British Journal of Ophthalmology, 1985, 69, 143-148

Gas gangrene infection of the eyes and orbitsGERARD W CROCK,' WILSON J HERIOT,' PATTABIRAMAN JANAKIRAMAN,'AND JOHN M WEINER2

From the 'Department of Ophthalmology, University ofMelbourne, and the2CH Greer Pathology Laboratory,the Royal Victorian Eye and Ear Hospital, East Melbourne, Australia

SUMMARY The literature on Clostridium perfringens infections is reviewed up to 1983. Anadditional case is reported with bilateral clostridial infections of the eye and orbit. One eyefollowed the classical course of relentless panophthalmitis, amaurosis, and orbital cellulitis endingin enucleation. The second eye contained intracameral mud and gas bubbles that were removed byvitrectomy instrumentation. Subsequent removal of the toxic cataract resulted in a final aidedvisual acuity of 6/18, N8. This is the third report of a retained globe, and we believe the only knowncase where the patient was left with useful vision.

Clostridium perfringens is a ubiquitous Gram-positive bacillus found in soil and bowel flora. It is themost common of four clostridia species identified incases of gas gangrene in man. ' All species are obligateanaerobes and are usually saprophytic rather thanpathogenic. Clostridium perfringens is a feared con-taminant of limb injuries and may result in death dueto the effects of its powerful exotoxins, which includelecithinase, phospholipase, neuraminidase, cyto-lysin, collegenase, and DNA-ase.'

Despite the potential frequency of contaminationintraocular infection is rare. When the infection isestablished, however, the outcome has been loss ofthe globe in almost every case. Systemic toxicity hasbeen reported rarely, perhaps because establishedpanophthalmitis has been almost uniformly treatedby surgical removal of the globe or orbital contents.Our recent experience from a case with bilateralocular and orbital involvement confirms the sinisternature of such an infection but, for the first time,provides evidence that curative measures are nowavailable.

Case report

A 38-year-old male construction worker struck astick of gelignite with a pick while digging a trench on28 August 1982. In the explosion that followed hesuffered extensive superficial injuries to the face,

Corrcspondence to Professor G W Crock, Univcrsity of Melbourne,Department of Ophthalmology, Royal Victorian Eyc and EarHospital, 32 Gisbornc Strcet, East Melbourne, Victoria 3(X)2,Australia.

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arms, chest, and abdomen. He was admitted to ageneral hospital, where he was examined underanaesthesia, and his injuries were attended to.Ocular findings. The right cornea and anteriorchamber were intact. There was a scleral lacerationover the superonasal area of the pars plana withvitreous prolapse. Pieces of stone were seen in thevitreous, and there was commotio retinae. Anattempt was made to remove the foreign bodies withSutherland forceps. This was unsuccessful, and thescleral wound was closed.

In the left eye there was a corneal perforationnasally with a tear in the underlying iris. Mud andother debris were present in the anterior chamberparticularly in the inferior angle. The corneal woundwas sutured with 10/0 monofilament nylon. Afterclosure of the corneal wound two ports (nasal andtemporal) were made inside the limbus, but it was notpossible to clear the anterior chamber with Suther-land forceps. The facial wounds were cleared out,and subconjunctival injections of gentamycin andcephalosporin were given. Parenteral therapy wasalso started with these same antibiotics. The patientwas transferred to the Royal Victorian Eye and EarHospital on 29 August 1982 and taken straight to theoperating theatre.

Operative findings 29 August 1982. The right eyeshowed diffuse corneal oedema, and multiplegranular particles of dirt were embedded in thestroma. There was a total hypopyon. A vitreousbiopsy was taken through the pars plana (single port)with the Intra Ocular Cutter (IOC) Micro-Fine,Australia. The aspirate was greyish-brown and fluid

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in consistency. Filtered air was injected into the eyetogether with 8 ,ug of gentamycin. There was grossoedema of both lids with multiple embedded foreignbodies.On the left side the lids were similarly swollen and

impregnated with foreign materials. There were fullthickness wounds in the superotemporal and infero-temporal regions that extended deep into the orbit.These tracks were filled with greyish pus and debris.They were irrigated and rubber drains were inserted.The left cornea was impregnated with small quartzand other particles of earth. There was an abscessaround the perforation site and generalised cornealoedema. A small gas bubble was evident in theanterior chamber that contained mud, quartzparticles, and hypopyon.The anterior chamber was cleared through two

limbal ports with the IOC. The mud was enmeshed ina dense fibrin layer all of which came away en massefrom the anterior surface of the iris after infusionaspiration. Streptomycin (250 mg) was injectedsubconjunctivally.At dressing on 30 August there was a purulent

discharge from the right eye. The cornea was com-pletely hazy. There was marked proptosis, externalophthalmoplegia, and no light perception. The leftcornea was reasonably clear except for the area ofinfiltration around the original laceration, and, apartfrom some residual exudate around the pupil margin,the left anterior chamber was satisfactory. The anti-biotic regimen was modified on receipt of the cultureand sensitivity reports.

