Int. J. Biosci.

2024

International Journal of Biosciences | IJB |

ISSN: 2220-6655 (Print), 2222-5234 (Online)
http://www.innspub.net
Vol. 25, No. 2, p. 103-113, 2024

RESEARCH PAPER OPEN ACCESS

Eye bacterial infections and antibiotic resistance patterns in

patients attending Abdel Fadeel Almaz Hospital, Khartoum
State, Sudan

Asmaa Ibrahim Mohammed Tahir*1, Muataz Mohamed Eldirdery2, Hatil Hashim EL-
Kamali3

1
Department of Zoology, Botany Department, Faculty of Science and Technology,
Omdurman Islamic University, Omdurman, Sudan
2
Department of Microbiology, Institute of Tropical Medicine, National Research Centre,
Khartoum, Sudan

Key words: Eye infections, Bacterial isolates, Staphylococcus spp., Pseudomonas ssp., Antimicrobial resistance

http://dx.doi.org/10.12692/ijb/25.2.103-113 Article published on August 05, 2024

Abstract
Antimicrobial resistance is a global public health concern involving bacteria becoming resistant to antibiotics,
making infections harder to treat. This study aimed to isolate and identify bacteria associated with eye infections
in humans in Khartoum State. We collected 121 eye swabs from patients at Abdel Fadeel Almaz Hospital between
February and May 2017. Of these samples, 85 (70.3%) yielded bacterial isolates. Identified Gram-positive
bacteria included Staphylococcus spp and Bacillus spp, while Gram-negative bacteria included Pseudomonas
spp. The predominant bacterium was Staphylococcus aureus. Antibiotic sensitivity tests showed that all isolates
were sensitive to ciprofloxacin and azithromycin, indicating these drugs as effective treatments for eye
infections. The study concluded that Gram-positive bacteria are the most common causative agents of eye
infections in humans, and ciprofloxacin and azithromycin are effective treatment options.
* Corresponding Author: Asmaa Ibrahim Mohammed Tahir  [email protected]

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Introduction Gram-positive bacteria. It is often used in the

Eye infections are a global health concern, affecting treatment of bacterial conjunctivitis and keratitis.
millions of people each year. These infections can be
caused by a variety of pathogens, including bacteria, Azithromycin, a macrolide antibiotic, is also widely
viruses, fungi, and parasites. The prevalence and used to treat ocular infections due to its broad
types of eye infections can vary depending on spectrum of activity and good tissue penetration,
geographic location, climate, socioeconomic especially in cases of bacterial conjunctivitis and
conditions, and healthcare infrastructure (Modarres trachoma. (Tzu et al., 2021).
et al., 1998). The common types of eye infections are :
(1) conjunctivitis : an inflammation of the Cataracts remain the leading cause of blindness
conjunctiva, often caused by bacteria (such as globally, with trachoma also being a significant cause
Staphylococcus aureus, Streptococcus pneumoniae, (World Health Organization, 2017). Although
and Haemophilus influenzae). (2) Keratitis : An cataracts are often age-related, they can also result
infection of the cornea, which can be bacterial (e.g., from infections caused by microbiota (Forbes et al.,
Pseudomonas aeruginosa, Staphylococcus aureus), 2002).
viral (e.g., herpes simplex virus), fungal (e.g.,
Fusarium species), or parasitic (e.g., Acanthamoeba). Limited research has been conducted on eye
(3) Endophthalmitis: a severe inflammation of the infections, particularly in Sudan, emphasizing the
interior of the eye, typically caused by bacteria (e.g., need for further studies in this field.
Staphylococcus epidermidis, Staphylococcus aureus, This study aims to :
Streptococcus species) or fungi (e.g., Candida - identify potential bacterial isolates responsible for
species). (4) Blepharitis: an inflammation of the eye inflammation in adult patients attending an eye
eyelids, often associated with bacterial infections hospital in Khartoum State from February to May
(e.g., Staphylococcus aureus) or skin conditions like 2017.
seborrheic dermatitis (Modarres et al., 1998). - To isolate and identify pathogenic bacteria causing
eye infections.
The susceptibility of bacterial isolates from eye - To evaluate the antibiotic sensitivity of each
infections varies depending on the region and the bacterial isolate.
specific bacterial strain. Generally, the following
antibiotics are commonly tested and used: 1. Materials and methods
Fluoroquinolones: Such as ciprofloxacin, Materials
moxifloxacin, and ofloxacin, are often effective The study was conducted at Abdel Fadeel Almaz
against a broad range of bacteria, including Hospital in Khartoum State, Sudan, to isolate and
Pseudomonas aeruginosa. 2. Aminoglycosides: Such identify pathogenic bacteria causing eye infections
as gentamicin and tobramycin, are effective against from February to May 2017.
Gram-negative bacteria and some Gram-positive
bacteria. 3. Macrolides: Such as erythromycin and Sample size
azithromycin, are used primarily for Gram-positive A total of 121 swab samples were collected from
bacteria and some Gram-negative bacteria. 4. infected eyes of patients at Abdel Fadeel Almaz
Tetracyclines: Such as doxycycline, are used for Hospital during the study period (Abdel Fadeel Almaz
atypical pathogens like Chlamydia trachomatis. 5. In Hospital records, 2017).
the context of ocular infections, ciprofloxacin and
azithromycin are commonly used antibiotics. Study design
Ciprofloxacin is a fluoroquinolone antibiotic that is This descriptive cross-sectional study was conducted
effective against a broad range of Gram-negative and from February to May 2017 , according to Forbes et

