DOI: 10.1542/Peds.2012-2996 ; Originally Published Online

Screening Examination of Premature Infants for Retinopathy of Prematurity AMERICAN ACADEMY OF PEDIATRICS Section on Ophthalmology, AMERICAN ACADEMY OF OPHTHALMOLOGY, AMERICAN ASSOCIATION FOR PEDIATRIC OPHTHALMOLOGY AND STRABISMUS and AMERICAN ASSOCIATION OF CERTIFIED ORTHOPTISTS Pediatrics 2013;131;189; originally published online December 31, 2012; DOI: 10.1542/peds.2012-2996

The online version of this article, along with updated information and services, is located on the World Wide Web at: http://pediatrics.aappublications.org/content/131/1/189.full.html

PEDIATRICS is the official journal of the American Academy of Pediatrics. A monthly publication, it has been published continuously since 1948. PEDIATRICS is owned, published, and trademarked by the American Academy of Pediatrics, 141 Northwest Point Boulevard, Elk Grove Village, Illinois, 60007. Copyright © 2013 by the American Academy of Pediatrics. All rights reserved. Print ISSN: 0031-4005. Online ISSN: 1098-4275.

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Organizational Principles to Guide and Deﬁne the Child Health Care System and/or Improve the Health of all Children

POLICY STATEMENT Screening Examination of Premature Infants for Retinopathy of Prematurity

AMERICAN ACADEMY OF PEDIATRICS Section on Ophthalmology, AMERICAN ACADEMY OF OPHTHALMOLOGY, abstract AMERICAN ASSOCIATION FOR PEDIATRIC OPHTHALMOLOGY This statement revises a previous statement on screening of preterm AND STRABISMUS, and AMERICAN ASSOCIATION OF CERTIFIED ORTHOPTISTS infants for retinopathy of prematurity (ROP) that was published in KEY WORDS 2006. ROP is a pathologic process that occurs only in immature retinal retinopathy of prematurity, preterm infants tissue and can progress to a tractional retinal detachment, which can ABBREVIATION result in functional or complete blindness. Use of peripheral retinal ROP—retinopathy of prematurity ablative therapy by using laser photocoagulation for nearly 2 decades This document is copyrighted and is property of the American has resulted in a high probability of markedly decreasing the incidence Academy of Pediatrics and its Board of Directors. All authors of this poor visual outcome, but the sequential nature of ROP creates fi fl have led con ict of interest statements with the American a requirement that at-risk preterm infants be examined at proper Academy of Pediatrics. Any conflicts have been resolved through a process approved by the Board of Directors. The American times and intervals to detect the changes of ROP before they become Academy of Pediatrics has neither solicited nor accepted any permanently destructive. This statement presents the attributes on commercial involvement in the development of the content of which an effective program for detecting and treating ROP could be this publication. based, including the timing of initial examination and subsequent reex- All policy statements from the American Academy of Pediatrics – automatically expire 5 years after publication unless reaffirmed, amination intervals. Pediatrics 2013;131:189 195 revised, or retired at or before that time.

INTRODUCTION Retinopathy of prematurity (ROP) is a disorder of the developing retina of low birth weight preterm infants that potentially leads to blindness in a small but significant percentage of those infants. In almost all term infants, the retina and retinal vasculature is fully developed, and ROP cannot occur; however, in preterm infants, the development of the retina, which proceeds from the optic nerve head anteriorly during the course of gestation, is incomplete, with the extent of the immaturity of www.pediatrics.org/cgi/doi/10.1542/peds.2012-2996 the retina depending mainly on the degree of prematurity at birth. doi:10.1542/peds.2012-2996 The Multicenter Trial of Cryotherapy for Retinopathy of Prematurity PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275). demonstrated the efficacy of peripheral retinal cryotherapy (ie, cry- Copyright © 2013 by the American Academy of Pediatrics oablation of the immature, avascular peripheral retina) in reducing unfavorable outcomes for threshold ROP, defined as morphologic changes beyond which the incidence of unfavorable outcome was >50%.1 The study’s 15-year follow-up report2 confirmed the following lasting benefits: unfavorable structural outcomes were reduced from 48% to 27%, and unfavorable visual outcomes (ie, best corrected visual acuity worse than 20/200) were reduced from 62% to 44%. Subsequently, laser photocoagulation has been used for peripheral retinal ablation with at least equal success and is now the preferred method of ablation.3–6 More recently, the Early Treatment for Reti- nopathy of Prematurity Randomized Trial confirmed the efficacy of