Enucleation of the right eye was performed on 30August 1982. The operation was virtually bloodless.The resolution of signs was rapid, and a prosthesiswas fitted three weeks later.The postoperative course was marked by tempera-

ture spikes that subsided within the week and byleucopenia. The vision of the left eye improved fromperception of light to counting fingers at 2 feet (60cm). The cornea cleared except for scarring aroundthe perforation site. There were anterior andposterior subcapsular lens opacities that progressedover the next two months. Repeated ultrasono-graphy failed to show any evidence of an intraocularforeign body. A planned extracapsular cataractextraction was done on 22 November 1982. Con-valescence on this occasion was uneventful.The best recorded visual acuity on 10 February

1983 was 6/18 with + 13-0/-2-25 axis 1100 and N8 witha +3-0 addition. The fundus appeared normal. Thelimitation in distance acuity was due to the cornealscar that intruded on the pupil area nasally and tosome thickening of the posterior lens capsule (Fig. 1).Pathological findings. Gram-positive bacilli andpolymorphs were identified in smears of material

:.: : ~~~~~~~~~~~~~~~~...

Fig. 1 Slit-lamp photograph ofthe anterior segment oftheleft eyefollowing extracapsular cataract extraction. Bestacuity 6118, N8.

from both eyes, and Clostridium perfringens wascultured from each eye.

Histopathological examination of the enucleatedright eye showed a panophthalmitis (Fig. 2). Therewas a heavy infiltrate of polymorphs in the anteriorchamber, vitreous, subretinal space, choroid, andsclera. The retina was detached and partly necrotic.Very few Gram-positive bacilli were identified withinthe inflammatory exudate.

1 .1

Fig. 2 Photomicrograph ofhistological section oftheenucleated right eye. The retina is totally detached, and thereis an acute inflammatory exudate through all coats ofthe eye.(Haematoxylin and eosin, x3).

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Gas gangrene infection ofthe eyes and orbits

Discussion

SYNOPSIS OF PREVIOUS CASE REPORTSThe modern literature on gas gangrene of the eye wasinaugurated by the French between 1904 and 1906.3-6More than 20 years later Frederick Ridley could citeonly five case reports. In a brief but masterful paperhe described a single additional case and defined theclinical hallmarks of this disease.7 In 1936 Klueverand O'Brien" added another single case and, inreviewing the literature, referred to gangrenousdacryocystitis. They conducted extensive laboratoryand animal experiments on the causative organismfrom their case. As early as 1938 it was noted bySidney Walker that ocular infection by Clostridiumperfringens did not carry the same risk of mortality aswas associated with contaminated limb wounds, northe same frequency of occurrence."The first instance of the use of antibiotics against

clostridial ophthalmitis was contained in McGregor'sreport of the case of a maltster who presented with afive day history of severe pain in the right eye andgrossly swollen lids."' Small incisions had been madein the outer third of both lids close to the orbitalmargins. Brown pus and bubbles were escaping fromthe wounds. The smell was foul. Sinus lavages wererepeated over six weeks, then a radical antrostomywas performed. Staphylococcus aureus and Gram-positive bacilli with filamentous forms, someresembling spores, were isolated. The patient wastreated with antigas-gangrene serum and sulpha-thiazole. Fundus examination showed optic atrophyonly. There was no perception of light in the eye.The use of penicillin was first reported by Capus in

1946" in an injury sustained after the explosion of awooden military mine. The left eye at eviscerationwas found to contain an intraocular wooden foreignbody and coffee coloured exudate, with gas of acharacteristic odour. - Clostridium perfringens wasisolated and cultured from this material. The righteye, though injured superficially, was not similarlyinfected. The author noted that clostridial infectionhad occurred despite the early use of penicillin andsulphadiazine.By 1951, when Kennedy and Vogel'2 added

another civilian case of panophthalmitis due toClostridium perfringens, the literature count hadreached 28. In their patient the inexorable progressof the panophthalmitis was interrupted by intensivesystemic penicillin therapy, though the eventual out-come for the eye was evisceration 60 hours afterinjury.

