- Email: [email protected]
Incidence of and Factors Associated with Glaucoma after Surgery for Congenital Cataract
Incidence of and Factors Associated with Glaucoma after Surgery for Congenital Cataract Findings from the British Congenital Cataract Study Melanie Chak, MD, MRCOphth,1 Jugnoo Sangeeta Rahi, PhD, FRCOphth,1,2 on behalf of the British Congenital Cataract Interest Group* Purpose: To report the incidence of and factors associated with postoperative open-angle glaucoma in a nationally representative group of children undergoing surgery for congenital or infantile cataract. Design: Noncomparative interventional cohort study. Participants: All children in the United Kingdom who were newly diagnosed with congenital or infantile cataract in a 12-month period in 1995 and 1996 (the British Congenital/Infantile Cataract Study) were eligible for this study. One hundred sixty-five children with congenital or infantile cataract underwent cataract surgery. Methods: All the children were traced through their managing ophthalmologists. Standardized outcome data were collected at least 6 years after diagnosis. For children undergoing cataract extraction, Cox regression analysis was performed to determine incidence of postoperative open-angle glaucoma and the effect of key factors considered, a priori, potentially to be associated with it (i.e., age at detection and surgery, type of cataract surgery, primary intraocular lens implantation, severe postoperative uveitis, and microphthalmia). Main Outcome Measures: Development of open-angle glaucoma after cataract surgery. Results: Postoperative glaucoma developed in 27 of 275 eyes of 165 children who underwent cataract surgery. The overall annual incidence of postoperative glaucoma was 5.25 per 100 cataract operations. The median time to development of postoperative glaucoma was 1.34 years (range, 0.39 months– 6.73 years). Younger age at detection of cataract was the only factor independently associated with the development of glaucoma when all other factors of interest (which were all statistically associated with age at detection) were accounted for. A 10-fold increase in the age at detection (for example, 30 days compared with 3 days) was associated with a 64% decrease in the hazard ratio (95% confidence interval, 41%–79%; P⬍0.001). Conclusions: Median time to development of postoperative open-angle glaucoma in the present study was lower than that reported previously, emphasizing the need for vigilance from the early postoperative period. Earlier detection of cataract was the only significant factor associated with the development of glaucoma after surgery for congenital cataract. Ophthalmology 2008;115:1013–1018 © 2008 by the American Academy of Ophthalmology.
Postoperative open-angle glaucoma is emerging as potentially the most important visually disabling consequence of surgery for congenital or infantile cataract.1 It has been reported to occur in between 6% and 58.7% of children after cataract extraction, depending on the population studied and
the length of follow-up.2–11 It is insidious, can be difficult to detect, and may occur many years after surgery.2,5,6,12,13 Thus, it is now advised that all children should be considered at risk for the remainder of their lives.14 Treatment of pediatric aphakic glaucoma is challenging.
Originally received: March 6, 2007. Final revision: September 5, 2007. Accepted: September 5, 2007. Available online: December 27, 2007. Manuscript no. 2007-311. 1 Centre for Paediatric Epidemiology, Institute of Child Health, London, United Kingdom. 2 Division of Epidemiology, Institute of Ophthalmology, London, United Kingdom. Supported by the Guide Dogs for the Blind Association, Reading, United Kingdom (grant no. Fre07801 OR2001–26b). Research at the Institute of
Child Health and Great Ormond Street Hospital for Children National Health Service Trust benefits from research and development funding received from the National Health Service Executive, London, United Kingdom. There are no conflicts of interest. Correspondence to Jugnoo Sangeeta Rahi, PhD, Centre for Paediatric Epidemiology, Institute of Child Health, 30 Guilford Street, London WC1N 1EH, United Kingdom. *See “Appendix” for a full list of members of the British Congenital Cataract Interest Group (available at http://aaojournal.org).
© 2008 by the American Academy of Ophthalmology Published by Elsevier Inc.
ISSN 0161-6420/08/$–see front matter doi:10.1016/j.ophtha.2007.09.002
1013
Ophthalmology Volume 115, Number 6, June 2008 Treatment with antiglaucoma topical medication usually is a temporizing measure, with the definitive approaches being surgery, laser treatment, or both.15 However, the outcomes of surgical intervention often are disappointing in the long term.15–17 There is a need to identify factors associated with increased risk of postoperative open-angle glaucoma to decide on treatment and prevention strategies. From reports of selected individual case series, the following factors have been postulated to influence the risk of developing glaucoma: age at detection of cataract, age at cataract surgery, cataract surgery procedure, primary intraocular lens implantation, significant postoperative uveitis, and microphthalmia.4 – 6,8,18 –23 However, there has been limited populationbased research, which has particular strengths in relation to avoidance of bias and confounding. The authors report the incidence and factors associated with postoperative openangle glaucoma in a nationally representative group of children who underwent surgery for congenital or infantile cataract in the United Kingdom.
Patients and Methods All children newly diagnosed with congenital or infantile cataract in the United Kingdom during a 12-month period in 1995 and 1996 (previously identified for the British Congenital/Infantile Cataract study24 –28) and who underwent surgery were eligible for the present study. The authors previously reported24 –28 the methodologic details. To summarize, ophthalmologists and pediatricians actively reported, through 2 independent national surveillance schemes, all children younger than 16 years with newly diagnosed visually significant congenital or infantile cataract, regardless of treatment undertaken. Cases diagnosed after the age of 1 year were eligible only if, on review, they were the result of a congenital cause or had specific ophthalmic features indicative of early onset, such as cataract morphologic features or associated congenital
Figure 1. Flow chart showing study subjects with descriptive statistics.
1014
ocular anomaly. Children in whom cataract was acquired, for example as result of trauma, uveitis, irradiation, or drugs, were not eligible. All children in the original cohort were traced through their managing ophthalmologist, and those who had undergone cataract surgery were eligible for inclusion in the present study. Detailed clinical information about management and outcomes was collected using specifically designed questionnaires at least 6 years after diagnosis (between September 2002 and April 2003 inclusive). For data validation, patients managed at ophthalmic units contributing more than 4 children were examined independently by the principal investigator. Children were considered to have postoperative open-angle glaucoma for the purposes of this study if they underwent sustained treatment for glaucoma with drops, laser, surgery, or a combination thereof having been diagnosed by the managing consultant as having postoperative open-angle glaucoma. Other forms of glaucoma such as closed-angle glaucoma were excluded from the present analysis.
Statistical Analysis Based on the extant literature summarized earlier,4 – 6,8,18 –23 the factors considered, a priori, to be of interest in relation to the development of postoperative open-angle glaucoma were age at detection of cataract, age at cataract surgery, cataract surgery procedure, primary intraocular lens implantation, significant postoperative uveitis, and microphthalmia. First, the statistical relationships between these potential predictors were investigated. By convention, the authors then undertook univariate analysis and, subsequently, multivariate Cox regression analyses (using factors significant at Pⱕ0.05 level in univariate analysis) to examine the joint effects of these factors on time to development of glaucoma (hazard rate). For children with bilateral cataract who underwent surgery to both eyes, the correlation of the development of glaucoma in the same individual was accounted for by the use of 2-level hierarchical models: level 1 is the eye and level 2 is the child (http://www.cmm.bristol.ac.uk/ learning-training/index.shtml). Analysis was undertaken using STATA
Chak et al 䡠 Factors Associated with Glaucoma after Congenital Cataract Surgery
Figure 2. Graph showing the occurrence of postoperative glaucoma over time since surgery (Nelson-Aalen hazard curve).
software (Stata Corp., College Station, TX). Results are presented with 95% confidence intervals (CIs). The study followed the tenets of the Declaration of Helsinki, institutional review board/ethics committee approval was obtained, and the study adhered to extant research governance requirements.
