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Eur J Ophthalmol 2010 ; 20 ( 5): 931-937

ORIGINAL ARTICLE

Screening criteria for retinopathy of prematurity in developing countries
İ pek Akman1, Utku Demirel2, Özlem Yenice3, Hacer İ lerisoy3, Haluk Kazokoğ lu3, Eren Özek1
Department of Neonatology, Marmara University Hospital, Istanbul - Turkey Department of Pediatrics, Marmara University Hospital, Istanbul - Turkey 3 Department of Ophthalmology, Marmara University Hospital, Istanbul - Turkey
1 2

PurPose. Retinopathy of prematurity (ROP) is a serious problem which potentially can lead to blindness. The objective of this study is to detect the incidence of ROP and the number of preterm babies requiring treatment for ROP in our center and to establish the screening criteria for our country. Methods. A total of 801 babies with a gestational age less than 37 weeks were screened for ROP. Babies with a gestational age (GA) less than 32 weeks (n=348) were assigned as group 1. Babies with a GA between 32 and 34 weeks (n=335) were assigned as group 2 and between 35 and 37 weeks (n=98) were assigned as group 3. Clinical features and ROP screening results of the cases were documented. results. In group 1, ROP was detected in 176 (50.9%) babies, 41 (11.8%) of whom were treated with laser/cryotherapy. In group 2, 83 (25%) cases of ROP were detected, and 11 of them (3.1%) required therapy. In group 3, 9 (9.1%) infants were diagnosed with ROP, and none of them required treatment. Clinical factors associated with ROP in group 1 were gestational age, birthweight, duration of ventilation, duration of oxygen supplementation, sepsis, and bronchopulmonary dysplasia. ConClusions. In developing countries, the criteria for ROP screening programs should be designed according to local conditions. In our country, screening all premature babies with a gestational age less than 34 weeks or a birthweight less than 1850 g appears to be appropriate. (Eur J Ophthalmol 2010; 20: 931-7) Key Words. Developing country, Retinopathy of prematurity, Screening criteria
Accepted: February 2, 2010

INTRODUCTION
Retinopathy of prematurity (ROP) is a largely preventable proliferative retinal vascular disease which potentially can lead to blindness in premature infants (1-4). Currently, the available data suggest that at least 50,000 children are blind due to ROP worldwide (5). ROP is the leading cause of blindness in middle income countries of Latin America and Eastern Europe (6-8). When it was first recognized in 1950s, retrolental fibroplasia (earlier terminology for ROP) was found to be significantly associated with unmonitored use of supplemental

oxygen (first epidemic) (9). Despite conservative and monitored oxygen therapy, ROP remains frequent in industrialized countries, partly due to improvements in neonatal care leading to increased survival of premature infants (second epidemic) (10). Being influenced by the availability of neonatal care and effective screening and treatment programs, the proportion of blindness due to ROP varies among countries. In some regions of Mexico, 62% of childhood blindness is reported to be due to ROP (10). In Sweden and the United Kingdom, however, ROP accounts for 4% and 3% of 931

