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Home , Vibrio alginolyticus, Vibrio vulnificus

Cornea 19(1): 26–29, 2000. © 2000 Lippincott Williams & Wilkins, Inc., Philadelphia

Vibrio Ocular Infections on the U.S. Gulf Coast

Rebecca L. Penland, M.(A.S.C.P.), Milton Boniuk, M.D., and Kirk R. Wilhelmus, M.D., M.P.H.

Purpose. To describe the epidemiology of eye infec- consumption of raw in the United States (5,6). tions. Method. We reviewed the records of a patient from our , the most virulent of the noncholera institution with V. vulnificus keratitis and conducted a literature Vibrio organisms, is a cause of septicemia associated search for other cases of ocular infections with Vibrio species. Results. A 39-year-old fisherman was struck in his left eye with the consumption of raw oysters and infec- with an shell fragment, developed suppurative V. vul- tions (7–9). We isolated V. vulnificus from a patient with nificus keratitis, and was successfully treated with combined keratitis and searched the literature for other cases to cefazolin and gentamicin. Including our patient, 17 cases of eye identify the risk factors for eye infections caused by infections with Vibrio spp. have been reported, and 11 (65%) halophilic noncholera Vibrio species. involved exposure to seawater or shellfish. Of the seven cases due to V. vulnificus (six keratitis and one endophthalmitis), six had known exposure to shellfish or seawater along the U.S. CASE REPORT coast of the Gulf of Mexico. Of five cases of V. alginolyticus conjunctivitis, three had been exposed to fish or shellfish. A 39-year old Hispanic man was selecting oysters for Three infections with V. parahaemolyticus (one keratitis and harvest on a boat off the Texas Gulf Coast when a shell two endophthalmitis) were reported; two of these occurred in people exposed to brackish water on or near the Gulf Coast. fragment hit his left eye. Because of progressive pain and Two cases of postsurgical endophthalmitis, one with V. alben- decreasing vision, he was seen 2 days after the injury and sis and one with V. fluvialis, also were reported. Conclusions. found to have visual acuity of 20/100 and a paracentral In addition to septicemia, , and wound infec- suppurative corneal ulcer with small hypopyon. Acridine tions, halophilic noncholera Vibrio species can cause sight- orange- and Gram-stained smears of corneal scrapings threatening ocular infections. Ocular trauma by shellfish from contaminated water is the most common risk factor for Vibrio showed occasional gram-negative rods and coccobacilli conjunctivitis and keratitis. Nearly one half of reported Vibrio and a few neutrophils. The patient was hospitalized and infections of the eye occurred along the U.S. coast of the Gulf treated with topical cefazolin, 5%, and gentamicin, 1.4% of Mexico. eyedrops, half-hourly. Prednisolone acetate, 1% drops, Key Words: Vibrio—Keratitis—Conjunctivitis—Endophthal- was added the following day. mitis—Gulf Coast—Oyster. Moderate growth of an oxidase-positive, curved gram- negative rod with polar flagella was isolated on horse blood, chocolate, and Brucella agar plates within 24 h of Halophilic noncholera Vibrio species are normally incubation. Susceptibility testing showed minimal inhibi- found in temperate and warm marine environments (1), tory concentrations of Յ0.25 ␮g/ml gentamicin, 1 ␮g/ml including the Gulf of Mexico (2,3). Twelve of the >30 tobramycin, Յ8 ␮g/ml cefoperazone, Յ8 ␮g/ml cefo- Vibrio species are implicated as human (4). taxime, Յ4 ␮g/ml , and Յ0.25 ␮g/ml cipro- Two species, V. parahaemolyticus and V. vulnificus, floxacin. The isolate was identified as V. vulnificus by cause the majority of noncholera infections (4). biochemical testing. causes gastroenteritis in By the third day of hospitalization, the corneal infil- many parts of the world (4) and was recently associated trate was diminishing, and the hypopyon had resolved. with large outbreaks of diarrheal disease linked to the On the fifth treatment day, topical cefazolin was switched to , 0.3%, and gentamicin was re- duced to 0.3%. All medications were gradually reduced and discontinued after 5 weeks of treatment. A superfi- Submitted February 9, 1999. Revision received April 30, 1999. Ac- cial corneal opacity limited vision to 20/30. cepted May 3, 1999. From the Sid W. Richardson Ocular Microbiology Laboratory, Cullen Eye Institute, Baylor College of Medicine, Houston, Texas, U.S.A. RESULTS Address correspondence and reprint requests to Dr. K.R. Wilhelmus, 6565 Fannin Street, NC205, Houston, TX 77030, U.S.A. E-mail: We searched MEDLINE (1966–1998) and EMBASE [email protected] (1974–1998) by using the following keywords: vibrio?

