Retinopathy of Prematurity in Zone I posterior (Zone Half): Neonatal Profile, Clinical characteristics, and outcomes

doi:10.21203/rs.3.rs-2099203/v1

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Retinopathy of Prematurity in Zone I posterior (Zone Half): Neonatal Profile, Clinical characteristics, and outcomes

https://doi.org/10.21203/rs.3.rs-2099203/v1

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Objective

To report the demographic profile,clinical characteristics, and outcomes of retinopathy of prematurity (ROP) in Zone I posterior.

Methods

In a partly retrospective (ten years) and partly prospective (one year) study, we analyzed the demographic profile, clinical characteristics, treatment type, recurrences, and outcomes of babies with ROP in Zone I posterior.

Results

The study included 130 eyes of 67 infants with a mean gestational age and birth weight of 29.3 (± 2.2) weeks and 1217.3 (± 381.9) grams, respectively. All babies had received unblended oxygen with a poor weight gain in the majority.The ROP subtypes included aggressive,threshold, hybrid, stage 4, and atypical type in 78, 20, 11, 15, and 6 eyes, respectively. Fibrovascular proliferation when present,was prominent nasally, occasionally overriding the disc margin. Extensive arteriovenous tortuosity was more prominent than vascular dilatation. Atypical observations included bleb-like detachment(n = 6 eyes), candle wax-like preretinal deposits (n = 23 eyes), and large arteriovenous shunts (n = 9eyes). Primary treatment included intravitreal anti-VEGF in 119 eyes and laser in 11 eyes. Among those with follow-upfor more than 6 months, the recurrence was seen in 48.3% (n = 29) of eyes with anti-VEGF; with additional laser treatment, the outcome was favorable in 90.5% (n = 116) of eyes.

Conclusions

Zone I posterior ROP has a distinct profile with several atypical characteristics; it differsfrom ROP in other zones. Primary anti-VEGF treatment is beneficial but inadequate; most babies need additional laser or surgery.Improved neonatal care, earlier screening, and a combination of intravitreal anti-VEGF and laser are recommended.

1.ROP in Zone I posterior is difficult to treat; majority have an unfavourable outcome

2.Success rate with laser is poorerthanROP in other zones

What this study adds

1.While Aggressive retinopathy of Prematurity (AROP) was the commonest subtype, there was no stage 1 disease in zone I posterior eyes.

2.Retinopathy in zone 1 posterior could have many atypical features. We observed retinal vascular tortuosity without dilatation in some, bleb-like retinal detachment, excessive candle wax- like pre retinal deposits,long arterio venous shunts bridging the ends of multiple arteries and veins, prominentfibrovascular ridge, and overriding optic disc nasally

3.There is high risk of recurrence or inadequate response (in this study, 76.6%) with primary intravitreal Anti-VEGF,and the outcome is favourable when combined with laser (in this study,90.5%).

With improved neonatal care and greater availability of basic neonatal life-saving measures, even in low-resource regions, smaller and sicker babies are increasingly surviving. It has resulted in a rise in the number and spectrum of babies with retinopathy of prematurity (ROP), including the posterior retinal locations. ROP in Zone I have been described.^1,2 It progresses rapidly, and the outcome is poor following ablative therapy- poor results were reported in 77.8% and 55.2% of eyes in CRYOROP³ and ETROP⁴studies, respectively. However, with early screening, timely treatment with adequate laser, surgery when needed, and close follow-ups, up to 87.5% of babies could have a favourable outcome.² But, the Zone I posterior diseases are even more challenging to treat. The zone I posterior is confined between the optic disc and the foveal centre.^1,5 Response to laser monotherapy has been poor, and the outcome with intravitreal anti-vascular endothelial growth factor (VEGF) therapy has not been studied enough. ^5,6,7The current report describesthe characteristics and outcomesof ROP in this zone collected over a decade in a tertiary eye care facility in India.

