Ophthalmic Surgery, Lasers and Imaging Retina

Brief Report 

Visual and Anatomic Outcomes of Premacular Hemorrhage in Non-Accidental Trauma Infants Managed With Observation or Vitrectomy

Ogul E. Uner, BA; Christopher R. Stelton, MD; G. Baker Hubbard, MD; Prethy Rao, MD, MPH

Abstract

BACKGROUND AND OBJECTIVE:

The management of premacular hemorrhage secondary to non-accidental trauma (NAT) is unclear. The authors describe the outcomes of NAT infants referred for surgical evaluation of premacular hemorrhage.

PATIENTS AND METHODS:

Retrospective institutional review board-approved case series between 2000 and 2019 of vision-threatening premacular hemorrhage (sub-hyaloid or sub-internal limiting membrane hemorrhage without vitreous hemorrhage) in NAT infants. Time to hemorrhage resolution, vision, and comorbidities were collected.

RESULTS:

Thirty-six patients (62 eyes) with mean age of 5.4 months (range: 2–10 months) were included. Nine eyes (14.5%) underwent vitrectomy. Median time to hemorrhage resolution by observation was 75 days (interquartile range [IQR]: 60–120 days), and time to vitrectomy was 54.5 days (IQR: 47.8–58.5 days). Eight eyes (12.9%) had amblyopia, which was not significantly different between groups. Despite hemorrhage clearance, a higher proportion of eyes in the vitrectomy group had pigmentary changes (P = .04) and strabismus (P = .002) at follow-up.

CONCLUSIONS:

Most cases of NAT-related premacular hemorrhage resolve within 3 months without surgical intervention. Comorbidities may limit visual prognosis.

[Ophthalmic Surg Lasers Imaging Retina. 2020;51:715–722.]

Abstract

BACKGROUND AND OBJECTIVE:

The management of premacular hemorrhage secondary to non-accidental trauma (NAT) is unclear. The authors describe the outcomes of NAT infants referred for surgical evaluation of premacular hemorrhage.

PATIENTS AND METHODS:

Retrospective institutional review board-approved case series between 2000 and 2019 of vision-threatening premacular hemorrhage (sub-hyaloid or sub-internal limiting membrane hemorrhage without vitreous hemorrhage) in NAT infants. Time to hemorrhage resolution, vision, and comorbidities were collected.

RESULTS:

Thirty-six patients (62 eyes) with mean age of 5.4 months (range: 2–10 months) were included. Nine eyes (14.5%) underwent vitrectomy. Median time to hemorrhage resolution by observation was 75 days (interquartile range [IQR]: 60–120 days), and time to vitrectomy was 54.5 days (IQR: 47.8–58.5 days). Eight eyes (12.9%) had amblyopia, which was not significantly different between groups. Despite hemorrhage clearance, a higher proportion of eyes in the vitrectomy group had pigmentary changes (P = .04) and strabismus (P = .002) at follow-up.

CONCLUSIONS:

Most cases of NAT-related premacular hemorrhage resolve within 3 months without surgical intervention. Comorbidities may limit visual prognosis.

[Ophthalmic Surg Lasers Imaging Retina. 2020;51:715–722.]

Introduction

Retinal hemorrhage is a cardinal manifestation of pediatric non-accidental trauma (NAT), in which violent repeated acceleration-deceleration forces that damage the retina via vitreomacular traction.1 In 1971, Guthkelch first described the concept of “whiplash-shaking” and “jerking” of infants resulting in severe deleterious effects to an infant's brain and eyes.2 Since then, much work has gone into understanding the mechanisms and spectrum of clinical findings associated with pediatric NAT.3 However, the specific management of premacular hemorrhage (sub-hyaloid or sub-internal limiting membrane [ILM]) has not been as well studied. Minimal consensus exists on the optimal timing for surgical intervention or whether surgery is beneficial. The purpose of this single-center, retrospective study was to evaluate the clinical characteristics, course, and management of infants referred for surgical evaluation of premacular hemorrhage due to NAT. To our knowledge, this is the largest retrospective series that has evaluated NAT eyes specifically with premacular hemorrhage as the predominant feature for surgical evaluation and intervention.

