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Br J Ophthalmol: first published as 10.1136/bjo.71.12.933 on 1 December 1987. Downloaded from

British Journal of , 1987, 71, 933-937

Spontaneous hyphaema and corneal haemorrhage as complications of microbial

L DAVID ORMEROD' AND KATHLEEN M EGAN2 From the Departments of 'Ophthalmology and 2Epidemiology, Massachusetts and Ear Infirmary, Harvard Medical School, and the 'Eye Research Institute of Foundation, Boston, Massachusetts, USA

SUMMARY Hyphaema developed spontaneously in 16 of 458 patients with microbial keratitis treated at two centres on the East and West Coasts of the United States. Chronic corneal conditions were often present, and three cases had . Inflamed vessels were assumed to be the source of the haemorrhage. The hyphaemas tended to persist longer than is usual, particularly when coincident with a . Recurrent hyphaemas are reported in two patients from outside this series. Spontaneous corneal haemorrhage was seen in three cases. Subepithelial settled rapidly, but a combined midstromal and pre-Descemet's haematoma cleared more slowly. Anterior segment bleeding was significantly associated with advanced age, female sex, infection with Gram-positive organisms, and hypopyon. copyright.

Anterior segment haemorrhage is uncommon in the Subjects and methods absence of trauma. Bleeding diatheses'" or the rupture of pathological blood vessels are sometimes Bacterial keratitis was defined as an inflammatory implicated. Bleeding may be caused by iris neo- infiltration and ulceration of the corneal stroma, vascularisation, as in diabetic rubeosis,1 or by associated with an epithelial defect, from which one abnormal tumour vessels in melanoma,6 retino- or more bacterial or fungal species were cultured.

blastoma,7 or juvenile xanthogranuloma.7 The records of the patients were studied retro- http://bjo.bmj.com/ Vascularised surgical wounds" and iris neovascular spectively at the University of Southern California tufts, occurring in proximity to the pupillary frill,""' (USC), Los Angeles, and at the Massachusetts Eye have recently been described as causes of spon- and Ear Infirmary, Boston. Standard microbiological taneous hyphaema. Occlusive vasculitic processes'2 techniques' were used at both centres. in, for example, herpetic or Stevens-Johnson The inpatient and outpatient charts of458 consecu- syndrome, may also disrupt iris vessels. The spon- tive cases of microbial keratitis were examined by taneous hyphaemas of Fuchs's uveitis syndrome' probably arise from the iris rubeosis characteristic of Table 1 Prevalence data comparing microbial keratitis on September 30, 2021 by guest. Protected this condition. Bleeding originating from presumably groups with and without haemorrhagic complications normal, if secondarily inflamed, iris vessels has not been reported. Age atpresentationt* Intracorneal haemorrhage'4 has generally been -54years >54 years described after surgery or incidental trauma; other associated conditions have included severe Group Male Female Male Femnale Total and chemical burns. 14 15 No. (N/.) No. (%) No. (%) No. (%) We report the clinical findings and course of 16 Patients with patients with spontaneous hyphaema and three with haemorrhagic corneal haemorrhage occurring in a large series of complications 2(1.3) 1(1.3) 4(3-5) 11(9.6) 18 patients with suppurative inflammation of the Patients without . Two illustrative case reports are included. haemorrhagc 152 (98-7) 74 (98 7) 111(96 5) 103 (90-4) 440 Total 154 75 115 114 458 Correspondence to Dr L David Ormerod, Eye Research Institute, 20 Staniford Street Library, Boston, MA 02114, USA. *Data stratified round the median age of 54 years. 933 Br J Ophthalmol: first published as 10.1136/bjo.71.12.933 on 1 December 1987. Downloaded from

934 L David Ormerod and Kathleen M Egan

Table 2 Clinical characteristics ofmicrobial keratitis patients with spontanieous hyphaema