In 1955 Robert Leavelle' reviewed the literatureand added three new cases of gas gangrene panoph-thalmitis. He briefly described a fourth case (notpanophthalmitis)-a massive penetrating wound of

the globe with confirmed Clostridium perfringenscontamination. He detailed 24 authors who betweenthem -had described 53 cases since 1904. Four char-acteristics were common to every instance of gasgangrene panophthalmitis: infection followed a per-forating wound of the globe; despite any and allmeasures undertaken the infection progressed anddestroyed all visual function; the infected globe waseither eviscerated or enucleated, or the entire orbitexenterated; postoperative recovery was essentiallyuneventful and complete. In all cases the course wasfulminating regardless of the magnitude of theoriginal injury. The three cases of Lutz were theexception in not following such a course.'3The diagnosis was suspected clinically in several

cases but was not established by laboratory means inany case until more than 48 hours after injury. Theend result was the same in all cases-complete dis-organisation of the visual function and the finalnecessity for removal of the destroyed tissues bysurgical means. Exenteration was necessary in twocases.

Clostridium perfringens conjunctivitis was firstdescribed as a clinical entity in 1963 by Henkind andFedukowicz.'4 They reviewed the chronic unilateralClostridium perfringens dacryocystitis followed bypanopthalmitis as described by Beneditti,'5 the threecases of gas infection of the cornea after gunshotwounds to the eye described Pringle,' and the reportof Clostridium perfringens contamination of thelashes without other evidence of infection.Henkind and Fedukowicz reported on two

patients,'4 both severely ill, who were faecally in-continent. Though the conjunctivitis was of themoderate exudative type, multiple small haem-orrhages were present; the entire process was con-fined to the lower fornices and adjacent bulbarconjunctiva. A culture of Clostridium perfringensobtained from one patient was used to prepare asuspension for experimental purposes. Conjunctivitisoccurred in one of three guinea-pigs into which thesuspension had been injected. In 1970 Levitt andStam'7 described the case of a young child injured bya splinter of wood. Therapy resulted in a retainedglobe with traumatic cataract and perception of light.

Bristow et al. '" wrote from South Africa and con-tributed case 62 in 1971. This was the first recordedcase in which hyperbaric oxygen was used as anadjuvant to therapy. They suggested that suchtherapy was indicated only when there is clinical. evi-dence of extraocular extension of the gas gangrene.The disease was again cut short by evisceration. Inthe same issue of the journal case 63 was reportedfrom England,'9 another fulminant panophthalmitiswhere a ring corneal abscess developed. These twopapers evoked an editorial comment2" which ended

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with the ominous statement that 'so far, no eye withproved gas gangrene panophthalmitis has ever beensaved by antibiotic treatment alone.'The contrast in systemic complications of general

versus ocular clostridial infections was highlighted bya series of papers in 1973.21-24 Involvement of the eyeand orbit by gas gangrene was not discussed and hasnot been recorded in Australia previously.

In 1974 Frantz et al.2s reported the only known caseof Clostridiumperfringens endophthalmitis producedby endogenous spread. The patient presented withsimultaneous abdominal pain and loss of vision. Atoperation a perforated gangrenous gall bladder wasfound. The patient died and at necropsy botheyes were enucleated. The left eye was the seat ofclostridial endophthalmitis. Detailed histologicalfindings are given in the paper. After the single caseof Kessler et al. in 1976 from Switzerland26 thepresent report becomes the 67th to be presented.

COMMENTSThe literature of ophthalmic gas gangrene infectionscontains many single case reports that are depress-ingly repetitive in the final outcome, despite a varietyof therapeutic initiatives. The classical course of thisinfection was succinctly summarised by Duke-Elder27(Table 1). He stated, 'In every case, usually within 24hours after injury, a characteristic fulminating pan-ophthalmitis develops with six distinctive clinicalfeatures, the recognition of which is importantbecause of the necessity for urgent and radicaltreatment.'One would be reluctant to add a further case report

were it not for several noteworthy features, the fore-

K

Fig. 3 Histologicalsectionfromthe enucleated right eye. The lenscapsule (asterisk) is enclosed onboth sides bypolymorphs.(Haematoxylin and eosin, x243).