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Follow-up examinations were performed on the basis of retinal findings of previous examinations. duration of mechanical ventilation (either continuous positive airway pressure or positive pressure ventilation). patent ductus arteriosus. more mature and of higher birthweight. The pupils were dilated by using 0. ROP screening examinations were performed according to American Association for Pediatric Ophthalmology and Strabismus criteria. should have screening examinations for ROP at least twice (5). Application of the screening criteria used in highly developed countries may be inappropriate in less developed countries. Continuous variables (birthweight.ISSN 1120-6721 . The first examination is recommended to be performed between 4 and 6 weeks of chronologic (postnatal) age or. The Royal College of Ophthalmologists of the United Kingdom recommends ROP screening for all premature babies born at less than 32 weeks of gestation and/or with a birthweight less than 1500 g (16). intraventricular hemorrhage. is at risk of developing this blinding disease (third epidemic) (7). whichever is later. Medical records of ROP screening examinations and clinical features of the babies were assessed. In middle income countries. that is. duration of oxygen supplementation. with respect to the severity of ROP. sepsis. a different type of baby. because of financial concerns. Groups 1 and 2 were each further split into 2 subgroups. gestational age. Eyes were examined with an infant speculum and a Kreissig scleral depressor. alternatively. The objectives of this observational study are to detect the incidence of ROP and the number of preterm babies requiring treatment for retinopathy in our center and to suggest a revision in ROP screening criteria for Turkey. surfactant treatment. Ethical clearance was obtained from the hospital ethics committee. ROP is an increasing problem in the developing economies of India and China (13-15). duration of ventilation. respectively (11. We used the term severe ROP to include infants who had stage 3 disease as well as those with stages 4 and 5.Screening criteria for retinopathy of prematurity childhood blindness. 12). Also. hypoxia. The screening was done with a binocular indirect ophthalmoscope. antenatal and postnatal risk factors known to affect ROP were obtained for each infant. Currently. until full dilatation was achieved. B. utilizing local available data while establishing screening criteria seems more plausible. Similarly. 18). anemia. duration of oxygen supplementation). Informed consent of the parents was also obtained. C. as well as selected infants between 1500 and 2000 g with an unstable clinical course who are believed to be at high risk by their attending pediatrician or neonatologist. Infants who had either culturepositive or clinical sepsis were assigned to have sepsis. Retinopathy findings were documented using the International Classification For Retinopathy of Prematurity classification. hypercapnia. Bronchopulmonary dysplasia (BPD) was defined according to NIH consensus definition (17. gestational age. exchange transfusion. the American Association For Pediatric Ophthalmology and Strabismus recommends that infants with a birthweight of less than 1500 g or with a gestational age of 28 weeks or less. within the 31st to 33rd week of postconceptional or postmenstrual age (gestational age at birth plus chronologic age). Thus. under topical anesthesia using 2% proparacaine drops. acidosis. and multiple gestation. apnea. which have higher birth rates and premature birth rates. MATERIALS AND METHODS A total of 801 babies born in our center or referred to our ophthalmology department for ROP screening examination between January 2000 and December 2009 with a gestational age less than 37 weeks were enrolled in the study. with limited resources and a lack of awareness and skilled personnel. duration of 40% oxygen supplementation.25% phenylephedrine eyedrops 2 or 3 times. hypocapnia. Before screening examinations. if needed. These risk factors were birthweight. The study population was grouped into 3 categories based on their gestational age. © 2010 Wichtig Editore . Group 1 included babies with <32 weeks of gestation. 1 week later or sooner if there was stage 1 or 2 ROP in zone 1. and group 3 included babies with a gestational age more than 34 weeks. group 2 included babies with a gestational age between 32 and 34 weeks. These subgroups— A. 2 to 3 weeks later if vascularization was immature and there was no ROP. The first ROP examination took place at 4–6 weeks of postnatal age.4% tropicamide +1. either from the patient’s file or directly from the attending physician. and D—were used to compare the clinical risk factors of the babies without ROP and with severe ROP. Respiratory distress syndrome (RDS) was defined according to clinical and radiologic findings (19). screening and treatment programs are often not in place. for babies with a gestational age >32 we932 eks. blood product transfusion.

