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Full-Term Neonatal Ophthalmic Screening in China: A Review of 4-Year OutcomesLi-Hong Li, MD;* Wei-Chi Wu, MD, PhD;* Na Li, MD; Jun Lu, MD; Guo-Ming Zhang, MD; Jun-Yang Zhao, MD; Yan Ma, MD

BACKGROUND AND OBJECTIVE: To report the 4-year outcomes of a neonatal ophthalmic screening pro-gram in the Kunming Maternity and Child Care Hos-pital of Kunming City, Kunming, China.

PATIENTS AND METHODS: This was a retrospective, observational case series study. Newborns who un-derwent neonatal eye screening using the RetCam system (Clarity Medical Systems, Pleasanton, CA) at the authors’ hospital from March 2010 to February 2014 were included.

RESULTS: Of the 15,284 full-term infants who par-ticipated in the program, 21% (3,171 of 15,284) had some ocular abnormalities. Among these abnor-malities, retinal hemorrhage was the most frequent finding, accounting for 19% (2,899 of 15,284) of all cases. Other anomalies were found in 2% (272 of 15,284) of the cases. No major ocular or systemic complications were found to be associated with the screening process.

CONCLUSION: Overall, 21% of the newborns who underwent the eye screening program were found to have an abnormality. The use of the RetCam for the screening program was both efficient and safe in identifying ocular anomalies.

[Ophthalmic Surg Lasers Imaging Retina. 2017;48:983-992.]

INTRODUCTION

Preschool children with vision problems rarely ac-tively complain about their visual impairment, which, if not treated, may become progressively worse. There-fore, effective eye screening programs and examina-tions to identify ocular disorders in young children are important. Eye examinations and testing for visual acuity (VA) in children are not usually performed until around 3 years of age in China. The majority of ocular health issues can be revealed by screening and subjec-tive VA tests as soon as the children are old enough to cooperate with such tests. However, some ocular dis-orders may have a delayed diagnosis due to testing at a later age, and a considerable number of children will go undetected with respect to vision and eye disorders despite being screened at an early age. Moving the tim-ing of eye examinations to the perinatal period may lead to the early detection and management of eye dis-orders in these children. Our prior 1-year study involv-ing a total of 3,573 healthy full-term newborns detect-ed 871 abnormal cases (24.4%), the majority of which were retinal hemorrhage (21.5%).1 Of note, 1.9% of the patients had a hemorrhage involving the macula.1 The other abnormal ocular findings included subconjunc-tival hemorrhage, congenital microphthalmos, con-genital corneal leukoma, posterior synechia, persistent pupillary membrane, congenital cataracts, enlarged cup/disc ratio, retinal hamartoma, retinoblastoma, op-tic nerve defects, macular pigment disorders and non-specific peripheral retinopathy.1 The results are very

From the Department of Ophthalmology, Kunming Maternity and Child Care Hospital, Yunnan, China (LHL, JL, NL); the Department of Ophthalmology, Chang Gung Memorial Hospital, Taoyuan, Taiwan (WCW); Chang Gung University, College of Medicine, Department of Medicine, Taoyuan, Taiwan (WCW); Shenzhen Eye Hospital, Jinan University, Shenzhen, China (GMZ); the Department of Ophthalmology, Beijing Children’s Hospital, Capital Medical Uni-versity, Beijing, China (JYZ); and the Department of Ophthalmology, Beijing Tongren Ophthalmic Center, Capital University of Medical Sciences, Beijing, China (YM).© 2017 Li, Wu, Lu, et al.; licensee SLACK Incorporated. This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 International (https://creativecommons.org/licenses/by-nc/4.0). This license allows users to copy and distribute, to remix, transform, and build upon the article non-commercially, provided the author is attributed and the new work is non-commercial.Originally submitted March 25, 2017. Revision received May 13, 2017. Accepted for publication August 2, 2017.This study was partially supported by a Chang Gung Memorial Hospital Research Grant (CMRPG3F0191~3) and a National Science Council Research Grant (MOST 104-2314-B-182A-100-MY2).The authors report no relevant financial disclosures.* Drs. Li-Hong Li, MD, and Wei-Chi Wu, MD, PhD, contributed equally to this work.Editor’s Note: Clarity Medical Systems, the original manufacturer of the RetCam III Imaging System mentioned in this study, has since been acquired by Natus Medical Incorporated.Address correspondence to Na Li, MD, No. 5, Huashan West Road, Department of Ophthalmology, Kunming Maternity and Child Care Hospital, Kunming, Yunnan, 650031, China; email: Done23@qq.com.doi: 10.3928/23258160-20171130-05

