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  Table of Contents    
ORIGINAL ARTICLE  
Year : 2017  |  Volume : 60  |  Issue : 2  |  Page : 214-220
Clinicomicrobiological profile of endophthalmitis: A 10 year experience in a Tertiary Care Center in North India


1 Department of Ocular Microbiology, Dr. Rajendra Prasad Centre for Ophthalmic Sciences, All India Institute of Medical Sciences, New Delhi, India
2 Department of Community Ophthalmology, Dr. Rajendra Prasad Centre for Ophthalmic Sciences, All India Institute of Medical Sciences, New Delhi, India
3 Department of Retina Services, Dr. Rajendra Prasad Centre for Ophthalmic Sciences, All India Institute of Medical Sciences, New Delhi, India
4 Department of Biostatistics, All India Institute of Medical Sciences, New Delhi, India

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Date of Web Publication19-Jun-2017
 

   Abstract 

Purpose: To determine the clinicomicrobiological profile of infectious agents and their antibiotic susceptibility in different type of endophthalmitis. Methods: A retrospective review of clinical and microbiological records from January 2001 to December 2010, was performed in 1110 patients diagnosed with different type of endophthalmitis (postoperative, posttraumatic, endogenous and post keratitis) to record the demographic details, clinical presentations; microbiological agents isolated with their antimicrobial sensitivity pattern. Antimicrobial susceptibility testing for various culture positive isolates (bacterial/fungal) was performed by the disc diffusion technique. Results: Out of the 1110 intra-ocular specimens processed, 384 (34.6%) were positive for bacteria. S epidermidis was the most predominant isolate accounting for 42.7% of all bacteria obtained, followed by Pseudomonas aeruginosa (24.5%). Besides Pseudomonas, Acinetobacter spp. were the next common gram negative bacilli detected (8.3%) followed by Klebsiella, E. coli, Enterobacter and Alkaligenes in 2.6%, 0.8%, 0.8% and 0.5% cases respectively. The predominant fungal species were Aspergillus spp., in 36.1%, followed by Fusarium spp. in 26.4% cases. Overall susceptibility pattern in our study showed that gram positive bacteria were most susceptible to glycopeptides like vancomycin (80-100%) and fluoroquinolones (87-91%). The sensitivity pattern of gram negative organisms like Pseudomonas and Klebsiella towards fluoroquinolones ranged between 61% - 82%. Conclusion: S epidermidis was the most common bacteria isolated in postoperative and posttraumatic endophthalmitis, Pseudomonas aeruginosa was the most common bacterial isolated in posttraumatic endophthalmitisAmongst fungi Aspergillus was the most common organism.

Keywords: Antibiotic susceptibility, bacteria, endophthalmitis, fungus, latent period

How to cite this article:
Satpathy G, Nayak N, Wadhwani M, Venkwatesh P, Kumar A, Sharma Y, Sreenivas V. Clinicomicrobiological profile of endophthalmitis: A 10 year experience in a Tertiary Care Center in North India. Indian J Pathol Microbiol 2017;60:214-20

How to cite this URL:
Satpathy G, Nayak N, Wadhwani M, Venkwatesh P, Kumar A, Sharma Y, Sreenivas V. Clinicomicrobiological profile of endophthalmitis: A 10 year experience in a Tertiary Care Center in North India. Indian J Pathol Microbiol [serial online] 2017 [cited 2019 Aug 20];60:214-20. Available from: http://www.ijpmonline.org/text.asp?2017/60/2/214/208413



   Introduction Top


Endophthalmitis is a severe vision threatening intra-ocular infection.[1] Infectious endophthalmitis may occur as exogenous (postoperative, posttraumatic) or endogenous. In the recent past, there are number of studies published on epidemiology, antibiotic susceptibility, type of organisms and clinicomicrobiological profile of patients with different type of endophthalmitis from various parts of the world and in India.[2],[3],[4],[5],[6] However, only a single series presented a complete and composite data on either exogenous (posttraumatic, postoperative) or endogenous endophthalmitis (EE).[1]

Thus, herein, we present a large single center retrospective study in all types of endophthalmitis with the objective to determine the spectrum of etiologic agents, to correlate the clinical presentation with the agents isolated and to depict the antibiogram profile of the bacterial agents.


