Microbial infection and antibiotic resistance patterns among Jordanian intensive care patients

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Asem A. Shehabi and Izdiad Baadran

ABSTRACT: Microbial infections were observed in 30% (155/519) of all patients consecutively admitted in 1993 to the adult intensive care unit in the Jordan University Hospital in Amman. Gram-negative bacteria were involved in 110 (49%), Gram-positive bacteria in 69 (31%), mixed bacteria species in 25 (11%) and Candida spp. in 19 (9%) of all 223 infection episodes. Five species were isolated most frequently: Staphylococcus aureus (40), Acinetobacter spp. (28) Pseudomonas spp. (22), Enterobacter spp. (20) and Klebsiella spp. (17). Resistance to most commonly available antibiotics was moderate to very high among Gram-positive and Gram-negative isolates. Almost all Gram-negative bacteria were sensitive to imipenem and ciprofloxacin.

L'infection microbienne et les schémas de résistance aux antibiotiques chez les malades des services des soins intensifs en Jordanie

RESUME: Des infections microbiennes ont été observées chez 30% (155/519) de l'ensemble des malades admis au service de soins intensifs pour adultes de l'Hôpital universitaire de Jordanie à Amman en 1993. Pour les 223 cas d'infection enregistrés en tout, il s'agissait dans 110 cas de bactéries à Gram négatif (49%), dans 69 cas de bactéries à Gram positif (31%), dans 25 cas d'espèces bactériennes associées (11%) et dans 19 cas de Candida spp (9%). Cinq espèces bactériennes ont été isolées plus fréquemment: Staphylococcus aureus (40), Acinetobacter spp (28), Pseudomonas spp (22), Enterobacter spp (20), et Klebsiella spp (17). La résistance à la plupart des antibiotiques couramment disponibles était de modérée à très forte parmi les isolats à Gram positif et négatif respectivement. Presque toutes les bactéries à Gram négatif étaient sensibles à l'imipénème et la ciprofloxacine.

Introduction

Infection caused by multidrug-resistant bacteria constitutes a serious problem for intensive care patients throughout the world [1-4]. The mortality rate associated with multidrug-resistant Gram-negative enteric bacteria in these patients is high in some intensive care units (ICUs). It is likely that patterns of microbial infection and antibiotic resistance in ICU patients differ widely from one hospital or country to another and are often facilitated by the increasing use of invasive techniques, immunosuppressive drugs and inappropriate antibiotic therapy [1,4-7]. In addition, certain types of pathogens are becoming common in each local community and represent an important risk factor for the morbidity and mortality of ICU patients [2,3,8].

Patients and methods

The objective of this study was to investigate the incidence of microbial infection in association with antibiotic resistance among patients consecutively admitted to the adult ICU in the Jordan University Hospital in Amman over a one-year period. Patients in the ICU were considered to have an infection when clinical findings were confirmed by any culture-positive clinical specimen taken after at least a 24-hour stay in the ICU.

All clinical isolates were first identified by conventional methods in a routine microbiology laboratory [9]. A large representative number of Gram-negative isolates were subsequently identified at the species level with API 20E and API 20NE (Bio Merieux Systems, France).

Antibacterial susceptibility testing was first performed for all isolates by a disk diffusion method on Mueller-Hinton agar [10]. Antibiotic disks were obtained from Biolife (Italy). Multiple bacterial isolates from a single patient with the same resistance patterns were considered as one isolate for studying minimum inhibitory concentration (MIC) using Micro Scan, Type TN dried panel (Baxter Health Care Corporation, West Sacramento, California, USA). Minimum inhibitory concentrations were interpreted according to approved break points [10].

Differences between groups were considered statistically significant if P values were < 0.05.

Results

During the one-year study, 519 consecutive patients were admitted to the ICU in the Jordan University Hospital. Of these, 155 (30%) showed evidence of infection as demonstrated by culture and clinical findings during their stay in the ICU.

The sites of infection and types of organisms recovered from the 155 patients are shown in Table 1. In all, 223 infection episodes were found in the clinically infected patients. Gram-negative bacteria were involved in 110 (49%; P < 0.05)of these episodes, Gram-positive bacteria in 69 (31%; P < 0.05), mixed bacteria species in 25 (11%) and Candida spp. in 19 (9%). The four leading sites of infection were skin and soft tissue (46%), respiratory tract (33%), urinary tract (14%) and blood (7%). The isolated pathogens, in descending order, were: Staph. aureus (40); Acinetobacter spp. (28); Pseudomonas spp. (22); Enterobacter spp.(20); coagulase-negative staphylococci (19); Candida spp. (19); Klebsiella spp. (17); Escherichia coli (15) and enterococcus (5).

