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International Journal of Antimicrobial Agents 14 (2000) 161 164 www.ischemo.

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Short communication

Antimicrobial susceptibility patterns of bacteria at the Makassed General Hospital in Lebanon


T.J. Shaar *, R. Al-Hajjar
Department of Laboratory Medicine, Makassed General Hospital, P.O. Box 6301, Beirut, Lebanon Received 30 January 1998; received in revised form 25 August 1998

Abstract Bacterial resistance to various antimicrobial agents is most common in areas with high usage of antibiotics such as in countries where over-the-counter availability promotes usage. In Lebanon, information about bacterial resistance to antimicrobial agents is limited. In this study, data on the antimicrobial susceptibility patterns have been collected for the last 7 years in addition to the rst 6 months of 1996 at the Makassed General Hospital in Lebanon. Enterobacteriaceae and Pseudomonas species proved to have high but variable rates of multidrug resistance. Among Staphylococcus aureus isolates, 17% were resistant to methicillin. A high percentage of resistance to penicillin (7688%) was noted among Streptococcus pneumoniae. These resistance patterns were generally comparable with those of other medical centres. 2000 Elsevier Science B.V. and International Society of Chemotherapy. All rights reserved.
Keywords: Antibiotic overuse; Antibiotic resistance; Data comparison

1. Introduction Bacterial resistance to antimicrobial agents has been increasing over the last few years due to many factors, including the overall increase in the number of prescriptions for antibiotics [1]. The multiresistant bacteria that cause problems in hospitals are staphylococci, enterococci and the Gram negative rods. In contrast, Staphylococcus aureus, pneumococci, gonococci, mycobacteria, shigella and invasive Salmonella species are the classic pathogens that are responsible for the resistance problems in the community, particularly in countries where antibiotic availability and use is not well regulated [2,3]. This study will focus on antimicrobial susceptibility patterns of bacterial isolates at the Makassed General Hospital (MGH) in Lebanon for 7 years up to and including the rst 6 months of 1996.

2. Materials and methods

2.1. Study location


The antimicrobial susceptibility tests were done in the clinical laboratories of the MGH. The latter is a 200 bed teaching hospital that provides medical care to all age groups. In 1995, the hospital had 10 088 admissions and 20 629 cases treated at the Emergency Unit.

2.2. Bacterial isolates


Bacteria that were recovered from culture and considered having medical pathogenic importance were each tested for the appropriate antimicrobial susceptibility discs. The routine laboratory methods were used to identify bacterial species according to the standard laboratory procedures [4]. Further tests were performed for some species using API 20E, API 20NE and API NH systems (bioMerieux, Marcy lEtoile, France). Identical isolates for the same patient and site were excluded.

* Corresponding author. Fax: +961-646589. E-mail address: mghadmin@cyberia.net.lb (T.J. Shaar)

0924-8579/00/$20 2000 Elsevier Science B.V. and International Society of Chemotherapy. All rights reserved. PII: S 0 9 2 4 - 8 5 7 9 ( 9 8 ) 0 0 0 1 9 - 3

162 T.J. Shaar, R. Al-Hajjar / International Journal of Antimicrobial Agents 14 (2000) 161164

Table 1 Antimicrobial susceptibility pattern of Gram-negative bacteriaa Antibiotics E. coli 6763 Enterobacter species 537 70 8175 50 7167 8669 1423 8089 10090 10081 5582 6084 6050 Proteus species 1060 5038 91 100 9078 98100 100 8889 6658 100 100 9998 10097 9588 9490 5271 H. inuenzae 635 8884 100 10093 10094 100 100 100 10097 8570 100 100 10098 10099 10099 Acinetobacter species 713 3313 4613 222 533 372 10036 838 5710 375 Salmonella species 140 96100 100 100 100 100 100 100 Pseudomonas species 2387 8186 86 4649 9384 5657 10090 10072 6870 9583 9273 7876 Klebsiella species 1927 9571 5968 10089 8177 9884 9890 9094 10085 10097 9788 9883 9074 9174 7965

