla (Gorilla gorilla go-rilla) is found in the dense tropical rain forests ofthe Central African Republic, western Congo to theCongo River, equatorial Guinea, Gabon, and north-western Cameroon.3 The species is considered vul-nerable by the International Union for the Conser-vation of Nature with fewer than 40,000 in the wild,and about 500 are found in zoos.3,7

Western lowland gorillas are as tall as 2 m andcan weigh more than 200 kg.2 They are herbivores,feeding on fruit, shoots, bulbs, tree bark, andleaves.7 Gorillas live in troops of 5–15 adult fe-males and their offspring, led by a silverback, theoldest dominant male.7 Gorillas thrive on their se-cure family structure.8

As with most animals, but particularly thosehighly intelligent and social, vision is an importantsense. Gorillas with poor vision have increased dif-ficulties in social interactions and survival. In thewild, gorillas can live up to 40 yr, and in captivitythey are now living more than 50 yr.3 With thisincreased longevity, gorillas are presenting increas-

From The University of Texas Southwestern MedicalCenter at Dallas, 5323 Harry Hines Boulevard, Dallas,Texas 75390-9057, USA (Liang, Oral, Vargas, Denena,McCulley) and the Dallas Zoo, 650 South R. L. ThorntonFreeway, Dallas, Texas 75203-3013, USA (Alvarado).Correspondence should be directed to Dr. McCulley.

ingly with cataracts. Recently, a gorilla at the Bris-tol Zoo Gardens, United Kingdom, underwent cat-aract surgery (Alex Kirby, personal communica-tion). The cataract was successfully removed withstandard phacoemulsification, and an artificial in-traocular lens designed for humans (Homo sapiens)was placed. It was reported that the gorilla had adramatic improvement of vision and began to ex-plore its surroundings and interact with companionsappropriately (Alex Kirby, personal communica-tion). Four other successful cataract removal sur-geries have been performed on captive gorillas:Rotterdam Zoo, Netherlands (n 5 2), CincinnatiZoo and Botanical Gardens, Ohio (n 5 1), and Ho-gle Zoo, Utah (n 5 1). To date, however, there havebeen no published baseline data on gorilla eyes.The purpose of this study was to compare and con-trast the western lowland gorilla eye to the humaneye.

MATERIALS AND METHODS

Ten eyes of five western lowland gorillas at theDallas Zoo in Dallas, Texas, were evaluated in thisprospective, nonrandomized, nonmasked studyfrom 17 June 2002 to 26 January 2003 (Table 1).These examinations were conducted opportunisti-cally while the gorillas were placed under generalanesthesia for physical and dental examinations.Anesthesia was coordinated by attending veterinar-ians. The weight range of the gorillas was 90.9 kg

431LIANG ET AL.—GORILLA EYES

Table 1. Demographics of the gorillas studied.

Name Sex Age (yr)

Gorilla AGorilla BGorilla CGorilla DGorilla E

MMMMF

1212363748

to 159 kg. Gorillas A, B, C, and E were immobi-lized with a combination of tiletamine and zolaze-pam (Telazolt, Fort Dodge, Iowa 50501, USA, 6mg/kg), administered by hand syringe or dart (Tel-inject USA, Sagus, California 91350, USA). GorillaD was immobilized with a combination of mida-zolam (Midazolam HCl, Baxter-Mova, Caguas, PR00725, USA, 50 mg/kg) and ketamine (Ketasett,Fort Dodge, Iowa 50501, USA, 9 mg/kg), admin-istered by dart. After intubation, anesthesia wasmaintained for all five gorillas with isoflurane inoxygen (Isoflurane USP, Halocarbon Laboratories,River Edge, New Jersey 07661, USA).