PEDIATRICS Volume 131, Number 1, January 2013 189 Downloaded from pediatrics.aappublications.org by guest on March 18, 2013 treatment of high-risk prethreshold lected infants with a birth weight infant’s postmenstrual age. The on- ROP and redefined the indications for between 1500 and 2000 g or gesta- set of serious ROP correlates better treatment.7 tional age of >30 weeks with an with postmenstrual age (gestational Because of the sequential nature of unstable clinical course, including age at birth plus chronologic age) ROP progression and the proven ben- those requiring cardiorespiratory than with postnatal age.11 That is, efits of timely treatment in reducing support and who are believed by the more preterm an infant is at the risk of visual loss, effective care their attending pediatrician or neo- birth, the longer the time to de- now requires that at-risk infants receive natologist to be at high risk for velop serious ROP. This knowledge carefully timed retinal examinations by ROP, should have retinal screening has been used previously in devel- an ophthalmologist who is experienced examinations performed after pu- oping a screening schedule.12,13 in the examination of preterm infants pillary dilation by using binocular Table 1 was developed from an for ROP using a binocular indirect indirect ophthalmoscopy with a lid evidence-based analysis of the Mul- ophthalmoscope on a scheduled basis speculum and scleral depression ticenter Trial of Cryotherapy for according to their gestational age at (as needed) to detect ROP. Dilating Retinopathy of Prematurity natural birth and their subsequent disease drops should be sufficient to allow history data and confirmed by the severity and that all pediatricians or any adequate examination of the fundi, Light Reduction in ROP Study, other primary care providers who care but care should be used in using which was conducted a decade for these at-risk preterm infants be multiple drops if the pupil fails to later.14 It represents a suggested aware of this schedule. dilate, because poor pupillary dila- schedule for the timing of the initial eye examinations based on This statement outlines the principles tion can occur in advanced ROP, postmenstrual age and chrono- on which a program to detect ROP in and administering multiple doses logic (postnatal) age to detect infants at risk might be based. The goal of dilating drops can adversely af- ROP before it becomes severe of an effective ROP screening program fect the systemic status of the in- enough to result in retinal detach- is to identify the infants who could fant. Sterile instruments should be ment while minimizing the number benefit from treatment and make ap- used to examine each infant to of potentially traumatic examina- propriate recommendations on the avoid possible cross-contamination tions.15 Although Table 1 provides timing of future screening and treat- of infectious agents. One examina- a schedule for detecting ROP po- ment interventions. Because un- tion is sufficientonlyifitunequivo- tentially damaging to the retina checked ROP can lead to permanent cally shows the retina to be fully with 99% confidence, it should be blindness, it is important that all at- vascularizedinbotheyes.Effort risk infants be screened in a timely may be made to minimize the dis- fashion, recognizing that not all infants comfort and systemic effect of this TABLE 1 Timing of First Eye Examination require treatment. On the basis of examination by pretreatment of the Based on Gestational Age at Birth information published thus far, the eyes with a topical anesthetic agent Gestational Age Age at Initial sponsoring organizations of this state- such as proparacaine; consideration at Birth, wk Examination, wk ment suggest the following guidelines also may be given to the use of pac- Postmenstrual Chronologic for the United States. It is important to ifiers, oral sucrose, and so forth. 22a 31 9 recognize that other world locations 23a 31 8 2. Retinal examinations in preterm 24 31 7 could have different screening param- infants should be performed by 25 31 6 eters.8,9 It is also important to note that an ophthalmologist who has suffi- 26 31 5 despite appropriate timing of exami- cient knowledge and experience to 27 31 4 nations and treatment, a small number 28 32 4 identify accurately the location and 29 33 4 of infants at risk progress to poor sequential retinal changes of ROP. 30 34 4 – outcomes.3 6 The International Classification of Older gestational 4 age, high-risk Retinopathy of Prematurity Revis- factorsb RECOMMENDATIONS 10 ited should be used to classify, Shown is a schedule for detecting prethreshold ROP with diagram, and record these retinal 99% confidence, usually before any required treatment. 1. Infants with a birth weight of a fi This guideline should be considered tentative rather ≤1500 g or gestational age of 30 ndings at the time of examination. than evidence-based for infants with a gestational age weeks or less (as defined by the of 22 to 23 wk because of the small number of survivors 3. The initiation of acute-phase ROP in these postmenstrual-age categories. attending neonatologist) and se- screening should be based on the b Consider timing based on severity of comorbidities.