Microbial Ulcer Preduipositfig Other ocular Case Age Sex aetiologv, size* (clses conditions 1 28 M Staph. aureus M Staple 2 78 F Staph. aurcus M , extended-wear CL 3 87 F Staph. aureus M Trauma, pseudophakia 4 78 F Stapl. aureus M Bullous keratopathy Rubeotic glaucoma 5 68 F Coagulase-negative staphylococcus M Bullous keratopathy Granulomatous uveitis 6 69 M Coagulase-negative staphylococcus M Zostcr keratitis 71 76 F Str. pnleunoniae M Bullous kcratopathy Ruheotic glaucoma 8 79 F Str. pnteumnooiae M 2 months post-PK Postoperative glaucoma 9 81 M Str. pteumnotiae M It) 63 M 0-streptococcus + 0-streptococcus M Assault (2 types) 11 60) F P-strcptococcus L Table injury 12 73 F Pseudoinotas aeruginosa L Aphakia, daily-wear CL 13 58 M Pseudoinonas aerugiltosa S Bullous keratopathy Latc-stage glaucoma 14 68 F Pseudoinotnas inesophilica M Neurotrophic keratitis 15 62 F NA M Bullous keratopathy Rubeotic glaucoma 16 52 M Culture negative M Tree branch injury

*S=small (<2 mm)); M= moderate (2-6 mm); L= large (>6 mm). tHyphacma and corneal hacrmorrhagc developed concurrently.

CL=Contact lcns. PK= Pcnetrating keratoplasty. NA= Not available. copyright.

means of detailed protocols. The study population complications was 68-5 years (range 28 to 87 years). was distributed as follows: Los Angeles County-USC Twelve (67%) of the haemorrhagic group were Medical Center (LAC-USC) 227 patients, 1972- female. Prevalence data for patients with and with- 1983; the Estelle Doheny Eye Foundation (EDEF), out haemorrhage are contrasted in Table 1. The Los Angeles 55 patients, 1978-1984; and the patients with haemorrhagic complications were Massachusetts Eye and Ear Infirmary (MEEI), significantly older (t=2.96, with df 456;

p<0 005) and http://bjo.bmj.com/ Boston-176 patients, 1977-1981. Information was more likely to be female (x'=5-05, df 1; p<0-05) than collected on several demographic and clinical the group without haemorrhage. Male patients variables including age, sex, duration of the con- developing haemorrhagic complications were on dition, systemic and local predisposing factors, prior average 10 years older, and female patients were 14-5 medications, features of the , micro- years older, than their counterparts without such biological culture results, complications, and treat- complications. ment. Patients with a spontaneous onset of To explore whether women were at greater risk hyphaema or intracorneal haemorrhage, occurring at because they were older we stratified the patients by on September 30, 2021 by guest. Protected presentation or during the treatment period, were age, using the median (54 years) as an arbitrary cut- selected for additional study. Two patients from off point (Table 1). In the younger group there were outside the series are included for discussion. twice as many men as women, and both sexes were equally likely to have haemorrhage into the anterior Results segment. The numbers of males and females over 54 years of age were equal, and the age distribution by Of the 458 cases 16 developed a spontaneous decade was almost identical. The proportion of older hyphaema and three (including one combined with patients with haemorrhage was significantly greater hyphaema) had intracorneal bleeding. Therefore than that of younger patients (X'=8-32, df 1; during the acute stage of the inflammation approxi- p<0-01). Older patients of both sexes were at higher mately 4% of the patients had anterior segment risk than younger patients, but hyphaema or intra- haemorrhage. corneal bleeding developed in women nearly three The median age of the 458 patients was 54 years. times as often as in men in patients over 54 years old. The median age of the group with haemorrhagic The clinical characteristics of the 16 patients with Br J Ophthalmol: first published as 10.1136/bjo.71.12.933 on 1 December 1987. Downloaded from

