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Journal of Perinatology (2008) 28, 566–572 r 2008 Nature Publishing Group All rights reserved. 0743-8346/08 $30 www.nature.com/jp ORIGINAL ARTICLE Severe of prematurity and visual outcomes in British Columbia: a 10-year analysis

V Schiariti1, C Matsuba1, JS Hoube´1,2 and AR Synnes1,2 1Department of Pediatrics, Sunny Hill Health Centre, British Columbia Children’s Hospital, University of British Columbia, Vancouver, BC, Canada and 2Department of Pediatrics, Centre for Health Innovation and Improvement, University of British Columbia, Vancouver, BC, Canada

Introduction Objective: To describe the incidence trend and long-term visual outcomes Over the past decade, there has been an increase in the survival of of infants diagnosed with stages 3 to 4 retinopathy of prematurity (ROP) or very low birth weight (BW) infants (BW <1250 g).1–5 This has laser-treated ROP born in British Columbia (Canada). raised concerns of an absolute increase in children with Study Design: Data from all (n ¼ 1384) neonates with birth weight neurosensory disabilities as severe neurosensory disorders occur in (BW) <1250 g, admitted to British Columbia Children’s Hospital between 10 to 25% of the survivors.6–10 Preterm infants are at risk for period 1 (January 1992 to December 1996) and period 2 (January 1997 to retinopathy of prematurity (ROP), a condition confined to the December 2001) were analyzed. Ophthalmologic records of infants with developing retinal vascular system of preterm babies. This stages 3 to 4 ROP or laser-treated ROP were abstracted. w2- and t-test were condition, if untreated, may result in . In used to compare neonatal characteristics between periods. Logistic developed countries, ROP accounts for 6 to 20% of childhood regression was used to identify risk factors associated with visual blindness.11,12 However, in developing countries, ROP is emerging impairment (defined as p20/60 or visual field restriction of as a major cause of . 201 binocularly). Retinopathy of prematurity (ROP) is described by severity Result: Of 1159 surviving infants, 887 were examined for acute ROP (stages 1 to 5), location (zones I to III), extent by sector (clock 13 (473 in period 1, 414 in period 2). Stages 3 to 4 ROP or laser-treated ROP hours) and by the presence of ‘plus’ disease. Severity stages 1 and were present in 35 infants in period 1 (7%) and 59 in period 2 (14%), 2 are considered mild because, unless they progress to stage 3, they P 0001. Infants born in period 2 had lower mean BW and gestational resolve spontaneously without disabling sequelae. Stages 3 to 5 are p 14,15 age. Among infants who developed severe ROP or laser-treated ROP, considered severe. In stage 3, children with ROP are at binocular was present in eight children in period significant risk of poor visual outcome. By stages 4 and 5 1 and seven in period 2. Refractive errors, including and (conditions of retinal detachment), children have a dismal , were increased in period 2. Children who developed prognosis for vision. A child with threshold ROP has a risk of 16 periventricular leucomalacia had the highest risk of visual impairment at blindness of about 50% if untreated. Thus, treatment by laser is 4 to 6 years of age. recommended. Recently, treatments at an even earlier stages have been considered, to reduce the number of adverse outcomes.17 To Conclusion: During the 10-year study period, a significant increase in date, ROP is still the most important ocular abnormality of the rates of stages 3 to 4 or laser-treated ROP was not associated with premature infant, with as many as 12.5% of infants born between increases in visual impairment rates. 23 and 26 weeks gestation requiring treatment for threshold Journal of Perinatology (2008) 28, 566–572; doi:10.1038/jp.2008.34; ROP.18,19 However, the incidence of severe ROP may be decreasing, published online 27 March 2008 possibly because of screening programs and early treatment with Keywords: retinopathy of prematurity; visual outcomes; visual laser therapy, or because of improvements in oxygen and ventilator impairment; prematurity; follow-up studies; neonatology management of respiratory diseases in the preterm.20 Population- based studies suggest that ophthalmic impairments remain 21–25 Correspondence: Dr V Schiariti, Department of Pediatrics, Sunny Hill Health Centre, British common in very low BW infants. In a prospective cohort 16 Columbia Children’s Hospital, University of British Columbia, Room S112C, 3644 Slocan study, O’Connor et al. showed that visual impairments Street, Vancouver, BC, Canada V5M 3E8. are associated with low BW and severe ROP. This study E-mail: [email protected] Received 29 October 2007; revised 11 February 2008; accepted 14 February 2008; published demonstrates that alone has an impact on the online 27 March 2008 immature from the to the cortex. However, Retinopathy of prematurity and visual outcomes V Schiariti et al 567 severe ROP is associated with the highest rate of visual were involved in the ROP diagnosis and follow-up assessments in impairments. our center; one of them worked throughout the study period and Long-term visual outcomes of premature infants born in British the other one started working in 1994. Columbia (BC) and