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appreciated that infants born be- stage 3 ROP: zone II zone III retinal vascularization ’ fore 25 weeks gestational age the presence or suspected pres- attained without previous zone I should be considered for earlier ence of aggressive posterior ROP or II ROP (if there is examiner screening on the basis of severity doubt about the zone or if the post- of comorbidities (6 weeks’ chrono- 1- to 2-Week Follow-up menstrual age is less than 35 logic age, even if before 31 weeks’ fi weeks, con rmatory examinations postmenstrual age to enable ear- immature vascularization; poste- may be warranted); lier identification and treatment rior zone II full retinal vascularization in of aggressive posterior ROP [a se- stage 2 ROP: zone II close proximity to the ora ser- vere form of ROP that is charac- unequivocally regressing ROP: zone rata for 360°—that is, the nor- terized by rapid progression to I mal distance found in mature advanced stages in posterior ROP] retina between the end of vascu- that is more likely to occur in this 2-Week Follow-up larization and the ora serrata. extremely high-risk population). stage 1 ROP: zone II This criterion should be used 4. Follow-up examinations should be for all cases treated for ROP recommended by the examining immature vascularization: zone II —no ROP solely with bevacizumab; ophthalmologist on the basis of retinal findings classified accord- unequivocally regressing ROP: zone postmenstrual age of 50 weeks ing to the international classifica- II and no prethreshold disease (de- fi tion (see Fig 1).8 The following ned as stage 3 ROP in zone II, any schedule is suggested: 2- to 3-Week Follow-up ROP in zone I) or worse ROP is present; or stage 1 or 2 ROP: zone III regression of ROP16 (care must 1-Week or Less Follow-up regressing ROP: zone III be taken to be sure that there is 5. The conclusion of acute retinal no abnormal vascular tissue immature vascularization: zone I— screening examinations should present that is capable of reacti- no ROP be based on age and retinal oph- vation and progression in zone II immature retina extends into pos- thalmoscopic findings.13 Findings or III). terior zone II, near the boundary of that suggest that examinations 6. The use of digital photographic ret- zone I can be terminated include the inal images that are captured and stage 1 or 2 ROP: zone I following: sent for remote interpretation is a developing approach to ROP screening17,18; however, outcomes comparison between large-scale operational digital-imaging sys- tems with remote interpretation versus binocular indirect ophthalmoscopy have not been published. Nevertheless, some neonatal cen- ters are conducting remote ROP screening for infants still in the hospital.17 At a minimum, programs that employ this method should comply with the timing and other recommendations out- FIGURE 1 lined in the preceding guidelines. Scheme of retina of the right and left eyes showing zone borders and clock hours used to describe the location and extent of ROP. Diagrammatic representation of the potential total area of the premature Protocol modifications may be retina, with zone I (the most posterior) symmetrically surrounding the optic nerve head (the earliest required to allow for additional to 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 4 time for communication, pro- are usually recorded on a diagram such as this one. cessing, transportation, or other

