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Journal of Clinical Microbiology, August 2003, p. 3998-4000, Vol. 41, No. 8
0095-1137/03/$08.00+0     DOI: 10.1128/JCM.41.8.3998-4000.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.

CASE REPORT

Rhizobium (Agrobacterium) radiobacter Identified as a Cause of Chronic Endophthalmitis Subsequent to Cataract Extraction

Hassan Namdari,^1* Sirus Hamzavi,² and Randall R. Peairs²

Clinical Laboratories Inc., Throop,¹ Northeastern Eye Institute, Scranton, Pennsylvania²

Received 31 October 2002/ Returned for modification 24 February 2003/ Accepted 25 April 2003

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Herein, we report a case of chronic endophthalmitis caused by a ceftazidime-resistant Rhizobium radiobacter strain in a 62-year-old male. The patient underwent an uneventful cataract extraction of the right eye a week prior to the appearance of symptoms (pain, redness, and blurring vision) which developed following a golf outing. Upon admission the patient received an emergency vitrectomy. The patient remained symptomatic, and R. radiobacter was isolated repeatedly from vitreous fluid cultures over a 5-month period. Ultimately, the infection responded to intravitreal gentamicin, oral ciprofloxacin, and removal of the lens implant.

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A 62-year-old male who underwent an uncomplicated cataract extraction of the right eye in May 2001 presented with decreased visual acuity, pain, and redness of the eye 1 week later. When the patient was admitted, the visual acuity and intraocular pressure were 20/60 and 29 mm Hg, respectively, for his right eye and 20/20 and 21 mm Hg, respectively, for his left eye. Examination of the eye showed moderate conjunctival injection, anterior chamber inflammation without obvious hypopyon, and a retina that appeared flat with no sign of intraretinal inflammation. A vitreous biopsy was performed, the specimen was processed microbiologically, and the patient was treated empirically with an intravitreal injection of amikacin (0.4 mg) and vancomycin (1 mg). Culture of the vitreous biopsy specimen produced a Rhizobium radiobacter strain resistant to ceftazidime and vancomycin but susceptible to ciprofloxacin. Subsequently, the patient remained asymptomatic until he was readmitted 2 months later with an acute exacerbation of symptoms. A pars plana vitrectomy was performed with the intravitreal administration of gentamicin (0.4 mg) and a course of oral ciprofloxacin (500 mg twice daily for 10 days). Again, the vitreous fluid grew the same R. radiobacter organism. Exactly 2 months later, the patient showed worsened vision and a prominent hypopyon; he underwent another vitrectomy with removal of the intraocular lens and the capsule and was given intravitreal gentamicin (0.4 mg). His therapy was continued with the same dosage of oral ciprofloxacin for 2 weeks, and 1 drop each of 1% atropine sulfate (four times a day for 3 days), 0.2% brimonidine tartrate (twice a day for 3 days), and 1% prednisolone acetate (every 3 h for 4 days). Ultimately, the patient's chronic R. radiobacter endophthalmitis was cured by the simultaneous removal of the intraocular implant and treatment with intravitreal gentamicin and oral ciprofloxacin.

