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Research ArticleDry Eye Disease following Refractive Surgery: A 12-MonthFollow-Up of SMILE versus FS-LASIK in High Myopia

Bingjie Wang,1 Rajeev K. Naidu,2 Renyuan Chu,1 Jinhui Dai,1 Xiaomei Qu,1 and Hao Zhou1

Key Myopia Laboratory of Chinese Health Ministry, Department of Ophthalmology, Eye & EN Hospital, Fudan University,No. , Fenyang Road, Shanghai , China

Te University of Sydney, Camperdown, NSW , Australia

Correspondence should be addressed to Hao Zhou; [email protected]

Received July ; Revised October ; Accepted October

Academic Editor: George Kymionis

Copyright © Bingjie Wang et al. Tis is an open access article distributed under the Creative Commons Attribution License,which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Purpose. o compare dry eye disease ollowing SMILE versus FS-LASIK. Design. Prospective, nonrandomised, observational study.Patients. patients undergoing reractive surgery or myopia were included. eyes underwent SMILE and eyes underwentFS-LASIK. Methods. Evaluation o dry eye disease was conducted preoperatively and at , , , and months postoperatively,using the Salisbury Eye Evaluation Questionnaire (SEEQ) and BU. Results. BU reduced ollowing SMILE at and months( < 0.001) and at , , and months ollowing FS-LASIK ( < 0.001). BU was greater ollowing SMILE than FS-LASIK at ,, and months ( < 0.001, < 0.001, and = 0.009, resp.). SEEQ scores increased (greater symptoms) ollowing SMILE at month ( < 0.001) and months ( = 0.003) and at , , and months ollowing FS-LASIK ( < 0.001). SMILE produced lowerSEEQ scores (ewer symptoms) than FS-LASIK at , , and months ( < 0.001). Conclusion. SMILE produces less dry eye diseasethan FS-LASIK at months postoperatively but demonstrates similar degrees o dry eye disease at months.

1. Introduction

Dry eye disease is a common ocular surace disease andplays a signicant role in the ocular comort and visualperormance o patients, with the potential to have a greatimpact on their quality o lie [–]. Dry eye is known to be arequently reported and observed nding ollowing reractivesurgery, particularly in the period immediately ollowing

surgery [–]. With reractive surgery cases increasing innumber, dry eye is becoming an increasing challenge orreractive surgeons to overcome, with a large proportion o patients experiencing dry eye symptoms to varying degrees[, , –]. Dry eye has also been associated with a delayedwound healing response and may predispose patients toreractive regression in moderate to severe cases [, ].

While the pathophysiology o this complication is stillevolving, a number o theories have been proposed to explainwhy dry eye occurs ollowing reractive surgery, includingexacerbation o preexisting dry eye disease [], medicamen-tosa rom postoperative medications [, ], and damage toconjunctival goblet cells increasing tear hyperosmolarity and

inammation [, –]. Te interaction between the ocularsurace and eyelids is an important actor in maintainingtear production and ow, which is also altered ollowingsurgery [, ]. Perhaps the biggest actor, however, is theimpact surgery has on corneal nerves and sensation [, ,, ]. Intact corneal sensation is required oradequate blink requency and tear production, and corneal denervationresulting rom disruption and damage to corneal nerves has

been shown to play a signicant role in the development o dry eye disease ollowing reractive surgery [–].

Laser-assisted in situ keratomileusis (LASIK) continuesto be a popular reractive surgical option [, ]; however,almost hal o all LASIK patients continue to report dry eye symptoms ollowing surgery []. Te introduction o theemtosecond laser (FS) has seen FS-LASIK become a moreaccurate and sae surgical option, with a reduced rate o dry eye disease, which is likely due to reduced neurotrophiceffects on the corneal nerves during ormation o the cornealap []. A recent advancement in reractive surgery hasbeen small-incision lenticule extraction (SMILE), which wasestablished as a “apless” procedure in which an intrastromal

