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In-the-Bag Versus Ciliary Sulcus Secondary Intraocular Lens Implantation for Pediatric Aphakia: A Prospective Comparative Study

  • Zhenzhen Liu
    Affiliations
    Zhongshan Ophthalmic Center (Z.L., H.L., G J., X.T., B.Q., L.J., X.C., W.W., X. H., J.X., M.H., N.C., W.C., L.L., Y.L.) State Key Laboratory of Ophthalmology, Sun Yat-sen University, Guangzhou, Guangdong, China
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  • Haotian Lin
    Affiliations
    Zhongshan Ophthalmic Center (Z.L., H.L., G J., X.T., B.Q., L.J., X.C., W.W., X. H., J.X., M.H., N.C., W.C., L.L., Y.L.) State Key Laboratory of Ophthalmology, Sun Yat-sen University, Guangzhou, Guangdong, China
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  • Guangming Jin
    Affiliations
    Zhongshan Ophthalmic Center (Z.L., H.L., G J., X.T., B.Q., L.J., X.C., W.W., X. H., J.X., M.H., N.C., W.C., L.L., Y.L.) State Key Laboratory of Ophthalmology, Sun Yat-sen University, Guangzhou, Guangdong, China
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  • Xuhua Tan
    Affiliations
    Zhongshan Ophthalmic Center (Z.L., H.L., G J., X.T., B.Q., L.J., X.C., W.W., X. H., J.X., M.H., N.C., W.C., L.L., Y.L.) State Key Laboratory of Ophthalmology, Sun Yat-sen University, Guangzhou, Guangdong, China
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  • Bo Qu
    Affiliations
    Zhongshan Ophthalmic Center (Z.L., H.L., G J., X.T., B.Q., L.J., X.C., W.W., X. H., J.X., M.H., N.C., W.C., L.L., Y.L.) State Key Laboratory of Ophthalmology, Sun Yat-sen University, Guangzhou, Guangdong, China
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  • Ling Jin
    Affiliations
    Zhongshan Ophthalmic Center (Z.L., H.L., G J., X.T., B.Q., L.J., X.C., W.W., X. H., J.X., M.H., N.C., W.C., L.L., Y.L.) State Key Laboratory of Ophthalmology, Sun Yat-sen University, Guangzhou, Guangdong, China
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  • Xiaoyun Chen
    Affiliations
    Zhongshan Ophthalmic Center (Z.L., H.L., G J., X.T., B.Q., L.J., X.C., W.W., X. H., J.X., M.H., N.C., W.C., L.L., Y.L.) State Key Laboratory of Ophthalmology, Sun Yat-sen University, Guangzhou, Guangdong, China
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  • Wei Wang
    Affiliations
    Zhongshan Ophthalmic Center (Z.L., H.L., G J., X.T., B.Q., L.J., X.C., W.W., X. H., J.X., M.H., N.C., W.C., L.L., Y.L.) State Key Laboratory of Ophthalmology, Sun Yat-sen University, Guangzhou, Guangdong, China
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  • Xiaotong Han
    Affiliations
    Zhongshan Ophthalmic Center (Z.L., H.L., G J., X.T., B.Q., L.J., X.C., W.W., X. H., J.X., M.H., N.C., W.C., L.L., Y.L.) State Key Laboratory of Ophthalmology, Sun Yat-sen University, Guangzhou, Guangdong, China
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  • Jingmin Xu
    Affiliations
    Zhongshan Ophthalmic Center (Z.L., H.L., G J., X.T., B.Q., L.J., X.C., W.W., X. H., J.X., M.H., N.C., W.C., L.L., Y.L.) State Key Laboratory of Ophthalmology, Sun Yat-sen University, Guangzhou, Guangdong, China
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  • Guishuang Ying
    Affiliations
    Department of Ophthalmology (G.Y.), Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania, USA
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  • Ying Han
    Affiliations
    Department of Ophthalmology (Y.H.), University of California, San Francisco, San Francisco, California, USA
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  • Mingguang He
    Affiliations
    Zhongshan Ophthalmic Center (Z.L., H.L., G J., X.T., B.Q., L.J., X.C., W.W., X. H., J.X., M.H., N.C., W.C., L.L., Y.L.) State Key Laboratory of Ophthalmology, Sun Yat-sen University, Guangzhou, Guangdong, China
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  • Nathan Congdon
    Affiliations
    Zhongshan Ophthalmic Center (Z.L., H.L., G J., X.T., B.Q., L.J., X.C., W.W., X. H., J.X., M.H., N.C., W.C., L.L., Y.L.) State Key Laboratory of Ophthalmology, Sun Yat-sen University, Guangzhou, Guangdong, China

    Center for Public Health (N.C.), Queen's University Belfast, Belfast, United Kingdom

    Orbis International (N.C.), New York, New York, USA
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  • Weirong Chen
    Affiliations
    Zhongshan Ophthalmic Center (Z.L., H.L., G J., X.T., B.Q., L.J., X.C., W.W., X. H., J.X., M.H., N.C., W.C., L.L., Y.L.) State Key Laboratory of Ophthalmology, Sun Yat-sen University, Guangzhou, Guangdong, China
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  • Author Footnotes
    ⁎ Correspondence: Dr Z. Liu and Dr H. Lin served jointly as first authors. Dr W. Chen and Dr Y. Liu served jointly as senior authors
    Lixia Luo
    Footnotes
    ⁎ Correspondence: Dr Z. Liu and Dr H. Lin served jointly as first authors. Dr W. Chen and Dr Y. Liu served jointly as senior authors
    Affiliations
    Zhongshan Ophthalmic Center (Z.L., H.L., G J., X.T., B.Q., L.J., X.C., W.W., X. H., J.X., M.H., N.C., W.C., L.L., Y.L.) State Key Laboratory of Ophthalmology, Sun Yat-sen University, Guangzhou, Guangdong, China
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  • Author Footnotes
    ⁎⁎ Inquiries to Yizhi Liu or Lixia Luo, Zhongshan Ophthalmic Center, Sun Yat-sen University, No. 7 Jinsui Rd, Guangzhou, 510000, China
    Yizhi Liu
    Footnotes
    ⁎⁎ Inquiries to Yizhi Liu or Lixia Luo, Zhongshan Ophthalmic Center, Sun Yat-sen University, No. 7 Jinsui Rd, Guangzhou, 510000, China
    Affiliations
    Zhongshan Ophthalmic Center (Z.L., H.L., G J., X.T., B.Q., L.J., X.C., W.W., X. H., J.X., M.H., N.C., W.C., L.L., Y.L.) State Key Laboratory of Ophthalmology, Sun Yat-sen University, Guangzhou, Guangdong, China
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  • Author Footnotes
    ⁎ Correspondence: Dr Z. Liu and Dr H. Lin served jointly as first authors. Dr W. Chen and Dr Y. Liu served jointly as senior authors
    ⁎⁎ Inquiries to Yizhi Liu or Lixia Luo, Zhongshan Ophthalmic Center, Sun Yat-sen University, No. 7 Jinsui Rd, Guangzhou, 510000, China
Open AccessPublished:October 12, 2021DOI:https://doi.org/10.1016/j.ajo.2021.10.006

      HIGHLIGHTS

      • In secondary intraocular lens implantation for pediatric aphakia, in-the-bag implantation greatly reduces the risk of postoperative adverse events, particularly glaucoma-related adverse events, and achieves better intraocular lens centration and visual acuity compared to ciliary sulcus implantation.

