Original Research Paper

Retinopathy of prematurity and associated factors in Lagos, Nigeria I. B. Fajolu1, A. Rotimi-Samuel2, O. T. Aribaba2, K. O. Musa2, F. B. Akinsola2, V. C. Ezeaka1, A. O. Onakoya2 Departments of 1Paediatrics and 2Ophthalmology, College of Medicine, University of Lagos, Nigeria Background: Screening and early treatment of retinopathy of prematurity (ROP) is important to reduce visual impairment in at risk infants. Aim: To determine the frequency and risk factors associated with ROP in preterm infants in Lagos University Teaching Hospital. Methods: This was a prospective cohort study of preterm infants with gestational age (GA) less than 32 weeks conducted from November 2011 to May 2014. The infants’ eyes were examined using an indirect ophthalmoscope at 4-6 weeks of life or at 34 weeks post-conceptual age. Examinations were repeated weekly until regression or progression to a high risk pre-threshold disease. Staging was according to the revised International Classification for ROP and treatment criteria were as defined by the Early Treatment for ROP study. The GA, birth weight (BW), use of oxygen, presence of respiratory distress syndrome and other risk factors were recorded and tested for significance. Results: Twelve (15%) of the 80 infants examined had any ROP and six (7.5%) had treatable ROP. The mean (SD) GA and BW for infants with ROP were both lower than for those without ROP; 28.2 (1.7) weeks vs 29.1 (1.6) weeks and 1124 (212) g vs 1251 (274) g for GA and BW, respectively. Risk factors such as supplemental oxygen, sepsis, respiratory distress and anaemia were not significantly associated with ROP. Conclusion: The frequency of ROP and treatable ROP was high; it is therefore recommended that routine care of preterm infants should include screening for ROP and that affordable treatment facilities should be provided in public hospitals. Keywords: Frequency, Retinopathy of prematurity, Risk factors, Treatment, Neonatal unit, Lagos, Nigeria

Introduction Retinopathy of prematurity (ROP) is a multifactorial, potentially blinding vasoproliferative disorder that affects the retina of preterm infants.1 ROP often regresses or heals but can lead to severe visual impairment or blindness; early recognition and treatment is therefore recommended to prevent severe visual impairment. The risk of ROP is inversely proportional to gestational age (GA) and birthweight (BW),1 thus, with improvement of neonatal services, more very low-birthweight and extremely low-birthweight infants are surviving, resulting in an increased population at risk of ROP. ROP is prevalent worldwide and studies in developed and developing countries have reported incidences varying from 5.5% in Nigeria2 to 16.3% in South Africa,3 36.48% in Taiwan4 and 65.8% in the United States.5 This relatively lower incidence in developing countries has been attributed to poor

Correspondence to: I B Fajolu, Department of Paediatrics, College of Medicine, University of Lagos, Nigeria. Email: [email protected]

ß W. S. Maney & Son Ltd 2015

DOI 10.1179/2046905515Y.0000000045

survival of high risk, very small and immature preterm infants and a lack of diagnostic facilities for these preterm infants; however, ROP in middleincome countries is increasingly becoming a cause of blindness.6 This increase is possibly because survival of preterm infants is improving, thus increasing the number of infants at risk of ROP and the associated compromised care of these infants, and the non-availability of screening and treatment programmes.6 Severe disease is seen mainly in infants with a birthweight v1250g and gestational age (GA) v30 weeks with 6% of such neonates progressing to threshold ROP.7 Threshold ROP is defined as five or more contiguous or eight cumulative 30 degrees sector (clock hours) of stage 3 ROP in zone I or II in the presence of ‘plus’ disease (a degree of dilatation and tortuosity of the posterior retinal blood vessels meeting or exceeding that of a standard photograph).8 Retinal vessels begin to develop at around 16 weeks gestation from the hyaloid vessels at the optic disc growing towards the periphery (from the