Results One hundred sixty-five children (275 eyes) underwent surgery for congenital cataract, as summarized in Figure 1, at a median age of 4.5 months (range, 5 days–12.29 years) for bilateral cases and 2.8 months (range, 15 days–5.74 years) for unilateral cases. Follow-up data were available for all children despite 24 children being lost to follow-up and 3 deceased children. Denominators for different data items vary (according to completeness of data) and are reported separately in the figures and tables, as appropriate. One hundred twenty children (47%; 56 girls) had bilateral cataract and median age at the follow-up data collection for the present study of 6.79 years, whereas 45 (56%, 25 girls) with unilateral disease had a median age of 6.73 years at follow-up. Postoperative open-angle glaucoma developed in 10% (n ⫽ 24) of eyes of children with bilateral cataract and 7% (n ⫽ 3) of eyes of children with unilateral disease. The median time to development of postoperative glaucoma was 1.34 years (range, 0.39 months to 6.73 years). Postoperative closed-angle glaucoma occurred in 0.004% (n ⫽ 1) of eyes of children with bilateral cataracts and 7% (n ⫽ 3) of eyes of children with unilateral disease. The overall annual incidence rate of postoperative glaucoma was 5.25 cases per 100 eyes undergoing cataract extraction. The proportion of eyes developing glaucoma as a function of time to
occurrence is shown in Figure 2; the graph is truncated at postoperative follow-up of 6.95 years. Table 1 shows the type of cataract surgery performed, with most children undergoing aspiration and vitrectomy. In 4% (4/90) of children undergoing primary intraocular lens implantation, glaucoma developed, compared with 12% (23/185) of aphakic children (95% CI for difference in 2 proportions, 2%–14%; P ⫽ 0.01). Glaucoma developed in 22% (7/32) of children with microphthalmia versus 8% (20/236) without microphthalmia (95% CI for difference between two proportions, –1% to 28%; P ⫽ 0.08). There were strong statistical correlations between the key factors of interest in relation to the rate of development of aphakic glaucoma as shown in Table 2 (available at http://aaojournal.org); in particular, age at detection was highly correlated with age at surgery. Table 3 shows the results of the univariate analyses of the associations between individual factors of interest and the rate of development of postoperative open-angle glaucoma. These are depicted as the hazard ratio for developing postoperative glaucoma in the presence of the factor of interest (categoric predictors) or with a unit change in the factor (numeric predictors). Importantly, these analyses took into account the within-person correlation between eyes. The effect of this was a strengthening of the univariate associations between glaucoma and age at detection and age at surgery but a weakening of the univariate associations between primary intraocular implantation and microphthalmia. When the multivariate model was constructed, to examine the effects of each factor while accounting for the others, age at detection remained the only statistically significant (Pⱕ0.05) independently associated factor, with a hazard ratio of 0.36 (95% CI, 0.22– 0.59; P⬍0.0001). Thus, a 10-fold increase in the age at detection (for example, 10 days compared with 1 day or 30 days compared with 3 days) was associated with a 64% decrease in the hazard ratio (95% CI, 41%–79%; P⬍0.0001). The statistical correlation between age at detection and age at surgery may account for the fact that the latter was not statistically significant in the multivariate model (hazard ratio, 0.70; 95% CI, 0.21–2.30; P ⫽ 0.56). Figures 3 and 4 (both truncated at postoperative follow-up of 6.95 years) illustrate the variation in rate of development of postoperative glaucoma with variation in age at detection of cataract and age at surgery, respectively.
Discussion The overall annual incidence of aphakic glaucoma was 5.25 per 100 cataract operations during the first 7 postoperative years. Although in half of all cases glaucoma had occurred by 16 months (1.34 years) after cataract surgery, with the earliest onset being at 12 days after surgery (0.39 months), it is notable that the latest case occurred during the seventh postoperative year (6.73 years). Younger age at cataract detection was the only factor independently associated with its development when other relevant factors (with which it was strongly correlated statistically) as well as within-child
Table 1. Distribution of Postoperative Open-Angle Glaucoma by Type of Cataract Surgery Procedure (Median and Range of Duration of Follow-up)
Percentage with postoperative open-angle glaucoma
Lens Aspiration and Vitrectomy (5.86 yrs; 1.44–7.34)
Lens Aspiration Alone (5.94 yrs; 0.85–7.35)
Lensectomy-Vitrectomy (6.19 yrs; 0.87–7.29)
14% (18/107)
6% (5/81)
7% (4/51)
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Ophthalmology Volume 115, Number 6, June 2008 Table 3. Findings of Univariate Analysis (Cox Regression) of Association between Glaucoma and Variables of Interest Variable Log (increasing age at detection in days) Log (increasing age at cataract surgery age in days) Type of cataract surgery (lens aspiration alone†; baseline) Type of cataract surgery (lens aspiration and vitrectomy)† Type of cataract surgery (lensectomy-vitrectomy)† Primary intraocular lens implantation Significant postoperative uveitis Microphthalmia
Hazard Ratio (95% Confidence Interval*)
P Value*
0.36 (0.20–0.59) 0.31 (0.15–0.63)
⬍0.0001 ⬍0.0001
0.45 (0.14–1.48) 1.60 (0.50–4.63) 0.36 (0.10–1.31) 1.17 (0.14–8.75) 2.47 (0.87–7.45)
0.19 0.48 0.12 0.92 0.11
*Adjusted for clustering within child. Lensectomy-vitrectomy versus lens aspiration alone (hazard ratio, 0.71; 95% confidence interval, 0.14 –2.71; P ⫽ 0.61).
†
clustering were accounted for. A 10-fold increase in the age at detection was associated with a 64% decrease in the hazard ratio (95% CI, 41%–79%; P⬍0.0001). The authors’ use of a case definition for glaucoma based on a clinical decision to treat was deliberately conservative and may have resulted in some cases being excluded that might have been included in other studies. Differing definitions7,29 have been used previously, reflecting the difficulties of using objective criteria such as assessment of disc changes or perimetry, which are challenging in young children. Direct comparisons of these findings with those previously reported are difficult because of differences in methodology and statistical analyses, but they are broadly consistent in terms of the proportion of children in whom postoperative glaucoma developed in the short to medium term.2– 6,10 Importantly, median time to development of postoperative open-angle glaucoma in the present study was lower than reported previously.2,3,5–7,19 –22,30 –32 This em-
phasizes the need for vigilance from the early postoperative period. However further work is required to understand the long-term natural history and estimate the lifetime risk of postoperative glaucoma after surgery for congenital cataract. Previous studies have not addressed the age of detection of the cataract specifically, and therefore, it is difficult to make direct comparisons. It is notable that age at detection was significantly statistically correlated with factors identified previously as potential risk factors.4 – 6,8,18 –23 The authors think it most likely that the effect of age at detection on development of glaucoma is mediated mainly through its impact on age at surgery: earlier detection enables earlier surgery. Unlike others,3,4,29 the authors did not find a significant association between type of cataract surgery and glaucoma, even with comparable follow-up for each procedure, a criticism of previous studies.3,15 The authors did not find an association between microphthalmia and glaucoma. However, the statistical correlation
Figure 3. Graph showing the development of postoperative open-angle glaucoma by age at detection (Nelson-Aalen hazard curve).