Hindawi Publishing CorporationJournal of Ophthalmology Volume 2015, Article ID 132417, 8 pageshttp://dx.doi.org/10.1155/2015/132417

http://dx.doi.org/10.1155/2015/132417http://dx.doi.org/10.1155/2015/132417


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Journal o Ophthalmology

lenticule is cut by a emtosecond laser and manually extractedthrough a peripheral corneal tunnel incision. Te reractivepredictability, saety, and patient satisaction o SMILE arecomparable to FS-LASIK. SMILE has the benet o beingminimally invasive, with a lesser degree o damage to thecornea and corneal nerves, and may thereore result in ewer

complications and reduced symptoms o dry eye []. Te key difference between FS-LASIK and SMILE and their impacton corneal innervation may lie in the act that FS-LASIKaffects the epithelium and anterior stroma, thus resulting ingreater resection o the sensory nerves o the cornea [–],while SMILE affects the posterior stromal bed with relatively greater preservation o the corneal subbasal nerve plexus [].

Few studies exist in the literature investigating the long-term effects o reractive surgery, specically comparingboth SMILE and FS-LASIK, on the development o dry eye syndromes. In this prospective observational study, wepresent the ndings o the objectively measured clinical signsand subjective reporting o dry eye symptoms ollowing

SMILE versus FS-LASIK or the correction o myopia in alarge group o demographically similar patients over a periodo months postoperatively.

2. Methods

.. Setting and Design. Tis institutional, prospective, observational study was approved prospectively by the institutionalreview board o Te Eye and EN Hospital o Fudan Univer-sity. Written inormed consent was obtained rom all patientsprior to participating in the study. Te study adhered to theguidelines and principles o the Declaration o Helsinki.

.. Patients. Patients who attended Te Eye andEN Hospi-tal o Fudan University, Shanghai, China, between the periodo January and January , or reractive treatment o their myopia were recruited.

Inclusion criteria included patient aged over years,Spherical Equivalent (SE) reractive error ≥ −. D, a stablereractive error in the last years, no contraindications tolaser reractive surgery, and no previous history o dry eyedisease. Additionally, prior to surgery, patients completed adry eye questionnaire (Te Salisbury Eye Evaluation) andonly those who yielded a total score o were included.Patients were excluded i they had undergone any ocularsurgery in the past months or were using medication that

could interere with the ocular surace. A complete dilatedophthalmicexamination was perormed to assess the patient’ssuitability or either SMILE or FS-LASIK. Central cornealthickness (CC) was determined with a Pentacam system(yp; Oculus; Wetzlar, Germany). Afer the nature o the two procedures was explained, the patients chose the typeo surgery they wished to undergo.

In total, patients who completed months o ollow-up were included in this study. patients underwent SMILEprocedures (SMILE group) while patients underwentFS-LASIK procedures (FS-LASIK group). Te mean age o patients undergoing SMILE was 25.21±6.51 years old, whichwas not signicantly different to the mean age o patients

undergoing FS-LASIK, which was 24.72±6.53 years old ( =0.722). Te mean preoperative SE was −7.46 ± 1.11 D in theSMILE group and −7.44 ± 1.13 D in the FS-LASIK group,with no signicant difference between the two groups. Temean preoperative BU was 9.87 ± 1.57 seconds in theSMILE group and 9.56±1.35 seconds in the FS-LASIK group,

again with no signicant difference between the two groups( = 0.948). Written inormed consent was obtained romeach patient afer the details o the study were ully explained.

... ear-Film Breakup ime (BU). BU was assessedprior to surgery and was repeated at month, months, months, and months afer surgery. BU wasassessed withuorescein paper strips that were wetted with unpreservedsaline solution. One drop was instilled in each eye in thelower conjunctival sac, and the patient was instructed toblink several times. A cobalt lter was attached to a slit-lamp biomicroscope, and the time it took rom a completeblink until the rst signs o a break in the tear lm was

recorded. Te test was repeated times and averaged. Tesame observer perormed the test.

