- Email: [email protected]
Vitreous Hemorrhage in Children
Vitreous Hemorrhage in Children Marc J. Spirn, MD,1 Michael J. Lynn, MS,2 G. Baker Hubbard III, MD1 Purpose: To describe the presentations, etiologies, and visual outcomes of spontaneous and traumatic vitreous hemorrhage in children. Design: Retrospective case series of patients seen over 8 consecutive years. Participants: One hundred sixty-eight patients (186 eyes), younger than 18 years, with vitreous hemorrhage not secondary to active retinopathy of prematurity (ROP). Methods: Charts were reviewed and data were compiled with special attention to demographic information, diagnosis, examination findings, visual acuity (VA) on presentation and last follow-up, treatment type, and length of follow-up. Main Outcome Measures: Etiologies, presenting symptoms, initial and final VAs, and management modalities. Results: Among 168 patients (186 eyes), the most common presenting symptom was decreased VA in older patients and strabismus and nystagmus in younger patients. Seventy-three percent of cases occurred secondary to manifest and occult trauma, with blunt (29.6%) and penetrating (24.7%) trauma being most common. Twenty-seven percent of hemorrhages occurred spontaneously, with regressed ROP being most common. Of the cases, 90.5% were unilateral and 9.5% were bilateral. Shaken baby syndrome accounted for 50% of bilateral cases. The most common management modalities were observation (50.0%) and incisional surgery (45.7%), but frequency of management modality varied by etiology. Visual outcomes, which were limited by variable follow-up and nonstandardized acquisition, were poorest with penetrating trauma and best with regressed ROP. There was no statistical difference in severe vision loss between children older than 8 years and younger than 8. Conclusions: Pediatric vitreous hemorrhage may have multiple etiologies, but manifest and occult trauma are most common. Regressed ROP is a common cause of spontaneous vitreous hemorrhage. A substantial proportion of patients with vitreous hemorrhage had severe vision loss, but outcomes were highly dependent on underlying etiology. Ophthalmology 2006;113:848 – 852 © 2006 by the American Academy of Ophthalmology.
The etiologies, clinical features, and management strategies for vitreous hemorrhage (VH) have been well described in adults.1,2 In children, however, VH is uncommon, and although multiple etiologies have been reported,3–20 most of the published studies are case reports or small series describing a particular etiology or treatment modality. As a result, little is known about the relative frequency of different causes, common presenting signs and symptoms, visual outcomes, and most frequent treatment modalities of VH in children. Originally received: March 13, 2005. Accepted: December 15, 2005. Manuscript no. 2005-228. 1 Department of Ophthalmology, Emory University School of Medicine, Atlanta, Georgia. 2 Department of Biostatistics, Rollins School of Public Health at Emory University, Atlanta, Georgia. Presented at: American Academy of Ophthalmology Annual Meeting, October 2004, New Orleans, Louisiana; Association for Research in Vision and Ophthalmology Annual Meeting, April 2004, Fort Lauderdale, Florida; Emory Eye Center Resident’s Day, June 2005, Atlanta, Georgia; and Association of Pediatric Retinal Surgeons meeting, January 2005, Duck Key, Florida. Supported in part by an unrestricted grant from Research to Prevent Blindness, New York, New York. The authors have no related commercial or financial interests. Correspondence and reprint requests to G. Baker Hubbard, MD, Emory Eye Center, 1365-B Clifton Road, NE, Atlanta, GA 30322. E-mail: [email protected].
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© 2006 by the American Academy of Ophthalmology Published by Elsevier Inc.
Multiple factors may cause children to differ from adults in these areas. Outcomes after VH in children likely are, as in adults, significantly dependent upon the underlying condition that gave rise to the hemorrhage. However, because of the inability of children to verbalize complaints and because of the immaturity of the visual system, children may be more likely to manifest strabismus, nystagmus, or other findings. Additionally, in children younger than 9 years, visual deprivation from VH may also result in amblyopia, which further impacts final vision independently from the underlying condition.21 In the current study, we look at features of VHs in children. We report the clinical features, etiologies, management strategies, and visual acuity (VA) outcomes for VH in children seen at the Emory Eye Center over an 8-year period. We also analyze VA outcomes and compare patients ⬍8 years old with those ⱖ8 years old.
Patients and Methods This study was approved by the institutional review board of the Emory University School of Medicine. Patients were identified by a computerized search of the Emory Eye Center database for patients younger than 18 years with the International Classification of Diseases 9 diagnostic code of VH. After reviewing all charts, infants with active stages of retinopathy of prematurity (ROP) were excluded because the great majority of these are examined in ISSN 0161-6420/06/$–see front matter doi:10.1016/j.ophtha.2005.12.027
Spirn et al 䡠 Vitreous Hemorrhage in Children a neonatal intensive care unit at an outside facility. We believe that an analysis of the subset of these patients evaluated in the outpatient clinics of the Emory Eye Center would not be representative of this diagnostic group and is best performed as a separate study. A detailed retrospective chart review was performed, and data were compiled using a specially prepared form. Data tabulated included demographic information, laterality, presenting symptoms and signs, initial and final VAs (best spectacle-corrected or pinhole-corrected acuity), other examination findings, diagnosis, associated ocular conditions, treatment type and date, and total length of follow-up. Data were analyzed with particular emphasis on the above factors. A 1-tailed z test was utilized to assess statistical significance. For statistical analysis, Snellen acuities were converted to logarithm of the minimum angle of resolution vision. To do so, counting fingers vision was considered equal to 20/2000, hand movements vision equal to 20/4000, light perception (LP) equal to 20/8000, and no LP equal to 20/16000.
