British Journal of Ophthalmology 1995; 79: 672-677

ORIGINAL ARTICLES - Laboratory science

Irradiation of rabbit retina with diode andNd:YAG lasers

Dominic McHugh, Ceri England, Eugen van der Zypen, John Marshall,Franz Fankhauser, Sylwia Fankhauser-Kwasnieska

AbstractAims-This study was carried out tocompare the effects of continuous waveinfrared laser radiation on pigmentedand albino rabbit retinas at two wave-lengths: 810 nm (diode) and 1064 nm(Nd:YAG).Methods-Transpupillary laser pulseswere applied with a spot size of 200 ,umand durations of 200 ms (pigmentedrabbits) and 05-1 s (albino rabbits).Light and electron microscopic analyseswere performed immediately afterexposure.Results-In pigmented rabbits, thresholdlesions were induced using a power of100 mW with the diode and 200 mWwith the Nd:YAG lasers. Damage wasincurred by the retinal pigment epithe-lium with extension into the superficialand mid choroid posteriorly and into theouter retina anteriorly. In albino rabbits,lesions of comparable anteroposteriorextension were identified using a powerof 10 W with the Nd:YAG laser. Usingdiode laser irradiation, a maximumpower output of 1-2 W failed to producediscernible lesions.Conclusions-The observed patterns ofmorphological damage are produced bycomplex tissue radiation interactions. Inpigmented animals, this was primarilyrelated to absorption ofradiant energy bymelanin within the retinal pigmentepithelium and the choroidal melano-cytes. In albino rabbits, laser inducedeffects occurred as a consequence ofmultiple scattering, together with absorp-tion within haemoglobin and possibly alsowithin tissue water. The data obtainedprovide further insight into the biologicalmechanisms arising from retinalphotocoagulation with near infraredlasers.(BrJ Ophthalmol 1995; 79: 672-677)

Photocoagulation has been employed in thetreatment of retinal conditions for over40 years. Meyer-Schwickerath initially usedfocused sunlight and subsequently the xenonarc photocoagulator, which provided asource of broad band optical radiation and

successfully produced full thickness chorio-retinal lesions.' Xenon arc devices are ofproved effectiveness in the treatment of pro-liferative diabetic retinopathy2 and are stillcommonly used in retinal therapy.

After its introduction in 1960,3 the rubylaser (emitting at 694-3 nm) aroused interestamong ophthalmologists. Although it wasreasonably successful in producing chorio-retinal adhesions in the treatment ofretinal breaks, results obtained in treatingretinal vascular conditions were disappoint-ing.4

Lasers emitting at other wavelengths weresubsequently developed and adapted for usein ophthalmology. These include the argon(488-515.5 nm), the krypton red (647 nm),and the tunable dye lasers. Many studies havedemonstrated their efficacy in the treatment ofcommon retinal conditions, such as prolifera-tive diabetic retinopathy,5 forms of diabeticmaculopathy,6 the complications ensuing fromretinal vein thrombosis,7 and subretinal neo-vascular membranes.8

Although argon, krypton, and dye lasershave different emission wavelengths theireffects are broadly similar in terms of bothretinal damage and therapeutic efficacy. Theseobservations lend support to the view thatwavelength is relatively unimportant as a deter-minant of clinical response. The advent ofsolid state continuous wave diode (810 nm)and Nd:YAG (1064 nm) lasers allows this con-cept to be tested in relation to tissue irradiationwith near infrared energy. Analysis of diodeand Nd:YAG laser retinal lesions in pilotstudies have indicated that they are similar tothose produced by conventional clinical photo-coagulators and in particular to those inducedusing krypton lasers.9-12 Initial clinical studieshave also demonstrated comparable resultswith earlier trials employing argon and kryptonlasers.13 14The aim of the current study was to

compare the morphological effects of con-tinuous wave diode and Nd:YAG irradiationon rabbit retina, thereby gaining a clearerinsight into the thermal damage processesinduced after laser tissue interactions. It wasanticipated that the information obtainedwould help to optimise treatment variables forperforming near infrared laser retinal photo-coagulation.