Spontaneous hyphaema and corneal haemorrhage 935

(Table 2 continued) Hyphaetna Onset of Prior coincident hvphaeton Systemic topical with S/C (daysfromn conditions Hypopy on steroids injectios admission) Outcome + + I Small. Settled in 4 days + + 5 20% hyphaema. Layered. Slow to resolve + 0 Small. developed + () 50% hyphaema. Organised. Enucleation day 27. Warfarin (pulmonary + 3 15% hyphacma. Settled in I week embolism) + + 12 10/% hyphacma. Layered. Cleared in >2weeks + + 4 30(% hyphaema. Cleared in 2 weeks + + + 5 Small. Settled in 5 days Dementia + + 7 75% hyphaema. Layered. Slow to resolve. Late cnucleation Chronic alcoholism 0 25% hyphaema. Slow to resolve

Diabetes + - 12 Microhyphacma. Settled in 3 days + - 12 Small. Cleared rapidly ---- 8 Small. Settled in I week + - 2 20% hyphaema. Intermixed with hypopyon. Slow to resolve + 0 10(% hyphaema. Intermixed with hypopyon. Enucelated + 3 Small. Intermixed with hypopyon. Settled in 6 days copyright.

spontaneous hyphaema are shown in Table 2 and of CASE A the three patients with corneal haemorrhage in Table A 65-year-old South African black male developed a 3. Late hyphaemas developed in five traumatised moderate-size paracentral Streptococcus viridans (patients 1, 3, 10, 11, 16), all following the onset microbial keratitis. Several days later, at admission, of corneal infection. Both hyphaema and corneal he had a 10% hyphaema, without hypopyon, and was haemorrhage developed spontaneously in one treated with subconjunctival injections of cephalo- patient (case 7). thin and gentamicin and with topical chloram- http://bjo.bmj.com/ The microbial keratitis involved Gram-positive phenicol. The corneal infection improved rapidly, organisms in 13 of the 16 culture-positive cases. but on day 4 after admission secondary bleeding Hypopyon was twice as prevalent in patients with into the anterior chamber and a 50% hyphaema spontaneous haemorrhage into the anterior segment developed. Resolution occurred over a period of (13 of 18) as in patients in the overall series (149 of three weeks. There were no permanent sequelae. 440) without bleeding (X'=1I 1, df 1; p<0O001). The two subepithelial corneal haemorrhages CASE B on September 30, 2021 by guest. Protected cleared rapidly, but the midstromal and pre- A 72-year-old male was treated at Massachusetts Eye Descemet's haematoma (case 7), associated with and Ear Infirmary for a moderate-size suppurative hyphaema, cleared much more slowly. Blood stain- corneal ulcer caused by a Klebsiella oxytoca infection ing or other sequelae were not noted, and corneal of a trophic ulcer. When admitted, he bleeding did not pose a significant problem in this had a 50% hyphaema, without hypopyon, and an series. of 42 mmHg. He was treated The bleeding site was not seen in any patient; the with frequent high-dose topical cephazolin and conditions of microbial keratitis inhibit fine observa- gentamicin eye drops. Despite a rapid improvement tion of the iris and anterior chamber. Iris neovascular of the keratitis the hyphaema increased to fill most of tufts were not reported. Secondary bleeding, the anterior segment, and early corneal blood stain- glaucoma (apart from the four cases with premorbid ing was noted on day 5. Three anterior chamber glaucoma). and corneal blood staining were not irrigations were performed over the next two weeks, observed. However, we have recently seen two each followed by severe bleeding. The intraocular patients with major complications of hyphaema not pressure remained at 40 mmHg for nearly one month observed in this series; their case reports follow. despite maximal glaucoma therapy. Ultimately the Br J Ophthalmol: first published as 10.1136/bjo.71.12.933 on 1 December 1987. Downloaded from

936 L David Ormerod and Kathleen M Egan

Table 3 Clinical characteristics ofmicrobial keratitis patients with intracorneal haemorrhage

