Bacterial Spectrum and Antimicrobial Susceptibility Pattern of Peripheral and Central Bacterial Keratitis in South Korea for Ten Years

doi:10.21203/rs.3.rs-4695589/v1

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Bacterial Spectrum and Antimicrobial Susceptibility Pattern of Peripheral and Central Bacterial Keratitis in South Korea for Ten Years

https://doi.org/10.21203/rs.3.rs-4695589/v1

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Purpose: To evaluate the bacterial spectrum and antimicrobial susceptibility pattern of bacterial keratitis in South Korea for ten years.

Methods: 143 eyes of 143 patients who have been diagnosed with bacterial keratitis from January 2010 to April 2019 were retrospectively enrolled. Corneal scraping was done for Gram stain in all patients, and cultures were plated on blood, chocolate, Sabouraud dextrose agar, and thioglycolate broth. Empirical fourth generation fluoroquinolone or fortified vancomycin and ceftazidime were treated for every patient.

Results: Ocular trauma (n=29, 24.0%) and contact lens (n=18, 14.9%) were the most common causes in patients with bacterial keratitis. Most of the bacterial keratitis was gram-positive (n=85, 70%) and the gram-negative is only 6% (7 eyes). Most of central and peripheral keratitis were Gram positive (n=57, 65% and n=29, 85%). There was no gram-negative stain in peripheral keratitis. Vancomycin and ciprofloxacin were the most susceptible (n=68, 56.2% and n=51, 42.1%) and least resistant (n=0, 0% and n=18, 14.9%) in the antibiotic susceptibility test. Treatment time (month) and best corrected visual acuity after treatment in the gatifloxacin group were better than those in the moxifloxacin group (P<0.05).

Conclusion: The most common cause of bacterial keratitis was ocular trauma and contact lenses. There was a different bacterial spectrum in central and peripheral keratitis. Gatifloxacin was more effective for early corneal healing and recovery of visual acuity than moxifloxacin.

bacterial keratitis

bacterial spectrum

antimicrobial susceptibility

central keratitis

peripheral keratitis

The most common cause of microbial keratitis is bacterial keratitis.[1, 2] Bacterial keratitis is one of the most common causes of vision impairment in working-age individuals.[3] Gram-positive bacteria are most commonly associated with infections after ocular surgery or disease, and less commonly associated with keratitis after ocular trauma or contact lens wear, where environmental organisms predominate, particularly Pseudomonas aeruginosa in contact lens-related disease.[4] The most common gram-positive pathogen recovered is coagulase-negative staphylococcus, with either Staphylococcus aureus or Streptococcus pneumoniae as the most common single isolate and Pseudomonas aeruginosa, the most common gram-negative pathogen.[4] Less common organisms reported in Asia include non-tuberculous mycobacteria and Microsporidia spp.[5] In the initial treatment of bacterial keratitis, the usage of commercially available fourth-generation fluoroquinolones versus compounded fortified antibiotics such as vancomycin and tobramycin has been debated.[6, 7] According to the AAO 2018 study on bacterial keratitis, fluoroquinolone monotherapy is at least as effective as combination therapy with fortified drops.[8] On the other hand, fluoroquinolone resistance was very common among bacteria from ocular infections in central India, although there has been a recent decline in resistance to several fluoroquinolones.[9] But, for all gram-positive bacteria examined, the minimum inhibitory concentrations (MICs) for fourth-generation fluoroquinolones were significantly lower than those for second-generation fluoroquinolones.[10] When the two fourth-generation fluoroquinolones were compared, moxifloxacin had lower MICs for most gram-positive bacteria and gatifloxacin had lower MICs for most gram-negative bacteria.[10, 11] And gatifloxacin 0.3% or moxifloxacin 0.5% were safe enough not to result in severe epithelial damage in healthy human corneas.[12] There were a lot of reports about the pathogens and antibiotic susceptibilities of bacterial keratitis.[13–17]

However, there was no report about the comparison of the bacterial spectrum and antimicrobial susceptibility pattern in the peripheral and central keratitis.

Thus, the objective of this study was to evaluate the bacterial spectrum and antimicrobial susceptibility pattern of peripheral and central bacterial keratitis in South Korea for ten years. And we also evaluated the efficacy of empirical treatment with gatifloxacin and moxifloxacin in bacterial keratitis.

We performed a retrospective chart review and data analysis in this study.. This study was carried out in accordance with Institutional Review Board standards and the Helsinki Declaration. This study protocol was approved by Bucheon St. Mary Hospital's Institutional Review Board (IRB)/Ethics Committee.

