screening examination of premature infants for retinopathy of prematurity

POLICY STATEMENT

Screening Examination of Premature Infants forRetinopathy of Prematurity

abstractThis statement revises a previous statement on screening of preterminfants for retinopathy of prematurity (ROP) that was published in2006. ROP is a pathologic process that occurs only in immature retinaltissue and can progress to a tractional retinal detachment, which canresult in functional or complete blindness. Use of peripheral retinalablative therapy by using laser photocoagulation for nearly 2 decadeshas resulted in a high probability of markedly decreasing the incidenceof this poor visual outcome, but the sequential nature of ROP createsa requirement that at-risk preterm infants be examined at propertimes and intervals to detect the changes of ROP before they becomepermanently destructive. This statement presents the attributes onwhich an effective program for detecting and treating ROP could bebased, including the timing of initial examination and subsequent reex-amination intervals. Pediatrics 2013;131:189195

INTRODUCTION

Retinopathy of prematurity (ROP) is a disorder of the developing retinaof low birth weight preterm infants that potentially leads to blindnessin a small but signicant percentage of those infants. In almost all terminfants, the retina and retinal vasculature is fully developed, and ROPcannot occur; however, in preterm infants, the development of theretina, which proceeds from the optic nerve head anteriorly during thecourse of gestation, is incomplete, with the extent of the immaturity ofthe retina depending mainly on the degree of prematurity at birth.

The Multicenter Trial of Cryotherapy for Retinopathy of Prematuritydemonstrated the efcacy of peripheral retinal cryotherapy (ie, cry-oablation of the immature, avascular peripheral retina) in reducingunfavorable outcomes for threshold ROP, dened as morphologicchanges beyond which the incidence of unfavorable outcome was>50%.1 The studys 15-year follow-up report2 conrmed the followinglasting benets: unfavorable structural outcomes were reduced from48% to 27%, and unfavorable visual outcomes (ie, best corrected vi-sual acuity worse than 20/200) were reduced from 62% to 44%.Subsequently, laser photocoagulation has been used for peripheralretinal ablation with at least equal success and is now the preferredmethod of ablation.36 More recently, the Early Treatment for Reti-nopathy of Prematurity Randomized Trial conrmed the efcacy of

AMERICAN ACADEMY OF PEDIATRICS Section onOphthalmology, AMERICAN ACADEMY OF OPHTHALMOLOGY,AMERICAN ASSOCIATION FOR PEDIATRIC OPHTHALMOLOGYAND STRABISMUS, and AMERICAN ASSOCIATION OFCERTIFIED ORTHOPTISTS

KEY WORDSretinopathy of prematurity, preterm infants

ABBREVIATIONROPretinopathy of prematurity

This document is copyrighted and is property of the AmericanAcademy of Pediatrics and its Board of Directors. All authorshave led conict of interest statements with the AmericanAcademy of Pediatrics. Any conicts have been resolved througha process approved by the Board of Directors. The AmericanAcademy of Pediatrics has neither solicited nor accepted anycommercial involvement in the development of the content ofthis publication.

All policy statements from the American Academy of Pediatricsautomatically expire 5 years after publication unless reafrmed,revised, or retired at or before that time.

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PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275).

Copyright 2013 by the American Academy of Pediatrics

PEDIATRICS Volume 131, Number 1, January 2013 189

FROM THE AMERICAN ACADEMY OF PEDIATRICS

Organizational Principles to Guide and Dene the ChildHealth Care System and/or Improve the Health of all Children

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treatment of high-risk prethresholdROP and redened the indications fortreatment.7

Because of the sequential nature ofROP progression and the proven ben-ets of timely treatment in reducingthe risk of visual loss, effective carenow requires that at-risk infants receivecarefully timed retinal examinations byan ophthalmologist who is experiencedin the examination of preterm infantsfor ROP using a binocular indirectophthalmoscope on a scheduled basisaccording to their gestational age atbirth and their subsequent diseaseseverity and that all pediatricians or anyother primary care providers who carefor these at-risk preterm infants beaware of this schedule.