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similar to a recent study of Newborn Eye Screen Test (NEST) conducted in the U.S.2 In the NEST study, the birth prevalence of fundus hemorrhage was 20.3% and the fovea was involved in 3% of all newborns.2 The initial outcomes of this newborn eye screening pro-gram suggest that early screening is valuable in terms of making an early diagnosis of visual pathologies, and the incidence of eye abnormalities detected by this program was higher than expected.

In this study, we aimed to update the outcomes with data from almost 4 years of newborn eye screen-ing in Kunming, Yunnan Province, China. The issues of safety associated with the screening program were investigated in a large cohort of 15,284 healthy new-borns who completed the eye examinations.

PATIENTS AND METHODS

This was a retrospective study reviewing all cases who attended our newborn eye screening program at Kunming Maternity and Child Care Hospital, Kun-

ming, Yunnan Province, China, between March 2010 and February 2014. This study was approved by the Institutional Review Board of the hospital.

After the parents or the legal guardians of the pa-tient provided written consent, the eye screening test was arranged. If the newborns were inborn patients, the tests were usually arranged within 28 days of birth, and preferably within 7 days of birth. Not all the in-born children received eye screening because this was not a free service. If the patients were from outside our hospital, the date of examination was arranged as soon as possible, usually later than 28 days of birth. These newborns were sent to our hospital for screening be-cause eye screening was not available in the hospitals where they were born, and because their parents want-ed them to receive eye examinations.

The examinations were performed by a team con-sisting of an ophthalmologist and an assisting nurse. An external examination of the eyes was performed first, which included the anterior segment and pupil-

Figure 1. Retinal hemorrhage found in the newborn eye screening program. Extensive retinal hemorrhage involving the macula and disc was found in a full-term newborn.

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lary light reflex using a standard flashlight. Oral food and fluids were withheld 1 hour before the examina-tion. The pupils of the infants were then dilated with 0.5% tropicamide administered every 10 minutes for two to three times starting from 1.5 hours before the examination. Further treatment was given if a mini-mum of 4 mm of pupil dilation was not achieved. A topical anesthetic was then instilled. Gel was used to help lubricate the corneal surface and a pediatric lid speculum was used.

A sterile eyelid speculum was then placed in the eye to be examined. A wide-angle digital fundus cam-era (RetCam III; Clarity Medical Systems, Pleasanton, CA) was then used first in one eye and then the other. The anterior segment was examined using a non-contact wide-angle portrait camera lens. The anterior chamber angle was then evaluated with a 130° lens, tilted appropriately to image the angle in at least four quadrants. Photos were taken of the posterior pole, including the optic nerve and macula. The superior, inferior, nasal, and temporal retinal fields were im-

aged when possible. The photos were taken using a systematic protocol in terms of angle and the retinal fields imaged. For the patients in whom the eye exam revealed an abnormal finding, a further examination or referral to the ophthalmology clinic was arranged at a later date.

Hemorrhages were classified according to their lo-cation in three retinal regions. Zone I encompassed one disc diameter around the optic nerve head and fovea, zone II extended from the anterior boundary of zone I to the equator, and zone III was anterior to zone II, extending to the ora serrata.3 The degree or severity of the hemorrhage was classified by the num-ber of hemorrhages per eye as follows: grade 1, one or two hemorrhages; grade 2, three to 10 hemorrhages; and grade 3, more than 10 hemorrhages.4 The shape, location, and other associated features of the hemor-rhages were determined by the photos taken with the RetCam system.

Data from the examinations were logged onto a spreadsheet, and Pems 3.3 (Package for Encyclopae-

Figure 2. Disc hemorrhage found in the newborn eye screening program. Disc hemorrhage was noted in a full-term newborn.

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dia of Medical Statistics) software package was used for analysis. The Chi-square test was used to compare differences between the findings before and after 28 days of screening, as well as differences in categorical variables between the two groups.