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al., 2002). Citrate utilization

Simmon's citrate agar medium was inoculated with
Study area the tested organism and incubated at 37°C for 24
The study took place at Abdel Fadeel Almaz Hospital hours. A blue color indicated positive citrate
in Khartoum State (Abdel Fadeel Almaz Hospital utilization, while no color change indicated a negative
records, 2017). result.

Collection and transportation of samples Kligler's iron agar test (KIA)

Eye samples were collected using the method The tested organism was inoculated into Kligler ion
described by Forbes et al. (2002). Purulent material agar medium and incubated at 37°C for 24 hours.
from the lower conjunctival sac and inner canthus of Yellow butt-red or pink slant indicated glucose
the infected eye was aseptically collected with sterile fermentation only; yellow slant and yellow butt
swabs to avoid skin contamination. indicated fermentation of lactose and possibly
glucose. Red-pink slant and butt indicated no
Samples were immediately transported to the fermentation. Cracks and bubbles in the medium
Tropical Medicine Research Institute Laboratory for indicated gas production from glucose fermentation,
bacteriological examination. and blackening along the stab line or throughout the
medium indicated hydrogen sulfide production.
Tests for gram-positive bacteria
(Forbes et al., 2002) : (Tables 1 – 2) Indole production
Peptone water medium was inoculated with the tested
Catalase test organism and incubated at 37°C for 24 hours. After
2 ml of 3% hydrogen peroxide solution was placed in incubation, 2 drops of Kovac's reagent were added
a test tube. A small amount of the tested organism's and shaken well. A red ring formation at the surface
colony from nutrient agar was added to the hydrogen of the media indicated a positive reaction.
peroxide using a wooden stick. Gas bubble production
indicated a positive result. Oxidase test
A solution of oxidase reagent was prepared by
Coagulase test dissolving 1g of reagent in 100 ml of distilled water.
This test identifies bacteria producing the coagulase The solution was added to isolated bacteria on
enzyme. nutrient agar for five minutes, and the excess reagent
was discharged. After 15 minutes, a color change to
Slide method purple indicated a positive result, while no color
A single colony from a 24-hour nutrient agar plate change indicated a negative result.
was emulsified in diluted plasma on a microscopic
slide. Clumping within 5 seconds indicated a positive Sensitivity tests
result. Antibiotic sensitivity tests were performed using the
diffusion susceptibility test (Kirby-Bauer method,
Tests for gram-negative bacteria Cowan and Steel, 1974). Five similar colonies from a
Urease test 24-hour nutrient agar pure culture were selected
A urea agar medium slope was inoculated with the using a sterile wire loop, inoculated in 5 ml of
tested organism and incubated at 37°C for 24 hours. nutrient broth medium, and incubated at 37°C for 8
hours until light visible turbidity appeared,
A color change to pink indicated a positive reaction, comparable to the 0.5 McFarland barium sulfate
while no change indicated a negative reaction. turbidity standard. Using a sterile cotton swab, the

