Journal of Pediatric Ophthalmology and Strabismus

Original Article 

Persistent Avascular Retina in Infants With a History of Type 2 Retinopathy of Prematurity: To Treat or Not to Treat?

Rasha Al-Taie, FRCSI, FRANZCO; Samantha K. Simkin, PhD; Erica Douçet, MD, FRCSC; Shuan Dai, MBBS, MSc, FRANZCO

Abstract

Purpose:

To investigate persistent avascular retina in infants with type 2 retinopathy of permaturity (ROP) that persisted after 45 weeks' post-menstrual age when regular ROP screening ceased.

Methods:

A prospective observational study where fundus fluorescein angiography (FFA) was completed on consecutive infants who had a history of type 2 ROP and avascular retina during ROP screening that persisted after 45 weeks' post-menstrual age.

Results:

FFA was completed on 72 eyes of 36 infants (53% male), with a mean gestational age of 26.0 ± 2.2 weeks and a mean birth weight of 834.6 ± 216.3 grams. The mean age at discharge from ROP screening was 47.6 weeks' post-menstrual age. All patients had type 2 ROP at the worst stage of their disease, with predominantly stage 2 disease. FFA was performed at a mean age of 18.8 ± 10.3 months post-menstrual age. All patients had detectable avascular retina in peripheral zone II or III on FFA. Peripheral vessel leakage was present in 3 eyes of 2 infants (5.5%), who both subsequently received peripheral laser treatment.

Conclusions:

Premature infants with type 2 ROP may have persistent peripheral avascular retina with unknown long-term ocular complications, which can present management dilemmas. Retinal FFA is recommended to determine retinal ischemia and aid decision making for treatment in these cases.

[J Pediatr Ophthalmol Strabismus. 2019;56(4):222–228.]

Abstract

Purpose:

To investigate persistent avascular retina in infants with type 2 retinopathy of permaturity (ROP) that persisted after 45 weeks' post-menstrual age when regular ROP screening ceased.

Methods:

A prospective observational study where fundus fluorescein angiography (FFA) was completed on consecutive infants who had a history of type 2 ROP and avascular retina during ROP screening that persisted after 45 weeks' post-menstrual age.

Results:

FFA was completed on 72 eyes of 36 infants (53% male), with a mean gestational age of 26.0 ± 2.2 weeks and a mean birth weight of 834.6 ± 216.3 grams. The mean age at discharge from ROP screening was 47.6 weeks' post-menstrual age. All patients had type 2 ROP at the worst stage of their disease, with predominantly stage 2 disease. FFA was performed at a mean age of 18.8 ± 10.3 months post-menstrual age. All patients had detectable avascular retina in peripheral zone II or III on FFA. Peripheral vessel leakage was present in 3 eyes of 2 infants (5.5%), who both subsequently received peripheral laser treatment.

Conclusions:

Premature infants with type 2 ROP may have persistent peripheral avascular retina with unknown long-term ocular complications, which can present management dilemmas. Retinal FFA is recommended to determine retinal ischemia and aid decision making for treatment in these cases.

[J Pediatr Ophthalmol Strabismus. 2019;56(4):222–228.]

Introduction

Retinopathy of prematurity (ROP) is a vasoproliferative disorder affecting the retinas of premature and low–birth-weight infants.1 ROP is one of the leading causes of preventable childhood blindness throughout the world.2 Both the Cryotherapy for ROP (CRYO-ROP) and the Early Teatment for ROP (ETROP) studies have well-defined treatment guidelines for high-risk ROP cases, such as those with threshold disease (five consecutive clock hours or eight cumulative clock hours of stage 3 with plus disease in zone I or II) or type 1 ROP (zone II stage 2 or 3 ROP with plus disease, zone I any stage ROP with plus disease, or zone I stage 3 ROP without plus disease).2–4 Infants who develop type 2 ROP (zone I stage 1 or 2 ROP without plus disease or zone II stage 3 ROP without plus disease) as defined by the ETROP study are recommended for continued screening until resolution of ROP, a post-menstrual age of 45 weeks, or complete vascularization.2,3 However, patients with avascular retina that persists after 45 weeks' post-menstrual age fall outside clear management guidelines. Infants with persistent avascular retina have unknown long-term structural and functional risks, and theoretically could develop disease requiring treatment, including retinal breaks or tractional bands. Literature is scarce on the appropriate treatment of patients who do not fit within existing treatment criteria but pose significant concern to clinicians. Decisions regarding treatment of these infants are often based on the consulting ophthalmologist's clinical judgment rather than established guidelines or management consensus. Treatment options may vary from observation to retinal laser photocoagulation.