   Patients and Methods Top


A retrospective analysis based on the ophthalmic records of patients suffering from endophthalmitis, at a tertiary center in Dr. Rajendra Prasad Center for Ophthalmic Sciences, All India Institute of Medical Sciences, New Delhi, India and microbiological data of the same patients from the Department of Ocular Microbiology were carried out.

Data with respect to a total of 1110 patients, clinically diagnosed as endophthalmitis during a 10 year period from January 2001 to December 2010, were analyzed for the demographic details, clinical presentations; microbiological agents isolated with their antimicrobial sensitivity pattern. In addition to the above details, interval between duration of trauma or surgery and the onset of symptoms was also reported from the history in these records.

Our records revealed that majority of PTE cases were farmers/field workers by occupation and belonged to the rural community.

During the time of admission, all the patients underwent detailed ophthalmic examination including visual acuity (VA), refraction, detailed slit lamp examination for the evaluation of anterior chamber and posterior segment evaluation using indirect ophthalmoscopy. Ultrasound B scan was performed in eyes with media opacity (corneal edema, anterior chamber exudates) made anterior and posterior segment examination difficult. The diagnosis of endophthalmitis was made and vitreous biopsy was undertaken. Laboratory diagnosis has been attempted in all the cases by collecting vitreous aspirate/biopsy by the standard protocol.[2] To collect an idea vitreous sample, vitreous aspiration was done at the pars plana 3 mm away from the limbus with a sterile tuberculin syringe and a 26-gauge needle. Undiluted vitreous sample 0.2–0.5 ml was collected from all the cases before intraocular injection using a syringe attached to vitrectomy cannula and sample was sent immediately to laboratory for microbiological analysis.

Patients with VA <6/60 but projection of rays PR accurate, with sufficient corneal clarity underwent pars plana vitrectomy. Vitreous biopsy was collected from the mid vitreous cavity by applying aspiration with a 2 cc disposable syringe plugged into the suction tubing of the vitreous cutter. For better recovery of microorganisms, it was useful to obtain an undiluted sample before starting the infusion fluid. The collected vitreous specimen was sent to the laboratory in the same syringe used for collection with the sterile cork struck into the needle.[2],[3]

The specimens were subjected to direct microscopic examination, that is, Gram-staining, Giemsa, calcofluor white, 10% KOH wet mount, bacterial culture and sensitivity and fungal culture by employing the recommended techniques.[2],[3],[4] Briefly, the specimens, immediately after collection, were inoculated onto blood agar, chocolate agar, MacConkey agar plates, and Sabouraud's dextrose agar (SDA) tubes. SDA tubes were incubated at 25°C and the remaining media at 37°C. Any bacterial growth was identified using API System (bioMerieux, France) and fungal identification was based on colony characteristics and microscopic features. All patients with positive smear/culture were subjected to standard three port pars plana vitrectomy. To consider any culture as positive following criteria was used (i) a culture was considered positive when there was growth of the same organism on ≥2 media, and/or (ii) confluent growth at the site of inoculation on one solid medium, and/or (iii) growth in one medium with consistent direct microscopy findings. Antimicrobial susceptibility testing for various culture positive isolates (bacterial/fungal) was performed by the disc diffusion technique.[3]

After collection of vitreous sample all the patients received intravitreal vancomycin 1 mg/ml and ceftazidime 2.25 mg/ml as per the treatment guidelines of endophthalmitis by the institute. Postvitrectomy all the patients were treated with systemic and topical antibiotics. Patients with fungal infection were given intravitreal amphotericin B (5 μg/0.1 ml). The data were recorded to determine the relationship between etiology, presenting signs and symptoms (latent period, corneal infiltrate, corneal abscess, posterior vitreous detachment (PVD), retinal detachment (RD), retained intraocular foreign body (RIOFB), VA at presentation and discharge). The details of microorganisms isolated and their respective antibiogram profiles were recorded.

Statistical analysis was carried out using Pearson Chi-square test and sample t-test and a P< 0.05 was considered statistically significant.


