Next Article in Journal
Research Updates of Plasmid-Mediated Aminoglycoside Resistance 16S rRNA Methyltransferase
Previous Article in Journal
Cefiderocol for Carbapenem-Resistant Bacteria: Handle with Care! A Review of the Real-World Evidence
 
 
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Case Report

A Rare Case of Endophthalmitis with Rhizobium radiobacter, Soon after a Resolved Keratitis: Case Report

by
Andrei Theodor Balasoiu
1,
Ovidiu Mircea Zlatian
2,*,
Alice Elena Ghenea
2,*,
Livia Davidescu
3,
Alina Lungu
4,
Andreea Loredana Golli
5,
Anca-Loredana Udriștoiu
6 and
Maria Balasoiu
2
1
Department of Ophthalmology, University of Medicine and Pharmacy of Craiova, 200349 Craiova, Romania
2
Department of Bacteriology-Virology-Parasitology, University of Medicine and Pharmacy of Craiova, 200349 Craiova, Romania
3
Department of Ophthalmology, County Clinical Emergency Hospital of Craiova, 200642 Craiova, Romania
4
Department of Infectious diseases, County Clinical Emergency Hospital of Craiova, 200642 Craiova, Romania
5
Department of Epidemiology, University of Medicine and Pharmacy of Craiova, 200349 Craiova, Romania
6
Faculty of Automation, Computers and Electronics, University of Craiova, 200776 Craiova, Romania
*
Authors to whom correspondence should be addressed.
Antibiotics 2022, 11(7), 905; https://doi.org/10.3390/antibiotics11070905
Submission received: 16 June 2022 / Revised: 3 July 2022 / Accepted: 4 July 2022 / Published: 6 July 2022
(This article belongs to the Section Antibiotic Therapy in Infectious Diseases)

Abstract

:
Background: Rhizobium (Agrobacterium) species are plant aerobic bacteria, which in some cases can produce endophthalmitis in humans after corneal trauma. Case presentation: A 42-year-old female patient presented in the Emergency Department of the Emergency County Hospital of Craiova, Romania, reporting pain, epiphora, and blurry vision in her right eye for about five days. This initial infectious keratitis episode was successfully resolved, but after 20 days she presented again after trauma with a leaf with corneal abscess. In the conjunctival secretion, R. radiobacter was identified. Despite antibiotherapy, the patient’s state did not improve, and ultimately the eye was eviscerated. Methods: A search was performed in the ProQuest, PubMed, and ScienceDirect databases for the terms Agrobacterium, Rhizobium, radiobacter, and eye. We eliminated non-human studies, editorials and commentaries, and non-relevant content, and excluded the duplicates. Results: In total, 138 studies were initially obtained, and then we selected 26 studies for retrieval. After the selection process, we ended up including 17 studies in our analysis. Most studies reported R. radiobacter endophthalmitis after ocular surgical procedures or outdoor activities that involve exposure to soil. Conclusion: R. radiobacter is a rare cause of endophthalmitis after eye trauma that generally responds well to usual antibiotherapy, but occasionally can evolve to severe, leading to the loss of the eye.

1. Introduction

Endophthalmitis is a leading cause of eye loss worldwide, despite the prophylactic antibiotherapy used for eye trauma, whether accidental or surgical [1,2,3,4]. Table 1 summarizes the main infectious agents involved in endophthalmitis, which is caused by different mechanisms, including trauma, eye surgery, contact lenses, eye injections or other related procedures, or hematological inoculation.
A rare cause of endophthalmitis is infection with Rhizobium (Agrobacterium) radiobacter, which is a plant aerobic bacterium belonging to the Gram-negative bacilli, which are common in the environment—especially in soil [21]—and cause plant diseases such as gall tumors and hairy root disease. Several cases of Rhizobium radiobacter endophthalmitis have been reported, usually after cataract surgery, but have only rarely been reported to produce human infections, most often in immunocompromised patients [22,23,24,25]. The main risk factors are non-adherence to aseptic techniques [26,27], paracentesis of the anterior chamber, and eyelid manipulation [2,28].
Here, we describe a case of bacterial keratitis with severe evolution.

