Suprachoroidal hemorrhage (SCH) is the accumulation of blood within the potential space between the choroid and sclera. Most pathophysiological theories implicate hypotony precipitating sudden changes in the vascular gradient, decreased uveoscleral outflow, shearing of the choroidal vasculature (especially the substantially traversing long posterior ciliary arteries), and eventually rupture into the suprachoroidal space.1,2
SCH may occur intraoperatively (expulsive) or postoperatively as a delayed complication (DSCH) hours to months after surgery. Commonly recognized risk factors for SCH include older age, aphakia, glaucoma, choroidal anomalies commonly associated with oculocutaneous or syndromic disorders, hypertension or cardiovascular disease, and intraoperative tachycardia.3,4 Likewise, risk factors classically associated with DSCH include anticoagulation, axial myopia, and prior intraocular surgery.5,6 The occurrence of this complication remains difficult to approximate, as smaller hemorrhages may often go unrecognized or underreported in clinical records, and the incidence of SCH is likely variable based on the type of intraocular surgery performed.3 Based on the assessment of several studies, the reported incidence of SCH ranges from 0.06% to 1.8% in adults.7–9,10,11,12–14 The estimated incidence of SCH in younger patients is reported at 0.36% and is similarly most commonly associated with glaucoma surgery.15
Herein, we review cases of SCH occurring in either pediatric patients or eyes with a history of pediatric vitreoretinal disease at a single tertiary pediatric retina referral center (Associated Retinal Consultants, Royal Oak, MI), as well as present a discussion of pertinent risk factors and preferred management specific to SCH in younger patients.
A 20-year-old female with developmental delay and a history of retinopathy of prematurity (ROP) in both eyes (Stage 4A in the right eye [OD] status post laser and lens-sparing vitrectomy, and Stage 4B in the left eye [OS] status post three vitrectomies and lensectomy) underwent cataract surgery for a hyper-mature white cataract with superior zonular dehiscence OD. On postoperative day (POD) 1, her vision was light perception (LP) (baseline of hand motions [HM] vision) with an elevated intraocular pressure (IOP) by palpation. Examination disclosed a lens fragment in the anterior chamber with 3+ cell and flare, aphakia, and a vitreous hemorrhage (VH) with no view to the posterior pole OD. B-scan ultrasonography revealed non-appositional hemorrhagic choroidal detachments (Figure 1). She was managed conservatively with topical prednisolone acetate 1% and IOP-lowering drops for 1 week. Repeat B-scan showed an interval decrease in the size of the suprachoroidal hemorrhage. Given the persistent presence of the lens fragment, inflammation, VH, and SCH after 1 week, she underwent an anterior chamber washout, 20-gauge pars plicata vitrectomy, and a partial fluid-healon exchange, achieving a postoperative IOP of 12 mm Hg. The decision was made to not drain the suprachoroidal hemorrhage given its non-appositional nature and apparent proclivity toward self-resolution. At postoperative month (POM) 2, visual acuity returned to baseline of HM with an IOP of 13 mm Hg. The SCH had resolved entirely, and the posterior pole was attached.
B-scan ultrasonography of patient from Case 1 on postoperative day 1 disclosed non-appositional hemorrhagic choroidal detachments with vitreous hemorrhage (1).
A 5-year-old female with history of microspherophakia presented to her pediatric ophthalmologist with bilateral anterior cataractous lens subluxation OD and pupillary block glaucoma OS with IOP of 48 mm Hg. She underwent a lensectomy OS, which was complicated by an expulsive SCH. The patient was then referred to our pediatric retina service. At postoperative week 1, she exhibited new-onset pupillary block glaucoma with an IOP of 29 mm Hg OD (Figure 2A) and a relatively clear cornea, shallow anterior chamber, and an IOP of 5 mm Hg OS (Figure 2B). Ultrasound showed a fully attached retina OD, whereas fundus examination OS disclosed a large nasal suprachoroidal hemorrhage with an overlying hemorrhagic retinal attachment.
Examination under anesthesia of patient from Case 2 at postoperative week 1, where patient disclosed new onset of pupillary block glaucoma with intraocular pressure (IOP) of 29 mm Hg in the right eye (A) and a relatively clear cornea, shallow anterior chamber, and an IOP of 5 mm Hg in the left eye (B).
The decision was made to proceed with bilateral simultaneous surgery. For the left eye, an anterior chamber maintainer was first established followed by conjunctival peritomy, isolation of recti muscles, and an external equatorial sclerotomy with a 20-gauge myringotomy blade to drain the suprachoroidal hemorrhage. The nasal subretinal hemorrhage was left unaddressed. The right eye then underwent a pars plicata vitrectomy and lensectomy to relieve the pupillary block.