   Results Top


A total of 1110 cases were investigated of which 243 (22%) were diagnosed as postoperative endophthalmitis (POE), 810 (73%) were diagnosed as posttraumatic endophthalmitis (PTE), 43 (3.9%) as EE and 14 (1.3%) following keratitis. Clinical parameters and demographic data were traced to all 1110 subject's records. The mean age of onset was 44.5, 28.4, and 38.6 years for POE, PTE, EE, respectively with male:female ratio being 154:90, 577:233, 26:17, and 10:4, respectively for POE, PTE, EE and those following keratitis [Table 1]. The severity of presenting symptoms (corneal infiltrate, corneal abscess, PVD, RD, RIOFB) were the most severe in posttraumatic cases, none of the patients were diagnosed cases of immune-compromising states such as HIV disease, blood dyscrasias, uncontrolled diabetes; neither was any patient on prolonged corticosteroids or immunosuppressive drugs. No significant improvement was observed in the VA even after conservative management or vitrectomy [Table 1].
Table 1: Clinical features and visual outcome of 1110 cases of endophthalmitis

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Out of the 1110 intra-ocular specimens processed, 384 (34.6%) were positive for bacteria. The spectrum of bacterial agents isolated has been depicted in [Table 2]. Staphylococcus epidermidis was the most predominant isolate accounting for 42.7% (164 out of 384) of all bacteria obtained, followed by Pseudomonas aeruginosa (24.5%, i.e., 94 of 384). These two organisms were responsible for majority of the posttraumatic cases (64.6% and 76.6% of cases, respectively). Besides Pseudomonas, Acinetobacter spp. were the next common Gram-negative bacilli detected accounting for 32 (8.3%) of the total 384 bacterial organisms followed by Klebsiella, Escherichia coli, Enterobacter and Alcaligenes in 2.6%, 0.8%, 0.8%, and 0.5% cases, respectively, whereas Staphylococcus aureus was the other most commonly isolated Gram-positive bacterium (22 of 384, i.e., 5.7%), Streptococcus pneumoniae and viridans streptococci were detected in 2.3% and 3.9% cases, respectively. Overall culture positivity for bacteria was seen in 29.1% (112 of 384) of POE cases, 65.1% (250 of 384) of PTE cases and in 3.9% (15 of 384) of cases with EE. In postkeratitis cases, however, there were a total of 7 isolates from 14 cases, all 7 cases yielding mixed growth. Latent period, that is, the time from event to diagnosis did not vary much in accordance with the etiological agents isolated, excepting in case of Acinetobacter, where it ranged between 2 and 8 weeks [Table 2].
Table 2: Spectrum of bacterial agents

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Spectrum of fungal agents isolated from different categories of patients along with latent period of presentation has been depicted in [Table 3]. The predominant fungal species were Aspergillus spp., in 36.1%, followed by Fusarium spp. in 26.4% of cases. These two fungi were also commonly found in posttrauma and EE whereas Aspergillus flavus was the most common isolate (58.3%) in EE, Aspergillus fumigatus, was commonly encountered (77%) in posttrauma cases. Fusarium was most commonly seen in PTE (52.6%) and EE (42.1%). The latent periods observed in patients with Aspergillus and Fusarium infections ranged between 7 days to 2 months. However, a 2 month latent period was noticed only in one case each, meaning thereby that all the cases due to Aspergillus and Fusarium species had a very short latent period.
Table 3: Spectrum of fungal agents isolated

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Fungal infections, however, do not show such a trend and percentage of fungi detected from all culture proven cases ranges from as low as 1.3% to as high as 22%. Among the fungi, Aspergillus still remains the most common etiologic agent prevailing over the last three decades, whereas bacterial endophthalmitis due to S. aureus has declined, and there is an increase in the incidence of those caused by S. epidermidis. Among the Gram-negative bacteria, Pseudomonas spp. were reported to be the most common, especially in postoperative cases.