admitted to British Columbia Children’s Hospital (BCCH) neonatal intensive care unit (NICU) have not Long-term visual outcomes been fully studied. BCCH is a tertiary-care hospital that services Newborns with severe ROP (stages 3 to 4 or laser-treated ROP) children throughout the province. Unlike other communities, diagnosed and/or treated at BCCH were linked with their long-term BCCH has unique characteristics to allow investigation into the visual outcomes using the seven-digit personal identification visual outcome of children with ROP. First, the majority of numbers. Searches were made directly at the departments of children with ‘threshold’ ROP are screened and treated in BCCH’s and the VIP. nursery. Further, two subspecialty programs, the Visual Impairment At 4 to 6 years of age, children with severe ROP had the Program (VIP) and Ophthalmology Clinic provide the intervention following tests of visual functions measured: VA charts for distal and follow-up for all children with ROP in the province. and near vision (Snellen) and for younger children matching The purposes of this retrospective study were to describe charts (HOTV) or force-choice acuity cards (Teller Acuity Cards), incidence trend and visual outcomes of infants, born in the years perimetry (Damato campimeter) to measure the visual field and 1992 to 2001, diagnosed with severe ROP or laser-treated ROP and for younger children (kinetic perimetry was used). Tests of to study the relationship between perinatal characteristics and later (cover test and prism tests) and refractive state by visual outcomes. cycloplegic were also conducted. Spherical equivalents were calculated in patients with astigmatic refractive errors. Anterior and posterior segments of the eye were assessed by slit Methods lamp. Stereopsis was tested with the Titmus test. This descriptive study is a retrospective review of a sample of very Patients were considered visually impaired if they met at least low BW infants. The study population consists of all babies one of the following criteria: VA of 20/60 or worse for children older admitted to BCCH with BW <1250 g from 1 January 1992 to 31 than four and half years, or VA below the fifth percentile for age for December 2001. The 10-year period was divided in period 1 children based on a force-choice preferential acuity or a visual field (1 January 1992 to 31 December 1996) and period 2 (1 January restriction of 201 or narrower binocularly. Blindness was defined as 1997 to 31 December 2001). The time period was selected, as laser VA of <20/400 in the better eye, which is in accord with the 26 treatment first became available at BCCH in 1992. The 2001 end definition by the World Health Organization. Strabismus was point was selected in order to gather information on defined as the presence of a manifest deviation in the primary ophthalmologic assessments at 4 to 6 years of age for all patients. position at any distance, with or without . BCCH was the sole site of the research project. Ethical approval was obtained from the Universities of BC The primary outcome of interest was visual impairment. Other and BCCH. visual function and ophthalmologic outcomes including best binocular visual acuity (VA), strabismus, myopia, astigmatism and Analysis were also analyzed. Additionally, comparison of severe All data were investigated for normality to determine whether ROP rates between the two time periods, together with the perinatal parametric or nonparametric methods should be used. The trends characteristics, were made. in incidence of stages 3 to 4 or laser-treated ROP and perinatal characteristics were assessed by comparing the first 5-year period Neonatal ophthalmologic assessment with the latter 5-year period. The w2, Mann–Whitney and t-test During NICU admission, infants with BW <1250 g were examined were used to assess differences between periods. Incidence of ROP by an ophthalmologist skilled in indirect ophthalmoscopy at 6 was defined as the rate of new ROP cases present in infants who weeks of age, and had further review if ROP was detected or the eye had an ophthalmology exam. When different stages of ROP were not fully vascularized. The criteria for laser treatment were ROP found in both , the maximum stage of ROP in either eye was stage 2 in zone I, and ROP stage 3 in at least four contiguous clock used. Descriptive statistics on visual outcomes were assessed for hours in zone II, even in the absence of plus disease. Infants who children with stages 3 to 4 or laser-treated ROP. Monocular and did not have an ophthalmologic exam at our center were Binocular VAs are presented. Differences were considered to be transferred to other centers, had ophthalmologic examined in those statistically significant at P- p0.05. Further perinatal risk centers, or died before reaching 6 weeks of age and were not factors in the stages 3 to 4 or laser-treated ROP group were considered in the ROP incidence calculation. There were no examined to determine their relationship to visual impairment. changes in ophthalmology practices regarding ROP diagnosis and Multiple logistic regressions were performed to identify independent intervention throughout the 10-year period. Two ophthalmologists factors (as shown in Table 1, including astigmatism and myopia)

