Al-Shara Mohammad

Department of Pharmacology, Faculty of Nursing, Irbid National University, Irbid (Jordan).

Abstract

To identify the etiology of ocular bacterial infections and to assess the in vitro susceptibility of these ocular bacterial isolates to commonly used antibiotics. Retrospective analysis of consecutive samples submitted for microbiological evaluation from children aged below 15 years who were clinically diagnosed with ocular infections and were treated at princess Rahmah hospital in North Jordan between January 2005 and December 2009. A total of 284 ocular samples were submitted for microbiological evaluation, of which 154 (54.2%) had positive bacterial growth. The most common bacterial species isolated was Staphylococcus aureus (56.6%) followed by Streptococcus pneumoniae (14.9%). Klebsiella sp (12.9%), Enterobacter spp (9.1%), Pseudomonas (5.2%) and Moraxella (1.3%). The most of gram-positive isolates was susceptible to vancomycin (93.6%) and cefotaxime (84.3%), and gram-negative isolates to ciprofloxacin (77.7%) and tobramycin (48.1%). Over all isolates, ciprofloxacin was the most effective antimicrobial agents with susceptibility rate of 78.0%. Gram-positive cocci were the most frequent bacteria isolated from ocular infections and were sensitive to vancomycin and cefotaxime, while gram-negative isolates were more sensitive to ciprofloxacin and tobramycin.

Keywords

Ocular pathogens; Ocular infection; Antimicrobial susceptibility patterns

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Introduction

Ocular Infections is a common infectious condition that can affect children and both genders. It is most commonly characterized by conjunctival hyperemia (red eye” or “pink eye) and ocular discharge which consequently may results in severe visual loss.[1]

The most common bacterial pathogens that cause ocular Infections in children include Staphylococcus species, Haemophilus species, Streptococcus pneumoniae, and Moraxella species.[2-4] One prospective study (428 children from southern Israel with a clinical diagnosis of conjunctivitis) found that, in 55% of the children, conjunctivitis was caused by S pneumoniae, H influenzae, or M catarrhalis . [5]

Treatment of bacterial ocular Infections is usually take place with empirical broad spectrum antibiotics without waiting for pathogen identification and antibiotic susceptibility tests.[6] However, frequent indiscriminate use of antibiotics results in emerge development of resistance to many commonly used antimicrobials [7-9]

The bacterial pathogens causing acute bacterial infections of the eye and their pattern of antibiotic sensitivity have recently been reported from the UK and the USA. [10,11]

Many antimicrobials have been used for the treatment of conjunctivitis includes: penicillin, streptomycin, tetracycline, chloramphenicol, gentamycin, erythromycin, and cloxacillin. Colxacillin was the best drug for staphylococcal while resistance of 30.9% was to chloramphenicol [12]. The etiologies and their antibiotic sensitivities pattern of ocular infections have been gradually changed over the years [12-14].

Little information about etiology and antimicrobial susceptibility pattern of ocular Infections is available in Jordan.  Therefore, this study was conducted to assess the causative organisms and antimicrobials susceptibility pattern of ocular infections pathogens isolated from children between January 2005 and December 2009, at Princess Rahmah Hospital in Irbid, Jordan. The importance of this study is to aid clinicians to facilitate the empiric treatment and management of children with symptoms of ocular infections. Moreover, the data would also help authorities to formulate antibacterial prescription policies.

Materials and Methods

This retrospective study was conducted on 154 children patients (< 15 years of age) with clinically diagnosed of ocular infections, at the Princess Rahmah Hospital in Irbid, Jordan between January 2005 and December 2009.  Data of microorganisms and antibacterial susceptibility were obtained from the records of clinical microbiology laboratory which filled in a prepared data sheet. The inferior conjunctival sac was swabbed in a single sweep for secretions or discharge with a sterile Dacron swab. Bacteriological specimens were processed and identified with standard cultures.   All isolates were tested for their susceptibilities to at least 12 out of 15 antimicrobials using antimicrobials diffusion discs [15]. Bacterial sensitivity was tested for the following antimicrobials: amoxicillin-clavulanic acid, ampicillin, cefaclor, cefixime, cephalothin, cotrimoxazole, ciprofloxacin, cefotaxime, gentamicin, oxacillin, piperacillin, tobramycin and vancomycin.    Data were analyzed statistically using SPSS (version 15 for Windows) program calculating the frequencies and cross tables.