2. Case Report

A 42-year-old female patient presented in the Emergency Department of the Emergency County Hospital of Craiova, Romania, on 4 April 2022, reporting pain, epiphora, and blurry vision in her right eye for about five days. Anamnesis revealed a history of chemically treated soil contact with her right eye about seven days before the presentation, as she lives in the countryside and works in agriculture. The patient had not been immunocompromised or treated with steroids. Uncorrected visual acuity was 0.25 in her right eye and 1 in her left eye; the best-corrected visual acuity (BCVA) in her right eye was 0.25 (normal visual acuity is 1). Intraocular pressure (IOP) was 17 mmHg in her right eye and 15 mmHg in her left eye (the normal range is between 10 and 21 mmHg). Slit-lamp examination in the right eye revealed conjunctival hyperemia, a 4 mm white–yellow central corneal ulceration with infiltrated margins that retained the methylene blue stain, Descemet folds at the lesion and endothelial edema, a normal-depth anterior chamber, less than five cells in the aqueous, miotic, and reflexive pupil (Figure 1). Due to corneal haze, fundus examination was difficult to perform in the right eye, but it was normal in the left eye. Corneal sensitivity was tested in the right eye, and the result was hyperesthesia. A clinical diagnosis of infectious keratitis of the left eye was established. A SARS-CoV-2 rapid antigen test was performed, and as it was negative the patient was admitted to hospital in the Ophthalmology Clinic.
Conjunctival secretion and corneal scraping samples were collected and sent to the hospital’s laboratory for microbiology diagnosis and antibiogram; standard blood tests were also performed. Intravenous empirical broad-spectrum antibiotherapy was introduced immediately after sampling (third-generation cephalosporin/beta-lactamase inhibitor—cefoperazone/sulbactam), doubled by local antibiotherapy (topical moxifloxacin). Lubricants, mydriatics, topical NSAIDs, and eye patching were also prescribed.
Microbiology results were negative for bacteria and fungi; the rest of the tests were also normal. Fortunately, the evolution was favorable: the ulceration’s size started to decrease daily, the Descemet folds became thinner, and visual acuity was also improving, so on 10 April 2022, the patient was discharged from hospital. Clinical examination of the right eye that day revealed that the uncorrected visual acuity was 0.9, IOP was 16 mmHg, the slit-lamp examination showed minimal conjunctival hyperemia, paracentral corneal 3 mm leucoma, and a quiet anterior chamber, and the fundus was also normal. The recommendation was topical treatment with lubricants, moxifloxacin, and NSAIDs, and ambulatory appointment after one week.
The patient presented ambulatory, one week after hospital discharge, in the Ophthalmology Clinic, where the slit-lamp examination revealed a quiet right eye, no conjunctival hyperemia, paracentral corneal 3 mm leucoma, normal aspect of the fundus, and 0.9 visual acuity. Topical antibiotics and NSAIDs were interrupted after this examination, but the eye lubricants were kept and the patient returned to work.
On 29 April 2022, the patient presented again in the Emergency Department of the Emergency County Hospital of Craiova, Romania, reporting severe pain, photophobia, epiphora, and a severe decrease in visual acuity in her right eye. The symptoms started four to five days before the presentation; she linked the debut with eye trauma caused by plant leaves. Visual acuity in the right eye was counting fingers at two meters, IOP was 18 mmHg, and the slit-lamp examination revealed a 6 mm white corneal abscess with perilesional infiltration, thick Descemet folds, Tyndall ++, and myotic pupil. The clinical diagnosis was corneal abscess with exogenous uveitis of the right eye. A SARS-CoV-2 rapid antigen test was performed, and as it was negative the patient was admitted to hospital in the Ophthalmology Clinic.
Conjunctival secretions and corneal scrapings were again collected and sent to the hospital’s laboratory for microbiology diagnosis and antibiogram; standard blood tests were also performed (10.6 × 103/µL leukocytosis and 87.3%/9.2 × 103/µL neutrophilia). Intravenous empirical double antibiotherapy was introduced immediately after sampling (third-generation cephalosporin/beta-lactamase inhibitor—cefoperazone/sulbactam and gentamycin), doubled by local antibiotherapy (topical levofloxacin). Lubricants, mydriatics, topical NSAIDs, and eye patching were also prescribed. The patient presented dizziness, nausea, and a body temperature raised to 37.5 °C; thus, she was booked for examination in the Internal Medicine Clinic. The general examination did not stress any pathological findings, and blood pressure was 100/60 mmHg. Recommendations were as follows: RT PCR SARS-CoV-2 (which was negative), hemoculture if the temperature rises above 38 °C (did not happen), hydration (according to blood pressure), and NSAIDs in case of fever.
The evolution was unfavorable as the visual acuity decreased to counting fingers at one meter, the corneal abscess remained the same size, a 2 mm hypopyon appeared, and the subjective pain increased (30 April). An infectious disease specialist was asked to see the patient, and the recommendations were as follows: further serological investigations for HIV, cytomegalovirus, and hepatitis viruses B and C, which were negative. It was also recommended to stop cefoperazone/sulbactam + gentamicin therapy and change to a teicoplanin + azithromycin regimen. Despite antibiotic changes, the patient’s state did not improve: visual acuity in the right eye was limited to hand movement, the whole cornea was infiltrated, the abscess was 6–7 mm, and the hypopyon was 3–4 mm (1 May) (Figure 2).
The microbiology results then came in. Bacteriologically, the samples were inoculated under aerobic, anaerobic, and microaerophilic conditions in Columbia blood agar, chocolate agar supplemented with PVX, and MacConkey culture medium for 24 h at 37 °C in aerobiose (48 h in anaerobiose and microaerophily). We observed in both samples on blood agar in large (2–4 mm), convex, non-pigmented, light beige, non-hemolytic, raised aerobiotic colonies, with a dry central portion and wet at the edges (Figure 3).
Biochemically, the strain was glucose-non-fermenting, oxidase-positive, mobile, indole-negative, and urease-positive. The biochemical identification on a VITEK2 automated system (Biomerieux) with a GN card identified R. radiobacter with 99% probability after 3.8 h of analysis (Figure 4).
In the microscopic exam we observed long and thin unsporulated Gram-negative rods with a tendency of adhesion between them (Figure 5).
Antibiotic susceptibility testing on the VITEK2 Compact system using the card AST-N233/AST-XN05 showed susceptibility to ticarcillin and ticarcillin–clavulanate (MIC ≤ 8), piperacillin and piperacillin–tazobactam (MIC ≤ 4), cefepime (MIC ≤ 1), imipenem, and meropenem (MIC ≤ 0.25). Aminoglycosides were also susceptible (amikacin MIC ≤ 2, gentamycin MIC ≤ 1, tobramycin ≤ 1), as were the quinolones (ciprofloxacin/ofloxacin MIC ≤ 0.25 and levofloxacin MIC ≤ 0.12). The strain was resistant to colistin (MIC ≥ 16). The MIC for tigecycline was ≤0.5, which the system interpreted as resistant.
On 2 May 2022, the patient requested transfer to the Emergency Eye Diseases Hospital in Bucharest, Romania, and it was granted. The right eye status was as follows: visual acuity was light perception, severe conjunctival hyperemia, infiltrated cornea, 6–7 mm corneal abscess, 4 mm hypopyon, and fundus examination was not possible due to corneal opacity. The clinical and microbiological diagnosis was severe bacterial keratitis (corneal abscess with R. radiobacter) and exogenous endophthalmitis.
Unfortunately for this patient, the evolution was unfavorable, and within days after she was transferred to Bucharest the eye was eviscerated to prevent orbital, sinus, and cerebral infection complications.

