CLINICAL SCIENCE
Ocular Pathogens and Antibiotic Sensitivity in Bacterial
Keratitis Isolates at King Khaled Eye Specialist
Hospital, 2011 to 2014
Huda S. Al-Dhaheri, MD,* Mashael D. Al-Tamimi, MD,* Rajiv B. Khandekar, MS (Ophth), PG Dip (Epi),*
Mohammed Khan, PhD,* and Donald U. Stone, MD*
Background: To investigate prevalence and in vitro susceptibility
trends of bacteria isolated from patients with bacterial keratitis from
2011 to 2014 in a tertiary care eye hospital in Saudi Arabia.
Methods: Retrospective review of bacterial isolates from corneal
scraping of eyes with microbial keratitis. The most common isolates
and their antibiotic resistance proles were identied; trend analysis
was performed over the study period.
Results: A total of 2037 bacterial isolates met inclusion criteria
during the study period. Gram positives accounted for 91.4% of
isolates, including Staphylococcus epidermidis 962 (27.4%), other
coagulase-negative staphylococci 289 (8.2%), Staphylococcus aureus
237 (6.8%), and Streptococcus pneumoniae 159 (4.5%). Pseudomonas
aeruginosa was the most common gram-negative isolate (38.4%). All
tested Gram positive isolates were sensitive to vancomycin. As
a whole, isolates were most sensitive to moxioxacin and ciproox-
acin with resistance of 3.7% and 3.3%, respectively. Oxacillin
resistance was increasingly found in S. aureus (14.8% in 2011,
27.8% in 2014, P = 0.06), but was without signicant change in
S. epidermidis and other coagulase-negative Staphylococci (range
19.4%32.0%). There was an increase in moxioxacin resistance
among S. epidermidis, increasing from 0.9% to 12.7%. Using a logistic
regression model, the overall change in resistance of bacteria to
antibiotics by year was not signicant.
Conclusions: Gram-positive bacteria represented the majority of
bacteria isolated, with a possibly increasing prevalence of oxacillin
Received for publication October 13, 2015; revision received February 1,
2016; accepted February 23, 2016. Published online ahead of print April
14, 2016.
From the *King Khaled Eye Specialist Hospital, Riyadh, Kingdom of Saudi
Arabia; and Wilmer Eye Institute of Johns Hopkins University,
Baltimore, MD.
The authors have no funding or conicts of interest to disclose.
H. S. Al-Dhaheri and M. D. Al-Tamimi these authors contributed equally to
this manuscript.
This study was performed with the approval of the King Khaled Eye
Specialist Hospital Institutional Review Board and adhered to the Tenets
of the Declaration of Helsinki. All authors contributed to and approved
the nal manuscript. This article discussed antibiotics within the context
of keratitis, which is not an US Food and Drug Administration
approved indication.
Reprints: Donald U. Stone, MD, Research Department, King Khaled Eye
Specialist Hospital, P.O. Box 7191, Arouba Rd, Riyadh, Kingdom of
Saudi Arabia 11462 (e-mail: dstone@kkesh.med.sa).
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Cornea  Volume 35, Number 6, June 2016
Copyright 2016 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
resistance in S. aureus. Fluoroquinolone resistance is uncommon,
and no vancomycin-resistant gram-positive strains were identied.
There was no overall signicant trend in antibiotics resistance;
however, future surveillance studies are recommended.
Key Words: keratitis, corneal ulcer, antimicrobial, antibiotic
resistance
(Cornea 2016;35:789794)
B acterial keratitis is a serious ocular infection that can lead
to severe visual disability or even blindness.14 Early
recognition and initiation of appropriate antimicrobial agents
is crucial to prevent its devastating sequelae. Corneal
scraping and initiation of broad-spectrum antibiotic therapy
remain the mainstay of treatment.5 The etiology of microbial
keratitis and the bacteriological prole varies, depending
upon the geographic location and referral patterns and other
variables. However, Staphylococcus epidermidis, Staphylo-
coccus aureus, other coagulase-negative Staphylococcus
species, Streptococcus pneumonia, and Pseudomonas aeru-
ginosa remain the most commonly encountered pathogens in
bacterial keratitis.6
Antimicrobial resistance poses a serious challenge to
the management of various infections, and microbial keratitis
is not an exception. Among ocular isolates, accumulating
evidence suggests emergence of resistance to commonly used
antibiotics and the rst-line therapeutic agents for bacterial
keratitis such as the uoroquinolones.79 Injudicious and
prolonged used of topical antibiotics is a promoting factor
for bacterial resistance or multidrug resistance among ocular
bacterial ora.7,10,11 Antibiotic resistance of ocular pathogens
creates an additional challenge in the management of
infectious keratitis, especially when determining empiric
therapy in the absence of diagnostic data.