Patients’ examination

143 eyes of 143 patients who have been diagnosed with bacterial keratitis from January 2010 to April 2019 were enrolled. Corneal scraping using Kimura spatulas was performed for Gram stain in all patients, and cultures were performed on blood, chocolate, Sabouraud dextrose agar, and thioglycolate broth. Empirical fourth-generation fluoroquinolone or fortified vancomycin and ceftazidime were treated for every patient.

The patients were divided into two groups: group 1 (central keratitis, 87 eyes) and group 2 (peripheral keratitis, 34 eyes). And the patients were divided into four groups according to initial treatment; group 1 (gatifloxacin 0.3%, 70 eyes), group 2 (moxifloxacin 0.5%, 40 eyes), group 3 (ciprofloxacin 1.5%, 2 eyes), and group 4 (fortified vancomycin 2.5% and ceftazidime 5%, 8 eyes).

The clinical data were collected from each medical record: age, gender, previous history of ocular morbidity, contact lens use, and history of ocular surgery or trauma.

Their clinical data were recorded after a complete ophthalmological examination. Causative organisms, antibiotic susceptibility test, mean treatment time (month), and best corrected visual acuity (BCVA) were examined before and after treatment.

An automated Vitek 2 system (bioMe'rieux, Inc., Marcy l'Etoile, France) was used for antimicrobial identification and susceptibility testing. Isolates were classified as sensitive, intermediate, or resistant to the antibiotics examined. Vancomycin, cefazolin, cefuroxime, chloramphenicol, oxacillin, penicillin, ciprofloxacin, levofloxacin, moxifloxacin, carbapenem (meropenem and imipenem), tobramycin, ceftazidime, amikacin, and gentamicin were among the antibiotics studied. The isolated bacteria were classified into four types for analysis: gram-positive cocci, gram-positive bacilli, gram-negative cocci, and gram-negative bacilli.

Statistical Analysis

All statistical analyses were performed using a commercial program (SPSS for Windows, version 21.0.1; SPSS Inc., Chicago, IL). The Wilcoxon signed rank test was used to compare the data before and after treatment. Comparisons among all groups were performed with one-way analysis of variance (ANOVA) with Bonferroni post hoc comparison. If the variances were not homogeneous, the Tamhane test was used for the post hoc comparison between pairs of groups. The chi-square test was used for the comparison among groups of different proportions. P values < 0.05 were considered statistically significant. P values < 0.05 were considered statistically significant.

Table 1 represents the characteristics of patients in each group. BCVA after treatment (0.23 ± 0.12 logMAR) was better than BCVA before treatment (0.36 ± 0.15) in patients with bacterial keratitis (p < 0.05).

Table 1

Data of patients
Parameter
Number of patients	30
F:M	48:73
Age, years (range)	51.9 ± 22.1
BCVA before treatment (logMAR)	0.36 ± 0.15
BCVA after treatment (logMAR)	*0.23 ± 0.12
BCVA after treatment was better than BCVA before treatment in patients with bacterial keratitis (p < 0.05).
BCVA: best corrected visual acuity
logMAR : Logarithm of the Minimum Angle of Resolution
Values are presented as mean ± SD. *: P < 0.05

Causes of bacterial keratitis

Ocular trauma (n = 29, 24.0%) and contact lenses (n = 18, 14.9%) were the most common causes in patients with bacterial keratitis. The other known causes of bacterial keratitis were ocular disease (uveitis, recurrent corneal erosion, and entropion), ocular surgery (cataract and keratoplasty), exposure keratopathy, and herpes keratitis (Table 2).

Table 2

Causes of bacterial keratitis.
Diagnosis	Eyes
Trauma	29
Contact lenses	18
Ocular disease (uveitis, RCE, entropion)	8
Ocular surgery (Cataract, KP)	8
Exposure keratopathy	5
Herpes keratitis	4
Unknown	49
Total	121
Ocular trauma and contact lenses were the most common causes in patients with bacterial keratitis.
RCE: recurrent corneal erosion
KP: keratoplasty

Gram Stain

Most of the bacterial keratitis was gram-positive (n = 85, 70%), and gram-negative was only 6% (7 eyes). 24% (29 eyes) were not detected with gram stain (Fig. 1A). Most of the results of culture were gram-positive cocci (GPC) (n = 63, 52%) and gram-negative bacilli (GNB) (n = 21, 17%). Gram-positive bacilli (GPB) (n = 6, 5%) and mixed infection with GPC and GNB (n = 5, 4%) were also detected. 22% (26 eye) was not detected with culture (Fig. 1B).