Journal of Perinatology Retinopathy of prematurity and visual outcomes V Schiariti et al 568

Table 1 Comparison of perinatal characteristics between periods

Characteristics Period 1 (N ¼ 764) Period 2 (N ¼ 620)

ROP (À)a Stages 3–4 and/or ROP (À) Stages 3–4 and/or lasered ROP+ lasered ROP+

N 729 35 561 59 BW in grams, mean (s.d.) 949.5 (192) 757.6 (136.4) 902.4 (210)b 723.6 (154.9) GA in weeks, mean (s.d.) 27.5 (2.6) 25.7 (2.3) 26.9 (2.3)b 24.9 (1.6) Inborn, n (%) 605 (83) 23 (65) 464 (81) 42 (71)

Days on O2, median (IQR) 24 (2–56) 83.5 (43.7–116.2) 17 (2–51) 72.5 (31.5–117) CPAP days, median (IQR) 0 (0–2) 0 (0–1.5) 2 (0–10)b 5 (0–15)c Mechanical ventilation days, median (IQR) 15 (3–15) 45 (33–54) 10 (2–27)b 47 (28–69) IVH grades 3–4, n (%) 81 (11.0) 2 (5.7) 99 (17.6)b 13 (22)c Periventricular Leucomalacia, n (%) 80 (10.9) 4 (11.4) 54 (9.6) 6 (10) Antenatal steroids, n (%) 502 (68.8) 23 (65) 450 (80) 45 (76) Blood transfusionsd, n (%) 342 (47) 22 (62.8) 385 (68.6)b 49 (80)c

