Polymicrobial endophthalmitis: prevalence, causative organisms, and visual outcomes

  • Animesh Jindal1,

    Affiliated with

    • Mayur R Moreker2,

      Affiliated with

      • Avinash Pathengay1Email author,

        Affiliated with

        • Manav Khera1,

          Affiliated with

          • Subhadra Jalali2,

            Affiliated with

            • Ajit Majji2,

              Affiliated with

              • Annie Mathai2,

                Affiliated with

                • Savitri Sharma3,

                  Affiliated with

                  • Taraprasad Das3 and

                    Affiliated with

                    • Harry W FlynnJr4

                      Affiliated with

                      Journal of Ophthalmic Inflammation and Infection20133:6

                      DOI: 10.1186/1869-5760-3-6

                      Received: 18 October 2012

                      Accepted: 18 October 2012

                      Published: 7 January 2013

                      Abstract

                      Background

                      The purpose of the present study is to evaluate the prevalence, causative organisms, and visual acuity outcome in patients with culture-proven polymicrobial endophthalmitis. The method used in this study is the non-comparative, consecutive case series using a retrospective analysis of patients diagnosed with polymicrobial endophthalmitis for the period 2000 to 2010.

                      Results

                      Polymicrobial endophthalmitis was identified in 43/1,107 (3.88%) patients. Forty-two patients had two isolates, and one patient had grown three isolates, yielding a total of 87 isolates. Gram-positive cocci were the most common isolate (n = 53; 60.9%) including Staphylococcus epidermidis (n = 14/53; 16.1%) and Streptococcus pneumoniae (n = 13/53; 13.8%). The etiologies included posttraumatic (n = 31/43; 72.1%) and postoperative (n = 9/43; 20.9%) endophthalmitis. Antibiotic susceptibilities among Gram-positive bacteria were vancomycin (100%) and chloramphenicol (96%). Susceptibilities among Gram-negative bacteria were ciprofloxacin (86.4%) and ofloxacin (81.2%). A maximum number of secondary interventions were done in traumatic cases (38.7%) and cases having coinfection with Gram-negative bacteria and fungus (66.7%). Visual acuity (VA) < 20/200 was more frequently observed in posttraumatic cases (n = 27/31; 87.1%) as compared with postoperative cases (n = 4/9; 44.4%). Of the 43 patients, only 9 patients (20.9%) achieved a VA ≥ 20/200 on final follow-up. Four out of twelve patients (33.3%), with fungus as one of the isolates, had a VA ≥ 20/200.

                      Conclusions

                      Although polymicrobial infection in endophthalmitis is uncommon, it is generally associated with poor visual acuity outcomes especially in eyes with open-globe injuries. Coinfection with Gram-negative bacteria or fungi was associated with most unfavorable visual outcome.

                      Keywords

                      Polymicrobial Endophthalmitis Antibiotic susceptibilities

                      Background

                      Endophthalmitis is one of the most vision-threatening ocular complications following intraocular surgeries and open-globe injuries. The incidence of polymicrobial infection in the report of the Endophthalmitis Vitrectomy Study (EVS) Group was 9.3% [1]. The incidence of polymicrobial endophthalmitis after open-globe injuries has been reported from 5.3% to 47.6% [26], while it has been reported to be 0.0% to 17% in various postoperative endophthalmitis series [612]. There are limited published series reporting the etiology and outcome of polymicrobial endophthalmitis [12]. No large series are available in the literature on etiology and visual acuity (VA) outcomes of polymicrobial endophthalmitis cases.

                      The purpose of the present study is to evaluate the prevalence, causative organisms, and visual acuity outcomes in patients with culture-proven polymicrobial endophthalmitis in a teaching hospital.

                      Results and discussion

                      Results

                      Polymicrobial endophthalmitis was seen in 43 (3.88%) out of 1,107 culture-proven endophthalmitis patients. There were 31 male patients as compared to 12 female patients with polymicrobial infection. Forty-two patients had grown two isolates and one patient had grown three isolates, yielding a total of 87 isolates (Table 1).
                      Table 1

                      Clinical profile of patients with polymicrobial endophthalmitis

                      SR number

                      Age/gender

                      Setting

                      Visual acuity (presenting)

                      Primary intervention

                      Secondary intervention (Y/N)

                      Visual acuity (final)