      PURPOSE

      To compare outcomes of in-the-bag vs ciliary sulcus secondary intraocular lens (IOL) implantation for pediatric aphakia.

      DESIGN

      Prospective interventional case series.

      METHODS

      This institutional study was conducted in 202 children (355 aphakic eyes) diagnosed as having congenital cataracts and who underwent cataract extraction before age 24 months. Pediatric aphakic eyes underwent in-the-bag or ciliary sulcus secondary IOL implantation according to the amount of residual lens capsule and were monitored for 3 years postoperatively. The main outcome measures were adverse events (AEs), IOL tilt and decentration, and best corrected visual acuity (BCVA) in the operative eye.

      RESULTS

      A total of 144 eyes (40.6%, 89 children) received in-the-bag IOL implantation (capsular group), and 211 eyes (59.4%, 132 children) underwent ciliary sulcus IOL implantation (sulcus group). Kaplan-Meier curves showed that the time-dependent incidence of glaucoma-related AEs (GRAEs) (P = .005) and any AEs (P = .002) were higher in the sulcus group. In-the-bag IOL implantation was a strong protective factor against GRAE (hazard ratio, 0.08; 95% CI, 0.01-0.53; P = .009) and any AEs (hazard ratio, 0.21; 95% CI, 0.08-0.57; P = .002). Clinically significant IOL decentration (>0.4 mm) was more common in the sulcus group compared with the capsular group (vertical decentration: 29.8% vs 15.7%, P = .005; horizontal decentration: 30.3% vs 9.35%, P < .001). BCVA in the capsular group was better than that in the sulcus group (logMAR, 0.56 vs 0.67, P = .014).

      CONCLUSIONS

      Compared with ciliary sulcus secondary IOL implantation, in-the-bag IOL implantation reduced AEs and yielded better IOL centration and BCVA for pediatric aphakia.
      Secondary intraocular lens (IOL) implantation is a common treatment for pediatric aphakia.
      • Solebo AL
      • Cumberland P
      • Rahi JS
      British isles congenital cataract interest group. 5-year outcomes after primary intraocular lens implantation in children aged 2 years or younger with congenital or infantile cataract: findings from the iolunder2 prospective inception cohort study.
      • Lambert SR
      • Cotsonis G
      • DuBois L
      • et al.
      Long-term effect of intraocular lens vs contact lens correction on visual acuity after cataract surgery during infancy: a randomized clinical trial.
      • Bothun ED
      • Wilson ME
      • Vanderveen DK
      • et al.
      Outcomes of bilateral cataracts removed in infants 1 to 7 months of age using the toddler aphakia and pseudophakia treatment study registry.
      In short- to midterm follow-up of 12 to 60 months, the incidence of adverse events (AEs) after IOL implantation in pediatric aphakia has been reported to be as high as 19.5% to 28.5%, affecting the prognosis and visual function in these patients.
      • Wood KS
      • Tadros D
      • Trivedi RH
      • Wilson ME.
      Secondary intraocular lens implantation following infantile cataract surgery: intraoperative indications, postoperative outcomes.
      • Wilson Jr, ME
      • Hafez GA
      • Trivedi RH.
      Secondary in-the-bag intraocular lens implantation in children who have been aphakic since early infancy.
      • Nihalani BR
      • Vanderveen DK.
      Secondary intraocular lens implantation after pediatric aphakia.
      • Trivedi RH
      • Wilson Jr, ME
      • Facciani J.
      Secondary intraocular lens implantation for pediatric aphakia.
      • Crnic T
      • Weakley Jr, DR
      • Stager Jr, D
      • Felius J.
      Use of acrysof acrylic foldable intraocular lens for secondary implantation in children.
      In most pediatric aphakic eyes the amount of residual lens capsule after cataract extraction is insufficient or the anterior and posterior capsules of the lens are adherent and scarred, so an IOL can only be implanted in the ciliary sulcus.
      • Koch CR
      • Kara-Junior N
      • Serra A
      • Morales M.
      Long-term results of secondary intraocular lens implantation in children under 30 months of age.
      ,
      • Shenoy BH
      • Mittal V
      • Gupta A
      • et al.
      Complications and visual outcomes after secondary intraocular lens implantation in children.
      Studies of adult IOL implantation have reported that the contact between ciliary sulcus–implanted IOLs and the iris leads to complications such as inflammation, secondary glaucoma, and unstable IOL position.
      • Kristianslund O
      • Raen M
      • Ostern AE
      • Drolsum L.
      Glaucoma and intraocular pressure in patients operated for late in-the-bag intraocular lens dislocation: a randomized clinical trial.
      • Ollerton A
      • Werner L
      • Strenk S
      • et al.
      Pathologic comparison of asymmetric or sulcus fixation of 3-piece intraocular lenses with square versus round anterior optic edges.
      • Uy HS
      • Chan PS.
      Pigment release and secondary glaucoma after implantation of single-piece acrylic intraocular lenses in the ciliary sulcus.
      Because the blood-aqueous barrier is immature in children, some researchers have expressed concern that the high incidence of AEs after secondary IOL implantation in pediatric aphakia may be related to the use of ciliary sulcus–implanted IOLs.
      • Mehta R
      • Aref AA.
      Intraocular lens implantation in the ciliary sulcus: challenges and risks.
      ,
      • Zhao YE
      • Gong XH
      • Zhu XN
      • et al.
      Long-term outcomes of ciliary sulcus versus capsular bag fixation of intraocular lenses in children: an ultrasound biomicroscopy study.
      To reduce AEs, we and other researchers have modified the technique of cataract extraction and secondary IOL implantation in pediatric aphakic eyes to achieve secondary in-the-bag IOL implantation.
      • Nihalani BR
      • Vanderveen DK.
      Secondary intraocular lens implantation after pediatric aphakia.
      ,
      • Lin H
      • Tan X
      • Lin Z
      • et al.
      Capsular outcomes differ with capsulorhexis sizes after pediatric cataract surgery: a randomized controlled trial.
      • Luo L
      • Lin H
      • Chen W
      • et al.
      In-the-bag intraocular lens placement via secondary capsulorhexis with radiofrequency diathermy in pediatric aphakic eyes.
      • Wilson Jr, ME
      • Englert JA
      • Greenwald MJ.
      In-the-bag secondary intraocular lens implantation in children.
      • Grewal DS
      • Basti S.
      Modified technique for removal of soemmerring ring and in-the-bag secondary intraocular lens placement in aphakic eyes.
      However, there are currently no large, prospective studies comparing complication rates and visual prognosis of in-the-bag vs. ciliary-sulcus secondary IOL implantation in pediatric patients.
      This prospective study compared the outcomes of these two methods to identify the one providing better clinical outcomes for children with congenital cataract. In conjunction with the Childhood Cataract Program of the Chinese Ministry of Health (CCPMOH), we consecutively enrolled 226 patients (395 aphakic eyes) diagnosed with congenital cataract and undergoing secondary in-the-bag or ciliary sulcus IOL implantation. Patients were monitored in a standardized manner for 3 years. The main outcomes were best-corrected visual acuity (BCVA) in the operated-on eye and the incidence of postoperative AEs, including glaucoma-related adverse events (GRAEs), visual axis opacification (VAO), iris-related AEs, and IOL tilt and decentration.