26 VIBRIO OCULAR INFECTIONS ON THE U.S. GULF COAST 27 and (eye? or cornea? or conjunctiv? or keratitis or en- Five cases of V. alginolyticus conjunctivitis were re- dophthalmitis) and found 16 reported cases of eye infec- ported, four with known contact with shellfish fragments tions involving Vibrio species (Table 1). Including our or seawater. Although a conjunctival isolate from a per- patient, of seven cases due to V. vulnificus (six keratitis son who had been in contact with seawater was origi- and one endophthalmitis), six had known exposure to nally included in a study of suspected V. parahaemolyti- shellfish or seawater along the U.S. coast of the Gulf of cus isolates reported in 1969, several of these isolates Mexico. Whereas two cases without hypopyon resolved were later identified as V. alginolyticus (13,14). A second rapidly with treatment that included gentamicin (10), two conjunctival isolate was identified in 1973 as Beneckea cases with hypopyon required debridement, and one re- alginolytica (15), a species later renamed V. alginolyticus quired a partial lamellar keratectomy in addition to gen- (16). Three subsequent cases of V. alginolyticus conjunc- tamicin (11). Vibrio vulnificus was recovered from a case tivitis were reported in an alcoholic fish cutter (17), a of polymicrobial endophthalmitis involving injury with a critically ill patient who handled seashell fragments (18), fishhook baited with fresh shrimp (12). and a fisherman who had sustained a fishhook injury (19).

TABLE 1. Reported cases of Vibrio ocular infections

Case Reference Species Type of infection Location Risk factor Antibiotic treatment Outcome 1 Baumann et al. V. vulnificus Keratitis Virginia ND ND ND 1973 2 Harris et al. V. vulnificus Keratitis Florida Injury with oyster Gentamicin and Resolved 1985 shell fragment carbenicillin (topical and subconjunctival) 3 Harris et al. V. vulnificus Keratitis Florida Injury with oyster Fortified gentamicin, Resolved 1985 shell fragment tobramycin, and neomycin-polymyxin B (topical) 4 DiGaetano et al. V. vulnificus Keratitis Louisiana Shucking oysters Gentamicin, polymyxin 20/20 1989 B-bacitracin-neomycin, and cefazolin (topical) 5 DiGaetano et al. V. vulnificus Keratitis Louisiana Injury with crab Gentamicin 20/20 1989 shell (subconjunctival and topical); bacitracin, and tobramycin (topical) 6 Penland et al. V. vulnificus Keratitis Texas Injury with oyster Gentamicin, cefazolin 20/30 1999 shell fragment and ciprofloxacin (topical) 7 Butt et al. 1997 V. vulnificus Endophthalmitis Louisiana Penetrating injury Gentamicin (intraocular Enucleation with fish hook and i.v.); piperacillin/tazobactam and cefazolin (i.v.) 8 Twedt et al. V. alginolyticusa Conjunctivitis United States Recreational ND ND 1969 contact with seawater 9 Baumann et al. V. alginolyticus Conjunctivitis California ND ND ND 1973 10 Schmidt et al. V. alginolyticus Conjunctivitis New Jersey Fish cutter Sulfisoxazole (topical) Resolved 1979 11 Lessner et al. V. alginolyticus Conjunctivitis New York Handled seashell Gentamicin (topical) Resolved 1985 fragments 12 Ratnam et al. V. alginolyticus Conjunctivitis Canada Fisherman, prior Gentamicin (topical) Resolved 1985 penetrating injury 13 Hollis et al. 1976 V. parahaemolyticus Keratitis ND ND ND ND 14 Steinkuller et al. V. parahaemolyticus Endophthalmitis Texas Sharp eye pain Gentamicin (sub-tenon, 20/60 1980 while swimming topical and i.v.); in Galveston methicillin (sub-tenon Bay; shellfish and i.v.); cephalexin parts seen in (oral) water 15 Tacket et al. V. parahaemolyticus Endophthalmitis Georgia Foreign body Gentamicin and colistin Enucleation 1982 injury, from oil (topical) refinery equipment in brackish water 16 Tendolkar and V. albensis Endophthalmitis India Cataract extraction Chloramphenicol No improvement Deodhar, (subconjunctival and in visual acuity 1990 i.m.) 17 Hassan et al. V. fluvialis Endophthalmitis England Cataract extraction ND ND 1992

ND, not determined; i.v., intravenous; i.m., intramuscular. a Case 8 was originally reported as V. parahaemolyticus.

Cornea, Vol. 19, No. 1, 2000 28 R.L. PENLAND ET AL.