Patients and Methods

We performed a single-center, retrospective review of children younger than 2 years of age who were referred to the Emory Eye Center (Atlanta, GA) between January 1, 2000, and February 1, 2019, for surgical evaluation of premacular hemorrhage due to NAT. Patients were identified by a computerized search of billing records at the Emory Eye Center for children younger than 2 years with the International Classification of Disease (ICD 9 and ICD 10) codes for “vitreous hemorrhage,” “retinal hemorrhage,” “shaken infant syndrome,” and “other and unspecified injuries of the eye.”

We included infants with a diagnosis of NAT based on multi-disciplinary evaluation and exhibited a vision-threatening premacular hemorrhage. Premacular hemorrhage was defined as a hemorrhage confined to the sub-internal limiting membrane (ILM) or sub-hyaloid spaces in the macula. We excluded children with solely intramacular, submacular, or significant vitreous hemorrhage. Charts were reviewed and the following data were extracted: age, race, gender, visual function at presentation, fundus findings at presentation, ocular co-morbidities at presentation, time to resolution of premacular hemorrhage, time to vitrectomy, visual function at last follow-up, ocular abnormalities at last follow-up, and associated neurologic history. Retcam3 (Natus, Pleasanton, CA) color fundus photographs were also obtained retrospectively when available.

All patients were evaluated by a single retina specialist (GBH) at Emory Eye Center. Premacular hemorrhages were followed for at least 4 weeks with monthly serial examinations. Improvement of hemorrhage was defined as resolution or displacement of the hemorrhage outside of the visual axis. If the premacular hemorrhage did not improve after 4 weeks, a 20-gauge or 23-gauge pars plana/plicata vitrectomy (PPV) with membrane peeling of the posterior hyaloid/ILM complex was performed. If the hemorrhage started to improve, the patients were observed with monthly examinations until resolution. If the hemorrhage did not continue to resolve after the initial serial examinations (ie, initial improvement after 4 weeks but no further improvement after 8 to 12 weeks), the patient underwent a PPV (Figure 1).

Flow chart demonstrating the management of non-accidental trauma infants in the study based on the status of premacular hemorrhage.

Figure 1.

Flow chart demonstrating the management of non-accidental trauma infants in the study based on the status of premacular hemorrhage.

Descriptive statistics were used to summarize characteristics of infants and eyes using the statistical software XLSTAT for Microsoft Excel (Addinsoft, Paris, France). Eyes were divided into two groups: premacular hemorrhage eyes that were observed and those that underwent a pars plana vitrectomy (PPV). Baseline and visual outcomes were compared based on treatment group using the Fisher's exact test (categorical variables) and the Mann-Whitney U test (continuous variables). Wilcoxon signed-rank test was used to compare baseline and final visual acuities. A P value below .05 was deemed significant.

Institutional review board approval for the data collection and study was granted by Emory University School of Medicine. The study complied with the Health Insurance Portability and Accountability Act, and research adhered to the tenets of the Declaration of Helsinki.

Results

Initial search of billing records identified 707 patients. Of these, 45 patients were cases of suspected NAT. Nine patients were excluded due to the absence of premacular hemorrhage in either eye. Among the 36 patients (72 eyes), 10 eyes were further excluded due to central vitreous hemorrhage (n = 2) or absence of premacular hemorrhage (n = 8). A total of 62 eyes (36 patients) were ultimately included in the analysis. Among the 62 included eyes, 53 (85.5%) were observed and 9 (14.5%) underwent a PPV. Fifty-eight eyes (93.5%) exhibited a premacular hemorrhage that involved the fovea.

The four eyes (6.5%) without fovea-threatening premacular hemorrhages were in the observation group only. There was no significant difference between the proportion of eyes with fovea-threatening hemorrhage in the observation and the vitrectomy group (P > .99).

Table 1 shows the baseline clinical characteristics of the 36 study patients (n= 28 observed, n = 8 PPV). The mean age at time of NAT was 5.4 months (range: 2.0 to 10.0 months). There were 24 males (66.6%) and 12 females (33.3%). The majority of the infants identified as white (80.0%). Thirty of 36 patients (83.3%) had at least one neurologic comorbidity, with intracranial hemorrhage being the most common diagnosis (26 infants, 72.2%). Other neurologic injuries included seizure disorder (12 infants, 33.3%), developmental delay (five infants, 13.9%), cerebral visual impairment (three infants, 8.3%), and hypoxic ischemic encephalopathy (3 infants, 8.3%). There were no significant differences in age, gender, race, and neurologic co-morbidities between the observed and vitrectomy groups.

