optical properties of conjunctiva, sclera, and the ciliary body and their consequences for...

Optical properties of conjunctiva, sclera,and the ciliary body and their consequences fortransscleral cyclophotocoagulation

Babak Nemati, H. Grady Rylander III, and Ashley J. Welch

A number of recent studies have demonstrated the success of Nd:YAG and diode laser transscleralcyclophotocoagulation in the treatment of advanced glaucoma. Wavelength selection, however, hasseldom been based on a clear understanding of the optical properties of tissues involved. The opticalproperties of conjunctiva, sclera, and the ciliary body adjacent to the limbus were investigated to find anoptimal wavelength range for transscleral cyclophotocoagulation. The absorption and scatteringcoefficients of these layers were determined in the 300–1200-nm wavelength range by the use of aone-dimensional inverse adding–doubling method. The measured optical properties of conjunctiva,sclera, and the ciliary body provide a basis for a comparative analysis of the laser wavelengths usedclinically for transscleral cyclophotocoagulation. r 1996 Optical Society of America

1. Introduction

The glaucomas are a family of diseases that result inoptic atrophy through cupping of the optic disc andare considered second only to diabetes mellitus asthe leading cause of new cases of blindness in theUnited States. They are generally associated withcharacteristic visual-field loss and often 1but notinvariably2 an elevated intraocular pressure 1IOP2.The increase in IOP stems from increased resistanceto the outflow of aqueous humor. A variety ofmedical and surgical approaches have been used toestablish a healthy balance between these two aque-ous-transport processes. Among the surgical treat-ments of an elevated IOP, cyclodestructive proce-dures in general possess a very narrow therapeuticwindow. A heavy treatment may cause hypotonyresulting from an insufficient number of remainingfunctional ciliary processes, and a light or inad-equate treatment will not provide the desired reduc-tion of intraocular pressure. Despite the fewer andless profound side effects of cyclophotocoagulation incomparison with cyclocryopexy, there still exists thepossibility of serious complications, such as severe

The authors are with the Biomedical Engineering Laser Labora-tory, Biomedical Engineering Program, University of Texas atAustin, Austin, Texas 78712.Received 16 November 1995; revised manuscript received 20

February 1996.0003-6935@96@193321-07$10.00@0r 1996 Optical Society of America

uveitis, pain, anterior-segment ischemia, lens dislo-cation, and phthisis bulbi.1 Cyclophotocoagulationis generally reserved as a last-resort treatment whenother medical or surgical procedures have proven tobe ineffective.Historically, a number of different approaches

were developed to ablate the ciliary processes, datingas far back as the early 1930’s,1 ranging from dia-thermy2 to beta-irradiation,3 cyclocryotherapy,4 andfinally cyclophotocoagulation.5,6 Beckman and co-workers7 were the first to perform transscleral irra-diation of the ciliary body in patients with intrac-table glaucoma by using the ruby laser as their lightsource. In 1984, Beckman et al.8 reported a 10-yearfollowup on this study, and the results showed asuccess rate of 86% for aphakic open-angle glaucoma.Because of the very limited availability of the rubylaser, however, cyclocryotherapy remained the mostcommon last-resort treatment for patients with glau-coma and still serves as a standard by which othercyclodestructive procedures are measured.1,9Within the past few years a significant number of

studies have demonstrated the efficacy of contactneodymium:yttrium aluminum garnet 1Nd:YAG2 la-ser photocoagulation of the ciliary body in bothanimal and human eyes.10–13 More recent research,however, has suggested the equivalence or advan-tages of semiconductor diode lasers to produce trans-scleral thermal lesions.14,15 Even though light atthe wavelength of commercially available diode la-sers 1750–850 nm2 has a lower scleral transmission