At POM 1, she was found to have a clear cornea with a deep anterior chamber, aphakia, and attached retina with a hypoplastic optic nerve OD (Figure 3A), and a clear cornea with a deep anterior chamber, aphakia, and a persistent VH OS with no posterior pole view. Repeat B-scan ultrasound disclosed VH, residual subretinal hemorrhage, and complete resolution of the SCH. Given the amblyogenic potential of the non-clearing VH, she underwent limbal-based 23-gauge vitrectomy. Posterior hyaloidal separation was not performed given its strong adherence to the retinal surface and the presence of a temporal hemorrhagic retinal detachment (RD). At POM 3, she had complete resolution of the hemorrhagic RD (Figure 3B) and correction for aphakia was performed by her pediatric ophthalmologist.
Examination under anesthesia of patient from Case 2 at postoperative month 1 showing an attached retina with a hypoplastic optic nerve in the right eye (A) and following subsequent surgery, an attached retina with resolution of the hemorrhagic retinal detachment in the left eye (B).
In adults, SCH has been observed in the context of nearly all types of intraocular surgeries.16–19 The reported incidence of SCH ranges from 0.06% to 1.8%,7–9,10,11,12–14 with the highest association with glaucoma surgery.20 SCH in younger patients also occurs most commonly in glaucoma surgery, based on a comprehensive review of the literature that revealed only nine reported cases of SCH amongst a total of 2,491 pediatric glaucoma surgeries, citing an incidence of 0.36% (Table 1).15,21–25 The most consistent risk factor for SCH in the younger population (exemplified by the cases herein) appears to be aphakia,5,15,26 as the absence of an intact lens-iris-diaphragm makes the eye more prone to pressure fluctuations.
Published Cases of SCH in Younger Patients (Ages 0 to 18 Years)
The choroidal and scleral anatomy of younger patients differs compared to adults. It is well-established that pediatric patients have a more elastic sclera than adults. Age-dependent loss of scleral elasticity is most evident in the peripapillary region and is accelerated by high IOP and in those of African descent.27 The choroid also appears to be thicker in children compared to adults, with progressive scleral thinning most associated with myopic refractive error, lower body mass index, and advancing age.28,29 Thus, the combination of higher scleral higher elasticity (which may result in more scleral in-folding with hypotony), and thicker choroid (which may result in more ciliochoroidal effusion with hypotony precipitating ciliary artery stretch) may predispose pediatric eyes to SCH. Despite this, SCH remains less commonly reported in younger patients. One protective mechanism against SCH may be the increased vascular capacitance in younger eyes, which is secondary to decreased collagen degradation and therefore increased elasticity. However, further studies are needed to support this hypothesis.
Hemostatic dynamic properties also differ in younger patients. Pediatric patients have prolonged prothrombin time and possibly activated partial thromboplastin time compared to adults, but this seems to be significant only within the first year of life.30,31,28 Aside from the first 6 months of life (where neonates have decreased plasminogen and impaired plasminogen activation), it does not appear that time to clot dissolution is significantly different than adults.32 These hemostatic properties argue toward observing SCH for a period of 7 to 14 days (for clot dissolution) as in adults prior to attempted surgical drainage.
As in adults, non-appositional SCH in younger patients may be initially observed in the absence of severe pain or IOP issues refractory to medical therapy (Case 1). Our experience is that non-appositional SCH tends to resolve by 8 weeks, and we will typically repeat B-scan ultrasonography at each visit, if possible. Indications for surgical drainage include high IOP and/or collapsed anterior chamber refractory to medical therapy, appositional choroidals, and the combined presence of SCH and hemorrhagic RD, which in our experience represents an additional indication for drainage in pediatric patients (Case 2).
When draining pediatric SCH, our approach involves a trans-zonular anterior chamber infusion followed by making equatorial radially oriented sclerotomies in each quadrant with a 20-gauge myringotomy blade. A cyclodialysis spatula massaging the inner lip of the wound may facilitate drainage. We do not typically instill perfluorocarbon liquid to facilitate SCH drainage. Subsequent vitrectomy is only performed if deemed necessary by concomitant pathology. A fluid-healon exchange at the end of the case may facilitate ongoing postoperative choroidal re-attachment. Despite the typically urgent presentation of SCH, based on our experience in the two cases presented, we believe younger patients with SCH may achieve anatomic stability with appropriate and timely intervention. The management of SCH in pediatric patients, based on the combination of approaches discussed herein, is nearly identical to the management of SCH in adults.