This protocol was approved by the Ethics Committee of the ministry of health in Jordan (MOH, REC, 08, 0057).

Results

A total of 284 ocular samples obtained from children clinically diagnosed with ocular infections, was submitted for microbiological evaluation during the study period of 5 years. Of the 284 ocular specimens subjected to cultures, 154 (54.2%) had bacterial growth.

The predominant bacterial species isolated was Staphylococcus aureus (56.6%) followed by Streptococcus pneumoniae (14.9%). Klebsiella sp (12.9%), E. coli (9.1%), Pseudomonas (5.2%) and Moraxella (1.3%) (Table 1).

Table 1: Frequency of isolation of causative organisms of ocular infection in children

Total	Gender		2009	2008	2007	2006	2005	Organism
N (%)	Female (%)	Male (%)	N (%)	N (%)	N (%)	N (%)	N (%)
87 (56.6)	45	42	17 (58.6)	22 (56.4)	24 (72.8)	45.2))14	10 (45.4)	Staph. Aurous
23 (14.9)	9	14	6 (20.7)	5 (12.8)	3 (9.1)	5 (16.1)	4 (18.1)	Streptococcus
20 (12.9)	12	8	2 (6.9)	7 (18.0)	3 (9.1)	5 (16.1)	3 (13.6)	Klebsiella spp
14 (9.1)	10	4	0	2 (5.1)	2 (6.0)	6 (19.4)	4 (18.1)	Enterobacter spp
8 (5.2)	2	6	4 (13.8)	2 (5.1)	0	1 (3.2)	1 (4.5)	Pseudomonas
2 (1.3 )	1	1	0	1 (2.6)	1 (3.0)	0	0	Moraxella
154 (100.0)	79	75	29 (100.0)	39 (100.0)	33 (100.0)	31 (100.0)	22 (100.0)	Total

Over all isolates, ciprofloxacin was the most effective antimicrobial agent with susceptibility rate of 78.0%. The most of gram-positive isolates were susceptible to vancomycin (93.6%) followed by cefotaxime (84.3%), ciprofloxacin (78.0%), tobramycin (70.9%), amoxicillin-clavulanic acid (69.1%), cephalothin (65.7%), ampicillin (63.6%) and gentamicin (60.4%). The gram-negative organisms were susceptible in highest percentage to ciprofloxacin (77.7%) followed by tobramycin (48.1%) and cefotaxime (44.4%). The antimicrobial susceptibility of conjunctivitis isolates for 12 selected antimicrobial agents used in this study are summarized in (Table 2).

Table 2: Pattern of susceptibility to various antibiotics in children with ocular infection