Ampicillin Co-amoxiclav Piperacillin Aztreonam Cefamandole Cefotaxime Ceftazidime Ceftriaxone Cefuroxime Cephalexin Noroxacin Ooxacin Perloxacin Amikacin Gentamicin Tobramycin Trimethprim/ sulphamethoxazole

2924 83 6353 10090 8376 100 9998 9097 10096 10095 8293 9998 9395 9598 5952

100 100 100 95100 95100 100

a The ranges of highest and smallest percentages of susceptible strains from 1989 to 1995 including the rst 6 months of the year 1996. Only urine specimens were tested for noroxacin and trimethoprim/sulfamethazole.

T.J. Shaar, R. Al-Hajjar / International Journal of Antimicrobial Agents 14 (2000) 161164

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2.3. Antimicrobial susceptibility testing


Commercially available antibiotic discs (Sano Diagnostics Pasteur, Marnes-la-Coquette, France; Becton Dickinson, Cockeysville, USA; BioMerieux sa, Marcy lEtoile, France. Oxoid, Hampshire, UK) and Mueller Hinton agar (Becton Dickinson) were used to do the antimicrobial susceptibility testing according to the standardized disk diffusion method recommended by the US Food and Drug Administration [5] and by the National Committee for Clinical Laboratory Standards (NCCLS) [6]. The quality of performance was controlled using the following reference strains: Escherichia coli (American Type Culture Collection (ATCC) 25 922), Pseudomonas aeruginosa (ATCC 27 853) and Staphylococcus aureus (ATCC 25 923) and results were satisfactory. The plates were incubated at 37C for 18 24 h. For Staphylococcus species, when tested for oxacillin, the plates contained 4% NaCl and were incubated at 35C so to identify the methicillin-resistant Staphylococci. The results were interpreted as susceptible, intermediate susceptible, or resistant according to the inhibition zone diameter criteria of the NCCLS [6].

3. Results and discussion Tables 1 and 2 show the antimicrobial susceptibility of each species against various antimicrobial agents (19891996). Changes in antimicrobial resistance have occurred here over the last few years especially for some highly resistant pathogenic species [7 9]. Escherichia coli has lost susceptibility to ampicillin and some cephalosporins. About 48% are resistant to trimethoprim-sulphamethoxazole, which is comparable with results of Saudi Arabia, South America and Thailand [10] but not with those of USA where resistance is still low (6% in 1993) [7].
Table 2 Antimicrobial susceptibility pattern of Gram-positive bacteriaa Antibiotics Penicillin Ceftriaxone Cephalexin Clindamycin Methicillin Oxacillin Ooxacin Tobramycin Vancomycin Staph. aureus 1671 Str. pneumoniae 1329 7688 100 6055 9484 2219 7594 6246 100

10091 83b 9574 10098 9792 100

a The ranges of highest and smallest percentages of susceptible strains from 1989 to 1995 including the rst 6 months of the year 1996. b In the year 1995.