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than the wavelength of the Nd:YAG laser, diode laserwavelengths have a significantly higher absorptioncoefficient for melanin, the dominant chromophorein the ciliary epithelium. Two recent studies bySchuman and co-workers14 and Brancato et al.15 bothindicate that diode lasers produce thermal lesions ofthe rabbit ciliary body comparable with thoseachieved by the Nd:YAG laser. Moreover, the histo-logic and ultrastructural studies of Brancato et al.15indicate that diode laser radiation produces moreprofound damage to the ciliary pigmented structure,‘‘. . . causing deep coagulation necrosis of the pig-mented epithelium, wide disorganization of the colla-gen in the stroma, and intravascular coagulationphenomena in the ciliary vessels’’ 1p. 1589, Ref. 152.Such findings on the extent of coagulation necrosis ofthe ciliary body that is due to diode laser irradation,in conjuction with the technological advantages ofdiode lasers, such as their low cost, small size, longeroperating life, and use of standard current andair-cooling mechanisms, make them an attractivechoice for transscleral cyclophotocoagulation.In spite of the large number of case studies that

have been reported on the use of transscleral cyclo-photocoagulation 1TSCPC2, the choice of lasers andexposure parameters, for the most part, have beenspeculative and largely based on a clinical compari-son of results with various lasers, rather than on aclear understanding of the treatment mechanism,the optical and thermal properties of tissue, or asound theoretical model. This study, to the bestknowledge of the authors, is the first attempt toquantify the relative differences in the absorptionand transmission characteristics of all three tissuelayers involved in cyclophotocoagulation.The purpose of this study is to determine the

optical properties of the conjunctiva, sclera, and theciliary body to provide a basis for 1a2 the choice of anappropriate wavelength range for this procedure,and 1b2 a sound optical–thermal model for the laser–tissue interactions involved in TSCPC. We haveused the rabbit model, which is the most commonlyused animal model for the study of TSCPC and theprocedure’s long-term IOP-lowering effects.

A. Tissue Optics and the Radiative Transport Equation

Most of the recent advances in modeling laser–tissueinteraction have been based on the radiative trans-fer theory. This theory provides a heuristic modelthat deals directly with the transport of powerthrough turbid media. The following implicit as-sumptions must be made to apply the radiativetransfer theory to describe laser–tissue interactions:

x The tissue medium is homogeneous.x Each scattering element in the medium is suffi-

ciently isolated so that its scattering pattern isindependent of other elements.

x Scattering by all elements must be described bya single phase function.

3322 APPLIED OPTICS @ Vol. 35, No. 19 @ 1 July 1996

x Light propagation does not induce any lightsource within the medium 1e.g., fluorescence, phos-phorescence, etc.2.

x Polarization effects are neglegible.

The fundamental parameters that describe tissueoptics in terms of the radiative transfer theory arethe absorption coefficient µa 1in inverse centimeters2,the scattering coefficient µs 1also in inverse centime-ters2, and the average cosine of the scattering angleassociated with single-scattering phase function g.The application of the radiative transfer theory indescribing light propagation in tissues has beendiscussed at length by other investigators.16,17

B. Adding–Doubling Method

The adding–doublingmethod is a general, numericalsolution to the radiative transport equation. Thismethod is often chosen for solving radiative trans-port within biological media, primarily because ofthe speed of the numerical algorithms developed forthis method, as well as its flexibility in includinganisotropic scattering and internal reflection at theboundaries. Other solutions to the radiative trans-port equation, such as the Chandrasekhar X and Yfunctions,16 discrete ordinates,18 invariant embed-ding,19 or successive orders20 are generally either toocomputationally intensive 1slow2 or lack the flexibil-ity to include the necessary boundary conditionsneeded for turbid media with mismatched bound-aries.21We used an inverse adding–doubling program that

was developed by Prahl et al.21 to calculate theabsorption and scattering coefficients of tissue fromthe measured values for the total diffuse transmis-sion and reflection 1this procedure is an inversemethod, as the algorithm used is a reversal of theusual process of calculating reflection and transmis-sion from optical properties2. The algorithm for thisprogram consists of the following steps: 1a2 estimatea set of optical properties; 1b2 calculate the reflectionand transmission with the adding–doubling itera-tive method; 1c2 compare the calculated with themeasured values of reflection and transmission; 1d2repeat the above steps until a match 1within aspecified acceptance margin2 is reached. With thisiterative process the set of optical properties thatyields the closest match to the measured values ofreflection and transmission are taken as the opticalproperties of the medium.