Antimicrobial agent Number of tested isolates (%) susceptible						Year	Organism
COT	CLT	CF	CEC	AMP	AMC
5 (60.0)	3 (100.0)	4 (75.0)	4 (75.0)	4 (50.0)	4 (50.0)	2005	Gram –positive isolates
4 (50.0)	3 (33.3)	10 (60.0)	6 (66.6)	4 (50.0)	10 (90.0)	2006
21 (38.0)	19 (52.6)	20 (20.0)	16 (50.0)	21 (71.4)	24 (54.1)	2007
18 (33.3)	13 (84.6)	12 (0)	18 (50.0)	13 (53.8)	20 (80.0)	2008
19 (47.3)	0	15 (40.0)	13 (69.2)	18 (66.6)	10 (70.0)	2009
67 (41.7)	38 (65.7)	61 (31.1)	57 (57.8)	60 (63.6)	68 (69.1)	2005-2009
4 (50.0)	3 (33.3)	4 (0)	2 (50.0)	6 (33.3)	4 (25.0)	2005	Gram –negative isolates
4 (50.0)	3 (33.3)	4 (75.0)	4 (50.0)	6 (33.3)	7 (28.5)	2006
5 (20.0)	4 (25.0)	6 (50.0)	4 (75.0)	4 (25.0)	5 (40.0)	2007
4 (25.0)	6 (33.3)	7 (0)	6 (33.3)	6 (66.6)	9 (22.2)	2008
2 (0)	0	2 (0)	2 (0)	0	6 (0)	2009
19 (31.5)	16 (31.2)	23 (26.0)	18 (44.4)	22 (27.2)	31 (22.5)	2005-2009
9 (55.5)	6 (66.6)	8 (37.5)	6 (66.6)	10 (40.0)	8 (37.5)	2005	All pathogens
8 (50.0)	6 (33.3)	14 (64.2)	10 (60.0)	10 (40.0)	17 (64.7)	2006
26 (34.6)	23 (47.8)	26 (26.9)	20 (55.0)	25 (64.0)	29 (51.7)	2007
22 (31.8)	19 (68.4)	19 (0)	24 (45.8)	19 (42.1)	29 (62.0)	2008
21 (42.8)	2 (100.0)	17 (35.3)	15 (60.0)	18 (66.6)	16 (43.7)	2009
86 (39.5)	56 (57.1)	84 (29.7)	75 (54.6)	82 (53.6)	99 (54.5)	2005-2009

Amoxicillin-clavulanic acid (AMC), Ampicillin (AMP), Cefaclor (CEC), Cefixime (CF), Cephalothin (CLT), Ciprofloxacin (CPR),

Cotrimoxazole (COT), Cefotaxime (CTX), Gentamicin (GEN), Piprecillin (PIP), Tobramycin (TOB), Vancomycin (VAN).

Of twelve of tested antimicrobials, ciprofloxacin had the highest susceptibility rate (78.0%) for all tested isolates, followed by vancomycin (73.4%). Whereas, cefixime showed the lowest susceptibility rate of 29.7% (Table 2).

Table 2: Pattern of susceptibility to various antibiotics in children with ocular infection

Antimicrobial agent Number of tested isolates (%) susceptible						Year	Organism
VAN	TOB	PIP	GEN	CTX	CPR
3 (66.6)	8 (87.5)	10 (30.0)	9 (44.4)	4 (100.0)	10 (60.0)	2005	Gram –positive isolates
5 (80.0)	15 (86.6)	17 (35.3)	7 (57.1)	6 (83.3)	15 (40.0)	2006
12 (100.0)	10 (70.0)	5 (80.0)	26 (69.2)	25 (88.0)	20 (95.0)	2007
20 (95.0)	10 (70.0)	0	25 (52.0)	13 (76.9)	11 (81.8)	2008
7 (100.0)	12 (41.6)	6 (100.0)	14 (71.4)	3 (66.6)	17 (100.0)	2009
47 (93.6)	55 (70.9)	38 (50.0)	81 (60.4)	51 (84.3)	73 (78.0)	2005-2009
2 (50.0)	4 (25.0)	6 (50.0)	8 (12.5)	7 (14.2)	4 (50.0)	2005	Gram –negative isolates
2 (50.0)	8 (37.5)	9 (33.3)	8 (62.5)	10 (30.0)	6 (33.3)	2006
1 (0)	3 (100.0)	0	4 (100.0)	6 (66.6)	5 (100.0)	2007
8 (12.5)	6 (33.3)	0	12 (33.3)	9 (66.6)	10 (100.0)	2008
4 (0)	6 (66.6)	4 (50.0)	6 (66.6)	4 (50.0)	2 (100.0)	2009
17 (17.6)	27 (48.1)	19 (42.1)	38 (36.8)	36 (44.4)	27 (77.7)	2005-2009
5 (60.0)	12 (66.6)	16 (37.5)	17 (29.4)	11 (45.4)	14 (57.1)	2005	All isolates
7 (71.4)	23 (69.5)	26 (34.6)	15 (33.3)	16 (50.0)	21 (38.1)	2006
13 (92.3)	13 (76.9)	5 (80.0)	30 (73.3)	31 (83.8)	25 (96.0)	2007
28 (71.4)	16 (56.2)	0	37 (45.9)	22 (72.7)	21 (90.4)	2008
11 (63.6)	18 (50.0)	10 (80.0)	20 (70.0)	7 (57.1)	19 (100.0)	2009
64 (73.4)	82 (63.4)	57 (47.3)	119 (52.9)	87 (67.8)	100 (78.0)	2005-2009