and 3 are given in Table I. Treatment for ROP was not indicated for any of the infants in group 3 (Tab.9±0.1)/42 (42.ISSN 1120-6721 Group 2 (32–34 weeks) (n=355) 272 (76. mean ± SD BPD. Mean birthweights and gestational ages of outborn babies were 1240 g and 29 weeks. RESULTS The demographic features of groups 1. n (%) Treatment.4) 0.15 48 (13.5) 14 (3.7 299 (85. In group 3. n (%)* *Both culture-positive and clinical sepsis were included.3) Group 3 (>34 wk) (n=98) 1924±452 35. Median duration of oxygen supplementation of treated and untreated infants was 6 days and 2 days.1%).16 — 16 (16. Mean birthweight of babies diagnosed with ROP was 1632±197 g and babies without ROP in the same group had a mean birthweight of 1953±461 g (p=0.9) TABLE II .3%) were born in another hospital and referred to our ophthalmology department for ROP screening examination. Median gestational age of treated and untreated infants was 32 weeks and 33 weeks.18±7. 1769±387 g.04). SPSS 13. BPD = bronchopulmonary dysplasia. 41 infants (11. All of these patients were referred to our center after 6 TABLE I . d. 2.3) 4. A p value less than 0.RESULTS OF ROP SCREENING BY GESTATIONAL AGE GROUPS Group 1 (< 32 weeks) (n=348) No ROP. n (%) ROP = retinopathy of prematurity.8%) required treatment with either laser or cryotherapy (Tab. n (%) RDS.6) 69 (19. Mean birthweight of babies in group 2 who did not require laser/cr- yotherapy was 1778±388 g. n (%) Duration of O2 supplement. n (%) Duration of ventilation. RDS = respiratory distress syndrome. RDS. II).5) 1. d. II). and 1924±452 g in groups 1.5) 41 (11.3) 182 (52.5%) had stage 1 or 2 disease and 14 infants (3.93 5 (1.4%) had stage 1 or 2 retinopathy.1) 116 (33. and gender) were compared using χ2 test. n (%) Ventilator treatment.4) 65 (18.05 was considered significant.0 program was used for statistical analysis. n (%) Stage 1 or 2. g.Akman et al if normally distributed.3) 1274±339 29. Among 52 babies who were treated with laser/cryotherapy.9) 5 (5. Eleven patients (3. with a mean birthweight of 1460±189 g.9)/143 (41. 16 (30.007). Categorical variables (sepsis.001).42±5. n (%) Stage 3 or more.9) 11 (3.8) 9 (9. in group 2 were included in treatment programs (Tab. II).37±14. © 2010 Wichtig Editore . 116 infants (33.9%) had severe disease.1) — — 171 (49.1) 112 (31. 9 babies (9. Group 2 (32–34 wk) (n=355) 1769±387 32. The mean birthweight was 1274±339 g.9) 11.1) 182 (52.97±5. In group 2. Mean birthweights and gestational ages of the babies born in our center were 1105 g and 28 weeks. were compared by Student t-test. Clinical features of the infants born in our center and infants referred from another hospital were also compared.001.1±1. mean ± SD M/F.8 201 (56.1%) had stage 1 or 2 disease.89 63 (64. n (%) Sepsis. 69 infants (19. and 3. respectively. respectively (p=0. mean ± SD Gestational age.3) 4.1) 22 (22.8) 933 .1) Group 3 (>34 weeks) (n=98) 89 (90. BPD. 61 infants (17. respectively (p=0.4) 100 (28.6)/154 (43.3) 2.7%) were born in our center and 36 babies (69. Five of 801 patients were diagnosed with either unilateral or bilateral retinal detachment at the time of first screening examination. 2.5%) had severe disease (stage 3 or more). In group 1. Median gestational age and birthweight of these 5 infants were 29 weeks and 1300 g.4) 61 (17. p<0.04 253 (71.5 205 (58.3±0.4 56 (57.CLINICAL CHARACTERISTICS OF INFANTS IN DIFFERENT GESTATIONAL AGE GROUPS Group 1 (<32 wk) (n=348) Birthweight.44±3.74±1. mean ± SD O2 supplement. In this group. wk.8) 132 (37.

8) Group D (high-grade ROP) (n=14) 32. infants whose gestational age is over 32 weeks are not screened.Screening criteria for retinopathy of prematurity TABLE III .3 1362±348 102/69 32 (18.COMPARISON OF CLINICAL FEATURES OF CASES WITH AND WITHOUT ROP IN GROUPS 1 AND 2 Group 1 (<32 wk) (n=348) Group A (no ROP) (n=171) Gestational age. n (%) Duration of O2 supplement.9) 6. respectively (Tab. the incidence of retinopathy was found to be 90% in babies with a birthweight less than 750 g.05 >0.6%. n=171) and patients with severe ROP (group B. wk.5) 34 (55. p<0. mean ± SD BPD.7 — 4 (28. Infants with BPD and sepsis had higher risks of developing severe ROP. BPD = bronchopulmonary dysplasia.2±4.2±4. 6.003.6 vs 6.7 vs 29.8% vs 67. respectively. III). The mean gestational age (28. 934 DISCUSSION This study reports that the frequency of ROP was 50.ISSN 1120-6721 .001* <0. III).5 13 (92.6±9.2%. Cases with severe ROP had a mean birthweight and gestational age of 1217 g and 29.7) 1. Gestational age in group C slightly exceeded that of group D.04) were significantly higher in the severe ROP group.7 1441±183 8/6 1(7. more mature babies are at risk of developing ROP in comparison to babies of industrialized countries. the birthweight was significantly less compared to group C (1441±183 vs 1818.4±1. Additionally.4% of the study group was treated with laser/cryotherapy for ROP.001* <0.7 1155±305 35/26 34 (55.1. the duration of ventilator treatment (9. †Both culture-positive and clinical sepsis were included.5) p Group B (high-grade ROP) (n=61) 28.2) 53 (30. n (%)† *Significant. mean ± SD Birthweight.04* >0.5±0.001) and oxygen supplementation (18. p<0.1±2.7) 44 (72.2.003* >0.05 >0.3 weeks.4±5. Nine percent of babies with a gestational age more than 34 weeks had mild ROP in our center. respectively.3%.8) 6.2) 3.9% and 23.1) 9. RDS = respiratory distress syndrome. The incidence of ROP in 58 extremely low birthweight babies was 36. and 47% in babies with a birthweight between 1000 and 1250 g (20). n=272) and patients with severe ROP (group D. Duration of ventilation was almost the same in both groups and duration of oxygen supplementation was longer in group D than group C but these differences lacked statistical significance (Tab.6 15 (24.05 >0. Group 1 was further split into 2 subgroups: patients without ROP (group A. In the study of Chaudhari et al (21).001* 0. p=0.1 135 (78.2 2 (0.008* >0. p<0.9±372 151/121 20 (7.7% vs 28. it is stated that mean birthweight of babies with severe ROP is 750 g in industrialized countries and 1500 g in developing countries (6).001 and p=0. Similarly. III). mean ± SD O2 supplement. p<0.7±5.05 weeks of postnatal age from other hospitals. in 381 very low birthweight infants it was 23.05 >0.7) 75 (43.05 >0.2%. d. but this difference failed to attain statistical significance. ROP = retinopathy of prematurity.4 183 (67.7) 43 (15.2 9 (5.1) 5 (35.4% in babies with a gestational age less than 32 weeks and gestational age between 32 and 34 weeks.18±12.9±17.05 0. p<0.8) 2. and in 105 infants weighing 1500– © 2010 Wichtig Editore . n (%) Ventilator treatment. n=14). n=61).6±9.001) were significantly longer in infants with severe ROP.05 0. In group D.8 1818.4±1. d.1±2.3) 1.001* <0. p<0.008) and ventilator treatment (35.7) 29. III).001* <0.9±17. the incidence of ROP in 552 infants screened in a tertiary care center in India was presented. the number of patients who received supplemental oxygen (92. In the CRYO ROP study.6±1.3) 18.001* <0.9±372. In most developed countries.05 >0. mean ± SD M/F RDS. g.3 vs 2.001) (Tab. In the literature.001) were significantly lower in infants with severe ROP in group 1 (Tab.18±12.6±1.9) <0.3.001* >0. n (%) Duration of ventilation. p=0.3) 77 (28.3 60 (98. Group 2 was also divided into 2 subgroups: patients without ROP (group C. 78% in babies with a birthweight between 750 and 999 g.001) and birthweight (1155±305 vs 1362±348. n (%) Sepsis.05 0. Group 2 (32–34 wk) (n=355) p Group C (no ROP) (n=272) 33±0. In developing countries.