Moorfields EyeHospital, LondonD McHugh

Institute ofAnatomy,University ofBern,Bern, SwitzerlandC EnglandE van der Zypen

Department ofOphthalmology, StThomas's Hospital,LondonJ Marshall

Lindenhof Hospital,Bern, SwitzerlandF FankhauserS Fankhauser-Kwasniewska

Correspondence to:Dominic McHugh,Department ofOphthalmology, King'sCollege Hospital, DenmarkHill, London SE5 9RS.Accepted for publication2 March 1995

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Irradiation of rabbit retina with diode and Nd:YAG lasers

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Figure 1 Light micrographs of acute retinal lesions produced in pigmented rabbits using(a) diode (power 250 mW; pulse duration 200 ms) and (b) Nd:YAG (power 800 mW;pulse duration 200 ms) laser radiation. Each impact is sharply defined laterally, theextension in this direction depending on the pulse power employed and is characterised by acentral, strongly coagulated region exhibiting minimal structural distortion and peripheralzones manifesting predominantly swelling and disruptive phenomena. In the meridionaldirection, strong coagulative effects also give way to swelling and disruptive ones, the degreeof inner extension depending upon the pulse power used. In (b), these latter phenomenacommence at, and are limited predominantly to, the outer nuclear layer which exhibits areduction in nuclei density; whereas in (a), they begin at the border between the outernuclear and outer plexiform layers and extend to the inner limiting membrane, thus givingrise to a prominent inner buckling of the sensory retina. Semi-thin sections stained withtoluidine blue. Negative magnifications: (a) X26; (b) X39.

Materials and methods

LASERSThe diode laser used in these studies was aportable device (Microlase, Keeler HoldingsPlc, Windsor, UK), which could be mountedon a Haag-Streit slit-lamp microscope (Haag-Streit, Bern, Switzerland). The cone angle ofthe treatment beam was 14 degrees; the aim-ing beam was furnished by a second diodelaser source (wavelength 670 nm). Selectedspot size was 200 p,m and pulse duration200 ms (pigmented rabbits), or 990 ms(albino rabbits). The maximum availablepower was 1 2 W.A Nd:YAG laser operating in the con-

tinuous wave mode was employed (MR3Meridian, Bern, Switzerland). The coneangle of the treatment beam was 9 degreesand aiming was accomplished with a heliumneon laser (wavelength 632 nm). Selectedspot size was 200 p,m, and pulse duration200 ms (pigmented rabbits) or 0-5-1 s (albinorabbits). The maximum available power was10W.

RABBITSAll procedures were conducted in compliancewith the ARVO statement for the use ofanimals in ophthalmic and vision research.General anaesthesia (Rompun-Ketalar) wasinduced in four pigmented and two albinorabbits. Pupillary mydriasis was induced usingcyclopentolate drops 1%. The retina ofone eyein each animal was irradiated through aplanoconcave Goldmann contact lens witheither the Nd:YAG or diode lasers. The energyrequired to produce a visible reaction wasdetermined in preliminary experiments byincreasing pulse power in 100 mW incrementsfrom subthreshold values. Impacts were deliv-ered to the mid-peripheral region of the retinainferior to the myelinated fibre layer. Thepower was increased in 50 mW (diode), or200-300 mW (Nd:YAG) increments to pro-duce progressively more intense lesions.

TISSUE PREPARATIONAnimals were killed by an overdose of sodiumpentobarbitone immediately after irradiation.They were then perfused via the aorta, initiallywith Ringer's solution (containing procainehydrochloride (5 g/l) and heparin (25 000 U/1))at 37°C and then with 2-5% (v/v)glutaraldehyde solution (in 90 mM phosphatebuffer, pH 7 4, 350 mosmol) at 4°C. Perfusionpressure was maintained within the range115-120 mm Hg.The eyes were enucleated and transferred

to glutaraldehyde solution (as above), withinwhich they were divided into anterior andposterior segments by cutting slightly pos-terior to the ora serrata. After fixationovernight at 4°C, lesions were photographedwith a Wild M400 biomicroscope. Impactsites were further dissected for light (LM) andtransmission electron (TEM) microscopy.Tissue blocks were washed three times in 90mM phosphate buffer (pH 7 4, 350 mosmol),postfixed in 2% (w/v) osmium tetroxidesolution for 3 hours, stained with uranylacetate (0-5% (w/v) in 50 mM maleatebuffer), and then dehydrated in a gradedseries of increasing ethanol concentrationbefore embedding in Epon. Sections were cuton a Reichert-Jung Ultracut E, ultramicro-tome. Semi-thin (-3-4 ,um) sections werephotographed in a Vanox photomicroscope;ultrathin sections (-70 nm) were stained with7% (w/v) lead citrate and 6% (w/v) uranylacetate, and examined in a Philips EM-300electron microscope.

Results

ACUTE LESIONS

Ophthalmoscopicdbiomicroscopic appearancesPigmented rabbits. Ophthalmoscopically visiblelesions were produced using powers of 100 mW(diode laser) and 200 mW (Nd:YAG laser) anda pulse duration of200 ms. More intense effectswere realised with each laser using higher pulsepowers.

