PANTOEA AGGLOMERANS ENDOPHTHALMITIS Clinical Features and Outcomes ADITYA SUDHALKAR, MS,* AJIT B. MAJJI, MD,* JAY CHHABLANI, MS,* GURUPRASAD MANDERWAD, PHD† Purpose: To determine the clinical profile and outcomes of patients with Pantoea agglomerans endophthalmitis as seen at a tertiary eye care center in India. Methods: Retrospective observational case series. Data collected included demographics, history, the initial and final corrected distance visual acuity, details of the ocular and systemic examination, surgeries performed, and the final anatomical outcome. The final corrected distance visual acuity and the anatomical outcome were the outcome measures. Results: Four patients had traumatic endophthalmitis; the fifth developed endophthalmitis after cataract surgery. All patients were men with a mean age of 34.24 ± 23.34 years. Three patients had corneal laceration and traumatic cataract. All patients underwent vitreous sampling with intraocular antibiotic injection with or without lensectomy and corneal wound repair. The visual acuity at presentation ranged from hand motion to perception of light. One patient ended up with phthisis in the affected eye. One patient developed postoperative retinal detachment and underwent successful surgery. The final visual acuity ranged from 20/25 to no light perception. Conclusion: P. agglomerans is a likely source of infection in traumatic and postoperative cases. Though variable, it appears sensitive to common antibiotics. The visual and anatomical prognosis seems fair in most cases. Special care needs to be taken to ensure the organism is not missed, given the rarity of the condition and the isolation techniques required. RETINA 34:1702–1706, 2014

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through contaminated intravenous fluid, the anesthetic agent propofol, total parenteral nutrition, and blood products.4–10 Ocular infections with Pantoea species have been reported.11 There is scant literature, however, on the occurrence of Pantoea endophthalmitis, with a couple of reports from South Korea being the only recently published data on the same to date.12,13 We present the clinical–microbiologic profile and outcomes of a series of cases of endophthalmitis caused by Pantoea species at a tertiary eye care center in India.

antoea agglomerans (formerly Enterobacter agglomerans) is a gram-negative aerobic bacillus in the family Enterobacteriaceae. All species of the genus Pantoea can be isolated from feculent material, plants, and soil,1 where they can be either pathogens or commensals.2 P. agglomerans is the most commonly isolated species of the Enterobacteriaceae family in humans and ubiquitous in nature.3 This organism causes soft tissue or bone/joint infections after penetrating trauma by vegetation, or bacteremia From the *Smt. Kanuri Santhamma Center for Vitreoretinal Diseases, LV Prasad Eye Institute, KAR Campus, Hyderabad, India; and †Jhaveri Microbiology Centre, KAR Campus, Hyderabad, India. Paper presented as a poster at AAO, Chicago, IL, November 13, 2012. None of the authors have any financial/conflicting interests to disclose. Reprint requests: Jay Chhablani, MS, Smt. Kanuri Santhamma Centre for Vitreoretinal Diseases, LV Prasad Eye Institute, Banjara Hills Road no. 2, Hyderabad, -500034, Andhra Pradesh, India; e-mail: [email protected]

Material and Methods A retrospective database search was made for culture-proven endophthalmitis because of Pantoea species from January 1, 1994 to May 31, 2012, as per guidelines set out for chart reviews. The Institutional Review Board of the LV Prasad Eye Institute, 1702

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Table 1. An Outline of the Demographics, Etiology, Initial and Final VA, and Final Anatomical Outcome of all Patients With Pantoea Endophthalmitis S. No.

Age/Sex

Etiology

1

40/M

2

11/M

3

29/M

4

35/M

Trauma (wooden splinter) Trauma (wooden splinter) Trauma (wooden splinter) Trauma (thorn)

5

55/M

Postoperative

Time to Presentation, days

Baseline CDVA

Final CDVA

Follow-up Duration, months

2

PL+

CF 1.5 m

2

4

PL+

NPL

8

1

HM+

20/20p

6

30

PL+

CF 2 m

1

1

PL+

20/100

24

Anatomical Outcome Retina attached Phthisis Retinal attached Retina attached Retina attached

All patients received a debulking vitrectomy and empirical intravitreal vancomycin and ceftazidime (empirically) at presentation. Patient 5 additionally received intravitreal dexamethasone at presentation. Patient 4 additionally received intravitreal amphotericin at presentation. CDVA, corrected distance visual acuity; CF, counting fingers; HM, hand motion; NPL, no light perception; PL, perception of light.