C. Proposed Approach

In this study we use a Varian Cary 5E UV-Vis-NIRspectrophotometer to make total-transmission anddiffuse-reflectionmeasurements in the 300–1200-nmwavelength range for rabbit and porcine conjunctiva,sclera, and ciliary body. The one-dimensional in-verse adding–doubling algorithm outlined above isthen used to estimate absorption µa and scattering µscoefficients for each tissue layer, with the assump-

tion of a fixed anisotropy of 0.9. The clinical conse-quence of these results are discussed below.

2. Materials and Methods

A. Experimental Setup

The principal instrument used for our measure-mentswas a computer-drivenVarianCary 5EUV-Vis-NIR spectrophotometer with a diffuse-reflectanceaccessory 1an integrating sphere2. The system wasturned on for a minimum of 2 h prior to each set ofexperiments to establish thermal equilibrium. Tis-sue optical properties were obtained with the follow-ing experimental protocol: 1a2 A baseline was ini-tially recorded for the wavelength range of interest1300–1200 nm2 with a Labsphere standard reflec-tance plate. 1b2 For each tissue sample the thick-ness, diffuse reflectance Rd, and total transmissionTd were measured. 1c2 The diffuse-reflectance read-ings were calibrated on the basis of reflectancevalues furnished by Labsphere for the standardreflectance plates. 1d2 The inverse adding–doublingprogram was used to calculate the absorption µa andscattering µs coefficients for each sample. For thesesimulations a fixed anisotropy factor 1g 5 0.92 andrefractive index were used. A refractive index ofn 5 1.38 1Ref. 222 was used for conjunctiva and theciliary body, and the scleral refractive index 1n 5 1.422was calculated as the average of the refractive indexof the inhomogeneously distributed collagen fibrils1n 5 1.472 and of the ground substance surroundingthe fibrils 1n 5 1.362.Because the calibration data for the Labsphere

standard reflectance plates were given by the manu-facturer in increments of 50 nm, reflectance andtransmission data points were selected in incre-ments of 50 nm for the calculation of the absorptionand scattering coefficients. As such, in the analysisbelow, we have used 500 nm as an approximatewavelength for the argon laser, 550 nm for thekrypton yellow laser, 700 nm for the ruby laser, and1050 nm for the Nd:YAG laser.The spectral bandwidth was set at 2 nm. We

used a signal-averaging time of 0.067 s at a scan rateof 900 nm@min. Each scan was normalized to thebaseline that was measured and recorded at thebeginning of each measurement sequence.The following assumptions were incorporated into

the calculation of the absorption and scatteringcoefficients:

x The anisotropy of the tissue is fixed and is setequal to 0.9.

x Refractive indices of tissue samples are con-stant.

x Refractive indices of air, glass, quartz, andtissue are not a function of wavelength within thewavelength range of interest.

x The Henyey–Greenstein phase function used inthe adding–doubling algorithm provides a good ap-

proximation for single-scattering phenomena for thethree tissue layers under study.

B. Sample Preparation

The samples of conjunctiva, sclera, and ciliary bodywere extracted from the eyes of four pigmentedrabbits. The dissection and measurements on theeyes were performed within 2–4 h postmortem.After enulceation, each eye was inflated with saline.The limbal conjunctiva and Tenon’s capsule weredissected and excised with a pair of blunt Wescottscissors. A no. 64 Beaver blade was then used tooutline a 20 mm 3 10 mm section of sclera from thelimbus to the equator of the globe. Incisions weredeepened to the supra-choroidal space. The sectionof sclera was then lifted off the intact choroid andciliary body. The pars plicata was visually identi-fied as a light gray band. Several 2 mm 3 20 mmstrips of ciliary body were then excised with sharpWescott scissors. The prepared sample was thenplaced between two quartz slides 1GM, Associated,part 7525-022 and pressed in the sample assembly forthe diffuse-reflectance and transmission measure-ments required for the calculation of the absorptionand scattering coefficients.