This statement outlines the principleson which a program to detect ROP ininfants at risk might be based. The goalof an effective ROP screening programis to identify the infants who couldbenet from treatment and make ap-propriate recommendations on thetiming of future screening and treat-ment interventions. Because un-checked ROP can lead to permanentblindness, it is important that all at-risk infants be screened in a timelyfashion, recognizing that not all infantsrequire treatment. On the basis ofinformation published thus far, thesponsoring organizations of this state-ment suggest the following guidelinesfor the United States. It is important torecognize that other world locationscould have different screening param-eters.8,9 It is also important to note thatdespite appropriate timing of exami-nations and treatment, a small numberof infants at risk progress to pooroutcomes.36

RECOMMENDATIONS

1. Infants with a birth weight of1500 g or gestational age of 30weeks or less (as dened by theattending neonatologist) and se-

lected infants with a birth weightbetween 1500 and 2000 g or gesta-tional age of >30 weeks with anunstable clinical course, includingthose requiring cardiorespiratorysupport and who are believed bytheir attending pediatrician or neo-natologist to be at high risk forROP, should have retinal screeningexaminations performed after pu-pillary dilation by using binocularindirect ophthalmoscopy with a lidspeculum and scleral depression(as needed) to detect ROP. Dilatingdrops should be sufcient to allowadequate examination of the fundi,but care should be used in usingmultiple drops if the pupil fails todilate, because poor pupillary dila-tion can occur in advanced ROP,and administering multiple dosesof dilating drops can adversely af-fect the systemic status of the in-fant. Sterile instruments should beused to examine each infant toavoid possible cross-contaminationof infectious agents. One examina-tion is sufcient only if it unequivo-cally shows the retina to be fullyvascularized in both eyes. Effortmay be made to minimize the dis-comfort and systemic effect of thisexamination by pretreatment of theeyes with a topical anesthetic agentsuch as proparacaine; considerationalso may be given to the use of pac-iers, oral sucrose, and so forth.

2. Retinal examinations in preterminfants should be performed byan ophthalmologist who has suf-cient knowledge and experience toidentify accurately the location andsequential retinal changes of ROP.The International Classication ofRetinopathy of Prematurity Revis-ited10 should be used to classify,diagram, and record these retinalndings at the time of examination.

3. The initiation of acute-phase ROPscreening should be based on the

infants postmenstrual age. The on-set of serious ROP correlates betterwith postmenstrual age (gestationalage at birth plus chronologic age)than with postnatal age.11 That is,the more preterm an infant is atbirth, the longer the time to de-velop serious ROP. This knowledgehas been used previously in devel-oping a screening schedule.12,13

Table 1 was developed from anevidence-based analysis of the Mul-ticenter Trial of Cryotherapy forRetinopathy of Prematurity naturalhistory data and conrmed by theLight Reduction in ROP Study,which was conducted a decadelater.14 It represents a suggestedschedule for the timing of the ini-tial eye examinations based onpostmenstrual age and chrono-logic (postnatal) age to detectROP before it becomes severeenough to result in retinal detach-ment while minimizing the numberof potentially traumatic examina-tions.15 Although Table 1 providesa schedule for detecting ROP po-tentially damaging to the retinawith 99% condence, it should be

TABLE 1 Timing of First Eye ExaminationBased on Gestational Age at Birth

Gestational Ageat Birth, wk

Age at InitialExamination, wk

Postmenstrual Chronologic

22a 31 923a 31 824 31 725 31 626 31 527 31 428 32 429 33 430 34 4

Older gestationalage, high-riskfactorsb

4

Shown is a schedule for detecting prethreshold ROP with99% condence, usually before any required treatment.a This guideline should be considered tentative ratherthan evidence-based for infants with a gestational ageof 22 to 23 wk because of the small number of survivorsin these postmenstrual-age categories.b Consider timing based on severity of comorbidities.

190 FROM THE AMERICAN ACADEMY OF PEDIATRICS at West Virginia Univ Lib on March 11, 2015pediatrics.aappublications.orgDownloaded from

appreciated that infants born be-fore 25 weeks gestational ageshould be considered for earlierscreening on the basis of severityof comorbidities (6 weeks chrono-logic age, even if before 31 weekspostmenstrual age to enable ear-lier identication and treatmentof aggressive posterior ROP [a se-vere form of ROP that is charac-terized by rapid progression toadvanced stages in posterior ROP]that is more likely to occur in thisextremely high-risk population).