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factors.4,7,14–20 Ethnicity has also been reported as a risk factor for severe ROP with Asian and black infants having a higher risk than white infants of developing threshold ROP, even after adjusting for gestational age and birthweight.21 This may be owing to VEGF polymorphisms as it has been reported that VEGF 936CwT polymorphism is as an independent risk factor for threshold ROP and also a possible predictor of threshold ROP in Japanese neonates of j30 weeks gestational age,22 thus suggesting the important role of vascular endothelial growth factor (VEGF) in ROP-related retinal neo-vascularization. However, some smaller studies reported a higher risk of retinopathy and more severe cases in Caucasian infants than in blacks and Hispanics,23,24 while another study reported no ethnic differences in the risk of developing ROP.25 In a Singapore study, the risk factors identified by regression analysis for developing threshold ROP were maternal pre-eclampsia, birthweight, pulmonary haemorrhage, duration of ventilation and duration of continuous positive airway pressure (CPAP).26 There is a paucity of data on the prevalence of ROP in Nigeria and sub-Saharan Africa in general with only three reports from Nigeria.2,27,28 This could be attributed to the relatively poorer facilities for preterm infants in sub-Saharan Africa, leading to poorer survival of these newborns. However, more preterm infants now survive in Lagos University Teaching Hospital (LUTH) owing to improvement in facilities. It is therefore necessary to determine the frequency of and risk factors for ROP in countries such as Nigeria in order to develop screening criteria and offer early treatment for this potential cause of visual impairment and blindness in these vulnerable infants. The aim of this study was to determine the frequency and risk factors associated with ROP in preterm infants in LUTH.

posterior aspect of the globe towards the anterior). These vessels reach the nasal and temporal retinal periphery by the 8th and 10th months of gestation, respectively.9 Following preterm delivery, normal retinal vascular maturation ceases. Exposure of newborn premature infants to conditions such as hyperoxia and hypotension causes down-regulation of retinal vascular endothelial growth factor 10,11 (VEGF). This results in constriction of blood vessels which become obliterated and delay normal retinal vascular development; this is the first phase of ROP.11 During the hypoxic (second) phase of ROP, the increased metabolic demand of the growing eye causes the avascular retina to be relatively hypoxic, causing excessive VEGF production, which leads to ROP.10,11 The revised version of the International Classification of Retinopathy of Prematurity classified ROP into five stages, refined the definition of ‘plus’ disease and described aggressive posterior ROP (AP-ROP) as well as pre-plus disease.11 Stage 1 is the development of a thin, flat, white demarcation line between the vascularized and non-vascularized retina. In stage 2, the line has developed into a ridge, and retinal vessels may extend into it while stage 3 is when extra-retinal vessels protrude from the ridge. Proliferation of extra-retinal vessels may exert traction on the retina, resulting in subtotal retinal detachment (stage 4) or total retinal detachment (stage 5).11 ‘Plus’ disease is defined as the presence of sufficient vascular dilation and tortuosity in at least two quadrants of the retina while pre-plus disease is vascular abnormalities of the posterior pole which are insufficient for the diagnosis of ‘plus’ disease but demonstrate more venous dilatation and arterial tortuosity than normal.11 Aggressive posterior ROP (AP-ROP) is a rapidly progressive, illdefined ROP, usually located posteriorly, with prominent ‘plus’ disease which usually does not progress through the classic stages of 1 to 3.11 Peripheral retinal ablation with laser or cryotherapy is recommended for high-risk pre-threshold disease.12 The Early Treatment for Retinopathy of Prematurity (ETROP) study defines high-risk prethreshold disease as zone I, any stage of ROP with plus disease; zone I, stage 3 ROP without plus disease; or zone II, stage 2 or 3 ROP with plus disease.12 This treatment can reduce but not eliminate the risk of ROP progressing to the potentially blinding stages 4 and 5 where there is retinal detachment which would require other therapies such as scleral buckling or vitreous surgery.13 Low birthweight, low gestational age (GA), severity of illness such as respiratory distress syndrome (RDS), bronchopulmonary dysplasia (BPD) and sepsis have all been documented as associated