Therefore, we evaluated the retinal vasculature features of infants with type 2 ROP who had persistent peripheral avascular retina after 45 weeks' post-menstrual age with fundus fluorescein angiography (FFA) and wide-field retinal imaging to provide useful information for evidence-based decision making in the treatment of such patients.

Patients and Methods

The current study was an observational prospective study of consecutive cases of infants with type 2 ROP and persistent avascular retina after 45 weeks' post-menstrual age who underwent a fundus fluorescein examination. All infants included in the study received ROP screening following the New Zealand ROP screening guidelines.5 Parental consent was obtained for all patients. Children were excluded from the study if they were deemed systemically unstable for general anesthesia or had an ocular comorbidity. The study was approved by the local hospitals' research committees and followed the tenets of the Declaration of Helsinki.

A complete ocular examination under anesthesia was completed for each participant. Adequate pupil dilatation was achieved with topical 1.0% tropicamide and 2.5% phenylephrine (Bausch & Lomb, Rochester, NY). The ocular examination included portable slit-lamp biomicroscopy, optical coherence tomography of the macula with the Envisu C2300 system (Leica Microsystems GmbH, Wetzlar, Germany), and retinal photography and FFA with the RetCam digital imaging system (Clarity Medical Systems, Inc., Pleasanton, CA).

FFA was completed via an intravenous bolus injection of 10% fluorescein solution (AKORN, Inc., Lake Forrest, IL) with a dosage of 7.7 mg/kg. Video FFA images were captured up to 5 minutes after dye injection to detect potential vascular non-perfusion and late dye leakage. Examination results were reviewed to determine the presence and extent of avascular retina, vascular leakage, neovascularization, or shunt vessels on FFA.

Results

Seventy-two eyes of 36 infants, 53% male, received FFA for examination of persistent avascular retina (Table 1). Thirty-one infants had bilateral avascular retinas, and 5 infants had unilateral eye involvement. Infants included in this study had a mean gestational age at birth of 26.0 ± 2.2 weeks and a mean birth weight of 834.6 ± 216.3 grams. All infants in this cohort required some respiratory support during their neonatal period. In addition, all infants had a history of anemia during their neonatal course, with a mean lowest hemoglobin level of 87.2 ± 11.8 g/dL.

Demographics, ROP Grading, and FFA Outcome

Table 1:

Demographics, ROP Grading, and FFA Outcome

The mean age at the end of ROP screening was 47.6 weeks (range: 39.0 to 56.6 weeks). All patients had type 2 ROP at the worst stage of their disease, with predominantly stage 2 disease. The location of ROP disease at the worst stage was in zone II or III for all participants. Infants had a mean age of 18.8 ± 10.3 months (range: 3 to 39 months) at FFA. All patients had detectable avascular retina on both wide-field digital imaging and FFA with the RetCam. All avascular retina was in peripheral zone II or III. Apart from avascular retina, there were no other retinal abnormalities observed.

RetCam fundus photographs obtained during examination under anesthesia revealed persistent peripheral avascular retina in peripheral zone II or III in all infants involved in this study, although the defined edge of the vascular/avascular border can be hard to detect. However, the avascular retinal zone was clearly identified with fluorescein angiography, with some cases of abnormal vasculature at this border (Figure 1). In some patients, FFA demonstrated hyperfluorescent spots or popcorn lesions, with no loss of the capillary bed. In 3 eyes (5.5%) of 2 children aged 11 and 32 months, FFA demonstrated abnormal terminal punctate leakage and aberrant retinal vessels. These time points are indicated on the Kaplan–Meier survival curve in Figure 2. Both patients did not show leakage until 4 minutes after fluorescein dye injection. Retinal images and FFA of the infant with bilateral leakage are displayed in Figure 3. The 3 eyes that showed leakage at the late phase of FFA were treated with diode laser photocoagulations to the ischemic area and posterior to the ridge in the same session.

Retinal images and fundus fluorescein angiography (FFA) of pediatric retinas demonstrating persistent avascular retina and vascular abnormalities at the vascular/avascular junction. Retinal images (top) and FFA (middle) of the same eyes showing avascular peripheral retina. Abnormal vessels at the avascular border are indicated by a percent symbol (%) and vessel end budding are indicated with a plus sign (+). FFA (bottom) of another patient with avascular peripheral retina demonstrates vessel anastomoses/shunting and are indicated with an asterisk (*).