Bacterial keratitis consisted of central keratitis (87 eyes, 72.0%) and peripheral keratitis (34 eyes, 38.0%). Most of the central bacterial keratitis was Gram positive (n = 57, 65%) and the Gram negative is only 8% (7 eyes). 24% (27 eyes) was not detected with Gram stain (Fig. 2A). Most of the peripheral bacterial keratitis was Gram positive (n = 29, 85%) and the Gram negative is none. 15% (5 eyes) was not detected with Gram stain (Fig. 2B).

Causative organisms of bacterial keratitis

Staphylococcus epidermidis (n = 43, 35.5%) was the most common causative organism in patients with central and peripheral bacterial keratitis. Moraxella, Pseudomonas aeruginosa, Staphylococcus aureus, Propionibacterium acnes, Staphylococcus hominis, and mixed organisms were detected only in central keratitis. Enterobacter and Staphylococcus caprae were detected only in peripheral keratitis (Table 3).

Table 3

Causative organisms of bacterial keratitis.
Causative organism	Central	Peripheral	Total
Staphylococcus epidermidis	22	21	43
Serratia marcescens	2	2	4
Moraxella	4	0	4
Pseudomonas aeruginosa	3	0	3
Staphylococcus capitis	3	2	5
Staphylococcus aureus	3	0	3
Enterobacter	0	2	2
Staphylococcus caprae	0	2	2
Propionibacterium acnes	2	0	2
Staphylococcus hominis	2	0	2
Mixed organisms	5	0	5
Other organism	14	6	20
No growth	21	5	26
Total	87	34	121
Staphylococcus epidermidis was the most common causative organism in patients with central and peripheral bacterial keratitis.
RCE: recurrent corneal erosion
KP: keratoplasty

Antibiotics susceptibility of bacterial keratitis

Vancomycin was the most susceptible (n = 68, 56.2%) and least resistant (n = 0, 0%) antibiotic and ciprofloxacin was second most susceptible (n = 51, 42.1%) and second least resistant (n = 18, 14.9%) antibiotic in patients with bacterial keratitis. There were no results in every antibiotic susceptibility test from 46 (38.0%) to 57 (47.1%) patients (Table 4).

Table 4

Antibiotics susceptibility of bacterial keratitis.
	Inhibitory	Resistant	Susceptible	No result	Total
Ciprofloxacin	6	18	51	46	121
Erythromycin	3	31	33	54	121
Gentamycin	9	17	38	57	121
Penicilline	1	52	15	53	121
Tetracycline	0	22	46	53	121
Vancomycin	0	0	68	53	121
Vancomycin was the most susceptible and least resistant antibiotic and ciprofloxacin was second most susceptible and the second least resistant antibiotic in patients with bacterial keratitis.

Comparison of the effectiveness of antibiotics

Duration of treatment and BCVA after treatment (1.73 ± 0.74 months and 0.21 ± 0.10 logMAR) in the gatifloxacin group were significantly better than those (2.51 ± 0.95 and 0.30 ± 0.13) in the moxifloxacin group (P < 0.05). The percentage of duration of treatment less than 1 month in the gatifloxacin group (n = 30, 42.9%) was higher than that in the moxifloxacin group (n = 15, 37.5%). And the percentage of duration of treatment greater than 3 months in the gatifloxacin group (n = 13, 18.5%) was less than that in the moxifloxacin group (n = 9, 22.5%). The other groups were not incomparable with in the gatifloxacin and moxifloxacin groups because of the small number of cases. But the duration of treatment with vancomycin and ceftazidime ranged from 1 month to 3 months because of the initial severe condition of bacterial keratitis.