RESULTS

Between March 2010 and February 2014, a total of 17,688 full-term infants were born at our hospital, of whom 14,662 (83%) received neonatal eye exami-nations. Another 622 newborns from other hospitals also received eye examinations, and the combined total of 15,284 full-term newborns were included in this study. We defined a normal newborn as having a gestational age of 37 weeks or older, a body weight of 2,500 g or greater, no evidence of systemic diseases, and an Apgar score of 7 or more.1 There were 7,881 (52%) male patients and 7,403 (48%) female patients. Vaginal delivery was performed in 8,846 patients and Cesarean section in 6,438. There were 98 sets of twins

(all born via Cesarean section) and the rest of the pa-tients were singletons.

Among the newborns, 14,786 (97%) were screened at an age of 1 day to 28 days, and 498 (3%) were screened at an age of 29 days to 365 days. Overall, 79% (12,113 of 15,284) of the patients passed the eye screening test and 21% (3,171 of 15,284) did not and were found to have ocular abnormalities. The main causes of failed screening were retinal hemorrhages, including grade 1 to 3 hemorrhages in the retina, mac-ula, and optic disc in 19% (2,899 of 15,284) of the overall patients (Table 1; Figures 1 and 2), and 91% (2,899 of 3,171) of the ocular abnormalities found in the eye screening program. There was a higher incidence rate of retinal hemorrhages in the cases screened before 28 days than in those screened after 28 days (χ2=102.120; P < .001). Potentially vision-threatening macula hemorrhages occurred in 3% (428 of 14,786) and 0.2% (one of 498) of the patients when screened before and after 28 days, respectively.

Figure 3. Subretinal calcification (arrows) noted in the newborn eye screening program. Etiology accounting for this presentation remains unknown.

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The other 272 (2%) ocular abnormalities detected by the screening program are listed in Table 2. The most frequently detected anomalies included subret-inal lipid or calcium deposition (0.61%) (Figure 3), which resembled what Moshfeghi5 described as re-active astrocytic hyperplasia. Other findings includ-ed familial exudative vitreoretinopathy (0.36%), congenital cataracts (0.13%), tortuosity and dila-tion of retina vessels (0.09%), persistent pupillary membrane (0.09%), neonatal conjunctivitis or dac-ryocystitis (0.07%), retinoblastoma (0.06%), and oc-ular albinism (0.06%). Other less commonly found abnormal findings included high cup/disc ratio, ab-normal retinal pigmentation (Figure 4), congenital anomalies of the disc, persistent fetal vasculature syndrome (PFVS), retina, choroid or macula dys-trophy, dermoid, microphthalmia, iris hemorrhage, Coats disease (Figure 5), iris defect, corneal opacity, neovascularization in angle (Figure 6), and anoph-thalmia.

The ocular complications associated with the screening program are listed in Table 3. Subcon-junctival hemorrhage was the most commonly noted ocular complication associated with the newborn eye screening program. These hemorrhages always reabsorbed within days without leaving any sequel-ae. The systemic complications associated with the screening program are listed in Table 4. Throwing up milk was the most commonly noted non-ocular complication associated with the screening program. These babies were screened 30 minutes later, and no other sequelae were found. Other complications in-cluded transient apnea and transient cyanosis. The screening procedures were stopped immediately in these newborns, who were then gently patted on their backs. Oxygen was given, and all of the pa-tients resumed crying with resolution of the cyano-sis. None of the cases had tachycardia or bradycardia requiring medical interventions, stopped breathing, or died after the eye screening examination.

Figure 4. Diffuse retinal pigmentation noted in the newborn eye screening program. Diffuse retinal pigmentation discovered in a full-term infant.

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DISCUSSION

Our results of almost 4 years involving 15,284 participants showed that a universal newborn eye screening program is an effective and safe procedure to identify the patients with ocular disorders at an earlier period. The most common ocular abnormal-ity was retinal hemorrhage, which accounted for 91% of all abnormalities. Potentially vision-threatening macula hemorrhage occurred in 3% of the patients when screened before 28 days of age, and a higher

likelihood of detecting retinal hemorrhage was ob-served when the screening was performed before 28 days of age. Overall, 2% of the patients were found to have ocular abnormalities other than retinal hemor-rhage. Of the ocular abnormalities not related to reti-nal hemorrhage, the most common were subretinal lipid or calcium deposition (0.61%), familial exuda-tive vitreoretinopathy (0.36%), congenital cataracts (0.13%), tortuosity and dilation of retina vessels (0.09%), and persistent pupillary membrane (0.09%).