... Te Salisbury Eye Evaluation Questionnaire for Dry Eye Symptoms. Te Salisbury Eye Evaluation Questionnaire,translated into Chinese, was given to each subject or sel-evaluation o dry eye symptoms beore operation and at , ,, and months afer operation. Te questionnaire contains items pertaining to dry eye symptoms. Questions includethe ollowing: () Do your eyes ever eel dry? () Do you evereel a gritty or sandy sensation in your eye? () Are your eyesever red? () Do your eyes ever have a burning sensation? ()Do you notice much crusting on your lashes? () Do youreyes ever get stuck shut in the morning? Te subject answerseach question on the questionnaire based on how ofen they experience these symptoms as rarely, sometimes, ofen, or allthe time. Symptoms that were experienced ofen or all thetime were given a score o , and the other two responses weregiven a score o . Te scores were added up to give a totalscore or each subject.

.. Surgical echnique. All surgeries were perormed underlocal anesthesia by one surgeon (Hao Zhou) with patientsundergoing either SMILE or FS-LASIK.

SMILE was perormed using the VisuMax emtosecond

laser system (Carl Zeiss Meditec) with a repetition rate o kHz, pulse energy o – nJ, intended cap thicknesso – m, cap diameter o . mm, lenticule diameter o . to . mm (depending on the reractive error), and a ∘-angle side cut with a circumerential length o . mm at thesuperior position.

FS-LASIK was perormed with the VisuMax system orap creation ollowed by Mel excimer laser (Carl ZeissMeditec) or stromal ablation, with an intendedap thicknesso m and pulse energy o nJ. Te hinge was located atthe superior position.

A standard postoperative topical steroid (Fluorometho-lone .%) was tapered over days; topical antibiotic


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: Demographic data o the subjects included in this study.

Mean ± standard deviation value

SMILE ( = 47) FS-LASIK ( = 43)

Age (y) . ± . . ± . .

Gender (F/M) / / .

Preop SE (D) −

. ±

. −

. ±

. .

Preop CC (m) . ± . . ± . .

Preop BU (sec) . ± . . ± . .

: Lenticule thickness/ablation depth.

Mean ± standard deviation value

SMILE ( = 47) FS-LASIK ( = 43)

Lenticule thickness/Ablation depth(m)

. ± . . ± . .

(obramycin.%) QID or days, and unpreservedocularlubricant times a day was prescribed or a month.

.. Statistical Analysis. In all cases, only data rom the rsteye (right eye) on which the procedure was perormed wasused in the statistical analysis. Te sample size o this study was determined based on the standard deviation reportedrom a previous study [], with the signicance level set at = 0.05 (two tailed) and a power o %, and a sample sizeo at least was required in each group. Allowing or a %dropout rate, at least subjects were required. All statisticalanalyses were perormed with a statistics program (SPSS. IBM Corporation, Armonk, NY, USA). Independent-samples -test was used to compare the differences between

groups. One-way repeated measures ANOVA test was usedto compare BU change and SEEQ score change withingroups over time. ukey’s honestly signicant difference(HSD) post hoc test wasperormed to evaluate the differencesin parameters between groups. Spearman’s correlation testwas used to assess relationship between BU and SEEQscores. < 0.05 was considered signicant.

3. Results

In total, patients were recruited or the study, with atotal o eyes (the rst eye to have surgery perormed oreach patient) included in the analysis. Tere were a total o

eyes in the SMILE group and eyes in the FS-LASIKgroup. Tere were no signicant differences between the twogroups preoperatively in terms o age, SE reractive error,central corneal thickness (CC), or preoperative BU.Demographic data or all subjects included in this study isoutlined in able .

Objective surgical changes in corneal parameters weresimilar between the two groups, with no signicant differencein lenticule thickness/ablation depth between the two groups(able ).

.. ear-Film Breakup ime (BU). Preoperatively, therewas no signicant difference in BU between the SMILE

: BU between SMILE and FS-LASIK.