3. Systematic Review

We searched ProQuest, PubMed, and ScienceDirect for the terms Agrobacterium, Rhizobium, radiobacter, and eye (the exact search string was “(Agrobacterium OR Rhizobium) AND radiobacter and eye”). The eligibility criteria included human studies of infections of the eye with R. radiobacter, and all article types except for comments, editorials, etc. The database search yielded 138 studies: 96 from the ProQuest database, 8 from PubMed, and 34 from ScienceDirect; 110 studies were not retrieved as they were non-human studies. We excluded two more studies as they were editorials or comments. Therefore, we selected 26 studies for retrieval: 7 studies from the PubMed database, 10 from ProQuest, and 9 from ScienceDirect; 5 studies were duplicates. We excluded 4 more studies from the analysis after reading the abstracts: two studies identified R. radiobacter in solutions used for the storage of contact lenses [29,30]; one study referred to sepsis with R. radiobacter originating from a central venous catheter [31]; and one study identified this pathogen in surgical equipment used in ophthalmology (vacuum control manifold) [32] (Figure 6).
Therefore, we included 17 studies in the systematic review (Table 2).
Rohowetz et al. [33] reported endophthalmitis with R. radiobacter in a 79–year-old male patient with type II diabetes mellitus and diabetic retinopathy, who received treatment with intravitreal aflibercept. The patient was treated empirically with intravitreal injections of ceftazidime and vancomycin. After the laboratory results came in, the patient’s therapy was changed to oral azithromycin and levofloxacin. The infection was resolved at 1-month follow-up.
The same author, one year later, reported a case of endophthalmitis in an 85-year-old male associated with insertion of an inferonasal Baerveldt tube [34]. R. radiobacter was identified in aqueous humor culture, and was resistant to cefazolin, ceftazidime, amikacin, tobramycin, and trimethoprim–sulfamethoxazole. Because the explantation of the drainage implant was not efficient, pars plana vitrectomy was performed with removal of the intraocular lens, associated with silicone oil infusions and intravitreal antibiotics. The patient’s visual acuity improved after 2 weeks, but then it was lost to follow-up.
Barker et al. [35] reported a series of four cases with R. radiobacter in young patients: one after corneal traumatism and three in long-term contact lens wearers. The patients were treated with steroidal anti-inflammatory drugs and with antibiotic drops. All cases had a favorable evolution, with total sight recovery. Furthermore, Fenner et al. [36] reported keratitis in a young patient who was a contact lens wearer.
Another case of R. radiobacter infection was reported after phakic intraocular lens implantation in the posterior chamber of the eye in a young patient (29 years old) with myopia [37]. The endophthalmitis was resolved after intravitreal injections of vancomycin and ceftazidime.
One study identified one strain of R. radiobacter (1.14%) in 88 patients expressing symptoms consistent with conjunctivitis [40]. Another study included 44 patients with polymicrobial keratitis, from which R. radiobacter was isolated in one case (2.27%).
Nine studies were research articles, which included 912 patients who had undergone cataract surgery [4,5,6,7,8,9,10,11,41]. From those, in 18 cases (1.97%), R. radiobacter was isolated. In 7 of those 18 cases, R. radiobacter was associated with endophthalmitis, but in the remaining 11 cases it was considered an environmental contaminant. Moreover, Namdari et al. [42] in 2003 reported a case of chronic endophthalmitis after cataract extraction produced by R. radiobacter, which was resistant to vancomycin, amikacin, and ceftazidime—drugs often used in empirical therapy. Ultimately, the infection was resolved after changing the therapy to intravitreal injections of gentamycin and oral ciprofloxacin.
Therefore, endophthalmitis with R. radiobacter is rare, and is usually encountered after cataract surgery—mostly in old people and immunosuppressed patients, but also in young patients who wear contact lenses for extended periods of time.

4. Discussion

Rhizobium is a rare agent of endophthalmitis in patients who come into contact with plants [21]. Initially classified as Agrobacterium, after the introduction of 16s RNA genetic sequencing in the 1990s, many species were reclassified into the genus Rhizobium. The genus is divided into species based largely on pathogenic properties in plants: R. radiobacter (non-pathogenic), R. tumefaciens (the causative agent of crown gall tumors), R. rhizogenes (the causative agent of hairy root disease), and R. vitis (the causative agent of tumors and necrotic disease on grapevines). There are also less well-studied proposed species such as R. rubi isolated from cane galls on Rubus plant species.
The first Rhizobium strains were isolated from human infections in 1967 [43]. The first infection with R. radiobacter was reported in a case of endocarditis on a prosthetic valve [44]. In 1996, the first case of Rhizobium radiobacter endophthalmitis was reported after cataract surgery [42] and intravitreous injections [45]. Few cases have been reported since then [33]. In our clinic, this is the first confirmed case of R. radiobacter endophthalmitis.
The reported cases of ocular R. radiobacter infections occurred after traumatic medical procedures involving the eye, such as cataract surgery [42] or intravitreal injections [33]. Our patient, however, developed endophthalmitis after eye trauma caused by a plant leaf. In this case, our understanding is that the first episode was a local infection, which indeed resolved, but acted as a risk factor for infection with R. radiobacter after the eye trauma caused by the plant leaf. Indeed, as Rhizobium species are predominantly found in soil and plants, it is thought that cases of endophthalmitis after eye surgery are associated with outdoor activities and contamination of the eye with dust.
Although R. radiobacter infections are usually reported in immunocompromised hosts, our patient was immunocompetent; in this case, the eye trauma directly inoculated the eye with the pathogen at a much higher dose than that found in dust that contaminated the eye after medical procedures in other reported cases.

5. Conclusions

To summarize, R. radiobacter is a soil bacterium that rarely causes human infection. Nevertheless, patients with eye surgery or other procedures that provide a continuity solution of the cornea, including endophthalmitis, can develop endophthalmitis following exposure to soil. It is therefore recommended that patients who undergo surgical procedures such as cataract surgery or intravitreal injections should avoid outdoor activities that involve exposure to soil and plants (yardwork, farming, etc.).

Author Contributions

Conceptualization, A.T.B., A.E.G., O.M.Z., and M.B.; methodology, A.T.B., A.-L.U., and A.E.G.; software, A.E.G., O.M.Z., A.-L.U., and A.T.B.; validation, A.T.B., A.E.G., M.B., and O.M.Z.; formal analysis, O.M.Z., L.D., A.L., A.L.G., and A.E.G.; resources, A.T.B., O.M.Z., and A.E.G.; data curation, L.D., A.T.B., M.B., and A.L.; writing—original draft preparation, A.T.B., A.E.G., O.M.Z., and M.B.; writing—review and editing, A.E.G., A.T.B., O.M.Z., A.L.G, A.-L.U., and L.D.; supervision, M.B., A.E.G., and A.T.B. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Informed consent was obtained from the subject of this report. Written informed consent has been obtained from the patient to publish this paper.