PEDIATRICS Volume 131, Number 1, January 2013 191 Downloaded from pediatrics.aappublications.org by guest on March 18, 2013 logistical issues.19 Captured im- ROP care that includes off-site that refers to specific morphologic ages and their interpretation photographic interpretation re- features defined in the Multi- should be incorporated into the quires close collaboration among center Trial of Cryotherapy for Ret- permanent medical record. It is neonatologists, imaging staff, and inopathy of Prematurity, is no also recommended that indirect ophthalmologists. As with all longer the least severe ROP for ophthalmoscopy be performed ROP screening programs, spe- which intervention should be con- at least once by a qualified oph- cific responsibilities of each sidered. Threshold ROP, as defined thalmologist before treatment or individual must be carefully in the Multicenter Trial of Cryother- termination of acute phase delineated in a written protocol apy for Retinopathy of Prematurity screening of ROP for infants at in advance so that repeat study, is now included in type 1 fi risk for ROP. imaging and/or con rmatory ROP. Digital image capture (taking of examinations and required treat- Certain levels of high-risk prethres- photographs) requires skill, ex- ments can be performed without hold disease also respond better to delay. ablative treatment than observa- perience, practice, a broad un- tion. Special care must be used in derstanding of the infant eye, and Treatment determining the zone of disease. ideally, a knowledge of the path- The revised International Classifica- ophysiology of ROP (zone, stage, 7. The presence of plus disease (defined as abnormal dilation and tor- tion of Retinopathy of Prematurity and plus). Remote ROP graders fi tuosity of the posterior retinal Revisited classi cation gives spe- should have the same training fi blood vessels in 2 or more quad- ci c examples on how to identify requirements as bedside exam- zone I and zone II disease by using iners and a mentored experience rants of the retina meeting or ex- ceeding the degree of abnormality a 28-diopter lens with binocular in- in interpretation of digital images represented in reference photo- direct ophthalmoscopy. As noted for ROP. Interpretation requires graphs1,8; see below) in zones I or previously, the presence of plus dis- not only expert knowledge about II suggests that peripheral ablation, ease rather than the number of ROP but also understanding of the rather than observation, is appro- clock hours of disease may be the limitations of interpreting static priate.13 determining factor in recommend- images and the special care that Treatment should be initiated for ing ablative treatment. Treatment must be taken to schedule more the following retinal findings: should generally be accomplished, frequent imaging sessions that zone I ROP: any stage with plus when possible, within 72 hours of may be required because of those disease determination of treatable disease limitations. Remote interpreters to minimize the risk of retinal de- zone I ROP: stage 3—no plus dis- tachment. Follow-up is recommen- must provide clinical input on the ease timing of follow-up imaging ses- ded in 3 to 7 days after treatment zone II: stage 2 or 3 with plus sions and ophthalmoscopic to ensure that there is no need for disease examinations and appropriate additional treatment in areas where methodology, and these findings 8. Practitioners involved in the oph- ablative treatment was not com- need to be communicated in thalmologic care of preterm in- plete. 9. Recently published data22 indicate a manner that is compliant with fants should be aware that the retinal findings that require strong that intravitreal bevacizumab mo- rules of the Health Insurance consideration of ablative treatment notherapy, as compared with con- Portability and Accountability Act were revised according to the Early ventional laser therapy, in infants (HIPAA). Treatment of Retinopathy of Prema- with stage 3+ ROP showed a signif- Digital retinal imaging may also turity Randomized Trial study.7 This icant benefit for zone I but not be a useful tool for objective recommendation is based on the zone II disease. Development of documentation of retinal findings findings of improved visual out- normal-appearing peripheral reti- and for teaching NICU staff and comes with earlier treatment rec- nal vessels continued after treat- parents about examination ommended by the Final Visual ment with intravitreal bevacizumab, results, even if it is not the pri- Acuity Results in the Early Treat- but conventional laser therapy mary method used for ROP ment of Retinopathy of Prematurity led to apparent permanent de- screening in the NICU.20 Study.21 “Threshold ROP,” a term struction of the peripheral retina,

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although published studies indi- visual outcome develops. Docu- expertise in examination of pre- cate that this apparent destruction mentation of such conversations term infants for ROP can be wasassociatedwithonlyamodest with parents in the nurse or phy- arranged at the appropriate time visual field loss. This trial was too sician notes is highly recommen- at the receiving facility or on an small to assess safety and effects ded, along with the use of outpatient basis if discharge is on future development of brain standardized parental educa- contemplated before the need for and other tissues. Consideration tional materials. continued examination has ceased, may be given to treatment of 11. Responsibility for examination and as outlined in Diagnosis Recommen- infants with zone I, stage 3+ ROP follow-up of infants at risk for ROP dation 6. If responsibility for with intravitreal injection of beva- must be carefully defined by the arranging follow-up ophthalmo- cizumab; however, bevacizumab is staff and consultants of each NICU. logic care after discharge is del- not approved by the US Food and Unit-specific criteria with respect egated to the parents, they must Drug Administration for the treat- to birth weight and gestational be made to understand the po- ment of ROP. If intravitreal injec- age for examination for ROP tential for severe visual loss, in- tion of bevacizumab for zone should be established for each cluding blindness; that there is I stage 3+ ROP is contemplated, NICU by consultation and agree- a critical examination time sched- it is essential that treatment be ment between neonatology and ule to be met if treatment is to be administered only after obtaining ophthalmology services. These cri- successful; and that timely follow- a detailed informed consent, be- teria should be recorded and up examination is essential to suc- cause there remain unanswered should automatically trigger oph- cessful treatment. This information questions involving dosage, timing, thalmologic examinations. If hos- should be communicated both ver- safety, visual outcomes, and other pital discharge or transfer to bally and in writing and should be long-term effects. Infants treated another neonatal unit or hospital carefully documented in the infant’s with bevacizumab injection should is contemplated before retinal de- medical record. If such arrange- be monitored weekly after injec- velopment into anterior zone III ments for communication and tion by using techniques in accord has taken place or if the infant follow-up after transfer or dis- with these published ROP examina- has been treated by ablation for charge cannot be made, the infant tion guidelines until retinal vascular- ROP and there is either incomplete should not be transferred or dis- ization is completed. Because in the regression or incomplete retinal charged until appropriate follow- BEAT-ROP study,22 recurrence of ROP healing, the availability of appro- up examination can be arranged after bevacizumab injection tended priate follow-up ophthalmologic by the unit staff who are discharg- to occur considerably later than examination must be ensured, ing the infant. that after conventional laser periph- and specific arrangement for that Regardless of whether infants at eral retinal ablative treatment (16 ± examination must be made before risk develop ROP requiring treat- 4.6 weeks vs 6.2 ± 5.7 weeks), lon- such discharge or transfer occurs. ment, pediatricians and other ger follow-up is required for infants The transferring primary care physicians who care for infants treated with bevacizumab to ensure physician, after communication who have had ROP should be aware that ROP requiring treatment does with the examining ophthalmolo- that these infants are at risk for not recur. gist, should have the responsibility other seemingly unrelated visual 10. Communication with parents by for communicating to the infant’s disorders, such as strabismus, am- members of the care team is new primary care physician what blyopia, high refractive errors, cata- very important, as is documenta- eye examinations are needed and ract, and so forth. Ophthalmologic tion of those communications. their required timing. The new follow-up for these potential prob- Parents should be aware of ROP primary care physician should as- lems after discharge from the NICU examinations and should be in- certain the current ocular exami- is indicated within 4 to 6 months formed if their child has ROP, nation status of the infant by after discharge. with subsequent updates on reviewing the record and commu- This statement replaces the previous ROP progression. The possible nicating with the transferring phy- statement on ROP from the Ameri- consequences of serious ROP sician so that any necessary can Academy of Pediatrics, Ameri- should be discussed at the time examinations by an ophthalmolo- can Academy of Ophthalmology, and that a significant risk of poor gist with ongoing experience and American Association for Pediatric