      METHODS

      This study was approved by the Zhongshan Ophthalmic Center (Guangzhou, China) Institutional Review Board (2013PRLL001). Written informed consent was obtained from the guardians of all pediatric patients. The study adhered to the tenets of the Declaration of Helsinki.

       Eligibility Criteria

      Children were eligible for inclusion in this study if they (1) underwent unilateral or bilateral extraction of a congenital cataract before age 24 months and (2) received secondary IOL implantation.
      Exclusion criteria were (1) preexisting ocular disease that might affect the selection of method and outcome of secondary IOL implantation, including and not restricted to microphthalmia (axial length <17.5 mm for children aged between 1 and 4 months at surgery and <18.5 mm for those aged 4-7 months), microcornea (corneal diameter <9.5 mm), megalocornea (corneal diameter >12.5 mm), corneal opacity, iris anomaly, uveitis, or persistent fetal vasculature or trauma; and (2) suture fixation or other methods of secondary IOL implantation were used.

       Study Design

      Participants were enrolled at Zhongshan Ophthalmic Center (ZOC), and followed the standardized protocol of the CCPMOH for evaluation and follow-up.
      • Lin H
      • Chen W
      • Luo L
      • et al.
      Effectiveness of a short message reminder in increasing compliance with pediatric cataract treatment: a randomized trial.
      Briefly, a profile for every eligible participant was recorded in detail by 3 ophthalmologists (H.T.L., Z.Z.L., and B.Q.) at enrollment. Documentation included sex, ocular and systemic comorbidities, age at cataract surgery, age at IOL implantation, and surgical details, including IOL type, power, and intraoperative complications.
      All operations, including initial cataract extraction and secondary IOL implantation, were performed by 2 experienced surgeons (Y.Z.L. and W.R.C.). Both doctors were experienced senior cataract surgeons who had completed more than 100,000 cataract operations before the initiation of this study. As described in our previous publications,
      • Lin H
      • Tan X
      • Lin Z
      • et al.
      Capsular outcomes differ with capsulorhexis sizes after pediatric cataract surgery: a randomized controlled trial.
      use of a 4- to 5-mm anterior and 3.5- to 4-mm posterior capsulectomy in all children allowed the preservation of sufficient lens capsule during cataract extraction to promote the formation of a volumized Soemmering ring and facilitate secondary in-the-bag IOL implantation.
      The choice of in-the-bag or ciliary sulcus implantation was made at the time of surgery as follows. Before IOL insertion, the surgeon used viscoelastic to further dilate the pupil to determine whether there was a volumized Soemmering ring sufficient for in-the-bag IOL implantation or the adhesion of the capsular leaflets was present. If the amount of anterior and posterior lens capsule was sufficient and there was no adhesion between the anterior and posterior leaflets, a cystotome or electric capsulorhexis was used to reopen the Soemmering ring, and an IOL was implanted in the capsular bag. In case the amount of anterior and posterior lens capsule was insufficient or adhesions between anterior and posterior leaflets could not be separated, an IOL was placed in the ciliary sulcus (Supplemental Figure 1).
      The general approach adopted regarding age at IOL placement was as follows:
      • 1.
        Generally, primary IOL implantation was performed for patients aged >24 months.
      • 2.
        For unilateral cataract, the age for primary/secondary IOL placement could be aged <24 months to prevent amblyopia, mainly, depending on the axial length of the operated-on eye.
      • 3.
        For bilateral cataract, secondary IOL implantation was performed before reaching school age, to prevent large myopic shifts after IOL implantation.
      All follow-up visits and regular ocular examinations were provided free of charge with funding support from the CCPMOH. Regular follow-up appointments for each participant were scheduled according to the CCPMOH study protocol at 1 week, 1, 3, and 6 months, and then every 6 months after surgery. Spectacles or contact lenses (only for children with unilateral aphakia and whose guardians were able to afford and willing to use them) were prescribed (H.T.L., Z.Z.L., or B.Q.) to correct residual refractive error after IOL implantation.
      Postoperative AEs, BCVA, refractive status, and ocular biometry were recorded at each follow-up visit. Definitions for GRAEs were as reported in the Infant Aphakia Treatment Study (IATS).
      • Grewal DS
      • Basti S.
      Modified technique for removal of soemmerring ring and in-the-bag secondary intraocular lens placement in aphakic eyes.
      BCVA was evaluated with Teller acuity cards for patients aged <3 years, with Lea Symbol charts for patients aged 3 to 6 years, and with Early Treatment Diabetic Retinopathy Study charts for patients aged >6 years. Intraoperative complications and other postoperative AEs, including VAO, iris synechiae, corectopia and discoria, were recorded separately according to criteria reported in prior CCPMOH studies.
      • Lin H
      • Chen W
      • Luo L
      • et al.
      Effectiveness of a short message reminder in increasing compliance with pediatric cataract treatment: a randomized trial.
      ,
      • Wang J
      • Chen J
      • Chen W
      • et al.
      Incidence of and risk factors for suspected glaucoma and glaucoma after congenital and infantile cataract surgery: a longitudinal study in china.
      IOL position (tilt and decentration) was measured using Scheimpflug images, as previously described,
      • Baumeister M
      • Neidhardt B
      • Strobel J
      • Kohnen T.
      Tilt and decentration of three-piece foldable high-refractive silicone and hydrophobic acrylic intraocular lenses with 6-mm optics in an intraindividual comparison.
      using a digital Scheimpflug camera (Pentacam, Oculus) connected to a computer. After pupil dilation with a drop each of tropicamide 0.5% and phenylephrine 0.5%, administered 3 times at 5-minute intervals, 2 Scheimpflug slitlamp images were taken at slit angles of 90° and 180°. The anterior and posterior surfaces of the cornea and IOL were marked in the digital image to determine the visual axis of the eye and the optical center of the IOL. The tilt of the optical axis of the IOL relative to the visual axis and the distance between the IOL optical center and the visual axis were calculated using Image-Pro Plus 6.0 (Media Cybernetics).

       Statistical Analysis

      Data are described as mean (SD) for continuous variables and frequency (%) for categorical variables. Baseline characteristics of the capsular and sulcus groups were compared using the χ2 test or Fisher exact test for demographic data, and linear mixed modeling for ocular characteristics, adjusting for correlations between the 2 eyes of a participant.
      The cumulative incidence rates of AEs over the 3-year follow-up after secondary IOL implantation were compared between the 2 groups using generalized estimated equations, accounting for the correlation between 2 eyes of a participant, or the Fisher exact test for AEs with low incidence. Kaplan-Meier curves were drawn to show the incidence of AEs over time after secondary IOL implantation, and intergroup differences were assessed using Cox proportional hazard models controlling for the correlation between 2 eyes of a single participant. For AEs with incidence differing significantly between groups, univariable and multivariable regression analyses were performed to estimate adjusted hazard ratios (HR) and 95% CIs. All variables with P < .05 in the univariable analysis were included in the multivariable regression model.
      The differences of IOL tilt and decentration between groups were compared using linear mixed models for continuous data or generalized estimated equation models for binary data, with adjustment for the correlation between eyes. The within-group changes in BCVA, ocular refractive power, and ocular biometry were assessed using linear mixed models, taking into account the clustering of eyes within a single participant. A linear plot was drawn to illustrate between-group differences in logMAR visual acuity at each year of follow-up after baseline. All statistical analyses were performed using Stata 16 software (StataCorp).