3. Results

A total of four eyes 1one from each rabbit2 and up totwo samples from each eye were used for each tissuetype 1conjunctiva, sclera, and ciliary body2. Figures1 and 2 illustrate typical diffuse-reflectance andtransmittancemeasurements for conjunctiva, sclera,and ciliary-body tissue samples. These measure-ments were used to calculate the absorption andscattering coefficients for each specimen. Figures 3and 4 show the average absorption µa and scattering

Fig. 1. Plots of typical diffuse-reflectance measurements forrabbit conjunctiva, sclera, and ciliary body. Sample thicknesses:tconjunctiva 5 150 µm, tsclera 5 425 µm, and tciliary body 5 125 µm.


µs coefficients for the three tissue types under inves-tigation.

A. Rabbit Conjunctiva

Three specimens of rabbit conjunctiva were used formeasurements, with an average measured thicknessof 158 µm 1standard deviation SD 5 38 µm2. Theabsorption coefficient of the conjunctiva remainsfairly small 1average value of µa < 0.09–0.86 cm212for the entire spectrum under study. The absorp-tion coefficient, on the other hand, is approximately10 fold smaller for the 1050-nm wavelength, ascompared with the µa for the 300-nm wavelength.The absorption coefficient for the argon laser wave-length 1500 nm2 is approximately twice that for thediode 1850 nm2 and the Nd:YAG 1approximately 1050nm2 laser wavelengths, but because the values are sosmall, it is unlikely that there would be a significant

Fig. 2. Plots of typical total-transmittance measurements forrabbit conjunctiva, sclera, and ciliary body. Sample thicknesses:tconjunctiva 5 150 µm, tsclera 5 425 µm, and tciliary body 5 125 µm.

Fig. 3. Plots of the average absorption coefficient µa versus thewavelength of rabbit conjunctiva, sclera, and ciliary body. Theerror bars represent the respective standard errors. Number ofsamples: nconjunctiva 5 3, nsclera 5 8, and nciliary body 5 8.


difference in the attenuation of light caused byconjunctival absorption for these three wavelengths.The scattering coefficients are significantly larger

than the absorption coefficient for this layer andrange from 9.95 cm21 for the 1200-nm wavelength to59.1 cm21 for the 300-nm wavelength, indicatingthat the primary mechanism of attenuation in theconjunctiva, for the wavelength range under study isdue to scattering.Table 1 lists the average values for the absorption

and scattering coefficients of conjunctiva, for thewavelengths of argon 1approximately 500 nm2, kryp-ton yellow 1approximately 550 nm2, ruby 1approxi-mately 700 nm2, diode 1850 nm for GaAs diode laser2,and Nd:YAG 1approximately 1050 nm2 lasers. Allthe above lasers have been previously, or are pres-ently, under investigation as potential sources fortransscleral cyclophotocoagulation.

B. Rabbit Sclera

Eight samples of rabbit sclerawere used formeasure-ments, with an average measured thickness of 263

Fig. 4. Plots of the average scattering coefficient µs versus thewavelength of rabbit conjunctiva, sclera, and ciliary body. Theerror bars represent the respective standard errors. Number ofsamples: nconjunctiva 5 3, nsclera 5 8, and nciliary body 5 8. g 5 0.9.

Table 1. Average Absorption ma and Scattering ms Coefficients forRabbit Conjunctiva at Various Wavelengths a

Wavelength 1nm2

Conjunctiva Absortion andScattering Coefficients

µa 1cm212 µs 1cm212

500 0.14 6 0.08 19.40 6 9.78550 0.18 6 0.09 17.07 6 7.25700 0.06 6 0.03 11.55 6 4.74850 0.07 6 0.04 9.54 6 3.321050 0.05 6 0.04 8.41 6 3.06

aThe values reported are the average values, plus and minusthe corresponding SD. g 5 0.9.