Figure 5. A case of Coats disease before and after treatment. (A) Above, before treatment, tortuosity and aneurismal dilatation of retinal vessels and subretinal exudation was found in a newborn case of Coats disease. (B) Below, after treat-ment, tortuosity and dilation of reti-nal vessels were attenuated with a significant reduction in subretinal exudates.

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Life-threatening retinoblastoma was detected in nine cases (0.06%). No serious ocular or systemic compli-cations were noted in this study. Compared to the in-cidence of other disorders screened at the newborn period (phenylketonuria [1:25,000],6 hemoglobinopa-thies [1:575-4,243],7 hypothyroidism [1:1,700],6 cys-tic fibrosis [1:2,700],8 and hearing loss [1:500]),9 eye disease is more prevalent. According to the benefits and risks associated with perinatal eye examinations, this program may play a positive role in promoting pediatric eye health in healthy newborns.

The American Academy of Pediatrics, American Association for Pediatric Ophthalmology and Strabis-mus, and American Academy of Ophthalmology all recommend red reflex testing shortly after birth.10 Red reflex testing is a simple tool used to detect any ab-normal or asymmetric ocular reflex in newborns, with the aim of identifying ocular abnormalities at an early period. However, although such tests are important, with a reported specificity of 42% in detecting ocu-

lar pathology,11 they are primitive tests and fundi of the eyes are not checked directly, which means that small lesions such as macular hemorrhage, reti-noblastoma or familial exudative vitreoretinopathy may remain largely undetected.

The early identification of treatable ocular disor-ders such as congenital cataracts, glaucoma, occlu-sive persistent pupillary membrane, Coats disease, PFVS, or retinoblastoma can result in better visual outcomes and prevent serious visual complications in newborns. Furthermore, the early treatment of retinoblastoma can also be life-saving. The early identification of untreatable ocular disorders such as congenital anomalies of the disc can also prompt other associated neuro-imaging or endocrine inves-tigations to reduce the impact of poor and delayed developmental outcomes. The identification of other untreatable disorders such as microphthalmia can also prompt further genetic investigations.12,13 In ad-dition, one-third and one-half of affected individu-

Figure 6. Angle hemorrhage found during the newborn eye screening. Extensive angle hemorrhage noted in a full-term newborn by the RetCam imaging system.

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als have microphthalmia as part of a syndrome that affects other organs and tissues in the body. Early eye screening can thus lead to a more thorough in-vestigation of the systemic association, treatment, and perhaps rehabilitation to help promote the wel-fare of the patients.

Grade 1 or 2 retinal hemorrhage can be absorbed quickly without leaving a trace and causing no dis-cernible effect on visual development. Third-degree macular hemorrhage, however, can leave a long-term impact on vision.14,15 In this study, Grade 3 hemor-rhages accounted for 40% of all retinal hemorrhages.

TABLE 1

The Occurrence of Retinal Hemorrhage Screened Before and After 28 Days Screen Age Grade 1 or 2

Hemorrhage N (%)

Grade 3 Hemorrhage N (%)

Macular Hemorrhage N (%)

Optic Disc Hemorrhage N (%)

P Value

< 28 days (n = 14,786) 1,721 (12) 1,171 (8) 428 ( 3) 9 (0.06) < .001

> 28 days (n = 498) 6 (1) 1 (0.2) 1 (0.2) 0 (0)

TABLE 2

Ocular Abnormalities in 272 Cases Out of 15,284 Newborns Detected by the Eye Screening Program

Pathology Screened < 28 Days (n = 14,786)

Screened > 28 Days (n = 498)