Baseline Characteristics of 36 Infants With Pre-Macular Hemorrhage Secondary toNon-Accidental Trauma Who Were Managed With Observation or PPV

Table 1:

Baseline Characteristics of 36 Infants With Pre-Macular Hemorrhage Secondary toNon-Accidental Trauma Who Were Managed With Observation or PPV

The median duration of follow-up was 6.0 months (interquartile range [IQR]: 3.0 – 30.0 months) and the mean time of follow-up was 22.2 months (Table 1). There was no significant difference in the duration of follow-up between groups (P = .94). Follow-up of 3 months or more was available in 49 of 62 eyes (79.0%), with 43 of 53 eyes (81.1%) in the observation group and six of nine eyes (66.6%) in the PPV group. The proportion of patients with follow-up of 3 months or more was not significantly different between observed and vitrectomized eyes (P = .38). In the observation group, the median time to resolution of premacular hemorrhage was 75.0 days (IQR: 60.0–120.0 days) and the mean time to resolution of premacular hemorrhage was 87.4 days (Figure 2). For the PPV group, the median time to vitrectomy was 54.5 days (IQR: 47.8 – 58.5 days), and the mean time to vitrectomy was 57.5 days (Figure 3).

Color fundus photograph of the right eye of a 4-month-old male shaken by his father with a large sub-internal limiting membrane hemorrhage and mild inferior vitreous hemorrhage. He was observed, with clearance of blood 20 weeks after initial presentation; no amblyopia was reported.

Figure 2.

Color fundus photograph of the right eye of a 4-month-old male shaken by his father with a large sub-internal limiting membrane hemorrhage and mild inferior vitreous hemorrhage. He was observed, with clearance of blood 20 weeks after initial presentation; no amblyopia was reported.

Color fundus photograph of the left eye of a 5-month-old male shaken by his father with an arcade-to arcade sub-internal limiting membrane hemorrhage. He underwent a vitrectomy 7 weeks after initial presentation and later developed strabismus.

Figure 3.

Color fundus photograph of the left eye of a 5-month-old male shaken by his father with an arcade-to arcade sub-internal limiting membrane hemorrhage. He underwent a vitrectomy 7 weeks after initial presentation and later developed strabismus.

Visual Outcomes

The visual outcomes of the 62 study eyes are shown in Table 2. Visual acuity (VA) was subdivided into two categories (fix and follow or better versus cannot fix or follow) in order to provide the most robust or meaningful visual function. Fifty-eight eyes (93.5%) had a documented VA. Of these, 57 eyes (91.9%) had VA recorded both at initial consultation and the final visit. Of the five eyes without both initial and final VA, four were from the observation group. Forty-two eyes (72%) could not fix or follow at baseline. There was no significant difference in VA at baseline or follow-up between the treatment groups (P = 1.0 and P = 0.46, respectively). There was a statistically significant improvement in vision between baseline and final VA in the observation group (P < .001, Wilcoxon rank test) but no difference in the PPV group (P = .16).

Final Visual and Anatomic Outcomes of 62 Eyes With Pre-Macular Hemorrhage Secondary to Non-Accidental Trauma That Was Managed With Observation or PPV at Most Recent Follow-Up

Table 2:

Final Visual and Anatomic Outcomes of 62 Eyes With Pre-Macular Hemorrhage Secondary to Non-Accidental Trauma That Was Managed With Observation or PPV at Most Recent Follow-Up

Eight of 58 eyes (12.9%) exhibited amblyopia at the final visit with no significant difference among the treatment groups. However, there was a statistically significant higher percentage of strabismus in the PPV group compared to observation (two of 50 eyes [4.0%] observed vs. four of eight eyes [50.0%] PPV group; P = .002, respectively).

Anatomic Outcomes

Among the surgical group, seven infants underwent unilateral PPV and one underwent a bilateral PPV (n = 9 total eyes). Two of eight eyes (25.0%) exhibited an epiretinal membrane preoperatively. One eye had a full-thickness macular hole discovered intraoperatively after the premacular hemorrhage was cleared (Figure 4).