Thorough ophthalmic examinations were per-formed, consisting of slit-lamp biomicroscopy, di-lated fundus examination, cycloplegic retinoscopy,tonometry, corneal diameter and thickness mea-surements, A-scan and B-scan ultrasonography,keratometry, and cultures of eyelid margins andbulbar conjunctiva. Standard wire eyelid speculawere used to assist in the examinations. Keratom-etry was performed on both eyes of four gorillas,using a portable keratometer (Alcont Auto-Kera-tometer, Alcon, Inc., Fort Worth, Texas 76134,USA). Tonometry was performed with a Schiotztonometer (Miltex Schiotz Tonometer, Miltex, Inc.,York, Pennsylvania 17402, USA). Eyelid margincultures were performed with calcium alginateswabs dipped in thioglycolate broth, which weresubsequently plated on blood agar, chocolate agar,Sabauroud’s dextrose agar, nonnutrient agar withEscherichia coli overlay, Lowenstein-Jensen media,and finally placed into the thioglycolate broth. Sep-arate cultures of the bulbar conjunctiva were per-formed in the same manner. Cultures of the eyelidmargins and bulbar conjunctiva were performed onboth eyes of each gorilla and plated separately. Fol-lowing culture, one drop each of phenylephrine2.5% (Phenylephrine Hydrochloride OphthalmicSolution USP 2.5%, Bausch and Lomb, Inc., Tam-pa, Florida 33637, USA) and tropicamide 1% (Tro-picamide Ophthalmic Solution USP 1%, Bauschand Lomb, Inc., Tampa, Florida 33637, USA) wereplaced on the eye for dilation. Biomicroscopy wasperformed with a portable slit lamp (Kowa SL-5,

Kowa Optimed, Inc., Torrance, California 90502,USA). The corneal vertical and horizontal diame-ters were measured with standard surgical calipers.Central corneal thickness was measured by themean of three measurements by an ultrasound pa-chymeter (Sonogage Corneo-GageTM Plus, Sono-gage, Inc., Cleveland, Ohio 44128, USA). Themean was used, rather than the thinnest measure-ment, for the purpose of obtaining an anatomicmeasurement closest to what the actual central cor-neal thickness may be. The indirect ophthalmo-scope and a 20-diopter condensing lens (Volk, Inc.,Mentor, Ohio 44060, USA) were used for the di-lated fundus examination. Retinoscopy was per-formed with skiascopy bars (Luneau SkiaskcopyBars, Luneau, S.A., B.P. 252, 28005 Chartres Ced-ex, France) and a standard retinoscope (Welch Al-lyn Retinoscope, Welch Allyn, Skaneateles Falls,New York 13153, USA). The mean and standarddeviation were calculated for all the parameters ex-cept the eyelid margin and bulbar conjunctival cul-tures. The unpaired Student’s t-test was used to de-termine statistical significance of the measure-ments.

RESULTS

The mean spherical equivalent refractive error bycycloplegic retinoscopy was 11.20 6 0.59 diopters(range 10.50 to 12.50 diopters). This is similar tothe mean spherical equivalent refractive error in hu-mans, which is 11.00 diopters.18 The mean intra-ocular pressure by Schiotz tonometry was 12.0 64.3 mm Hg (range 7.0–17.0 mm Hg). This is slight-ly lower than the mean intraocular pressure bySchiotz tonometry in humans, which is 15.8 6 2.57mm Hg.14 The mean optic nerve head cup to discratio was 0.42 6 0.11 (range 0.30–0.40). This islarger than the mean optic nerve head cup to discratio in humans, which is 0.38; however, the dif-ference was not statistically significant.4 The meanhorizontal corneal diameter was 13.4 6 0.8 mm(range 12–14.5 mm), and mean vertical cornea di-ameter was 12.7 6 0.8 mm (range 12–14 mm). Thisis larger than the mean horizontal corneal diameterof 12.6 mm in humans and the mean vertical corneadiameter of 11.7 mm in humans.6 The mean centralcorneal thickness by ultrasound pachymetry was489 6 52 mm (range 437–590 mm). This is thinnerthan the mean central corneal thickness in humansof 520 mm; however, the difference was not statis-tically significant.6 The mean axial length of the eyeby A-scan was 22.75 6 0.71 mm (range 21.84–24.03 mm), and the mean lens thickness by A-scanwas 4.23 6 0.34 mm (range 3.79–4.66 mm), whichare slightly lower than mean values in humans

432 JOURNAL OF ZOO AND WILDLIFE MEDICINE

Table 2. A comparison of the gorilla eye to the human eye.