The present study combinesprospective analysis of systematically collected retrospective data (10 years)and prospectively collected data(1 year), conducted at a tertiary centre in India (the eastern state of Odisha) from January 2011 to December 2021.The study included babies from several neonatal care centreswith different levels of care. This period also witnessed a treatment transitionfrom retinallasermonotherapytointravitreal anti-VEGF injection alone or in combination with laser for ROP. Informed written consentfrom the parents for sharing the de-identified images was already available from the subjects collected earlier (10 years),and new consent was obtained for the prospectively collected images. Zone I posterior disease was identified when the extent of retinal vascularization had not reached the foveal centre or centre of macula⁸or was within a four-disc diameter (DD) radius from the disc margin where the foveal anatomy was ill-defined.We presumed the disc fovea distance to be approximately 4.4 DD ± 0.4 DD as per the published reports.⁹We termed the disease Zone I posterior or Zone Half, used in an earlier publication from India.⁷We excluded the subjects with incomplete details or lack of consent. The classification of ROP was done per the International Classification of ROP (ICROP) standardsI, II, and III^8,10−12and the hybrid ROP described in the literature. ¹ Some of the previous diagnoses were revised as per ICROP III classification based on the available images during the data analysis of the study.

The demographic details of the infants,including gestational age (GA), gender, birth weight (BW),and postmenstrual age (PMA) at the time of first screening, were noted. Details of the perinatal risk factors, including mode and duration of oxygen supplementation, multiple gestations, systemic sepsis, blood transfusion,birth asphyxia, weight on presentation, weight gain/loss, etc., were analysed.We analysed the clinical profile of the disease, such as disease symmetry, rubeosis iridis,dilatation and tortuosity of retinal vessels, arteriovenous shunting and arcading, the avascular zone within the vascularized retina,the appearance of the central retinal vascular trunk and the posterior-most location of the disease measured in disc diameters. The speed of vascular outgrowth was calculated in disc diameter per week as per our earlier publication.¹³The treatment type, recurrence, treatment modality for recurrence, and outcome at least 6 months post-treatment were analysed.We termed Stage 4 and 5 ROP as advanced ROP.We defined an unfavourable outcome as the appearance of a posterior retinal fold involving the macula, a retinal detachment involvingany zone, or a retrolental mass that obscures the view of the posterior pole. ³Thedata were entered into an excel sheet and analysed using descriptive statistics.

This cohort included 130 eyes of 67 babies (retrospective:53 and prospective:14).The demographic details,perinatal risk factors, and retinopathy characteristics are shown in Tables1and 2. In general, the babies were smaller,sicker, and stayed in the NICU for more than one month with 100% unblended oxygen supplementation and poor weight gain in the majority. While all the babies (100%) had respiratory distress,45 (69.2%) babies had additional systemic comorbidities like respiratory distress, anaemia, sepsis, pneumonia,hydrocephalus, and intracranial haemorrhage.All babies had bilateral affection and severe disease. In this cohort, 63 babies had the disease in zone I posterior in both eyes;only one eye had zone I posterior disease in 4 babies, while the other eye had retinopathy in a different zone. Aggressive ROP was the most prevalent type (60%;n=78 eyes)followed by threshold (15.3%; n=20 eyes),hybrid (8.4%, n= 11 eyes),stage 5 (7.6 %; n=10 eyes),atypical (4.6%; n=6 eyes) and stage 4 (3.8 %; n=5 eyes) ROP. (Figures1 and 2). None of the babies had stage 1 disease.

There were many atypical findings (Figures 1 and 2),such as long arteriovenous shunts (9 eyes,6.9%), corkscrew-likeretinal vascular tortuosity (Figure 2a) in 16 eyes (12.3%), candle-wax preretinal deposits (Figure 2c) in 23 eyes (17.6%),and absence of vascular dilatation despite tortuosity in 23 eyes(17.6%).Some of these morphological changes were difficult to classify as per existing ICROP nomenclature.

The posterior limit of the disease was at an average of 1.85 DD from the optic disc.The average rate of vascular growth of the posterior and anterior-most blood vessels was slower at 0.16 DD and 0.42 DD/week, respectively, than a normal of 0.7DD/week.¹³A ridge was noted in 79 eyes, and 18 of them had broad nasal proliferation.Therewerecandle wax-like preretinal deposits in 23 eyes, including AROP,hybrid, and threshold ROPs.

One baby with bilateral Zone I posterior disease expired before treatment. While we included this subject for the demographic and clinical profile analysis, we analysed the outcome data of 66 babies (128 eyes).The treatment profile and outcome are depicted in Figure 3 and Table 3.