Figure 1.

Retinal images and fundus fluorescein angiography (FFA) of pediatric retinas demonstrating persistent avascular retina and vascular abnormalities at the vascular/avascular junction. Retinal images (top) and FFA (middle) of the same eyes showing avascular peripheral retina. Abnormal vessels at the avascular border are indicated by a percent symbol (%) and vessel end budding are indicated with a plus sign (+). FFA (bottom) of another patient with avascular peripheral retina demonstrates vessel anastomoses/shunting and are indicated with an asterisk (*).

Kaplan–Meier survival curve of the percentage of participants not requiring laser treatment based on post-menstrual age in months.

Figure 2.

Kaplan–Meier survival curve of the percentage of participants not requiring laser treatment based on post-menstrual age in months.

Bilateral persistent avascular retina with vessel leakage and ridge is visible. RetCam (Clarity Medical Systems, Inc., Pleasanton, CA) images (top), early phase fundus fluorescien angiography (FFA) (middle), and late phase FFA (bottom). A plus symbol (+) indicates a ridge on the retinal digital image and an asterisk (*) indicates leakage in the late phase of FFA.

Figure 3.

Bilateral persistent avascular retina with vessel leakage and ridge is visible. RetCam (Clarity Medical Systems, Inc., Pleasanton, CA) images (top), early phase fundus fluorescien angiography (FFA) (middle), and late phase FFA (bottom). A plus symbol (+) indicates a ridge on the retinal digital image and an asterisk (*) indicates leakage in the late phase of FFA.

Discussion

Management guidelines for type 1 ROP are well studied and clearly defined.2 These guidelines have resulted in significant improvement of structural and visual outcomes in children with ROP.2,6 However, limited evidence is available for the appropriate treatment of patients who do not have type 1 ROP but do have persistent avascular retina, in particular infants with type 2 ROP in peripheral zone II that persists after 45 weeks' post-menstrual age without complete vascularization. This is of concern because active ROP screening often ceases at this age.7

In 1994, Mintz-Hittner and Kretzer8 reported the potential for late rhegmatogenous peripheral retinal detachments in former preterm infants, highlighting the need for close observation. Prolonged retinal traction by remnant shunt or extra-retinal fibrovascular proliferation between a stable prenatally vascularized retina in the posterior pole and an unstable postnatally vascularized retina may lead to the development of retinal holes characteristically located in the fragile, anterior undifferentiated avascular retina.8 Limited evidence is available for the appropriate treatment of patients with ROP who do not have type 1 ROP but do have persistent avascular retina, in particular infants with a history of type 2 ROP who have persistent avascular retina in peripheral zone II or ROP in zone III after 45 weeks' post-menstrual age, and whether it is associated with later complications.

In the current study, two patients were 39 months' post-menstrual age at FFA examination, but there were no other retinal abnormalities expect for persistent avascular retina. Therefore, the lifetime risk of avascular retina in peripheral zone II or zone III is relatively unknown. Recently, Golas et al.9 reported exudative and tractional retinal detachment as late sequelae of ROP in a 19-year-old patient. The authors suggested that the late reactivation is likely due to persistent avascular retina producing constant low levels of vascular endothelial growth factor.9

Previous data focused on the retinal development and vascularity in infants with type 1 ROP. One large retrospective study of 370 infants who underwent laser treatment for ROP reported nine infants who received laser treatment after 45 weeks' post-menstrual age.10 Three of these infants had late development of type 1 ROP, and an additional six infants had no ROP but avascular peripheral retina, evidence of peripheral neovascularization, or ROP in zone III with persistent plus disease.10 This reveals the challenge to detect the small percentage of infants with persistent avascular retina or who have peripheral active ROP at 45 weeks' post-menstrual age, and whose disease can often be hard to visualize with the RetCam alone. For these patients, FFA may be helpful due to its ability to clearly identify the vascular and avascular retina, as demonstrated in this study. FFA can clearly delineate areas of avascular retina and demonstrate if any vessel leakage is present, which can then guide the clinician's management decision.