Hyderabad approved the study. Data collection included demographic information including ocular and medical history, previous ophthalmic surgery, details of the ocular and systemic examination, special investigations (ocular or systemic), time between event and diagnosis of endophthalmitis, culture sites, organism(s), antibiotic susceptibility and resistance patterns, administered treatment, and final outcomes. Vitreous samples were obtained by vitreous biopsy, with a vitreous cutter without starting infusion to avoid dilution of the sample as per the standard protocol followed in our institute. The ocular specimens were collected

and subjected for smears and cultures. All of the microbiologic testing was performed at the Jhaveri Microbiology Centre at our institute. The smear examination included Gram, Giemsa, KOH, and Calcofluor white. The culture media included blood agar, chocolate agar, brain heart infusion medium, thioglycolate broth, Sabouraud’s media, and potato dextrose agar. Isolates had been identified by either the BioMerieux strip method or Vitek II identification system (all five identified cases; BioMerieux, Marcy l’Etoile, France). Susceptibility testing was performed using the Kirby– Bauer disk diffusion method.

Fig. 1. Shows the diffuse (A) and slit-lamp (B) images along with the ultrasound B-scan (C) and corresponding A-scan (D) of Patient 5 who developed Pantoea agglomerans endophthalmitis postoperatively. The slit-lamp images (A and B) show severe conjunctival injection and hypopyon. The ultrasound scans (C and D) show low reflective dot echoes in the vitreous cavity. The findings were suggestive of endophthalmitis.

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Fig. 2. Shows the Pantoea agglomerans colonies on blood and chocolate agar, grown from the vitreous sample taken from Patient 5. The colonies are yellow, translucent to opaque, and clustered around the area of inoculation.

All patients were managed in consult with a physician to rule out concurrent systemic foci of infection. All patients initially received empirical intraocular antibiotic therapy at the time surgical intervention, including vancomycin and amikacin or ceftazidime. Intravitreal antibiotic injections were repeated later as per the sensitivity report, along with steroids. Additional procedures, such as cataract extraction, corneal laceration repair, or retinal detachment surgery were performed as required, based on the individual merits of each case.

Results A total of 19 culture-proven cases of ocular infections secondary to Pantoea species, all of them identified as P. agglomerans, were obtained from our records. Five of these had endophthalmitis, and these constitute the content of this article. The mean age of the patients was 34.24 ± 23.34 years. All patients were men, and all were involved in agriculture professionally. The salient features of all the patients are described in Table 1, and the subsequent description refers to them as numbered serially in the table. At presentation, all patients had lid edema, a severe anterior chamber inflammatory reaction with hypopyon (average, 1.2 ± 0.74 mm; range, 0.5–2.5 mm) (Figure 1) and inflammatory vitreous opacities, which were confirmed with an ultrasound B-scan. The disk and first order blood vessels were visible on table at the end of vitrectomy in all patients except Patients 2 and 4. Postoperatively, all patients were started on topical fortified cefazolin (50 mg/mL) and ciprofloxacin (0.3%) eye drops every hour, along with hourly topical prednisolone (1%) and atropine (1%) eye drops

thrice daily. All patients were also given oral ciprofloxacin (750 mg) twice daily empirically, although the sensitivity reports were awaited. Further, therapy was as per the sensitivity report, the response to therapy, and the development of complications, if any. Gram-negative bacilli were identified in all patients on Gram and Giemsa stains, and culture (Figure 2). Table 2 lists the sensitivity patterns for all patients. Antibiotic sensitivity was quite variable, except for amikacin, vancomycin, ciprofloxacin, and ceftazidime, for which all samples were uniformly sensitive. In addition to the appropriate intravitreal antibiotic based on the sensitivity report, all patients received dexamethasone intravitreally with the second injection. The final visual acuity and significant findings for each patient have been mentioned in Table 1.

Discussion This small case series brings to the fore a relatively unknown microbe and the consequences of ocular infection secondary to it. The lack of data probably stems from it being primarily an uncommon human pathogen, especially regarding ocular infections, with only a few case reports available.11–14 It follows from its habitat that the most common mode of inoculation in the eye would be through trauma. It has been isolated from hospital sources,4,6,8 and one such source probably accounted for the solitary postoperative patient whom we have in our study. The organisms in our series were sensitive to commonly used medications, such as amikacin, vancomycin, ceftazidime, and imipenem, although the odd isolate did show resistance. This is similar to most