Color fundus photograph of the left eye of a 3-month-old male victim of non-accidental trauma with a fovea-involving pre-retinal hemorrhage who underwent a vitrectomy 7 weeks after initial presentation. A full-thickness macular hole was noted at the time of surgery. He did not exhibit amblyopia at his most recent follow-up.

Figure 4.

Color fundus photograph of the left eye of a 3-month-old male victim of non-accidental trauma with a fovea-involving pre-retinal hemorrhage who underwent a vitrectomy 7 weeks after initial presentation. A full-thickness macular hole was noted at the time of surgery. He did not exhibit amblyopia at his most recent follow-up.

The posterior segment findings at most recent follow-up included optic atrophy (23 eyes, 39.0%), submacular scar or significant pigmentary changes (17 eyes, 28.8%), and a visibly separated ILM (two eyes, 3.4%) (Table 2). Although there were a greater number of eyes with optic atrophy in the PPV group, the difference was not significant (P = .24). Of note, a statistically greater proportion of eyes exhibited submacular scars and/or significant retinal pigment epithelium (RPE) changes in the PPV group compared to the observed group (P = .04).

Discussion

We present a retrospective case series of NAT infants with a vision-threatening premacular hemorrhage who were treated with either observation or PPV to understand the optimal timing and management of premacular hemorrhage. In this study, we found that the majority of eyes cleared without surgery in less than 3 months, underscoring the importance of serial observations in NAT infants. To our knowledge, this is the single largest retrospective series evaluating NAT eyes that were surgically referred specifically for a vision-threatening premacular hemorrhage (sub-hyaloid or sub-ILM).

Adequate stimulation of the visual system during the critical period is one of the main driving forces in the management of premacular hemorrhages during infancy. However, the exact timing of intervention to reduce the risk of the deprivational amblyopia is unknown. Much of the optimal timing is derived from the congenital cataract literature where unilateral and bilateral cataract interventions are no later than 6 and 10 weeks from birth, respectively.4 In our study, however, we found only eight of 62 eyes (12.9%) developed amblyopia and most hemorrhages cleared within 3 months from initial presentation. The exact reason for the discrepancy is not clear, however, the difference in timing may be secondary to location and the dynamic appearance of the hemorrhage over time. Congenital cataracts may be a constant, more complete obstruction of the entire visual axis, whereas premacular hemorrhages are locally confined and may fluctuate over time. Additionally, peripheral retinal stimulation may still be adequate in the short term to promote visual stimulation.

VA measurements were difficult in this patient population due to a variety of confounding factors, including age, neurological status, and co-existing posterior pathology such as optic atrophy. Therefore, these results need to be interpreted with caution and may not reflect true visual and functional outcomes in this patient population. We speculate that minimal vision improvement in the surgical group may be secondary to underlying retinal ischemia/damage5,6,7 or as a result of the unreliability of visual measurements in this patient population. In this study, most eyes did not undergo fluorescein angiography, as the majority cleared with serial examinations in the office. However, anatomically, we observed a significantly greater proportion of eyes with postoperative macular scarring and RPE changes in the surgical group compared to observation, indicating more extensive underlying retinal injury. Additionally, the proportion of eyes with strabismus was higher in the surgical group.

Serial follow-up visits represent a critical component of the management of NAT infants. However, few studies describe management and timing of premacular hemorrhage due to NAT. Conway and colleagues report four eyes of two children with pre-retinal hemorrhage due to NAT that were managed with three weekly injections of tissue plasminogen activator (tPA) and SF6 gas as an alternative to vitrectomy.8 Azzi et al. describe a single case of NAT with bilateral sub-ILM hemorrhages that resolved after 10 weeks of observation.9 Binenbaum et al. report the largest natural history series of 91 eyes that underwent pediatric head trauma (accidental and nonaccidental), of which 68 eyes (75%) exhibited pre-retinal hemorrhages.10 Pre-retinal hemorrhages persisted between 5 and 111 days. However, the location (macular versus extramacular) and specific characteristics of the pre-retinal hemorrhages were not evaluated.