Results From June 1, 1995 to June 1, 2003, there were 239 patients identified and 222 (92.8%) charts were available for review. Of these 222 patients, 19 were noted to have diagnoses other than VH (i.e., the billing diagnosis was incorrect), and 5 patients were found to have incomplete or insufficient charts making review impossible. Thirty infants were found to have had VH secondary to acute ROP and were excluded. Therefore, 168 patients (186 eyes) were included in the study. Demographic features are shown in Table 1. The mean age of diagnosis was 7.5 years, and males outnumbered females by 73.8% to 26.2%. Age on presentation varied by diagnosis, with shaken baby (mean age ⫽ 0.6 years) and birth trauma (mean age ⫽ 0.1 years) presenting earliest and pars planitis (mean age ⫽ 10.0 years), nonpenetrating trauma (mean age ⫽ 10.8 years), and penetrating trauma (mean age ⫽ 9.9 years) presenting later. The most common presenting signs and symptoms by age are shown in Figure 1. Presenting signs and symptoms were available in 80 of 168 patients. In patients in whom presenting signs and symptoms were noted, decreased vision (72.5%) was the most frequent complaint. Other less common presentations included strabismus (12.5%), abnormal pupillary reflex (10.0%), pain (10.0%), behavioral change (8.8%), nystagmus (7.5%), and floaters (6.3%). Ten patients (12.5%) had multiple signs or symptoms. There were 26 different causes of VHs (Table 2). Traumatic causes accounted for 73.1% of all VHs. These included nonpenetrating trauma (29.6%), penetrating trauma (24.7%), Table 1. Demographic Features of 168 Patients (186 Eyes) with Vitreous Hemorrhage Age (yrs) Mean Median Range Gender [no. of eyes (%)] Male Female Laterality [no. of eyes (%)] Unilateral Bilateral Involved eye [no. of eyes (%)] Right Left
7.5 8.2 0.01–17.9 124 (73.8) 44 (26.2) 152 (90.5) 16 (9.5) 92 (49.5) 94 (50.5)
Figure 1. Most common presenting signs/symptoms by age range. Data available on 80 eyes. VA ⫽ visual acuity.
shaken baby syndrome (8.6%), postocular surgery (5.4%), and birth trauma (4.8%). The mechanism of injury causing penetrating trauma was quite varied, ranging from motor vehicle collisions to self-inflicted bottle rocket and BB injuries. Of the penetrating trauma patients, 21.7% had a retained intraocular foreign body on examination. Diagnoses of birth trauma were made when a full-term infant presented after an unusually Table 2. Causes of Vitreous Hemorrhage No. of Eyes (%) Traumatic Nonpenetrating trauma Penetrating trauma Shaken baby syndrome Postoperative Birth trauma Spontaneous Regressed ROP Idiopathic No associations Associated with Marfan’s syndrome Peters’ anomaly Microphthalmos Encephalopathy FEVR Pars planitis PFV Retinoblastoma Terson’s syndrome Valsalva Astrocytoma Cavernous hemangioma Choroidal melanoma Ciliary body neovascularization Coats’ disease Congenital cytomegalovirus Eales’ disease Norrie’s disease Posterior uveitis Radiation retinopathy Thrombocytopenia Total retinal detachment X-linked juvenile retinoschisis
136 (73.1) 55 (29.6) 46 (24.7) 16 (8.6) 10 (5.4) 9 (4.8) 50 (26.9) 11 (5.9) 9 (4.8) 3 (1.6) 1 (0.5) 2 (1.1) 1 (0.5) 2 (1.1) 4 (2.2) 4 (2.2) 3 (1.6) 2 (1.1) 2 (1.1) 2 (1.1) 1 (0.5) 1 (0.5) 1 (0.5) 1 (0.5) 1 (0.5) 1 (0.5) 1 (0.5) 1 (0.5) 1 (0.5) 1 (0.5) 1 (0.5) 1 (0.5) 1 (0.5)
FEVR ⫽ familial exudative vitreoretinopathy; PFV ⫽ persistent fetal vasculature; ROP ⫽ retinopathy of prematurity.