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Chak et al 䡠 Factors Associated with Glaucoma after Congenital Cataract Surgery
Figure 4. Graph showing the development of postoperative open-angle glaucoma by age at cataract surgery (Nelson-Aalen hazard curve).
of age at detection and microphthalmia may be relevant, because the presence of the latter arguably may lead to earlier detection of cataract and in turn, earlier surgery, where undertaken. Notably, in previous studies suggesting the most significant factor to be age at cataract surgery, the children had a disproportionately high proportion of other ocular abnormalities such as microphthalmia.5 Equally, the authors found no association between postoperative uveitis and glaucoma, but the statistical correlation between younger age at detection and postoperative uveitis may be relevant, although the role of uveitis in the cause of aphakic glaucoma remains uncertain.2– 6,8,21 The authors also found no association between intraocular lens implantation and glaucoma, and again, the statistical correlation with age at detection may be relevant. Finally, however, it is important to note that many prior reports postulating a role for primary intraocular lens implantation, microphthalmia, and uveitis have not explicitly accounted for the correlation between the 2 eyes of the same individual, and this may have resulted in erroneous statistical significance testing. It seems that earlier detection of cataract incorporates all the risk factors that have been noted in previous papers to be independent risk factors. Earlier detection of cataract does not directly cause postoperative glaucoma, but earlier detection enables earlier surgery; this is the rationale for screening. Early surgery is essential to prevent amblyopia; however, previous reports have documented the higher frequency of complications with earlier surgery.10,30,33,34 Clinicians therefore are faced with the dilemma of balancing the timing of surgery to prevent amblyopia while minimiz-
ing postoperative complications. The point of equilibrium is unknown. A prospective study in which children were randomized to surgery at different ages within the critical period may address the question of optimum timing. In the meantime, the findings of this population-based study of postoperative open-angle glaucoma after congenital cataract surgery support the case for careful clinical surveillance for postoperative glaucoma from the earliest postoperative period and that this must continue in the long term.
References 1. Lambert SR, Drack AV. Infantile cataracts. Surv Ophthalmol 1996;40:427–58. 2. Asrani SG, Wilensky JT. Glaucoma after congenital cataract surgery. Ophthalmology 1995;102:863–7. 3. Chrousos GA, Parks MM, O’Neill JF. Incidence of chronic glaucoma, retinal detachment and secondary membrane surgery in pediatric aphakic patients. Ophthalmology 1984;91: 1238 – 41. 4. Keech RV, Tongue AC, Scott WE. Complications after surgery for congenital and infantile cataracts. Am J Ophthalmol 1989;108:136 – 41. 5. Mills M, Robb R. Glaucoma following childhood cataract surgery. J Pediatr Ophthalmol Strabismus 1994;31:355– 60. 6. Magnusson G, Abrahamsson M, Sjostrand J. Glaucoma following congenital cataract surgery: an 18-year longitudinal follow-up. Acta Ophthalmol Scand 2000;78:65–70. 7. Egbert JE, Wright MM, Dahlhauser KF, et al. A prospective study of ocular hypertension and glaucoma after pediatric cataract surgery. Ophthalmology 1995;102:1098 –101.
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Ophthalmology Volume 115, Number 6, June 2008 8. Parks MM, Johnson DA, Reed GW. Long-term visual results and complications in children with aphakia: a function of cataract type. Ophthalmology 1993;100:826 – 40, discussion 840 –1. 9. Johnson CP, Keech RV. Prevalence of glaucoma after surgery for PHPV and infantile cataracts. J Pediatr Ophthalmol Strabismus 1996;33:14 –7. 10. Vishwanath M, Cheong-Leen R, Taylor D, et al. Is early surgery for congenital cataract a risk factor for glaucoma? Br J Ophthalmol 2004;88:905–10. 11. Chen TC, Bhatia LS, Halpern EF, Walton DS. Risk factors for the development of aphakic glaucoma after congenital cataract surgery. J Pediatr Ophthalmol Strabismus 2006;43:274 – 80. 12. Wilson ME, Bluestein E, Wang X-H. Current trends in the use of intraocular lenses in children. J Cataract Refract Surg 1994;20:579 – 83. 13. Wilson ME, Elliot L, Johnson B, et al. AcrySof acrylic intraocular lens implantation in children: clinical indications of biocompatibility. J AAPOS 2001;5:377– 80. 14. Taylor D. Congenital cataract: the history, the nature and the practice. The Doyne Lecture. Eye 1998;12:9 –36. 15. Papadopoulos M, Khaw PT. Meeting the challenge of glaucoma after paediatric cataract surgery. Eye 2003;17:1–2. 16. Mandal AK, Bagga H, Nutheti R, et al. Trabeculectomy with and without mitomycin-C for paediatric glaucoma in aphakia and pseudophakia following congenital cataract surgery. Eye 2003;17:53– 62. 17. Azuara-Blanco A, Wilson RP, Spaeth GL, et al. Filtration procedures supplemented with mitomycin C in the management of childhood glaucoma. Br J Ophthalmol 1999;83: 151– 6. 18. Lundvall A, Zetterstrom C. Complications after early surgery for congenital cataracts. Acta Ophthalmol Scand 1999;77: 677– 80. 19. Wallace DK, Plager DA. Corneal diameter in childhood aphakic glaucoma. J Pediatr Ophthalmol Strabismus 1996;33: 230 – 4. 20. Miyahara S, Amino K, Tanihara H. Glaucoma secondary to pars plana lensectomy for congenital cataract. Graefes Arch Clin Exp Ophthalmol 2002;240:176 –9. 21. Rabiah PK. Frequency and predictors of glaucoma after pediatric cataract surgery. Am J Ophthalmol 2004;137:30 –7.