Microbiological investigation. Agrobacterium species have recently been reclassified in the genus Rhizobium based on comparative 16S rRNA gene analyses (7, 8). Plant-pathogenic, soil inhabitant R. radiobacter is not characterized as a true human pathogen. It is an opportunistic pathogen of minor clinical significance and has been substantiated as a rare cause of bacteremia, endocarditis, and peritonitis mostly in catheterized immunocompromised patients and as a cause of urinary tract infection (2, 3, 4). However, this is the second documented case of endophthalmitis caused by this organism in a patient after cataract extraction surgery. The patient became symptomatic after a day of golfing and was admitted for emergency vitrectomy within 12 h. The vitreous biopsy specimen obtained was processed by Gram staining and inoculated onto 5% sheep blood agar, MacConkey agar, chocolate agar, brucella agar, thioglycolate broth, and Sabouraud's dextrose agar (Becton Dickinson Microbiology Systems, Sparks, Md.). The Gram stain showed gram-negative rods, with some appearing to have been internalized by neutrophils (Fig. 1). Cultures grew a nonfermenting, gram-negative bacillus, producing dry, tenacious colonies on blood agar, chocolate agar, and on MacConkey agar. The organism was identified as R. radiobacter by both conventional biochemical reactions and the API 20NE (biotype 1667754) identification system (bioMerieux, Hazelwood, Mo.), and the identification was confirmed by two other independent laboratories, one using conventional biochemical methodology and the other using the Biology a bacterial identification system (Biolog, Inc., Hayward Calif.). The isolate reduced nitrate, fermented glucose, and hydrolyzed both esculin and urea (Table 1). The antibacterial susceptibility of the isolate determined by using the Etest (AB Biodisk, Solna, Sweden) and the gram-negative combination type 25 dried MicroScan panel (Dade International, Inc., West Sacramento, Calif.) showed it to be resistant to tobramycin (MIC > 8 µg/ml), ceftazidime (MIC = 128 µg/ml), and vancomycin (MIC = 96 µg/ml); moderately resistant to gentamicin (MIC = 8 µg/ml) and amikacin (MIC = 32 µg/ml); and susceptible to ciprofloxacin (MIC = 0.016 µg/ml) (Table 1). While both the Etest and MicroScan were appropriate systems for determining the MICs for the isolate, MicroScan misidentified the isolate as Chryseobacterium indologenes despite the fact that it was not an indole producer. On the patient's readmission 2 months later, both the Gram stain and the culture of vitreous fluid yielded the same organism with an identical antibacterial susceptibility pattern, confirming R. radiobacter chronic endophthalmitis in this patient.

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FIG. 1. Gram stain of vitreous fluid showing bacillary R. radiobacter, with some rods appearing to have been internalized by neutrophils.

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TABLE 1. Biochemical characteristics and antibacterial susceptibility of the R. radiobacter strain isolated from vitreous fluid

As R. radiobacter is an environmental soil organism, it was suspected that the patient's exposure to the outdoor environment and moist soil, not the cataract operation per se, remained the source of the organism involved in the eye infection. This assumption is in accordance with the report of Miller et al. (6) of a patient who worked in the garden on the evening after his cataract surgery and subsequently developed R. radiobacter-like endophthalmitis. Although this organism is an uncommon cause of endophthalmitis, patients who have had cataract extraction surgery should be advised to avoid outdoor activities which involve direct contact with soil until the surgical wounds are completely healed.

Our patient was empirically treated with an intravitreal injection of vancomycin and amikacin as a routine ophthalmologic practice while microbiology culture results were pending. Because the R. radiobacter isolate was resistant to vancomycin and moderately resistant to amikacin, the initial antibacterial therapy was unable to eradicate the infection, which reoccurred 2 months later and prompted a second vitrectomy. In the process, in addition to an intravitreal injection of gentamicin, the patient's therapy was augmented with oral ciprofloxacin. Chronic endophthalmitis in this patient was due to R. radiobacter, which appeared inherently resistant and moderately resistant to ceftazidime and amikacin, respectively, agents approved by the Food and Drug Administration (FDA) for direct intravitreal administration. These are also the drugs of choice for treatment of endophthalmitis caused by more common environmental gram-negative organisms such as pseudomonads. Although the isolate was highly susceptible to ciprofloxacin, an agent not approved by the FDA for intravitreal injection, its oral administration was unsuccessful in eradicating the infection until the implanted lens was removed.

In this case the lens and capsule of the intraocular implant were associated with chronic infection, and its presence in situ prevented bacterial eradication by multiple courses of antibacterial therapy agents until the complete removal of the intraocular implant was accomplished. According to an earlier report (1), R. radiobacter adheres to silicone present in the implant, thereby necessitating its removal for enhancing the effect of the antibacterial treatment. Indwelling foreign bodies are often associated with the persistence of R. radiobacter infection (4), and as indicated in this case, the lens implant served as the source of chronic endophthalmitis.