Antibiogram profile depicted that cloxacillin, which was found to be the most effective drug in the past against Gram-positive bacteria, can no longer be relied on because of its low sensitivity profile (28.5%–62.0%) toward these organisms [Table 4]. At the same time it is noteworthy that Gram-positive cocci such as staphylococci were most susceptible to vancomycin, cephazolin, gatifloxacin and moxifloxacin, with gatifloxacin and moxifloxacin showing more promising results than ciprofloxacin. Sensitivity patterns of Gram-negative bacteria, although were quite encouraging against polymyxin B and quinolones such as ciprofloxacin, gatifloxacin, and moxifloxacin majority of these were poorly susceptible to other classes of antimicrobials including cephalosporins (cephazolin) and aminoglycosides (tobramycin and amikacin).
Table 4: Antimicrobial susceptibility pattern of the microorganisms isolated

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Overall susceptibility pattern in our study showed that Gram-positive bacteria were the most susceptible to glycopeptides such as vancomycin (80%–100%) and fluoroquinolones such as ciprofloxacin, gatifloxacin, and moxifloxacin (87%–91%, 88%–97%, and 88%–98%, respectively). The sensitivity pattern of Gram-negative organisms such as Pseudomonas and Klebsiella toward fluoroquinolones ranged between 61% and 82%; the pattern toward ciprofloxacin in particular was less encouraging among the Pseudomonas isolates.


   Discussion Top


The present study represents a large series exploring the detailed microbiological profile and antimicrobial susceptibility patterns, in addition to the clinical spectrum of the patients in all categories of endophthalmitis, based on a retrospectively collected data. On review of literature no other study has done such large series.[5],[6],[7],[8],[9] Our study represents the first of its type which has compared all the parameters noted above, and that too, in all clinical forms of endophthalmitis of both bacterial and fungal origin. There has been numerous studies done on posttraumatic, postoperative in a multivariable analysis in various studies in various parts of country like South and central India.[1],[2],[7],[8]

The main objective of this study was to determine any association between clinical presentation and microorganisms isolated. It was observed that of the total of 1110 cases analyzed, the VA was poor and the presenting symptoms were severe in posttraumatic cases. Similar observations in view of presenting signs and symptoms and visual outcome were noted by Das et al.[5] The VA did not show much variation even after intensive management, which is similar in agreement with the observations of others.[1],[5] The reason for involvement of more males in all type of endophthalmitis is more exposure to outdoor activities and therefore increased chances to trauma in them as compared to females.

Overall antibiotic susceptibility pattern in our study showed that Gram-positive bacteria were most susceptible to glycopeptides such as vancomycin (80%–100%) and fluoroquinolones such as ciprofloxacin, gatifloxacin and moxifloxacin (87%–91%, 88%–97%, and 88%–98%, respectively). In this study, the sensitivity pattern of Gram-negative organisms like Pseudomonas and Klebsiella toward fluoroquinolones ranged between 61% and 82%, similar observations were noted by Kunimoto et al.[6] in their study done on POE, they found 100% sensitivity to fluoroquinolones (cioprofloxacin) for Pseudomonas. This sensitivity pattern towards ciprofloxacin in particular, which is often recommended in ophthalmic practice in the empiric therapy for Pseudomonas infections based upon smear findings and clinical judgment, makes its usage more cautious and reflects such rampant use of this drug in clinical practice.

From our data it appears that vancomycin remains effective against Gram-positive bacteria in vitro and should remain the intra-vitreal drug of choice for antimicrobial therapy against these organisms. By contrast, cephazolin and tobramycin as the first-line drugs, as adviced by many centers, should be reconsidered based on the present data. The same was true for cephazolin so far as the Gram-negative bacteria were concerned. The data of sensitivity pattern of cephazolin against all Gram-negative organisms revealed that substantial positive conclusion regarding their efficacy in the context of the present study cannot be drawn. Similar results were reported in a series of POE and PTE cases in the recent past in which 4%–28% and 11%–66%, respectively of Gram-negative organisms were shown to be sensitive to cephazolin.[6],[7],[10]

From the above forementioned comparative analysis, it appeared that there was a drastic change in the antibiogram profile of the organisms over the years. For example, cloxacillin that remained the useful therapeutic option for most Gram-positive bacteria in the late 1980s and 1990s no longer seems promising.[10],[11] Rather majority of the staphylococci (98%–100%) were sensitive to vancomycin and newer quinolones such as gatifloxacin and moxifloxacin (>71%). This observation is similar to the study by others.[11],[12]

S. epidermidis, Pseudomonas and Acinetobacter were the most common bacterial agents obtained in our series. Similar findings were noted by the previous investigators from our center in the past as well as by others from across the country.[6],[7],[8],[9],[10],[11],[12],[13] This clearly indicates that the bacteriological profile, although has not changed much, the sensitivity patterns of bacteria toward various antibiotics or antibiotic combinations has undergone a switch, thus reflecting their much un-advocated empiric use.