Table 1 Signs and symptoms ofgas gangrenepanophthalmitis

I Rapid onset with unusually scvcrc pain2 Brawny swelling of cyclids3 Early risc in ocular tcnsion4 Blood of a thin coffcc colourcd dischargc5 Gas bubbles in antcrior chamber6 Rapid developmcnt of total amaurosis

most of which is a final visual acuity of 6/18, N8 in theleft eye. Although survival of the globe with opticatrophy"' and with dense cataract and perception oflight'7 has been reported, this would seem to be thefirst case of bilateral infection in which the clinicalcourse of the two eyes is vividly contrasted. Theclassical outcome on the right side, with amaurosisand hypopyon within 24 hours of sustaining an intra-vitreal foreign body, reinforces the justly feareddevastation due to an established Clostridium per-fringens infection. The left side, with a confirmedintracameral infection and gas bubble, was treated byvitrectomy instrumentation and antibiotics. Theposterior pole was observed to be normal after theremoval of the toxic cataract. The traumatic cornealleucoma and wrinkling of the posterior lens capsulewere of sufficient degree to account for the reductionin the final visual acuity to 6/18, N8.The involvement of both orbits showed differing

clinical patterns-the right, secondary to theclostridial panophthalmitis; the left, by directpenetration of soil. The right orbit was not involvedin the primary trauma, the site of penetration beingseveral millimetres posterior to the limbus. Within 24

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Gas gangrene infection ofthe eyes and orbits

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hours there were signs of orbital cellulitis witha marked proptosis accompanying the intraocularsuppuration. The orbital cellulitis was almostcertainly part of the panophthalmitis and not theresult of a separate inoculation. Histopathologicalexamination of the enucleated eye confirmed a pan-ophthalmitis with only occasional identifiable micro-organisms. This is consistent with previous reports,' l8where scanty organisms were found in the affectedglobe despite severe disruption of the contents.These findings highlight the powerful effect of theexotoxins produced by Clostridium perfringens,which not only cause rapid destruction of the lens, asseen in the present case (Fig. 3), retina, and choroid(Fig. 4), but also affect the extraocular tissues.The degree of proptosis of the right globe was

marked. In contrast there was minimal swelling of theleft orbit, despite deep tracts into it, contaminated bysoil containing Clostridium perfringens. The dif-ference in the degree of tissue swelling was probablyattributable to the effective decompression of the leftorbital septum by the explosive penetrations.With regard to management the significant factor

that differs from all earlier reports is the use ofvitrectomy instrumentation. Because of early opaci-fication in the media of the right eye its applicationwas limited to a vitreous biopsy on that side.However, in the left eye the removal of the fibrin-enmeshed mud from the iris and inferior angle wasdramatic both in execution and effect. Culture of thismaterial confirmed the presence of Clostridiumperfringens, and the gas bubble attested to its activity.While the useful visual outcome may be attributed tothe removal of the mud and inoculum of organisms

Fig. 4 Photomicrograph ofthechoroidfrom the enucleated righteye. There is a heavy infiltrate ofpolymorphs in the choroid. Thereare moderate numbers ofpolymorphs in thesubretinal space(long arrow). (Haematoxylin andeosin, x61) Inset: Gram-positivebacilli (short arrow) are identifiedwithin the inflammatory exudate.(Gram stain, oil immersion, x608).

..

from the anterior chamber, one must be cautious inaccording the success entirely to surgical intervention.

Clostridium perfringens requires specific con-ditions for fulminant growth and the production ofexotoxins. Von Sallman,28 using an experimentalmodel to test antibiotic sensitivities, could produceclostridial panophthalmitis only by inoculation oforganisms deep into the nucleus of the lens. After sixhours penicillin could not arrest the bacterial growth.By contrast Staphylococcus aureus and Streptococcuspneumoniae would reliably induce panophthalmitisafter inoculation into the anterior chamber after onlya few superficial scratches were made on the anteriorsurface of the lens. Von Sallman's work highlightedthe importance of the low redox potential necessaryfor the growth of Clostridium perfringens. In the eyethis is found in the avascular tissue of the lens andvitreous. Owing to the vascularity of the iris theanterior chamber has a higher oxygen level than thevitreous or lens and is less favourable to the growth ofanaerobes. With regard to the case presented herethe successful culture of the organisms some 24 hoursafter trauma, and the production of the gas bubble,confirms that the anterior chamber will support-thegrowth of Clostridium perfringens in the presence ofdebris.The successful outcome on the left side invites

speculation that early vitrectomy with removal of allforeign material may have altered the outcome forthe right eye. While simple removal (by magnet) of aforeign body, even within six hours of trauma, hasnot prevented panophthalmitis,29 the early removalof the avascular vitreous would theoretically reducethe size of the inoculum, remove the majority of the

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avascular tissue, and irrigate the vitreous cavity withoxygenated fluid.The major obstacle to implementation of such

management is the fact that microbiological con-

firmation may not be available for 24 hours or more.