The in vitro antibacterial susceptibility of this isolate was in agreement with the findings of Alnor et al. (1), who reported that R. radiobacter strains are susceptible to ciprofloxacin and suggested it as the drug of choice for systemic infections. R. radiobacter has also been reported as being consistently resistant to tobramycin (4), while our strain was resistant to ampicillin, trimethoprim-sulfamethoxazole, and vancomycin in addition to tobramycin. Its resistance to common antibacterial agents approved by the FDA for direct intravitreal administration may underscore the value of oral ciprofloxacin therapy for R. radiobacter endophthalmitis in conjunction with the removal of the implant, if present. R. radiobacter species possesses a wide variety of mechanisms for antibacterial resistance (3, 5) because of the coexistence of many antibiotic-producing organisms in soil. Some strains of R. radiobacter, including our isolate, may acquire such resistance; therefore, therapy must be directed on the basis of the susceptibility pattern of the individual strain to antibacterial agents.

 
* Corresponding author. Mailing address: Clinical Laboratories, Inc., a LabCorp Company, 901 Keystone Industrial Park, Throop, PA 18512. Phone: (570) 346-1759. Fax: (570) 941-3588. E-mail: hnamdari{at}clinical.com.

Top Abstract Case report References

 

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1. Alnor, D., N. Frimodt-Moller, F. Espersen, and W. Frederiksen. 1994. Infections with the unusual human pathogens Agrobacterium species and Ochrobactrum anthropi. Clin. Infect. Dis. 18:914-920.[Medline]
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2. Dunne, W. M., Jr., J. Tillman, and J. C. Murray. 1993. Recovery of a strain of Agrobacterium radiobacter with a mucoid phenotype from an immunocompromised child with bacteremia. J. Clin. Microbiol. 31:2541-2543.[Abstract/Free Full Text]
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3. Edmond, M. B., S. A. Riddler, C. M. Baxter, B. M. Wicklund, and A. W. Pasculle. 1993. Agrobacterium radiobacter: a recently recognized opportunistic pathogen. Clin. Infect. Dis. 16:388-391.[Medline]
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4. Hulse, M., S. Johnson, and P. Ferrieri. 1993. Agrobacterium infections in humans: experience at one hospital and review. Clin. Infect. Dis. 16:112-117.[Medline]
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5. Martinez, J. L., J. Martinez-Suarez, E. Culebras , J. C. Perez-Diaz , and F. Baquero. 1989. Antibiotic inactivating enzymes from a clinical isolate of Agrobacterium radiobacter. J. Antimicrob. Chemother. 23:283-284.[Free Full Text]
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6. Miller, J. M., C. Novy, and M. Hiott. 1996. Case of bacterial endophthalmitis caused by an Agrobacterium radiobacter-like organism. J. Clin. Microbiol. 34:3212-3213.[Abstract]
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7. Sawada, H., H. Ieki, H. Oyaizu, and S. Matsumoto. 1993. Proposal for rejection of Agrobacterium tumefaciens and revised descriptions for the genus Agrobacterium and for Agrobacterium radiobacter and Agrobacterium rhizogenes. Int. J. Syst. Bacteriol. 43:694-702.[Abstract/Free Full Text]
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8. Young, J. M., L. D. Kuykendall, E. Martinez-Romero, A. Kerr, and H. Sawada. 2001. A revision of Rhizobium Frank 1889, with an emended description of the genus, and the inclusion of all species of Agrobacterium Conn 1942 and Allorhizobium undicola de Lajudie et al. 1998 as new combinations: Rhizobium radiobacter, R. rhizogenes, R. rubi, R. undicola and R. vitis. Int. J. Syst. Evol. Microbiol. 51:89-103.[Abstract]

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Journal of Clinical Microbiology, August 2003, p. 3998-4000, Vol. 41, No. 8
0095-1137/03/$08.00+0     DOI: 10.1128/JCM.41.8.3998-4000.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.

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