Abnormal FFA features have been reported in infants with type 1 ROP. A large study of infants who went on to have laser treatment for type 1 ROP observed delayed choroidal perfusion, arterio-venous shunting, vascular leakage along the ROP ridges, retinal non-perfusion, and hyperfluorescent rosary bead pattern on FFA, which all suggest active ROP.11 FFA observation in infants who received anti-vascular endothelial growth factor treatment for type 1 ROP detected persistent avascular retina up to 80 months after treatment.12 A significant number of these patients had fluorescein leakage with no retinal detachment, type 1 ROP, or other significant complications reported.12 However, the management of leaking cases was not reported, so it is unknown if they were observed or received peripheral photocoagulation laser treatment.12 The FFA pattern prior to treatment in active ROP demonstrates leakage along the entire ridge and surrounding area, whereas after anti-VEGF treatment, leakage was only in small, localized areas at the vascular/avascular border.11,12 Therefore, data are clear that infants with type 1 ROP have abnormal peripheral retinal vasculature both before and after treatment.

The current study's cohort of 36 cases differs from the other reported studies in that none of the children had either type 1 ROP or severe ROP disease that required treatment. The majority of cases had normal dichotomous branching at the vascular avascular junction, and “capillary bulbs” were observed at the retinal vessel termini without obvious FFA leakage. These features indicate that these vessels are relatively mature and thus less likely to lead to adverse events. However, in two cases late leakage on FFA was reported after 4 minutes, one unilateral and one bilateral. Both children had a history of persistent but stable stage 2 ROP and underwent FFA at 11 and 32 months, respectively. In one patient, the vessels crossed the ROP ridge but the persistent avascular area remained. This case highlights that avascular retina can persist in infants with ROP and blood vessels crossing the ridge does not rule out the possibility of leakage later. Due to the vessel leakage, indicating localized retinal ischemia at the avascular border, retinal laser photocoagulation was applied.

All infants in this cohort had a history of anemia during the neonatal period. The duration of anemia during the first week of life has been reported as an independent risk factor for ROP.13 Further research is required to determine if there is a similar association with persistent avascular retina in this same population. In addition, further research on the impact of treatment or prevention of early anemia on the development of ROP and persistent avascular retina is needed.

One might advocate laser photocoagulation in all ROP cases with persistent avascular retina after 45 weeks' post-menstrual age to reduce the number of examinations. In addition to the increased workload for the screening ophthalmologist, this approach could increase the systemic and ocular risks for those infants due to both the general anesthesia and laser treatment. The current study demonstrated that only 5.5% of patients showed vascular leakage indicating localized retinal ischemia, so it would be hard to justify treating the remaining 94.5% of patients without any features to suggest retinal ischemia. Clinical evidence and guidelines are needed to determine if certain types of avascular retina are deemed to be of higher risk, which may justify laser treatment. FFA is an essential tool to provide such information of vessel integrity and presence of retinal ischemia in the avascular retina. Larger studies are required to answer these questions with certainty.

A recent study by Warren et al.14 identified peripheral avascular retina persisting after 45 weeks' post-menstrual age in 16 children with a history of ROP, some of whom had received intravitreal bevacizumab injections. Abnormal and leaking peripheral vasculature was observed with FFA in groups with and without a history of ROP treatment.14 This study only included children without a history of ROP treatment; however, both studies highlight the importance of FFA to identify potential vascular abnormalities. The findings from the current study support the argument that premature infants with avascular retina persisting until 45 weeks' post-menstrual age should have FFA to determine if any high-risk features, including leakage or capillary drop out, are present prior to consideration of laser treatment. Patients with normal FFA vascular patterns can be left untreated and be clinically observed for 6 to 12 months as outpatients. However, the best timing for FFA after ROP screening cessation in these infants is also yet to be determined. Based on our experience, we consider any time between 3 and 6 months after discharge from active ROP screening is appropriate. Patients in our cohort were up to 3 years after discharge from ROP screening with no structural abnormalities except the avascular retina. This again suggests it may be safe to leave these patients untreated. Of note, when the avascular retinal area on the retinal images at FFA was compared to the avascular retinal area on the images obtained from ROP screening at 45 weeks' post-menstrual age, there were no obvious changes. This indicates that the avascular area in affected infants does not appear to change in size with time. However, further investigation into changes in the avascular retina itself, including the development of retinal holes or degeneration, warrants further study.

Limitations of our study are the relatively small number of children and the short duration of follow-up. Some of the patients without FFA leakage could still potentially pose longer term risk, although this is unlikely given its peripheral location. Patients with small areas of vascular leakage may be safe to be watched, but further data are needed to validate such an approach.