      RESULTS

      From January 2013 to December 2017, 226 consecutive participants (395 aphakic eyes) undergoing unilateral or bilateral cataract extraction for congenital cataract before age 24 months and who were expected to receive secondary IOL implantation, were enrolled and evaluated. We excluded 11 participants (18 eyes) for comorbidities potentially affecting secondary IOL implantation, including microcornea (6 participants, 11 eyes), megalocornea (3 participants, 5 eyes), and persistent fetal vasculature (2 participants, 2 eyes). One participant (2 eyes) was excluded due to the requirement for suture fixation during secondary IOL implantation. Twelve participants (21 eyes) failed to return for follow-up. In total, 355 eyes from 202 participants were eligible for inclusion and underwent data analysis (Figure 1).
      FIGURE 1
      FIGURE 1Flowchart of patient enrollment and data analysis for the secondary intraocular lens (IOL) implantation cohort.
      Among 161 participants (79.7%) diagnosed with bilateral congenital cataract, both eyes were included in 153 participants. Among the remaining 8 patients (4.97%), the second eye was excluded due to mild lens opacity (3 eyes), remaining aphakia (1 eye), requirement for suture fixation during secondary IOL implantation (1 eye), and having received primary IOL implantation (3 eyes). Included in the study were 41 participants (20.3%) diagnosed with unilateral congenital cataract.
      The capsular group included 144 eyes (40.6%) from 89 participants (mean follow-up, 34.1 [SD, 6.19] months), and the sulcus group comprised 211 eyes (59.4%) from 132 participants (mean follow-up, 32.4 [SD, 6.26] months). The capsular group had a higher percentage of boys compared with the sulcus group (72.9% vs 57.5%, P = .036) (Table 1). Neurodevelopmental anomaly was identified in 14 eyes (3.96%, 8 participants). Mean ages at cataract surgery and IOL implantation were 7.20 (SD, 4.49) months and 48.3 (SD, 18.5) months respectively, with an interval of 41.1 (SD, 18.3) months for the whole cohort and no difference in surgical age or interval between the 2 groups (Table 1). The preoperative axial length (AL; P = .663), intraocular pressure (IOP; P = .439), and BCVA (P = .301) did not differ between groups (Table 1). The distribution of surgery types was similar between surgeons. W.R.C. completed 99 eyes (68.7%) in the capsular group and 152 eyes (72.0%) in the sulcus group, and Y.Z.L. completed 45 eyes (31.3%) in the capsular group and 59 eyes (28.0%) in the sulcus group.
      TABLE 1The Baseline Characteristics of the Participants (202 Children, 355 Eyes)
       VariablesTotalCapsular BagSulcusP
      Patients, n (eyes)202 (355)89 (144)132 (211)
       Bilateral included, same location134 (272)55 (110)79 (158)
       Bilateral included, different location19 (38)19 (19)19 (19)
       Unilateral included49 (49)15 (15)34 (34)
      Characteristics based on patient, n (%)202 (100)70 (38.3)
      Excluding subjects with two eyes in different group.
      113 (61.7)
      Excluding subjects with two eyes in different group.
       Male sex128 (63.4)51 (72.9)
      Excluding subjects with two eyes in different group.
      65 (57.5)
      Excluding subjects with two eyes in different group.
      .036
      Bold P value is statistically significant (P < .05) by χ2 test.
       Neurodevelopmental impairment8 (3.96)3 (4.29)
      Excluding subjects with two eyes in different group.
      5 (4.42)
      Excluding subjects with two eyes in different group.
      1.000
      Fisher exact test.
      Characteristics based on eyes (n = 355)
       Age at cataract surgery, mo7.20 (4.49)6.85 (4.44)7.43 (4.52).989
      Linear mixed model with adjustment of correlation between 2 eyes within same person. BCVA = best corrected visual acuity; IOL = intraocular lens. Note: Data are presented as mean (SD) unless noted otherwise.
        Range1.90-23.31.90-22.12.10-23.3
       Age at IOL surgery, mo48.3 (18.5)41.7 (16.0)52.8 (18.8).826
      Linear mixed model with adjustment of correlation between 2 eyes within same person. BCVA = best corrected visual acuity; IOL = intraocular lens. Note: Data are presented as mean (SD) unless noted otherwise.
        Range16.3-10816.3-82.720.3-108
       Operation interval, mo41.1 (18.3)34.8 (14.8)45.4 (19.2).830
      Linear mixed model with adjustment of correlation between 2 eyes within same person. BCVA = best corrected visual acuity; IOL = intraocular lens. Note: Data are presented as mean (SD) unless noted otherwise.
        Range6.10-1048.17-78.16.10-104
       AL before IOL implantation, mm22.2 (1.93)21.9 (1.79)22.4 (2.00).663
      Linear mixed model with adjustment of correlation between 2 eyes within same person. BCVA = best corrected visual acuity; IOL = intraocular lens. Note: Data are presented as mean (SD) unless noted otherwise.
       Intraocular pressure, mm Hg14.7 (3.66)14.3 (3.68)15.0 (3.63).439
      Linear mixed model with adjustment of correlation between 2 eyes within same person. BCVA = best corrected visual acuity; IOL = intraocular lens. Note: Data are presented as mean (SD) unless noted otherwise.
      Characteristics based on eyes (n = 190)
       BCVA before IOL implantation (logMAR)1.26 (0.49)1.29 (0.50)1.23 (0.49).301
      Linear mixed model with adjustment of correlation between 2 eyes within same person. BCVA = best corrected visual acuity; IOL = intraocular lens. Note: Data are presented as mean (SD) unless noted otherwise.
      a Excluding subjects with two eyes in different group.
      b Bold P value is statistically significant (P < .05) by χ2 test.
      c Fisher exact test.
      d Linear mixed model with adjustment of correlation between 2 eyes within same person.BCVA = best corrected visual acuity; IOL = intraocular lens.Note: Data are presented as mean (SD) unless noted otherwise.
      The most common AEs were GRAEs (23/253 eyes [9.09%]), identified in 1.02% of eyes (1/98) in the capsular group and 14.2% in the sulcus group (22/155 eyes, P = .017). The incidence of other AEs stratified by group is described in Table 2. The overall rate of AEs was 17.5% (44/251 eyes): 6.12% (6/98 eyes) in the capsular group and 24.8% (38/153 eyes, P = .003) in the sulcus group.
      TABLE 2Cumulative Adverse Events at 3 Years After Secondary Intraocular Lens Implantation
      Adverse eventTotalCapsular BagCiliary SulcusP
      Events/n (%)Events/n (%)Events/n (%)
      Glaucoma related adverse event23/253 (9.09)1/98 (1.02)22/155 (14.2).017
      Generalized estimated equation model was used adjusting for correlation between eyes.
      Iris synechia13/244 (5.33)2/96 (2.08)11/148 (7.43).104
      Generalized estimated equation model was used adjusting for correlation between eyes.
      Corectopia and/or Discoria8/243 (3.29)1/96 (1.04)7/147 (4.76).148
      Generalized estimated equation model was used adjusting for correlation between eyes.
      Intraocular lens dislocation3/241 (1.24)0/96 (0.00)3/145 (2.07).278
      Fisher exact test was used without adjusting for correlation between eyes due to rare events in both groups. Note: Censored patients were not included in the denominator.
      Visual axis opacification9/243 (3.70)4/98 (4.08)5/145 (3.45).771
      Generalized estimated equation model was used adjusting for correlation between eyes.
      Retina detachment0/240 (0.00)0/96 (0.00)0/144 (0.00)
      Corneal endothelium decompensation0/240 (0.00)0/96 (0.00)0/144 (0.00)
      Uveitis0/240 (0.00)0/96 (0.00)0/144 (0.00)
      Overall adverse events44/251 (17.5)6/98 (6.12)38/153 (24.8).003
      Generalized estimated equation model was used adjusting for correlation between eyes.
      a Generalized estimated equation model was used adjusting for correlation between eyes.
      b Fisher exact test was used without adjusting for correlation between eyes due to rare events in both groups.Note: Censored patients were not included in the denominator.