The purpose of this study was to determine the
bacteriological prole of cases of presumed microbial kera-
titis at the King Khaled Eye Specialist Hospital (KKESH) and
determine the incidence of antibiotic resistance during the
study period.
MATERIALS AND METHODS
After approval by the institutional review board,
microbiology records of all culture-positive microbial kerati-
tis cases seen at KKESH, Riyadh, Saudi Arabia, between
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Al-Dhaheri et al Cornea  Volume 35, Number 6, June 2016

January 2011 and December 2014 were reviewed. The study last accessed on 18 December, 2015). Resistance and no
period began in 2011 to coincide with implementation of the resistance as the outcome variable and type of bacteria,
current laboratory data management system; previous results year, and organisms as dependent variables were inserted
were not available. Only bacterial isolates in the setting of into a binominal regression model, and adjusted odds ratio,
microbial keratitis were considered in this study. Atypical 95% condence interval, and 2-sided P values were obtained.
mycobacteria, Nocardia, and other lamentous bacteria, MantelHaenszel extended x2 was used for summarizing
diphtheroids, Propionibacterium acnes, and organisms iso- linear trends.
lated fewer than 25 times during the study period were
excluded. Specimens were obtained according to the treating
physicians discretion and were typically performed by
residents or fellows. The usual technique included swabbing
RESULTS
the cornea with a sterile swab and directly inoculating the A total of 3506 bacterial isolates were obtained from all
Petri dishes in a C shape, so that any colonies outside of the positive corneal cultures, of which 2037 isolates were
C were ignored as contaminants. Blood, chocolate, and included for detailed antibiotic susceptibility analysis. The
Sabourad plates and thioglycolate broth were typically used. most commonly isolated bacteria are presented in Table 1,
Positive cultures were determined at the discretion of the with trend analysis of relative incidence of each organism
microbiologist, but the protocol is to report positive cultures during the study period.
and defer clinical correlation to the clinician. Cultures Gram-positive bacteria accounted for 91.4% of the
obtained from conjunctival swabs in keratitis cases were isolates. Staphylococcus epidermidis was the most commonly
excluded. Identication and sensitivity were performed using identied gram-positive bacteria [962 of 3186 (30.2%)],
the automated Vitek2 system (bioMrieux, Marcy lEtoile, whereas P. aeruginosa was the most common gram-
France); during the study period, the manufacturer frequently negative isolate [123 of 254 (48.4%)]. Pseudomonas aerugi-
modied the susceptibility cards. Pseudomonas aeruginosa nosa demonstrated a slight decrease in relative incidence from
isolates were tested with AST-N116, N232, and nally N291 2011 to 2014 (5.9%3.9%, odds ratio = 0.228), no other
cards. Staphylococcus species used AST-P580. Streptococcus statistically signicant trends were observed regarding the
used AST-P576 cards. Streptococcus oralis, S. mitis, and S. distribution of bacterial isolates over the study period.
viridans isolates were subjected to in vitro antimicrobial When all isolates tested for specic antibiotic sensitiv-
sensitivity testing using the KirbyBauer Disc Diffusion ity were analyzed as a group, resistance to ciprooxacin
Method for chloramphenicol, clindamycin, erythromycin, (3.3%), gentamicin (3.3%), and moxioxacin (3.7%) were the
and vancomycin; the E test (AB Biodisk, Remel Inc, Lenexa, lowest among all tested antibiotics. Resistance to the tested
KS) was used for penicillin (using benzylpenicillin) and antibiotics among all bacteria from 2011 to 2014 is illustrated
ooxacin. For Haemophilus inuenzae, the KirbyBauer disk in Figure 1.
diffusion method was used with Haemophilus Test Medium
and beta-lactamase testing with Cenase disks (BD Diag- Staphylococcus aureus
nostics, Franklin Lakes, NJ). All results were interpreted Of the 237 S. aureus isolates, 46 (19.4%) were oxacillin
according to the National Committee for Clinical Laboratory resistant (ORSA). Oxacillin resistance was increasingly found
Standards. The details of isolates, including the speciation and in S. aureus, although this was of marginal statistical
antibiotic sensitivity results, were retrieved from the clinical signicance (14.8% in 2011, 27.8% in 2014, P = 0.06).
laboratory database. Based on the minimum inhibitory When tested for uoroquinolone sensitivity, 11 (7.5%) of all
concentration systemic breakpoints, all isolates were inter- S. aureus were found to be ooxacin resistant but none were
preted to be susceptible, intermediate, or resistant. The resistant to moxioxacin. All isolates were susceptible to
intermediate sensitivity responses were grouped in the vancomycin, 42 (18.6%) were resistant to erythromycin, and
sensitive group for nal analysis, except for vancomycin, 11% were resistant to clindamycin.
for which intermediate sensitivity was grouped with the
resistant category.