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Methods This prospective cohort study was undertaken in the neonatal unit of LUTH, a government-owned tertiary health institution which caters for the majority of preterm infants born in the state. The neonatal unit has two wards, one for newborns delivered in the hospital’s labour ward and the other for those delivered outside the hospital and subsequently referred for specialist care. The hospital also has an ophthalmology department with trained ophthalmologists. All newborns delivered before 32 completed weeks of gestation with a birthweight j1500 g admitted to the neonatal unit from November 2011 to May 2014 who were still alive at 4 weeks of life or 34 weeks

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post-conceptual age were enrolled in the study. Newborns with a major congenital anomaly or dysmorphic features or whose parents refused consent were excluded. All infants were managed routinely and their eyes examined at 4 weeks post-natal age or 34 weeks post-conceptual age, whichever was the earlier. Before the study commenced, routine screening was not undertaken in the hospital but was introduced a year after the study began. Eyes were examined by a consultant ophthalmologist using a Keeler binocular indirect ophthalmoscope with a 30-dioptre lens. The eyes were dilated at least 30 minutes before the examination by instilling one drop of a combination of tropicamide 0.5% and phenylephrine 2.5% into both eyes, repeated after 10 minutes. Gentle pressure was applied to the medial canthus and excess eye drop fluid that flowed out of the eyes was wiped away to prevent any possible systemic absorption. The infant’s vital signs were monitored during and after the procedure. Tetracaine hydrochloride 0.5% eye drops were instilled for anaesthesia before the insertion of the speculum for the examination. The disease was staged according to the revised version of the International Classification of ROP.11 The eye examination was repeated weekly for infants with pre-threshold disease until regression occurred or it progressed to high-risk pre-threshold disease. All infants with threshold and high-risk pre-threshold disease at the initial or repeat examination were referred to a private hospital in Lagos with facilities for retinal ablative therapy for treatment as soon as they were stable (retinal ablative therapy facilities are not available in LUTH or any of the government hospitals in the state). The stage of the eye with the worse disease at the last examination was used to classify the child. Using the ETROP criteria for treatment, the disease was also categorized into two groups: treatable ROP (tROP) and non-treatable ROP (NtROP).12 Type 1 ROP (zone 1, stages 1–3 with plus disease; zone I, stage 3 without plus; zone II, stage 2 or 3 ROP with plus disease) and threshold ROP were categorized as tROP while type 2 ROP (zone I, stages 1–2 without plus disease, or zone II, stage 3 ROP without plus disease) was categorized as NtROP.12 Data on gestational age, birthweight and factors such as anaemia, duration of oxygen therapy, blood transfusion, sepsis and RDS were recorded for all enrolled infants.

Data management Data were analysed using SPSS version 21. Frequencies were generated and presented as tables and graphs. Means and standard deviations were generated for continuous variables and percentages were generated for categorical variables. Student’s t-test

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and the x2 test were used to test association and Pv0.05 was considered significant.

Ethics approval Approval was obtained from the Ethics and Research Committee of LUTH, and informed consent was obtained before enrollment from the parents or guardian of all infants.