      Kaplan-Meier curves (Figure 2) showed that the time-dependent incidence of GRAEs (P = .005) and overall AEs (P = .002) was higher in the sulcus than in the capsular group. No significant difference was found between the 2 groups for the time-dependent incidence of iris synechiae (P = .081), corectopia and/or discoria (P = .135), IOL dislocation (P = .151), and VAO (P = .849).
      FIGURE 2
      FIGURE 2Longitudinal comparisons for the incidence of (A) intraocular lens (IOL) dislocation, (B) glaucoma-related adverse events (GRAE), (C) iris synechia, (D) visual axis opacification (VAO), (E) corectopia and/or discoria, and (F) overall complications (N = 355 eyes)
      Univariable analysis in the Cox proportional hazard model (Table 3) showed a lower risk for GRAE was conferred by in-the-bag IOL implantation (HR, 0.06; 95% CI 0.01-0.44; P = .005) and younger age at IOL implantation (HR, 1.03; 95% CI, 1.00-1.07; P = .034). In the multivariable analysis, in-the-bag IOL implantation was the only variable associated with decreased risk of GRAE (HR, 0.08; 95% CI, 0.01-0.53; P = .009). In-the-bag IOL implantation also conferred a lower risk for overall AEs (capsular implant: HR, 0.21; 95% CI, 0.08-0.57; P = .002).
      TABLE 3Cox Proportional Hazard Model for Assessing the Effect of Intraocular Lens Location and Other Potential Risk Factors on Adverse Events After Secondary Intraocular Lens Implantation (N =355 Eyes)
      Adverse eventsFactorsUnivariable Regression AnalysisMultivariable Regression Analysis
      Variables with P < .05 in univariable analysis were included in the multivariable regression model. The bold P value is statistically significant. Note: Censoring was defined as lost to follow-up in random before 3 years postoperatively without presence of any adverse events. GRAE = glaucoma related adverse event, IOL = intraocular lens.
      Hazard Ratio95% CIPHazard Ratio95% CIP
      GRAEIn-the-bag IOL0.060.01-0.44.0050.080.01- 0.53.009
      Age at cataract removal0.950.82-1.10.479
      Age at IOL implant1.031.00-1.07.0341.020.99-1.06.177
      Male sex1.040.37-2.94.941
      Unilateral0.370.05-2.81.334
      Iris synechiaeIn-the-bag IOL0.260.06-1.18.081
      Age at cataract removal1.050.96-1.14.270
      Age at IOL implant1.000.98-1.03.702
      Male sex0.900.26-3.06.861
      Unilateral2.530.68-9.43.167
      Corectopia and/or discoriaIn-the-bag IOL0.200.03-1.64.135
      Age at cataract removal1.040.94-1.15.471
      Age at IOL implant0.990.96-1.02.506
      Male sex0.930.23-3.78.915
      Unilateral2.770.56-13.6.210
      Overall adverse eventsIn-the-bag IOL0.210.08-0.57.002
      Age at cataract removal1.000.94-1.08.901
      Age at IOL implant1.021.00-1.04.119
      Male sex0.990.48-2.01.969
      Unilateral0.820.28-2.38.718
      a Variables with P < .05 in univariable analysis were included in the multivariable regression model. The bold P value is statistically significant.Note: Censoring was defined as lost to follow-up in random before 3 years postoperatively without presence of any adverse events.GRAE = glaucoma related adverse event, IOL = intraocular lens.
      Mean IOL decentration was smaller in the capsular group compared with the sulcus group (vertical decentration: 0.24 [SD, 0.21] mm vs 0.33 [SD, 0.29] mm, P = .003; horizontal decentration: 0.23 [SD, 0.14] mm vs. 0.32 [SD, 0.26] mm, P < .001) (Table 4). Vertical IOL decentration >0.4 mm occurred in 22 of 140 eyes (15.7%) in the capsular group, while the proportion in the sulcus group was significantly higher at 59 of 198 eyes (29.8%, P = .005). In the capsular group, 13 of 139 eyes (9.35%) had horizontal IOL decentration >0.4 mm, while the proportion in the sulcus group was significantly higher at 60 of 198 eyes (30.3%; P < .001). Degree of IOL tilt was similar in the 2 groups (vertical tilt: capsular 1.21° [SD, 1.05°] vs sulcus 1.24° [SD, 1.11°], P = .835; horizontal tilt: capsular 0.82° [SD, 0.83°] vs sulcus 0.91° [SD, 0.91°], P = .401). In the sulcus group, 1 eye (0.51%) had vertical tilt >7°, and 1 eye (0.51%) had horizontal tilt >7°. There were no eyes in the capsular group with vertical or horizontal tilt >7°.
      TABLE 4Intraocular Lens Tilt and Decentration at the Last Study Visit After Secondary Intraocular Lens Implantation (N = 355 eyes)
      Capsular (n = 144)Ciliary Sulcus (n = 211)P
      Vertical decentration
       Mean (SD), mm0.24 (0.21)0.33 (0.29).003
      Linear mixed model was used adjusting for correlation between eyes.
       >0.4 mm, eyes (%)22 (15.7)59 (29.8).005
      Generalized estimated equation was used adjusting for correlation between eyes. Note: Missing data attributed to image quality, n (%): vertical tilt, 19 (5.35); horizontal tilt, 18 (5.07); vertical decentration, 17 (4.79); and horizontal decentration, 18 (5.07).
      Horizontal decentration
       Mean (SD), mm0.23 (0.14)0.32 (0.26)<.001
      Linear mixed model was used adjusting for correlation between eyes.
       >0.4 mm, eyes (%)13 (9.35)60 (30.3)<.001
      Generalized estimated equation was used adjusting for correlation between eyes. Note: Missing data attributed to image quality, n (%): vertical tilt, 19 (5.35); horizontal tilt, 18 (5.07); vertical decentration, 17 (4.79); and horizontal decentration, 18 (5.07).
      Vertical tilt
       Mean (SD),°1.21 (1.05)1.24 (1.11).835
      Linear mixed model was used adjusting for correlation between eyes.
       >7°, eyes (%)0 (0.00)1 (0.51)
      Horizontal tilt
      s Mean (SD)0.82 (0.83)0.91 (0.91).401
      Linear mixed model was used adjusting for correlation between eyes.
       7°, eyes (%)0 (0.00)1 (0.51)
      a Linear mixed model was used adjusting for correlation between eyes.
      b Generalized estimated equation was used adjusting for correlation between eyes.Note: Missing data attributed to image quality, n (%): vertical tilt, 19 (5.35); horizontal tilt, 18 (5.07); vertical decentration, 17 (4.79); and horizontal decentration, 18 (5.07).
      BCVA at 1 and 2 years after IOL implantation did not differ between groups (P = .795 and P = .212, respectively). However, the capsular group showed better logMAR BCVA compared with the sulcus group at 3 years after IOL implantation (0.56 [SD, 0.29] vs 0.67 [SD, 0.32], P = .014) (Figure 3 and Supplemental Table 1). Ninety-two eyes (25.9%) of 53 children with postoperative follow-up <2.5 years due to the COVID-19 epidemic were excluded from analysis on changes in ocular refraction and biometry at 3 years, while 73 more eyes (20.6%, 49 children) were excluded from the analysis of vision due to congenital fundus anomalies (Supplemental Table 1).
      FIGURE 3
      FIGURE 3Longitudinal comparison of best-corrected visual acuity (BCVA) in the capsular and the sulcus group.
      The postoperative spherical equivalent (SE) in both groups showed myopic shift 3 years after IOL implantation (capsular: −2.21 [SD, 1.31] diopter [D], sulcus: −2.02 [SD, 1.52] D, P = .915). Postoperative corneal astigmatism was stable after secondary IOL implantation (capsular: 2.20 [SD, 1.84] D at 3 months vs 2.03 [SD, 1.51] D at 3 years, P = .298; sulcus: 1.93 [SD, 1.60] D at 3 months vs 1.71 [1.18] D at 3 years, P = .080). The postoperative mean anterior chamber depth (ACD) was greater in the capsular group compared with the sulcus group at 3 months (3.45 [SD, 0.49] mm for capsular and 2.83 [SD, 0.44] mm for sulcus, P < .001) and at 3 years (3.48 [SD, 0.47] mm for capsular and 2.87 [SD, 0.45] mm for sulcus, P < .001).
      The subgroup analysis of the above-mentioned outcomes remained the same when (1) including either the right eyes or the left eyes only for bilateral cases, (2) analyzing bilateral and unilateral cases separately, and (3) excluding those eyes with fundus anomalies. However, due to (1) rare or no AEs when the data were separated into subgroups and (2) small numbers of unilateral cases, no significant between-group differences were detected among unilateral cases, and it was not possible to draw survival curves or to detect any remaining significant factors in multivariate analysis in some subgroups (Supplemental Subgroup Analysis).