Bacterial keratitis is a serious ophthalmic emergency that is one of the leading causes of corneal blindness and visual loss.[18, 19] Early diagnosis and treatment of appropriate antimicrobial medication is very important to prevent its fatal complications.[20] Bacterial keratitis is far more common in developing nations, where access to hospital facilities is limited and hazardous jobs such as farming and agriculture are more common.[21]

Zhang Z et al. reported that the overall positive culture rate was 47% (95% confidence interval, 42–52%). In a meta-analysis of bacterial keratitis, gram-positive cocci were the most common (62%), followed by gram-negative bacilli (30%), gram-positive bacilli (5%), and gram-negative cocci (5%).[14] In our report, the overall positive gram stain rate was 76% and the positive culture rate was 78%. The culture rate of bacterial keratitis in our study was much higher than in other reports. Most of the bacterial keratitis was gram-positive (n = 85, 70%) and the gram-negative is only 6% (7 eyes) (Fig. 1A). Most of the results of culture were gram-positive cocci (GPC) (n = 63, 52%) and gram-negative bacilli (GNB) (n = 21, 17%). Gram positive bacilli (GPB) (n = 6, 5%) and mixed infection with GPC and GNB (n = 5, 4%) were also detected (Fig. 1B). The bacterial strains of the culture in our study were similar to those in earlier reports.

The bacteriological profile and causation of bacterial keratitis differ based on geographic region, referral patterns, and other factors.[22] But Staphylococcus epidermidis, Staphylococcus aureus, other coagulase-negative Staphylococcus species, Streptococcus pneumonia, and Pseudomonas aeruginosa were describeded to be the most prevalent organisms in bacterial keratitis.[22] But Palmer GS. Et al. reported that Pseudomonas was the most common bacterial cause of infected keratitis, followed by Staphylococcus and Bacillus.[15] In our study, Staphylococcus epidermidis (n = 43, 35.5%) was also the most common causative organism in patients with central and peripheral bacterial keratitis.

The characteristics of central keratitis were reported to be larger ulcerations (> 4 mm²) with inflammation and more often positive culture results.[23] In our study, bacterial keratitis consisted of central keratitis (87 eyes, 72.0%) and peripheral keratitis (34 eyes, 38.0%).

The central keratitis and peripheral keratitis had different gram stain pattern. Most of the central bacterial keratitis was gram-positive (n = 57, 65%) and the gram-negative was only 8% (7 eyes) (Fig. 2A). Most of the peripheral bacterial keratitis was Gram positive (n = 29, 85%) and the Gram negative was none (Fig. 2A).

The central keratitis and peripheral keratitis also had different pathogen patterns. Moraxella, Pseudomonas aeruginosa, Staphylococcus aureus, Propionibacterium acnes, Staphylococcus hominis, and mixed organisms were detected only in central keratitis. Enterobacter and Staphylococcus caprae were detected only in peripheral keratitis (Table 3).

Predisposing factors for bacterial keratitis were reported to be ocular surface disease (26/57 = 45.6%), contact lens wear (26/57 = 45.6%),[24] and previous trauma (5/57 = 8.8%).[23] On the other hand, the most common cause of bacterial keratitis was ocular trauma (n = 29, 24.0%), followed by contact lenses (n = 18, 14.9%), ocular disease (n = 8, 6.6%), and ocular surgery (n = 8, 6.6%) in our result. The unknown causes were the most common in our study (n = 49, 40.5%) (Table 2)

Austin A. et al. reported that the initial treatment of bacterial keratitis differs from clinicians in the USA being more likely to use fortified antibiotics versus fluoroquinolone monotherapy.[6] Fluoroquinolones prescribed as an empiric first-line treatment of bacterial keratitis are at least as effective as fortified antibiotics.[7] But, resistance to fluoroquinolones was common among bacterial keratitis.[9] And S. epidermidis strains isolated from three ocular pathologies were resistant to gatifloxacin and moxifloxacin due to mutations on the gyrA and parC genes.[1]

Therefore, we usually use fluoroquinolone as an empirical therapy in common bacterial keratitis, but fortified antibiotics such as vancomycin and ceftazidime were used in severe corneal infiltration[25] in the initial examination. Vancomycin was the most susceptible and least resistant antibiotic and ciprofloxacin was second most susceptible and the second least resistant antibiotic in patients with bacterial keratitis (Table 4). There was no treatment failure in both of the empirical therapies with fluoroquinolone or fortified antibiotics in our study (Table 5)