Abbreviations: BW, birth weight; CPAP, continuous positive airway pressure; GA, gestational age; IQR, interquartile range; ROP, retinopathy of prematurity. aIncludes infants who developed stages 1–2 ROP. bComparison between infants without stages 3–4 ROP or lasered ROP, P-value p0.05. cComparison between infants with stages 3–4 ROP or lasered ROP, P-value p0.05. dOne or more transfusions. associated with visual impairment. Variables independently In both periods, perinatal characteristics of infants transferred associated with visual impairment were analyzed further by before eye exam were similar to those infants who did not develop stepwise logistic regression analysis. severe ROP (period 1: BW 941.82±194.57 g, GA 27.39±2.68; All statistical analyses were conducted with SPSS for Window XP, period 2: BW 890.87±212.48 g, GA 26.89±2.37). and SAS (Cary, Inc., USA). As shown in Figure 2, among those children who developed stages 3 to 4 or laser-treated ROP, 29 of 35 patients in period 1 and 49 of 59 patients in period 2 had an ophthalmologic assessment at Results 4 of 6 years of age. Six patients had binocular visual impairment Of 1384 infants with BW <1250 g admitted to BCCH’s level 3 NICU (VA p20/60) in period 1 and five patients met criteria in period 2. from 1992 to 2001, surviving to 6 weeks of age, 887 had an In both periods, children with neurologic complications (IVH or ophthalmologic exam (n ¼ 473 in period 1, n ¼ 414 in period 2). periventricular leucomalacia (PVL)) had a lower VA than those Stages 3 to 4 or laser-treated ROP was present in 35 infants in without, data not shown. period 1 and 59 infants in period 2. Thus, incidence of stages 3 to 4 Nystagmus was present in two children in period 1 and four or laser-treated ROP was increased in period 2 (7% in period 1 vs children in period 2. Field restriction of 201 or binocularly 14% in period 2; P-value, 0.0009) Figure 1. narrower was present in four children in period 1 and four children As shown in Table 1, perinatal characteristics varied in period 2. Two patients in each period also met criteria for visual among the 10-year study period. For infants who did not develop impairment based on VA. severe ROP, we found that in period 2, infants had on average In our study sample, eight children in period 1 (six children lower BW and lower gestational age (GA). The incidence of with VA p20/60 and two children with significant field intraventricular hemorrhage (IVH) was significantly increased in restrictions) and seven children in period 2 (five children with VA period 2 (11% in period 1 vs 17% in period 2). Blood transfusions, p20/60 and two children with significant field restrictions) met median number of days of continuous positive airway pressure criteria for binocular visual impairment. The rates of visual (CPAP) and mechanical ventilation were also increased in impairment remained stable during the study period (1.0% in period 2. period 1, 1.1% in period 2). As we assessed visual outcomes In period 2, infants with stages 3 to 4 or laser-treated ROP of patients who developed severe or laser-treated ROP, we can had on average lower BW and lower GA. They also had a only estimate the rate of visual impairment in the premature statistically significant higher median number of days of nasal population at risk of developing ROP (BW <1250 g). As CPAP, higher number of blood transfusions and also higher rates BCCH is the primary tertiary center for the management and of grades 3 to 4 IVH. follow-up of severe ocular abnormalities. It is unlikely that

Journal of Perinatology Retinopathy of prematurity and visual outcomes V Schiariti et al 569

1384 infants BW< 1,250 grams admitted to NICU

Period 1 N=764 Period 2 N=620 Died before eye exam Died before eye exam N=130 N=95

Eye exam Not examined Not examined N=473 N=161 Eye exam N=111 N=414

Normal exam Abnormal exam Normal exam Abnormal exam N=353 N=120 N=224 N=184

Stage Total Laser Stage Total Laser treatment treatment ROP 1 62 - ROP 1 90 - ROP 2 12 1 ROP 2 30 7 ROP 3 23 19 ROP 3 43 34 ROP 4 11 9 ROP 4 9 8 Others 12 - Others 7 -

Incidence stage 3-4 or Incidence stage 3-4 or laser treated ROP laser treated ROP 35/473 x 100 = 7% 59/414 x 100 = 14%

Figure 1 Distribution of retinopathy of prematurity (ROP), incidence of stages 3 to 4 or laser-treated ROP.

Period 1 Period 2 3-4 ROP or laser 3-4 ROP or laser N=35 N=59

Loss to FU Loss to FU - Child died = 3 - Child died =1 - Refuse FU = 3 - Refuse FU = 2 - Missing data = 2 - Missing data = 3 - Family moved = 2

Period 1 Period 2 Ophthalmologic Ophthalmologic FU at 4-6 yo FU at 4-6 yo N= 29 N= 49

Binocular Distance Visual Acuity Binocular Distance Visual Acuity Mild Moderate Visual Impairment¶ Mild Moderate Visual Impairment¶ 20/40 or <20/40- <20/60- 20/40 or <20/40- <20/60- better ≥20/60 ≥20/400 <20/400 better ≥20/60 ≥20/400 <20/400 n= 27 subjects* 20 2 42 n = 48 subjects* 32 11 50 ∗ two subjects had severe visual impairment in one eye, ∗ one subject had severe visual impairment in one eye, binocular vision not not tested tested ¶ 2 subjects met criteria for visual impairment based on significant field ¶ 2 subjects met criteria for visual impairment based on significant field restrictions restrictions Figure 2 Ophthalmologic follow-up and visual outcomes.