The data were imported into a Microsoft Excel spread- TABLE 1. Distribution of Most Commonly Isolated Bacteria
sheet le. The total tests and the number of positive isolates of From Keratitis Cultures With Trend Analysis 20112014
each bacteria type for each of the 4 years were the units. For Species Isolated Number (%) Trend x Value Trend P
these, sensitivity reports of different antibiotics were listed.
Staphylococcus epidermidis 962 (47.2%) 0.96 0.326
After cleaning the data, they were transferred into a spreadsheet
Other CNS 289 (14.2%) 0 0.981
of Statistical Package for Social studies (SPSS 16; IBM,
Staphylococcus aureus 237 (11.6%) 1.21 0.272
Chicago). The univariate and multivariate analysis was carried
Streptococcus pneumonia 159 (7.8%) 0 0.995
out using a parametric method. The frequency and percentage
Pseudomonas aeruginosa 123 (6%) 26.78 2.28 1027
proportions of resistance of each antibiotic every year and of
Streptococcus mitis/oralis 111 (5.4%) 0.11 0.735
total 4 years were estimated along with their 95% condence
Haemophilus inuenza 86 (4.2%) 0.29 0.593
intervals. The percentage proportions with 95% condence
Moraxella group 45 (2.2%)
intervals of resistance were plotted on the graph. The x2 and the
Streptococcus viridans 25 (1.2%) 0.11 0.737
2-sided P values were calculated with the Open Epi software
2037
(http://www.openepi.com/DoseResponse/DoseResponse.htm

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Cornea  Volume 35, Number 6, June 2016
FIGURE 1. Antibiotic resistance
among keratitis isolates at KKESH
(201114). CAZ, ceftazidime;
CHLOR, chloramphenicol; CIPRO,
ciprofloxacin; CLIN, clindamycin;
ERY, erythromycin; FA, fucidic
acid; GENT, gentamicin; MOX,
moxifloxacin; OFLOX, ofloxacin;
OXA, oxacillin; PCN, penicillin;
SXT, trimethoprim-sulfamethoxazole;
TETRA, tetracycline. Error bars repre-
sent 95% confidence intervals.
Staphylococcus epidermidis and Other
Coagulase-Negative Staphylococci
A total of 962 (27.4%) S. epidermidis were isolated. In
addition, 289 (8.2%) isolates from other Coagulase-Negative
Staphylococci (CNS) species were identied, including Staph-
ylococcus auricularis (n = 5), Staphylococcus capitis (n = 48),
Staphylococcus haemolyticus (n = 31), Staphylococcus hominis
(n = 78), Staphylococcus warneri (n = 50), and other CNS that
were not further specied (n = 77). From S. epidermidis
isolates 40.3% (407 of 962) were oxacillin resistant. In other
CNS isolates, 32.4% were oxacillin resistant (93 of 289).
Vancomycin susceptibility of all CNS was 100%, including the
oxacillin-resistant CNS. Staphylococcus epidermidis demon-
strated a trend of increasing moxioxacin resistance over time,
increasing from 0.9% in 2011 to 12.7% in 2014 (odds ratio =
13.8, x2 = 39.32, P , 1 1027).
Streptococcus pneumoniae
Streptococcus pneumoniae was the fourth most com-
monly isolated bacteria with a total of 159 isolates. Penicillin
resistance was observed in 46 (31.9%) of the isolates. Fifty-
two of the isolates (38.2%) were resistant to erythromycin.
All the isolates were sensitive to vancomycin, ceftriaxone,
ooxacin, and moxioxacin. No statistically signicant trends
were observed among Streptococcus pneumonia when tested
for specic antibiotics over the 4 years of the study.
Haemophilus inuenzae
A total of 86 isolates were identied during the study
period. Five of the isolates (5.8%) were resistant to ceftazidime,
whereas 2 (2.3%) of the isolates were chloramphenicol
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KKESH Bacterial Keratitis Antibiogram
resistant. The number of resistant organisms was too small to
allow trend analysis.