Following anti-VEGF monotherapy, 48.3% (29 of 60) eyes had a recurrence, and 28.3% (17 of 60)eyes had inadequate treatment response. In all eyes treated with ranibizumab (6 eyes), there was either a recurrence (4 eyes,66.6%) or an inadequate response (2 eyes,33.3%). In the bevacizumab group the recurrence rate was 46.2% (n= 25 eyes).After re-treatmentwith laser, 23 of 29 eyes (16babies) showed regression, and 3 babies (6 eyes) were lost to follow-up. The median time to recurrence after anti-VEGF monotherapy was11 (Average 12.1,Range1.2 to 25.1) weeks. Two of 5 eyes in the laser monotherapy group had a recurrence and required surgery.

We did a subgroup analysis of the treatment outcome in 37 babies (73 eyes) who had completed at least 6 months of follow-up (Table 3). There was a favourable outcome in 90.5 % of cases.The 8 eyes that did not benefit from treatment had advanced ROP, such as stage4B (4 of 8 eyes), atypical bleb-like presentation (2 of 4 eyes), and threshold ROP or AROP (one eye each).

There are limited reports on ROP in Zone I posterior.^1,5,6We noticed several features in our cohort of zone I posterior ROP worth mentioning. The disease was associated with using unblended oxygen, and most babies had a long NICU stay, poor weight gain, and multiple systemic comorbidities. A higher incidence of ROP has been reported in babies staying longer in the hospital. ¹⁴Longer hospital stays could indirectly mean a poor systemic status and susceptibility to multiple systemic abnormalities, which in turn can increase the severity of ROP. The average NICU stay was more than a month for most of the babies in this cohort. A poor weight gain at an average of 55.37 grams/week (against the normal of approximately100grams per week) probably influenced the stunting of vascular growth and disease development in this zone.^15,16,17In this cohort, 21 eyes (16.1%) of babies had advanced disease (Stage 4/5 or atypical bleb-like detachment) at the time of presentation. Six of 8 babies who did not improve with treatment had advanced disease at presentation. Of the 73 eyes of 37 babies who had completed a 6-month follow-up, 31 eyes of 16 babies (42.5%) were screened on time. In this cohort, 4 eyes of 2 babies(12.9%) required surgery and had an unfavourable outcome. Whereas in the remaining 42 eyes of 22 babies (57.5%) who were not screened on time, 30.9% ultimately required surgery. This indicates that early and timely screening and disease detection are vital to improved care and treatment outcomes.

Retinal vascularization starts at GA 16 weeks and reaches the optic disc margin at 17 weeks; thereafter, the rate of vascular growth is 0.7 DD or 0.7mm/week (taking into consideration that the optic disc diameter in neonates is 1.05 DD). ¹⁸Considering that fovea is approximately 4DD away from the optic disc in the neonates, the retinal vascular growth should reach the fovea approximately by 23weeks. In this series, 51 babies (76%) had GA of more than 23 weeks, but their retinal vascular growth was still posterior to the fovea. The reasons could be either decelerated growth antenatally^3,19−21 or supplemental oxygen causing obliteration of the peripheral segment of the blood vessels, a condition similar to oxygen-induced retinopathy. ^19–23

We also observed several vascular abnormalities. These were arterio-venous shunting at multiple levels, large vessel-free pockets within the vascular loops, retinal vascular tortuosity disproportionately more than dilatation, and absence of dilatation despite tortuosity in some vessels. Arteriovenous shunting is a phenomenon to compensate for peripheral ischemia. In our cohort, around 80% of eyes had this shunting, indicating a greater impact of peripheral non-perfusion in the pathogenesis of ROP in this zone. Unlike classic AV shunting, we observed around 14% of eyes had long AV shunts bridging multiple arteries and veins. We have earlier reported similar large arterio- venous loops in ROP treated with intravitreal bevacizumab. But these were not as dilated and tortuous as in the babies with zone I posterior ROP seen in this series of babies. This possibly suggests a role of extensive hypoxia and higher demand to compensate in this zone. Also, 12% of eyes in this cohort had a characteristic “corkscrew” tortuosity. This could probably be secondary to severe backlogging of the blood column within a small segment of blood vessels. The central trunks were well formed in most eyes, though it was poorly developed in approximately 18% of eyes and was difficult to identify even in relatively clear media (Fig. 2b). We are unsure if it influences the treatment outcomes.

