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Brazilian Journal of Pharmaceutical Sciences

On-line version ISSN 2175-9790

Braz. J. Pharm. Sci. vol.52 no.3 São Paulo July/Sept. 2016 


Antimicrobial susceptibility patterns among bacteria isolated from intensive care units of the largest teaching hospital at the northwest of Iran

Hadi Hamishehkar1 

Pegah Shadmehr2 

Ata Mahmoodpoor3 

Simin Ozar Mashayekhi4 

Taher Entezari-Maleki1  5  * 

1Applied Drug Research Center, Tabriz University of Medical Sciences, Tabriz, Iran

2Student Research Committee, Tabriz University of Medical Sciences, Tabriz, Iran

3Faculty of Medicine, Tabriz University of Medical Sciences, Tabriz, Iran

4Tabriz Health Services Management Research Center, Tabriz University of Medical Sciences, Tabriz, Iran

5Cardiovascular Research Center, Tabriz University of Medical Sciences, Tabriz, Iran


This study was conducted to determine the antimicrobial susceptibility patterns among common pathogens in the intensive care units (ICUs) of a university hospital in northwestern Iran. A retrospective study was done on laboratory records of patients with nosocomial infection who were admitted to five ICUs of Imam Reza Hospital during a 21-month period from March 2010 to January, 2012. A total number of 556 isolates from 328 patients were evaluated. The most common sites of infections included respiratory (51.7%), urinary (24.8%), and blood (10.4%). The most frequently isolated microorganisms were Enterobacter aerogenes (50.6%) followed by Escherichia coli (16.7%) and Pseudomonas aeruginosa (7.5%). Staphylococcus aureus was the most frequent pathogen among gram-positives (39.7%). The rate of methicillin-resistant Staphylococcus aureus (MRSA) was 87.5%. Multidrug-resistant (MDR) gram-negative bacteria were documented in 25.8% of Acinetobacter, 20% of Klebsiella, and 16.6% of Pseudomonas. The most active antimicrobials were vancomycin (93.5%) followed by amikacin (71.5%) and gentamicin (46%). The overall antibiotic susceptibility was as follows: 36% ciprofloxacin, 19% imipenem, 20% trimethoprim-sulfamethoxazole, 20.5% ceftazidime, and 12% ceftriaxone. Due to the high rate of antimicrobial resistance in the ICU setting, more surveillance and control of the use of antimicrobials is needed to combat infections.

Uniterms: Intensive care units/anti-infective agents/cross infection; Hospital University/Iran.


Patients admitted to intensive care units (ICUs) are more vulnerable to various nosocomial infections because of their underlying illnesses and exposure to various invasive medical devices (Jatin, Mary, 2012; Archibald et al., 1997; Fridkin, 2001; Kollef, Fraser, 2001; Rhomberg et al., 2006).

Hospital infections affect approximately two million patients annually and lead to 90,000 deaths and a cost of $4.5 to $5.7 billion according to reports from the United States (Weinstein, 1998; Jarvis, 2001). They involve 5-10% of ICU patients (CDC, 1992; Stone, Larson, Kawar, 2002).

Antibiotics are the mainstay tools in the management of infections. Disappointingly, a number of studies have reported inappropriate uses of antimicrobials as well as the emergence of antibiotic resistance in most parts of the world (Tunger et al., 2009; Bergman et al., 2006). Today, the emergence of multidrug-resistant (MDR) gram-negative and methicillin-resistant Staphylococcus aureus (MRSA) pathogens has become a major public health concern. Moreover, they negatively influence patients' outcomes and increase the length of hospital stays and healthcare costs (Giske et al., 2008; De Kraker et al., 2011; Resch, Wilke, Fink, 2009; Mulvey, Simor, 2009).

Many studies have also showed that controlled use of antibiotics leads to improved microorganism sensitivity to antimicrobial agents (Lee et al., 2010; Takesue et al., 2010). The emergence of resistant pathogens and their negative impact on patient survival and healthcare costs need the evaluation of antimicrobial susceptibility in each health center and hospital in order to control infection. Therefore, this study assessed antimicrobial susceptibility patterns in the ICUs of the largest teaching hospital in northwestern Iran. To the best of the authors' knowledge, this is the first report of bacterial resistance in ICUs at this location.


Study Design and Setting

A retrospective study was done on laboratory records of the positive cultures patients with nosocomial infection who were admitted at the five ICUs of Imam Reza Hospital, a 500-bed tertiary care hospital affiliated to Tabriz University of Medical Sciences during a 21-month period (March 2010 to January 2012). This study was approved in the ethic committee of the university.