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colony suspension was spread on Muller Hinton agar Results

medium, left to dry at room temperature for 15 This study was conducted at Abdel Fadeel Almaz
minutes, and antibiotic discs were placed on the Hospital in Khartoum State, Sudan, and included 121
medium surface with sterile forceps. patients with eye infections. The study population
comprised both males and females, aged between 20
The plates were incubated at 37°C for 18-24 hours, and 80 years. The highest frequency of eye infections
and the zone of growth inhibition around the discs was observed in the age group 61-70 years (27
was measured with a ruler. Four antibiotic discs— patients, 22.3%). Females were more affected than
fusidic acid, azithromycin, ciprofloxacin, and males, with 92 (76%) female patients and 29 (24%)
optochin were used for the sensitivity test (Table 3). male patients (Fig. 1).

Table 1. Biochemical Test for Staphylococcus aureus and Staphylococcus intermedius Isolated from Infected
Eyes.
Characters S. aureus S. intermidius
Catalase test + +
Coagulase test. + +
Vp test + _
Gram reaction + +

+ : Positive reaction.
- : Negative reaction.

Table 2. Biochemical Test for Pseudomonas aeruginosa, Bacillus lentus, Bacillus spp, and Staphylococcus
epidermidis Isolated from Infected Eyes.
Characters Pseudomonas aeruginosa Bacilus lentus S.epidermidis
Gram reaction - + +
Catalase test +
Co-agulase test. -
Oxidase test + +
KIA test +
Peptone water test - -
Citrate test + -
Urease test - +

+ : Positive reaction.
- : Negative reaction.

Aerobic incubation of the eye swab samples revealed Staphylococcus intermedius (15 isolates, 17.6%),
different bacterial species. Out of the 121 samples, 36 Staphylococcus epidermidis (4 isolates, 4.7%),
showed no growth while 85 exhibited bacterial Bacillus spp (2 isolates, 2.3%), Bacillus lentus (1
growth. The isolated bacteria included isolate, 1.7%), and Pseudomonas aeruginosa (1
Staphylococcus aureus (62 isolates, 72.9%), isolate, 1.7%) (Fig. 2).

Table 3. Standard zone of inhibition to different Antibiotics.

Antibiotic disk Disk potency Zone of inhibition (diameter in mm)
Resistant Intermediate Sensitive
Azithromycin(AZM) 15mcg 13 or less 14-17 18 or more
Ciprofloxacin(CIP) 5mcg 15 or less 16-20 21 or more
Fusidic acid(FA) 10mcg 24 or less - 24 or more
Optochin ( OP) 10mcg 14 or less - 14 or more

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The prevalence of eye infections was higher in urban Housewives had the highest frequency of eye
residents (87 cases, 71.9%) compared to rural infections (63 cases, 52.1%), while teachers had the
residents (34 cases, 28.1%) (Fig. 3). lowest frequency (2 cases, 1.7%) (Fig. 4).

Table 4. Comparison of sensitivity of bacterial spp to antibiotics used.

Isolated bacteria OP. N (%) CIP. N (%) FA. N (%) AZM. N(%)
B.lentus 0 1(100) 1(100) 1(100)
Bacillusspp 0 2(100) 0 (0) 1(50.0)
Pseudomonasspp 0 1(100) 1(100) 1(100)
S.aureus 0 45(72.6) 34(54.8) 26(41.9)
S.epidermidis 0 2(50.0) 2(50.0) 2(50.0)
S.intermidus 0 9(60.0) 6(40.0) 7(46.7)
P-value 0.996 0.837 0.406 0.672
CIP = ciprofloxacin, AZM = azithiromycin, OP = Optochin, FU = Fusidic acid.

The highest percentage of eye infections was among lowest percentage was among those with secondary
illiterate individuals (56 cases, 46.3%), while the school education (12 cases, 9.9%) (Fig. 5).

Fig. 1. Distribution of the eye infections according to the gender.

Fig. 2. Percentage of bacteria isolated from infected eyes of human.