Data Availability Statement

The data presented in this study are available upon request from the corresponding author.

Acknowledgments

The Article Processing Charges were funded by the University of Medicine and Pharmacy of Craiova, Romania.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Kowalski, R.P.; Nayyar, S.V.; Romanowski, E.G.; Shanks, R.M.Q.; Mammen, A.; Dhaliwal, D.K.; Jhanji, V. The Prevalence of Bacteria, Fungi, Viruses, and Acanthamoeba from 3004 Cases of Keratitis, Endophthalmitis, and Conjunctivitis. Eye Contact Lens 2020, 46, 265–268. [Google Scholar] [CrossRef] [PubMed]
  2. Helbig, H.; Noske, W.; Kleineidam, M.; Kellner, U.; Foerster, M.H. Bacterial Endophthalmitis after Anterior Chamber Paracentesis. Br. J. Ophthalmol. 1995, 79, 866. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  3. Hoevenaars, N.E.D.; Gans, D.; Missotten, T.; van Rooij, J.; Lesaffre, E.; van Meurs, J.C. Suspected Bacterial Endophthalmitis Following Intravitreal Anti-VEGF Injection: Case Series and Literature Review. Ophthalmol. J. Int. D’ophtalmol. Int. J. Ophthalmol. Z. Augenheilkd. 2012, 228, 143–147. [Google Scholar] [CrossRef] [PubMed]
  4. Mishra, D.; Satpathy, G.; Chawla, R.; Venkatesh, P.; Ahmed, N.H.; Panda, S.K. Utility of Broad-Range 16S RRNA PCR Assay versus Conventional Methods for Laboratory Diagnosis of Bacterial Endophthalmitis in a Tertiary Care Hospital. Br. J. Ophthalmol. 2019, 103, 152–156. [Google Scholar] [CrossRef]
  5. Hsu, H.Y.; Lind, J.T.; Tseng, L.; Miller, D. Ocular Flora and Their Antibiotic Resistance Patterns in the Midwest: A Prospective Study of Patients Undergoing Cataract Surgery. Am. J. Ophthalmol. 2013, 155, 36–44.e2. [Google Scholar] [CrossRef]
  6. Shirodkar, A.R.; Pathengay, A.; Flynn, H.W.; Albini, T.A.; Berrocal, A.M.; Davis, J.L.; Lalwani, G.A.; Murray, T.G.; Smiddy, W.E.; Miller, D. Delayed- versus Acute-Onset Endophthalmitis after Cataract Surgery. Am. J. Ophthalmol. 2012, 153, 391–398.e2. [Google Scholar] [CrossRef] [Green Version]
  7. Haapala, T.T.; Nelimarkka, L.; Saari, J.M.; Ahola, V.; Saari, K.M. Endophthalmitis Following Cataract Surgery in Southwest Finland from 1987 to 2000. Graefe’s Arch. Clin. Exp. Ophthalmol. Albrecht Graefes Arch. Klin. Exp. Ophthalmol. 2005, 243, 1010–1017. [Google Scholar] [CrossRef]
  8. Ambiya, V.; Das, T.; Sharma, S.; Chhablani, J.; Dave, V.; Jalali, S.; Narayanan, R.; Joseph, J. Comparison of Clinico-Microbiological Profile and Treatment Outcome of in-House and Referred Post Cataract Surgery Endophthalmitis in a Tertiary Care Center in South India. J. Ophthalmic Inflamm. Infect. 2016, 6, 45. [Google Scholar] [CrossRef] [Green Version]
  9. Ness, T.; Kern, W.V.; Frank, U.; Reinhard, T. Postoperative Nosocomial Endophthalmitis: Is Perioperative Antibiotic Prophylaxis Advisable? A Single Centre’s Experience. J. Hosp. Infect. 2011, 78, 138–142. [Google Scholar] [CrossRef]
  10. Chiquet, C.; Aptel, F.; Combey-De Lambert, A.; Bron, A.M.; Campolmi, N.; Palombi, K.; Thuret, G.; Rouberol, F.; Cornut, P.L.; Creuzot-Garcher, C. Occurrence and Risk Factors for Retinal Detachment after Pars Plana Vitrectomy in Acute Postcataract Bacterial Endophthalmitis. Br. J. Ophthalmol. 2016, 100, 1388–1392. [Google Scholar] [CrossRef]
  11. Friling, E.; Montan, P. Bacteriology and Cefuroxime Resistance in Endophthalmitis Following Cataract Surgery before and after the Introduction of Prophylactic Intracameral Cefuroxime: A Retrospective Single-Centre Study. J. Hosp. Infect. 2019, 101, 88–92. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  12. Ferrer, C.; Alio, J.; Rodriguez, A.; Andreu, M.; Colom, F. Endophthalmitis Caused by Fusarium Proliferatum. J. Clin. Microbiol. 2005, 43, 5372–5375. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  13. McCannel, C.A. Meta-Analysis of Endophthalmitis after Intravitreal Injection of Anti-Vascular Endothelial Growth Factor Agents: Causative Organisms and Possible Prevention Strategies. Retina 2011, 31, 654–661. [Google Scholar] [CrossRef]
  14. Miller, J.J.; Scott, I.U.; Flynn, H.W.; Smiddy, W.E.; Murray, T.G.; Berrocal, A.; Miller, D. Endophthalmitis Caused by Bacillus Species. Am. J. Ophthalmol. 2008, 145, 883–888. [Google Scholar] [CrossRef] [PubMed]
  15. Pflugfelder, S.C.; Flynn, H.W.; Zwickey, T.A.; Forster, R.K.; Tsiligianni, A.; Culbertson, W.W.; Mandelbaum, S. Exogenous Fungal Endophthalmitis. Ophthalmology 1988, 95, 19–30. [Google Scholar] [CrossRef]
  16. Al-Torbak, A.A.; Al-Shahwan, S.; Al-Jadaan, I.; Al-Hommadi, A.; Edward, D.P. Endophthalmitis Associated with the Ahmed Glaucoma Valve Implant. Br. J. Ophthalmol. 2005, 89, 454–458. [Google Scholar] [CrossRef] [PubMed]
  17. Hatami, H.; Ghaffari Jolfayi, A.; Ebrahimi, A.; Golmohammadi, S.; Zangiabadian, M.; Nasiri, M.J. Contact Lens Associated Bacterial Keratitis: Common Organisms, Antibiotic Therapy, and Global Resistance Trends: A Systematic Review. Front. Ophthalmol. 2021, 1, 5. [Google Scholar] [CrossRef]
  18. Zhang, H.; Liu, Z. Endogenous Endophthalmitis: A 10-Year Review of Culture-Positive Cases in Northern China. Ocul. Immunol. Inflamm. 2010, 18, 133–138. [Google Scholar] [CrossRef]
  19. Regan, K.A.; Radhakrishnan, N.S.; Hammer, J.D.; Wilson, B.D.; Gadkowski, L.B.; Iyer, S.S.R. Endogenous Endophthalmitis: Yield of the Diagnostic Evaluation. BMC Ophthalmol. 2020, 20, 1–7. [Google Scholar] [CrossRef]
  20. Gajdzis, M.; Figuła, K.; Kamińska, J.; Kaczmarek, R. Endogenous Endophthalmitis—The Clinical Significance of the Primary Source of Infection. J. Clin. Med. 2022, 11, 1183. [Google Scholar] [CrossRef]
  21. Lai, C.C.; Teng, L.J.; Hsueh, P.R.; Yuan, A.; Tsai, K.C.; Tang, J.L.; Tien, H.F. Clinical and Microbiological Characteristics of Rhizobium Radiobacter Infections. Clin. Infect. Dis. 2004, 38, 149–153. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  22. Chen, C.Y.; Hansen, K.S.; Hansen, L.K. Rhizobium Radiobacter as an Opportunistic Pathogen in Central Venous Catheter-Associated Bloodstream Infection: Case Report and Review. J. Hosp. Infect. 2008, 68, 203–207. [Google Scholar] [CrossRef] [PubMed]