The number of plasmid-mediated extended-spectrum cephalosporinases in Klebsiella species has increased dramatically [11] and this may explain the increased resistance to ceftazidime (16% at MGH in the rst 6 months of 1996 and 11% at the American University of Beirut Medical Center (AUBMC) in 1993) and to other i-lactams (piperacillin 32%). Serratia marcescens, Enterobacter, Citrobacter and Proteus species exhibited recently resistance against most antimicrobial agents. Most resistance of Enterobacter to i-lactams is due to constitutive i-lactamases [12] and this may explain the 2535% resistance to the third generation cephalosporins. Salmonella species were still susceptible to most antimicrobial agents. Shigella exneri were still susceptible to the third generation cephalosporins and uoroquinolones but had lost susceptibility to ampicillin and chloramphenicol. These results agree with those of other hospitals in Lebanon and in the Middle East [7]. Pseudomonas species showed increasing resistance for aminoglycosides and i-lactams; aztreonam (424%), piperacillin (1434%) and quinolones (1025%). Resistance to ceftazidime increased (16% in the rst 6 months of 1996) [9]. Resistance of Pseudomonas species was comparable with that of the American University of Beirut [7]. Xanthomonas maltophilia showed high resistance to all antibiotics and particularly to imipenem. Acinetobacter species were resistant to almost all antibiotics with the exception of imipenem which is now the treatment of choice. The increased prevalence of i-lactamase-producing strains of Haemophilus inuenzae contributed to the increasing resistance to ampicillin [9] (16% for the rst 6 months of 1996). Methicillin-resistant Staphylococcus aureus (MRSA). These strains are often resistant to other antibiotics in addition to methicillin and the options for antibiotic therapy in patients infected with MRSA are limited, [1315]. Streptococcus pneumoniae showed a stable but high percentage of susceptibility to penicillin (7688%) over the last 7 years [16]. Streptococcus pyogenes, has remained susceptible to the tested antimicrobial agents. Penicillin resistance has not been described so routine susceptibility tests are not needed [17]. Other Streptococci including groups B and D were highly susceptible to ampicillin and to cephalosporins. Of 35 isolates of Streptococcus group D, only one was resistant to vancomycin. The patient infected with a drug-resistant organism is more likely to require hospitalization and has a longer hospital stay and has an increased risk of death [18]. Resistance also requires the need to use more toxic or

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T.J. Shaar, R. Al-Hajjar / International Journal of Antimicrobial Agents 14 (2000) 161164 fourth edition. Approved standard M2 A4. National Committee for Clinical Laboratory Standards, Villanova, Pa, 1990. Araj GF, Uwaydah MM, Alami SY. Antimicrobial susceptibility patterns of bacterial isolates at the American University Medical Center in Lebanon. Diagn Microbiol Infect Dis 1994;20:1518. Farrar WE. Antibiotic resistance in developing countries. J Infect Dis 1985;152(6):1103 6. Neu HC. The crisis in antibiotic resistance. Science 1992;257:1064 73. Murray BE, Alvarado T, Kim KH, et al. Increasing resistance to trimethoprim-sulfamethoxazole among isolates of Escherichia coli in developing countries. J Infect Dis 1985;152(6):110713. Rice LB, Carias LL, Bonomo RA, Shlaes DM. Molecular genetics of resistance to both ceftazidime and i-lactam-i-lactamase inhibitor combinations in Klebsiella pneumoniae and in vivo response to i-lactam therapy. J Infect Dis 1996;173:151 8. Jacoby GA, Archer GL. New mechanisms of bacterial resistance to antimicrobial agents. New Engl J Med 1991;324(9):60112. Abdo RA, Araj GF, Talhouk RS. Methicillin resistant Staphylococcus aureus (MRSA): disease spectrum, biological characteristics, resistant mechanisms and typing methods. J Med Liban 1996;44(1):21 30. McNeil M, Solomon S. The epidemiology of methicillin-resistant Staphylococcus aureus. Antimicrob Newslet 1985;2(7):49 56. Boyce JM, Causey WA. Infect Control 1982;3:377 83. Redondo E, Clynes N, Hofmann J. Drug-resistant Streptococcus pneumoniae. New Engl J Med 1996;334(1):53 5. Thornsberry C. Antimicrobial susceptibility testing: general considerations. In: Balows A, Hausler WJ, Herrmann KL, Isenberg HD, Shadomy HJ, editors. Manual of Clinical Microbiology, 5th edn. Washington: American Society for Microbiology, 1991:1059 1064. Homberg SD, Solomon SL, Blake PA. Health and economic impacts of antimicrobial resistance. Rev Infect Dis 1987;9:1065 78. Levy SB, Burke JP, Wallace CK. Antibiotic use and antibiotic resistance worldwide. Rev Infect Dis 1987;9:3.

more expensive antibiotics [19]. Resistance affects the antibiotic options available to every practitioner and is a problem in the developing countries [12]. Resistance can be reduced not only by the prescriber but also by adherence to control of infection practices and improved drug regulation.

[7]

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Acknowledgements We thank Dr R. Moghnieh for her constructive comments.


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