                      Organisms

                      1

                      7 years/F

                      Trauma

                      PR inacc

                      PPV + IOAB

                      N

                      No PL

                      Staphylococcus epidermidis, Streptococcus pneumoniae

                      2

                      5 years/M

                      Trauma

                      PR inacc

                      STR + PPV + IOAB

                      N

                      CF 2 m

                      Alpha hemolytic Streptococcus, Haemophilus influenzae

                      3

                      60 years/M

                      Cataract surgery

                      20/200

                      Vit Bx + IOAB

                      N

                      20/400

                      Bacillus, Corynebacterium

                      4

                      6 years/F

                      Trauma

                      PR inacc

                      STR + PPV + IOAB

                      N

                      No PL

                      Alpha hemolytic Streptococcus, Acromonas

                      5

                      8 years/F

                      Trauma

                      PR inacc

                      STR + PPV + IOAB

                      N

                      No PL

                      Bacillus, S. pneumoniae

                      6

                      35 years/F

                      Trauma

                      PR inacc

                      IOFB removal + PPV + IOAB

                      N

                      CF 1/2 m

                      Aspergillus sp., Bacillus

                      7

                      45 years/M

                      Trauma

                      PR inacc

                      STR + PPV + IOAB

                      N

                      No PL

                      S. epidermidis, Bacillus

                      8

                      15 years/M

                      Trauma

                      PR acc

                      IOFB removal + PPV + IOAB

                      N

                      20/60

                      Alpha hemolytic Streptococcus, Clostridium

                      9

                      64 years/M

                      Penetrating keratoplasty

                      20/1200

                      Vit Bx + IOAB

                      N

                      20/160

                      S. epidermidis, S. pneumoniae

                      10

                      36 years/M

                      Trabeculectomy

                      PR inacc

                      PPV + IOAB

                      N

                      20/40

                      S. pneumoniae, Fusarium

                      11

                      73 years/M

                      Cataract surgery

                      PR acc

                      PPV + IOAB

                      N

                      PR inacc

                      S. epidermidis, Aspergillus

                      12

                      8 years/M

                      Trauma

                      PR inacc

                      IOFB removal + PPV + IOAB

                      N

                      No PL

                      S. epidermidis, Alpha hemolytic Streptococcus

                      13

                      39 years/F

                      Trauma

                      PR inacc

                      STR + PPV + IOAB

                      N

                      PR inacc

                      Chrysomonads, Fusarium

                      14

                      23 years/M

                      Trauma

                      PR acc

                      PPV + IOAB

                      N

                      20/400

                      S. epidermidis, Aspergillus

                      15

                      4 years/M

                      Trauma

                      PR inacc

                      STR + PPV + IOAB

                      N

                      PR acc

                      S. epidermidis, Aspergillus

                      16

                      16 years/M

                      Trauma

                      PR inacc

                      IOFB removal + PPV + IOAB

                      N

                      PR inacc

                      S. epidermidis, S. pneumoniae

                      17

                      71 years/M

                      Trabeculectomy

                      PR acc

                      STR + PPV + IOAB

                      N

                      20/50

                      Moraxella, S. epidermidis

                      18

                      45 years/M

                      Cataract surgery

                      20/25

                      Vit Bx + IOAB

                      N

                      20/25

                      S. epidermidis, Aspergillus

                      19

                      18 years/M

                      Trauma

                      PR acc

                      PPV + IOAB

                      N

                      20/1200

                      S. epidermidis, Aspergillus

                      20

                      38 years/M

                      Trauma

                      PR acc

                      PPV + IOAB

                      N

                      20/40

                      S. epidermidis, Clostridium

                      21

                      60 years/M

                      Cataract surgery

                      PR acc

                      PPV + IOAB

                      N

                      PR inacc

                      Corynebacterium, Aspergillus

                      22

                      38 years/M

                      Trauma

                      PR acc

                      STR + PPV + IOAB

                      Y

                      PR acc

                      Bacillus, Alpha hemolytic Streptococcus

                      23

                      14 years/M

                      Endogenous

                      Pr acc

                      PPL + PPV + IOAB

                      N

                      No PL

                      S. pneumoniae, S. aureus

                      24

                      4 years/F

                      Trauma

                      PR acc

                      PPV + IOAB

                      N

                      No PL

                      S. pneumoniae, H. influenzae