Total Cases %

Subretinal lipid or calcium deposition 57 35 92 0.61

Familial exudative vitreoretinopathy 48 7 55 0.36

Congenital cataracts 11 9 20 0.13

Tortuosity and dilation of retina vessels 14 0 14 0.09

Persistent pupillary membrane 12 1 13 0.09

Neonatal conjunctivitis or dacryocystitis 11 0 11 0.07

Retinoblastoma 3 6 9 0.06

Ocular albinism 8 1 9 0.06

Enlarged cup/disc ratio 7 1 8 0.05

Abnormal retinal pigmentation 7 1 8 0.05

Congenital anomalies of disc 4 3 7 0.05

Persistent fetal vasculature syndrome 4 0 4 0.03

Retina, choroid, or macula dystrophy 2 2 4 0.03

Dermoid 2 1 3 0.02

Microphthalmia 3 0 3 0.02

Iris hemorrhage 3 0 3 0.02

Coats disease 1 1 2 0.01

Iris defect 1 1 2 0.01

Corneal leukoma 2 0 2 0.01

Neovascularization in angle 2 0 2 0.01

Anophthalmia 1 0 1 0.006

Total 203 69 272 2

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In addition, macular and disc hemorrhages accounted for 15% and 0.3% of the retinal hemorrhages, respec-tively. However, it is not known whether amblyopia diagnosed in some children was actually due to a macular hemorrhage in the perinatal stage. Long-term observational studies are needed to determine the im-pact of retinal hemorrhages on future visual outcomes and development in this group of children, and par-ticularly in those with macular hemorrhages detected during the ocular examination.

The RetCam digital imaging system provides high-quality and accurate data, with a capacity to compare and track disease over time, as well as the ability to transfer information between clinicians. As part of a comprehensive newborn health examination process, this imaging system may prove invaluable in discov-ering ocular pathology at an early stage. The result-ing images can also be sent digitally, making its use in telemedicine a possibility. The background data of these images taken during the neonatal stage can also provide useful information as a reference for cases of ocular pathology detected at school age or later. However, images of the peripheral retina can be less clear compared with the central part, and therefore if there is any doubt about the ocular findings, indirect ophthalmoscopic examinations with a retinal inden-tation or further examinations are suggested. Finally, although some doctors may be concerned about the

safety of this imaging technique for newborns, we found that it can be performed safely without causing major complications in full-term healthy newborns. It has also been used to screen retinopathy of prematu-rity in premature babies, and it has been shown to be useful and safe.16-18

There are some limitations of this study. First, the study was retrospective in nature. The collections of ocular as well as systemic complications might be un-derestimated because complications were not active-ly assessed in these patients. The reported compli-cations included only the ones which were actively reported to study team or as much as the study team was aware of. In addition, such newborn eye exami-nations may not be applicable for every child, and this is therefore a study limitation. Finally, we are unable to provide the data of the location of retinal hemorrhages within the fundus, which contained im-portant information related to the future prognosis of the patient.2 However, we are confident that our data are representative of the general population, because 83% of the newborns born in our hospital were in-cluded in this study. In addition, we included a large cohort (15,284 participants), and the study covered a span of 4 years.

Our newborn eye screening program involving 15,284 full-term newborns enabled us to detect hem-orrhage in the retina, macula, or optic disc in 2,899

TABLE 3

Ocular Complications Associated With the Newborn Screening ProgramComplications n %

Subconjunctival hemorrhage 4 0.03

Palpebral conjunctival hemorrhage 1 0.007

Corneal epithelial defect 0 0

Corneal opacity 0 0

TABLE 4

Systemic Complications Associated With the Newborn Eye Screening ProgramComplications n %

Throwing up milk 9 0.06

Transient apnea 8 0.05

Transient cyanosis 1 0.007

Tachycardia or bradycardia needing medical interventions 0 0

The need for intubation 0 0

Death 0 0

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cases (19%) and other ocular abnormalities in 272 cases (2%). Life-threatening retinoblastoma was de-tected in nine cases (0.06%). Most of the cases with ocular abnormalities were referred for treatment or further testing and are actively being followed up. The use of the RetCam system for newborn eye screening was safe, and only a few ocular and systemic compli-cations were associated with the program. Moving the timing of the initial eye examinations from preschool age to the perinatal period can help to identify impor-tant treatable and fatal ocular disorders at an earlier time point. However, further studies on perinatal eye screening programs are still needed to investigate the risks and benefits of such programs and to help better streamline the logistics associated with its implemen-tation. A cohort study of full-term babies with results stratified by varying Apgar score, and/or with evi-dence of systemic diseases may also be an important topic for future research.

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