Postop BU (sec) Mean ± standard deviation

valueSMILE ( = 47) FS-LASIK ( = 43)

month . ± . . ± . .

months . ± . . ± .


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S E E Q s c o r e

SMILE

FS-LASIK

x

x

x

x

x

0.0

0.5

1.0

1.5

2.0

2.5

12 months6 months3 months1 monthPreop

Time

F : Salisbury Eye Evaluation Questionnaire results in SMILEand FS-LASIK groups at , , , and months afer operation. “”:statistically signicantly greater than preoperative values, < 0.05.

higher score indicating a greater degree o experienced dry eye symptoms. Preoperative scores were , per the inclusioncriteria. One-way ANOVA testing ound a statistically sig-nicant difference in SEEQ scores within groups over thetime period o review or both SMILE ((4, 230) = 23.127, < 0.001) and FS-LASIK ((4, 210) = 91.161, < 0.001).

Post hoc tests showed that, in the SMILE group, SEEQscores were statistically signicantly higher at month ( <0.001) and months ( = 0.003) afer operation thanpreoperative values. By and months, this difference wasno longer statistically signicant ( = 0.640 and =

0.991, resp.). For FS-LASIK, post hoc test evaluation oundthat SEEQ scores at month, months, and monthsafer operation were statistically signicantly higher thanpreoperative values ( < 0.001 or all ollow-up timeperiods). By months, this difference was no longer ound( = 0.636) (Figure ).

Postoperatively at the -, -, and -month ollow-upintervals, the SEEQ score was higher in the FS-LASIK groupthan the SMILE group ( < 0.001 or all ollow-up timeintervals). months afer operation, this difference was nolonger statistically signicant ( = 0.109) (able ).

Spearman’s correlation test revealed a moderate negativecorrelation between SEEQ scores and BU at month afer

operation or the SMILE group ( = −0.599, < 0.001) aswell as in the FS-LASIK group (

= −0.518, < 0.001).

4. Discussion

Dry eye disease continues to be a common complication o reractive surgery, affecting not only the ocular comort o patients, but also their visual quality [, ]. Tis can havea direct impact on their overall satisaction and quality o lie ollowing surgery. Although a requently noted condition,dry eye disease remains a complex syndrome with a wide-ranging spectrum o clinical signs and subjective symptomsthat do not always show a great degree o correlation [, ].

: SEEQ scores between SMILE and FS-LASIK.

Postop SEEQ Mean ± standard deviation

valueSMILE ( = 47) FS-LASIK ( = 43)

month . ± . . ± .


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Tese results suggest that SMILE may be superior to FS-LASIK, inducing a shorter duration o tear-lm disturbanceand leading to a quicker recovery o tear-lm unctionpostoperatively. Our results also indicate that this advantageo the SMILE procedure was noted subjectively with thepatient’s experience o dry eye symptoms, as demonstrated

by the results o the SEEQ. Patients in the SMILE groupreported lower SEEQ scores (ewer dry eye symptoms)compared to patients in the FS-LASIK group at , , and months postoperatively, beore equalizing at monthspostoperatively. Tereore, patients who underwent SMILEwere less prone to dry eye symptoms, as assessed with bothclinical and subjective measures, than those who underwentFS-LASIK in the rst months ollowing surgery, but they demonstrated similar degrees o dry eye disease afer months o ollow-up.

Several hypotheses have been proposed to explain thepathophysiology underlying the development o dry eyedisease ollowing reractive surgery. Changes in cornealinnervation and sensitivity induced by reractive surgery arekey in understanding the pathogenesis o dry eye disease andrevolve around the idea that corneal sensitivity is reduceddue to transection o the corneal nerves, thus resulting indysunction o the cornea-lacrimal gland unctional unit [,]. ransection o the sensory nerves o the cornea, as itoccurs during FS-LASIK, is thought to lead to a decreasein the innervation to the autonomic nerve bres supplyingthe lacrimal gland that would otherwise stimulate tear pro-duction via the neural reex arc [, ]. Tis change may result in tear-lm dysunction via a number o mechanisms,including changes in the composition o the tears, ocularsurace changes, and decreased blink requency [, ].