                      25

                      50 years/M

                      Trauma

                      PR inacc

                      ECCE + PPV + IOAB

                      Y

                      No PL

                      S. pneumoniae, Pseudomonas

                      26

                      57 years/M

                      Penetrating keratoplasty

                      PR acc

                      PPV + IOAB

                      N

                      CF-1/2m

                      S. pneumoniae, H. influenzae

                      27

                      7 years/F

                      Trauma

                      PR acc

                      STR + PPV + IOAB

                      Y

                      No PL

                      S. pneumoniae, E. coli

                      28

                      7 years/F

                      Trauma

                      PR acc

                      PPL + PPV + IOAB

                      N

                      No PL

                      S. pneumoniae, Neisseria

                      29

                      3 years/M

                      Trauma

                      PR acc

                      PPV + IOAB

                      N

                      No PL

                      S. pneumoniae, Pseudomonas

                      30

                      8 years/M

                      Trauma

                      PR acc

                      PPL + PPV + IOAB

                      Y

                      No PL

                      S. pneumoniae, H. influenzae

                      31

                      11 years/M

                      Trauma

                      PR inaac

                      CTR + PPL + PPV + IOAB

                      N

                      No PL

                      Bacillus, Enterococcus, Pantoea

                      32

                      6 years/M

                      Trauma

                      PR acc

                      STR + PPL + PPV + IOAB + IOFB Removal

                      Y

                      PL

                      Enterococcus, Stenotrophomonas

                      33

                      3 years/F

                      Trauma

                      No PL

                      STR + PPL + PPV + IOAB

                      N

                      No PL

                      Paenibacillus thiaminolyticus, Enterobacter

                      34

                      1 month/M

                      Endogenous

                      PL

                      Vit Bx + IOAB

                      N

                      No PL

                      S. pneumoniae, Pseudomonas

                      35

                      4 years/M

                      Trauma

                      PR acc

                      CTR + PPL + PPV + IOAB

                      Y

                      HM+

                      Streptococci, Fusarium

                      36

                      57 years/F

                      Cataract surgery

                      20/40

                      Vit Bx + IOAB

                      Y

                      20/20

                      Pseudomonas, Aspergillus

                      37

                      3 years/M

                      Trauma

                      PL+

                      CTR + PPL + PPV + IOAB

                      Y

                      CF-2m

                      S. epidermidis, Corynebacterium

                      38

                      14 years/M

                      Trauma

                      PR inacc

                      PPL + PPV + IOAB

                      Y

                      20/200

                      Streptococcus mitis, Fusarium

                      39

                      5 years/M

                      Trauma

                      PR acc

                      PPV + IOAB

                      Y

                      PL

                      Streptococci, Pseudomonas

                      40

                      31 years/M

                      Endogenous

                      PR acc

                      PPV + IOAB

                      Y

                      HM+

                      S. epidermidis, E. coli

                      41

                      18 years/F

                      Trauma

                      PL

                      PPL + PPV + IOAB + Ampho B

                      Y

                      20/25

                      Pseudomonas, S pneumonia

                      42

                      19 years/M

                      Trauma

                      HM+

                      CTR + PPL + PPV + IOAB + Ampho B

                      Y

                      PL

                      Streptococci, Pseudomonas

                      43

                      34 years/F

                      Trauma

                      PL

                      PPV + IOAB

                      Y

                      PL

                      Corynebacterium, Aspergillus

                      PR acc, projection of rays accurate; PR inacc, projection of rays inaccurate; HM+, hand motion close to face present; PL, perception of light; PPL, pars plana lensectomy; PPV, pars plana vitrectomy; Vit Bx, vitreous biopsy; IOAB, intraocular antibiotics; IOFB, intraocular foreign body; CTR, corneal tear repair; STR, scleral tear repair; Ampho B, intravitreal amphotericin B.

                      Clinical presentation

                      Overall, the presenting visual acuity was light perception in 38 patients and was greater than or equal to hand motion in 5 patients. Thirty-eight patients underwent core vitrectomy, and five patients underwent vitreous biopsy as the first intervention. In all the patients, the organisms were isolated and identified from the first vitreous sample, collected during the first procedure (vitreous biopsy/vitrectomy). Gram-positive organisms were the most common isolates (n = 53; 60.9%), followed by Gram-negative organisms (n = 22; 25.3%) and fungi (n = 12; 13.8%). Staphylococcus epidermidis (n = 14; 16.1%) and Streptococcus pneumoniae (n = 13; 14.9%) were the most common organisms. The endophthalmitis categories were open-globe injury (31/43; 72.1%), postoperative endophthalmitis (9/43; 20.9%), and endogenous endophthalmitis (3/43; 6.9%) (Table 2).
                      Table 2

                      Comparison of secondary interventions and visual outcome among different etiologies of polymicrobial endophthalmitis

                       