Aspergillus spp. were the most common isolates (36.1%) in our series as were reported earlier from our center as well as from other parts of India.[14],[15],[16] As is evident from [Table 5], incidence of Aspergillus endophthalmitis was documented in 1.3%–22% of cases from various centers. Notwithstanding the above, ours was the only major study involving all clinical categories of endophthalmitis of both bacterial and fungal origin, whereas all others included only postoperative cases or posttraumatic cases or both. Many even reported fungal endophthalmitis series alone.[5],[14],[15],[16] This may be the sole reason for the inconsistency in the proportion of fungal endophthalmitis reported by various hospitals [Table 5]. It also exhibits the comparative analysis of data of the present study with those reported in the past from our center as well from others. It seems that there is a decline in the proportion of bacterial infections in the present decade as opposed to those in the 1980s or 1990s. Nevertheless, the latent periods in most of our cases due to Aspergillus spp. as well as due to Fusarium spp were 7 days, excepting in one occasion each, in which it was as long as 2 months. This suggests the inherent virulence of these fungi and therefore, in early onset fungal endophthalmitis, organisms such as Aspergillus and Fusarium should be sought for in the differential diagnosis. Similar short latent periods in Aspergillus and Candida endophthalmitis were reported by others.[14],[15]
Table 5: Endophthalmitis data from various centers in India

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Although Aspergillus endophthalmitis occurs most frequently from exogenous sources, our finding of this organism in 58% (7 out of 18) cases of endogenous warrants attention. However, reports of Aspergillus endophthalmitis were documented in the past in patients with immuncompromised state, history of intravenous drug use and in those who had undergone intra-ocular surgery or had received presumably contaminated dextrose infusions.[15],[16] Although in our series A. fumigatus was more commonly detected in POE and PTE patients, a finding similar to those documented earlier [13],[14] a very high rate of isolation of A. flavus was observed in endogenous cases. As stated above, Aspergillus endophthalmitis is commonly encountered as an exogenous infection. However, it may occasionally result from hemotogenous seeding.[14],[15],[16] Similar findings have been highlighted earlier.[17]Fusarium was the next common agent detected in our series. Fusarium, a known etiologic agent of keratitis, was detected in endophthalmitis in the immunucompromised host.[17] In our series, however, we could not trace the immune status of majority of our patients in the records.

In postoperative cases, we encountered Aspergillus spp. in 15%–17% of our cases. In a report from India, the authors found Aspergillus as the most common agent in POE accounting for 11.2% of their cases.[13] As reported previously,[16] postoperative fungal endophthalmitis is usually seen in clusters due to the use of contaminated intra-ocular irrigating solution. Furthermore, most cases of fungal endophthalmitis in clusters had occurred within 4 weeks [14],[15] a finding similar to ours. Thus we believe that possible sources of contamination in our patients were in the operating theater which could have possibly happened due to less stringent practices. Poor qualities of control measures in rural eye camp settings are often blamed for such contamination during surgery and postoperative care. Since most of our patients with postcataract endophthalmitis were operated in a hospital setting, there is a definite need for major improvement in surgical practices, not only in eye camps but also in hospitals in the developing countries.


   Conclusion Top


Thus, our study highlights the importance of various types of endophthalmitis with their etiological agents, microbiological profile and changing antibiogram for further management.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

 
   References Top

1.
Sharma S, Padhi TR, Basu S, Kar S, Roy A, Das T. Endophthalmitis patients seen in a tertiary eye care centre in Odisha: A clinico-microbiological analysis. Indian J Med Res 2014;139:91-8.  Back to cited text no. 1
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2.
Sharma S, Jalali S, Adiraju MV, Gopinathan U, Das T. Sensitivity and predictability of vitreous cytology, biopsy, and membrane filter culture in endophthalmitis. Retina 1996;16:525-9.  Back to cited text no. 2
    