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Ophthalmology Volume 113, Number 5, May 2006 difficult or prolonged delivery with a fully vascularized retina, VH, and no other pertinent pathology. In one case, for example, the umbilical cord was noted to be wrapped around the newborn’s neck 5 times. Spontaneous etiologies comprised 26.9% of all VHs. More common spontaneous causes included regressed ROP (5.9%), familial exudative vitreoretinopathy (FEVR) (2.2%), pars planitis (2.2%), and idiopathic causes (4.8%). The idiopathic group of patients was further broken down into idiopathic with no other associated eye findings (1.6%), with associated Marfan’s syndrome and a subluxated lens (0.5%), with associated Peters’ anomaly (1.0%), with associated microphthalmos (0.5%), and with associated encephalopathy related to meconium aspiration (1.0%). In this series, there were 13 diagnostic categories containing only one patient each. In this series, 90.5% (n ⫽ 152) of patients had unilateral involvement, while 9.5% (n ⫽ 16) had bilateral involvement. Nine diagnoses accounted for the 16 patients with bilateral involvement. The most common diagnosis with bilateral presentation was shaken baby syndrome. All patients with shaken baby syndrome had bilateral involvement and accounted for 50.0% of the bilateral cases. Seven other diagnoses had 1 patient each with bilateral hemorrhage. Males outnumbered females in 7 of the 8 most common diagnoses as well as in the total group. This male–female difference differed statistically for the total population of patients, penetrating trauma, nonpenetrating trauma, regressed ROP, FEVR, and pars planitis. Observation (50.0%) was the most common treatment modality (Fig 2). Incisional surgery, comprised of vitrectomy, scleral buckle, or enucleation, was performed in 45.7% of patients. Nonincisional laser or cryotherapy was elected in 4.3% of patients. Whereas nonpenetrating trauma was most often observed (74.5%), penetrating trauma commonly required incisional surgical treatment (82.6%). Pars planitis was most likely to be treated with laser or cryotherapy (75.0%). In this series, birth trauma was always observed, whereas shaken baby syndrome patients and postoperative patients equally were observed and underwent surgery. Nine of 10 (90.0%) penetrating trauma patients with an intraocular foreign body underwent incisional surgery. The one patient who was observed presented with no LP vision and an inert foreign
Observation Incisional Non-incisional
Pe n N on etra -p t en ing et tr a ra tin um a g Sh trau ak m a R eg en ba re by ss ed RO Po P st B irt -o p h tr Pa au m rs pl a an iti s FE VR
100 90 80 70 60 50 40 30 20 10 0
body. Enucleation was performed in only 2 cases in this series. In both cases, patients presented with no LP vision after penetrating trauma and retained the intraocular foreign body. Enucleation was elected in these cases in an effort to mitigate the risk of sympathetic ophthalmia. Mean total follow up was 16 months (range, 0-116). Familial exudative vitreoretinopathy had the longest follow-up duration (mean ⫽ 4.5 years), and birth trauma had the shortest mean follow-up period (mean ⫽ 0.2 years). Among the 69 patients able to read Snellen vision charts and observed for at least 3 months, the overall initial VA was 20/40 or better in 8.7%, between 20/50 and 20/400 in 17.4%, and worse than 20/400 in 73.9% of patients. The final VA was 20/40 or better in 36.2%, 20/50 to 20/400 in 28.9%, and worse than 20/400 in 34.8% of patients. For our population as a whole, the mean overall initial VA was 20/1665, and the mean overall final VA was 20/277. Among all 26 different diagnostic groups, 5 groups had ⱖ4 patients with Snellen VAs on initial and final visits that allowed for calculation of a mean VA. These patients included those with VHs secondary to penetrating trauma, nonpenetrating trauma, regressed ROP, pars planitis, and postoperative patients. Among these groups, penetrating trauma (mean initial Snellen ⫽ 20/5170, mean final Snellen ⫽ 20/582) and postoperative patients (mean initial Snellen ⫽ 20/4756, mean final Snellen ⫽ 20/211) presented with the worst initial VAs but overall had the most improvement in total vision on last followup. Nonpenetrating trauma (mean initial Snellen ⫽ 20/1225, mean final Snellen ⫽ 20/134) and pars planitis (mean initial Snellen ⫽ 20/502, mean final Snellen ⫽ 20/112) patients presented with and ended up with moderately better overall acuity. Regressed ROP (mean initial Snellen ⫽ 20/27, mean final Snellen ⫽ 20/31) patients presented with the best overall VA but showed little overall improvement in VA from presentation to last follow-up. Among 103 patients, severe visual loss, defined as ⱕ20/800 Snellen VA, no blink to light, or no fix and follow on last follow-up examination, occurred slightly more often in children younger than 8 years (n ⫽ 21) than in children over 8 (n ⫽ 19) (P ⫽ 0.128). Severe vision loss occurred in a total of 40 eyes (38.8%) of patients observed for ⱖ3 months. Although 12
Figure 2. Treatment modalities by etiology. FEVR ⫽ familial exudative vitreoretinopathy; ROP ⫽ retinopathy of prematurity.
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Spirn et al 䡠 Vitreous Hemorrhage in Children Table 3. Etiologies of Severe Visual Loss* †
No. of Eyes (% of Total Severe Visual Loss Cases) Penetrating trauma Nonpenetrating trauma Postoperative FEVR Retinoblastoma Idiopathic, associated with Peters’ anomaly Neovascularization of the ciliary body Pars planitis Regressed retinopathy of prematurity Shaken baby syndrome X-linked juvenile retinoschisis
16 (40.0) 5 (12.5) 4 (10.0) 3 (7.5) 2 (5.0) 2 (5.0) 1 (2.5) 1 (2.5) 1 (2.5) 1 (2.5) 1 (2.5)
FEVR ⫽ familial exudative vitreoretinopathy. *Severe vision loss defined as ⱕ20/800, no blink to light, or no fix-andfollow visual acuity. † Total no. of eyes ⫽ all eyes with recorded final visual acuity, regardless of whether initial visual acuity was measured.
etiologies resulted in severe visual loss, penetrating trauma was the most common single cause, accounting for 40.0% of eyes (Table 3).