Pseudomonas aeruginosa
Of 123 isolates, 7 (5.6%) were ceftazidime resistant and
6 were resistant to gentamicin (4.9%). Among the uoroqui-
nolones, 1 isolate was resistant to ooxacin and 6 (4.9%)
were resistant to ciprooxacin. All ciprooxacin-resistant P.
aeruginosa were isolated in 2014, but the overall trend of
resistance among P. aeruginosa isolates could not be
analyzed because of the small numbers of resistant organisms.
DISCUSSION
Bacterial keratitis remains a common cause of ocular
morbidity in the Kingdom of Saudi Arabia (KSA).1214
Periodic surveillance reports of causative organisms and their
sensitivity proles allow clinicians to employ diagnostic and
therapeutic strategies tailored to the likely pathogens in
a given geographic region.
In this study, Gram-positive bacteria accounted for
91.4% of the isolates. This nding is similar to previous
reports by other authors in which Gram positives were the
predominant isolate in bacterial keratitis, accounting for
67%82%.1518 In accordance with previous reports in the
literature,13,15,17 in this study S. epidermidis was the most
commonly identied gram-positive bacteria (30.2%) and P.
aeruginosa was the most common gram-negative isolate
(38.4% of all gram negatives). Similarly, in a recent report
by Hernandez-Camarena et al,16 S. epidermidis (36%) and
other CNS (15%) were the most frequently isolated bacteria.
CNS including S. epidermidis were found to be the most
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Al-Dhaheri et al
common pathogens in other series from Hyderabad, India
(40.3%),19 and New Zealand (40.8%).20
However, the ratio of CNS to other pathogens is higher
than what was previously reported from the same institution
by Al Shehri et al; gram-positive isolates represented 70% of
the isolates in 1995 and 73% in 2005.13 This increase in
relative frequency could be attributed to the higher number of
coagulase-negative staphylococci species in our study, spe-
cically S. epidermidis which accounted for 30.2% of the
gram-positive isolates and 27% of the total isolated bacteria.
Potential explanations for this change include a true change in
the relative incidence of disease caused by these organisms,
more frequent contamination of culture specimens by skin or
ocular surface ora, or changes in microbiological laboratory
techniques that could inuence the culture sensitivity or
speciation results. It is possible that the small but statistically
signicant decrease in the relative incidence of Pseudomonas
isolates is a byproduct of the increase in CNS isolates, rather
than a change in the role of Pseudomonas as a pathogen.
There is a signicant variation in the incidence of
various bacteria in differing geographic regions and likely
within regions dependent upon the patient population and
referral patterns. Other populations seem to have a greater
incidence of Pseudomonas keratitis,2123 perhaps associated
with contact lens use. We are not aware of data on the relative
use of refractive or cosmetic contact lenses in Saudi Arabia,
but we propose that the dry climate contributes to a lower
prevalence of contact lens wear, and therefore a lower
incidence of contact lensassociated pathogens.
Methicillin/oxacillin-resistant S. aureus and S. epider-
midis (MRSA and MRSE) strains have been of increasing
concern in systemic and ocular infection. In ophthalmology,
this is an important development, as Staphylococcus species
comprise one of the more common causative organisms of
microbial keratitis in many parts of the world.6 Initially,
MRSA was consider a nosocomial pathogen; however, recent
reports highlight the emergence of MRSA infections among
otherwise healthy individuals with no particular risk factors.24
A report from the United States suggested MRSA ocular
infections were increasing in incidence from 2000 to 2005.25
Our current study suggests a nonstatistically signicant trend
of increasing MRSA prevalence, but the 4-year study duration
limits the conclusions that can be drawn regarding changes
over time. MRSA represented 19.4% of S. aureus in this
series, which is lower than what has been reported from
Taiwan (60%),26 Canada (43.1%),17 and Mexico (45%).16
Data regarding the community prevalence of MRSA coloni-
zation in KSA are limited, but one report found that 25% of
outpatients were carriers.27 The relatively lower incidence of
MRSA among keratitis pathogens in our study may reect
a lower incidence of MRSA colonization in the community or
other undetermined factors.
Antibiotic resistance among S. epidermidis and other
CNS is a common nding; in this study, 39.7% of CNS were
oxacillin/methicillin resistant (MRCNS), which is comparable
with 43.1% reported in a series from Canada.17 There have been
reports highlighting the emergence of vancomycin-resistant
MRSA among ocular isolates.8,16 However, none of the MRSA
or MRCNS isolates were resistant to vancomycin in our study.