  23. Paphitou, N.I.; Rolston, K.V.I. Catheter-Related Bacteremia Caused by Agrobacterium Radiobacter in a Cancer Patient: Case Report and Literature Review. Infection 2003, 31, 421–424. [Google Scholar] [CrossRef] [PubMed]
  24. Hanada, S.; Iwamoto, M.; Kobayashi, N.; Ando, R.; Sasaki, S. Catheter-Related Bacteremia Caused by Agrobacterium Radiobacter in a Hemodialysis Patient. Intern. Med. 2009, 48, 455–457. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  25. Miller, J.M.; Novy, C.; Hiott, M. Case of Bacterial Endophthalmitis Caused by an Agrobacterium Radiobacter-like Organism. J. Clin. Microbiol. 1996, 34, 3212–3213. [Google Scholar] [CrossRef] [Green Version]
  26. Doshi, R.R.; Leng, T.; Fung, A.E. Povidone-Iodine before Lidocaine Gel Anesthesia Achieves Surface Antisepsis. Ophthalmic Surg. Lasers Imaging 2011, 42, 346–349. [Google Scholar] [CrossRef] [PubMed]
  27. Friedman, D.A.; Mason, J.O.; Emond, T.; McGwin, G. Povidone-Iodine Contact Time and Lid Speculum Use during Intravitreal Injection. Retina 2013, 33, 975–981. [Google Scholar] [CrossRef]
  28. Avery, R.L.; Bakri, S.J.; Blumenkranz, M.S.; Brucker, A.J.; Cunningham, E.T.; D’amico, D.J.; Dugel, P.U.; Flynn, H.W.; Freund, K.B.; Haller, J.A.; et al. Intravitreal Injection Technique and Monitoring: Updated Guidelines of an Expert Panel. Retina 2014, 34 (Suppl. 12), S1–S18. [Google Scholar] [CrossRef]
  29. Donzis, P.B.; Mondino, B.J.; Weissman, B.A.; Bruckner, D.A. Microbial Contamination of Contact Lens Care Systems. Am. J. Ophthalmol. 1987, 104, 325–333. [Google Scholar] [CrossRef]
  30. Clark, B.J.; Harkins, L.S.; Munro, F.A.; Devonshire, P. Microbial Contamination of Cases Used for Storing Contact Lenses. J. Infect. 1994, 28, 293–304. [Google Scholar] [CrossRef]
  31. Romano, L.; Spanu, T.; Calista, F.; Zappacosta, B.; Mignogna, S.; Sali, M.; Fiori, B.; Fadda, G. Tsukamurella Tyrosinosolvens and Rhizobium Radiobacter Sepsis Presenting with Septic Pulmonary Emboli. Clin. Microbiol. Infect. 2011, 17, 1049–1052. [Google Scholar] [CrossRef]
  32. Miño De Kaspar, H.; Grasbon, T.; Kampik, A. Automated Surgical Equipment Requires Routine Disinfection of Vacuum Control Manifold to Prevent Postoperative Endophthalmitis. Ophthalmology 2000, 107, 685–690. [Google Scholar] [CrossRef]
  33. Rohowetz, L.J.; Yannuzzi, N.A.; Gupta, S.; Patel, N.A.; Miller, D.; Flynn, H.W. Endophthalmitis Caused by Agrobacterium Radiobacter Following Intravitreal Aflibercept for Diabetic Retinopathy. Case Rep. Ophthalmol. 2020, 11, 22–27. [Google Scholar] [CrossRef] [PubMed]
  34. Rohowetz, L.J.; Patel, N.A.; Quan, A.V.; Fan, K.C.; Yannuzzi, N.A.; Reyes-Capó, D.P.; Laura, D.; Ansari, Z.A.; Patel, U.; Dubovy, S.R.; et al. Agrobacterium Radiobacter Endophthalmitis Associated with Baerveldt Tube Exposure. Case Rep. Ophthalmol. 2021, 12, 921–926. [Google Scholar] [CrossRef]
  35. Barker, N.H.; Thompson, J.M.; Mullen, M.G.; Weekes, M.A.; Nguyen, L.N.; Haynes, C.K.M.; Miller, D. Rhizobium Radiobacter: A Recently Recognized Cause of Bacterial Keratitis. Cornea 2016, 35, 679–682. [Google Scholar] [CrossRef] [PubMed]
  36. Fenner, B.J.; Kumar, A.; Tan, N.Y.Q.; Ang, M. Case of Isolated Rhizobium Radiobacter Contact Lens-Related Infectious Keratitis: A Plant Microbe Now Emerging as a Human Pathogen. Am. J. Ophthalmol. Case Rep. 2019, 15, 100476. [Google Scholar] [CrossRef]
  37. Al-Abdullah, A.A.; Al-Falah, M.; Al-Rashaed, S.; Khandekar, R.; Arevalo, J.F. Endophthalmitis Caused by Rhizobium Radiobacter After Posterior Chamber Phakic Intraocular Lens Implantation to Correct Myopia. J. Refract. Surg. 2015, 31, 561–563. [Google Scholar] [CrossRef]
  38. CLSI. Performance Standards for Antimicrobial Susceptibility Testing, 30th ed.; CLSI supplement M100; Clinical Laboratory Standards Institute: Wayne, PA, USA, 2020. [Google Scholar]
  39. Harbiyeli, I.I.; Oruz, O.; Erdem, E.; Cam, B.; Demirkazik, M.; Acikalin, A.; Kibar, F.; Ilkit, M.; Yarkin, F.; Yagmur, M. Clinical Aspects and Prognosis of Polymicrobial Keratitis Caused by Different Microbial Combinations: A Retrospective Comparative Case Study. Int. Ophthalmol. 2021, 41, 3849–3860. [Google Scholar] [CrossRef]
  40. Tellegen, E.; ter Riet, G.; Sloos, J.H.; van Weert, H.C.P.M. Diagnosis of Conjunctivitis in Primary Care: Comparison of Two Different Culture Procedures. J. Clin. Pathol. 2009, 62, 939–941. [Google Scholar] [CrossRef]
  41. Chiquet, C.; Maurin, M.; Thuret, G.; Benito, Y.; Cornut, P.L.; Creuzot-Garcher, C.; Rouberol, F.; Pechinot, A.; Lina, G.; Romanet, J.P.; et al. Analysis of Diluted Vitreous Samples from Vitrectomy Is Useful in Eyes with Severe Acute Postoperative Endophthalmitis. Ophthalmology 2009, 116, 2437–2441. [Google Scholar] [CrossRef]
  42. Namdari, H.; Hamzavi, S.; Peairs, R.R. Rhizobium (Agrobacterium) Radiobacter Identified as a Cause of Chronic Endophthalmitis Subsequent to Cataract Extraction. J. Clin. Microbiol. 2003, 41, 3998–4000. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  43. Lautrop, H. Agrobacterium spp. Isolated from Clinical Specimens. Acta Pathol. Microbiol. Scand. Suppl. 1967, 187, 63–64. [Google Scholar]
  44. Plotkin, G.R. Agrobacterium Radiobacter Prosthetic Valve Endocarditis. Ann. Intern. Med. 1980, 93, 839–840. [Google Scholar] [CrossRef] [PubMed]
  45. Joshi, L.; Morarji, J.; Tomkins-Netzer, O.; Lightman, S.; Taylor, S.R.J. Rhizobium Radiobacter Endophthalmitis Following Intravitreal Ranibizumab Injection. Case Rep. Ophthalmol. 2012, 3, 283–285. [Google Scholar] [CrossRef] [PubMed] [Green Version]
Figure 1. Slit-lamp examination of the right eye showing conjunctival hyperemia, a 4 mm white–yellow central corneal ulceration with infiltrated margins that retains the stain, Descemet folds at the lesion, and endothelial edema (methylene blue staining).
Figure 1. Slit-lamp examination of the right eye showing conjunctival hyperemia, a 4 mm white–yellow central corneal ulceration with infiltrated margins that retains the stain, Descemet folds at the lesion, and endothelial edema (methylene blue staining).