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22. Brady KM, Atkinson CS, Kilty LA, Hiles DA. Glaucoma after cataract extraction and posterior chamber lens implantation in children. J Cataract Refract Surg 1997;23(suppl):669 –74. 23. Asrani SG, Freedman SF, Hasselblad V, et al. Does primary intraocular lens implantation prevent “aphakic” glaucoma in children? J AAPOS 2000;4:33–9. 24. Rahi JS, Dezateux C, British Congenital Cataract Interest Group. Capture-recapture analysis of ascertainment by active surveillance in the British Congenital Cataract Study. Invest Ophthalmol Vis Sci 1999;40:236 –9. 25. Rahi JS, Dezateux C, British Congenital Cataract Interest Group. National cross sectional study of detection of congenital and infantile cataract in the United Kingdom: role of childhood screening and surveillance. BMJ 1999;318:362–5. 26. Rahi JS, Dezateux C, British Congenital Cataract Interest Group. Congenital and infantile cataract in the United Kingdom: underlying or associated factors. Invest Ophthalmol Vis Sci 2000;41:2108 –14. 27. Rahi JS, Botting BJ, British Congenital Cataract Interest Group. Ascertainment of children with congenital cataract through the National Congenital Anomaly System in England and Wales. Br J Ophthalmol 2001;85:1049 –51. 28. Rahi JS, Dezateux C, British Congenital Cataract Interest Group. Measuring and interpreting the incidence of congenital ocular anomalies: lessons from a national study of congenital cataract in the UK. Invest Ophthalmol Vis Sci 2001;42: 1444 – 8. 29. Simon JW, Mehta N, Simmons ST, et al. Glaucoma after pediatric lensectomy/vitrectomy. Ophthalmology 1991;98: 670 – 4. 30. Lundvall A, Kugelberg U. Outcome after treatment of congenital bilateral cataract. Acta Ophthalmol Scand 2002;80: 593–7. 31. Russell-Eggitt IM, Zamiri P. Review of aphakic glaucoma after surgery for congenital cataract. J Cataract Refract Surg 1997;23(suppl):664 – 8. 32. Walton DS. Pediatric aphakic glaucoma: a study of 65 patients. Trans Am Ophthalmol Soc 1995;93:403–13. 33. Hing S, Speedwell L, Taylor D. Lens surgery in infancy and childhood. Br J Ophthalmol 1990;74:73–7. 34. Magnusson G, Abrahamsson M, Sjostrand J. Changes in visual acuity from 4 to 12 years of age in children operated for bilateral congenital cataracts. Br J Ophthalmol 2002;86: 1385–9.
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Appendix: Members of the British Congenital Cataract Interest Group Mr Abdel-Khalek, Boston; Mr Aclimandos, London; Ms Adams, London; Mr Aftab, Scunthorpe; Ms Allen, Cambridge; Mr Amanat, Great Yarmouth; Mr Armstrong, Chester; Mr Assaf, Milton Keynes; Mr Astbury, Norwich; Mr Bannerjee, Wigan; Dr Barr, Dumferline; Ms Beck, Cardiff; Mr Beckingsale, Colchester; Mr Bedford, Dumfries; Mr Benjamin, Aylesbury; Ms Billington, Reading; Ms Blamires, Leicester; Mr Bloom, London; Mr Boase, Portsmouth; Mr Bolger, Hertfordshire; Ms Boodhoo, Chertsey; Mr Bowell, Dublin; Mr Bradbury, Bradford; Mr Brazier, London; Prof Bron, Oxford; Mr Brosnahan, Sheffield; Mr Brown, Shropshire; Mr Brown, Stoke-on-Trent; Mr Bryan, London; Mr Bryars, Belfast; Prof Buckley, London; Ms Burgess, Swindon; Mr Burke, Sheffield; Ms Butler, Birmingham; Mr Calver, London; Mr Casswell, Brighton; Mr Chandna, Liverpool; Mr Church, Aberdeen; Mr Clarke, Middlesborough; Mr Clarke, Newcastle-upon-Tyne; Dr Coffey, Republic of Ireland; Mr Cole, Devon; Mr Condon, Chertsey; Mr Corridan Wolverhampton; Mr Dang, Darlington; Mr Darvell, Kent; Mr Das, Worcestershire; Mr Davies, Norwich; Mr Daya, West Sussex; Mr De Cock, Margate; Mr Dees, Darlington; Mr Dodd, Manchester; Mr Doran, Leeds; Prof Dutton, Glasgow; Mrs. Duvall-Young, High Wycombe; Mr Edelston, Ipswich; Mr Edwards, Kent; Mr El-Kasaby, Essex; Mr Elston, Oxford; Ms Enoch, Barnstable; Mr Evans, Plymouth; Mr Evans, Portsmouth; Mr Fahy, Republic of Ireland; Prof Fielder, London; Mr Fisher, Bedford; Ms Flaye, Bishop’s Stortford; Dr Fleck, Edinburgh; Ms Frank, Poole; Dr Gaskell, Ayr; Dr George, Dundee; Ms Gibbens, Kent; Mr Greaves, Kent; Mr Gregory, East Sussex; Mr Gregson, Nottingham; Mr Hardman, Ip-
swich; Mr Haworth, Nottingham; Mr Heravi, Kent; Mr Hodgkins, Southampton; Mr Holden, Derby; Mr Humphry, Salisbury; Mr Hutchinson, Halifax; Mr Innes, Hull; Mr Jalili, Peterborough; Mr Jenkins, Maidstone; Dr Johnson, Gloucester; Mr Kaushik, Wrexham; Mrs. Kayali, London; Mr Keightley, Basingstoke; Prof Khaw, London; Mr Kinnear, London; Mr Kotta, Grimsby; Mr Kumar Cornwall; Dr Lavy, Glasgow; Mr Laws, Swansea; Ms Leitch, Surrey; Mr Liu, Brighton; Mr Lloyd, Manchester; Ms MacEwen, Dundee; Mr Macfarlane, Kent; Mr Mackintosh, Cheltenham; Mr Mandal, South Yorkshire; Mr Markham, Bristol; Mr McConnell, Kent; Mr McGinnity, Belfast; Mr McLeod, Brighton; Mr Mishra, Nottinghamshire; Mr Mohamad, Chesterfield; Prof Moore, London; Mr Moriarty, Cheshire; Dr Morrice, Stirling; Mr Morris, Southampton; Mr Munton, Kent; Mr Neugebauer, Cheshire; Mr Newman, Liverpool; Mr Nischal, London; Mr Nolan, Republic of Ireland; Mr O’Connor, Republic of Ireland; Mr O’Keefe, Republic of Ireland; Ms Ohri, London; Mr Perry, Kidderminster; Mr Phillips, Wirral; Mrs. Pieris, Bedford; Dr Power. Dumfries; Mr Price, Cheltenham; Mr Quinn, Devon; Mr Qureshi, Rochdale; Mr Rahman, Boston; Mr Rennie, Aberdeen; Mr Ridgway, Manchester; Mr Roper-Hall, Birmingham; Mr Rosen, Manchester; Ms Russell-Eggitt, London; Mr Shun Shin, Wolverhampton; Mr Simcock, Exeter; Mr Simmons, Leeds; Mr Tappin, Surrey; Mr Taylor, York; Prof Taylor, London; Dr Thaller, Plymouth; Mr Thoung, Essex; Mr Tormey, Republic of Ireland; Mr Tuft, London; Mr Tutton, Chester; Mr Twomey, Somerset; Mr Verghese, West Cumberland; Ms Vickers, Brighton; Mr Vijaykumar, Blackburn; Mr Vivian, Bury St. Edmunds; Ms Williams, Bristol; Mr Willshaw, Birmingham; Mr Woodruff, Leicester; Mr Wright, Burnley; Mr Young, Republic of Ireland; Mr Zaidi, South Yorkshire.