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S R S S S

S R R S S

S S S S R

S S S S S

S S S S S

S S S S S

S S S S S

S S S S S

S S S S S

S S S S S

published studies.6,9–14 There is a variation in the sensitivity pattern in the published literature, although the strains in other series were sensitive to most commonly used antibiotics too; this could reflect some variations in strain characteristics, but also might be due to variations in susceptibility testing patterns across the globe. The visual outcomes in our series were quite variable, and were possibly influenced to some extent by the use of steroids. Two patients recovered to a visual acuity of .20/200. Two patients ended up with a visual acuity of light perception or worse, whereas one patient had barely ambulatory vision at the final follow-up. Possibly, fundus visualization on the table might be a marker of a better eventual visual outcome. There have only been a few case reports,11–14 with only two of them being recent, on P. agglomerans endophthalmitis. These include traumatic and endogenous cases. The visual outcomes in these reports have been quite variable when compared with our series. Identification of the pathogen has been reported successfully through both VITEK II and DNA sequencing.14,15 As per past reports, VITEK II offers reliable identification, with gene sequencing resorted to only if VITEK II gives inconsistent results.14–16 P. agglomerans strains generally show uniform susceptibility to aminoglycosides and most antibiotics in general, as per past reports.16 The time to presentation did not show any particular correlation with the final visual outcome (P = 0.32). The organism showed sensitivity to most commonly used antibiotics, and thus sensitivity currently does not seem to be a cause for concern. Again, the series is too small to comment upon sensitivity. To conclude, P. agglomerans is an uncommon, though increasingly reported, microbe that is significant for posttraumatic endophthalmitis. Finally, we noted a generally poor visual outcome in most cases despite relatively early intervention, with one patient ending up with a phthisical eye. Steroids seemed to play a role in decreasing the inflammation, with one patient gaining significantly visually. It should be borne in mind that most of the cases were posttraumatic, and the associated trauma too influenced the final visual outcome. This, to the best of our knowledge, is the largest case series reported on P. agglomerans endophthalmitis. R, resistance; S, sensitive.

S S S R S S R R S S S S S S S 1 2 3 4 5

Amoxicillin/ Clavulanic Case Acid Ampicillin Cefazolin Ceftazidime Ceftriaxone Gatifloxacin Gentamicin Imipenem Levofloxacin Moxifloxacin Norfloxacin Ofloxacin No. Amikacin

Table 2. Antibiotic Sensitivity Pattern for all Five Isolates

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Key words: Pantoea agglomerans, endophthalmitis, traumatic endophthalmitis. References 1. De Champs C, Le Seaux S, Dubost JJ, et al. Isolation of Pantoea agglomerans in two cases of septic monoarthritis after plant thorn and wood sliver injuries. J Clin Microbiol 2000; 38:460–461.

1706 RETINA, THE JOURNAL OF RETINAL AND VITREOUS DISEASES 2. Monier JM, Lindow SE. Aggregates of resident bacteria facilitate survival of immigrant bacteria on leaf surfaces. Microb Ecol 2005;49:343–352. 3. Cruz AT, Cazacu AC, Allen CH. Pantoea agglomerans, a plant pathogen causing human disease. J Clin Microbiol 2007;45: 1989–1992. 4. Alvarez FE, Rogge KJ, Tarrand J, Lichtiger B. Bacterial contamination of cellular blood components. A retrospective review at a large cancer center. Ann Clin Lab Sci 1995;25:283–290. 5. Andersson AM, Weiss N, Rainey F, Salkinoja-Salonen MS. Dust-borne bacteria in animal sheds, schools and children’s day care centres. J Appl Microbiol 1999;86:622–634. 6. Bennett SN, McNeil MM, Bland LA, et al. Postoperative infections traced to contamination of an intravenous anesthetic, propofol. N Engl J Med 1995;333:147–154. 7. Flatauer FE, Khan MA. Septic arthritis caused by Enterobacter agglomerans. Arch Intern Med 1978;138:788. 8. Habsah H, Zeehaida M, Van Rostenberghe H, et al. An outbreak of Pantoea spp. in a neonatal intensive care unit secondary to contaminated parenteral nutrition. J Hosp Infect 2005;61:213–218. 9. Kratz A, Greenberg D, Barki Y, et al. Pantoea agglomerans as a cause of septic arthritis after palm tree thorn injury; case report and literature review. Arch Dis Child 2003;88:542–544.



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10. Ulloa-Gutierrez R, Moya T, Avila-Aguero ML. Pantoea agglomerans and thorn-associated suppurative arthritis. Pediatr Infect Dis J 2004;23:690. 11. Lee NE, Chung IY, Park JM. A case of Pantoea endophthalmitis. Korean J Ophthalmol 2010;24:318–321. 12. Mason GI, Bottone EJ, Podos SM. Traumatic endophthalmitis caused by an Erwinia species. Am J Ophthalmol 1976;82: 709–713. 13. Seok S, Jang YJ, Lee SW, et al. A case of bilateral endogenous Pantoea agglomerans endophthalmitis with interstitial lung disease. Korean J Ophthalmol 2010;24:249–251. 14. Zeiter JH, Koch DD, Park ED II, Font RL. Endogenous endophthalmitis with lenticular abscess caused by Enterobacter agglomerans (Erwinia species). Ophthalmic Surg 1989;20:9–12. 15. Stone N, O’ Hara C, Williams P, et al. Comparison of disk diffusion, VITEK 2, and broth microdilution antimicrobial susceptibility test results for unusual species of Enterobacteriaceae. J Clin Microbiol 2007;45:340–346. 16. Delétoile A, Decré D, Courant S, et al. Phylogeny and Identification of Pantoea Species and Typing of Pantoea agglomerans Strains by Multilocus Gene Sequencing. J Clin Microbiol 2009;47.

Pantoea agglomerans endophthalmitis: clinical features and outcomes.

To determine the clinical profile and outcomes of patients with Pantoea agglomerans endophthalmitis as seen at a tertiary eye care center in India...
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