µm 1SD 5 105 µm2. Table 2 lists the calculatedabsorption and scattering coefficients for the wave-lengths of the argon, krypton yellow, ruby, diode, andNd:YAG lasers. As was the case with the conjunc-tiva, the absorption coefficient of the sclera is fairlysmall 1µa < 0.12–1.09 cm212 for the wavelength rangeunder study, with a steady 1approximately 10-fold2drop across the 300–1200-nm wavelength range.The scattering coefficient, however, is substan-

tially larger than the absorption coefficient, indicat-ing that the primary mechanism of light attenuationin sclera, particularly in the lower 1visible2 wave-lengths, is attributable to scattering. Notice thatthe absorption coefficient for the argon laser wave-length 1500 nm2 is only 2.8 times higher than that forthe Nd:YAG laser wavelength 11050 nm2, as com-pared with the value for the scattering coefficient,which is more than 5 times higher for the argon laserwavelength.

C. Rabbit Ciliary Body

Eight samples of rabbit ciliary body 1ciliary muscleand pigmented epithelium2 were used for measure-ments, with an average thickness of 428 µm 1SD 5 84µm2. Table 3 lists the calculated averages for theabsorption and scattering coefficients of rabbit cili-ary body 1ciliary muscle and the ciliary pigmentepithelium2 for the five wavelengths specified above.The average values indicate a steady exponentialdrop 1see Table 32 in the absorption coefficient thatmimics the absorption characteristics of the chromo-phore melanin, which is the primary chromophore inthe ciliary body of the enucleated eye. Notice thatthe absorption coefficient of the ciliary body for theargon laser wavelength 1µa 5 5.28 cm212 is more than6 times higher than that for the Nd:YAG laserwavelength 1µa 5 0.82 cm212.

4. Discussion

The aim in transscleral cyclophotocoagulation is toachieve focal cyclodestruction at the ciliary pig-mented epithelium without causing excessive dam-age to the tissues adjacent to this layer. Transcleralirradiation must travel through the conjunctiva, thewhite 1translucent2 sclera, and through the ciliarymuscle 1which is highly vacularized2 before reachingthe ciliary pigmented epithelium. Light therefore

Table 2. Average Absorption ma and Scattering ms Coefficients forRabbit Sclera at Various Wavelengths

Wavelength 1nm2

Sclera Absorption and Scattering Coefficients


500 0.39 6 0.12 85.96 6 29.08550 0.37 6 0.11 75.54 6 25.16700 0.22 6 0.06 50.40 6 15.39850 0.16 6 0.05 29.83 6 7.501050 0.14 6 0.06 16.28 6 3.20

aThe values reported are the average values, plus and minusthe SD. g 5 0.9.

attenuates significantly prior to reaching the target-tissue layer for cyclophotocoagulation. To maxi-mize therapeutic effects, it is important to choose anirradiation wavelength that has a relatively lowattenuation 1high transmission2 through the conjunc-tiva and sclera, and a high absorption within theciliary pigmented epithelium. The latter consider-ation has been validated by previous studies compar-ing laser effects in pigmented and albino rabbits.23These studies report a direct correlation between theextent of light absorption within the ciliary body andthe efficacy of cyclophotocoagulation in loweringintraocular pressure. Of the chromophores presentin the ciliary body, the most pronounced is melanin,which is dispersed throughout the ciliary muscle andis highly concentrated in the pigmented epithelium.One of the objectives of this study was to provide a

comparison of the scattering and absorption charac-teristics of a range of laser sources through thetissue layers involved in cyclophotocoagulation.Figures 3 and 4 demonstrate that the attenuation oflight within the thin layer of the conjunctiva isrelatively low inmagnitude and does not vary signifi-cantly over the spectral range under study. Scatter-ing far outweighs absorption in the sclera over thesame wavelength range. Table 2 shows that thescattering coefficient for the argon laser wavelengthis more than 5 times larger than that for the Nd:YAGlaser wavelength. It is therefore evident that thelower scleral transmission represents a major ob-stacle for the use of laser sources in the shorter-wavelength range.The benefit in the use of shorter-wavelength la-

sers, however, is in their higher absorption withinthe target-tissue layer, the ciliary body. Table 3indicates that the absorption of argon laser lightwithin the ciliary body is more than 6 times higherthan that for the Nd:YAG laser wavelength. Forlasers in the shorter-wavelength range, therefore,the lower scleral transmission is offset by the extentof absorption 1thermolysis2 within the ciliary body.These results suggest the utility of visible-wave-length lasers for cyclophotocoagulation, providedthat proper measures are taken to enhance scleraltransmission. One approach is the use of contactversus noncontact delivery of laser light.Noncontact transscleral cyclophotocoagulation has