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Ophthalmology Volume 115, Number 6, June 2008 Table 2. Statistical Correlations between Factors of Interest in Relation to Postoperative Open-angle Glaucoma
Age at detection Age at surgery Type of cataract surgery Primary intraocular lens Postoperative uveitis
*Spearman correlation coefficient. † Kruskal–Wallis score. ‡ Mann–Whitney U score. § Chi-square test.
1018.e2
Age at Surgery
Type of Cataract Surgery
Primary Intraocular Lens
Postoperative Uveitis
0.78* P⬍0.01
37.25† P⬍0.01 69.92† P⬍0.01
⫺2.27‡ P ⫽ 0.02 ⫺10.92‡ P⬍0.01 74.78§ P⬍0.01
⫺2.18‡ P ⫽ 0.03 ⫺2.94‡ P⬍0.01 0.80§ P ⫽ 0.67 7.69§ P ⫽ 0.06
Microphthalmia ⫺2.53‡ P ⫽ 0.01 ⫺2.83‡ P ⫽ 0.01 2.84§ P ⫽ 0.24 4.00§ P ⫽ 0.05 1.23§ P ⫽ 0.27
Postoperative open-angle glaucoma is emerging as potentially the most important visually disabling consequence of surgery for congenital or infantile cataract.1 It has been reported to occur in between 6% and 58.7% of children after cataract extraction, depending on the population studied and
the length of follow-up.2–11 It is insidious, can be difficult to detect, and may occur many years after surgery.2,5,6,12,13 Thus, it is now advised that all children should be considered at risk for the remainder of their lives.14 Treatment of pediatric aphakic glaucoma is challenging.
Originally received: March 6, 2007. Final revision: September 5, 2007. Accepted: September 5, 2007. Available online: December 27, 2007. Manuscript no. 2007-311. 1 Centre for Paediatric Epidemiology, Institute of Child Health, London, United Kingdom. 2 Division of Epidemiology, Institute of Ophthalmology, London, United Kingdom. Supported by the Guide Dogs for the Blind Association, Reading, United Kingdom (grant no. Fre07801 OR2001–26b). Research at the Institute of
Child Health and Great Ormond Street Hospital for Children National Health Service Trust benefits from research and development funding received from the National Health Service Executive, London, United Kingdom. There are no conflicts of interest. Correspondence to Jugnoo Sangeeta Rahi, PhD, Centre for Paediatric Epidemiology, Institute of Child Health, 30 Guilford Street, London WC1N 1EH, United Kingdom. *See “Appendix” for a full list of members of the British Congenital Cataract Interest Group (available at http://aaojournal.org).
© 2008 by the American Academy of Ophthalmology Published by Elsevier Inc.
ISSN 0161-6420/08/$–see front matter doi:10.1016/j.ophtha.2007.09.002
1013
Ophthalmology Volume 115, Number 6, June 2008 Treatment with antiglaucoma topical medication usually is a temporizing measure, with the definitive approaches being surgery, laser treatment, or both.15 However, the outcomes of surgical intervention often are disappointing in the long term.15–17 There is a need to identify factors associated with increased risk of postoperative open-angle glaucoma to decide on treatment and prevention strategies. From reports of selected individual case series, the following factors have been postulated to influence the risk of developing glaucoma: age at detection of cataract, age at cataract surgery, cataract surgery procedure, primary intraocular lens implantation, significant postoperative uveitis, and microphthalmia.4 – 6,8,18 –23 However, there has been limited populationbased research, which has particular strengths in relation to avoidance of bias and confounding. The authors report the incidence and factors associated with postoperative openangle glaucoma in a nationally representative group of children who underwent surgery for congenital or infantile cataract in the United Kingdom.
Patients and Methods All children newly diagnosed with congenital or infantile cataract in the United Kingdom during a 12-month period in 1995 and 1996 (previously identified for the British Congenital/Infantile Cataract study24 –28) and who underwent surgery were eligible for the present study. The authors previously reported24 –28 the methodologic details. To summarize, ophthalmologists and pediatricians actively reported, through 2 independent national surveillance schemes, all children younger than 16 years with newly diagnosed visually significant congenital or infantile cataract, regardless of treatment undertaken. Cases diagnosed after the age of 1 year were eligible only if, on review, they were the result of a congenital cause or had specific ophthalmic features indicative of early onset, such as cataract morphologic features or associated congenital
Figure 1. Flow chart showing study subjects with descriptive statistics.
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ocular anomaly. Children in whom cataract was acquired, for example as result of trauma, uveitis, irradiation, or drugs, were not eligible. All children in the original cohort were traced through their managing ophthalmologist, and those who had undergone cataract surgery were eligible for inclusion in the present study. Detailed clinical information about management and outcomes was collected using specifically designed questionnaires at least 6 years after diagnosis (between September 2002 and April 2003 inclusive). For data validation, patients managed at ophthalmic units contributing more than 4 children were examined independently by the principal investigator. Children were considered to have postoperative open-angle glaucoma for the purposes of this study if they underwent sustained treatment for glaucoma with drops, laser, surgery, or a combination thereof having been diagnosed by the managing consultant as having postoperative open-angle glaucoma. Other forms of glaucoma such as closed-angle glaucoma were excluded from the present analysis.
Statistical Analysis Based on the extant literature summarized earlier,4 – 6,8,18 –23 the factors considered, a priori, to be of interest in relation to the development of postoperative open-angle glaucoma were age at detection of cataract, age at cataract surgery, cataract surgery procedure, primary intraocular lens implantation, significant postoperative uveitis, and microphthalmia. First, the statistical relationships between these potential predictors were investigated. By convention, the authors then undertook univariate analysis and, subsequently, multivariate Cox regression analyses (using factors significant at Pⱕ0.05 level in univariate analysis) to examine the joint effects of these factors on time to development of glaucoma (hazard rate). For children with bilateral cataract who underwent surgery to both eyes, the correlation of the development of glaucoma in the same individual was accounted for by the use of 2-level hierarchical models: level 1 is the eye and level 2 is the child (http://www.cmm.bristol.ac.uk/ learning-training/index.shtml). Analysis was undertaken using STATA
Chak et al 䡠 Factors Associated with Glaucoma after Congenital Cataract Surgery
Figure 2. Graph showing the occurrence of postoperative glaucoma over time since surgery (Nelson-Aalen hazard curve).
software (Stata Corp., College Station, TX). Results are presented with 95% confidence intervals (CIs). The study followed the tenets of the Declaration of Helsinki, institutional review board/ethics committee approval was obtained, and the study adhered to extant research governance requirements.