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Bauer AW, Kirby WM, Sherris JC, Turck M. Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol 1966;45:493-6.  Back to cited text no. 3
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Das T, Kunimoto DY, Sharma S, Jalali S, Majji AB, Nagaraja Rao T, et al. Relationship between clinical presentation and visual outcome in postoperative and posttraumatic endophthalmitis in South central India. Indian J Ophthalmol 2005;53:5-16.  Back to cited text no. 4
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Das T, Dogra MR, Gopal L, Jalali S, Kumar A, Malpani A, et al. Postsurgical endophthalmitis: Diagnosis and management. Indian J Ophthalmol 1995;43:103-16.  Back to cited text no. 5
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Kunimoto DY, Das T, Sharma S, Jalali S, Majji AB, Gopinathan U, et al. Microbiologic spectrum and susceptibility of isolates: Part I. Postoperative endophthalmitis. Endophthalmitis Research Group. Am J Ophthalmol 1999;128:240-2.  Back to cited text no. 6
    
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Kunimoto DY, Das T, Sharma S, Jalali S, Majji AB, Gopinathan U, et al. Microbiologic spectrum and susceptibility of isolates: Part II. Posttraumatic endophthalmitis. Endophthalmitis Research Group. Am J Ophthalmol 1999;128:242-4.  Back to cited text no. 7
    
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Thompson JT, Parver LM, Enger CL, Mieler WF, Liggett PE. Infectious endophthalmitis after penetrating injuries with retained intraocular foreign bodies. National Eye Trauma System. Ophthalmology 1993;100:1468-74.  Back to cited text no. 8
    
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Gupta A, Gupta V, Gupta A, Dogra MR, Pandav SS, Ray P, et al. Spectrum and clinical profile of post cataract surgery endophthalmitis in North India. Indian J Ophthalmol 2003;51:139-45.  Back to cited text no. 9
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Mahajan VM. Postoperative ocular infections: An analysis of laboratory data on 750 cases. Ann Ophthalmol 1984;16:847-8.  Back to cited text no. 10
    
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Satpathy G, Vishalakshi P. Microbiology of infectious endophthalmitis: A 3 year study. Ann Ophthalmol 1997;29:50-3.  Back to cited text no. 11
    
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Anand AR, Therese KL, Madhavan HN. Spectrum of aetiological agents of postoperative endophthalmitis and antibiotic susceptibility of bacterial isolates. Indian J Ophthalmol 2000;48:123-8.  Back to cited text no. 12
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Chakrabarti A, Shivaprakash MR, Singh R, Tarai B, George VK, Fomda BA, et al. Fungal endophthalmitis: Fourteen years' experience from a center in India. Retina 2008;28:1400-7.  Back to cited text no. 13
    
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Narang S, Gupta A, Gupta V, Dogra MR, Ram J, Pandav SS, et al. Fungal endophthalmitis following cataract surgery: Clinical presentation, microbiological spectrum, and outcome. Am J Ophthalmol 2001;132:609-17.  Back to cited text no. 14
    
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Wykoff CC, Flynn HW Jr., Miller D, Scott IU, Alfonso EC. Exogenous fungal endophthalmitis: Microbiology and clinical outcomes. Ophthalmology 2008;115:1501-7, 1507.e1-2.  Back to cited text no. 15
    
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Gupta A, Gupta V, Dogra MR, Chakrabarti A, Ray P, Ram J, et al. Fungal endophthalmitis after a single intravenous administration of presumably contaminated dextrose infusion fluid. Retina 2000;20:262-8.  Back to cited text no. 16
    
17.
Robertson MJ, Socinski MA, Soiffer RJ, Finberg RW, Wilson C, Anderson KC, et al. Successful treatment of disseminated Fusarium infection after autologous bone marrow transplantation for acute myeloid leukemia. Am J Ophthalmol 1994;177:363-8.  Back to cited text no. 17
    

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Correspondence Address:
Meenakshi Wadhwani
Room No. 784, Department of Community Ophthalmology, Dr. Rajendra Prasad Centre for Ophthalmic Sciences, All India Institute of Medical Sciences, New Delhi - 110 029
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/IJPM.IJPM_794_15

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