Discussion Dana et al showed that, in a predominantly adult urban population with 96% of patients older than 10 years, the common causes of VH were proliferative diabetic retinopathy (35.2%), trauma (18.3%), vein occlusion (7.4%), retinal tear without detachment (7.0%), posterior vitreous detachment (6.5%), proliferative sickle retinopathy (5.7%), and retinal tear with detachment (4.8%).2 In the 4% of their patients under 10, trauma was the sole cause of VH. In the present study, which exclusively evaluated children under 18, there were many potential traumatic and spontaneous etiologies for VHs in children. Over a span of 8 years, there were 26 different causes of VH in our population. Trauma— penetrating and nonpenetrating—accounted for the vast majority of cases (54.3% combined). When combined with occult causes of trauma—namely, shaken baby syndrome and birth trauma—and postoperative patients, all trauma accounted for approximately 75% of cases. Spontaneous causes made up approximately 25% of cases, with regressed ROP being most frequent. Other relatively common causes included FEVR and pars planitis. Three etiologic groups deserve special attention. First is the group with regressed ROP. Although active ROP is a known cause of VH in the infant population,22,23 VH presenting later in life from previously quiescent ROP has received little attention in the English literature. These patients account for a significant minority of our population (5.9%), representing the most frequent cause of spontaneous VHs. The second group deserving special mention is the one that presented with bilateral VHs. Of all patients, 9.5% had bilateral VHs. Although there were 9 different diagnoses that accounted for the bilateral hemorrhages, shaken baby
syndrome comprised 50% of all bilateral cases. In our population, shaken baby syndrome totaled 8.6% of all cases, a significant percentage. This diagnosis should be considered in very young patients (mean age ⫽ 0.6 years) and especially in the setting of bilateral VH. It was the most common cause of bilateral hemorrhage in our series, and there were no cases of unilateral hemorrhage due to shaking. The third group that deserves special attention is the idiopathic group. A total of 7 patients (4.1%) developed VH without an inciting event or obvious disease entity. Although in 3 of these patients the cause was truly idiopathic— because no associated ocular findings or disease states were present—in the 4 other cases VH occurred in association with Marfan’s syndrome (n ⫽ 1), Peter’s anomaly (n ⫽ 1), microphthalmos (n ⫽ 1), and encephalopathy after meconium aspiration (n ⫽ 1). What is most important about this group is its relative rarity. Overall, over 95% of patients had the cause of their VH determined, suggesting that most cases of VH in children have an identifiable cause. Just as etiologies differed in children relative to adults, presenting signs and symptoms in these children also differed from those found in adults. When broken down by age, it is clear that the oldest children (⬎9 years) most frequently presented with decreased vision, floaters, and pain. This older group more closely parallels signs and symptoms seen in adults, where floaters and decreased vision are most prevalent. In contrast, the youngest children (⬍3 years) most frequently presented with strabismus, nystagmus, abnormal pupillary reflex, or behavioral change. Unlike adults and older children, VH in young children may insult the developing visual system, making them more likely to manifest strabismus or nystagmus. Our finding of 47.3% of patients without documented signs or symptoms is a result of multiple factors. First, younger children are more likely unable to explain their symptoms, resulting in a disproportionately high percentage of patients who do not express physical symptoms. Second, a majority of patients in this study had VHs noted incidentally on examination (e.g., during comprehensive eye examination after trauma) or were referred from an outside physician already with a diagnosis of VH. These patients frequently noted a chief complaint consistent with their injury or their referring diagnosis. More detailed documentation in some of these patients likely would have yielded more precise symptoms. On the whole, visual outcomes in this series were poor, with a mean final VA of 20/277 for patients able to read Snellen charts with ⬎3 months’ follow-up. Severe vision loss, defined in this series as Snellen VA of 20/800 or worse, no fixation behavior, or no blink to light, occurred in 40 of 103 eyes followed for ⱖ3 months. We found that, as expected, visual outcomes were highly dependent on the underlying etiology of the VH, with some diagnostic categories doing quite well and others quite poorly. Regressed ROP, for example, had a mean final VA of 20/31, whereas penetrating trauma had a mean final VA of 20/582. It is important to note that our VA data were limited by several factors. Because of the retrospective nature of this study, best-corrected VAs were not obtained in a standardized
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Ophthalmology Volume 113, Number 5, May 2006 fashion, nor were acuities obtained at scheduled follow-up visits. Furthermore, using last follow-up vision when patients were observed for varying lengths of time may introduce bias by either underestimating or overestimating achievable VA.24 We hypothesized that there would be a correlation between patient age and final vision in this study. Visual deprivation in younger children would be expected to exacerbate any underlying pathology associated with VH and might result in worse outcomes in younger children susceptible to deprivation amblyopia. Our data do show a higher percentage of younger children with severe visual loss compared with older children, but this difference was not statistically significant. The likely explanation for why our data do not show significantly worse outcomes in younger children is that there are numerous confounding factors in this retrospective study of VH due to multiple etiologies. Older children, for example, make up a larger percentage of patients with VH due to penetrating trauma, and penetrating trauma in our series connotes a poor prognosis for vision. Other limitations of this study include its retrospective nature and the fact that the study was conducted at a tertiary referral center. Our population, therefore, may not reflect the typical patient population of clinicians in the private setting. In summary, this study demonstrates that there are multiple different etiologies causing VH in the pediatric population. Manifest and occult traumas were the most common overall, and regressed ROP was the most frequent spontaneous cause. In very young children, shaken baby syndrome and birth trauma should be considered, with shaken baby syndrome being particularly likely in bilateral cases. Presenting symptoms may differ from those of adults, especially if the child is young. Outcomes in children with VH were generally poor and appear to be more dependent on etiology than age.
References 1. Spraul CW, Grossniklaus HE. Vitreous hemorrhage. Surv Ophthalmol 1997;42:3–39. 2. Dana MR, Werner MS, Viana MA, Shapiro MJ. Spontaneous and traumatic vitreous hemorrhage. Ophthalmology 1993;100: 1377– 83. 3. Simon J, Sood S, Yoon MK, et al. Vitrectomy for dense vitreous hemorrhage in infancy. J Pediatr Ophthalmol Strabismus 2005:42:18 –22. 4. Ferrone PJ, de Juan E Jr. Vitreous hemorrhage in infants. Arch Ophthalmol 1994;112:1185–9. 5. Braendstrup P. Vitreous haemorrhage in the newborn. A rare type of neonatal intraocular haemorrhage. Acta Ophthalmol (Copenh) 1969;47:502–13.