Gorilla Human

Mean spherical equivalent refractive error(P 5 0.295)

Mean intraocular pressure(P 5 0.012)

Mean optic nerve head cup-to-disc ratio(P 5 0.270)

11.20 diopters

12.0 mm Hg

0.42

11.00 diopters

15.8 mm Hg

0.38Mean horizontal corneal diameter

(P 5 0.006)Mean vertical corneal diameter

(P 5 0.001)Mean central corneal thickness

(P 5 0.080)

13.4 mm

12.7 mm

489 mm

12.6 mm

11.7 mm

520 mmMean axial length of eye

(P 5 0.001)Mean lens thickness

(P 5 0.002)Mean anterior chamber depth

(P 5 0.001)Mean keratometry reading

(P 5 0.032)

22.75 mm

4.23 mm

4.00 mm

44.38 diopters

23.60 mm

4.63 mm

3.24 mm

43.00 diopters

(23.6 mm and 4.63 mm, respectively).1,10–12,15–17

However, the mean anterior chamber depth by A-scan was 4.00 6 0.26 mm (range 3.68–4.5 mm),which is larger than that in humans (3.24 6 0.44mm).10 The mean keratometry reading was 44.38 61.64 diopters (range 42.56–46.81 diopters). This isslightly higher than the mean keratometry readingin humans, which is 43 diopters (Table 2).18

The eyelid margin and bulbar conjunctival cul-tures isolated Candida sp. (n 5 5), Staphylococcusaureus (n 5 4), Staphylococcus epidermidis (n 53), Staphylococcus saccharolyticus (n 5 3), andMicrococcus species (n 5 3).

Two older gorillas (gorillas D and E) had em-bryonal nuclear cataracts bilaterally, and one eyehad a posterior polar cataract. All five gorillas had3608 of dense, limbal, conjunctival melanosis bilat-erally, but only one gorilla had a heavily pigmentedfundus.

DISCUSSION

The preponderance of Candida sp., Staphylococ-cus saccharolyticus, and Micrococcus sp. isolatedmay relate to the gorilla’s more intimate contactwith soil. The normal eyelid and conjunctival florain humans is relatively consistent worldwide.13 Themost common bacterial organisms cultured fromthe conjunctiva are Staphylococcus epidermidis,Corynebacterium sp., Propionibacterium acnes,Staphylococcus aureus, and Streptococcus viri-dans.13 Fungus is cultured from the conjunctiva in

10% of adults, 5% of children, and 1% of infants.9

Similar organisms are found on the eyelid margin,and more frequently.13

The lower mean intraocular pressure in the go-rillas studied may have been related to anesthesiaand sedation. Most general anesthetic agents andsedatives lower intraocular pressure with the excep-tion of ketamine, which may raise intraocular pres-sure.5

It appears that a gorilla’s eye is slightly shorterthan a human’s eye despite having a larger cornealdiameter. The anterior chamber depth was slightlygreater than the mean in humans. This increaseddepth would likely allow for standard human oph-thalmic instruments to be used, including phaco-emulsification for cataracts. Lens thickness wasalso similar to humans, but thinner. These similar-ities validate the use of techniques and equipmentfor human eye surgery, such as those used for cat-aract extraction and intraocular lens implantation,to be successfully utilized for gorillas.

Cataract surgery may improve the quality of lifeof gorillas in captivity. Before cataract surgery, ker-atometry and A-scan ultrasonography are recom-mended to more accurately determine intraocularlens power considering the individual variability ofthese critical measurements. Given the larger cor-neal diameters and deeper anterior chambers in thegorillas studied, the use of intraocular lenses withlonger overall diameters within the lens capsularbag is suggested.

433LIANG ET AL.—GORILLA EYES

Acknowledgments: This study was supported inpart by NIH grant EY12430 and an unrestrictedgrant from Research to Prevent Blindness, Inc.,New York, New York, USA.

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9. Hammeke, J. C., and P. P. Ellis. 1960. Mycotic floraof the conjunctiva. Am. J. Ophthalmol. 49: 1174–1178.

10. Hoffer, K. J. 1981. Biometry of 7500 cataractouseyes. Am. J. Ophthalmol. 99: 360.

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17. Shammas, H. J. F. 1984. A comparison of immer-sion and contact techniques for axial length measure-ments. Am. Intraocular Implant Soc. J. 10: 444.

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Received for publication 22 December 2003