Antibiotics 11 00905 g001
Figure 2. Slit-lamp examination of the right eye highlighting severe conjunctival hyperemia, infiltrated cornea, 6–7 mm central corneal abscess, and hypopyon.
Figure 2. Slit-lamp examination of the right eye highlighting severe conjunctival hyperemia, infiltrated cornea, 6–7 mm central corneal abscess, and hypopyon.
Antibiotics 11 00905 g002
Figure 3. Radiobacter colonies on Columbia blood agar.
Figure 3. Radiobacter colonies on Columbia blood agar.
Antibiotics 11 00905 g003
Figure 4. Automated identification results of Rhizobium radiobacter on the VITEK2 compact system.
Figure 4. Automated identification results of Rhizobium radiobacter on the VITEK2 compact system.
Antibiotics 11 00905 g004
Figure 5. Microscopy of Radiobacter culture. Gram stain, magnification 1000×.
Figure 5. Microscopy of Radiobacter culture. Gram stain, magnification 1000×.
Antibiotics 11 00905 g005
Figure 6. PRISMA flow diagram of the selection process of studies included in this systematic review.
Figure 6. PRISMA flow diagram of the selection process of studies included in this systematic review.
Antibiotics 11 00905 g006
Table 1. Etiology of endophthalmitis by type.
Table 1. Etiology of endophthalmitis by type.
Endophthalmitis TypeEtiologyRecommended Intravitreal TreatmentRecommended Systemic Antibiotics
After cataract surgeryStaphylococcus epidermidis, Staphylococcus warneri,
Staphylococcus capitis, Staphylococcus haemolyticus, Staphylococcus aureus, Propionibacterium acnes, Streptococcus pneumoniae, Streptococcus agalactiae, Streptococcus intermedius, Abiotrophia defectiva, Bacillus cereus, Pseudomonas aeruginosa, Pseudomonas stutzeri, Klebsiella pneumoniae, Haemophilus influenzae, Acinetobacter baumannii, Agrobacterium tumefaciens,
Citrobacter freundii, Rhizobium radiobacter,
Escherichia coli, Enterococcus faecalis,
Stenotrophomonas maltophilia, Mycobacterium chelonae, Propionibacterium acnes (in chronic cases), fungi (Candida albicans, Candida parapsilosis, Acremonium strictum, Aspergillus fumigatus, Paecilomyces variotti, Fusarium proliferatum) [5,6,7,8,9,10,11,12]
Vancomycin, ceftazidimeRarely used
(in severe cases)
After intravitreal injectionsStaphylococcus aureus, Streptococcus viridans, Streptococcus mitis, Streptococcus viridans, Enterococcus faecalis [3,13]Vancomycin, ceftazidimeQuinolones
(moxifloxacin)
After eye traumatismStaphylococcus aureus, S. epidermidis, S. capitis, Staphylococcus warneri, S. pasteuri, S. auricularis, S. piscifermentans, S. lugdunensis, Streptococcus mutans, S. salivarium, S. mutans, S. oralis, S. sanguinis, S. vestibularis, S. termophilus, Enterococcus faecalis, Rhizobium radiobacter, Bacillus cereus, Escherichia coli,
Candida parapsilosis, Candida albicans, Candida glabrata, Candida famata, Aspergillus flavus, Acremonium curvulum, Fusarium solani, Fusarium proliferatum) [10,14,15]
Vancomycin, ceftazidime, amphotericin (if suspicion of fungal infection)Vancomycin, ceftazidime, ciprofloxacin
After Baerveldt tube exposure (in glaucoma treatment)Haemophilus influenzae, Streptococcus pneumoniae, Streptococcus agalactia, Streptococcus mitis, Corynebacterium spp., Pseudomonas aeruginosa, Aspergillus flavus, Aspergillus fumigatus [16]Aancomycin, ceftazidimeRarely used
After long-term wear of contact lensesPseudomonas aeruginosa, Serratia marcescens, Staphylococcus epidermidis, Staphylococcus aureus, Streptococcus mitis, Streptococcus salivarium, Streptococcus mutans, Streptococcus pneumoniae, Klebsiella oxytoca, Enterobacter cloacae, Propionibacterium acnes [17]Aminoglycosides, fluoroquinolones, 3rd-generation cephalosporins,
vancomycin
Rarely used
Endogenous endophthalmitisStaphylococcus aureus, Staphylococcus epidermidis, Staphylococcus lugdunensis, Streptococcus viridans, Streptococcus pyogenes, Streptococcus agalactiae, Streptococcus pneumoniae, Enterococcus faecalis, Escherichia coli, Klebsiella pneumoniae, Serratia marcescens, Kingella kingae, Pseudomonas aeruginosa, (Candida albicans, Candida parapsilosis, Candida glabrata, Aspergillus flavus, Aspergillus fumigatus) [18,19,20]Vancomycin, ceftazidime (or amikacin)Antibiotics according to etiology
Table 2. The studies included in this review.
Table 2. The studies included in this review.
AuthorsJournalTitleArticle TypeNo. of Samples/PatientsMean Age (Years)Pre-Existent Eye ConditionsEye TraumaAntibiotic Susceptibility ResultsDrug TherapyOutcome
Rohowetz et al. (2020) [33]Case Reports in OphthalmologyEndophthalmitis Caused by Agrobacterium radiobacter Following Intravitreal Aflibercept for Diabetic RetinopathyCase report179Diabetic retinopathyIntravitreal aflibercept-Intravitreal vancomycin and azithromycin;
oral gentamicin and levofloxacin
Infection resolved
Rohowetz et al. (2021) [34]Case Reports in OphthalmologyAgrobacterium radiobacter Endophthalmitis Associated with Baerveldt Tube ExposureCase report185Angle-closure glaucomaBaerveldt tube insertionResistance to cefazolin, ceftazidime, amikacin, tobramycin, and trimethoprim–sulfamethoxazoleInjection of intravitreal vancomycin
(1 mg) and ceftazidime (2.25 mg).
Drops of 0.5% moxifloxacin every 2 h.
Injection of 0.2 mg of intravitreal gentamicin
Visual acuity improvement after 2 weeks and then lost to follow-up
Barker et al. (2016) [35]CorneaRhizobium radiobacter: A Recently Recognized Cause of Bacterial KeratitisCase series426None identifiedCement-splash injurySusceptibility to ciprofloxacin and minocyclineMoxifloxacin drops.
Oral ketoconazole.
Ciprofloxacin drops hourly and oral ciprofloxacin (250 mg) twice daily
Infection resolved
26Contact lens wearer-Ciprofloxacin, ceftazidime,
levofloxacin, minocycline.
Resistant to trimethoprim–sulfamethoxazole
Drops with vancomycin and tobramycin.
Vancomycin dropped and ciprofloxacin added
Infection resolved
19Contact lens wearerCorneal ulcerSusceptibility to