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McHugh, England, van der Zypen, Marshall, Fankhauser, Fankhauser-Kwasniewska

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Figure 2 Transmission electron micrograph depicting pigmented retinal epithelium andinner choroid of impact centre after irradiation with the diode laser (power 250 mW; pulseduration 200 ms; acute lesion). Bruch 's membrane remains intact, although constituentcollagen fibrils exhibit signs of thermal damage (increased cross sectional diameter). Theendothelium of the choriocapillaris illustrated has undergone coagulation; within the vessellumen, heat precipitated proteins and damaged erythrocytes (Er) are to be seen. In thestroma, both normal and thermally damaged collagenfibrils are apparent. Fb= coagulatedcytoplasmic process ofa fibroblast. Negative magnification: X 2175.

Albino rabbits. Nd:YAG laser radiation pro-duced clearly visible lesions, with an alteredlight reflex at a power of 8 W and an exposureduration of 500 ms; a more pronounced reac-tion was realised using a 10 W/1 s combina-tion. The diode laser failed to produce either avisible response or any light microscopicchange at its maximum power output (1I 2 W).

MicroscopyPigmented rabbits. At the light microscopiclevel, diode and Nd:YAG laser radiation

induced lesions of similar morphologicalappearance, differences in lateral and meri-dional extensions being a function of the pulsepower employed.

Lesions were sharply defined laterally(Fig 1), and in sections traversing the impactcore two zones could be distinguished. At thecentre, the tissue showed the least structuraldisturbance. At low pulse powers, this effectextended from the pigmented retinal epithe-lium to the inner segments of photoreceptorcells, whereas at higher powers their perikaryawere also included, as evidenced by the com-pact appearance of the outer nuclear layer(Fig la). A characteristic band of enhancedstaining affinity at the level of inner segments(Fig lb) denoted intense thermal damage.The inner boundary of coagulated tissuewas recognised by an abrupt dislocation,decreased compactness, and increased struc-tural disturbance of the adjacent layers, sinceregions which had incurred minimal thermalinsult were more susceptible to secondaryswelling and distortion during the post-irradi-ation period. At low pulse powers, this effectwas limited principally to the outer nuclearlayer, whereas at higher powers it commencedat the border between outer nuclear and outerplexiform layers and extended to a variabledegree inwards. The swelling thereby in-curred gave rise to an inward buckling of thesensory retina (Fig la). External to the pig-mented retinal epithelium, coagulation of thechoriocapillaris was observed and the lateralextension of this response corresponded wellwith the lesion borders in the retinal pigmentepithelium (Fig lb). Coagulative effect

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Figure 3 Light micrograph of acute retinal lesion produced in albino rabbit using Nd:YAG laser radiation (power 8 W;pulse duration 500 ms). At the impact centre, photoreceptor cell outer and inner segments are strongly coagulated, asindicated by the minimal structural disturbance manifested in these layers. The outer nuclear layer exhibits both thermal(intensely stained nuclei) and swelling phenomena (reduction in nuclei density); strata further inwards revealpredominantly the latter effects, thus giving rise to buckling. In the lateral direction, peripheral regions also manifestpredominantly swelling/disruptive phenomena; note the severe structural disturbance incurred at the levels ofphotoreceptorcell outer and inner segments. Within the choriocapillaris, no signs of bloodflow stasis are apparent. Semi-thin sectionstained with toluidine blue. Negative magnification: x 55.

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Irradiation of rabbit retina with diode and Nd:YAG lasers

Table 1 Approximate percentages of transmission andabsorption for diode and Nd:YAG laser retinalphotocoagulation in rabbits

Diode Nd:YAG810 nm 1064 nm

Transmission (%/6) 98 70Absorption (O/6)Melanin* 35 12Melanint 7 2Oxyhaemoglobin31 8 8Reduced haemoglobin" 8 <1Water (cm-1)35 0 4 0 04

*Retinal pigment epithelium and choroid.tRetinal pigment epithelium alone.26

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cytoplasm exhibited the granulation effecttypical of coagulated cells. Within capillarylumens, signs of coagulation were evinced bytheir fine floccular appearance, this manifesta-tion being engendered by heat induced precip-itation of plasma proteins.Albino rabbits. Similar phenomena to thosedescribed for pigmented rabbits were observedin albino animals using Nd:YAG laser radia-tion. A notable exception was the choriocapil-laris, which exhibited no signs of blood flowstasis (Fig 3).