Discussion

This current study provides information regarding the most common bacteria isolated from ocular specimens which was Staphylococcus aureus (56.6%) followed by Streptococcus pneumoniae (14.9%). These results are in agreement with other studies that reported S. aureus as the most common bacteria isolated from children with ocular infection. [2-4,16] While, Streptococcus pneumonia was the predominant agent of conjunctivitis followed by other microorganisms. [5] Though Staphylococci and Streptococci along with other bacteria like Pseudomonas, Moraxella are part of the normal flora of the conjunctiva, under appropriate conditions they cause infections.[17,18] Among gram-negative bacilli, the most common pathogen was Klebsiella spp (12.9%) followed by Enterobacter spp (9.1%) Pseudomonas spp. (5.2%) and Moraxella (1.3%). The gram-negative bacilli, Klebsiella spp., Enterobacter spp., etc., are found in soil and sewage and are opportunistic pathogens causing ocular infection when the host defenses are low. [19]

Sensitivity and resistance based on in vitro testing may not reflect true clinical resistance and response to an antibiotic because of the host factors and penetration of the drug.

In this study, vancomycin, cefotaxime and ciprofloxacin revealed a higher efficacy against gram-positive isolates compared with other antibacterial agents. Similar finding was reported for susceptibility pattern of conjuntivitis S. aureus isolates to vancomycin and ciprofloxacin. [20,21] Whereas, cefixime and cotrimoxazole showed the lower efficacy rate against gram-positive isolates.

However, gram-negative isolates showed high susceptibility rate to ciprofloxacin, while vancomycin showed the lowest efficacy. In addition, this study reveled that ciprofloxacin had a higher efficacy against both gram-positive and gram-negative isolates compared with other antibacterial agents. These findings for ciprofloxacin suggest that the behavior of these pathogens in our setting is the same as that reported in the international literature. [22-24]

Susceptibility rate of gram-negative isolates to all tested antimicrobial agents was lower than that of gram-positive isolates. This my due to over use of these antimicrobial agents in treatment of infection due to gram-negative bacteria [25]. The relationship between antibiotic use and resistance is complex. Improper selection of antibiotics, inadequate dosing and poor compliance to therapy may play as important a role in increasing resistance as their overuse. [21]

Medical literature has shown an increase in the incidence of antibiotic-resistant bacterial strains. Several cofactors have been implicated, among which the frequent use of antimicrobial agents is highlighted [7-9]

Conclusion

Ocular infection in children is mainly caused by Staphylococcus aureus organisms, which develop resistance to commonly used antimicrobials. This emergence of multiple drug resistance call for judicious antibiotic use to avoiding the development of further resistance to available agents for ocular infection. Its also calls for a continuous monitoring and reviewing of antimicrobial policy in the hospital and the country at large. The information provided in this study would also aid the clinician in formulating rationale-based decisions in the antibiotic treatment of bacterial ocular infections that cause major public health problems.
Moreover, the data would also help authorities to formulate antimicrobial prescription policies.

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