Tere hasbeen increasing evidence supporting the theory that damage to the corneal nerve density occurs ollowingreractive surgery, particularly affecting the subbasal nerveplexus [, , , , –]. Te main consequence o thischange in nerve density is a reduction in corneal sensitivity.Tis results in a hypoesthetic cornea and is likely the key actor in the development o postreractive dry eye disease[, , , , , , ]. With the aid o in vivo conocalmicroscopy, Denoyer et al. demonstrated that SMILE pre-served the corneal subbasal nerve plexus better than LASIK[]. Tey ound a greater nerve density, number o long nervebres and nerve bre branchings in patients that underwentSMILE compared to those that underwent LASIK. Tey alsoound that corneal sensitivity was greater in the SMILE group

in the short-term but ound no signicant difference betweenSMILE and LASIK afer months afer surgery []. Tisloss in nerve bre density does start to regenerate monthsafer surgery, with almost complete recovery by to yearspostoperatively [, –].

Te degree o injury to corneal nerves is understandably expected to be different between the two surgical procedures,owing to the differing nature o each procedure. Te twoprocedures differ in the method o ablation and the layers o the cornea affected, with FS-LASIK affecting the epitheliumand anterior stroma, with the creation o a ap, while SMILEmainly affects the posterior stromal bed, only requiring asmall tunnel incision []. Our results demonstrated a clear

difference in the degree o injury and in the time to recovery o tear unction between SMILE and FS-LASIK, as assessedby the BU. SMILE not only showed a more rapid recovery o tear unction, with a return in BU to preoperativelevels at months compared to months or FS-LASIK,but also showed a signicantly lower degree o loss in BU

compared to FS-LASIK at , , and months postoperatively.Recent studies have demonstrated that SMILE preservescorneal sensitivity better than LASIK but demonstrated thatboth procedures eventually result in the recovery o cornealsensitivity to levels seen in healthy controls [, , , , ].Tis may help to explain the transient nature and the long-term return o BU and SEEQ scores to preoperative levelsin both groups afer months.

Li et al., who examined corneal sensitivity and dry eyeollowing SMILE and FS-LASIK surgery, ound that cornealsensitivity was less reduced and thus better in patientsthat underwent SMILE at all postoperative time intervalscompared to those patients that underwent FS-LASIK [].Te present study ound that patients who underwent SMILEnot only recovered tear-lm unction quicker than thosewho underwent FS-LASIK, but also were less symptomaticin the rst months. We also ound a moderate correlationbetween the BU and SEEQ scores at month postoper-atively in both the SMILE and FS-LASIK groups; however,this correlation did not persist, suggesting that the clinicalsigns do not always correlate with reported symptoms. Tisdiscrepancy between clinical signs and patient symptoms hasbeen previously noted, as Demirok et al. demonstrated thatalthough both SMILE and FS-LASIK resulted in a decrease incorneal sensation up to months postoperatively, there wasno change in dry eye symptoms at any point in their patients[].

Ocular surace changes, including those to the con- junctiva, induced by the two procedures would also differ.Coupled with the effects o hypoesthesia o the cornea,these changes may help to urther explain the differencein the development o dry eye disease between SMILEand FS-LASIK patients. Contour changes may impact thedistribution o tears over the corneal surace and are likely to pose a greater problem ollowing FS-LASIK than SMILEdue to disruption o the epithelium during the ormationo the epithelial ap [, ]. Damage to and loss o mucin-producing conjunctival goblet cells have been shown to occurollowing LASIK, resulting in tear-lm instability through areduction o the mucin layer o the tear lm [, , ]. Tis

change may, however, return to baseline afer months andmay contribute to the transient nature o the postreractivedry eye disease. An increase in the osmolarity o tears ollow-ing reractive surgery has also been demonstrated to occurafer LASIK [, , ]. Hyperosmolarity o the tears occursdue to decreased blinking and increased evaporative loss o tears, reduced secretion o tears rom the lacrimal gland,and the loss o goblet cells producing the mucin layer o thetear lm []. Tis hyperosmolar environment results in thetriggering o an inammatory cascade with an upregulationo inammatory cytokines, leading to continuing ocularsurace irritation, a reduction in BU, and the developmento dry eye symptoms [].