4. Follow-up examinations should berecommended by the examiningophthalmologist on the basis ofretinal ndings classied accord-ing to the international classica-tion (see Fig 1).8 The followingschedule is suggested:

1-Week or Less Follow-up

immature vascularization: zone Ino ROP

immature retina extends into pos-terior zone II, near the boundary ofzone I

stage 1 or 2 ROP: zone I

stage 3 ROP: zone II the presence or suspected pres-

ence of aggressive posterior ROP

1- to 2-Week Follow-up

immature vascularization; poste-rior zone II

stage 2 ROP: zone II unequivocally regressing ROP: zone

I

2-Week Follow-up

stage 1 ROP: zone II immature vascularization: zone II

no ROP

unequivocally regressing ROP: zoneII

2- to 3-Week Follow-up

stage 1 or 2 ROP: zone III regressing ROP: zone III

5. The conclusion of acute retinalscreening examinations shouldbe based on age and retinal oph-thalmoscopic ndings.13 Findingsthat suggest that examinationscan be terminated include thefollowing:

zone III retinal vascularizationattained without previous zone Ior II ROP (if there is examinerdoubt about the zone or if the post-menstrual age is less than 35weeks, conrmatory examinationsmay be warranted);

full retinal vascularization inclose proximity to the ora ser-rata for 360that is, the nor-mal distance found in matureretina between the end of vascu-larization and the ora serrata.This criterion should be usedfor all cases treated for ROPsolely with bevacizumab;

postmenstrual age of 50 weeksand no prethreshold disease (de-ned as stage 3 ROP in zone II, anyROP in zone I) or worse ROP ispresent; or

regression of ROP16 (care mustbe taken to be sure that there isno abnormal vascular tissuepresent that is capable of reacti-vation and progression in zone IIor III).

6. The use of digital photographic ret-inal images that are captured andsent for remote interpretation isa developing approach to ROPscreening17,18; however, outcomescomparison between large-scaleoperational digital-imaging sys-tems with remote interpretationversus binocular indirect ophthal-moscopy have not been published.Nevertheless, some neonatal cen-ters are conducting remote ROPscreening for infants still inthe hospital.17 At a minimum, pro-grams that employ this methodshould comply with the timingand other recommendations out-lined in the preceding guidelines.Protocol modications may berequired to allow for additionaltime for communication, pro-cessing, transportation, or other

FIGURE 1Scheme of retina of the right and left eyes showing zone borders and clock hours used to describe thelocation and extent of ROP. Diagrammatic representation of the potential total area of the prematureretina, with zone I (the most posterior) symmetrically surrounding the optic nerve head (the earliestto develop). A larger retinal area is present temporally (laterally) rather than nasally (medially)(zone III). Only zones I and II are present nasally. The retinal changes discussed in recommendation 4are usually recorded on a diagram such as this one.




logistical issues.19 Captured im-ages and their interpretationshould be incorporated into thepermanent medical record. It isalso recommended that indirectophthalmoscopy be performedat least once by a qualied oph-thalmologist before treatment ortermination of acute phasescreening of ROP for infants atrisk for ROP.Digital image capture (taking ofphotographs) requires skill, ex-perience, practice, a broad un-derstanding of the infant eye, andideally, a knowledge of the path-ophysiology of ROP (zone, stage,and plus). Remote ROP gradersshould have the same trainingrequirements as bedside exam-iners and a mentored experiencein interpretation of digital imagesfor ROP. Interpretation requiresnot only expert knowledge aboutROP but also understanding of thelimitations of interpreting staticimages and the special care thatmust be taken to schedule morefrequent imaging sessions thatmay be required because of thoselimitations. Remote interpretersmust provide clinical input on thetiming of follow-up imaging ses-sions and ophthalmoscopicexaminations and appropriatemethodology, and these ndingsneed to be communicated ina manner that is compliant withrules of the Health InsurancePortability and Accountability Act(HIPAA).

Digital retinal imaging may alsobe a useful tool for objectivedocumentation of retinal ndingsand for teaching NICU staff andparents about examinationresults, even if it is not the pri-mary method used for ROPscreening in the NICU.20

ROP care that includes off-sitephotographic interpretation re-quires close collaboration amongneonatologists, imaging staff, andophthalmologists. As with allROP screening programs, spe-cic responsibilities of eachindividual must be carefullydelineated in a written protocolin advance so that repeatimaging and/or conrmatoryexaminations and required treat-ments can be performed withoutdelay.