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Cornea  Volume 35, Number 6, June 2016
Given the rare but increasing development of vancomycin
resistance among gram-positive organisms such as MRSA and
Enterococcus, it is likely that these organisms will ultimately be
isolated in any region in which patients (and their microbial
ora) have exposure to vancomycin.
Presumed sensitivity of MRSA/MRCNS to vancomycin
has led some authors to recommend the use of vancomycin as
the gram-positive antibiotic of choice for culture-proven
MRSA/MRCNS or high-risk cases of bacterial keratitis.28,29
It has been proposed that judicious use of vancomycin based
on culture and sensitivity results would help limit the
emergence of vancomycin-resistant ocular bacterial strains,30
32
but the minimal number of bacteria exposed to vancomycin
with ocular use may have a negligible effect on the commu-
nitywide prevalence of resistance and can therefore be justied
as initial empiric therapy in vision-threatening conditions,33
especially in populations with frequent resistance to other
antibiotics, such as cephalosporins, uoroquinolones, and
clindamycin. The ideal antibiotic or combination of antibiotics
remains to be determined.34
When considered as a whole, isolates were most
sensitive to moxioxacin and ciprooxacin with resistance
of 3.7% and 3.3%, respectively. However, S. epidermidis
demonstrated an increasing trend toward moxioxacin resis-
tance over time. We speculate that community exposure to
systemic uoroquinolones applies selection pressure that
promotes the development of resistance in the bacterial
population as a whole; individual patients are also more
likely to develop resistant organisms after exposure to a given
antibiotic, and it is possible that the resistant organisms were
the result of previous ocular uoroquinolone use. Further-
more, among P. aeruginosa isolates, 3.3% were resistant to
ciprooxacin, which is higher than what has been reported in
Taiwan (1%), and no resistance to ciprooxacin was found in
2 other reports from United States and Australia.3537 Other
studies have found a similar or higher rate of uoroquinolone
resistance.22,38 This discrepancy could be partially explained
by access to antibiotics including systemic and topical
uoroquinolones without a prescription in KSA.39,40 The
relative frequency of previous exposure to topical antibiotics
may have been higher in this study population because of the
referral patterns of KKESH, including many postoperative
patients and those who have failed treatment elsewhere. Other
changes in socioeconomic and healthcare delivery factors
could also be contributing to the increase in uoroquinolone
resistance, as could other inherent differences when compared
with other populations.
In addition to the retrospective nature of the study, there
are other limitations. The detection of bacteria via culture
does not conclusively dene a pathogenic role, and it is
acknowledged that an unknown percentage of the samples
reported herein are contaminants or unrelated to the under-
lying disease process. The indication to obtain a corneal
scraping for culture likely varies among the treating physi-
cians and was not standardized or controlled for. Because of
the lack of standardized protocols and concentration break-
points for ocular infection, the in vitro susceptibility testing
was performed using the National Committee for Clinical
Laboratory Standards, which was designed for systemic
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Cornea  Volume 35, Number 6, June 2016
infectious diseases. This may underestimate or overestimate
the true efcacy of treatment in clinical practice. Furthermore,
KKESH is a referral-based tertiary eye care center with active
surgical facilities, which may lead to overrepresentation of
specic isolates related to previous ocular surgery, severity of
disease, or failure of initial therapy because of antibiotic
resistance or other factors. Other preexisting factors such as
ocular and systemic comorbidities, previous antimicrobial
treatment, and geographic location may be contributing
factors in bacterial isolate distribution and their sensitivity
prole compared with other studies. Regarding the trend
analysis, the relatively brief duration of the study period limits
the ability to extrapolate the results.
In conclusion, bacterial keratitis remains a major cause
of ocular morbidity in our region. The current study
delineates the bacteria isolated from patients with microbial
keratitis and highlighted current resistance patterns that can
be used to guide clinical management. This study also
provides an interesting comparison with the bacteriological
proles of regions with differing demographics, climate, and
healthcare systems. The overall pattern of antibiotic resistance
seems to lie between developing countries in Asia and
countries with the greatest access to health care in Europe
and North America; with the rapid development of access to
health care in Saudi Arabia, it is likely that antibiotic
susceptibility will continue to diminish among ocular patho-
gens. Ongoing surveillance studies will shed light on the
mechanisms and epidemiology of this trend and it is hoped to
be of benet in guiding the care of individual patients and
informing policy and practice pattern recommendations.
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