gentamicin, ciprofloxacin, levofloxacin, ceftazidime, and polymyxin
Ofloxacin, tobramycin and cefazolin.
Cyclopentolate 3 times daily.
Prednisolone 1%
Infection resolved with a residual scar
19Contact lens wearer-Susceptibility to gentamicin,
ceftazidime, amikacin, and polymyxin
Oral acyclovir 400 mg and gatifloxacin twice
daily.
Scopolamine 3 times daily
Lost to follow-up
Fenner et al. (2019) [36]American Journal of Ophthalmology Case ReportsCase of Isolated Rhizobium radiobacter Contact-Lens-Related Infectious Keratitis: A Plant Microbe Now Emerging as a Human PathogenCase report126Contact lens wearer-Susceptibility to cefepime, ciprofloxacin, and gentamicin
Hourly cefazolin (50 mg/mL) and gentamicin (14 mg/mL).
Hourly 0.02% chlorhexidine.
Hourly 1.5% levofloxacin, hourly cefazolin, and two-hourly chlorhexidine to both eyes
during waking hours, and 0.3% ciprofloxacin ointment overnight.
Levofloxacin 1.5% monotherapy for
both eyes at four weeks
Favorable evolution with central anterior-to-mid-stromal scar
Al-Abdullah et al. (2015) [37]
(no full text available)
Journal of Refractive SurgeryEndophthalmitis Caused by Rhizobium radiobacter After Posterior Chamber Phakic Intraocular Lens Implantation to Correct MyopiaCase report129MyopiaPosterior chamber phakic intraocular lens implantation-Intravitreal injections of vancomycin and ceftazidimeInfection resolved
Mishra et al. (2019) [4]The British Journal of OphthalmologyUtility of Broad-Range 16S rRNA PCR Assay Versus Conventional Methods for Laboratory Diagnosis of Bacterial Endophthalmitis in a Tertiary Care HospitalResearch article8 out of 195 vitreous aspirates from endophthalmitis patients--Cataract surgerySusceptible to all tested antibiotics (according to document M45 of CLSI 2010 [38])--
Shirodokar et al. (2012) [6]American Journal of OphthalmologyDelayed- Versus Acute-Onset Endophthalmitis after Cataract SurgeryResearch article1 out of 119 patients with endophthalmitis--Cataract surgery---
Hsu et al. (2013) [5]American Journal of OphthalmologyOcular Flora and their Antibiotic Resistance Patterns in the Midwest: A Prospective Study of Patients Undergoing Cataract SurgeryResearch article1 out of 183 conjunctival cultures--Cataract surgerySusceptible to cefazolin, ceftazidime, gentamycin, tobramycin, amikacin, ciprofloxacin, and levofloxacin--
Harbiyeli et al. (2021) [39]International OphthalmologyClinical Aspects and Prognosis of Polymicrobial Keratitis Caused by Different Microbial Combinations: A Retrospective Comparative Case StudyResearch article1 out of 44 corneal scrapings-Polymicrobial keratitis-Susceptible to ciprofloxacin and moxifloxacin--
Haapala et al. (2005) [7]Graefe’s Archive for Clinical and Experimental OphthalmologyEndophthalmitis Following Cataract Surgery in Southwest Finland from 1987 to 2000Research article1 out of 47 patients--Postoperative
endophthalmitis after cataract surgery
---
Tellegen et al. (2009) [40]Journal of Clinical PathologyDiagnosis of Conjunctivitis in Primary Care: Comparison of Two Different Culture ProceduresResearch article1 out of 88 patients-Infectious conjunctivitis----
Chiquet et al. (2016) [10]The British Journal of OphthalmologyOccurrence and Risk Factors for Retinal Detachment after Pars Plana Vitrectomy in Acute Post-Cataract Bacterial EndophthalmitisResearch article1 out of 123 vitreous aspirates--Post-cataract bacterial endophthalmitis treated with pars plana vitrectomy---
Ambiya et al. (2016) [8]Journal of Ophthalmic Inflammation and InfectionComparison of Clinico-Microbiological Profile and Treatment Outcome of In-House and Referred Post-Cataract-Surgery Endophthalmitis in a Tertiary Care Center in South IndiaResearch article1 out of 100 patients Cataract surgerySusceptible to amikacin, ceftazidime,
gatifloxacin, moxifloxacin, ciprofloxacin,
and ofloxacin.
Resistant to chloramphenicol
Intraocular antibiotics
(1 mg of vancomycin in 0.1 mL of normal saline;
2.25 mg of ceftazidime in 0.1 mL of normal saline).
Intravitreal dexamethasone
(0.4 mg in 0.1 mL).
Topical 1% prednisolone acetate
(every 4 h).
Cycloplegia.
Systemic ciprofloxacin (1500 mg/day in two divided doses)
-
Ness et al. (2011) [9]The Journal of Hospital InfectionPostoperative Nosocomial Endophthalmitis: Is Perioperative Antibiotic Prophylaxis Advisable? A Single Centre’s ExperienceResearch article1 out of 16 patients with endophthalmitis--Cataract surgerySusceptibility to gentamicin, ciprofloxacin, and ofloxacin--
Chiquet et al. (2009) [41]OphthalmologyAnalysis of Diluted Vitreous Samples from Vitrectomy is Useful in Eyes with Severe Acute Postoperative EndophthalmitisResearch article1 out of 34 patients with endophthalmitis-Diabetes mellitus
immunosuppression
Cataract surgery---
Friling (2019) [11]The Journal of Hospital InfectionsBacteriology and Cefuroxime Resistance in Endophthalmitis Following Cataract Surgery before and after the Introduction of Prophylactic Intracameral Cefuroxime: A Retrospective Single-Centre StudyResearch article3 out of 95 patients with endophthalmitis--Cataract surgery-Intravitreal injection of
1 mg of cefuroxime;
2.27 mg of ceftazidime
and 1 mg of vancomycin.
Oral
dose of prednisone (60 mg for five days)
-
Namdari et al. (2003) [42]Journal of Clinical MicrobiologyRhizobium (Agrobacterium) radiobacter Identified as a Cause of Chronic Endophthalmitis Subsequent to Cataract ExtractionCase report162Uncomplicated cataract extraction-Susceptibility to ciprofloxacin, resistance to
ceftazidime and vancomycin
Intravitreal injection of amikacin (0.4 mg) and vancomycin (1 mg).
Intravitreal administration of gentamicin (0.4 mg).
Oral ciprofloxacin (500 mg twice daily for 10 days)
Infection resolved
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Balasoiu, A.T.; Zlatian, O.M.; Ghenea, A.E.; Davidescu, L.; Lungu, A.; Golli, A.L.; Udriștoiu, A.-L.; Balasoiu, M. A Rare Case of Endophthalmitis with Rhizobium radiobacter, Soon after a Resolved Keratitis: Case Report. Antibiotics 2022, 11, 905. https://doi.org/10.3390/antibiotics11070905