It seems reasonable to screen all babies born at less than 34 weeks of gestation or with a birthweight less than 1850 g. Only one baby had a gestational age of >35 weeks. They reported that using United States criteria (birthweight <1500 g or gestational age <29 weeks. but all were stage 1 or stage 2. prolonged duration of ventilator treatment. 41 (7. No ROP was found in infants weighing ≥2000 g or with a gestational age more than 36 weeks. The mean age at detection was 5. Similarly.6 weeks (range. The incidence of ROP was 26.ISSN 1120-6721 . possibly missing only one baby. Low gestational age. all babies with ROP would have been detected. 11 babies with severe disease would have been missed. All the stage 3 ROP and the threshold ROP cases were in babies with birthweight <1000 g and gestational age below 28 weeks. Out of the 552 infants who were screened for ROP. As a result.8 g).2%). if birthweight was a few grams higher. 11 patients with a gestational age more than 32 weeks required cryo/laser therapy for severe ROP. Thirty-one babies had birthweights more than 1500 g (27. 112 of 120 babies with severe retinopathy of prematurity would have been detected and 8 would have been missed. screening criteria should be modified accordingly.2%) infants exceeded UK screening criteria. If UK screening criteria (birthweight <1500 g or gestational age <32 weeks. gestational age. they would have detected 104 of 120 cases and 16 would have been missed. In a study of Jalali et al (23). birthweight. All but one of these 9 patients had a birthweight less than 1850 g. and stage 3 in 10 (4. In accordance with our findings. 9 had ROP and none of them required treatment. BPD.7% and 7. Out of 98 infants with gestational ages more than 34 weeks. 26–36 weeks). stage 2 in 24 (11. and respiratory morbidities are reported to be the most important risk factors for ROP.8%) babies.9%) infants born between 29 and 32 weeks had ROP.4%) needed laser photocoagulation.6%. The mean gestational age was 29. 15 (71. their study confirms that severe ROP occurs in their population in a significant number of babies who fall outside the screening criteria of high-income countries. in our study screening premature neonates whose gestational ages are less than 34 weeks or birthweight less than 1850 g would have identified all infants with severe ROP. Similarly.8±1. In our study. 18 (16. The maximum stage reached was stage 1 in 27 (13. Unless these 83 babies were screened.4%) exceeded the criteria used in the United States. An incidence of 64/205 (31. There were 5 (8%) babies with birthweight >1250 g and 8 (12%) babies with gestational age >30 weeks among babies with ROP. If our suggested screening criteria had been used.1% in babies with a gestational age between 28 and 32 weeks and those with a gestational age more than 32 weeks. and 34 (30. Threshold ROP was present in 3 (1. similarly.Akman et al 1999 g it was 11. 56 (30. the mean gestational age was 29. more frequent in babies with low birthweight.2%).1%) of them were treated with laser or cryotherapy. and 10 (7. respectively. ROP was. In contrary to the situation in middle 935 © 2010 Wichtig Editore . 83 babies (23%) born with a gestational age between 32 and 34 weeks were diagnosed with ROP.4%) of 335 screened infants born at less than 28 weeks of gestation had ROP. Eleven (3.5%) infants born between 33 and 36 weeks of gestation had ROP. In our study. 73%) babies would have been examined had a birthweight of <1251 g and a gestational age <30 weeks been applied. ROP is a multifactorial disease.4%. or both) were applied.7%). in their center. had a birthweight of 2170 g. The birthweight of 115 babies ranged from 710 to 2000 g (1254±280. Criteria that combine gestational age of <34 weeks and birthweight of <1750 g would have identified all 120 babies. The incidence of retinopathy for babies born <28 weeks was reported to be 63. Several articles from Turkey revealed similar results. Ten cases had gestational ages more than 32 weeks. Significantly fewer (150/205. Mathew et al (26) reported ROP findings of 205 infants either with a birthweight below 1500 g or a gestational age of less than 32 weeks who were screened for ROP during an 8-year period. in our study.5%) babies. Chen and Li (22) analyzed data from 114 babies admitted to a tertiary referral center in China and treated for severe ROP. Kulaçoğlu et al (25) reported that. This study suggests that not only the gestational age and birthweight but also the clinical course of the infants are crucial determinants for the development of ROP. ROP screening examination results of 306 infants with gestational ages ≤37 weeks were presented. who was referred to our center from another hospital. Six infants with a gestational age between 33 and 34 weeks needed laser therapy and these patients would have been missed if they were not screened. In 120 babies with severe retinopathy. or both).9 weeks (range 26–34 weeks) and the mean birthweight was 1432±319 g (range 760–2500 g).2%) ROP was noted. data obtained from an eye institute from Southern India between October 1999 and December 2002 were analyzed. and oxygen supplementation. Overall. In a study by Öner et al (24) from Turkey. sepsis.5±2 weeks. One infant.