Ultrastructural changes to the non-pig-mented retinal epithelium (Fig 4) werecomparable with those described for pig-mented rabbits. Within the choroid, thermaldamage was incurred both by stromal com-ponents (Fig 4) and vascular endothelial cells,but signs of blood flow stasis were not mani-fested.

DiscussionThis study represents the first direct com-parison of retinal lesion morphology afterirradiation with continuous wave diode andNd:YAG laser. Radiation from each laserinduced impacts of comparable appearance inpigmented rabbits, although higher pulseenergies were required to realise moderateeffects with Nd:YAG as compared with diodelaser irradiation. In albinos, visible laser bumswere produced only by exposure to Nd:YAGlaser energy. With both lasers and in pig-mented and non-pigmented fundi, lesionswere produced with an epicentre locatedwithin the retinal pigment epithelium.The findings may be explained in terms of

the relative beam tissue interaction characteris-tics of diode (810 nm) and Nd:YAG (1064nm) lasers. There are four principal com-ponents to this process - namely, the trans-mission, scatter, and absorption of radiationwithin the target tissue, and the morphologicalexpression of their combined effects.

Transpupillary retinal irradiation is in-fluenced by the transmission characteristicsthrough the ocular media of the wavelengthselected. Although transmission is high forboth diode and Nd:YAG lasers, it is approxi-mately 30% greater in the former than in thelatter,'5 16 with a consequently higher irradia-tion at the retina for any given exposure(Table 1).The intrinsic optical properties of a tissue

will influence the degree of scattering and

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McHugh, England, van der Zypen, Marshall, Fankhauser, Fankhauser-Kwasniewska

absorption and thus the distribution of radiantenergy within it. Scatter increases withdecreasing wavelength of incident radiationand also with increasing tissue thickness17;hence, for exposures in the near infrared regionof the spectrum, it will be less than at visiblewavelengths. In the presence of melanin,located within the pigmented retinal epithe-lium and choroid, the influence of primaryabsorption will dominate over that of photonscatter in inducing an absorption event. In thealbino retina, which lacks melanin, internalscatter must assume a greater significance,with the increased pathlength of a scatteredphoton increasing the possibility of absorptionoccurring within the tissue.

Within the time domain between 100 ms to10 second exposures, lesions are produced byphotocoagulation.18 This process involves theabsorption of radiant energy by a chromo-phore, and its conversion to heat by linear opti-cal processes. The amount of energy absorbedby a pigment is a complex function of wave-length and energy of the incident radiation, aswell as of pigment density and the pathlengthover which the chromophore is distributed.'9The kinetics of coagulation are temperature

and time dependent. A sustained temperatureelevation of 10-20°C above the physiologicallevel will result in disruption of enzymaticprocesses, protein denaturation, and the pro-duction of a threshold lesion.2021 If collage-nous tissue is heated to 47°C above bodytemperature, collagen fibrils disintegrate intosubfibrillar units.22 23 In practice, the peaktemperature achieved at the centre of retinallesions following photocoagulation may be inexcess of 1000C21 24 and at this level, collagenfibrils are no longer recognisable as discreteentities, a more or less homogeneous massbeing produced.Thermal diffusion from the centre of

primary absorption will modify the damageprofile of the lesion, this process being relatedto the density, specific heat and thermaldiffusivity of the tissue, the rate of depositionof photon energy, and the peak temperatureelevation.25The chromophores which have been identi-

fied as the primary sites of absorption in retinallaser irradiation are melanin within the pig-mented retinal epithelium and choroidalmelanocytes and haemoglobin within theretinal and choroidal vasculature. Althoughintraretinal vessels are absent in the rabbitneuroretina, it is in the nature of infrared laserretinal photocoagulation that the principalzone of thermal destruction is centred uponthe retinal pigment epithelium and innerchoroid with some extension of tissue damageto the outer retina and mid choroid. Previoushistological studies of diode laser irradiation ofhuman retina have shown no evidence of laserrelated damage to vascular elements in theneurosensory retina. This would be predictablegiven a low absorption ofany infrared radiationwithin haemoglobin. Although vascular flowmay serve to dissipate any locally generatedheat transients, again, previous studies appearto indicate that this would be a relatively minor

effect.9 10 The higher absorption of 810 nmcompared with 1064 nm radiation withinmelanin26 27 (Table 1) explains the differencein pulse powers required to produce moder-ately intense lesions.The retinal damage profiles induced by diode

and Nd:YAG laser exposures reflect thedistribution of melanin within the pigmentedretinal epithelium and choroid. The totalamount of optical radiation absorbed within thechoroid will exceed that dissipated by the pig-mented retinal epithelium, owing to the largertotal amount of melanin within the former.However, although the total pigmentation ofthepigmented retinal epithelium is significantly lessthan that within the choroid, it is confined to alayer 5-10 p,m thick, whereas in the choroid itmay extend over 200-400 ,um.9 Thus for anygiven exposure, the absorbed energy per unitpathlength is far greater in the pigmented retinalepithelium and consequently, higher tempera-tures are generated within this layer.