AMA Style

Balasoiu AT, Zlatian OM, Ghenea AE, Davidescu L, Lungu A, Golli AL, Udriștoiu A-L, Balasoiu M. A Rare Case of Endophthalmitis with Rhizobium radiobacter, Soon after a Resolved Keratitis: Case Report. Antibiotics. 2022; 11(7):905. https://doi.org/10.3390/antibiotics11070905

Chicago/Turabian Style

Balasoiu, Andrei Theodor, Ovidiu Mircea Zlatian, Alice Elena Ghenea, Livia Davidescu, Alina Lungu, Andreea Loredana Golli, Anca-Loredana Udriștoiu, and Maria Balasoiu. 2022. "A Rare Case of Endophthalmitis with Rhizobium radiobacter, Soon after a Resolved Keratitis: Case Report" Antibiotics 11, no. 7: 905. https://doi.org/10.3390/antibiotics11070905

APA Style

Balasoiu, A. T., Zlatian, O. M., Ghenea, A. E., Davidescu, L., Lungu, A., Golli, A. L., Udriștoiu, A. -L., & Balasoiu, M. (2022). A Rare Case of Endophthalmitis with Rhizobium radiobacter, Soon after a Resolved Keratitis: Case Report. Antibiotics, 11(7), 905. https://doi.org/10.3390/antibiotics11070905

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop