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Cataract surgery with primary intraocular lens implantation in children with uveitis: Long-term outcomes
ARTICLE
Cataract surgery with primary intraocular lens implantation in children with uveitis: Long-term outcomes Celine Terrada, MD, PhD, Karina Julian, MD, Nathalie Cassoux, MD, PhD, Anne-Marie Prieur, MD, Marianne Debre, MD, Pierre Quartier, MD, PhD, Phuc LeHoang, MD, PhD, Bahram Bodaghi, MD, PhD
PURPOSE: To report long-term outcomes of cataract surgery with primary posterior chamber intraocular lens (IOL) implantation in children with chronic uveitis. SETTING: Department of Ophthalmology, Pitie-Salp^etriere Hospital, Paris, France. DESIGN: Case series. METHODS: This case series comprised patients younger than 16 years with chronic uveitis who underwent phacoemulsification with primary implantation of a heparin surface-modified poly(methyl methacrylate) posterior chamber IOL in the capsular bag. The intraocular inflammation was fully controlled for at least 3 consecutive months before surgery in all cases. The main outcome measures were final corrected distance visual acuity (CDVA), postoperative inflammation, complications, and level of immunosuppressive treatment. RESULTS: Twenty-two eyes of 16 children (7 girls, 9 boys; median age at surgery 9.5 years old) were included. Underlying uveitic entities were juvenile idiopathic arthritis in 9 patients; idiopathic uveitis in 4; and Behc‚et disease, sarcoidosis, and varicella zoster-associated uveitis in 1 patient each. The final CDVA was 0.3 logMAR or better in all cases. Postoperative complications included posterior capsule opacification requiring laser capsulotomy in 2 eyes, glaucoma in 4 eyes, and cystoid macular edema/macular dysfunction in 3 eyes. The mean dose of oral prednisone was 29.5 mg/day preoperatively and 8.13 mg/day at the last follow-up. The median follow-up was 6 years (range 5 to 19 years). CONCLUSION: The results indicate that uveitis is not a formal contraindication to primary IOL implantation in the management of pediatric cataract surgery in cases with full control of intraocular inflammation. Financial Disclosure: No author has a financial or proprietary interest in any material or method mentioned. J Cataract Refract Surg 2011; 37:1977–1983 Q 2011 ASCRS and ESCRS
Cataract development is the most frequent complication in children with chronic uveitis1 and can occur as a sequel of the long-standing inflammation or secondary to corticosteroid treatment. It can be predicted to appear at a rate of 0.16 events per patient and year of follow-up.2 Although adult uveitic cataracts are commonly managed with phacoemulsification and primary intraocular lens (IOL) implantation,3 surgical treatment of uveitis-related pediatric cataract remains challenging, with no approach accepted as the standard one. Cataract aspiration with primary IOL implantation has been shown to be safe and effective in Q 2011 ASCRS and ESCRS Published by Elsevier Inc.
children older than 2 years without uveitis4; however, these results are not easily extrapolated to the management of uveitic pediatric cataract. A major point of controversy is whether to implant an IOL because it has been thought that IOLs might aggravate inflammation, mainly in cases of juvenile idiopathic arthritis (JIA)–associated uveitis in which the IOL may act as a scaffold for cyclitic membrane formation, leading to chronic hypotony and phthisis bulbi.5 In recent years, the development of new therapeutic antiinflammatory modalities (local or systemic) has allowed better control of inflammation, leading to 0886-3350/$ - see front matter doi:10.1016/j.jcrs.2011.05.037
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the idea that primary IOL implantation in these cases may be possible. We report the long-term outcomes of cataract surgery with primary IOL implantation in a group of children with chronic uveitis. PATIENTS AND METHODS Clinical files of all pediatric patients with uveitis who had cataract surgery with primary IOL implantation between January 1996 and December 2001 at the Ophthalmology Department, Pitie-Salp^etriere Hospital, Paris, France, were reviewed. Inclusion criteria were chronic uveitis with full control of intraocular inflammation (!1C cells in anterior chamber or vitreous body) for at least 3 consecutive months before surgery, reduced corrected distance visual acuity (CDVA) (%20/50) due to cataract or the presence of cataract that would preclude thorough posterior segment evaluation, phacoemulsification/phacoaspiration with primary posterior chamber heparin surface-modified (HSM) poly(methyl methacrylate) (PMMA) IOL implantation, and a minimum follow-up of 5 years. Patients younger than 4 years or older than 16 years at the time of surgery, patients who did not receive an IOL, and cases with follow-up shorter than 5 years were excluded. Cataracts were evaluated using the Lens Opacities Classification System III.6 All surgical procedures were performed under general anesthesia using a standard phacoemulsification technique. Briefly, after a clear corneal incision was made, a continuous curvilinear capsulorhexis (CCC) was created and phacoemulsification and phacoaspiration were performed. In some cases, lysis of a pupillary membrane, pupil expansion, and posterior capsulorhexis with core vitrectomy were performed. After in-the-bag implantation of an HSM PMMA IOL, 200 mg of dexamethasone was injected into the anterior chamber. Preoperative topical corticosteroid therapy was adjusted on an individual basis to obtain the minimum achievable level of inflammation. For 3 days, perioperative treatment consisted of increased oral corticosteroids (prednisone 0.5 mg/kg/day) adjusted to the corticodependence level. Intravenous corticosteroids (5 to 10 mg/kg) were administrated during surgery followed by 1 mg/kg/day oral treatment with an individualized tapering regimen. Topical corticosteroids were instilled hourly in all cases with a nighttime dexamethasone ointment during the first 4 postoperative days and then tapered according to inflammation. All patients were examined preoperatively and postoperatively at 1 day, 1, 2, and 3 weeks, 3, 6, and 12 months, and twice a year thereafter. This schedule was modified if clinical
Submitted: August 15, 2010. Final revision submitted: April 14, 2011. Accepted: May 5, 2011. From the Department of Ophthalmology (Terrada, Julian, Cassoux, LeHoang, Bodaghi), University of Paris VI, Pitie-Salp^etriere Hospital, and the Immuno-Hematology and Rheumatology Units (Prieur, Debre, Quartier), APHP, Necker Hospital, Paris, France. Corresponding author: Celine Terrada, MD, PhD, Department of Ophthalmology, University of Paris VI, Pitie-Salp^etriere Hospital, 47 Boulevard de l’H^opital, 75013 Paris, France. E-mail: [email protected].
symptoms were present. Postoperative data gathered included CDVA, intraocular pressure, degree of intraocular inflammation, and current topical and/or systemic treatment. The Student t test was used to evaluate visual outcomes before and at different time points after surgery and to analyze corticosteroid and immunosuppressant dosages before surgery and during the follow-up. A P value of 0.05 or less was considered statistically significant.
RESULTS Twenty-two eyes of 16 children (7 girls and 9 boys) were included. Table 1 shows the patients’ main clinical characteristics. The median age at uveitis diagnosis was 5 years old (mean 9.8; range 4 to 15 years) and the median age at surgery, 9.5 years old (mean 6; range 4 to 10 years). Juvenile idiopathic arthritis–associated uveitis was the most frequent etiology (9 patients, 56.26%) followed by idiopathic uveitis (4 patients, 25%). The diagnosis in the remaining 3 cases was Behc¸et disease, sarcoidosis, and varicella zoster virus-associated uveitis, respectively. Twenty-one eyes had moderate to severe posterior subcapsular cataract and 1 eye, total cataract. Band keratopathy was present in 9 cases (40.9%) and posterior synechiae in 18 cases (81.8%). The median follow-up was 6 years (mean 6.2; range 5 to 9 years). All patients received systemic corticosteroids as part of their treatment at some time during the course of the disease. Immunosuppressants (methotrexate or azathioprine) were added in addition to steroids to control ocular inflammation (posterior synechiae membranes or posterior complications; ie, macular edema) and in cases of corticodependence or resistance. Methotrexate was added in 6 cases (10 eyes) between 6 months and 1 year after cataract surgery. In 2 of 6 cases (eyes 12, 13, and 21, 22), methotrexate was switched to azathioprine because of a lack of efficacy. Before surgery, 14 children were on systemic corticosteroids, with a mean dose of 29.5 mg/day. Methotrexate was given preoperatively at a mean dose of 16 mg/week (10 to 25 mg) to 6 patients, 5 (10 eyes) of who had JIA. Six patients (37.5%) had bilateral cataract surgery; at least 1 month elapsed between the 2 surgeries. Posterior capsulorhexis and anterior vitrectomy were performed in 18 eyes (81.8%) (Figure 1). The mean CDVA was 0.87 logMAR preoperatively, 0.34 logMAR 1 month postoperatively, 0.17 logMAR at 3 months, 0.23 logMAR at 6 months and 1 year, and 0.33 logMAR at 5 years. The difference between the preoperative CDVA and the postoperative CDVA was statistically significant at all time points. The CDVA improved initially in 20 eyes (90.9%). At the 5-year visit, the CDVA remained better that preoperatively in 19 eyes, had stabilized to preoperative
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Table 1. Patients characteristics. IOL Onset Uveitis Duration Cataract Preop Conditions Eye/Pt/Sex Age (Y) Preop (Y) Eye Type in Affected Eye 1/A/M 2/A/M 3/B/M 4/C/M 5/C/M 6/D/M 7/E/F 8/E/F 9/F/F 10/G/F 11/G/F 12/H/M 13/H/M 14/I/F 15/J/M 16/K/F 17/L/M 18/M/F 19/N/M 20/O/F 21/O/F 22/P/M
9 9 5 6 6 4 4 4 5 4 4 4 4 9 10 8 4 5 9 4 4 10
3.0 3.0 2.0 2.0 2.0 2.0 2.0 2.0 5.0 0.8 1.0 1.0 1.0 4.0 10.0 1.0 11.0 6.0 6.0 10.0 11.0 2.0
R L R L R R R L L R L L R L R L L R L R L R
SC SC SC CM CM SC SC SC SC SC SC SC SC SC SC Total SC SC SC SC SC SC
Surgery
KP CE/PC IOL KP CE/PC IOL CE/PC IOL PSyn 360 CE/PC IOL PCap AV PSyn 360 CE/PC IOL PCap AV PSyn 360 CE/PC IOL PCap AV PSyn 90 BK CE/PC IOL PCap AV PSyn 360 CE/PC IOL PCap AV PSyn 360 Trabeculectomy CE/PC IOL PCap AV PSyn 360 BK KP CE/PC IOL PCap AV PSyn 360 BK KP CE/PC IOL PCap AV CE/PC IOL PCap AV PSyn 360 BK CE/PC IOL PCap AV PSyn 360 BK C11E/PC IOL PCap AV PSyn 360 CE/PC IOL PCap AV PSyn 90 CE/PC IOL PCap AV PSyn 360 KP CE/PC IOL PCap AV CE/PC IOL PCap AV PSyn 360 BK CE/PC IOL PCap AV PSyn 360 CE/PC IOL PCap AV PSyn 360 CE/PC IOL PCap AV PSyn 360 CE/PC IOL PSyn 45
Material HSM PMMA HSM PMMA HSM PMMA HSM PMMA HSM PMMA HSM PMMA HSM PMMA HSM PMMA HSM PMMA HSM PMMA HSM PMMA HSM PMMA HSM PMMA HSM PMMA HSM PMMA HSM PMMA HSM PMMA HSM PMMA HSM PMMA HSM PMMA HSM PMMA HSM PMMA
Optic Diameter (mm) FU (Y) 7.0 7.0 6.5 6.5 6.5 7.0 7.0 7.0 6.5 7.0 7.0 6.5 7.0 7.0 7.0 7.0 6.5 7.0 6.5 7.0 7.0 7.0
9 9 7 7 7 10 11 11 7 8 8 7 7 7 11 7 7 8 7 10 9 8
AV Z anterior vitrectomy; BK Z band keratopathy; CE Z cataract extraction; CM Z cyclitic membrane; FU Z follow-up; HSM PMMA Z heparin-surfacemodified poly(methyl methacrylate); IOL Z intraocular lens; KP Z kerathopathy; PC Z posterior chamber; PCap Z posterior capsulorhexis; PSyn Z posterior synechiae; SC Z subcapsular opacification
levels in 2 eyes, and was worse than preoperatively in 1 eye (P ! .01) (Figure 2). The visual outcome was poor in 1 case of Behc¸et disease and another case of idiopathic uveitis. The Behc¸et case presented with severe retinal sequelae from retinitis and scars before surgery. The patient with idiopathic uveitis developed retinal detachment related to inflammation and intravitreal triamcinolone injection. A vitreous tent with pupil deformation requiring surgical revision occurred in 1 case (patient K); this was the only early postoperative complication in this series. Late postoperative complications included visual axis opacification (posterior capsule opacification [PCO]), cell proliferation on the anterior hyaloid surface, Elschnig pearl proliferation onto the optic axis, glaucoma (3 cases required trabeculectomy), giant cell deposits on the anterior IOL surface, and cystoid macular edema (Table 2 and Figure 3). A neodymium:YAG (Nd:YAG) laser capsulotomy was performed in 4 cases of PCO; the mean time between cataract surgery and laser treatment was 14 months (mean 13.75; range 11 to 16 months). One eye required a second Nd:YAG procedure to remove
Elschnig pearl growth at the borders of the first capsulotomy. The mean dose of oral prednisone was 29.5 mg/day G 9 (SD) preoperatively, 19.2 G 9.9 mg/day 6 months postoperatively, and 8.13 G 9.5 mg/day at the end of the follow-up period (P ! .005). Three months after surgery, and despite maximum local treatment with prednisone, 4 patients developed Cushingoid features. DISCUSSION Cataract surgery with primary IOL implantation is a common and accepted procedure in adult patients with uveitis. Even though good results are achieved in most cases, childhood uveitis has classically been considered a contraindication to IOL implantation and its management remains controversial. Pediatric cataract surgery is associated with a high degree of postoperative inflammation, with a fibrinous reaction present in almost 100% of cases. Reports in the 1990s5,7 recommended not implanting IOLs in cases of pediatric cataract secondary to uveitis. Pars plana vitrectomy, lens aspiration, and aphakia seemed a safe
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Figure 2. Mean logMAR CDVA over time. The horizontal bars represent the standard deviation (M Z month; Y Z year).
Figure 1. Preoperative view of the anterior segment in an affected eye and postoperative results. A: Examination of the anterior chamber after iris dilation with tropicamide. B: Cataract surgery was performed using a CCC followed by phacoaspiration. Posterior capsulorhexis was followed by a large anterior vitrectomy. An HSM PMMA posterior chamber IOL was implanted in the capsular bag.
and effective procedure in these cases. However, children with uveitis are sometimes bad candidates for contact lens adaptation, mainly because of the presence of band keratopathy. Also, in the case of unilateral cataract, the patient faces a high risk for irreversible amblyopia. Probst and Holland8 were the pioneers of primary IOL implantation in JIA-associated uveitis. In their small series of 7 patients, 5 patients were adults and 2 were younger than 10 years at the time of surgery. They found that postoperative complications were significantly more important in children than in adults, which highlights that tissue reactivity depends not only on the uveitis status but also on the patient's age at the time of surgery. Several studies of cataract surgery in cases of pediatric uveitis9 12 have been published; they used
different types of IOLs and report different results. Table 2 shows a comparison of several series.8 10,13 This change in attitude when approaching uveitisrelated pediatric cataract reflects the improvement in the medical control of inflammation, surgical techniques, and IOL design and materials. Lundvall and Zetterstr€ om9 describe 10 eyes of 7 children with uveitis who had cataract extraction with IOL implantation and posterior capsulectomy. The postoperative CDVA reached 20/50 to 20/20 in all but 2 eyes. Complications were reported in 70% of operated eyes, and these included opacities or membranes requiring reoperation in 7 eyes and glaucoma in 3 eyes. At the end of the mean 28-month postoperative follow-up, patients were on antiinflammatory treatment, but 1 showed signs of active uveitis. Lam et al.10 describe IOL implantation in 6 eyes of 5 patients with JIA-associated uveitis. Their retrospective study had good results over longer follow-up than in previous series. The authors attribute their results to the aggressive antiinflammatory treatment used to control intraocular inflammation. In a multicenter retrospective study of 18 children with uveitis, Nemet et al.11 compared 2 populations: patients with JIA-associated uveitis and patients with other types of pediatric uveitis. They found no difference in visual outcomes or complications between the 2 groups. This finding reflects progress in the medical management of JIA and JIA-associated uveitis and is parallel to the reduction in the prevalence of complications reported in recent series.14 BenEzra and Cohen13 concluded that children with JIA-associated uveitis usually have a complicated postoperative course because of increased disease severity and should be managed as a different population of childhood uveitis. However, Qui~ ones et al.12 found no statistically significant n
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Table 2. Comparison of late complications after cataract surgery between present study and other published series.* Study*/Year Complication
†
Posterior synechiae PCO Glaucoma Elschnig pearls Cells on IOL Recurrent CME
Present (N Z 16)
10
Lam 2003 (N Z 6)
Probst8/1996 (N Z 3)
Lundvall9/2000 (N Z 10)
BenEzra13/2000 (N Z 10)
d/d 2/2 d/5 3/3 2/1 3/0
d 5 2 1 d 1
d 1 2 d d d
d 7 3 d d d
3/1 d/4 d/1 d/d d/d 2/1
CME Z cystoid macular edema; IOL Z intraocular lens; JIA Z juvenile idiopathic arthritis; N Z total number of eyes; PCO Z posterior capsule opacification *First author † The number on the left side of the slashes represents an etiology other than JIA; the number on the right side of the slash represents JIA etiology. For example, 2 patients with PCO in the other group/2 patients in the JIA group
difference in outcomes between JIA-associated uveitis cases and cases with other causes of childhood uveitis. They concluded that immunomodulatory therapy set the stage for more favorable outcomes
in JIA patients through induction of a durable uveitis remission. In our analysis, we considered all 16 uveitis children as a group without differentiating between JIA and
Figure 3. Late postoperative complications. Late postoperative complications after cataract surgery included moderate (A) or excessive (B) giant cell proliferation on the IOL surface, Elschnig pearl formation (C), and PCO (D). J CATARACT REFRACT SURG - VOL 37, NOVEMBER 2011
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non-JIA cases because all cases were under strict control of inflammation by the time surgeries were performed. Although children with JIA-associated uveitis tend to develop a greater inflammatory response and have more severe and chronic eye disease, once they are on a good immunomodulatory therapeutic scheme and achieved a quiescent inflammatory status, primary IOL implantation was proposed. In all cases, we placed an HSM PMMA IOL in the capsular bag, the gold standard in pediatric cataract at the time children had surgery. In-the-bag IOL fixation is essential in the management of these cases because it prevents iris chaffing, with a subsequent increase in intraocular inflammation. A randomized study of cataract not related to uveitis15 compared biocompatibility between the HSM IOL we used and an acrylic hydrophobic IOL and found lower rates of inflammatory cell adhesion and anterior capsule opacification in the acrylic group, suggesting its use in pathologies with blood–ocular barrier damage. Another randomized series of adult cataract related to uveitis16 compared HSM PMMA, silicone, and hydrophobic acrylic and concluded that acrylic performs best in uveitic eyes. Although the best biomaterial for uveitic patients must still be established, we believe that the new generation of foldable hydrophobic acrylic IOLs has not only the advantage of better biocompatibility but also the possibility of being introduced through smaller incisions, which decrease the risk for complications and postoperative inflammation. Most of our patients had posterior capsulorhexis with anterior vitrectomy. BenEzra and Cohen17 evaluated the role of posterior capsulotomy and anterior vitrectomy in uveitic cataract in children and concluded that in most cases, eyes having a primary opening of the posterior capsule during initial surgery achieved better visual acuity than their follow eyes. More recently, Jensen et al.18 discussed the necessity and interest of posterior capsulotomy in children. Their results indicate that posterior capsulotomy is necessary in children younger than 6 years and that a posterior CCC in the absence of vitrectomy should not be considered. The two most recent studies of JIA-associated uveitis19,20 confirmed the requirement of maximum perioperative control of inflammation without an increased risk for ocular complications. The most common postoperative complication reported in the literature is PCO, with a frequency of 70% to 100% (Table 2). In our series, this complication appeared at a lower rate because of the primary posterior capsulorhexis. We recommended the primary posterior capsulorhexis to avoid a later need for Nd:YAG laser capsulotomy and to decrease the risk for uveitis flare-ups.