Data and Sample Collection

For doing the study a questionnaire form was designed in order to record patients' data included age, sex, file number, ward, culture results, site of infection, diagnostic species, and antibiogram test results. Prescribed drugs for ICU cultures were demonstrated using the hospital information system (HIS). All samples were taken in aseptic conditions. The sources of specimen included blood, urine, sputum, bronchial washing, wound, catheter, cerebrospinal fluid (CSF), tracheal, peritoneal, pleural, and synovial fluids.

Antimicrobial Susceptibility Testing

The Kirby-Bauer disk diffusion method was used to test antimicrobial susceptibility (in Mueller-Hinton agar medium, Merck, Germany) according to the guidelines of the National Committee for Clinical Laboratory Standards (NCCLS, 1997).

The performed antibiogram disks (Himedia laboratories, Mumbai, India) included vancomycin (V, 30 mcg), ciprofloxacin (CIP, 5 mcg), clindamycin (CD, 2 mcg), trimethoprim-sulfamethoxazole(SXT, 30 mcg), gentamicin (GM, 10 mcg), ofloxacin (OFX, 5 mcg), penicillin G (P, 10 mcg), oxacillin (OXA, 5 mcg), amikacin (AMK, 30 mcg), cefotaxime (CTX, 30 mcg), ceftazidime (CAZ, 30 mcg), ceftriaxone (CTR, 30 mcg), cefazolin (CZ, 30mcg), chloramphenicol (CHL, 30 mcg), piperacillin (PIP, 100 mcg), imipenem (IPM, 10mcg), nitrofurantoin (FM, 50 mcg), ampicillin (AM, 10 mcg) and rifampin (RIF, 5 mcg).

Determination of Pattern of Antibiotic Prescriptions

A clinical pharmacist and two intensive care sub-specialists evaluated the appropriateness of prescribed antibiotics based on result of each isolated cultures from ICU patients.

Patterns of antibiotic prescription based on culture results were divided into four groups: Group 1) Adherence with culture results, according to culture the drug is added or discontinued. Group 2) Not adherence with culture results as follows: 2-1) No change in medication; While, culture results showed resistance to antibiotics or following antibiotic therapy. We need to change the antibiotics but physician did not notice to culture results and antibiotics continued. 2-2) inappropriate changes in medication: the doctor noticed that you need to change the antibiotic, but changes were not accordance to protocols and appropriate drug that affect antibiotic therapy to improve patient has not chosen.

Group 3) rational change without culture result guide: due to the lack of laboratory antibiogram test for all antibiotics, a rationale prescription of drugs by doctors was made.

Group 4) No judgment: Because there was no complete transparency in the medical record for patient, judgment in this case considered impossible by experts.

Antibiotics utilization rates in ICUs were determined by Defined Daily Dose (DDD) per 100 bed-days.

Data Analysis

Data were processed in SPSS 16. Results were shown as standard deviation for quantitative variables and percentage for categorical variables.


A total number of 556 cultures isolated from 328 patients who were admitted at the five ICUs of the hospital were included in the study. Of which, 55.5% (n=182) were males and 44.5% (n=146) were females. The mean (SD) forage of the patients was 54± 19.5 years old. Data were collected from the five ICUs of the hospital as follows: 31.1% (n=102) from brain ICU, 22.6% (n=74) neurology ICU, 28.4% (n=93) lung ICU, 16.5% (n=54) surgery ICU and 1.5% (n=5) from the general ICU. As shown, the brain ICU has the greatest number of patients.

The most common sites of infection included respiratory (40.6%), urine (24.8%) and blood (10.4%) followed by sputum (4.7%), CSF (4.7%), plural (3.9%), bronchial washing (3.6%), catheter (2.7%), abscess (2.2%), wound (2%), peritoneal (0.4%) and synovial (0.2%) specimen. The result of Gram staining showed that the majority of cultured samples (86.8%, n=483) were Gram-negative bacteria as well as 13.2% (n=74) were Gram-positive.

The most frequently isolated microorganisms were Enterobacter aerogenes (50.7%, n= 282) followed by Escherichia coli (16.7%) and Pseudomonas aeruginosa (7.5%). The prevalence of isolated microorganisms is given in Table I.