Journal of Perinatology Retinopathy of prematurity and visual outcomes V Schiariti et al 570 the children who were not assessed in follow-up had a visual Changes in incidence of ROP could be explained by differences impairment. in perinatal characteristics of the premature population between A total of 12 of 29 (41%) in period 1 and 30 of 49 (61%) of both periods. Smaller and younger infants were admitted in period children in period 2 had myopic refractive errors (defined as all 2. Higher incidence of grades 3 to 4 IVH and higher proportion of negative man spherical equivalents <0.0 D spheres) in one or both infants requiring blood transfusion were also noted in period 2. A eyes. In period 2, a higher proportion of children developed significant increase in the median number of days of nasal CPAP astigmatism (defined as X1 D) in one or both eyes, 2 of 15 (2%) was found in period 2. On the other hand, the median number of in period 1 vs 15 of 49 (30%) in period 2. In period 1, one patient days of mechanical ventilation and the median number of days of present mild left small . In period 2, five children had treatment with supplemental oxygen decreased in period 2. strabismus. Among infants who developed stages 3 to 4 or laser- Importantly, the policy for oxygen use did not change during the treated ROP, cortical visual impairment was present in one child in study period. It is possible that nasal CPAP use was associated with period 1 and also one child in period 2. more frequent fluctuations in oxygen saturation that may favor the Furthermore, we examined perinatal characteristics and progression of ROP.33,34 refractive errors (astigmatism and myopia) for their association Despite the increase rate of severe ROP, the rate of visual with visual impairment. GA, IVH, PVL, use of steroids during impairment remained stable during the study period. This finding pregnancy, CPAP days, total oxygen days, mechanical ventilation is probable because of improvements in ophthalmic and neonatal days, myopia, astigmatism and transfusions (X1) were care. We do not know to what extent ocular abnormalities would significantly associated with visual impairment. In the logistic have been found in the groups of children who did not have regression model, visual impairment was associated with PVL ophthalmologic examinations. However, in our province, (OR ¼ 28; CI: 2.9 to 282); and myopia (OR ¼ 4.1, CI: 1.2 to 13.7). the risk of having missed patients with serious visual outcomes seems slight. Our findings are in agreement with previous studies.35 Rudanko Discussion et al. in a retrospective cross-sectional study of visual impaired This is the first study reporting incidence trend of severe ROP children in Finland from 1972 to 1989, showed that ROP became a (stages 3 to 4 or laser ROP) as well as long-term visual outcomes less common cause of visual impairment or blindness. The severity in a premature population (BW <1250 g) in BC. The study period of ROP-related visual impairment also decreased. Neuro- consisted of 10 years (1992 to 2001) starting immediately after the ophthalmologic disease became the most common disorder in introduction of laser treatment for ROP in our center. We found relation to children born prematurely and visually impaired. The that the incidence of all ROP stages increased from period 1 (1992 mean annual incidence of preterm children with visual to 1996) to period 2 (1997 to 2001), 22.8% (108 of 473) to 41.5% impairment did not change between the 1970s and 1980s, with the (172 of 414), respectively. In period 2, the incidence of severe ROP exception of a relative increase in prematurely born blind children. also increased (7% in period 1 vs 14% in period 2). Among those The effect of damage to the posterior visual pathway and who developed severe ROP, we found that the proportion of refractive errors on VA has been reported.24,36 In accord with children with binocular visual impairment decreased in period 2, Fledelius, children with neurologic complications and mild to 27% (8 of 29) in period 1 vs 14% (7 of 49) in period 2. Two moderate myopia had poorer VA than those without. In a patients were blind (binocularly) in period 1 and none in period 2. population-based study comparing preterm and full-term children, On the other hand, refractive errors consisting of myopia and Larsson et al. showed that neurologic complications (including astigmatism increased in period 2. In addition, PVL and IVH) and astigmatism were significantly correlated with a reduced myopia were significantly associated with visual impairment at VA at 10 years of age. In our study, children who developed PVL 4 to 6 years of age. had the highest risk of a severe reduced VA (<20/60) at 4 to 6 Previous studies showed that low BW children are at risk of years of age. In addition, in our population, myopia seems to be a developing a range of ophthalmologic morbidity.9,16,21,22,24,27–32 for visual impairment in childhood. O’Connor et al.16 have shown that at 10 to 12 years of age Refractive errors are widely known consequence of low BW, premature infants with no or regressed mild ROP had similar especially after severe ROP.24,36 We have found that the proportion corrected VA than a control group of children born at term. On the of children with refractive errors increased in the last period. Again, other hand, severe ROP stages are well known to reduce vision. In we hypothesized that this could be related to changes in perinatal this study, we were able to assess whether changes in incidence of characteristics between the periods. severe ROP correlate with poorer long-term visual outcomes, This study provides information to further improved specifically binocular visual impairment, at 4 to 6 years of age. In ophthalmology follow-up services provided to infants with severe this hospital-based sample, a significant increase in severe ROP ROP in BC. Furthermore, increase incidence of severe ROP with was not correlated with increases rate of visual impairment. subsequent high prevalence of visual problems (refractive errors)