Results One hundred sixty-five children (275 eyes) underwent surgery for congenital cataract, as summarized in Figure 1, at a median age of 4.5 months (range, 5 days–12.29 years) for bilateral cases and 2.8 months (range, 15 days–5.74 years) for unilateral cases. Follow-up data were available for all children despite 24 children being lost to follow-up and 3 deceased children. Denominators for different data items vary (according to completeness of data) and are reported separately in the figures and tables, as appropriate. One hundred twenty children (47%; 56 girls) had bilateral cataract and median age at the follow-up data collection for the present study of 6.79 years, whereas 45 (56%, 25 girls) with unilateral disease had a median age of 6.73 years at follow-up. Postoperative open-angle glaucoma developed in 10% (n ⫽ 24) of eyes of children with bilateral cataract and 7% (n ⫽ 3) of eyes of children with unilateral disease. The median time to development of postoperative glaucoma was 1.34 years (range, 0.39 months to 6.73 years). Postoperative closed-angle glaucoma occurred in 0.004% (n ⫽ 1) of eyes of children with bilateral cataracts and 7% (n ⫽ 3) of eyes of children with unilateral disease. The overall annual incidence rate of postoperative glaucoma was 5.25 cases per 100 eyes undergoing cataract extraction. The proportion of eyes developing glaucoma as a function of time to
occurrence is shown in Figure 2; the graph is truncated at postoperative follow-up of 6.95 years. Table 1 shows the type of cataract surgery performed, with most children undergoing aspiration and vitrectomy. In 4% (4/90) of children undergoing primary intraocular lens implantation, glaucoma developed, compared with 12% (23/185) of aphakic children (95% CI for difference in 2 proportions, 2%–14%; P ⫽ 0.01). Glaucoma developed in 22% (7/32) of children with microphthalmia versus 8% (20/236) without microphthalmia (95% CI for difference between two proportions, –1% to 28%; P ⫽ 0.08). There were strong statistical correlations between the key factors of interest in relation to the rate of development of aphakic glaucoma as shown in Table 2 (available at http://aaojournal.org); in particular, age at detection was highly correlated with age at surgery. Table 3 shows the results of the univariate analyses of the associations between individual factors of interest and the rate of development of postoperative open-angle glaucoma. These are depicted as the hazard ratio for developing postoperative glaucoma in the presence of the factor of interest (categoric predictors) or with a unit change in the factor (numeric predictors). Importantly, these analyses took into account the within-person correlation between eyes. The effect of this was a strengthening of the univariate associations between glaucoma and age at detection and age at surgery but a weakening of the univariate associations between primary intraocular implantation and microphthalmia. When the multivariate model was constructed, to examine the effects of each factor while accounting for the others, age at detection remained the only statistically significant (Pⱕ0.05) independently associated factor, with a hazard ratio of 0.36 (95% CI, 0.22– 0.59; P⬍0.0001). Thus, a 10-fold increase in the age at detection (for example, 10 days compared with 1 day or 30 days compared with 3 days) was associated with a 64% decrease in the hazard ratio (95% CI, 41%–79%; P⬍0.0001). The statistical correlation between age at detection and age at surgery may account for the fact that the latter was not statistically significant in the multivariate model (hazard ratio, 0.70; 95% CI, 0.21–2.30; P ⫽ 0.56). Figures 3 and 4 (both truncated at postoperative follow-up of 6.95 years) illustrate the variation in rate of development of postoperative glaucoma with variation in age at detection of cataract and age at surgery, respectively.
Discussion The overall annual incidence of aphakic glaucoma was 5.25 per 100 cataract operations during the first 7 postoperative years. Although in half of all cases glaucoma had occurred by 16 months (1.34 years) after cataract surgery, with the earliest onset being at 12 days after surgery (0.39 months), it is notable that the latest case occurred during the seventh postoperative year (6.73 years). Younger age at cataract detection was the only factor independently associated with its development when other relevant factors (with which it was strongly correlated statistically) as well as within-child
Table 1. Distribution of Postoperative Open-Angle Glaucoma by Type of Cataract Surgery Procedure (Median and Range of Duration of Follow-up)
Percentage with postoperative open-angle glaucoma
Lens Aspiration and Vitrectomy (5.86 yrs; 1.44–7.34)
Lens Aspiration Alone (5.94 yrs; 0.85–7.35)
Lensectomy-Vitrectomy (6.19 yrs; 0.87–7.29)
14% (18/107)
6% (5/81)
7% (4/51)
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Ophthalmology Volume 115, Number 6, June 2008 Table 3. Findings of Univariate Analysis (Cox Regression) of Association between Glaucoma and Variables of Interest Variable Log (increasing age at detection in days) Log (increasing age at cataract surgery age in days) Type of cataract surgery (lens aspiration alone†; baseline) Type of cataract surgery (lens aspiration and vitrectomy)† Type of cataract surgery (lensectomy-vitrectomy)† Primary intraocular lens implantation Significant postoperative uveitis Microphthalmia
Hazard Ratio (95% Confidence Interval*)
P Value*
0.36 (0.20–0.59) 0.31 (0.15–0.63)
⬍0.0001 ⬍0.0001
0.45 (0.14–1.48) 1.60 (0.50–4.63) 0.36 (0.10–1.31) 1.17 (0.14–8.75) 2.47 (0.87–7.45)
0.19 0.48 0.12 0.92 0.11
*Adjusted for clustering within child. Lensectomy-vitrectomy versus lens aspiration alone (hazard ratio, 0.71; 95% confidence interval, 0.14 –2.71; P ⫽ 0.61).
†
clustering were accounted for. A 10-fold increase in the age at detection was associated with a 64% decrease in the hazard ratio (95% CI, 41%–79%; P⬍0.0001). The authors’ use of a case definition for glaucoma based on a clinical decision to treat was deliberately conservative and may have resulted in some cases being excluded that might have been included in other studies. Differing definitions7,29 have been used previously, reflecting the difficulties of using objective criteria such as assessment of disc changes or perimetry, which are challenging in young children. Direct comparisons of these findings with those previously reported are difficult because of differences in methodology and statistical analyses, but they are broadly consistent in terms of the proportion of children in whom postoperative glaucoma developed in the short to medium term.2– 6,10 Importantly, median time to development of postoperative open-angle glaucoma in the present study was lower than reported previously.2,3,5–7,19 –22,30 –32 This em-
phasizes the need for vigilance from the early postoperative period. However further work is required to understand the long-term natural history and estimate the lifetime risk of postoperative glaucoma after surgery for congenital cataract. Previous studies have not addressed the age of detection of the cataract specifically, and therefore, it is difficult to make direct comparisons. It is notable that age at detection was significantly statistically correlated with factors identified previously as potential risk factors.4 – 6,8,18 –23 The authors think it most likely that the effect of age at detection on development of glaucoma is mediated mainly through its impact on age at surgery: earlier detection enables earlier surgery. Unlike others,3,4,29 the authors did not find a significant association between type of cataract surgery and glaucoma, even with comparable follow-up for each procedure, a criticism of previous studies.3,15 The authors did not find an association between microphthalmia and glaucoma. However, the statistical correlation
Figure 3. Graph showing the development of postoperative open-angle glaucoma by age at detection (Nelson-Aalen hazard curve).