Few case reports11–13 in the literature have explored vitrectomy for NAT with favorable vision up to 20/4011 and fix and follow behavior postoperatively.12 Most recently, Min et al. report the largest series of PPVs in 32 children with pre-retinal or vitreous hemorrhages secondary to NAT. Eyes that were observed for 4 weeks with no resolution underwent PPV. The mean time to vitrectomy was 29 days; 15 eyes improved from no light perception to light perception or better.13 However, this study included infants with vitreous hemorrhage and did not specify the number of eyes in each hemorrhage subtype. In our series, nine of the 62 eyes underwent a PPV with a mean time 57.5 days with no significant difference in fix and follow behavior. This discrepancy may be multifactorial. It may be that our surgical cases were more severe and/or their series included cases that would have improved with longer observational follow up of more than 4 weeks. Interestingly, the majority of PPVs were unilateral, indicating that the timing of hemorrhage resolution may be unique to the configuration/location of the hemorrhage in each eye and not necessarily specific to the mechanism/severity of injury or other systemic factors of the infants themselves (Figure 5). The addition of ILM peel to PPV may also impact visual outcomes by contributing to increased macular pigmentation and photoreceptor injury.

Color fundus photographs of a 6-month-old male victim of non-accidental trauma without amblyopia. (a) There is a large subhyaloid hemorrhage of the right eye, as well as scattered intraretinal hemorrhages in the periphery. This eye was observed, with clearance of the blood in 10 weeks. (b) Color fundus photograph of the left eye of the same patient with a fovea-involving sub-internal limiting hemorrhage that spans the entire macula, multiple intraretinal hemorrhages, and non-central vitreous hemorrhage of the left eye. This eye underwent vitrectomy 8 weeks after initial presentation.

Figure 5.

Color fundus photographs of a 6-month-old male victim of non-accidental trauma without amblyopia. (a) There is a large subhyaloid hemorrhage of the right eye, as well as scattered intraretinal hemorrhages in the periphery. This eye was observed, with clearance of the blood in 10 weeks. (b) Color fundus photograph of the left eye of the same patient with a fovea-involving sub-internal limiting hemorrhage that spans the entire macula, multiple intraretinal hemorrhages, and non-central vitreous hemorrhage of the left eye. This eye underwent vitrectomy 8 weeks after initial presentation.

Limitations of our study include lack of a matched comparison group, smaller sample size, reporting of simplified ambulatory VA, and incomplete follow-up, with 21% of eyes having a follow-up duration of less than 3 months. However, the complex social situation of these patients needs to be considered. These infants are more feasible to follow immediately, as they are involved with the State Division of Family & Children Services, social work, and in the hospital. However, upon discharge, these children have variable involvement with foster care and may move to various locations, hindering long-term follow-up. Additional limitations include the lack of fluorescein angiography in the majority of eyes. This limited our ability to specifically grade the extent (size) of the premacular hemorrhage and retinal ischemia. Additionally, we evaluated patients with specific, localized premacular hemorrhages. This is in contrast to dense vitreous hemorrhages, which may behave differently in infants. Lastly, VA measurements and interpretation of visual outcomes remain a significant limitation in this patient population due to age and co-existing neurological abnormalities, which hinder the ability to distinguish between cortical visual impairment and retina dysfunction.

In conclusion, our series demonstrates that the majority of pediatric premacular hemorrhages improve without surgical intervention within 3 months. Vision may be limited by a complex interplay of ocular (structural and functional) and neurologic co-morbidities, which are not significantly responsive to vitrectomy. Therefore, the risk of deprivational amblyopia has to be considered in light of these counterbalancing factors, in addition to the risk of anesthesia for traumatized infants.

References

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  2. Guthkelch AN. Infantile subdural haematoma and its relationship to whiplash injuries. BMJ. 1971;2(5759):430–431. doi:10.1136/bmj.2.5759.430 [CrossRef] PMID:5576003
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  8. Conway MD, Peyman GA, Recasens M. Intravitreal tPA and SF6 promote clearing of premacular subhyaloid hemorrhages in shaken and battered baby syndrome. Ophthalmic Surg Lasers. 1999;30(6):435–441. PMID:10392730
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  13. Min FCL, Alagaratnam J, Ramasamy S, et al. Lens-sparing vitrectomy for shaken baby syndrome. Int Eye Sci. 2016;16:213–217.