                      Trauma

                      Postoperative

                      Endogenous

                      Number of patients

                      31

                      9

                      3

                      Undergoing secondary intervention

                      12 (38.7%)

                      1 (11.1%)

                      1 (33.3%)

                      Unfavorable visual outcome (VA < 20/200)

                      27 (87.1%)

                      4 (44.4%)

                      3 (100%)

                      Antibiotic susceptibilities

                      Gram-positive bacteria were most sensitive to vancomycin (100%) and chloramphenicol (96%). Gram-negative bacteria were most sensitive to ciprofloxacin (86.4%) and ofloxacin (81.2%) (Table 3).
                      Table 3

                      Antibiotic susceptibility of isolates in polymicrobial endophthalmitis

                      Antibiotic

                      Sensitivity of gram-positive bacteria (%)

                      Sensitivity of gram-negative bacteria (%)

                      Amikacin

                      57.1

                      61.9

                      Cefazolin

                      81.1

                      33.3

                      Ceftazidime

                      61.1

                      63.1

                      Ciprofloxacin

                      82.7

                      86.4

                      Chloramphenicol

                      96

                      72.7

                      Gentamycin

                      74

                      63.6

                      Gatifloxacin

                      82.6

                      80

                      Ofloxacin

                      67.7

                      81.2

                      Vancomycin

                      100

                      45.4

                      Moxifloxacin

                      88.2

                      70

                      Secondary intervention

                      Twelve out of 31 patients (38.7%) having endophthalmitis following open-globe injury had secondary intervention as compared to postoperative (1/9; 11.1%) and endogenous (1/3; 33.3%) endophthalmitis. The number of patients requiring additional procedures was maximum for combination of Gram-negative and fungus (66.7%) followed by Gram-positive and Gram-negative combination (42.1%) (Tables 2 and 4).
                      Table 4

                      Comparison of secondary interventions and visual outcome among different microbes in polymicrobial endophthalmitis

                       

                      Gram-positive and gram-negative combination

                      Gram-positive and gram-negative combination

                      Gram-positive and fungus combination

                      Gram negative and fungus combination

                      No. of patients

                      12

                      19

                      9

                      3

                      Undergoing secondary intervention

                      2 (16.7%)

                      8 (42.1%)

                      2 (22.2%)

                      2 (66.7%)

                      Unfavorable visual outcome (VA < 20/200)

                      9 (75%)

                      17 (89.5%)

                      6 (66.7%)

                      2 (66.7%)

                      Visual outcomes

                      An unfavorable visual outcome (VA < 20/200) resulted in 27 out of 31 patients (87.1%) having posttraumatic endophthalmitis and four out of nine (44.4%) patients having postoperative endophthalmitis. Combination of Gram-positive and Gram-negative organisms had the worst visual prognosis with only 10.5% patients having final VA ≥ 20/200. Out of the 43 patients, only 9 (20.9%) patients had a best corrected VA ≥ 20/200 at final follow-up. Eight out of 12 patients (66.67%) having fungi as one of the infecting organisms had a VA < 20/200 at final follow-up visit.

                      Discussion

                      Polymicrobial eye infections present a challenge not only in identifying two or more microorganisms, but also in instituting appropriate antimicrobial therapy. In the current study and in large series, polymicrobial infections seem to occur more frequently in open-globe injuries, underscoring the non-sterile conditions under which ocular trauma occurs. Polymicrobial infections have been reported following advanced keratitis, infected scleral buckles, and dacryocystitis [1315]. In a retrospective study from North India, Gupta et al. reported polymicrobial endophthalmitis in 8 eyes out of 47 culture-positive postoperative endophthalmitis eyes (17%) [11]. Pijl et al. from Netherlands found polymicrobial infection in 4 out of 166 culture-positive cases (2.4%) of postoperative endophthalmitis [12]. Anand et al., in a series of 170 culture-proven postoperative endophthalmitis, reported 3 cases (1.8%) of polymicrobial endophthalmitis [16]. Vedantham et al., reported 3 (7.7%) polymicrobial endophthalmitis cases in a series of 39 posttraumatic patients [17]. In the author's previous published report for the period 1991 to 1997, polymicrobial infections were identified in 12.5% (14 of 112) culture-positive postoperative cases, while it was present in 20.4% (23 of 113) culture-positive posttraumatic cases, with three trimicrobial cases [2, 9]. In the current series from 2000 to 2010, less prevalence of polymicrobial infection (3.88%) was observed compared with the earlier report. The cause for this decrease in prevalence of polymicrobial infection is uncertain.