Table 3. Average Absorption ma and Scattering ms Coefficients forRabbit Ciliary Body at Various Wavelengths

Wavelength1nm2

Ciliary Body Absorptionand Scattering Coefficients


500 5.28 6 2.86 65.75 6 38.84550 5.12 6 2.77 64.18 6 36.97700 4.08 6 2.07 59.66 6 29.32850 2.39 6 1.10 51.18 6 22.411050 0.82 6 0.35 49.40 6 19.62

aThe values reported are the average values, plus and minusthe SD. g 5 0.9.


been abandoned, and the majority of clinics pres-ently perform the procedure by means of a contactfiber-optic probe. Vogel et al.24 have demonstratedthat the difference in scleral transmission dimin-ishes with fiber contact, if strong pressure is appliedto the sclera. The increase of transmission result-ing from fiber contact may be explained by thedisplacement of the ground substance that is causedby the pressure of the fiber tip. The thinning of thesclera and the reduction of the distance betweencollagen fibrils 1because of the pressure exerted bythe fiber2 leads to changes in the interference of thelight scattered from adjacent fibrils.24 Becausemorewater than proteins or mucopolysaccharides aredisplaced, the concentration of the remaining groundsubstance increases, and its refractive index be-comes closer to that of the collagen fibrils.25 As aresult, when contact fibers are used, the scattering inthe sclera is reduced, and consequently the trans-scleral transmission is increased. These effects arestronger when increased pressure is applied to thesclera.24 Fiber contact also leads to an increase inthe percentage of light transmitted in the forwarddirection, which in turn reduces the energy require-ments for the delivered laser light.In summary, from the measured values of the

absorption and scattering coefficients, it is reason-able to hypothesize that the gain in melanin absorp-tion in the visible-wavelength range would morethan offset the decrease in scleral transmission overthe same wavelength range. This hypothesis issupported by our preliminary Monte Carlo simula-tion of light propagation in the multilayered tissuestructure, which suggests that the rate of heatgeneration 1or absorption-energy density2 within theciliary pigmented epithelium is more than 4 timeshigher for the argon 1500-nm2 laser wavelength, ascompared with the Nd:YAG 11050-nm2 laser wave-length. These results are based on the opticalproperties reported here for the rabbit model, whichhas been used extensively in the past as a convenientanimal model to evaluate transscleral cyclophotoco-agulation. Extrapolation of these results to thehuman model, however, would require the applica-tion of the same methods and analysis describedabove to characterize the optical properties of con-junctiva, sclera, and ciliary body excised from freshhuman eyes.

5. Conclusions

In this study we have measured the optical proper-ties of rabbit conjunctiva, sclera, and ciliary body inan effort to characterize light propagation in tissueduring cyclophotocoagulation. These optical proper-ties indicate that the choice of a desirable lasersource for TSCPC must be based on a trade-offbetween attenuation within the superficial layers ofconjunctiva and sclera and absorption within thetarget tissue, i.e., the ciliary body. Longer wave-lengths offer the highest transmission through theproximal tissue layers, whereas shorter wavelengthsabsorb mostly in the ciliary body. In addition to a


qualitative description of the optical events duringcyclophotocoagulation, the results also provide aquantitative basis for an optical–thermal model tocalculate the distribution of light within themultilay-ered tissue structure under irradiation.

A. J. Welch is the Marion E. Forsman CentennialProfessor of Electrical and Computer Engineeringand Biomedical Engineering.This research was supported in part by The Office

of Naval Research 1grant N00014-91-J-15642, Depart-ment of Energy 1DE-FG05-91ER6172262 and a grantfrom Coherent, Inc.

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