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Non-diabetic patients exhibited the highest infections was in patients aged 61-70 years (27 cases,
percentage of eye infections (99 cases, 81.8%), 22.3%), while the lowest distribution was in patients
whereas diabetic patients had a lower percentage (22 over 70 years (14 cases, 11.6%) (Fig. 7).
cases, 18.2%) (Fig. 6). The highest distribution of eye

Fig. 3. Prevalence of the eye infections according to the resident.

Patients who did not use antibiotics had a higher compared to those who used antibiotics (27 cases,
percentage of eye infections (94 cases, 78%) 22%) (Fig. 8).

Fig. 4. Frequency of the eye infections according to the occupations.

Antibiotic sensitivity test (45/62, 72.6%), fusidic acid (34/62, 54.8%), and
All isolates were resistant to optochin. B. lentus was azithromycin (26/62, 41.9%). Staphylococcus
sensitive to fusidic acid, ciprofloxacin, and epidermidis was sensitive to ciprofloxacin (2/4, 50%),
azithromycin. Bacillus spp were sensitive to fusidic acid (2/4, 50%), and azithromycin (2/4, 50%).
ciprofloxacin (2/2, 100%). Pseudomonas aeruginosa Staphylococcus intermedius was sensitive to
was sensitive to ciprofloxacin (1/1, 100%). ciprofloxacin (9/15, 60%), fusidic acid (6/15, 40%),
Staphylococcus aureus was sensitive to ciprofloxacin and azithromycin (7/15, 46.7%) (Table 4).

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Fig. 5. Percentage of the eye infections according to educational levels.

The bacteria were classified as sensitive or resistant isolates. Resistance patterns can vary widely based on
based on the diameter of the zone of inhibition for geographic location, healthcare practices, and
each antibiotic. Staphylococcus aureus was resistant antibiotic usage.
to optochin, but sensitive to azithromycin (zone of
inhibition: 2.5 cm), ciprofloxacin (zone of inhibition: This study aimed to isolate and identify bacteria
2 cm), and fusidic acid (zone of inhibition: 1.2 cm). associated with eye infections in humans. Eighty-five
bacterial species were isolated, 84 of which were
Isolation and identification bacteria associated with Gram-positive and one was Gram-negative.
eye infections
Eye infections are frequently reported worldwide, The most prevalent bacterium was Staphylococcus
with bacteria being the most common causative aureus, which aligns with previous studies conducted
agents (Modarres et al., 1998). Antimicrobial in Sudan (Nabila, 1985; Fowzia, 2002; Salma, 2003;
susceptibility testing provides critical data on which Iman, 2008) and in other regions (Jackson and
antibiotics are effective against specific bacterial Eykyn, 2003).

Fig. 6. Distribution of the eye infections according to diabetic status.

Staphylococcus epidermidis was also isolated, and Benz & Scott (2004). Only one Pseudomonas
consistent with findings by NanWang et al. (2015) aeruginosa was isolated, in agreement with studies

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 Int. J. Biosci. 2024

by Tilahun Aweke et al. (2014) and NanWang et al. of bacterial isolates were from patients aged 61-70
(2015). Bacillus lentus was isolated, which concurs years, consistent with a study by Deborah Dean et al.
with multiple studies (Greding et al., 1993; Fatimah (2008). Female patients were more frequently
et al., 1994; Seham et al., 1995; Moore et al., 1995; infected than male patients, aligning with Salah et al.
Kawther, 1997; Iman, 1997; Fowzia, 2002; Salma, (2016), but conflicting with studies by Deborah Dean
2003), but disagrees with Iman (2008). The majority et al 2008.

Fig. 7. Distribution of the eye infections according to the different ages.

The female patients (92(76%)) were more infected gender differences may be due to the Hygiene and
than male patients( 29 (24%) )this result agrees with behavior from area to another area. The patients who
Salah et al.,(2016),but disagrees with some previous were came from the urban areas (87(71.9%)) was
studies reported a high prevalence of the disease in more infected than patients which who came from the
male patients than female patients (Deborah Dean et rural area (34(28.1%) which is agreement with study
al., 2008). This can be explained by the fact that that reported by Mar Justel et al.,(2015).