      DISCUSSION

      The 3-year follow-up data from this large, prospective cohort study demonstrate that secondary in-the-bag IOL placement results in fewer complications, better IOL centration, and improved vision compared with implantation in the ciliary sulcus.
      Our results highlighted in-the-bag IOL implantation as a protective factor against GRAE, extending over 3 years of follow-up. This finding is consistent with findings from other large cohort studies of surgical outcomes of pediatric cataract patients, such as the Toddler Aphakia and Pseudophakia Treatment Study Registry (TAPS) and the IoLunder2 cohort, demonstrating that GRAE is a common complication threatening visual prognosis after cataract surgery in infants and young children,
      • Bothun ED
      • Wilson ME
      • Vanderveen DK
      • et al.
      Outcomes of bilateral cataracts removed in infants 1 to 7 months of age using the toddler aphakia and pseudophakia treatment study registry.
      ,
      • Bothun ED
      • Wilson ME
      • Yen KG
      • et al.
      Outcomes of bilateral cataract surgery in infants 7 to 24 months of age using the toddler aphakia and pseudophakia treatment study registry.
      • Solebo AL
      • Rahi JS
      British congenital cataract interest group. glaucoma following cataract surgery in the first 2 years of life: frequency, risk factors and outcomes from iolunder2.
      • Bothun ED
      • Wilson ME
      • Traboulsi EI
      • et al.
      Outcomes of unilateral cataracts in infants and toddlers 7 to 24 months of age: toddler aphakia and pseudophakia study (TAPS).
      with incidence increasing gradually over the postoperative interval. The Infant Aphakia Treatment Study (IATS) reported that the incidence of GRAE in children aged 1 to 6 months at the time of cataract extraction rose from 12% at 1 year to 40% at 10 years after surgery.
      • Freedman SF
      • Beck AD
      • Nizam A
      • et al.
      Glaucoma-related adverse events at 10 years in the infant aphakia treatment study: a secondary analysis of a randomized clinical trial.
      We have summarized similar studies concerning secondary IOL implantation in pediatric eyes and compared them with the current study (Supplemental Table 2).
      • Wood KS
      • Tadros D
      • Trivedi RH
      • Wilson ME.
      Secondary intraocular lens implantation following infantile cataract surgery: intraoperative indications, postoperative outcomes.
      • Wilson Jr, ME
      • Hafez GA
      • Trivedi RH.
      Secondary in-the-bag intraocular lens implantation in children who have been aphakic since early infancy.
      • Nihalani BR
      • Vanderveen DK.
      Secondary intraocular lens implantation after pediatric aphakia.
      • Trivedi RH
      • Wilson Jr, ME
      • Facciani J.
      Secondary intraocular lens implantation for pediatric aphakia.
      • Crnic T
      • Weakley Jr, DR
      • Stager Jr, D
      • Felius J.
      Use of acrysof acrylic foldable intraocular lens for secondary implantation in children.
      ,
      • Shenoy BH
      • Mittal V
      • Gupta A
      • et al.
      Complications and visual outcomes after secondary intraocular lens implantation in children.
      The incidence of GRAE after secondary IOL implantation in pediatric eyes in previous publications has ranged from 2.60% to 18.9%.
      • Wilson Jr, ME
      • Hafez GA
      • Trivedi RH.
      Secondary in-the-bag intraocular lens implantation in children who have been aphakic since early infancy.
      ,
      • Trivedi RH
      • Wilson Jr, ME
      • Facciani J.
      Secondary intraocular lens implantation for pediatric aphakia.
      ,
      • Crnic T
      • Weakley Jr, DR
      • Stager Jr, D
      • Felius J.
      Use of acrysof acrylic foldable intraocular lens for secondary implantation in children.
      ,
      • Shenoy BH
      • Mittal V
      • Gupta A
      • et al.
      Complications and visual outcomes after secondary intraocular lens implantation in children.
      ,
      • Freedman SF
      • Beck AD
      • Nizam A
      • et al.
      Glaucoma-related adverse events at 10 years in the infant aphakia treatment study: a secondary analysis of a randomized clinical trial.
      Because only the cumulative incidence of GRAE was reported, with greatly variable follow-up intervals between studies, it is difficult to draw conclusions from the existing published literature on the impact of different methods of secondary IOL implantation. By comparing 144 eyes with in-the-bag IOL implantation to 211 eyes with ciliary sulcus IOL implantation in the current study, we found that in-the-bag IOL implantation significantly reduced the cumulative risk of GRAE after secondary IOL implantation in aphakic eyes and improved the 1-, 2-, and 3-year GRAE-free survival rates. ACD in the capsule group was significantly deeper than that in the sulcus group. This finding indicates that in-the-bag IOL implantation may reduce the incidence of GRAE by stabilizing IOL position and avoiding potential contact between the IOL and the iris, thus diminishing postoperative uveitis and damage to the chamber angle.
      • Wu X
      • Liu Z
      • Wang D
      • et al.
      Preoperative profile of inflammatory factors in aqueous humor correlates with postoperative inflammatory response in patients with congenital cataract.
      To the best of our knowledge, the current report represents the first time that tilt and decentration of the IOL in pediatric eyes with secondary IOL implantation have been quantitatively analyzed. Previous studies in pediatric eyes only reported cases of severe decentration requiring surgical intervention or where the edge of the IOL optic could be visualized through the dilated pupil.
      • Nihalani BR
      • Vanderveen DK.
      Secondary intraocular lens implantation after pediatric aphakia.
      • Trivedi RH
      • Wilson Jr, ME
      • Facciani J.
      Secondary intraocular lens implantation for pediatric aphakia.