In summary, we report the results of cataract surgery and primary IOL implantation in the setting of pediatric uveitis. In accordance with previous studies, we recommend this approach in selected cases. Adequate diagnosis, full control of the underlying uveitic entity, and aggressive perioperative treatment of inflammation are essential to achieving good outcomes. REFERENCES 1. de Boer J, Wulffraat N, Rothova A. Visual loss in uveitis of childhood. Br J Ophthalmol 2003; 87:879–884. Available at: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC1771761/pdf/ bjo08700879.pdf. Accessed June 17, 2011 2. Rosenberg KD, Feuer WJ, Davis JL. Ocular complications of pediatric uveitis. Ophthalmology 2004; 111:2299–2306 3. Estafanous MFG, Lowder CY, Meisler DM, Chauhan R. Phacoemulsification cataract extraction and posterior chamber lens implantation in patients with uveitis. Am J Ophthalmol 2001; 131:620–625 4. Cassidy L, Rahi J, Nischal K, Russell-Eggitt I, Taylor D. Outcome of lens aspiration and intraocular lens implantation in children aged 5 years and under. Br J Ophthalmol 2001; 85:540–542. Available at: http://www.ncbi.nlm.nih.gov/pmc/articles/ PMC1723962/pdf/v085p00540.pdf. Accessed June 17, 2011 5. Foster CS, Barrett F. Cataract development and cataract surgery in patients with juvenile rheumatoid arthritisassociated iridocyclitis. Ophthalmology 1993; 100:809–817 6. Chylack LT Jr, Wolfe JK, Singer DM, Leske MC, Bullimore MA, Bailey IL, Friend J, McCarthy D, Wu S-Y, for the Longitudinal Study of Cataract Study Group. The Lens Opacities Classification System III. Arch Ophthalmol 1993; 111:831–836. Available at: http://archopht.ama-assn.org/cgi/reprint/111/6/831. Accessed June 17, 2011 7. Kanski JJ. Juvenile arthritis and uveitis. Surv Ophthalmol 1990; 34:253–267 8. Probst LE, Holland EJ. Intraocular lens implantation in patients with juvenile rheumatoid arthritis. Am J Ophthalmol 1996; 122:161–170 € m C. Cataract extraction and intraocular 9. Lundvall A, Zetterstro lens implantation in children with uveitis. Br J Ophthalmol 2000; 84:791–793. Available at: http://www.ncbi.nlm.nih.gov/ pmc/articles/PMC1723524/pdf/v084p00791.pdf. Accessed June 17, 2011 10. Lam LA, Lowder CY, Baerveldt G, Smith SD, Traboulsi EI. Surgical management of cataracts in children with juvenile rheumatoid arthritis-associated uveitis. Am J Ophthalmol 2003; 135:772–778 11. Nemet AY, Raz J, Sachs D, Friling R, Neuman R, Kramer M, Pandi SK, Sharma V, Assia EI. Primary intraocular lens implantation in pediatric uveitis; a comparison of 2 populations. Arch Ophthalmol 2007; 125:354–360. Available at: http://archopht. ama-assn.org/cgi/reprint/125/3/354. Accessed June 17, 2011 ~ones K, Cervantes-Castan ~eda RA, Hynes AY, Daoud YJ, 12. Quin Foster CS. Outcomes of cataract surgery in children with chronic uveitis. J Cataract Refract Surg 2009; 35:725–731 13. BenEzra D, Cohen E. Cataract surgery in children with chronic uveitis. Ophthalmology 2000; 107:1255–1260 14. Oren B, Sehgal A, Simon JW, Lee J, Blocker RJ, Biglan AW, Zobal-Ratner J. The prevalence of uveitis in juvenile rheumatoid arthritis. J AAPOS 2001; 5:2–4 15. Tognetto D, Toto L, Minutola D, di Nicola M, Di Mascio R, Ravalico G. Hydrophobic acrylic versus heparin surface-
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16.