Persistent avascular retina after 45 weeks' post-menstrual age can have active leakage in a small percentage of patients. Infants with type 2 ROP but without complete vascularization can present management dilemmas when screening and treating them. The long-term impact of peripheral avascular retina is still not known, and, until such information becomes available, retinal imaging with FFA is recommended, with potential laser treatment for those with high-risk features. Currently, long-term outcomes of patients with confirmed leaking are unclear and further research on the benefits of lasers is required. All infants with persistent avascular retina after ROP screening require regular outpatient clinical follow-up with dilated fundus examination.

References

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Demographics, ROP Grading, and FFA Outcome

Patient No. GA (Weeks) Gender BW (Grams) Worst ROP PMA at FFA (Months) Lowest Hb FFA Leakage
1 25.9 M 1,010 Zone II, stage 3, nil plus 20 79 No leakage
2 27 M 590 Zone II, stage 3, nil plus 21 91 No leakage
3 27 M 730 Zone II, stage 2, nil plus 21 80 No leakage
4 25.6 F 850 Zone II, stage 2, nil plus 24 97 No leakage
5 30.7 F 1,060 Zone II, stage 3, nil plus 21 82 No leakage
6 31 M 1,150 Zone II, stage 2, pre plus 39 75 No leakage
7 24.40 M 790 Zone II, stage 3, nil plus 37 71 No leakage
8 24.4 F 850 Zone II, stage 3, pre plus 12 87 No leakage
9 30.1 M 1,420 Zone II, stage 2, nil plus 28 107 No leakage
10 29.9 F 1,365 Zone II, stage 2, nil plus 36 102 No leakage
11 25.9 M 1,010 Zone II, stage 3, nil plus 20 79 No leakage
12 25.3 F 930 Zone II, stage 2, nil plus 33 79 No leakage
13 24 F 450 Zone II, stage 2, nil plus 25 70 No leakage
14 27 M 710 Zone II, stage 2, nil plus 25 85 No leakage
15 24 M 695 Zone II, stage 2, nil plus 22 94 No leakage
16 25 M 710 Zone II, stage 2, nil plus 11 90 No leakage
17 24 M 610 Zone II, stage 3, nil plus 13 104 No leakage
18 25 M 790 Zone II, stage 3, nil plus 8 95 No leakage
19 24.9 F 640 Zone II, stage 2, pre plus 9 95 No leakage
20 25 M 825 Zone II, stage 2, nil plus 8 94 No leakage
21 24 F 795 Zone II, stage 2, nil plus 23 82 No leakage
22 27.6 M 630 Zone II, stage 3, nil plus 8 79 No leakage
23 24.4 M 770 Zone II, stage 2, nil plus 8 81 No leakage
24 30.3 M 1,150 Zone II, stage 2, nil plus 7 63 No leakage
25 26.4 F 850 Zone II, stage 2, nil plus 5 72 No leakage
26 26 F 740 Zone II, stage 2, nil plus 28 90 No leakage
27 24 F 600 Zone II, stage 2, nil plus 27 108 No leakage
28 25 M 700 Zone II, stage 2, nil plus 11 84 Leaking present OU
29 28 F 800 Zone II, stage 2, nil plus 5 112 No leakage
30 26 F 1,080 Zone II, stage 2, nil plus 3 88 No leakage
31 25 F 800 Zone II, stage 2, nil plus 23 82 No leakage
32 25 M 960 Zone II, stage 2, nil plus 23 84 No leakage
33 26 F 904 Zone II, stage 2, nil plus 20 90 No leakage
34 23 F 520 Zone II, stage 2, nil plus 20 90 No leakage
35 27 F 860 Zone II, stage 3, nil plus 32 82 Leaking present OD
36 23 M 700 Zone II, stage 2, nil plus 3 94 No leakage
Authors

From the Department of Ophthalmology, The University of Auckland, Auckland, New Zealand (RA-T, SKS, ED, SD); the Department of Ophthalmology, Counties Manukau District Health Board, Auckland, New Zealand (RA-T, ED); the Department of Ophthalmology, Auckland District Health Board, Auckland, New Zealand (ED, SD); and the Department of Ophthalmology, Queensland Children's Hospital, Brisbane, Australia (SD).

The authors have no financial or proprietary interest in the materials presented herein.

Correspondence: Shuan Dai, MBBS, MSc, FRANZCO, Queensland Children's Hospital, P.O. Box 3474, South Brisbane, Queensland 4101, Australia. E-mail: shuandai@me.com

Received: December 12, 2018
Accepted: April 30, 2019

10.3928/01913913-20190501-01

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