      • Crnic T
      • Weakley Jr, DR
      • Stager Jr, D
      • Felius J.
      Use of acrysof acrylic foldable intraocular lens for secondary implantation in children.
      ,
      • Shenoy BH
      • Mittal V
      • Gupta A
      • et al.
      Complications and visual outcomes after secondary intraocular lens implantation in children.
      We found that ciliary sulcus implantation was inferior to in-the-bag implantation in maintaining IOL centration (Supplemental Figure 2). It has been reported in adult pseudophakia that IOL decentration >0.4 mm may result in significant reduction in the optical performance of aspherical IOLs.
      • Chen X
      • Gu X
      • Wang W
      • et al.
      Characteristics and factors associated with intraocular lens tilt and decentration after cataract surgery.
      • Lawu T
      • Mukai K
      • Matsushima H
      • Senoo T.
      Effects of decentration and tilt on the optical performance of 6 aspheric intraocular lens designs in a model eye.
      • Taketani F
      • Matuura T
      • Yukawa E
      • Hara Y.
      Influence of intraocular lens tilt and decentration on wavefront aberrations.
      We found that one-third of sulcus-fixated IOLs had horizontal or vertical decentration >0.4 mm, while in the capsule-implanted group, only 15.7% (22/144) patients had vertical decentration >0.4 mm and 9.35% (13/44) had horizontal decentration >0.4 mm. Our quantitative results provide a reference for the choice of IOL in pediatric eyes, suggesting that aspherical IOLs should be used with caution in pediatric eyes requiring sulcus implantation.
      In this study, eyes undergoing in-the-bag IOL implant achieved better BCVA compared with those with ciliary sulcus implant. Possible reasons for better vision in the capsular group include lower incidences of AEs and better IOL positional stability, both conducive to improved visual acuity. However, the prognosis of visual acuity in patients with pediatric cataract is affected by a variety of factors, including ocular and systemic comorbidities, age at surgery, and unilateral vs bilateral cataract.
      While secondary in-the-bag IOL implantation contributes to better prognosis of pediatric eyes, it should be recognized that the choice of method during secondary IOL implantation is greatly affected by intraoperative factors in cataract extraction. The chief difficulty in achieving secondary in-the-bag IOL implantation in pediatric aphakic eyes lies in scarring and destruction of the lens capsule. To achieve secondary in-the-bag IOL implantation, the peripheral lens capsule must be protected during cataract extraction. Our previous work and that of other researchers suggests that the anterior capsulorhexis diameter should be 4 to 5 mm and the posterior capsulorhexis 3.5 to 4 mm during cataract extraction to avoid damaging the lens epithelial cells and to promote the formation of a transparent and volumized Soemmering ring, which is conducive to secondary in-the-bag IOL implantation.
      • Lin H
      • Tan X
      • Lin Z
      • et al.
      Capsular outcomes differ with capsulorhexis sizes after pediatric cataract surgery: a randomized controlled trial.
      ,
      • Wilson Jr, ME
      • Englert JA
      • Greenwald MJ.
      In-the-bag secondary intraocular lens implantation in children.
      To our knowledge, this cohort is the largest to provide data on longitudinal outcomes of in-the-bag vs ciliary sulcus secondary IOL implantation in pediatric eyes. The strength of this study is that our use of regression modeling reduced the influence of potential confounders, such as preoperative visual acuity, age at cataract extraction and IOL implantation, and length of operative interval. Prospective data collection in our study ensured that participants had standardized follow-up time, which overcame the limitations of previous cross-sectional and retrospective studies. In addition, cumulative incidence, survival curves, and Cox proportional hazard analysis were used to assess the impact of IOL implantation modality on AEs from both cross-sectional and time-dependent perspectives, providing longitudinal evidence while controlling for potential confounding factors.
      The interpretation of these results must also allow for study limitations. Existing differences between the study groups before secondary IOL implantation must be considered. Notably, in this study, there were no significant intergroup differences before IOL implantation in preoperative BCVA, age at cataract extraction or IOL implantation, surgical interval, AL, or IOP.
      However, it is possible that those eyes in which the capsular bag could not be opened had a more complex initial cataract surgery or postoperative course, which could have made GRAE or other AEs more likely. Secondly, inconsistent methods of visual acuity assessment due to the varying ages of participants may affect the longitudinal comparability of our vision data.
      In conclusion, our study demonstrates that secondary in-the-bag IOL implantation is preferable to ciliary sulcus implantation in the treatment of pediatric aphakia. In-the-bag IOL implantation achieves a lower incidence of postoperative AEs, especially GRAEs, and better IOL centration and visual acuity in this Chinese cohort. Long-term follow-up of the cohort should be done to further validate the conclusions of the current study.
      Funding/Support: This study was supported by the National Natural Science Foundation of China (81873675, 81770967) and the Construction Project of High-Level Hospitals in Guangdong Province (303020102).
      Financial Disclosures: The authors indicate no financial support or conflicts of interest. All authors attest that they meet the current ICMJE criteria for authorship.
      Authorship: Dr Z. Liu and Dr H. Lin served jointly as first authors. Dr W. Chen and Dr Y. Liu served jointly as senior authors. Dr L. Luo and Dr Y. Liu served jointly as corresponding authors.