Treatment

7. The presence of plus disease (de-ned as abnormal dilation and tor-tuosity of the posterior retinalblood vessels in 2 or more quad-rants of the retina meeting or ex-ceeding the degree of abnormalityrepresented in reference photo-graphs1,8; see below) in zones I orII suggests that peripheral ablation,rather than observation, is appro-priate.13

Treatment should be initiated forthe following retinal ndings: zone I ROP: any stage with plus

disease

zone I ROP: stage 3no plus dis-ease

zone II: stage 2 or 3 with plusdisease

8. Practitioners involved in the oph-thalmologic care of preterm in-fants should be aware that theretinal ndings that require strongconsideration of ablative treatmentwere revised according to the EarlyTreatment of Retinopathy of Prema-turity Randomized Trial study.7 Thisrecommendation is based on thendings of improved visual out-comes with earlier treatment rec-ommended by the Final VisualAcuity Results in the Early Treat-ment of Retinopathy of PrematurityStudy.21 Threshold ROP, a term

that refers to specic morphologicfeatures dened in the Multi-center Trial of Cryotherapy for Ret-inopathy of Prematurity, is nolonger the least severe ROP forwhich intervention should be con-sidered. Threshold ROP, as denedin the Multicenter Trial of Cryother-apy for Retinopathy of Prematuritystudy, is now included in type 1ROP.Certain levels of high-risk prethres-hold disease also respond better toablative treatment than observa-tion. Special care must be used indetermining the zone of disease.The revised International Classica-tion of Retinopathy of PrematurityRevisited classication gives spe-cic examples on how to identifyzone I and zone II disease by usinga 28-diopter lens with binocular in-direct ophthalmoscopy. As notedpreviously, the presence of plus dis-ease rather than the number ofclock hours of disease may be thedetermining factor in recommend-ing ablative treatment. Treatmentshould generally be accomplished,when possible, within 72 hours ofdetermination of treatable diseaseto minimize the risk of retinal de-tachment. Follow-up is recommen-ded in 3 to 7 days after treatmentto ensure that there is no need foradditional treatment in areas whereablative treatment was not com-plete.

9. Recently published data22 indicatethat intravitreal bevacizumab mo-notherapy, as compared with con-ventional laser therapy, in infantswith stage 3+ ROP showed a signif-icant benet for zone I but notzone II disease. Development ofnormal-appearing peripheral reti-nal vessels continued after treat-ment with intravitreal bevacizumab,but conventional laser therapyled to apparent permanent de-struction of the peripheral retina,


although published studies indi-cate that this apparent destructionwas associated with only a modestvisual eld loss. This trial was toosmall to assess safety and effectson future development of brainand other tissues. Considerationmay be given to treatment ofinfants with zone I, stage 3+ ROPwith intravitreal injection of beva-cizumab; however, bevacizumab isnot approved by the US Food andDrug Administration for the treat-ment of ROP. If intravitreal injec-tion of bevacizumab for zoneI stage 3+ ROP is contemplated,it is essential that treatment beadministered only after obtaininga detailed informed consent, be-cause there remain unansweredquestions involving dosage, timing,safety, visual outcomes, and otherlong-term effects. Infants treatedwith bevacizumab injection shouldbe monitored weekly after injec-tion by using techniques in accordwith these published ROP examina-tion guidelines until retinal vascular-ization is completed. Because in theBEAT-ROP study,22 recurrence of ROPafter bevacizumab injection tendedto occur considerably later thanthat after conventional laser periph-eral retinal ablative treatment (16 4.6 weeks vs 6.2 5.7 weeks), lon-ger follow-up is required for infantstreated with bevacizumab to ensurethat ROP requiring treatment doesnot recur.

10. Communication with parents bymembers of the care team isvery important, as is documenta-tion of those communications.Parents should be aware of ROPexaminations and should be in-formed if their child has ROP,with subsequent updates onROP progression. The possibleconsequences of serious ROPshould be discussed at the timethat a signicant risk of poor

visual outcome develops. Docu-mentation of such conversationswith parents in the nurse or phy-sician notes is highly recommen-ded, along with the use ofstandardized parental educa-tional materials.