oysters recovered from the Gulf of Mexico in warmer months contain detectable levels of V. vulnificus and V. parahaemolyticus (3,28). Although the molecular pathogenesis of V. cholerae, mediated by toxin, is well understood (29), the pathogenic mechanisms of the noncholera Vibrio spp. have not been completely elucidated. Capsules, pili, and siderophores are putative virulence factors that enable noncholera Vibrio to establish infection, while metallo- proteases, cytolysins, and cytotoxins cause extensive tis- sue damage. Capsular polysaccharide (CPS) production is a major virulence determinant for V. vulnificus because it pro- FIG. 1. Location of V. vulnificus (solid circles) and V. para- tects the organism from complement-mediated lysis and haemolyticus (open circles) ocular infections on the U.S. and elicits the release of tumor Gulf Coast. The case in Georgia occurred in a refinery that factor (30). Capsule-producing strains are generally more received oil from the Gulf of Mexico. invasive (31); however, the isolate from the first reported Vibrio parahaemolyticus was first reported from a cor- case of V. vulnificus keratitis was found to produce less nea in a series characterizing halophilic Vibrio spp. iso- CPS than other clinical isolates (32). Although V. para- lated from various infections (20). Vibrio parahaemolyti- haemolyticus also produces a capsule (33,34), its role in cus also was isolated from two cases of endophthalmitis pathogenesis has not been as extensively studied. Pili involving contact with brackish water. The first involved may also be involved in adherence of V. vulnificus and V. injury while swimming in the Gulf of Mexico, where parahaemolyticus to host cells (35–37). shellfish fragments had been seen in the water. The day Siderophores are iron-binding chelators produced by after the injury, the cornea appeared bright green, and the several species of to obtain iron needed for vitreous resembled mint jelly (21). The second case in- growth. The siderophores vulnibactin, produced by V. volved penetrating injury from equipment in an oil re- vulnificus, and vibrioferrin, produced by V. parahaemo- finery that received crude oil shipments from the Gulf of lyticus and V. alginolyticus, differ in their ability to che- Mexico (22). late iron from iron-binding proteins. Vibrio vulnificus, Two cases of postsurgical endophthalmitis with Vibrio but not V. parahaemolyticus, can acquire iron from hu- species were reported. Vibrio albensis, classified as the man lactoferrin (38,39) and may be a reason that V. luminescent biotype of non-01 V. cholerae (23), was vulnificus infects the cornea. Although the exact mecha- recovered from a patient in India who developed a hy- nism of iron acquisition is unknown, outer-membrane popyon with a yellow glow behind the pupil (24). Vibrio proteins that function as receptors for the iron– fluvialis was recovered from a patient in England (25). siderophore complex have been demonstrated in some Vibrio organisms (39). Metalloproteases, in addition to cleaving iron-binding DISCUSSION proteins and facilitating iron uptake (38), are involved in Several noncholera Vibrio species cause gastrointesti- invasion and tissue destruction by Vibrio. Vibrio vulnifi- nal and extraintestinal infections, usually associated with cus is the most invasive due to its ability to degrade consumption of raw oysters or undercooked or several substrates, including collagen (40,41), chondroi- with exposure to seawater (7). Vibrio infections of the tin sulfate (9), mucin (9), and elastin (41,42). Vibrio eye are uncommon but include conjunctivitis, keratitis, parahaemolyticus also can attack elastin and chondroitin and endophthalmitis. Most are caused by V. vulnificus, V. sulfate (9,43). , a cause of conjunc- alginolyticus, or V. parahaemolyticus and frequently tivitis, is less virulent but also produces a metalloprote- involve accidental contact with shellfish or seawater ase that digests collagen (44). Noncholera Vibrio spp. (Fig. 1). also produce cytolysins and cytotoxins (4) that likely add Halophilic Vibrio species are part of the normal ma- to their ocular pathogenicity. rine flora and are concentrated by oysters and other filter Several noncholera Vibrio spp. are associated with feeders (26). Vibrio vulnificus and V. parahaemolyticus particular infections, such as V. vulnificus septicemia, V. can exist in a dormant “ state” parahaemolyticus gastroenteritis, and V. alginolyticus and are present year round in many parts of the world ear infections (4). Different species also appear to have a (27). High concentrations have been reported along the predilection for particular parts of the eye: V. vulnificus Eastern seaboard and Gulf Coast of the United States, keratitis, V. parahaemolyticus endophthalmitis, and V. particularly during the summer months (4). Nearly all alginolyticus conjunctivitis. The type of exposure and

Cornea, Vol. 19, No. 1, 2000 VIBRIO OCULAR INFECTIONS ON THE U.S. GULF COAST 29 virulence factors expressed by each species probably de- 19. Ratnam S, Watson M. Vibrio alginolyticus conjunctivitis. Arch termine tissue tropism. Knowing the clinical epidemiol- Ophthalmol 1985;103:1283–4. 20. Hollis DG, Weaver RE, Baker CN, Thornsberry C. Halophilic ogy of Vibrio infection can help direct the ophthalmolo- Vibrio species isolated from blood cultures. J Clin Microbiol 1976; gist and the laboratory investigation when oxidase- 3:425–31. positive, curved, gram-negative rods are isolated from 21. Steinkuller PG, Kelly MT, Sands SJ, Barber JC. Vibrio parahae- molyticus endophthalmitis. J Pediatr Ophthalmol Strabismus eye infections, particularly those involving injury with 1980;17:150–3. shellfish or exposure to seawater. 22. Tacket CO, Barrett TJ, Sanders GE, Blake PA. Panophthalmitis caused by Vibrio parahaemolyticus. J Clin Microbiol 1982;16:195–6. 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Cornea, Vol. 19, No. 1, 2000