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6. Lauer AK, Smith JR, Robertson JE, Rosenbaum JT. Vitreous hemorrhage is a common complication of pediatric pars planitis. Ophthalmology 2002;109:95– 8. 7. Cekic O, Totan Y, Batman C. Traumatic vitreous hemorrhage from a persistent hyaloid artery. J Pediatr Ophthalmol Strabismus 2000;37:117– 8. 8. Levy HL, Brown AE, Williams SE, de Juan E Jr. Vitreous hemorrhage as an ophthalmic complication of galactosemia. J Pediatr 1996;129:922–5. 9. Mohney BG. Axial myopia associated with dense vitreous hemorrhage of the neonate. J AAPOS 2002;6:348 –53. 10. Hattenbach LO, Beeg T, Kreuz W, Zubcov A. Ophthalmic manifestation of congenital protein C deficiency. J AAPOS 1999;3:188 –90. 11. Kumar P, Ferrone PJ, Fox J, Koppel R. Bilateral cataracts, retinal detachment and vitreous hemorrhage in a newborn with congenital diaphragmatic hernia. J Perinatol 2003;23:565– 6. 12. Kurz D, Ciulla TA. Leber congenital amaurosis associated with optic disk neovascularization and vitreous hemorrhage. Am J Ophthalmol 2003;135:723–5. 13. Noel LP, Botash AS, DeSilva A. Maternal antiphospholipid antibodies and vitreous hemorrhages in the newborn: a case report. Arch Ophthalmol 2001;119:914 – 6. 14. Costa E, Lopes AA, Sacramento E, Santos PA. Massive ocular hemorrhage resulting in blindness in a patient with the sickle cell trait who developed leptospirosis. Case report. Rev Inst Med Trop Sao Paulo 2000;42:287–9. 15. Marshman WE, Adams GG, Ohri R. Bilateral vitreous hemorrhages in an infant with low fibrinogen levels. J AAPOS 1999;3:255– 6. 16. Reddy SC, Menon BS. A prospective study of ocular manifestations in childhood acute leukaemia. Acta Ophthalmol Scand 1998;76:700 –3. 17. Ferrone PJ, Trese MT, Lewis H. Vitreoretinal surgery for complications of congenital retinoschisis. Am J Ophthalmol 1997;123:742–7. 18. Paciuc M, Garcia-Alonso P, Moragrega E. Hyphema and vitreous hemorrhage in a newborn [letter]. Ophthalmic Surg 1988;19:680. 19. Pulido JS, Lingua RW, Cristol S, Byrne SF. Protein C deficiency associated with vitreous hemorrhage in a neonate. Am J Ophthalmol 1987;104:546 –7. 20. Onder F, Cossar CB, Gultan E, Kural G. Vitreous hemorrhage from the persistent hyaloid artery. J AAPOS 2000;4:190 –1. 21. Lambert SR, Boothe RG. Amblyopia: basic and clinical science perspectives. Focal Points 1994;12:1–7. 22. Hutcheson KA, Nguyen AT, Preslan MW, et al. Vitreous hemorrhage in patients with high-risk retinopathy of prematurity. Am J Ophthalmol 2003;136:258 – 63. 23. Kwok AK, So AK, Lam SW, et al. Can vitreous haemorrhage indicate non-accidental injury if mild retinopathy of prematurity is present? Eye 2000;14:812–3. 24. DiLoreto DA Jr, Bressler NM, Bressler SB, Schachat AP. Use of best and final visual acuity outcomes in ophthalmological research. Arch Ophthalmol 2003;121:1586 –90.
The etiologies, clinical features, and management strategies for vitreous hemorrhage (VH) have been well described in adults.1,2 In children, however, VH is uncommon, and although multiple etiologies have been reported,3–20 most of the published studies are case reports or small series describing a particular etiology or treatment modality. As a result, little is known about the relative frequency of different causes, common presenting signs and symptoms, visual outcomes, and most frequent treatment modalities of VH in children. Originally received: March 13, 2005. Accepted: December 15, 2005. Manuscript no. 2005-228. 1 Department of Ophthalmology, Emory University School of Medicine, Atlanta, Georgia. 2 Department of Biostatistics, Rollins School of Public Health at Emory University, Atlanta, Georgia. Presented at: American Academy of Ophthalmology Annual Meeting, October 2004, New Orleans, Louisiana; Association for Research in Vision and Ophthalmology Annual Meeting, April 2004, Fort Lauderdale, Florida; Emory Eye Center Resident’s Day, June 2005, Atlanta, Georgia; and Association of Pediatric Retinal Surgeons meeting, January 2005, Duck Key, Florida. Supported in part by an unrestricted grant from Research to Prevent Blindness, New York, New York. The authors have no related commercial or financial interests. Correspondence and reprint requests to G. Baker Hubbard, MD, Emory Eye Center, 1365-B Clifton Road, NE, Atlanta, GA 30322. E-mail: [email protected].
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© 2006 by the American Academy of Ophthalmology Published by Elsevier Inc.
Multiple factors may cause children to differ from adults in these areas. Outcomes after VH in children likely are, as in adults, significantly dependent upon the underlying condition that gave rise to the hemorrhage. However, because of the inability of children to verbalize complaints and because of the immaturity of the visual system, children may be more likely to manifest strabismus, nystagmus, or other findings. Additionally, in children younger than 9 years, visual deprivation from VH may also result in amblyopia, which further impacts final vision independently from the underlying condition.21 In the current study, we look at features of VHs in children. We report the clinical features, etiologies, management strategies, and visual acuity (VA) outcomes for VH in children seen at the Emory Eye Center over an 8-year period. We also analyze VA outcomes and compare patients ⬍8 years old with those ⱖ8 years old.