The antibiograms of common isolates of Gram-negative bacteria using the minimum inhibitory concentration method are shown in Table 2. The majority of the isolates were highly resistant (66%-100%) to ampicillin and cephazolin, whereas resistance to other tested antibiotics varied (25%-90%) according to the species. However, most of these isolates were highly susceptible to imipenem and ciprofloxacin (0%-12% resistant) and to a less extent to amikacin (8%-29% resistant).

Coagulase-positive and -negative staphylococci were mostly moderately resistant to tested antibiotics except to penicillin drugs, where resistance was high (59%-83%) and to methicillin (35%- 42%). However, all staphylococci isolates were susceptible to vancomycin (Table 3).

Discussion

In this study, the infection rate among ICU patients due to monoorganism or polyorganisms was 30%. Gram-negative bacteria were significantly more involved in infections (49%; P < 0.05) than Gram-positive bacteria, mixed bacteria and candida isolates. It is well documented that the higher rates of infection and mortality among ICU patients are mostly related to factors such as exposure to invasive procedures, underlying disease conditions, duration of stay in the ICU, infection sites and association with nosocomial multidrug-resistant pathogens [1,3,6,8]. Our study included both major infection sites and types of organisms and their susceptibility to commonlyused antibacterial agents in the developing country of Jordan, but it did not attempt to investigate the underlying disease conditions of patients or the role of nosocomial infection.

The common infection sites in the present study were skin and soft tissue, followed by respiratory tract, urinary tract and blood. Species of Staphylococcus, Acinetobacter, Pseudomonas, Enterobacter, Klebsiella and Candida were the most prevalent pathogens recovered from our ICU patients (Table 1).

A multicentre study conducted in 13 European countries in 1992 [2] indicated that respiratory tract samples (39%) were the most frequent source of bacterial isolates, followed by blood (21%) and urinary tract samples (17%). The predominant bacterial isolates reported in the European study were similar to our results and Gram-positive isolates were found to account for about 35% of all isolates. The European study also revealed that the most common Gram-negative isolates were E. coli (17%), P. aeruginosa, (12%), K. pneumoniae (10%) and Enterobacter spp. (8%). Most of the available data on infections among ICU patients were collected in industrialized countries at least 10 years ago [10]. These studies reported overall infection rates and mortality rates between 10% and 50% [11,12].

Numerous studies have shown that multidrug-resistant bacteria, in particular aerobic Gram-negative bacteria, easily colonize the gastrointestinal tract and respiratory tract of hospitalized patients [6,11]. In addition, it is well known that multidrug-resistant bacteria are becoming increasingly prevalent in the hospital environment as a result of the extensive use of antibiotics [1-3,13]. The results of this study revealed that a few types of multidrug-resistant Gram-negative bacteria (A. baumanii, P. aeruginosa and K. pneumoniae) were the major cause of infection in our ICU patients during 1993. Many of the Gram-negative isolates were more than 25% resistant to the b-lactam drugs introduced in the early 1990s (ceftriaxone, ceftazidime, cefotaxime), and also to the much older aminoglycosides (amikacin, gentamicin, tobramycin). However, excellent activity against all Gram-negative isolates was shown for imipenem and ciprofloxacin. Neither of these drugs has been extensively used in the treatment of our patients. Of the other tested antibacterial drugs, only Augmentin and cefoxitin demonstrated excellent to good activity in vitro against K. pneumoniae, whereas aztreonam and piperacillin proved to be highly effective in vitro against P. aeruginosa. Reports from European countries and the United States of America indicate that extensive use of the new b-lactam and fluoroquinolone drugs has contributed to the rapid emergence of multidrug-resistant Gram-negative bacteria, particularly Klebsiella spp., Enterobacter spp., Pseudomonas spp. and Acinetobacter spp. [1,14-16].

The present study demonstrated that staphylococci, enterococci and fungi did not cause serious infections such as septicaemia or meningitis among our ICU patients.

In conclusion, we suggest that the most important strategies for controlling the problem of multidrug-resistant organisms in any ICU should be directed towards continuously monitoring the presence of these organisms, and the avoidance of excessive or continued use of any single drug over a long period of time.

Acknowledgement

This study was supported in part by Merck Human Division, Amman, Jordan.

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