Fig. 8. Percentage of the infections according to patients using antibiotic and patients not using antibiotic.

In this study the highest frequency of infection poor hygiene system. In the present study non
according to educational level was illiterates diabetic patients (99(81.8%) ) were more infected
(56(46.3%)) that may be due to low of education and than diabetic patients this might be due to good

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Hygiene, periodic follow-up and personal attention of Antibiotics: Inappropriate prescribing, inadequate
diabetic patients, this result was disagree with study dosing, and use in agriculture contribute to selective
that reported by Karim sab and Razak,(2013). pressure. (2) Poor Infection Control: Spread of
resistant bacteria in healthcare settings due to
Antibiotic resistance patterns inadequate hand hygiene and environmental
Susceptibility to infection was found to increase in contamination. (3) Lack of new antibiotics: Few new
elderly, because they are at a greater risk due to their antibiotics in development reduce treatment options
low immunity. In this study ciprofloxacin and for resistant infections. (4) Global Travel and Trade:
azithromycin antibiotics were drugs of choice against Spread of resistant bacteria across regions due to
ocular pathogens (Benz et al., 2004). international travel and trade. (5) Environmental
Factors: Antibiotics in wastewater, agriculture runoff,
The mechanisms of Antimicrobial Resistance may be and healthcare settings can contribute to resistance
one or more of the following: 1. Genetic Mutation: development.
Bacteria can mutate their DNA, acquiring resistance
to antibiotics they were once susceptible to. 2. Consequences of antimicrobial resistance may be one
Horizontal Gene Transfer: Bacteria can exchange of the following (1) Treatment Failures: Infections
genetic material (plasmids, transposons) containing become harder to treat, leading to prolonged illness
resistance genes with other bacteria, even across and increased mortality. (2) Increased Healthcare
different species. 3. Drug Inactivation or Costs: Longer hospital stays and use of more
Modification: Bacteria produce enzymes that expensive antibiotics contribute to economic burden.
inactivate antibiotics (e.g., beta-lactamases break (3) Public Health Threat: Resistant bacteria can
down beta-lactam antibiotics). 4. Reduced spread within communities and globally, limiting
Permeability: Bacteria alter their cell walls or treatment options (CDC, 2023; WHO, 2022).
membranes to prevent antibiotics from entering the
cell. 5. Efflux Pumps: Bacteria pump antibiotics out of Conclusion
their cells, reducing intracellular concentrations In conclution, this study found that Gram-positive
below effective levels. bacteria were the most common causative agents of
eye infections in human. Staphylococcus aureus was
The Common Antibiotic Resistance Mechanisms may found to be the predominant bacteria in eye
be one or more of the following: (1) Beta-lactam infections. All isolates were resistant to optochin. B.
Resistance that common in Gram-positive (e.g., lentus was sensitive to fusidic acid, ciprofloxacin, and
Staphylococcus aureus) and Gram-negative bacteria azithromycin. Bacillus spp were sensitive to
(e.g., Escherichia coli, Klebsiella pneumoniae) due to ciprofloxacin. Pseudomonas aeruginosa was sensitive
beta lactamase production. (2) Fluoroquinolone to ciprofloxacin. Staphylococcus aureus was sensitive
Resistance: Often due to mutations in DNA gyrase to ciprofloxacin, fusidic acid, and azithromycin.
and topoisomerase IV genes, reducing drug binding. Staphylococcus epidermidis was sensitive to
(3) Aminoglycoside Resistance: Mediated by enzyme ciprofloxacin, fusidic acid, and azithromycin.
modification (e.g., acetyltransferases,
phosphotransferases) or reduced uptake. (4) Staphylococcus intermedius was sensitive to
Macrolide Resistance: Often due to efflux pumps or ciprofloxacin, fusidic acid, and azithromycin.
modification of the ribosomal target site. (5) Ciprofloxacin and azithromycin are drugs of choice
Tetracycline Resistance: Mediated by efflux pumps or for treatment of eye infections. These in vitro
ribosomal protection proteins. The factors may antibiotic resistance data may assist clinicians in
contributing to antimicrobial resistance may be one selecting appropriate antibiotic for treat of eye
or more of the following: (1) Overuse and Misuse of infections.

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