Table 5

Comparison of effectiveness of antibiotics
	Gatifloxacin	Moxifloxacin	Ciprofloxacin	Vancomycin ceftazidime
Eyes	70	40	2	8
Substitution to fortified antibiotics	1	4	2	0
Treatment time (Month)	*1.73 ± 0.74	2.51 ± 0.95	1.50 ± 0.85	2.00 ± 0.75
Treatment less than 1 Month (eyes, %)	30 (42.9%)	15 (37.5%)	1	0
Treatment more than 3 Months (eyes, %)	13 (18.6%)	9 (22.5%)	0	0
BCVA before treatment (logMAR)	0.35 ± 0.12	0.33 ± 0.14	0.32 ± 0.20	0.35 ± 0.16
BCVA after treatment (logMAR)	*0.21 ± 0.10	0.30 ± 0.13	0.30 ± 0.15	0.31 ± 0.17
Treatment Failure	0	0	0	0
BCVA: best corrected visual acuity
logMAR : Logarithm of the Minimum Angle of Resolution
Duration of treatment and BCVA after treatment in the gatifloxacin group were significantly better than those in the moxifloxacin group (P < 0.05). The percentage of duration of treatment less than 1 month in the gatifloxacin group was higher than that in the moxifloxacin group. And the percentage of duration of treatment greater than 3 months in the gatifloxacin group was less than that in the moxifloxacin group.
Values are presented as mean ± SD. *: P < 0.05

There was a decrease in resistance to some of the fluoroquinolones.[9] The fourth-generation fluoroquinolones (gatifloxacin and moxifloxacin) were found to be more effective against Staphylococcus aureus isolates resistant to ciprofloxacin, ofloxacin, and levofloxacin.[10] Moxifloxacin and gatifloxacin were the most effective against MRSA bacteria in both planktonic and biofilm forms.[11] And gatifloxacin 0.3% or moxifloxacin 0.5% was very safe and had no epithelial damage in normal human corneas after instillation.[12] Gatifloxacin had a different antibacterial susceptibility compared with moxifloxacin. Moxifloxacin had lower MICs for the majority of gram-positive bacteria, whereas gatifloxacin had lower MICs for the majority of gram-negative bacteria.[10] In our study, duration of treatment and BCVA after treatment (1.73 ± 0.74 months and 0.21 ± 0.10 logMAR) in the gatifloxacin group were significantly better than those (2.51 ± 0.95 and 0.30 ± 0.13) in the moxifloxacin group (P < 0.05). The percentage of duration of treatment less than 1 month in the gatifloxacin group (n = 30, 42.9%) was higher than that in the moxifloxacin group (n = 15, 37.5%). And the percentage of duration of treatment greater than 3 months in the gatifloxacin group (n = 13, 18.5%) was less than that in the moxifloxacin group (n = 9, 22.5%) (Table 5).

A limitation of our investigation was that a multicenter clinical trial with a bigger sample size and a longer follow-up period was required to observe the bacterial spectrum and antimicrobial susceptibility pattern of peripheral and central bacterial keratitis.

In conclusion, there was a different bacterial spectrum in central and peripheral keratitis. The most common cause of bacterial keratitis was ocular trauma (n = 29, 24.0%), followed by contact lens (n = 18, 14.9%). Both of fortified antibiotics and fluoroquinolone were effective for empirical therapy. Gatifloxacin was more effective for early corneal healing and recovery of visual acuity than moxifloxacin.

GPC: gram-positive cocci, GNB : gram-negative bacilli, GPB: gram-positive bacilli (GPB)

Acknowledgements

None.

Authors’ contributions

DJ was involved in analysis and interpretation of data and drafting the manuscript. DJ, SYH, HSK, ECK made contribution to acquisition of data and drafting. ECK contributed to conception and design, analysis and interpretation of data, drafting and revising the manuscript. All authors read and approved the final manuscript.

Funding

This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korea government(MSIT) (No. 2022R1F1A1069218) and grant of Patient-Centered Clinical Research Coordinating Center (PACEN) funded by the Ministry of Health and Welfare, Republic of Korea (No. HC23C0130).

Availability of data and materials

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Ethics approval and consent to participate

This study was approved by the institutional review board at Bucheon St. Mary’s Hospital (HC22RASI0099); the informed consent was waived. All clinical investigations have been conducted according to the principles expressed in the Declaration of Helsinki.

Consent for publication

Not applicable.

Competing interests

The authors do not have any conflicts of interest or proprietary interests in the contents of this manuscript.

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No competing interests reported.

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Bacterial Spectrum and Antimicrobial Susceptibility Pattern of Peripheral and Central Bacterial Keratitis in South Korea for Ten Years

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Abstract

Figures

Introduction

Methods

Patients’ examination

Statistical Analysis

Results

Causes of bacterial keratitis

Gram Stain

Causative organisms of bacterial keratitis

Antibiotics susceptibility of bacterial keratitis

Comparison of the effectiveness of antibiotics

Discussion

Abbreviations

Declarations

References

Additional Declarations

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