In the current investigation, the morpho-logical appearance of burns corroboratesthese arguments: the primary site of damagewas located within the pigmented retinalepithelium, with a meridionally deeper zone ofdamage being incurred by the underlyingchoroid. Changes observed in the overlyingsensory retina may be ascribed principally tothermal flow from the pigmented retinalepithelium. The histological and ultrastruc-tural observations are in agreement with thoseof other studies relating to diode laser retinalirradiation9 28 29 and Nd:YAG laser.30That thermal damage was observed in

albino rabbit retinas following exposure toNd:YAG (but not diode) laser radiation sug-gests, naturally, the existence of an absorbingmedium other than melanin. Another pre-requisite appears to be a sufficiently highradiant exposure, given that a pulse energy of10 J was required to produce visible lesions.At high irradiances, haemoglobin within the

blood of choroidal vessels could absorb suffi-cient energy to induce thermal damage,although the absolute values for absorption ofnear infrared radiation within this tissue arelow3l (Table 1). Initiation of haemoglobindenaturation induces changes in the absorptiveproperties of blood, this being related to thechanges in light scattering properties and pos-sibly also to an increase in intraluminal fluiddensity caused by evaporation. These factorsmay serve to enhance the process of intravas-cular absorption of infrared energy and thusincrease the likelihood of thermal damage toadjacent structures.32-34 On the basis of thisargument, the absence of blood flow stasis inthe choriocapillaris was a somewhat surprisingfinding, given that the patterns of thermaldamage observed in choroidal vessel walls andin the surrounding stroma, as well as in theretina, were otherwise similar to those realisedin pigmented rabbits.Another absorbing medium which may pos-

sibly be relevant to albino exposures is water.Radiation at 1064 nm is absorbed to a slightextent only in water and that at 810 nm to aneven lesser degree35 (Table 1). However, at

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Irradiation of rabbit retina with diode and Nd:YAG lasers

high irradiances, it is possible that the combi-nation of a high photon density, with internaltissue scattering may be sufficient to induceabsorption events even within water, such thata lesion is produced. Although the absorptionof 810 nm radiation within blood is similar tothat at 1064 nm, its negligible absorptionwithin water and the lower maximum powerpotential of the system afford an explanationfor the lack of detectable lesions in albinoretinas exposed to diode laser irradiation.

Although the lasers described are relativelyrecent developments, there is increasinginterest in their clinical applications. Doubtshave been raised, however, as to their suit-ability for retinal therapy, particularly in rela-tion to their potential for inducing choroidaldamage.36 However, the recanalisation of thechoroidal vasculature which had occurred by 6weeks indicates the reversible nature of thedamage in this region. Clinical use of the diodelaser in the treatment of diabetic retinopathyhas failed to demonstrate any lasting adverseeffects on the choroidal vasculature.13 It mayalso be argued that a system which has a rela-tively greater penetration into the choroid thanoccurs with shorter wavelength systems,28 maybe more suitable for the treatment of choroidallesions. Confirmatory evidence is provided bystudies indicating the efficacy of diode laserphotocoagulation in the treatment of choroidalneovascular membranes.37 The low absorptionof infrared radiation within blood may also beof benefit in eyes with a haemorrhagic vitreousor preretinal opacities. Transmission will behigher than with the commonly used argonlaser (emitting at 488-514-5 nm) and thereforethe potential effectiveness of retinal coagula-tion will be enhanced. Again, there is clinicalevidence in support of this concept.13

In summary, the morphological effects ofnear infrared radiation upon retinal tissue are aconsequence of scattering and absorptiveevents within melanin of the pigmented retinalepithelium and choroid in pigmented eyes andpossibly within blood and water within thechoroid of albino eyes. No evidence was foundto contraindicate the clinical use of either laserand in certain situations their employment mayhave definite advantages.This study was supported by grants from the Swiss NationalScience Foundation (No 32.27748.89) and the SwissCommission for the promotion of Scientific Research (No1835).The authors are indebted to Wanda Giodano and Susanne

Zimmerman for their technical expertise.

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