Baseline Characteristics of 36 Infants With Pre-Macular Hemorrhage Secondary toNon-Accidental Trauma Who Were Managed With Observation or PPV

CharacteristicTotal Study Group (n = 36)Observed (n = 28, 77.8%)PPV (n = 8, 22.2%)P Value

Mean Age: Months (Range)*5.4 (2.0–10.0)5.3 (2.0–10.0)5.8 (3.0–8.0).59

Male gender: No./Total No. (%) 24/36 (66.6)17/28 (60.7)7/8 (87.5).22

White Race: No./Total No. (%) 28/35 (80.0)22/27 (81.5)6/8 (75.0).65

Number of eyes: No./Total No. (%)62 (100.0)53 (85.5)9 (14.5)NA

Bilateral premacular hemorrhage: No./Total No. (%) 26/36 (72.2)20/28 (71.4)6/8 (75.0)> .99

Baseline Neurologic Comorbidities: No./Total No. (%)
  Intracranial hemorrhage26/36 (72.2)22/28 (78.6)4/8 (50.0).18
  Seizure disorder12/36 (33.3)10/28 (35.7)2/8 (25.0).69
  Cerebral visual impairment3/36 (8.3)1/28 (3.6)2/8 (25.0).12
  Hypoxic ischemic encephalopathy3/36 (8.3)2/28 (7.1)1/8 (12.5).54
  Developmental delay5/36 (13.9)3/28 (10.7)2/8 (25.0).30

Timing*
  Median duration of follow-up: months (IQR)6.0 (3.0–30.0)6.0 (3.0–20.3)15.0 (2.0–39.8).94
  Median time to resolution of premacular hemorrhage with observation or PPV: days (IQR)NA75.0 (60.0–120.0)54.5 (47.8–58.5).06

Final Visual and Anatomic Outcomes of 62 Eyes With Pre-Macular Hemorrhage Secondary to Non-Accidental Trauma That Was Managed With Observation or PPV at Most Recent Follow-Up

CharacteristicTotal Study Group (n = 62)Observed (n = 53, 85.5%)PPV (n = 9, 14.5%) *P Value
Baseline Visual Acuity (Fix and Follow or Better): No./Total No. (%)16/58 (27.6)14/50 (28.0)2/8 (25.0)> .99
Final Visual Acuity at Most Recent Follow Up (Fix and Follow or Better): No./Total No. (%)36/60 (60.0)32/51 (62.8)4/9 (44.4)0.46
Amblyopia: No./Total No. (%)8/58 (12.9)6/50 (11.3)2/8 (25.0)0.30
Strabismus: No./Total No. (%)6/58 (10.3)2/50 (4.0)4/8 (50.0).002
Posterior Segment Findings: No./Total No. (%)
  Optic atrophy23/59 (39.0)18/51 (35.3)5/8 (62.5).24
  Visibly separated internal limiting membrane2/59 (3.4)2/51 (3.9)0/8 (0)> .99
  Submacular scar or significant pigmentary changes17/59 (28.8)12/51 (23.5)5/8 (62.5).04
Authors

From School of Medicine, Emory University, Atlanta, Georgia (OEU); the Department of Ophthalmology, Emory University School of Medicine, Atlanta, Georgia (OEU, CRS, GBH, PR); and SK Retina, Sarasota, Florida (CRS).

A preliminary version of this manuscript was presented June 7, 2014, at Resident Research Day, Emory Eye Center in Atlanta, Georgia, and again in poster format on May 7, 2015, at The Association for Research in Vision and Ophthalmology (ARVO) Annual Meeting in Denver, Colorado.

Supported by National Eye Institute Core Grant P30 EY006360.

Dr. Rao is a consultant for and receives royalties from Vortex Surgical outside the submitted work. The remaining authors report no relevant financial disclosures.

Address correspondence to Prethy Rao, MD, MPH, Department of Ophthalmology, Emory University, 1365B Clifton Road, Atlanta, GA 30322; email: prethy.rao@emory.edu.

Received: July 29, 2020
Accepted: October 07, 2020

10.3928/23258160-20201202-06

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