Patients and Methods This study was approved by the institutional review board of the Emory University School of Medicine. Patients were identified by a computerized search of the Emory Eye Center database for patients younger than 18 years with the International Classification of Diseases 9 diagnostic code of VH. After reviewing all charts, infants with active stages of retinopathy of prematurity (ROP) were excluded because the great majority of these are examined in ISSN 0161-6420/06/$–see front matter doi:10.1016/j.ophtha.2005.12.027
Spirn et al 䡠 Vitreous Hemorrhage in Children a neonatal intensive care unit at an outside facility. We believe that an analysis of the subset of these patients evaluated in the outpatient clinics of the Emory Eye Center would not be representative of this diagnostic group and is best performed as a separate study. A detailed retrospective chart review was performed, and data were compiled using a specially prepared form. Data tabulated included demographic information, laterality, presenting symptoms and signs, initial and final VAs (best spectacle-corrected or pinhole-corrected acuity), other examination findings, diagnosis, associated ocular conditions, treatment type and date, and total length of follow-up. Data were analyzed with particular emphasis on the above factors. A 1-tailed z test was utilized to assess statistical significance. For statistical analysis, Snellen acuities were converted to logarithm of the minimum angle of resolution vision. To do so, counting fingers vision was considered equal to 20/2000, hand movements vision equal to 20/4000, light perception (LP) equal to 20/8000, and no LP equal to 20/16000.
Results From June 1, 1995 to June 1, 2003, there were 239 patients identified and 222 (92.8%) charts were available for review. Of these 222 patients, 19 were noted to have diagnoses other than VH (i.e., the billing diagnosis was incorrect), and 5 patients were found to have incomplete or insufficient charts making review impossible. Thirty infants were found to have had VH secondary to acute ROP and were excluded. Therefore, 168 patients (186 eyes) were included in the study. Demographic features are shown in Table 1. The mean age of diagnosis was 7.5 years, and males outnumbered females by 73.8% to 26.2%. Age on presentation varied by diagnosis, with shaken baby (mean age ⫽ 0.6 years) and birth trauma (mean age ⫽ 0.1 years) presenting earliest and pars planitis (mean age ⫽ 10.0 years), nonpenetrating trauma (mean age ⫽ 10.8 years), and penetrating trauma (mean age ⫽ 9.9 years) presenting later. The most common presenting signs and symptoms by age are shown in Figure 1. Presenting signs and symptoms were available in 80 of 168 patients. In patients in whom presenting signs and symptoms were noted, decreased vision (72.5%) was the most frequent complaint. Other less common presentations included strabismus (12.5%), abnormal pupillary reflex (10.0%), pain (10.0%), behavioral change (8.8%), nystagmus (7.5%), and floaters (6.3%). Ten patients (12.5%) had multiple signs or symptoms. There were 26 different causes of VHs (Table 2). Traumatic causes accounted for 73.1% of all VHs. These included nonpenetrating trauma (29.6%), penetrating trauma (24.7%), Table 1. Demographic Features of 168 Patients (186 Eyes) with Vitreous Hemorrhage Age (yrs) Mean Median Range Gender [no. of eyes (%)] Male Female Laterality [no. of eyes (%)] Unilateral Bilateral Involved eye [no. of eyes (%)] Right Left
7.5 8.2 0.01–17.9 124 (73.8) 44 (26.2) 152 (90.5) 16 (9.5) 92 (49.5) 94 (50.5)
Figure 1. Most common presenting signs/symptoms by age range. Data available on 80 eyes. VA ⫽ visual acuity.
shaken baby syndrome (8.6%), postocular surgery (5.4%), and birth trauma (4.8%). The mechanism of injury causing penetrating trauma was quite varied, ranging from motor vehicle collisions to self-inflicted bottle rocket and BB injuries. Of the penetrating trauma patients, 21.7% had a retained intraocular foreign body on examination. Diagnoses of birth trauma were made when a full-term infant presented after an unusually Table 2. Causes of Vitreous Hemorrhage No. of Eyes (%) Traumatic Nonpenetrating trauma Penetrating trauma Shaken baby syndrome Postoperative Birth trauma Spontaneous Regressed ROP Idiopathic No associations Associated with Marfan’s syndrome Peters’ anomaly Microphthalmos Encephalopathy FEVR Pars planitis PFV Retinoblastoma Terson’s syndrome Valsalva Astrocytoma Cavernous hemangioma Choroidal melanoma Ciliary body neovascularization Coats’ disease Congenital cytomegalovirus Eales’ disease Norrie’s disease Posterior uveitis Radiation retinopathy Thrombocytopenia Total retinal detachment X-linked juvenile retinoschisis
136 (73.1) 55 (29.6) 46 (24.7) 16 (8.6) 10 (5.4) 9 (4.8) 50 (26.9) 11 (5.9) 9 (4.8) 3 (1.6) 1 (0.5) 2 (1.1) 1 (0.5) 2 (1.1) 4 (2.2) 4 (2.2) 3 (1.6) 2 (1.1) 2 (1.1) 2 (1.1) 1 (0.5) 1 (0.5) 1 (0.5) 1 (0.5) 1 (0.5) 1 (0.5) 1 (0.5) 1 (0.5) 1 (0.5) 1 (0.5) 1 (0.5) 1 (0.5) 1 (0.5)
FEVR ⫽ familial exudative vitreoretinopathy; PFV ⫽ persistent fetal vasculature; ROP ⫽ retinopathy of prematurity.