We have also earlier described atypical patterns such as bleb-like detachments and large candle wax-like deposits. ^24,25In this series, we observed this abnormality in 4.6% and 17.6% eyes, respectively. These appearances in human eyes are close to oxygen-induced retinopathy in animal models. ¹⁶The candle wax deposits have been hypothesised to occur due to the poorly formed retinal vessel and blood-retinal barrier break secondary to oxygen toxicity. ²⁵We need further studies to understand their origin,nature,pathogenesis, and clinical significance. The hyaloid vascular system, expected to disappear by the 7th month of GA, was persistent in 31% of eyes in the current cohort of babies. The persistence of the hyaloid plays an important role for vitreous to condense around it and can be one of the factors responsible for the closing of the retina over the optic disc, causing a posteriorly located closed funnel retinal detachment.

The choice of anti-VEGF monotherapy for primary treatment in the majority of eyes in this cohort was related to the posterior location of the disease, poor systemic status of the babies, and /or non-dilating pupils. But the disease recurrence after anti-VEGF monotherapy in Zone I posterior in this series was higher than the recurrence rate of ROP in other zones published in the literature.²⁶The recurrence/inadequate response to initial therapy was higher with ranibizumab than with bevacizumab monotherapy (100% vs. 62.5%, in this cohort), but the number of treated eyes with either molecule was too small to draw any meaningful inference.Laser was the preferred treatment modality to treat the disease recurrence, resulting in a better outcome in 90.5% of cases. Possibly, a combined intravitreal anti-VEGF and zone I sparing retinal laser as the first line of treatment could have further improved the success rate, as was done in two eyes in this cohort

Study limitations. Fundus fluorescein angiogramand optical coherence tomography were not performed on these babies. We also did not have all details of oxygen supplementation.Following treatment, the follow-ups were done weekly,bi-weekly, or monthly, not daily. Further, the disease could have recurred earlier thanthe visit date; we counted the date of presentation as the date of recurrence.

Study strengths. The present series on zone I posterior ROP is the largest in the literature (Medline search). The detailed clinical description provides the distinctive features that help distinguish these from retinopathy in other zones. The disease tends to be advanced in the majority, and the stage 1 disease is usually non-existent in this zone. In this study, there was high recurrence rate with anti-VEGF monotherapy; probably intravitreal anti-VEGF followed by laser could be optimal for retinopathy in this zone.Also, many could present with advanced disease;therefore a timely and early screeningimprovesthe outcome further.

Further research should address the atypical patterns, timing of screening, the chronology of events resulting in restriction of the vascular outgrowth to this zone, the rapidity of disease progression, and the standard of care in zone I posterior ROP.

AROP: Aggressive posterior retinopathy of prematurity

BW: Birth weight

DD: Disc diameter

FVP: Fibrovascular proliferation

FFA: Fundus Fluorescein angiography

GA: Gestational age

ICROP: International Classification of retinopathy of prematurity

OCT: Optical coherence tomography

PMA: Post menstrual age

ROP: Retinopathy of prematurity

VEGF: Vascular endothelial growth factor

Acknowledgment:None

Financial Support: Hyderabad Eye Research Foundation, Hyderabad, India. Though not directly related to this project, the institute’s ROP program as a whole has been supported by Miriam Hyman Memorial Trust, London; Queen Elizabeth Diamond Jubilee Trust, London; Public Health Foundation of India, RashtriyaBal SwasthyaKaryakram, India; Dalmia Holdings, New Delhi; and Cognizant Foundation at different point of time.

Conflict of interest: No conflicting relationship exists for any author.

Author Contribution Statement:

TRP: Concept, design, data acquisition, analysis, Interpretation, preparation of the draft, critical revision, final approval and agree to be accountable for all aspects of the work.ement

MS; Data acquisition, analysis, preparation of the draft, critical revision, final approval and agree to be accountable for all aspects of the work

SUS: Data acquisition , preparation of the draft, critical revision, final approval and agree to be accountable for all aspects of the work

TPD: Study design, Data analysis, Critical revision, final approval

UTB: Data acquisition, preparation of the draft, final approval and agree to be accountable for all aspects of the work

AS: Data acquisition, preparation of the draft, critical revision, final approval and agree to be accountable for all aspects of the work

SBN: Data acquisition, preparation of the draft, critical revision, final approval and agree to be accountable for all aspects of the work

SN: Data acquisition , critical revision, final approval and agree to be accountable for all aspects of the work

SAN: Concept and design, analysis,interpretation,preparation of the draft, critical revision, final approval and agree to be accountable for all aspects of the work.