Simple foreign body removal is all that is warrantedin many cases of penetrating injuries, and surgeonsare rightly loath to perform acute vitrectomy unlesscertain of its benefit. However, the catastrophic out-come of established clostridial panophthalmitisbrooks no delay for traditional microbiologicalculture methods. Therefore, cases of military andcivilian injuries should be regarded as being at just as

high a risk of clostridial infection in the eye as in thelimbs or abdomen. They should be assessed for thepptential benefit of debridement of avascular andnecrotic tissue, which, in the eye, would involve totalvitrectomy and also lensectomy if the lens were

involved.Ref6rences

I Leavelle RB. Gas gangrene panophthalmitis. Arch Ophthalmol1955; 53: 634-42.

2 McDonel JL. Clostridium perfringens toxins (Type A, B, C, Dand E). Pharmacol Ther (B) 1980; 10: 617-55.

3 Chaillous J. Infection traumatiquc du globe oculaire par un

microbe anaerobic (Bacillus perfringens). Rec Ophtalmol 1904;26: 678-80.

4 Chaillous J. Deux cas d'infection traumatiquc due globe oculairepar un microbe anaerobie (Bacillus perfringens). Ann Oculist(Paris) 1905; 134: 115.

5 Darier A. Panophtalmie et Bacillus pcrfringens. Clinique Oph-talmologique 1905; 11: 266.

6 Darier A. Panophtalmie gazeuse et bacillus perfringens. CliniqueOphtalmologique 1906; 12: 227-9.

7 Ridley F. Gas gangrene panophthalmitis. Trans Ophthalmol SocUK 1929; 49: 221-5.

8 Kluever HC, O'Brien CS. Panophthalmitis due to Clostridiumwelchii. Arch Ophthalmol 1936; 15: 1088-93.

9 Walker S. Prognosis of Bacillus welchii panophthalmitis. ArchOphthalmol 1938; 19:406-8.

10 McGregor IS. Orbital ceilulitis from gas producing organisms.Br MedJ 1942; i: 292-3.

11 Capus B. Clostridium weichii panophthalmitis. Report of a case.Arch Ophthalmol 1946; 36: 226-8.

12 Kennedy RJ, Vogel AW. Intraocular infection with the gas-forming bacillus Clostridium welchii. Arch Ophthalmol 1951; 45:528-30.

13 Lutz A. Uber einige Falle von ektogener Panophthalmie (infek-tionen mit Pneumococcus subtilis und anaerobionten). KlinMonatsbl Augenheilkd 1910; 48: 31.

14 Henkind P, Fedukowicz H. Clostridium welchii conjunctivitis.Arch Ophthalmol 1963; 70: 791-5.

15 Benedetti A. Panoftalmite a bacillo 'perfringens.' Clin Oculist(Palermo) 1970; 8: 3013.

16 Pringle JA. Three cases of gas infection of the cornea followinggunshot wounds to the eye. BrJ Ophthalmol 1919; 3: 110.

17 Levitt JM, Stam J. Clostridial perfringens panophthalmitis. ArchOphthalmol 1970; 84: 227-8.

18 Bristow JH, Kassar B, Sevel D. Gas gangrene panophthalmitistreated with hyperbaric oxygen. Br J Ophthalmol 1971; 55: 139-42.

19 Bhargava SK, Chopdar A. Gas gangrene panophthalmitis. Br JOphthalmol 1971; 55: 136-8.

20 Anonymous. Gas gangrene of the eye. (Editorial). Br Med J1971; ii: 419-20.

21 Unsworth IP. Gas gangrene in New South Wales. Med J Aust1973; i: 1077-80.

22 Shaw J, Vellar ID, Vellar D. Clostridial (gas gangrene) infectionin a general hospital. Med J Aust 1973; i: 1080-7.

23 McKinnon D, McDonald P. Gas gangrene-a ten-year surveyfrom the Royal Adelaide Hospital. Med J Aust 1973; i:1 0)87-90).

24 Deveridge RJ, Unsworth IP. Gas gangrene. Med J Aust 1973; i:1106-9.

25 Frantz JF, Lemp MA, Font RL, Stone R, Eisner E. Acuteendogenous panophthalmitis caused by Clostridium perfringens.Am J Ophthalmol 1974; 78: 295-303.

26 Kessler S, Schmid E, Pagon S. Panophthalmie durch Gas-branderreger. Klin Monatsbl Augenheilkd 1976; 168: 134-7.

27 Duke-Elder S. System of ophthalmology. London: Kimpton,1972; 14: 405-10.

28 von Sallman L. Penicillin and sulfadiazine in the treatment ofexperimental intraocular infections with Staphylococcus aureusand Clostridium welchii. Arch Ophthalmol 1944; 31: 54-63.

29 Walsh T. Clostridial ocular infections. Case report of gasgangrene panophthalmitis. BrJ Ophthalmol 1965; 49: 472-7.

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