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FS-LASIK has been proven to be a sae and successulprocedure or the surgical correction o reractive error overa number o years [, ]. SMILE, although in its clinicalinancy, is now proving to also be a sae and successulalternative or the correction o reractive error and may provide a more superior and saer reractive outcome than

FS-LASIK []. Extensive literature exists demonstrating thesaety, efficacy, and complications o FS-LASIK, including asubstantial amount o literature investigating the develop-ment o ocular surace and dry eye disease ollowing FS-LASIK [, , , , , , , ]. Recently, there havebeen limited studies investigating the development o dry eye ollowing SMILE, as well as studies comparing the twoprocedures [, , , ]. Te majority o the literature,however, has ocused on the short-term dry eye outcomesollowing SMILE and FS-LASIK, looking at the developmento dry eye disease up to to months postoperatively.Te present study advances on the current literature by investigating and comparing the clinical and subjective dry eye outcomes o patients undergoing SMILE and FS-LASIKover a longer period o ollow-up, with measures up to months postoperatively. One other advantage o the presentstudy is that all patients investigated had a moderate tohigh degree o myopia prior to surgery. Tis is signicant asthe large majority o patients undergoing reractive surgery each year are myopic, and the greater the degree o myopia,the greater the amount o stromal ablation or lenticularextraction required [, , ]. Tis is a potential area o utureresearch, investigating the development o dry eye disease inrelation to the degree o reractive error.

Future advancements canbe made on this studyto urtherinvestigate both the clinical and subjective dry eye outcomesollowing SMILE and FS-LASIK. Te present study was lim-ited in the scope o assessments it conducted, looking at only clinical indicators o dry eye: one objective measure usingthe BU and one subjective evaluation o patient symptomsusing the SEEQ. A more comprehensive combination o assessments, as suggested by the Dry Eye Workshop andother studies, would provide a more accurate diagnosis o dry eye disease [, , –]. Tis would include a measureo tear osmolarity, corneal sensitivity, BU, a measure o tear unction such as the Schirmer’s test, and with advancesin technology even the use o conocal microscopy. Also, amore rigorous questionnaire should be utilised, such as the-item Ocular Surace Disease Index (OSDI) or the -itemImpact o Dry Eye on Everyday Lie (IDEEL) questionnaires,

which have been shown to be more accurate indicators o dry eye disease [, , ]. Te SEEQ had the advantage o beingquick and easy to administer, with only items, but has beenshown to be outdated and having a low correlation with dry eye signs [].

Te present study demonstrated that SMILE resulted in alesser degree o dry eye disease and a aster recovery o tearunction compared to FS-LASIK in the short-term ollowingsurgery in those patients with no preexisting dry eye disease.Tis was ound using both clinical and subjective measures o dry eye and also demonstrated that the long-term outcomewas not signicantly different between the two proceduresafer months o ollow-up postoperatively. Tis short-term

change, however, can have a great impact on a patients’overall satisaction with their surgical and visual outcomeand may inuence their quality o lie. Further studies may aim to determine preventative measures that may be taken tohelp prevent or reduce the development o dry eye diseasein patients undergoing reractive surgery and help better

monitor and manage those that do.

Conflict of Interests

Te authors declare that there is no conict o interestsregarding the publication o this paper.

Acknowledgment

Tis study was supported by the Science and echnol-ogy Commission o Shanghai Municipality, Grant no.a.

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