Journal of Perinatology Retinopathy of prematurity and visual outcomes V Schiariti et al 571 in this premature population precludes increase health services use 11 Gilbert C, Rahi J, Eckstein M, O’Sullivan J, Foster A. Retinopathy of prematurity in and though our results are important for health services middle-income countries. Lancet 1997; 350(9070): 12–14. policymakers and health-care providers. 12 Steinkuller PG, Du L, Gilbert C, Foster A, Collins ML, Coats DK. Childhood blindness. J This study has some limitations. First, visual outcomes of AAPOS 1999; 3(1): 26–32. 13 Haines L, Fielder AR, Baker H, Wilkinson AR. UK population based study of severe premature infants who had no or mild ROP were not available. retinopathy of prematurity: screening, treatment, and outcome. Arch Dis Child Fetal These data could have shown a trend toward better VA in all Neonatal Ed 2005; 90(3): F240–F244. premature infants in period 2 and also an increase in refractive 14 Committee for the Classification of Retinopathy of Prematurity. An international errors and visual motility disorders over time suggesting a change classification of retinopathy of prematurity. Br J Ophthalmol 1984; 68(10): 690–697. in pattern of prematurity in visual development. Second, the study 15 International Committee for the Classification of Retinopathy of Prematurity. The international classification of retinopathy of prematurity revisited. Arch Ophthalmol lacks a comparison group of healthy full-term babies, which could 2005; 123(7): 991–999. show impact of prematurity per se on visual outcomes. 16 O’Connor AR, Stephenson T, Johnson A, Tobin MJ, Moseley MJ, Ratib S et al. Long- In summary, a significant increase in rates of stages 3 to 4 or term ophthalmic outcome of low birth weight children with and without retinopathy of laser-treated ROP has not been associated with increases in visual prematurity. Pediatrics 2002; 109(1): 12–18. impairment rates for those children receiving follow-up care at our 17 Early Treatment For Retinopathy Of Prematurity Cooperative, Group. Revised center. The functional significance of the ophthalmic sequelae in indications for the treatment of retinopathy of prematurity: results of the early treatment for retinopathy of prematurity randomized trial. Arch Ophthalmol 2003; terms of activities of daily living, school attainment and learning in 121(12): 1684–1694. our population warrants further investigations. 18 Todd D, Cassell C, Kennedy J, John E. Retinopathy of prematurity in infants <32 weeks’ gestation at birth in New South Wales in 1993 and 1994. J Paediatr Child Health 1999; 35(4): 355–357. 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