      Appendix. Supplementary materials

      REFERENCES

        • Solebo AL
        • Cumberland P
        • Rahi JS
        British isles congenital cataract interest group. 5-year outcomes after primary intraocular lens implantation in children aged 2 years or younger with congenital or infantile cataract: findings from the iolunder2 prospective inception cohort study.
        Lancet Child Adolesc Health. 2018; 2: 863-871
        • Lambert SR
        • Cotsonis G
        • DuBois L
        • et al.
        Long-term effect of intraocular lens vs contact lens correction on visual acuity after cataract surgery during infancy: a randomized clinical trial.
        JAMA Ophthalmol. 2020; 138: 365-372
        • Bothun ED
        • Wilson ME
        • Vanderveen DK
        • et al.
        Outcomes of bilateral cataracts removed in infants 1 to 7 months of age using the toddler aphakia and pseudophakia treatment study registry.
        Ophthalmology. 2020; 127: 501-510
        • Wood KS
        • Tadros D
        • Trivedi RH
        • Wilson ME.
        Secondary intraocular lens implantation following infantile cataract surgery: intraoperative indications, postoperative outcomes.
        Eye (Lond). 2016; 30: 1182-1186
        • Wilson Jr, ME
        • Hafez GA
        • Trivedi RH.
        Secondary in-the-bag intraocular lens implantation in children who have been aphakic since early infancy.
        J AAPOS. 2011; 15: 162-166
        • Nihalani BR
        • Vanderveen DK.
        Secondary intraocular lens implantation after pediatric aphakia.
        J AAPOS. 2011; 15: 435-440
        • Trivedi RH
        • Wilson Jr, ME
        • Facciani J.
        Secondary intraocular lens implantation for pediatric aphakia.
        J AAPOS. 2005; 9: 346-352
        • Crnic T
        • Weakley Jr, DR
        • Stager Jr, D
        • Felius J.
        Use of acrysof acrylic foldable intraocular lens for secondary implantation in children.
        J AAPOS. 2004; 8: 151-155
        • Koch CR
        • Kara-Junior N
        • Serra A
        • Morales M.
        Long-term results of secondary intraocular lens implantation in children under 30 months of age.
        Eye (Lond). 2018; 32: 1858-1863
        • Shenoy BH
        • Mittal V
        • Gupta A
        • et al.
        Complications and visual outcomes after secondary intraocular lens implantation in children.
        Am J Ophthalmol. 2015; 159: 720-726
        • Kristianslund O
        • Raen M
        • Ostern AE
        • Drolsum L.
        Glaucoma and intraocular pressure in patients operated for late in-the-bag intraocular lens dislocation: a randomized clinical trial.
        Am J Ophthalmol. 2017; 176: 219-227
        • Ollerton A
        • Werner L
        • Strenk S
        • et al.
        Pathologic comparison of asymmetric or sulcus fixation of 3-piece intraocular lenses with square versus round anterior optic edges.
        Ophthalmology. 2013; 120: 1580-1587
        • Uy HS
        • Chan PS.
        Pigment release and secondary glaucoma after implantation of single-piece acrylic intraocular lenses in the ciliary sulcus.
        Am J Ophthalmol. 2006; 142: 330-332
        • Mehta R
        • Aref AA.
        Intraocular lens implantation in the ciliary sulcus: challenges and risks.
        Clin Ophthalmol. 2019; 13: 2317-23123
        • Zhao YE
        • Gong XH
        • Zhu XN
        • et al.
        Long-term outcomes of ciliary sulcus versus capsular bag fixation of intraocular lenses in children: an ultrasound biomicroscopy study.
        PLoS One. 2017; 12e0172979
        • Lin H
        • Tan X
        • Lin Z
        • et al.
        Capsular outcomes differ with capsulorhexis sizes after pediatric cataract surgery: a randomized controlled trial.
        Sci Rep. 2015; 5: 16227
        • Luo L
        • Lin H
        • Chen W
        • et al.
        In-the-bag intraocular lens placement via secondary capsulorhexis with radiofrequency diathermy in pediatric aphakic eyes.
        PLoS One. 2013; 8: e62381
        • Wilson Jr, ME
        • Englert JA
        • Greenwald MJ.
        In-the-bag secondary intraocular lens implantation in children.
        J AAPOS. 1999; 3: 350-355
        • Grewal DS
        • Basti S.
        Modified technique for removal of soemmerring ring and in-the-bag secondary intraocular lens placement in aphakic eyes.
        J Cataract Refract Surg. 2012; 38: 739-742
        • Lin H
        • Chen W
        • Luo L
        • et al.
        Effectiveness of a short message reminder in increasing compliance with pediatric cataract treatment: a randomized trial.
        Ophthalmology. 2012; 119: 2463-2470
        • Wang J
        • Chen J
        • Chen W
        • et al.
        Incidence of and risk factors for suspected glaucoma and glaucoma after congenital and infantile cataract surgery: a longitudinal study in china.
        J Glaucoma. 2020; 29: 46-52
        • Baumeister M
        • Neidhardt B
        • Strobel J
        • Kohnen T.
        Tilt and decentration of three-piece foldable high-refractive silicone and hydrophobic acrylic intraocular lenses with 6-mm optics in an intraindividual comparison.
        Am J Ophthalmol. 2005; 140: 1051-1058
        • Bothun ED
        • Wilson ME
        • Yen KG
        • et al.
        Outcomes of bilateral cataract surgery in infants 7 to 24 months of age using the toddler aphakia and pseudophakia treatment study registry.
        Ophthalmology. 2021; 128: 302-308
        • Solebo AL
        • Rahi JS
        British congenital cataract interest group. glaucoma following cataract surgery in the first 2 years of life: frequency, risk factors and outcomes from iolunder2.
        Br J Ophthalmol. 2020; 104: 967-973
        • Bothun ED
        • Wilson ME
        • Traboulsi EI
        • et al.
        Outcomes of unilateral cataracts in infants and toddlers 7 to 24 months of age: toddler aphakia and pseudophakia study (TAPS).
        Ophthalmology. 2019; 126: 1189-1195
        • Freedman SF
        • Beck AD
        • Nizam A
        • et al.
        Glaucoma-related adverse events at 10 years in the infant aphakia treatment study: a secondary analysis of a randomized clinical trial.
        JAMA Ophthalmol. 2021; 139: 165-173
        • Wu X
        • Liu Z
        • Wang D
        • et al.
        Preoperative profile of inflammatory factors in aqueous humor correlates with postoperative inflammatory response in patients with congenital cataract.
        Mol Vis. 2018; 24: 414-424
        • Chen X
        • Gu X
        • Wang W
        • et al.
        Characteristics and factors associated with intraocular lens tilt and decentration after cataract surgery.
        J Cataract Refract Surg. 2020; 46: 1126-1131
        • Lawu T
        • Mukai K
        • Matsushima H
        • Senoo T.
        Effects of decentration and tilt on the optical performance of 6 aspheric intraocular lens designs in a model eye.
        J Cataract Refract Surg. 2019; 45: 662-668
        • Taketani F
        • Matuura T
        • Yukawa E
        • Hara Y.
        Influence of intraocular lens tilt and decentration on wavefront aberrations.
        J Cataract Refract Surg. 2004; 30: 2158-2162