Microbial Ulcer Predisposing Other ocular Systemic Case Age Sex Aetiology size* causes conditions conditions 7t 76 F Str. pneumoniae M Bullous kcratopathy Rubcotic glaucoma 17 78 F Coagulase-negative M Zoster keratouveitis - Chronic lymphatic Icukaemia staphylococcus 18 49 F a-streptococcus + L Dryeye - Chronic alcoholism coagulase-negative staphylococcus + spp. *S=small (<2 mm); M= moderate (2-6 mm); L=large (>6 mm). tHyphaema and corneal haemorrhagc developed concurrently. SC=subconjunctival. ocular cleared and the hyphaema Spontaneous hyphaema has been reported as a resolved slowly. The patient died before long-term complication of severe vasculitic uveitis,'21' "' but not sequelae could be assessed. following microbial keratitis. An important observa- tion is that the course of hyphaema complicating Discussion microbial keratitis often differs from that of trau- matic hyphaema.'9 Early bleeding mixed with the Haemorrhagic complications of microbial keratitis hypopyon to variable degrees; later haemorrhage are uncommon. They occurred in 4% of 458 patients layered over the hypopyon. In three eyes the bleed- in this series and also in 4% (6 of 140) of patients with ing filled >25% of the anterior chamber. Further copyright. microbial keratitis admitted to St Johns Hospital, bleeding did not occur in this series, but was seen in Soweto, South Africa, in March 1981-February two other patients (cases A and B). In case B corneal 1982 (unpublished data). The aetiology of the bleed- blood staining and a prolonged pressure rise were ing appeared to be multifactorial. Advancing age was major problems. In several cases the resorption of a significant prognostic factor in both men and the blood and hypopyon was unduly prolonged. women. The risk of anterior segment bleeding was The available follow-up was insufficient to provide also two to three times greater for women than for an adequate analysis of the long-term sequelae of men in the older age groups. These findings, how- haemorrhage in these severely inflamed eyes, as ever, are based on a relatively small number of distinct from those caused by the inflammatory http://bjo.bmj.com/ patients. The preponderance of Gram-positive process itself. Retention of blood in the anterior bacteria and the remarkably high prevalence of chamber can lead to fibrovascular organisation, hypopyon (72%) suggest that the microbial infection posterior and peripheral anterior synechiae forma- involved strains of moderate virulence but high tion, corneal blood staining, glaucoma, and optic phlogogenicity. Bacterial proteases, cytolytic toxins, atrophy."9 The frequently prolonged natural history and streptokinases might play an important part in of hyphaema in these inflamed eyes suggests that causing haemorrhage. intraocular bleeding is a potentially serious complica- on September 30, 2021 by guest. Protected Two-thirds of the patients had local ocular predis- tion of microbial keratitis, as illustrated in case B. posing factors (besides trauma), some of which may When spontaneous hyphaema has occurred, have been associated with chronic anterior segment may tamponade irideal vessels and control inflammation. Prior treatment with topical steroids in bleeding." It may sometimes be possible to photo- six patients may also have contributed to the intra- coagulate the bleeding site with argon laser, as ocular bleeding by increasing local vascular fragility. suggested for iris neovascular tufts. "'Aspirin therapy Trauma associated with subconjunctival injections should be stopped and the haemostatic status appeared unrelated. Three patients presumably bled investigated.' The intraocular pressure must be from pre-existing iris rubeosis (thrombotic closely monitored. After the corneal infection is glaucoma), and hyphaema developed spontaneously controlled, topical steroids may be beneficial in in one patient when long-term warfarin therapy was reducing the inflammation.'9 complicated by the advent of microbial keratitis. Two Duke-Elder and Leigh2' noted that corneal patients were chronic alcoholics and one patient had haemorrhage almost invariably occurs from areas of chronic lymphatic leukaemia, but all three had neovascularisation, particularly following interstitial normal haemostatic profiles. and mustard gas keratitis. There are several isolated Br J Ophthalmol: first published as 10.1136/bjo.71.12.933 on 1 December 1987. Downloaded from