- Manschot WA. Expulsive hemorrhage: Two remarkable anatomical discoveries. Acta Ophthalmol. 2009;19(3–4):237–254. doi:10.1111/j.1755-3768.1941.tb04329.x [CrossRef]
- Chu TG, Green RL. Suprachoroidal hemorrhage. Surv Ophthalmol. 1999;43(6):471–486. doi:10.1016/S0039-6257(99)00037-5 [CrossRef]
- Chandra A, Xing W, Kadhim MR, Williamson TH. Suprachoroidal hemorrhage in pars plana vitrectomy: Risk factors and outcomes over 10 years. Ophthalmology. 2014;121(1):311–317. doi:10.1016/j.ophtha.2013.06.021 [CrossRef]
- Ling R, Kamalarajah S, Cole M, James C, Shaw S. Suprachoroidal haemorrhage complicating cataract surgery in the UK: A case control study of risk factors. Br J Ophthalmol. 2004;88(4):474–477. doi:10.1136/bjo.2003.026179 [CrossRef]
- Jeganathan VSE, Ghosh S, Ruddle JB, Gupta V, Coote MA, Crowston JG. Risk factors for delayed suprachoroidal haemorrhage following glaucoma surgery. Br J Ophthalmol. 2008;92(10):1393–1396. doi:10.1136/bjo.2008.141689 [CrossRef]
- Tuli SS, WuDunn D, Ciulla TA, Cantor LB. Delayed suprachoroidal hemorrhage after glaucoma filtration procedures. Ophthalmology. 2001;108(10):1808–1811. doi:10.1016/S0161-6420(01)00763-1 [CrossRef]
- Davison JA. Acute intraoperative suprachoroidal hemorrhage in capsular bag phacoemulsification. J Cataract Refract Surg. 1993;19(4):534–537. doi:10.1016/S0886-3350(13)80618-9 [CrossRef]
- Davison JA. Acute intraoperative suprachoroidal hemorrhage in extra-capsular cataract surgery. J Cataract Refract Surg. 1986;12(6):606–622. doi:10.1016/S0886-3350(86)80075-X [CrossRef]
- Taylor DM. Expulsive hemorrhage: Some observations and comments. Trans Am Ophthalmol Soc. 1974;72:157–169.
- Speaker MG, Guerriero PN, Met JA, Coad CT, Berger A, Marmor M. A case-control study of risk factors for intraoperative suprachoroidal expulsive hemorrhage. Ophthalmology. 1991;98(2):202–209; discussion 210. doi:10.1016/S0161-6420(91)32316-9 [CrossRef]
- Ingraham HJ, Donnenfeld ED, Perry HD. Massive suprachoroidal hemorrhage in penetrating keratoplasty. Am J Ophthalmol. 1989;108(6):670–675. doi:10.1016/0002-9394(89)90859-3 [CrossRef]
- Speaker MG, Guerriero PN, Met JA, Coad CT, Berger A, Marmor M. A case-control study of risk factors for intraoperative suprachoroidal expulsive hemorrhage. Ophthalmology. 1991;98(2):202–210. doi:10.1016/S0161-6420(91)32316-9 [CrossRef]
- Hawkins WR, Schepens CL. Choroidal detachment and retinal surgery: A clinical and experimental study. Am J Ophthalmol. 1966;62(5):813–819. doi:10.1016/0002-9394(66)91903-9 [CrossRef]
- Piper JG, Han DP, Abrams GW, Mieler WF. Perioperative choroidal hemorrhage at pars plana vitrectomy. Ophthalmology. 1993;100(5):699–704. doi:10.1016/S0161-6420(93)31586-1 [CrossRef]
- Ghadhfan FE, Khan AO. Delayed suprachoroidal hemorrhage after pediatric glaucoma surgery. J AAPOS. 2009;13(3):283–286. doi:10.1016/j.jaapos.2009.03.001 [CrossRef]
- Bandivadekar P, Gupta S, Sharma N. Intraoperative suprachoroidal hemorrhage after penetrating keratoplasty: case series and review of literature. Eye Contact Lens. 2016;42(3):206–210. doi:10.1097/ICL.0000000000000164 [CrossRef]
- Stein JD. Serious adverse events after cataract surgery. Curr Opin Ophthalmol. 2012;23(3):219–225. doi:10.1097/ICU.0b013e3283524068 [CrossRef]
- Givens K, Shields MB. Suprachoroidal hemorrhage after glaucoma filtering surgery. Am J Ophthalmol. 1987;103(5):689–694. doi:10.1016/S0002-9394(14)74331-4 [CrossRef]
- Lakhanpal V, Schocket SS, Elman MJ, Dogra MR. Intraoperative massive suprachoroidal hemorrhage during pars plana vitrectomy. Ophthalmology. 1990;97(9):1114–1119. doi:10.1016/S0161-6420(90)32448-X [CrossRef]
- Vaziri K, Schwartz SG, Kishor KS, et al. Incidence of postoperative suprachoroidal hemorrhage after glaucoma filtration surgeries in the United States. Clin Ophthalmol. 2015;9:579–584.