                      Gram-positive bacteria (S. epidermidis and S. pneumoniae) are the most common isolates from polymicrobial endophthalmitis in the current series, contrasting with the previous series where Gram-negative bacteria and fungus were most common isolates.

                      Considering the very short half-life of fluoroquinolones but good penetration in vitreous cavity, this class of antibiotics can be considered for per-oral therapy, and vancomycin can be considered for intravitreal injections. Repeat intravitreal antibiotics if needed should be based on culture sensitivity report.

                      Patients with posttraumatic endophthalmitis had poorer visual outcomes when compared with postoperative endophthalmitis, which is consistent with our previous series and previous reported literature [2, 79]. Five out of nine postoperative patients (55.5%) having polymicrobial infection had favorable visual outcome as compared with only 4 patients out of 31 (12.9%) having posttraumatic endophthalmitis. The number of patients undergoing additional procedure was also more for posttraumatic cause (38.7%) as compared with postoperative cause (11.1%). We had three patients with endogenous source of infection who had polymicrobial infection, and all three had unfavorable visual outcome.

                      Although prevalence of fungus in our series has decreased, given the unsterile conditions under which traumatic endophthalmitis occurs and high probability of fungal contamination, intravitreal antifungal agents should be considered along with antibiotics, but decision should be individualized based on history and clinical examination. Limitations of the current study include the retrospective nature and lack of a definitive prospective treatment protocol.

                      Conclusions

                      Polymicrobial infections in endophthalmitis are uncommon and are often associated with trauma. Coinfection with Gram-negative bacteria or fungi may be associated with the most unfavorable visual acuity outcomes.

                      Methods

                      Approval was obtained from the local Institutional Review Board. All the patients who were diagnosed with endophthalmitis during the period 2000 to 2010 were analyzed. From the endophthalmitis database, information was obtained regarding the cause of endophthalmitis, microbiological work up including the vitreous isolates and their antibiotic susceptibilities, and the clinical outcomes. All patients with more than one isolate during microbiological workup were enrolled in the study.

                      The EVS recommendations were generally followed in postoperative endophthalmitis eyes. In endophthalmitis following open-globe injuries, three-port pars plana vitrectomy was performed in all eyes along with additional procedure if required (suturing scleral laceration, IOFB removal, endolaser, or silicone oil injection). Undiluted vitreous samples were sent immediately for microbiology evaluation. All eyes received intravitreal vancomycin (1.0 mg in 0.1 ml) and either amikacin (0.4 mg in 0.1 ml) or ceftazidime (2.25 mg in 0.1 ml) and additional intravitreal dexamethasone (0.4 mg in 0.1 ml) in postoperative cases. Intravitreal amphotericin B (5 μg in 0.1 ml) was administered on clinical suspicion based on surgeon’s treatment preference. Additional procedures were recorded when intravitreal antimicrobials or pars plana vitrectomy/vitreous lavage were repeated. Treatment and management decisions on secondary interventions were made by the individual treating physician without a predefined study protocol. Bacterial isolates were identified using Analytical Profile Index (API, bioMeriux, Marcy-l'Etoile, France). The antibiotic sensitivity was checked by Kirby Bauer disc diffusion method. Isolation of two or more different organisms from vitreous was considered to be a polymicrobial infection. The best-corrected visual acuity of less than 20/200 at final follow-up was defined as unfavorable visual outcome.

                      Declarations

                      Authors’ Affiliations

                      (1)
                      LV Prasad Eye Institute
                      (2)
                      LV Prasad Eye Institute
                      (3)
                      Bhubaneswar Eye Institute, LV Prasad Eye Institute
                      (4)
                      Department of Ophthalmology, Bascom Palmer Eye Institute, Miller School of Medicine, University of Miami