Spontaneous hyphaema and corneal haemorrhage 937

Corneal Onset of hemorrhage corneal Prior coincident haemorrhage topical with SC (daysfrom Corneal Hypopyon steroids injections admission) site Outcome

+ - 4 Midstromal and pre-Descemet's membrane Still present at I month + + 2 Subepithelial Cleared rapidly 22 Subepithelial Cleared over 1 week

reports of corneal haemorrhage complicating micro- 12 Duke-Elder S. Perkins ES. System of ophthalmology. Diseases bial keratitis."-4 Muenzler believes that haemorr- of the uveal tract. St Louis: Mosby, 1966; 9: 133. 13 Liesegang TI. Clinical features and prognosis in Fuchs' uveitis hages may not be uncommon in the vascularised syndrome. Arch Ophthalmol 1982; 100:1622-6. cornea and may go unnoticed because of their usually 14 Muenzler WS. Intracorneal hemorrhage. Am J Ophthalmol small size and limited duration.4 Large, superficial 1973; 76: 440-2. corneal haemorrhages may be drained by removing 15 Vestergaard JDE. Subepithelial hematoma of the cornea. Acta Ophthalmol (Kbh) 1928; 6: 173-80. the overlying epithelium with a moist cotton-tipped 16 Lennette EH, Balows A, Hausler WJ, Truant JP, eds. Manual of applicator.25 Deep corneal haemorrhages may, how- clinical microbiology. 3rd ed. American Society for Micro- ever, require formal surgical drainage67 because of biology, 1980. copyright. their tendency to occlude the drainage angle, their 17 Doggart JH. Spontaneous hyphaema. Acta, XVI Concilium Ophthalmologicum, Brittania, 1950. London: British Medical chronicity,2' and organisation with scarring. Association, 1951; 1: 450. References 18 Kinder RSL, Cowett RM. in infancy and childhood: a brief review and report of an unusual case. J Pediatr Ophthalmol I Massa J-M, de Vloo N. Jamotton L. The ocular manifestations of 1976; 13:139-40. the hemopathies. Bull Soc Beige Ophtalmol 1966; 142: 415-34. 19 Read JE, Crouch ER. Trauma: ruptures and bleeding. In: 2 Johnston SS, Ware CF. Iris involvement in leukemia. Br J Duane TD, ed. Clinical ophthalmology. Hagerstown: Harper Ophthaltnol 1973; 57: 320-4. and Row, 1984; 4: chapter 61: 13-14.

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initial manifestations of uveal malignant melanoma. Incidence of the cornea in Hansen's disease. A light- and electron- on September 30, 2021 by guest. Protected and prognosis. Arch Ophthalmol 1979; 97: 1311-4. microscopic study. Ophthalmologica 1980; 181: 314-9. 7 Howard GM. Spontaneous hyphema in infancy and childhood. 25 Hurwitz BS. Spontaneous intracorneal hemorrhage caused by Arch Ophthalmol 1962; 68: 615-20. aphakic contact wear. Antn Ophthalmol 1981; 13: 57-9. 8 Swan KC. Late hyphema due to wound vascularization. 26 BArdy K. A contribution on deep corneal hematoma. Klin Ophthalmology 1976; 81: 138-44. Monatsbl Augenheilkd 1965; 147: 838-48. 9 Watzke RC. from vascularization of the 27 Renardel de Lavalette JGC, Van Rij G. Intracorneal hemorr- incision. Ophthalmology 1980; 87: 19-23. hage. Doc Ophthalmol 1982; 52: 397-403. 10 Magauran DM. Unilateral spontaneous hyphaema. Br J 28 Sedan J. Spontaneous hematocornca. Ann Oculist (Paris) 1968; Ophthalmol 1973; 57: 945-7. 201:443-6. 11 Welch RB. Spontaneous anterior chamber hemorrhage from the iris: A unique cinematographic documentation. Trans Am Ophthalmnol Soc 1980; 78: 132-47. Acceptedfor publication 20 November 1986.