BVP: Concept and design,analysis ,preparation of the draft, criticalrevision, final approval and agree to be accountable for all aspects of the work.

KA: Concept and design, analysis, interpreparation of the draft, criticalrevision, final approval and agree to be accountable for all aspects of the work

B KS: Datacollection , interpretation,preparation of the draft, critical revision,final approval and agree to be accountable for all aspects of the work

SD:Data collection ,interpretation,preparation of the draft,criticalrevision,final approval and agree to be accountable for all aspects of the work

KSR:Datacollection,interpretation,preparation of the draft,criticalrevision,final approval and agree to be accountable for all aspects of the work

LP:Data collection,interpretation,preparation of the draft, critical revision,final approval and agree to be accountable for all aspects of the work.

SJ:Concept,design,analysis,interpretation,preparation of the draft,criticalrevision,final approval and agree to be accountable for all aspects of the work

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Table 1.Demographic and perinatal profile
	Mean	SD	Range	Median
Gestational Age(weeks)	29.4	2.2	22-34	29.8
Birth weight (grams)	1217.3	381.9	650-3500	1145
Duration of NICU stay (days)	35.9	20.3	7-122 days	30
PMA at presentation (weeks)	35.27	2.6	27-43	35
Weight gain/ week (grams)	48.5	32.8	3-125	41.81

SD: Standard deviation, NICU-Neonatal intensive care units , PMA-Post menstrual age,

Table 2: Disease profile and ocular characteristics, n=130 eyes,67 babies
	Number	Percentage
Bilateral disease (n=67babies)	63	94%
Disease symmetry (n=62 babies)	50	74.6%
Circumferential extent of thedisease:360 degree (n=114 eyes)	30	26.3%
Posterior most extent of retinopathy	Avg:1.8 DD
New Vessels Iris( n=130 eyes)	65	50%
Retinal vascular tortuosity (n=130 eyes)	121	93%
Pattern of retinal venous tortuosity(n=130 eyes) a) Arteries>veins b) Veins>Arteries c) Only arteries d) Only veins e) Arteries=Veins	49 32 13 1 2	37.6% 24.6% 10% 0.7% 1.5%
Corkscrew-like retinal vascular tortuosity(n=130 eyes)	16	12.3%
Long AV shunts	9	6.9%
Shunting (n=130 eyes)	105	80.7%
Presence of ridge tissue (n=130 eyes)	79	60.7%
Retinal/Pre retinal hemorrhages a) Edge haemorrhages (at or within 1 disc diameter from the vascular- avascular junction) b) Haemorrhages within the vascularized retina: c) Hemorrhage overlying the optic disc	65 40 19 6	49.2%
Central Vascular trunks near optic disc: poorly formed	28	21.5 %
Candle wax like pre retinal deposits	23	17.6%

Table 3. Treatment profile and outcome of babies with > 6m follow-up (N=73 eyes of 38 babies)
Treatment Profile	Total	Favorable outcome number	Percentage	Unfavorable outcome	Percentage
Those eyes that completed 6 m follow up	73 eyes	65 eyes	89	08 eyes	11
Could be managed with Anti-VEGF alone	15	15	100	0	0
Laser alone	3	3	100	0	0
Anti-VEGF+Laser	29	29	100	0	0
Anti-VEGF+anti-VEGF+Laser	3	3	100	0	0
Anti-VEGF+anti-VEGF	2	2	100	0	0
Laser+Laser+anti-VEGF+Surgery	2	2	100	0	0
Laser+Surgery	3	2	66.6	1	33.3
Anti-VEGF+Laser+ anti-VEGF	1	1	100	0	0
Anti-VEGF+Laser+Surgery	15	8	53.3	7	46.6

Anti-VEGF: Anti Vascular Endothelial growth factor

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Retinopathy of Prematurity in Zone I posterior (Zone Half): Neonatal Profile, Clinical characteristics, and outcomes

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