PEDIATRICS Volume 131, Number 1, January 2013 193 Downloaded from pediatrics.aappublications.org by guest on March 18, 2013 Ophthalmology and Strabismus23; ROP James Reynolds, MD Christie L. Morse, MD – American Association of care is evolving, and recommen- Michael F. Chiang, MD Pediatric Ophthalmology and Strabismus, ﬁ American Academy of Ophthalmology dations may be modi ed as additional George S. Ellis Jr, MD – American Academy of data about ROP risk factors, treat- EXECUTIVE COMMITTEE, AMERICAN Ophthalmology Council ments, and long-term outcomes are ACADEMY OF PEDIATRICS, SECTION ON OPHTHALMOLOGY, 2011–2012 published. James B. Ruben, MD, Chairperson STAFF LEAD AUTHOR David B. Granet, MD, Chairperson-Elect Jennifer G. Riefe, MEd Richard J. Blocker, MD Walter M. Fierson, MD Geoffrey E. Bradford, MD AMERICAN ACADEMY OF SUBCOMMITTEE ON RETINOPATHY OF Daniel J. Karr, MD Gregg T. Lueder, MD, Immediate Past OPHTHALMOLOGY PREMATURITY, AMERICAN ACADEMY Chairperson OF PEDIATRICS, SECTION ON Sharon S. Lehman, MD OPHTHALMOLOGY, 2007–2011 AMERICAN ASSOCIATION FOR R. Michael Siatkowski, MD PEDIATRIC OPHTHALMOLOGY AND Walter M. Fierson, MD, Chairperson STRABISMUS Richard A. Saunders, MD William Good, MD LIAISONS Earl A. Palmer, MD Kyle A. Arnoldi, CO – American Association of AMERICAN ASSOCIATION OF Dale Phelps, MD Certiﬁed Orthoptists CERTIFIED ORTHOPTISTS

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References This article cites 21 articles, 2 of which can be accessed free at: http://pediatrics.aappublications.org/content/131/1/189.full.ht ml#ref-list-1 Subspecialty Collections This article, along with others on similar topics, appears in the following collection(s): Section on Ophthalmology http://pediatrics.aappublications.org/cgi/collection/section_on _ophthalmology Ophthalmology http://pediatrics.aappublications.org/cgi/collection/ophthalmo logy Permissions & Licensing Information about reproducing this article in parts (figures, tables) or in its entirety can be found online at: http://pediatrics.aappublications.org/site/misc/Permissions.xh tml Reprints Information about ordering reprints can be found online: http://pediatrics.aappublications.org/site/misc/reprints.xhtml

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