However. Prof. 350: 12-4. Louis: Mosby. diagnosis and treatment. World Health Organization. 8. Rahi J. in developing countries. 9. with more larger. Gilbert C. American Association for Pediatric Ophthalmology and Strabismus. Gibson DL. ROP must be managed by vigilance with regular screening by skilled ophthalmologists who. Mukai S. 7. Pediatrics 1984. ROP remains a serious risk to extremely low birthweight babies in the developed world. Address for correspondence: Ipek Akman. American Academy of Ophthalmology. identify babies at risk of sight-threatening disease and arrange for treatment with laser ablative therapy. new screening modalities may be needed for the best practice. Semin Perinatol 1986. Serum growth factor (VEGF. IGF-1) levels obtained at this gestational period seem to be a promising screening tool for ROP (30). St. Uh SH. Update on retinopathy of prematurity. 86: 405-12. and standard screening criteria are not applicable to all at-risk babies. More studies are needed to define the high-risk babies accurately. These babies were all referred late and had poor outcome. VEGF requires IGF-1 secretion. Geneva: World Health Organization. Eckstein M. and worst clinical courses. Screening examination of premature infants for retinopathy of prematurity. Biglan AW. 10: 187-95. birthweights. more mature babies. Macpherson TA. 74: 127-33. This is especially true for babies with the lowest gestational ages. Screening criteria devised for industrialized countries are not applicable for developing 936 countries.com REFERENCES 1. Retinopathy of prematurity-induced blindness: birthweight-specific survival and the new epidemic. Sheps SB. whom to screen for ROP is debatable. Hunter DG. Gilbert C. Pediatrics 2006. An international classification of retinopathy of prematurity. using current updated screening guidelines. More research is needed before implementing routine use of these growth factors. In our study. 3. The first ROP screening examination should be undertaken at 4–6 weeks. while the patient is still in the neonatal intensive care unit (16). 6. Lancet 1997. O’Sullivan J. Mathew et al concluded that ophthalmic examination might be safely and efficiently concentrated in babies with birthweight <1251 g and gestational age below 30 weeks in order to lessen unnecessary examinations. 5 babies had retinal detachment at the first examination. which need to widen their screening criteria. 117: 572-6. Retinopathy of prematurity: pathogenesis. Section on Ophthalmology American Academy of Pediatrics. 2000.ISSN 1120-6721 . Selamiçeşme Kadıköy/Istanbul.Screening criteria for retinopathy of prematurity income countries. in order to exert its effect. Childhood blindness in the context of VISION 2020: The right to sight. Dr. Foster A. Bull World Health Organ 2001. screening all premature babies with a gestational age less than 34 weeks or babies with a poor clinical course appears to be appropriate. The authors report no proprietary interest or financial support. The examination is done at the bedside. Bağdat cad. which predominantly occurs at 31–32 weeks postmenstrual age. Retina. In our country. In conclusion. Retinopathy of prematurity. International Committee For Classification of ROP. 79: 227-32. 2001: 1472-99. Schechter MT. Brown DR. Pediatrics 1990. In fact. 4. 32: 163-84. the criteria for ROP screening programs should be designed according to local conditions. Programs for detecting babies needing treatment in low and middle income countries should take this into consideration and involve larger. and to more mature babies in developing countries. Turkey ipekakman@yahoo. 2. Preventing Blindness in Children: Report of WHO/IAPB Scientific Meeting. MD. Foster A. Int Ophthalmol Clin 1992. 5. © 2010 Wichtig Editore . Thus. The evidence suggests that the population of premature babies at risk of ROP needing treatment varies. Schachat AP. McCormick AQ. VEGF is required in retinal vascular development and is expressed in hypoxic states. Retinopathy of prematurity in middle-income countries. Recent research data emphasize the role of vascular endothelial growth factor (VEGF) and of insulin-like growth factor 1 (IGF-1) in the pathogenesis of ROP (27-29). more mature babies developing treatable disease in low and middle income countries than in industrialized countries. 149/3 Trak Apt.

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