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modified polymethylmethacrylate intraocular lens: a biocompatibility study. Graefes Arch Clin Exp Ophthalmol 2003; 241:625–630 JL, Chipont E, BenEzra D, Fakhry MA, International Ocular Alio Inflammation Society Study Group of Uveitic Cataract Surgery. Comparative performance of intraocular lenses in eyes with cataract and uveitis. J Cataract Refract Surg 2002; 28: 2096–2108 BenEzra D, Cohen E. Posterior capsulectomy in pediatric cataract surgery; the necessity of a choice. Ophthalmology 1997; 104:2168–2174 Jensen AA, Basti S, Greenwald MJ, Mets MB. When may the posterior capsule be preserved in pediatric intraocular lens surgery? Ophthalmology 2002; 109:324–327; discussion by JD Baker, 328 Sijssens KM, Los LI, Rothova A, Schellekens PAWJF, van de Does P, Stilma JS, de Boer HJ. Long-term ocular complications in aphakic versus pseudophakic eyes of children with juvenile
idiopathic arthritis-associated uveitis. Br J Ophthalmol 2010; 94:1145–1149 20. Grajewski RS, Zurek-Imhoff B, Roesel M, Heinz C, Heiligenhaus A. Favourable outcome after cataract surgery with IOL implantation in uveitis associated with juvenile idiopathic arthritis. Acta Ophthalmol (Oxf) 2011 Feb 11; [Epub ahead of print]
J CATARACT REFRACT SURG - VOL 37, NOVEMBER 2011
First author: Celine Terrada, MD, PhD Department of Ophthalmology, University of Paris VI, Pitie-Salp^etriere Hospital, Paris
Cataract surgery with primary intraocular lens implantation in children with uveitis: Long-term outcomes Celine Terrada, MD, PhD, Karina Julian, MD, Nathalie Cassoux, MD, PhD, Anne-Marie Prieur, MD, Marianne Debre, MD, Pierre Quartier, MD, PhD, Phuc LeHoang, MD, PhD, Bahram Bodaghi, MD, PhD
PURPOSE: To report long-term outcomes of cataract surgery with primary posterior chamber intraocular lens (IOL) implantation in children with chronic uveitis. SETTING: Department of Ophthalmology, Pitie-Salp^etriere Hospital, Paris, France. DESIGN: Case series. METHODS: This case series comprised patients younger than 16 years with chronic uveitis who underwent phacoemulsification with primary implantation of a heparin surface-modified poly(methyl methacrylate) posterior chamber IOL in the capsular bag. The intraocular inflammation was fully controlled for at least 3 consecutive months before surgery in all cases. The main outcome measures were final corrected distance visual acuity (CDVA), postoperative inflammation, complications, and level of immunosuppressive treatment. RESULTS: Twenty-two eyes of 16 children (7 girls, 9 boys; median age at surgery 9.5 years old) were included. Underlying uveitic entities were juvenile idiopathic arthritis in 9 patients; idiopathic uveitis in 4; and Behc‚et disease, sarcoidosis, and varicella zoster-associated uveitis in 1 patient each. The final CDVA was 0.3 logMAR or better in all cases. Postoperative complications included posterior capsule opacification requiring laser capsulotomy in 2 eyes, glaucoma in 4 eyes, and cystoid macular edema/macular dysfunction in 3 eyes. The mean dose of oral prednisone was 29.5 mg/day preoperatively and 8.13 mg/day at the last follow-up. The median follow-up was 6 years (range 5 to 19 years). CONCLUSION: The results indicate that uveitis is not a formal contraindication to primary IOL implantation in the management of pediatric cataract surgery in cases with full control of intraocular inflammation. Financial Disclosure: No author has a financial or proprietary interest in any material or method mentioned. J Cataract Refract Surg 2011; 37:1977–1983 Q 2011 ASCRS and ESCRS
Cataract development is the most frequent complication in children with chronic uveitis1 and can occur as a sequel of the long-standing inflammation or secondary to corticosteroid treatment. It can be predicted to appear at a rate of 0.16 events per patient and year of follow-up.2 Although adult uveitic cataracts are commonly managed with phacoemulsification and primary intraocular lens (IOL) implantation,3 surgical treatment of uveitis-related pediatric cataract remains challenging, with no approach accepted as the standard one. Cataract aspiration with primary IOL implantation has been shown to be safe and effective in Q 2011 ASCRS and ESCRS Published by Elsevier Inc.
children older than 2 years without uveitis4; however, these results are not easily extrapolated to the management of uveitic pediatric cataract. A major point of controversy is whether to implant an IOL because it has been thought that IOLs might aggravate inflammation, mainly in cases of juvenile idiopathic arthritis (JIA)–associated uveitis in which the IOL may act as a scaffold for cyclitic membrane formation, leading to chronic hypotony and phthisis bulbi.5 In recent years, the development of new therapeutic antiinflammatory modalities (local or systemic) has allowed better control of inflammation, leading to 0886-3350/$ - see front matter doi:10.1016/j.jcrs.2011.05.037
1977
1978
CATARACT SURGERY IN CHILDREN WITH UVEITIS
the idea that primary IOL implantation in these cases may be possible. We report the long-term outcomes of cataract surgery with primary IOL implantation in a group of children with chronic uveitis. PATIENTS AND METHODS Clinical files of all pediatric patients with uveitis who had cataract surgery with primary IOL implantation between January 1996 and December 2001 at the Ophthalmology Department, Pitie-Salp^etriere Hospital, Paris, France, were reviewed. Inclusion criteria were chronic uveitis with full control of intraocular inflammation (!1C cells in anterior chamber or vitreous body) for at least 3 consecutive months before surgery, reduced corrected distance visual acuity (CDVA) (%20/50) due to cataract or the presence of cataract that would preclude thorough posterior segment evaluation, phacoemulsification/phacoaspiration with primary posterior chamber heparin surface-modified (HSM) poly(methyl methacrylate) (PMMA) IOL implantation, and a minimum follow-up of 5 years. Patients younger than 4 years or older than 16 years at the time of surgery, patients who did not receive an IOL, and cases with follow-up shorter than 5 years were excluded. Cataracts were evaluated using the Lens Opacities Classification System III.6 All surgical procedures were performed under general anesthesia using a standard phacoemulsification technique. Briefly, after a clear corneal incision was made, a continuous curvilinear capsulorhexis (CCC) was created and phacoemulsification and phacoaspiration were performed. In some cases, lysis of a pupillary membrane, pupil expansion, and posterior capsulorhexis with core vitrectomy were performed. After in-the-bag implantation of an HSM PMMA IOL, 200 mg of dexamethasone was injected into the anterior chamber. Preoperative topical corticosteroid therapy was adjusted on an individual basis to obtain the minimum achievable level of inflammation. For 3 days, perioperative treatment consisted of increased oral corticosteroids (prednisone 0.5 mg/kg/day) adjusted to the corticodependence level. Intravenous corticosteroids (5 to 10 mg/kg) were administrated during surgery followed by 1 mg/kg/day oral treatment with an individualized tapering regimen. Topical corticosteroids were instilled hourly in all cases with a nighttime dexamethasone ointment during the first 4 postoperative days and then tapered according to inflammation. All patients were examined preoperatively and postoperatively at 1 day, 1, 2, and 3 weeks, 3, 6, and 12 months, and twice a year thereafter. This schedule was modified if clinical
Submitted: August 15, 2010. Final revision submitted: April 14, 2011. Accepted: May 5, 2011. From the Department of Ophthalmology (Terrada, Julian, Cassoux, LeHoang, Bodaghi), University of Paris VI, Pitie-Salp^etriere Hospital, and the Immuno-Hematology and Rheumatology Units (Prieur, Debre, Quartier), APHP, Necker Hospital, Paris, France. Corresponding author: Celine Terrada, MD, PhD, Department of Ophthalmology, University of Paris VI, Pitie-Salp^etriere Hospital, 47 Boulevard de l’H^opital, 75013 Paris, France. E-mail: [email protected].
symptoms were present. Postoperative data gathered included CDVA, intraocular pressure, degree of intraocular inflammation, and current topical and/or systemic treatment. The Student t test was used to evaluate visual outcomes before and at different time points after surgery and to analyze corticosteroid and immunosuppressant dosages before surgery and during the follow-up. A P value of 0.05 or less was considered statistically significant.
RESULTS Twenty-two eyes of 16 children (7 girls and 9 boys) were included. Table 1 shows the patients’ main clinical characteristics. The median age at uveitis diagnosis was 5 years old (mean 9.8; range 4 to 15 years) and the median age at surgery, 9.5 years old (mean 6; range 4 to 10 years). Juvenile idiopathic arthritis–associated uveitis was the most frequent etiology (9 patients, 56.26%) followed by idiopathic uveitis (4 patients, 25%). The diagnosis in the remaining 3 cases was Behc¸et disease, sarcoidosis, and varicella zoster virus-associated uveitis, respectively. Twenty-one eyes had moderate to severe posterior subcapsular cataract and 1 eye, total cataract. Band keratopathy was present in 9 cases (40.9%) and posterior synechiae in 18 cases (81.8%). The median follow-up was 6 years (mean 6.2; range 5 to 9 years). All patients received systemic corticosteroids as part of their treatment at some time during the course of the disease. Immunosuppressants (methotrexate or azathioprine) were added in addition to steroids to control ocular inflammation (posterior synechiae membranes or posterior complications; ie, macular edema) and in cases of corticodependence or resistance. Methotrexate was added in 6 cases (10 eyes) between 6 months and 1 year after cataract surgery. In 2 of 6 cases (eyes 12, 13, and 21, 22), methotrexate was switched to azathioprine because of a lack of efficacy. Before surgery, 14 children were on systemic corticosteroids, with a mean dose of 29.5 mg/day. Methotrexate was given preoperatively at a mean dose of 16 mg/week (10 to 25 mg) to 6 patients, 5 (10 eyes) of who had JIA. Six patients (37.5%) had bilateral cataract surgery; at least 1 month elapsed between the 2 surgeries. Posterior capsulorhexis and anterior vitrectomy were performed in 18 eyes (81.8%) (Figure 1). The mean CDVA was 0.87 logMAR preoperatively, 0.34 logMAR 1 month postoperatively, 0.17 logMAR at 3 months, 0.23 logMAR at 6 months and 1 year, and 0.33 logMAR at 5 years. The difference between the preoperative CDVA and the postoperative CDVA was statistically significant at all time points. The CDVA improved initially in 20 eyes (90.9%). At the 5-year visit, the CDVA remained better that preoperatively in 19 eyes, had stabilized to preoperative
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Table 1. Patients characteristics. IOL Onset Uveitis Duration Cataract Preop Conditions Eye/Pt/Sex Age (Y) Preop (Y) Eye Type in Affected Eye 1/A/M 2/A/M 3/B/M 4/C/M 5/C/M 6/D/M 7/E/F 8/E/F 9/F/F 10/G/F 11/G/F 12/H/M 13/H/M 14/I/F 15/J/M 16/K/F 17/L/M 18/M/F 19/N/M 20/O/F 21/O/F 22/P/M
9 9 5 6 6 4 4 4 5 4 4 4 4 9 10 8 4 5 9 4 4 10
3.0 3.0 2.0 2.0 2.0 2.0 2.0 2.0 5.0 0.8 1.0 1.0 1.0 4.0 10.0 1.0 11.0 6.0 6.0 10.0 11.0 2.0
R L R L R R R L L R L L R L R L L R L R L R
SC SC SC CM CM SC SC SC SC SC SC SC SC SC SC Total SC SC SC SC SC SC
Surgery
KP CE/PC IOL KP CE/PC IOL CE/PC IOL PSyn 360 CE/PC IOL PCap AV PSyn 360 CE/PC IOL PCap AV PSyn 360 CE/PC IOL PCap AV PSyn 90 BK CE/PC IOL PCap AV PSyn 360 CE/PC IOL PCap AV PSyn 360 Trabeculectomy CE/PC IOL PCap AV PSyn 360 BK KP CE/PC IOL PCap AV PSyn 360 BK KP CE/PC IOL PCap AV CE/PC IOL PCap AV PSyn 360 BK CE/PC IOL PCap AV PSyn 360 BK C11E/PC IOL PCap AV PSyn 360 CE/PC IOL PCap AV PSyn 90 CE/PC IOL PCap AV PSyn 360 KP CE/PC IOL PCap AV CE/PC IOL PCap AV PSyn 360 BK CE/PC IOL PCap AV PSyn 360 CE/PC IOL PCap AV PSyn 360 CE/PC IOL PCap AV PSyn 360 CE/PC IOL PSyn 45
Material HSM PMMA HSM PMMA HSM PMMA HSM PMMA HSM PMMA HSM PMMA HSM PMMA HSM PMMA HSM PMMA HSM PMMA HSM PMMA HSM PMMA HSM PMMA HSM PMMA HSM PMMA HSM PMMA HSM PMMA HSM PMMA HSM PMMA HSM PMMA HSM PMMA HSM PMMA
Optic Diameter (mm) FU (Y) 7.0 7.0 6.5 6.5 6.5 7.0 7.0 7.0 6.5 7.0 7.0 6.5 7.0 7.0 7.0 7.0 6.5 7.0 6.5 7.0 7.0 7.0
9 9 7 7 7 10 11 11 7 8 8 7 7 7 11 7 7 8 7 10 9 8
AV Z anterior vitrectomy; BK Z band keratopathy; CE Z cataract extraction; CM Z cyclitic membrane; FU Z follow-up; HSM PMMA Z heparin-surfacemodified poly(methyl methacrylate); IOL Z intraocular lens; KP Z kerathopathy; PC Z posterior chamber; PCap Z posterior capsulorhexis; PSyn Z posterior synechiae; SC Z subcapsular opacification
levels in 2 eyes, and was worse than preoperatively in 1 eye (P ! .01) (Figure 2). The visual outcome was poor in 1 case of Behc¸et disease and another case of idiopathic uveitis. The Behc¸et case presented with severe retinal sequelae from retinitis and scars before surgery. The patient with idiopathic uveitis developed retinal detachment related to inflammation and intravitreal triamcinolone injection. A vitreous tent with pupil deformation requiring surgical revision occurred in 1 case (patient K); this was the only early postoperative complication in this series. Late postoperative complications included visual axis opacification (posterior capsule opacification [PCO]), cell proliferation on the anterior hyaloid surface, Elschnig pearl proliferation onto the optic axis, glaucoma (3 cases required trabeculectomy), giant cell deposits on the anterior IOL surface, and cystoid macular edema (Table 2 and Figure 3). A neodymium:YAG (Nd:YAG) laser capsulotomy was performed in 4 cases of PCO; the mean time between cataract surgery and laser treatment was 14 months (mean 13.75; range 11 to 16 months). One eye required a second Nd:YAG procedure to remove
Elschnig pearl growth at the borders of the first capsulotomy. The mean dose of oral prednisone was 29.5 mg/day G 9 (SD) preoperatively, 19.2 G 9.9 mg/day 6 months postoperatively, and 8.13 G 9.5 mg/day at the end of the follow-up period (P ! .005). Three months after surgery, and despite maximum local treatment with prednisone, 4 patients developed Cushingoid features. DISCUSSION Cataract surgery with primary IOL implantation is a common and accepted procedure in adult patients with uveitis. Even though good results are achieved in most cases, childhood uveitis has classically been considered a contraindication to IOL implantation and its management remains controversial. Pediatric cataract surgery is associated with a high degree of postoperative inflammation, with a fibrinous reaction present in almost 100% of cases. Reports in the 1990s5,7 recommended not implanting IOLs in cases of pediatric cataract secondary to uveitis. Pars plana vitrectomy, lens aspiration, and aphakia seemed a safe
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Figure 2. Mean logMAR CDVA over time. The horizontal bars represent the standard deviation (M Z month; Y Z year).
Figure 1. Preoperative view of the anterior segment in an affected eye and postoperative results. A: Examination of the anterior chamber after iris dilation with tropicamide. B: Cataract surgery was performed using a CCC followed by phacoaspiration. Posterior capsulorhexis was followed by a large anterior vitrectomy. An HSM PMMA posterior chamber IOL was implanted in the capsular bag.
and effective procedure in these cases. However, children with uveitis are sometimes bad candidates for contact lens adaptation, mainly because of the presence of band keratopathy. Also, in the case of unilateral cataract, the patient faces a high risk for irreversible amblyopia. Probst and Holland8 were the pioneers of primary IOL implantation in JIA-associated uveitis. In their small series of 7 patients, 5 patients were adults and 2 were younger than 10 years at the time of surgery. They found that postoperative complications were significantly more important in children than in adults, which highlights that tissue reactivity depends not only on the uveitis status but also on the patient's age at the time of surgery. Several studies of cataract surgery in cases of pediatric uveitis9 12 have been published; they used
different types of IOLs and report different results. Table 2 shows a comparison of several series.8 10,13 This change in attitude when approaching uveitisrelated pediatric cataract reflects the improvement in the medical control of inflammation, surgical techniques, and IOL design and materials. Lundvall and Zetterstr€ om9 describe 10 eyes of 7 children with uveitis who had cataract extraction with IOL implantation and posterior capsulectomy. The postoperative CDVA reached 20/50 to 20/20 in all but 2 eyes. Complications were reported in 70% of operated eyes, and these included opacities or membranes requiring reoperation in 7 eyes and glaucoma in 3 eyes. At the end of the mean 28-month postoperative follow-up, patients were on antiinflammatory treatment, but 1 showed signs of active uveitis. Lam et al.10 describe IOL implantation in 6 eyes of 5 patients with JIA-associated uveitis. Their retrospective study had good results over longer follow-up than in previous series. The authors attribute their results to the aggressive antiinflammatory treatment used to control intraocular inflammation. In a multicenter retrospective study of 18 children with uveitis, Nemet et al.11 compared 2 populations: patients with JIA-associated uveitis and patients with other types of pediatric uveitis. They found no difference in visual outcomes or complications between the 2 groups. This finding reflects progress in the medical management of JIA and JIA-associated uveitis and is parallel to the reduction in the prevalence of complications reported in recent series.14 BenEzra and Cohen13 concluded that children with JIA-associated uveitis usually have a complicated postoperative course because of increased disease severity and should be managed as a different population of childhood uveitis. However, Qui~ ones et al.12 found no statistically significant n
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Table 2. Comparison of late complications after cataract surgery between present study and other published series.* Study*/Year Complication
†
Posterior synechiae PCO Glaucoma Elschnig pearls Cells on IOL Recurrent CME
Present (N Z 16)
10
Lam 2003 (N Z 6)
Probst8/1996 (N Z 3)
Lundvall9/2000 (N Z 10)
BenEzra13/2000 (N Z 10)
d/d 2/2 d/5 3/3 2/1 3/0
d 5 2 1 d 1
d 1 2 d d d
d 7 3 d d d
3/1 d/4 d/1 d/d d/d 2/1
CME Z cystoid macular edema; IOL Z intraocular lens; JIA Z juvenile idiopathic arthritis; N Z total number of eyes; PCO Z posterior capsule opacification *First author † The number on the left side of the slashes represents an etiology other than JIA; the number on the right side of the slash represents JIA etiology. For example, 2 patients with PCO in the other group/2 patients in the JIA group
difference in outcomes between JIA-associated uveitis cases and cases with other causes of childhood uveitis. They concluded that immunomodulatory therapy set the stage for more favorable outcomes
in JIA patients through induction of a durable uveitis remission. In our analysis, we considered all 16 uveitis children as a group without differentiating between JIA and
Figure 3. Late postoperative complications. Late postoperative complications after cataract surgery included moderate (A) or excessive (B) giant cell proliferation on the IOL surface, Elschnig pearl formation (C), and PCO (D). J CATARACT REFRACT SURG - VOL 37, NOVEMBER 2011