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Ophthalmology Volume 113, Number 5, May 2006 difficult or prolonged delivery with a fully vascularized retina, VH, and no other pertinent pathology. In one case, for example, the umbilical cord was noted to be wrapped around the newborn’s neck 5 times. Spontaneous etiologies comprised 26.9% of all VHs. More common spontaneous causes included regressed ROP (5.9%), familial exudative vitreoretinopathy (FEVR) (2.2%), pars planitis (2.2%), and idiopathic causes (4.8%). The idiopathic group of patients was further broken down into idiopathic with no other associated eye findings (1.6%), with associated Marfan’s syndrome and a subluxated lens (0.5%), with associated Peters’ anomaly (1.0%), with associated microphthalmos (0.5%), and with associated encephalopathy related to meconium aspiration (1.0%). In this series, there were 13 diagnostic categories containing only one patient each. In this series, 90.5% (n ⫽ 152) of patients had unilateral involvement, while 9.5% (n ⫽ 16) had bilateral involvement. Nine diagnoses accounted for the 16 patients with bilateral involvement. The most common diagnosis with bilateral presentation was shaken baby syndrome. All patients with shaken baby syndrome had bilateral involvement and accounted for 50.0% of the bilateral cases. Seven other diagnoses had 1 patient each with bilateral hemorrhage. Males outnumbered females in 7 of the 8 most common diagnoses as well as in the total group. This male–female difference differed statistically for the total population of patients, penetrating trauma, nonpenetrating trauma, regressed ROP, FEVR, and pars planitis. Observation (50.0%) was the most common treatment modality (Fig 2). Incisional surgery, comprised of vitrectomy, scleral buckle, or enucleation, was performed in 45.7% of patients. Nonincisional laser or cryotherapy was elected in 4.3% of patients. Whereas nonpenetrating trauma was most often observed (74.5%), penetrating trauma commonly required incisional surgical treatment (82.6%). Pars planitis was most likely to be treated with laser or cryotherapy (75.0%). In this series, birth trauma was always observed, whereas shaken baby syndrome patients and postoperative patients equally were observed and underwent surgery. Nine of 10 (90.0%) penetrating trauma patients with an intraocular foreign body underwent incisional surgery. The one patient who was observed presented with no LP vision and an inert foreign
Observation Incisional Non-incisional
Pe n N on etra -p t en ing et tr a ra tin um a g Sh trau ak m a R eg en ba re by ss ed RO Po P st B irt -o p h tr Pa au m rs pl a an iti s FE VR
100 90 80 70 60 50 40 30 20 10 0
body. Enucleation was performed in only 2 cases in this series. In both cases, patients presented with no LP vision after penetrating trauma and retained the intraocular foreign body. Enucleation was elected in these cases in an effort to mitigate the risk of sympathetic ophthalmia. Mean total follow up was 16 months (range, 0-116). Familial exudative vitreoretinopathy had the longest follow-up duration (mean ⫽ 4.5 years), and birth trauma had the shortest mean follow-up period (mean ⫽ 0.2 years). Among the 69 patients able to read Snellen vision charts and observed for at least 3 months, the overall initial VA was 20/40 or better in 8.7%, between 20/50 and 20/400 in 17.4%, and worse than 20/400 in 73.9% of patients. The final VA was 20/40 or better in 36.2%, 20/50 to 20/400 in 28.9%, and worse than 20/400 in 34.8% of patients. For our population as a whole, the mean overall initial VA was 20/1665, and the mean overall final VA was 20/277. Among all 26 different diagnostic groups, 5 groups had ⱖ4 patients with Snellen VAs on initial and final visits that allowed for calculation of a mean VA. These patients included those with VHs secondary to penetrating trauma, nonpenetrating trauma, regressed ROP, pars planitis, and postoperative patients. Among these groups, penetrating trauma (mean initial Snellen ⫽ 20/5170, mean final Snellen ⫽ 20/582) and postoperative patients (mean initial Snellen ⫽ 20/4756, mean final Snellen ⫽ 20/211) presented with the worst initial VAs but overall had the most improvement in total vision on last followup. Nonpenetrating trauma (mean initial Snellen ⫽ 20/1225, mean final Snellen ⫽ 20/134) and pars planitis (mean initial Snellen ⫽ 20/502, mean final Snellen ⫽ 20/112) patients presented with and ended up with moderately better overall acuity. Regressed ROP (mean initial Snellen ⫽ 20/27, mean final Snellen ⫽ 20/31) patients presented with the best overall VA but showed little overall improvement in VA from presentation to last follow-up. Among 103 patients, severe visual loss, defined as ⱕ20/800 Snellen VA, no blink to light, or no fix and follow on last follow-up examination, occurred slightly more often in children younger than 8 years (n ⫽ 21) than in children over 8 (n ⫽ 19) (P ⫽ 0.128). Severe vision loss occurred in a total of 40 eyes (38.8%) of patients observed for ⱖ3 months. Although 12
Figure 2. Treatment modalities by etiology. FEVR ⫽ familial exudative vitreoretinopathy; ROP ⫽ retinopathy of prematurity.
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Spirn et al 䡠 Vitreous Hemorrhage in Children Table 3. Etiologies of Severe Visual Loss* †
No. of Eyes (% of Total Severe Visual Loss Cases) Penetrating trauma Nonpenetrating trauma Postoperative FEVR Retinoblastoma Idiopathic, associated with Peters’ anomaly Neovascularization of the ciliary body Pars planitis Regressed retinopathy of prematurity Shaken baby syndrome X-linked juvenile retinoschisis
16 (40.0) 5 (12.5) 4 (10.0) 3 (7.5) 2 (5.0) 2 (5.0) 1 (2.5) 1 (2.5) 1 (2.5) 1 (2.5) 1 (2.5)
FEVR ⫽ familial exudative vitreoretinopathy. *Severe vision loss defined as ⱕ20/800, no blink to light, or no fix-andfollow visual acuity. † Total no. of eyes ⫽ all eyes with recorded final visual acuity, regardless of whether initial visual acuity was measured.
etiologies resulted in severe visual loss, penetrating trauma was the most common single cause, accounting for 40.0% of eyes (Table 3).