                      References

                      1. Han PD, Wisniewski SR, Wilson LA, Barza M, Vine AK, Doft BH, Kelsey SF: Spectrum and susceptibilities of microbiologic isolates in the Endophthalmitis Vitrectomy Study. Am J Ophthalmol 1996, 122: 1–17.PubMedView Article
                      2. Kunimoto DY, Das T, Sharma S, Jalali S, Majji AB, Gopinathan U, Athmanathan S, Rao TN: Microbiologic spectrum and susceptibility of isolates: part II. Posttraumatic endophthalmitis. Endophthalmitis Research Group. Am J Ophthalmol 1999, 128: 242–244. 10.1016/S0002-9394(99)00113-0PubMedView Article
                      3. Affeldt JC, Flynn HW, Forster RK, Mandelbaum S, Clarkson JG, Jarus GD: Microbial endophthalmitis resulting from ocular trauma. Ophthalmology 1987, 94: 407–413.PubMedView Article
                      4. Brinton GS, Topping TM, Hyndiuk RA, Aaberg TM, Reeser FH, Abrams GW: Post-traumatic endophthalmitis. Arch Ophthalmol 1984, 102: 547–550. 10.1001/archopht.1984.01040030425016PubMedView Article
                      5. Alfaro DV, Roth D, Liggett PE: Post-traumatic endophthalmitis: causative organisms, treatment, and prevention. Retina 1994, 14: 206–211. 10.1097/00006982-199414030-00004PubMedView Article
                      6. Boldt HC, Pulido JS, Blodi CF, Folk JC, Weingeist TA: Rural endophthalmitis. Ophthalmology 1989, 96: 1722–1726.PubMedView Article
                      7. Das T, Kunimoto DY, Sharma S, Jalali S, Majji AB, Rao TN, Gopinathan U, Athmanathan S, Endophthalmitis Research Group: Relationship between clinical presentation and visual outcome in postoperative and posttraumatic endophthalmitis in South Central India. Indian J Ophthalmol 2005, 53: 5–16. 10.4103/0301-4738.15298PubMedView Article
                      8. Nobe JR, Gomez DS, Liggett P, Smith RE, Robin JB: Post-traumatic and postoperative endophthalmitis: a comparison of visual outcomes. Br J Ophthalmol 1987, 71: 614–617. 10.1136/bjo.71.8.614PubMed CentralPubMedView Article
                      9. Kunimoto DY, Das T, Sharma S, Jalali S, Majji AB, Gopinathan U, Athmanathan S, Rao TN: Microbiologic spectrum and susceptibility of isolates: part I. Postoperative endophthalmitis. Endophthalmitis Research Group. Am J Ophthalmol 1999,128(2):240–242. 10.1016/S0002-9394(99)00112-9PubMedView Article
                      10. Endophthalmitis Vitrectomy Study Group: Results of the Endophthalmitis Vitrectomy Study: a randomized trial of immediate vitrectomy and intravenous antibiotics for treatment of postoperative bacterial endophthalmitis. Arch Ophthalmol 1995, 113: 1479–1496.View Article
                      11. Gupta A, Gupta V, Gupta A, Dogra MR, Pandav SS, Ray P, Chakraborty A: Spectrum and clinical profile of post cataract surgery endophthalmitis in North India. Indian J Ophthalmol 2003, 51: 139–145.PubMed
                      12. Pijl BJ, Theelen T, Tilanus MA, Rentenaar R, Crama N: Acute endophthalmitis after cataract surgery: 250 consecutive cases treated at a tertiary referral center in the Netherlands. Am J Ophthalmol 2010, 149: 482–487. 10.1016/j.ajo.2009.09.021PubMedView Article
                      13. Wong T, Ormonde S, Gamble G, McGhee CNJ: Severe infective keratitis leading to hospital admission in New Zealand. Br J Ophthalmol 2003, 87: 1103–1108. 10.1136/bjo.87.9.1103PubMed CentralPubMedView Article
                      14. Pathengay A, Karosekar S, Raju B, Sharma S, Das T, Hyderabad Endophthalmitis Research Group: Microbiologic spectrum and susceptibility of isolates in scleral buckle infection in India. Am J Ophthalmol 2004, 138: 663–664. 10.1016/j.ajo.2004.04.056PubMedView Article
                      15. Brook I, Frazier EH: Aerobic and anaerobic microbiology of dacryocystitis. Am J Ophthalmol 1998, 125: 552–554. 10.1016/S0002-9394(99)80198-6PubMedView Article
                      16. Anand AR, Therese KL, Madhavan HN: Spectrum of aetiological agents of postoperative endophthalmitis and antibiotic susceptibility of bacterial isolates. Indian J Ophthalmol 2000, 48: 123–128.PubMed
                      17. Vedantham V, Nirmalan PK, Ramasamy K, Prakash K, Namperumalsamy P: Clinico-microbiological profile and visual outcomes of post-traumatic endophthalmitis at a tertiary eye care center in South India. Indian J Ophthalmol 2006, 54: 5–10. 10.4103/0301-4738.21607PubMedView Article

                      Copyright

                      © Jindal et al.; licensee Springer. 2013

                      This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://​creativecommons.​org/​licenses/​by/​2.​0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.