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Chak et al 䡠 Factors Associated with Glaucoma after Congenital Cataract Surgery
Figure 4. Graph showing the development of postoperative open-angle glaucoma by age at cataract surgery (Nelson-Aalen hazard curve).
of age at detection and microphthalmia may be relevant, because the presence of the latter arguably may lead to earlier detection of cataract and in turn, earlier surgery, where undertaken. Notably, in previous studies suggesting the most significant factor to be age at cataract surgery, the children had a disproportionately high proportion of other ocular abnormalities such as microphthalmia.5 Equally, the authors found no association between postoperative uveitis and glaucoma, but the statistical correlation between younger age at detection and postoperative uveitis may be relevant, although the role of uveitis in the cause of aphakic glaucoma remains uncertain.2– 6,8,21 The authors also found no association between intraocular lens implantation and glaucoma, and again, the statistical correlation with age at detection may be relevant. Finally, however, it is important to note that many prior reports postulating a role for primary intraocular lens implantation, microphthalmia, and uveitis have not explicitly accounted for the correlation between the 2 eyes of the same individual, and this may have resulted in erroneous statistical significance testing. It seems that earlier detection of cataract incorporates all the risk factors that have been noted in previous papers to be independent risk factors. Earlier detection of cataract does not directly cause postoperative glaucoma, but earlier detection enables earlier surgery; this is the rationale for screening. Early surgery is essential to prevent amblyopia; however, previous reports have documented the higher frequency of complications with earlier surgery.10,30,33,34 Clinicians therefore are faced with the dilemma of balancing the timing of surgery to prevent amblyopia while minimiz-
ing postoperative complications. The point of equilibrium is unknown. A prospective study in which children were randomized to surgery at different ages within the critical period may address the question of optimum timing. In the meantime, the findings of this population-based study of postoperative open-angle glaucoma after congenital cataract surgery support the case for careful clinical surveillance for postoperative glaucoma from the earliest postoperative period and that this must continue in the long term.
References 1. Lambert SR, Drack AV. Infantile cataracts. Surv Ophthalmol 1996;40:427–58. 2. Asrani SG, Wilensky JT. Glaucoma after congenital cataract surgery. Ophthalmology 1995;102:863–7. 3. Chrousos GA, Parks MM, O’Neill JF. Incidence of chronic glaucoma, retinal detachment and secondary membrane surgery in pediatric aphakic patients. Ophthalmology 1984;91: 1238 – 41. 4. Keech RV, Tongue AC, Scott WE. Complications after surgery for congenital and infantile cataracts. Am J Ophthalmol 1989;108:136 – 41. 5. Mills M, Robb R. Glaucoma following childhood cataract surgery. J Pediatr Ophthalmol Strabismus 1994;31:355– 60. 6. Magnusson G, Abrahamsson M, Sjostrand J. Glaucoma following congenital cataract surgery: an 18-year longitudinal follow-up. Acta Ophthalmol Scand 2000;78:65–70. 7. Egbert JE, Wright MM, Dahlhauser KF, et al. A prospective study of ocular hypertension and glaucoma after pediatric cataract surgery. Ophthalmology 1995;102:1098 –101.
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Ophthalmology Volume 115, Number 6, June 2008 8. Parks MM, Johnson DA, Reed GW. Long-term visual results and complications in children with aphakia: a function of cataract type. Ophthalmology 1993;100:826 – 40, discussion 840 –1. 9. Johnson CP, Keech RV. Prevalence of glaucoma after surgery for PHPV and infantile cataracts. J Pediatr Ophthalmol Strabismus 1996;33:14 –7. 10. Vishwanath M, Cheong-Leen R, Taylor D, et al. Is early surgery for congenital cataract a risk factor for glaucoma? Br J Ophthalmol 2004;88:905–10. 11. Chen TC, Bhatia LS, Halpern EF, Walton DS. Risk factors for the development of aphakic glaucoma after congenital cataract surgery. J Pediatr Ophthalmol Strabismus 2006;43:274 – 80. 12. Wilson ME, Bluestein E, Wang X-H. Current trends in the use of intraocular lenses in children. J Cataract Refract Surg 1994;20:579 – 83. 13. Wilson ME, Elliot L, Johnson B, et al. AcrySof acrylic intraocular lens implantation in children: clinical indications of biocompatibility. J AAPOS 2001;5:377– 80. 14. Taylor D. Congenital cataract: the history, the nature and the practice. The Doyne Lecture. Eye 1998;12:9 –36. 15. Papadopoulos M, Khaw PT. Meeting the challenge of glaucoma after paediatric cataract surgery. Eye 2003;17:1–2. 16. Mandal AK, Bagga H, Nutheti R, et al. Trabeculectomy with and without mitomycin-C for paediatric glaucoma in aphakia and pseudophakia following congenital cataract surgery. Eye 2003;17:53– 62. 17. Azuara-Blanco A, Wilson RP, Spaeth GL, et al. Filtration procedures supplemented with mitomycin C in the management of childhood glaucoma. Br J Ophthalmol 1999;83: 151– 6. 18. Lundvall A, Zetterstrom C. Complications after early surgery for congenital cataracts. Acta Ophthalmol Scand 1999;77: 677– 80. 19. Wallace DK, Plager DA. Corneal diameter in childhood aphakic glaucoma. J Pediatr Ophthalmol Strabismus 1996;33: 230 – 4. 20. Miyahara S, Amino K, Tanihara H. Glaucoma secondary to pars plana lensectomy for congenital cataract. Graefes Arch Clin Exp Ophthalmol 2002;240:176 –9. 21. Rabiah PK. Frequency and predictors of glaucoma after pediatric cataract surgery. Am J Ophthalmol 2004;137:30 –7.
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22. Brady KM, Atkinson CS, Kilty LA, Hiles DA. Glaucoma after cataract extraction and posterior chamber lens implantation in children. J Cataract Refract Surg 1997;23(suppl):669 –74. 23. Asrani SG, Freedman SF, Hasselblad V, et al. Does primary intraocular lens implantation prevent “aphakic” glaucoma in children? J AAPOS 2000;4:33–9. 24. Rahi JS, Dezateux C, British Congenital Cataract Interest Group. Capture-recapture analysis of ascertainment by active surveillance in the British Congenital Cataract Study. Invest Ophthalmol Vis Sci 1999;40:236 –9. 25. Rahi JS, Dezateux C, British Congenital Cataract Interest Group. National cross sectional study of detection of congenital and infantile cataract in the United Kingdom: role of childhood screening and surveillance. BMJ 1999;318:362–5. 26. Rahi JS, Dezateux C, British Congenital Cataract Interest Group. Congenital and infantile cataract in the United Kingdom: underlying or associated factors. Invest Ophthalmol Vis Sci 2000;41:2108 –14. 27. Rahi JS, Botting BJ, British Congenital Cataract Interest Group. Ascertainment of children with congenital cataract through the National Congenital Anomaly System in England and Wales. Br J Ophthalmol 2001;85:1049 –51. 28. Rahi JS, Dezateux C, British Congenital Cataract Interest Group. Measuring and interpreting the incidence of congenital ocular anomalies: lessons from a national study of congenital cataract in the UK. Invest Ophthalmol Vis Sci 2001;42: 1444 – 8. 29. Simon JW, Mehta N, Simmons ST, et al. Glaucoma after pediatric lensectomy/vitrectomy. Ophthalmology 1991;98: 670 – 4. 30. Lundvall A, Kugelberg U. Outcome after treatment of congenital bilateral cataract. Acta Ophthalmol Scand 2002;80: 593–7. 31. Russell-Eggitt IM, Zamiri P. Review of aphakic glaucoma after surgery for congenital cataract. J Cataract Refract Surg 1997;23(suppl):664 – 8. 32. Walton DS. Pediatric aphakic glaucoma: a study of 65 patients. Trans Am Ophthalmol Soc 1995;93:403–13. 33. Hing S, Speedwell L, Taylor D. Lens surgery in infancy and childhood. Br J Ophthalmol 1990;74:73–7. 34. Magnusson G, Abrahamsson M, Sjostrand J. Changes in visual acuity from 4 to 12 years of age in children operated for bilateral congenital cataracts. Br J Ophthalmol 2002;86: 1385–9.
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Appendix: Members of the British Congenital Cataract Interest Group Mr Abdel-Khalek, Boston; Mr Aclimandos, London; Ms Adams, London; Mr Aftab, Scunthorpe; Ms Allen, Cambridge; Mr Amanat, Great Yarmouth; Mr Armstrong, Chester; Mr Assaf, Milton Keynes; Mr Astbury, Norwich; Mr Bannerjee, Wigan; Dr Barr, Dumferline; Ms Beck, Cardiff; Mr Beckingsale, Colchester; Mr Bedford, Dumfries; Mr Benjamin, Aylesbury; Ms Billington, Reading; Ms Blamires, Leicester; Mr Bloom, London; Mr Boase, Portsmouth; Mr Bolger, Hertfordshire; Ms Boodhoo, Chertsey; Mr Bowell, Dublin; Mr Bradbury, Bradford; Mr Brazier, London; Prof Bron, Oxford; Mr Brosnahan, Sheffield; Mr Brown, Shropshire; Mr Brown, Stoke-on-Trent; Mr Bryan, London; Mr Bryars, Belfast; Prof Buckley, London; Ms Burgess, Swindon; Mr Burke, Sheffield; Ms Butler, Birmingham; Mr Calver, London; Mr Casswell, Brighton; Mr Chandna, Liverpool; Mr Church, Aberdeen; Mr Clarke, Middlesborough; Mr Clarke, Newcastle-upon-Tyne; Dr Coffey, Republic of Ireland; Mr Cole, Devon; Mr Condon, Chertsey; Mr Corridan Wolverhampton; Mr Dang, Darlington; Mr Darvell, Kent; Mr Das, Worcestershire; Mr Davies, Norwich; Mr Daya, West Sussex; Mr De Cock, Margate; Mr Dees, Darlington; Mr Dodd, Manchester; Mr Doran, Leeds; Prof Dutton, Glasgow; Mrs. Duvall-Young, High Wycombe; Mr Edelston, Ipswich; Mr Edwards, Kent; Mr El-Kasaby, Essex; Mr Elston, Oxford; Ms Enoch, Barnstable; Mr Evans, Plymouth; Mr Evans, Portsmouth; Mr Fahy, Republic of Ireland; Prof Fielder, London; Mr Fisher, Bedford; Ms Flaye, Bishop’s Stortford; Dr Fleck, Edinburgh; Ms Frank, Poole; Dr Gaskell, Ayr; Dr George, Dundee; Ms Gibbens, Kent; Mr Greaves, Kent; Mr Gregory, East Sussex; Mr Gregson, Nottingham; Mr Hardman, Ip-
swich; Mr Haworth, Nottingham; Mr Heravi, Kent; Mr Hodgkins, Southampton; Mr Holden, Derby; Mr Humphry, Salisbury; Mr Hutchinson, Halifax; Mr Innes, Hull; Mr Jalili, Peterborough; Mr Jenkins, Maidstone; Dr Johnson, Gloucester; Mr Kaushik, Wrexham; Mrs. Kayali, London; Mr Keightley, Basingstoke; Prof Khaw, London; Mr Kinnear, London; Mr Kotta, Grimsby; Mr Kumar Cornwall; Dr Lavy, Glasgow; Mr Laws, Swansea; Ms Leitch, Surrey; Mr Liu, Brighton; Mr Lloyd, Manchester; Ms MacEwen, Dundee; Mr Macfarlane, Kent; Mr Mackintosh, Cheltenham; Mr Mandal, South Yorkshire; Mr Markham, Bristol; Mr McConnell, Kent; Mr McGinnity, Belfast; Mr McLeod, Brighton; Mr Mishra, Nottinghamshire; Mr Mohamad, Chesterfield; Prof Moore, London; Mr Moriarty, Cheshire; Dr Morrice, Stirling; Mr Morris, Southampton; Mr Munton, Kent; Mr Neugebauer, Cheshire; Mr Newman, Liverpool; Mr Nischal, London; Mr Nolan, Republic of Ireland; Mr O’Connor, Republic of Ireland; Mr O’Keefe, Republic of Ireland; Ms Ohri, London; Mr Perry, Kidderminster; Mr Phillips, Wirral; Mrs. Pieris, Bedford; Dr Power. Dumfries; Mr Price, Cheltenham; Mr Quinn, Devon; Mr Qureshi, Rochdale; Mr Rahman, Boston; Mr Rennie, Aberdeen; Mr Ridgway, Manchester; Mr Roper-Hall, Birmingham; Mr Rosen, Manchester; Ms Russell-Eggitt, London; Mr Shun Shin, Wolverhampton; Mr Simcock, Exeter; Mr Simmons, Leeds; Mr Tappin, Surrey; Mr Taylor, York; Prof Taylor, London; Dr Thaller, Plymouth; Mr Thoung, Essex; Mr Tormey, Republic of Ireland; Mr Tuft, London; Mr Tutton, Chester; Mr Twomey, Somerset; Mr Verghese, West Cumberland; Ms Vickers, Brighton; Mr Vijaykumar, Blackburn; Mr Vivian, Bury St. Edmunds; Ms Williams, Bristol; Mr Willshaw, Birmingham; Mr Woodruff, Leicester; Mr Wright, Burnley; Mr Young, Republic of Ireland; Mr Zaidi, South Yorkshire.
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Ophthalmology Volume 115, Number 6, June 2008 Table 2. Statistical Correlations between Factors of Interest in Relation to Postoperative Open-angle Glaucoma
Age at detection Age at surgery Type of cataract surgery Primary intraocular lens Postoperative uveitis
*Spearman correlation coefficient. † Kruskal–Wallis score. ‡ Mann–Whitney U score. § Chi-square test.
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Age at Surgery
Type of Cataract Surgery
Primary Intraocular Lens
Postoperative Uveitis
0.78* P⬍0.01
37.25† P⬍0.01 69.92† P⬍0.01
⫺2.27‡ P ⫽ 0.02 ⫺10.92‡ P⬍0.01 74.78§ P⬍0.01
⫺2.18‡ P ⫽ 0.03 ⫺2.94‡ P⬍0.01 0.80§ P ⫽ 0.67 7.69§ P ⫽ 0.06
Microphthalmia ⫺2.53‡ P ⫽ 0.01 ⫺2.83‡ P ⫽ 0.01 2.84§ P ⫽ 0.24 4.00§ P ⫽ 0.05 1.23§ P ⫽ 0.27