Results A total of 80 preterm infants had both eyes examined during the study period (35 males). The mean (SD) birthweight and gestational age were 1231 (268) g and 28.9 (1.7) weeks, respectively. Twelve (15%) of the infants examined had retinopathy of prematurity, ten of whom had bilateral disease. The proportion of infants with ROP was higher in infants whose GA was v30 weeks than in those whose GA was i30 weeks [9/46 (19.6%) compared with 3/34 (8.8%), respectively, P50.22]. There was a similar increase in the proportion of infants with ROP whose birthweights were v1250 g than in those whose birthweights were i1250 g [8/41 (19.5%) and 4/39 (10.3%), respectively, P50.35]. Six (7.5%) of the infants had treatable ROP, four had stage 3 threshold and two had zone II, stage 2 and 3, respectively, with plus disease. The severity of ROP stages according to the gestational age and birthweight is shown in Table 1. Two-thirds of the infants with ROP had birthweights v1250 g and were delivered at v30 weeks gestation. All the infants with tROP were referred for laser therapy but only one could afford the treatment. Two infants were relocated to their states of origin where the father hoped to obtain free treatment while the remaining two have been lost to follow-up. Only two of the 12 infants with ROP are still being followed up (one had stage 1 disease which has regressed and the other had stage 3T and has had laser therapy), while all the others have been lost to follow-up. The mean (SD) gestational age was lower for infants with ROP than for those without it

Table 1 Severity of retinopathy of prematurity according to gestational age and birthweight

Gestational age, wks ,30 30-32 Total Birthweight, g ,1250 $1250 Total tROP, treatable non-treatable ROP

tROP n (%)

NtROP n (%)

4 (66.7) 2 (33.3) 6 (100.0)

5 (83.3) 1 (16.7) 6 (100.0)

4 (66.7) 2 (33.3) 6 (100.0)

4 (66.7) 2 (33.3) 6 (100.0)

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[28.2 (1.7) vs 29.1 (1.6) weeks]. However, the difference was not statistically significant. Infants with ROP also had lower mean (SD) birthweights than those without ROP [1124 (212) vs 1251 (274) g, P50.13]. There was also no significant association of factors such as gender, use of supplemental oxygen, sepsis, anaemia and blood transfusion with the presence of ROP or severity of the disease (Table 2).

South Africa, respectively.3 These differences may be because the old criteria for treatment (stage 3 threshold and above) were used in the South African study while the ETROP criteria were used in this study. The infants with ROP were also smaller than those in the Port Harcourt study with mean birthweights of 1267 g and 1411 g, respectively. All the six infants with type 1 ROP were referred to a private hospital with retinal ablation facilities. However, only one family could afford the treatment (the cost of surgery is US$250–400 per eye in private hospitals). Another challenge in managing ROP is that the parents did not seem to appreciate the importance of the diagnosis as most could not observe any obvious problem with their infants’ eyes; only two are still attending the clinic, and others have been lost to follow-up. All the infants with ROP and 77% of those without had supplemental oxygen but, unlike in other reports which have associated oxygen with ROP, the difference was not significant.14,15 Mechanical ventilation is currently not available in LUTH, which exposes infants to higher concentrations of oxygen; mechanical ventilation for i48 hours is associated with ROP.26 The percentage of oxygen given and the time of administration are also significant factors in addition to duration of administration: 100% oxygen for a short duration soon after birth may pose a higher risk than 30% oxygen given for a longer period in the 2nd or 3rd week after birth. In this study, although all the preterm infants who received humidified supplemental oxygen commenced this within the 1st hour of life, the fraction of inspired oxygen (FiO2) was not measured owing to lack of functional oxygen analysers. Furthermore, even though the upper limit for oxygen saturation in preterm infants in the neonatal unit is 95%, the pulse oximeters available are only for intermittent monitoring. Another limitation of the study is the loss to follow-up of infants with ROP: only two of the 12 are still being seen at the eye clinic. This highlights the importance of sensitive, individualized, balanced and preferably written information for parents of preterm infants with ROP. Although the drop-out rate might be owing to ignorance, the unavailability of affordable treatment facilities within the hospital might also have contributed to the high drop-out rate. The frequency of ROP was high with almost 7.5% of at-risk infants having severe disease requiring treatment. As efforts to improve survival of preterm infants increase, there is an urgent need for government, non-government and private providers to offer facilities to prevent, recognise and treat infants with ROP. Pending the results of larger studies in