- Kafkala C, Hynes A, Choi J, Topalkara A, Foster CS. Ahmed valve implantation for uncontrolled pediatric uveitic glaucoma. J AAPOS. 2005;9(4):336–340. doi:10.1016/j.jaapos.2005.04.006 [CrossRef]
- Coleman AL, Smyth RJ, Wilson MR, Tam M. Initial clinical experience with the Ahmed Glaucoma Valve implant in pediatric patients. Arch Ophthalmol. 1997;115(2):186–191. doi:10.1001/archopht.1997.01100150188007 [CrossRef]
- Pakravan M, Homayoon N, Shahin Y, Ali Reza BR. Trabeculectomy with mitomycin C versus Ahmed glaucoma implant with mitomycin C for treatment of pediatric aphakic glaucoma. J Glaucoma. 2007;16(7):631–636. doi:10.1097/IJG.0b013e3180640f58 [CrossRef]
- Hill R, Ohanesian R, Voskanyan L, Malayan A. The Armenian Eye Care Project: Surgical outcomes of complicated paediatric glaucoma. Br J Ophthalmol. 2003;87(6):673–676. doi:10.1136/bjo.87.6.673 [CrossRef]
- Beck AD, Wilson WR, Lynch MG, Lynn MJ, Noe R. Trabeculectomy with adjunctive mitomycin C in pediatric glaucoma. Am J Ophthalmol. 1998;126(5):648–657. doi:10.1016/S0002-9394(98)00227-X [CrossRef]
- Duke R, Ikpeme A. Primary congenital glaucoma with delayed suprachoroidal hemorrhage following combined trabeculotomy trabeculectomy and 5-fluorouracil. Case Rep Ophthalmol Med. 2015;2015:163859.
- Grytz R, Fazio MA, Libertiaux V, et al. Age- and race-related differences in human scleral material properties. Invest Ophthalmol Vis Sci. 2014;55(12):8163–8172. doi:10.1167/iovs.14-14029 [CrossRef]
- Oesterling JE. Serum prostate-specific antigen in a community-based population of healthy men. Establishment of age-specific reference ranges. JAMA. 1993;270(7):860–864. doi:10.1001/jama.1993.03510070082041 [CrossRef]
- Nagasawa T, Mitamura Y, Katome T, et al. Macular choroidal thickness and volume in healthy pediatric individuals measured by swept-source optical coherence tomography. Invest Ophthalmol Vis Sci. 2013;54(10):7068–7074. doi:10.1167/iovs.13-12350 [CrossRef]
- Flanders MM, Crist RA, Roberts WL, Rodgers GM. Pediatric reference intervals for seven common coagulation assays. Clin Chem. 2005;51(9):1738–1742. doi:10.1373/clinchem.2005.050211 [CrossRef]
- Arslan FD, Serdar M, Merve Ari E, et al. Determination of age-dependent reference ranges for coagulation tests performed using Destiny Plus. Iran J Pediatr. 2016;26(3):e6177.
- Guzzetta NA, Miller BE. Principles of hemostasis in children: Models and maturation. Paediatr Anaesth. 2011;21(1):3–9. doi:10.1111/j.1460-9592.2010.03410.x [CrossRef]
Published Cases of SCH in Younger Patients (Ages 0 to 18 Years)
|Patient||Surgical Indication||Lens Status||Surgery|
|1||Juvenile idiopathic arthritis glaucoma||Aphakic||Ahmed Glaucoma Valve15,21|
|2||Juvenile idiopathic arthritis glaucoma||Aphakic||Ahmed Glaucoma Valve15,21|
|3||Congenital glaucoma||Not reported||Ahmed Glaucoma Valve15,22|
|4||Aphakic glaucoma||Aphakic||Ahmed Glaucoma Valve + mitomycin C15,23|
|5||Aphakic glaucoma||Aphakic||Ahmed Glaucoma Valve15,23|
|6||Unknown or undetermined||Not reported||Trabeculectomy + mitomycin C15,24|
|7||Unknown or undetermined||Not reported||Trabeculectomy + mitomycin C15,24|
|8||Unknown or undetermined glaucoma type||Not reported||Trabeculectomy + mitomycin C15,25|
|9||Unknown or undetermined glaucoma type||Not reported||Trabeculectomy + mitomycin C15,25|
|10||Hypermature cataract (H/O Stage 4A ROP)||Phakic||Cataract extraction|
|11||Pupillary block glaucoma||Phakic||Lensectomy|