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non-JIA cases because all cases were under strict control of inflammation by the time surgeries were performed. Although children with JIA-associated uveitis tend to develop a greater inflammatory response and have more severe and chronic eye disease, once they are on a good immunomodulatory therapeutic scheme and achieved a quiescent inflammatory status, primary IOL implantation was proposed. In all cases, we placed an HSM PMMA IOL in the capsular bag, the gold standard in pediatric cataract at the time children had surgery. In-the-bag IOL fixation is essential in the management of these cases because it prevents iris chaffing, with a subsequent increase in intraocular inflammation. A randomized study of cataract not related to uveitis15 compared biocompatibility between the HSM IOL we used and an acrylic hydrophobic IOL and found lower rates of inflammatory cell adhesion and anterior capsule opacification in the acrylic group, suggesting its use in pathologies with blood–ocular barrier damage. Another randomized series of adult cataract related to uveitis16 compared HSM PMMA, silicone, and hydrophobic acrylic and concluded that acrylic performs best in uveitic eyes. Although the best biomaterial for uveitic patients must still be established, we believe that the new generation of foldable hydrophobic acrylic IOLs has not only the advantage of better biocompatibility but also the possibility of being introduced through smaller incisions, which decrease the risk for complications and postoperative inflammation. Most of our patients had posterior capsulorhexis with anterior vitrectomy. BenEzra and Cohen17 evaluated the role of posterior capsulotomy and anterior vitrectomy in uveitic cataract in children and concluded that in most cases, eyes having a primary opening of the posterior capsule during initial surgery achieved better visual acuity than their follow eyes. More recently, Jensen et al.18 discussed the necessity and interest of posterior capsulotomy in children. Their results indicate that posterior capsulotomy is necessary in children younger than 6 years and that a posterior CCC in the absence of vitrectomy should not be considered. The two most recent studies of JIA-associated uveitis19,20 confirmed the requirement of maximum perioperative control of inflammation without an increased risk for ocular complications. The most common postoperative complication reported in the literature is PCO, with a frequency of 70% to 100% (Table 2). In our series, this complication appeared at a lower rate because of the primary posterior capsulorhexis. We recommended the primary posterior capsulorhexis to avoid a later need for Nd:YAG laser capsulotomy and to decrease the risk for uveitis flare-ups.
In summary, we report the results of cataract surgery and primary IOL implantation in the setting of pediatric uveitis. In accordance with previous studies, we recommend this approach in selected cases. Adequate diagnosis, full control of the underlying uveitic entity, and aggressive perioperative treatment of inflammation are essential to achieving good outcomes. REFERENCES 1. de Boer J, Wulffraat N, Rothova A. Visual loss in uveitis of childhood. Br J Ophthalmol 2003; 87:879–884. Available at: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC1771761/pdf/ bjo08700879.pdf. Accessed June 17, 2011 2. Rosenberg KD, Feuer WJ, Davis JL. Ocular complications of pediatric uveitis. Ophthalmology 2004; 111:2299–2306 3. Estafanous MFG, Lowder CY, Meisler DM, Chauhan R. Phacoemulsification cataract extraction and posterior chamber lens implantation in patients with uveitis. Am J Ophthalmol 2001; 131:620–625 4. Cassidy L, Rahi J, Nischal K, Russell-Eggitt I, Taylor D. Outcome of lens aspiration and intraocular lens implantation in children aged 5 years and under. Br J Ophthalmol 2001; 85:540–542. Available at: http://www.ncbi.nlm.nih.gov/pmc/articles/ PMC1723962/pdf/v085p00540.pdf. Accessed June 17, 2011 5. Foster CS, Barrett F. Cataract development and cataract surgery in patients with juvenile rheumatoid arthritisassociated iridocyclitis. Ophthalmology 1993; 100:809–817 6. Chylack LT Jr, Wolfe JK, Singer DM, Leske MC, Bullimore MA, Bailey IL, Friend J, McCarthy D, Wu S-Y, for the Longitudinal Study of Cataract Study Group. The Lens Opacities Classification System III. Arch Ophthalmol 1993; 111:831–836. Available at: http://archopht.ama-assn.org/cgi/reprint/111/6/831. Accessed June 17, 2011 7. Kanski JJ. Juvenile arthritis and uveitis. Surv Ophthalmol 1990; 34:253–267 8. Probst LE, Holland EJ. Intraocular lens implantation in patients with juvenile rheumatoid arthritis. Am J Ophthalmol 1996; 122:161–170 € m C. Cataract extraction and intraocular 9. Lundvall A, Zetterstro lens implantation in children with uveitis. Br J Ophthalmol 2000; 84:791–793. Available at: http://www.ncbi.nlm.nih.gov/ pmc/articles/PMC1723524/pdf/v084p00791.pdf. Accessed June 17, 2011 10. Lam LA, Lowder CY, Baerveldt G, Smith SD, Traboulsi EI. Surgical management of cataracts in children with juvenile rheumatoid arthritis-associated uveitis. Am J Ophthalmol 2003; 135:772–778 11. Nemet AY, Raz J, Sachs D, Friling R, Neuman R, Kramer M, Pandi SK, Sharma V, Assia EI. Primary intraocular lens implantation in pediatric uveitis; a comparison of 2 populations. Arch Ophthalmol 2007; 125:354–360. Available at: http://archopht. ama-assn.org/cgi/reprint/125/3/354. Accessed June 17, 2011 ~ones K, Cervantes-Castan ~eda RA, Hynes AY, Daoud YJ, 12. Quin Foster CS. Outcomes of cataract surgery in children with chronic uveitis. J Cataract Refract Surg 2009; 35:725–731 13. BenEzra D, Cohen E. Cataract surgery in children with chronic uveitis. Ophthalmology 2000; 107:1255–1260 14. Oren B, Sehgal A, Simon JW, Lee J, Blocker RJ, Biglan AW, Zobal-Ratner J. The prevalence of uveitis in juvenile rheumatoid arthritis. J AAPOS 2001; 5:2–4 15. Tognetto D, Toto L, Minutola D, di Nicola M, Di Mascio R, Ravalico G. Hydrophobic acrylic versus heparin surface-
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First author: Celine Terrada, MD, PhD Department of Ophthalmology, University of Paris VI, Pitie-Salp^etriere Hospital, Paris