Discussion The frequency of ROP (15%) is similar to the 16.2%, 12.7% and 17% in three studies from South Africa,3 China29 and Scotland,30 respectively. It is, however, higher than the 5.5% reported in an earlier report from Ibadan2 which studied a smaller number of infants. The Ibadan study was undertaken more than 15 years ago when survival rates of preterm infants were still very low. In two more recent studies in Port Harcourt28 and Canada,31 47.2% and 40.4%, respectively, of study infants had ROP. The Canadian study had smaller infants who are more likely to develop ROP with a mean GA and BW of 27.5 weeks and 1054 g, respectively, compared with 28.9 weeks and 1231 g in the present study. The infants in the Port Harcourt study had a higher mean gestational age and birthweight. The mean GA of infants with ROP was higher than in the Canadian study31 which might be because smaller infants of lower GA are more likely to survive in high-income countries owing to better facilities. The frequency of ROP increased with decreasing gestational age (19.6% vs 8.8% in infants v30 weeks and those i30 weeks GA, respectively) and decreasing birthweight (19.5% vs 10.3% in infants v1250 g and those i1250 g at birth). This is in keeping with other studies26,32 which have reported higher incidence of ROP in smaller infants. Treatable ROP was observed in six (7.5%) infants of v32 weeks GA, which is slightly higher than the 4% and 1.6% in studies in Port Harcourt28 and Table 2 Factors associated with retinopathy of prematurity Parameters

ROP (12)

No ROP (68)

P-value

Male Supplemental oxygen Sepsis Antenatal corticosteroids IVH RDS Anaemia Multiple BT Multiple gestation Phototherapy

3 (25.0) 12 (100.0) 6 (50.0) 9 (75.0) 2 (16.7) 9 (75.0) 7 (58.3) 5 (45.5) 5 (41.7) 11 (91.7)

32 (47.1) 54 (79.4) 24 (35.3) 31 (45.6) 11 (16.2) 37 (54.4) 49 (72.1) 41 (63.1) 23 (33.8) 62 (91.2)

0.21 0.11 0.35 0.12 1.0 0.22 0.49 0.36 0.74 1.00

ROP, retinopathy of prematurity; IVH, intraventricular haemorrhage; RDS, respiratory distress syndrome; BT, blood transfusions

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Nigeria, the suggested screening guidelines should follow the United Kingdom’s Retinopathy of Prematurity Guidelines 200833 which recommend screening of all preterm infants v32 weeks GA with a birthweight j1500 g.

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Acknowledgements We are grateful to the resident doctors who helped with data collection.

Disclaimer Statements Contributors The authors acknowledge the contributions of the resident doctors in the paediatrics and ophthalmology departments in data collection.

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Funding The study was funded by the authors. 19

Conflicts of interest The authors have no conflict of interest to declare. Ethics approval Ethical approval was obtained from the Health Research and Ethics Committee of the Lagos University Teaching Hospital, Lagos, Nigeria.