Discussion Dana et al showed that, in a predominantly adult urban population with 96% of patients older than 10 years, the common causes of VH were proliferative diabetic retinopathy (35.2%), trauma (18.3%), vein occlusion (7.4%), retinal tear without detachment (7.0%), posterior vitreous detachment (6.5%), proliferative sickle retinopathy (5.7%), and retinal tear with detachment (4.8%).2 In the 4% of their patients under 10, trauma was the sole cause of VH. In the present study, which exclusively evaluated children under 18, there were many potential traumatic and spontaneous etiologies for VHs in children. Over a span of 8 years, there were 26 different causes of VH in our population. Trauma— penetrating and nonpenetrating—accounted for the vast majority of cases (54.3% combined). When combined with occult causes of trauma—namely, shaken baby syndrome and birth trauma—and postoperative patients, all trauma accounted for approximately 75% of cases. Spontaneous causes made up approximately 25% of cases, with regressed ROP being most frequent. Other relatively common causes included FEVR and pars planitis. Three etiologic groups deserve special attention. First is the group with regressed ROP. Although active ROP is a known cause of VH in the infant population,22,23 VH presenting later in life from previously quiescent ROP has received little attention in the English literature. These patients account for a significant minority of our population (5.9%), representing the most frequent cause of spontaneous VHs. The second group deserving special mention is the one that presented with bilateral VHs. Of all patients, 9.5% had bilateral VHs. Although there were 9 different diagnoses that accounted for the bilateral hemorrhages, shaken baby
syndrome comprised 50% of all bilateral cases. In our population, shaken baby syndrome totaled 8.6% of all cases, a significant percentage. This diagnosis should be considered in very young patients (mean age ⫽ 0.6 years) and especially in the setting of bilateral VH. It was the most common cause of bilateral hemorrhage in our series, and there were no cases of unilateral hemorrhage due to shaking. The third group that deserves special attention is the idiopathic group. A total of 7 patients (4.1%) developed VH without an inciting event or obvious disease entity. Although in 3 of these patients the cause was truly idiopathic— because no associated ocular findings or disease states were present—in the 4 other cases VH occurred in association with Marfan’s syndrome (n ⫽ 1), Peter’s anomaly (n ⫽ 1), microphthalmos (n ⫽ 1), and encephalopathy after meconium aspiration (n ⫽ 1). What is most important about this group is its relative rarity. Overall, over 95% of patients had the cause of their VH determined, suggesting that most cases of VH in children have an identifiable cause. Just as etiologies differed in children relative to adults, presenting signs and symptoms in these children also differed from those found in adults. When broken down by age, it is clear that the oldest children (⬎9 years) most frequently presented with decreased vision, floaters, and pain. This older group more closely parallels signs and symptoms seen in adults, where floaters and decreased vision are most prevalent. In contrast, the youngest children (⬍3 years) most frequently presented with strabismus, nystagmus, abnormal pupillary reflex, or behavioral change. Unlike adults and older children, VH in young children may insult the developing visual system, making them more likely to manifest strabismus or nystagmus. Our finding of 47.3% of patients without documented signs or symptoms is a result of multiple factors. First, younger children are more likely unable to explain their symptoms, resulting in a disproportionately high percentage of patients who do not express physical symptoms. Second, a majority of patients in this study had VHs noted incidentally on examination (e.g., during comprehensive eye examination after trauma) or were referred from an outside physician already with a diagnosis of VH. These patients frequently noted a chief complaint consistent with their injury or their referring diagnosis. More detailed documentation in some of these patients likely would have yielded more precise symptoms. On the whole, visual outcomes in this series were poor, with a mean final VA of 20/277 for patients able to read Snellen charts with ⬎3 months’ follow-up. Severe vision loss, defined in this series as Snellen VA of 20/800 or worse, no fixation behavior, or no blink to light, occurred in 40 of 103 eyes followed for ⱖ3 months. We found that, as expected, visual outcomes were highly dependent on the underlying etiology of the VH, with some diagnostic categories doing quite well and others quite poorly. Regressed ROP, for example, had a mean final VA of 20/31, whereas penetrating trauma had a mean final VA of 20/582. It is important to note that our VA data were limited by several factors. Because of the retrospective nature of this study, best-corrected VAs were not obtained in a standardized
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Ophthalmology Volume 113, Number 5, May 2006 fashion, nor were acuities obtained at scheduled follow-up visits. Furthermore, using last follow-up vision when patients were observed for varying lengths of time may introduce bias by either underestimating or overestimating achievable VA.24 We hypothesized that there would be a correlation between patient age and final vision in this study. Visual deprivation in younger children would be expected to exacerbate any underlying pathology associated with VH and might result in worse outcomes in younger children susceptible to deprivation amblyopia. Our data do show a higher percentage of younger children with severe visual loss compared with older children, but this difference was not statistically significant. The likely explanation for why our data do not show significantly worse outcomes in younger children is that there are numerous confounding factors in this retrospective study of VH due to multiple etiologies. Older children, for example, make up a larger percentage of patients with VH due to penetrating trauma, and penetrating trauma in our series connotes a poor prognosis for vision. Other limitations of this study include its retrospective nature and the fact that the study was conducted at a tertiary referral center. Our population, therefore, may not reflect the typical patient population of clinicians in the private setting. In summary, this study demonstrates that there are multiple different etiologies causing VH in the pediatric population. Manifest and occult traumas were the most common overall, and regressed ROP was the most frequent spontaneous cause. In very young children, shaken baby syndrome and birth trauma should be considered, with shaken baby syndrome being particularly likely in bilateral cases. Presenting symptoms may differ from those of adults, especially if the child is young. Outcomes in children with VH were generally poor and appear to be more dependent on etiology than age.
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