11. Responsibility for examination andfollow-up of infants at risk for ROPmust be carefully dened by thestaff and consultants of each NICU.Unit-specic criteria with respectto birth weight and gestationalage for examination for ROPshould be established for eachNICU by consultation and agree-ment between neonatology andophthalmology services. These cri-teria should be recorded andshould automatically trigger oph-thalmologic examinations. If hos-pital discharge or transfer toanother neonatal unit or hospitalis contemplated before retinal de-velopment into anterior zone IIIhas taken place or if the infanthas been treated by ablation forROP and there is either incompleteregression or incomplete retinalhealing, the availability of appro-priate follow-up ophthalmologicexamination must be ensured,and specic arrangement for thatexamination must be made beforesuch discharge or transfer occurs.The transferring primary carephysician, after communicationwith the examining ophthalmolo-gist, should have the responsibilityfor communicating to the infantsnew primary care physician whateye examinations are needed andtheir required timing. The newprimary care physician should as-certain the current ocular exami-nation status of the infant byreviewing the record and commu-nicating with the transferring phy-sician so that any necessaryexaminations by an ophthalmolo-gist with ongoing experience and

expertise in examination of pre-term infants for ROP can bearranged at the appropriate timeat the receiving facility or on anoutpatient basis if discharge iscontemplated before the need forcontinued examination has ceased,as outlined in Diagnosis Recommen-dation 6. If responsibility forarranging follow-up ophthalmo-logic care after discharge is del-egated to the parents, they mustbe made to understand the po-tential for severe visual loss, in-cluding blindness; that there isa critical examination time sched-ule to be met if treatment is to besuccessful; and that timely follow-up examination is essential to suc-cessful treatment. This informationshould be communicated both ver-bally and in writing and should becarefully documented in the infantsmedical record. If such arrange-ments for communication andfollow-up after transfer or dis-charge cannot be made, the infantshould not be transferred or dis-charged until appropriate follow-up examination can be arrangedby the unit staff who are discharg-ing the infant.Regardless of whether infants atrisk develop ROP requiring treat-ment, pediatricians and otherphysicians who care for infantswho have had ROP should be awarethat these infants are at risk forother seemingly unrelated visualdisorders, such as strabismus, am-blyopia, high refractive errors, cata-ract, and so forth. Ophthalmologicfollow-up for these potential prob-lems after discharge from the NICUis indicated within 4 to 6 monthsafter discharge.

This statement replaces the previousstatement on ROP from the Ameri-can Academy of Pediatrics, Ameri-can Academy of Ophthalmology, andAmerican Association for Pediatric




Ophthalmology and Strabismus23; ROPcare is evolving, and recommen-dations may be modied as additionaldata about ROP risk factors, treat-ments, and long-term outcomes arepublished.

LEAD AUTHORWalter M. Fierson, MD

SUBCOMMITTEE ON RETINOPATHY OFPREMATURITY, AMERICAN ACADEMYOF PEDIATRICS, SECTION ONOPHTHALMOLOGY, 20072011Walter M. Fierson, MD, ChairpersonRichard A. Saunders, MDWilliam Good, MDEarl A. Palmer, MDDale Phelps, MD

James Reynolds, MDMichael F. Chiang, MD

EXECUTIVE COMMITTEE, AMERICANACADEMY OF PEDIATRICS, SECTIONON OPHTHALMOLOGY, 20112012James B. Ruben, MD, ChairpersonDavid B. Granet, MD, Chairperson-ElectRichard J. Blocker, MDGeoffrey E. Bradford, MDDaniel J. Karr, MDGregg T. Lueder, MD, Immediate PastChairpersonSharon S. Lehman, MDR. Michael Siatkowski, MD

LIAISONSKyle A. Arnoldi, CO American Association ofCertied Orthoptists

Christie L. Morse, MD American Association ofPediatric Ophthalmology and Strabismus,American Academy of OphthalmologyGeorge S. Ellis Jr, MD American Academy ofOphthalmology Council

STAFFJennifer G. Riefe, MEd

AMERICAN ACADEMY OFOPHTHALMOLOGY

AMERICAN ASSOCIATION FORPEDIATRIC OPHTHALMOLOGY ANDSTRABISMUS

AMERICAN ASSOCIATION OFCERTIFIED ORTHOPTISTS

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