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of prematurity: results of the early treatment of retinopathy of prematurity randomized trial. Arch Ophthalmol. 2003;121:1684–94. The Report of a Joint Working Party. Retinopathy of Prematurity: Guidelines for Screening and Treatment. London: The Royal College of Ophthalmologists and British Association of Perinatal Medicine; 1995. Anderson CG, Benitz WE, Madan A. Retinopathy of prematurity and pulse oximetry: a national survey of recent practices. J Perinatol. 2004;24:164–8. Abdel HA, Mohamed GB, Othman MF. Retinopathy of prematurity: A study of incidence and risk factors in NICU of Al-Minya University Hospital in Egypt. J Clin Neonatol. 2012;1:76–81. Dani C, Reali MF, Bertini G, Martelli E, Pezzati M, Rubaltelli FF. The role of blood transfusions and iron intake on retinopathy of prematurity. Early Hum Dev. 2001;62:57–63. O’Keefe M, Kafil-Hussain N, Flitcroft I, Lanigan B. Ocular significance of intraventricular hemorrhage in premature infants. Br J Ophthalmol. 2001;85:357–9. Brooks SE, Marcus DM, Gillis D, Pirie E, Johnson CS, Bhatia J. The effect of blood transfusion protocol on retinopathy of prematurity: a prospective, randomized study. Pediatrics. 1999;104:514–18. Holmstrom G, Broberger U, Thomassen P. Neonatal risk factors for retinopathy of prematurity – a population-based study. Acta Ophthalmol Scand. 1998;76:204–7. Englert JA, Saunders RA, Purohit D, Hulsey TC, Ebeling M. The effect of anaemia on retinopathy of prematurity in extremely low birth weight infants. J. Perinatol. 2001;21:21–6. Aralikatti AK, Mitra A, Denniston AK, Haque MS, Ewer AK, Butler L. Is ethnicity a risk factor for severe retinopathy of prematurity? Arch Dis Child Fetal Neonatal Ed. 2010;95:F174–F176, doi:10.1136/F174 adc.2009.160366. Yagi M, Yamamori M, Morioka L, Yokoyama N, Honda S, Negi A, et al. VEGF 936C.T is predictive of threshold retinopathy of prematurity in Japanese infants with a 30-week gestational age or less. Res Rep Neonatol. 2011;1:5–11. Ying GS, Quinn GE, Wade KC, Repka MX, Baumritter A, Daniel E, et al. Predictors for the development of referralwarranted retinopathy of prematurity in the telemedicine approaches to evaluating acute-phase retinopathy of prematurity (e-ROP) study. Ophthalmology. 2015;133:304–11. Husain SM, Sinha AK, Bunce C, Arora P, Lopez W, Mun KS, et al. Relationships between maternal ethnicity, gestational age, birth weight, weight gain, and severe retinopathy of prematurity. J Pediatr. 2013;163:67–72. Sabri K, Manktelow B, Anwar S, Field D, Woodruff G. Ethnic variations in the incidence and outcome of severe retinopathy of prematurity. Can J Ophthalmol. 2007;42:727–30. Shah VA, Yeo CL, Ling YL, Ho LY. Incidence, risk factors of retinopathy of prematurity among very low birth weight infants in Singapore. Ann Acad Med Singapore. 2005;34:169–78. Ademola-Popoola D, Adesiyun O, Obasa TO. Screening programme for retinopathy of prematurity in Ilorin, Nigeria: a pilot study. West Afr J Med. 2013;32:281–5. Adio AO, Ugwu RO, Nwokocha CG, Eneh AU. Retinopathy of prematurity in Port Harcourt, Nigeria. ISRN Ophthalmol.. 2014. Available from: http://dx.doi.org/10.1155/2014/481527 Chen Y, Xun D, Wang Y, Wang B, Geng S, Chen H, et al. Incidence and risk factors of retinopathy of prematurity in two intensive care units in North and South China. Chin Med J. 2015;128:914–18. Dhaliwal C, Fleck B, Wright E, Graham C, McIntosh N. Incidence of retinopathy of prematurity in Lothian, Scotland, from 1990 to 2004. Arch Dis Fetal Neonatal Ed. 2008;93:F422–6. Isaza G, Arora S, Bal M, Chaudhary V. Incidence of retinopathy of prematurity and risk factors among premature infants at a neonatal intensive care unit in Canada. J Pediatr Ophthalmol Strabismus. 2013;50:27–32. Kim TI, Sohn J, Pi SY, Yoon YH. Postnatal risk factors of retinopathy of prematurity. Paediatr Perinat Epidemiol. 2004;18:130–4. Royal College of Paediatrics and Child Health, Royal College of Ophthalmologists, British Association of Perinatal Medicine & BLISS. UK Retinopathy of Prematurity Guidelines, 2008

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Screening and early treatment of retinopathy of prematurity (ROP) is important to reduce visual impairment in at risk infants...
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