TABLE I Bacterial typing of ordered cultures Bacterial type 

Among Gram-positives, Staphylococcus aureus was the most frequently isolated pathogen (39.7%, n=29) followed by Staphylococcus epidermidis. Susceptibility rates of Gram-positive and Gram-negative microorganisms are shown in Table II and III respectively. Based on these findings, rate of methicillin resistance Staphylococcus aureus (MRSA) was 87.5%. However, all cases of Staphylococcus aureus and 90% of Staphylococcus epidermidis were sensitive vancomycin.

TABLE II Susceptibility rates of the most common Gram-positive cocci isolated from the ICUs 

R= Resistant, S= Sensitive, - = Not measured or not reported, AMP= Ampicillin, IPM= Imipenem, AMK= Amikacin, GEN= Gentamicin, CHL= Chloramphenicol, SXT= trimethoprim-sulfamethoxazole, NIT= Nitrofurantoin, CIP= Ciprofloxacin, CLI= Clindamycin, VAN= Vancomycin, RIF= Rifampine, A= Oxacillin, PEN= Penicillin, CEF= Cefazolin.

TABLE III Susceptibility rates of Gram-negative bacilli isolated from the ICU 

R= Resistant, S= Sensitive, - = Not measured or not reported, AMK= Amikacin, GEN= Gentamicin, SXT= trimethoprim-sulfamethoxazole, CIP= Ciprofloxacin, CHL= Chloramphenicol, CET= Ceftriaxone, CTX= Cefotaxime, CAZ= Ceftazidime, AMP= Ampicillin, IPM= Imipenem, OXA= Oxacillin, CEZ= Ceftizoxime, NIT= Nitrofurantoin, VAN= Vancomycin, CLI= Clindamycin, PEN= Penicillin, PIP= piperacillin.

In the present study, multidrug resistant (MDR) Gram-negative bacilli were documented in 25.8% of Acinetobacter, 20% of Klebsiella and 16.6% of Pseudomonas. The susceptibility rate of Enterobacter, Escherichia coli and Pseudomonas aeruginosa to imipenem were 16.4%, 16.6% and 46% respectively. These rates for ciprofloxacin were 34.5%, 43.5%, and 56.5% and to amikacin were 64.5%, 88%, and 62.5% respectively. Regarding gentamicin, these susceptibility rates were 42.5%, 53.7%, and 38.5% respectively.

Overall susceptibility rates of the microorganisms isolated from the ICUs are also shown in table IV. The most active antimicrobials were vancomycin (93.5%) followed by amikacin (71.5%) and gentamicin (46%). The overall susceptibility of isolated microorganisms to regular important antibiotics was as follows: 36% for ciprofloxacin, 19% for imipenem, 20% for trimethoprim-sulfamethoxazole, 20,5%for ceftazidime, and 12% for ceftriaxone.

TABLE IV Overall susceptibility rates of the microorganisms isolated from the ICUs 

AMK= Amikacin, GEN= Gentamicin, SXT= trimethoprim-sulfamethoxazole, CIP= Ciprofloxacin, CHL= Chloramphenicol, CET= Ceftriaxone, CTX= Cefotaxime, CAZ= Ceftazidime, AMP= Ampicillin, IPM= Imipenem, OXA= Oxacillin, CEZ= Ceftizoxime, NIT= Nitrofurantoin, VAN= Vancomycin, CLI= Clindamycin, PEN= Penicillin, PIP= piperacillin.

The most Staphylococcus strains were observed in lung and blood samples (31% and 17.2% respectively).

Enterobacter and E.coli were the most commonly isolated pathogens from urine samples (37.7% and 36.2% respectively as well as the most frequently isolated microorganisms from lung samples were Enterobacter (52.7%) followed by Pseudomonas aeruginosa (10.2%) and Acinetobacter (9.1%). Entrobacter aerogenes was the most common strain in all samples. Entrobacter aerogenes and E.coli was the most commonly detected microorganisms in most ICUs.

Pattern of antibiotic prescription showed that only 22.5% of prescriptions were in accordance with culture results and 34.5% were not adherence with culture results. Moreover, in 38% of prescriptions logical changes were made without culture result guide. In 5%, no judgment could be made.

The rate of antibiotics utilization included as follows: ciprofloxacin (8.7mg per 100 bed-days), meropenem (5.4 mg per 100 bed-days), cefepime (4.2 mg per 100 bed-days), imipenem (3.1 mg per 100 bed-days), ceftazidime (1.9 mg per 100 bed-days), amikacin (0.9 mg per 100 bed-days), gentamicin (0.8 mg per 100 bed-days), ceftriaxone (8 mg per 100 bed-days), vancomycin (4.3 mg per 100 bed-days), piperacillin-tazobactam (2.8 mg per 100 bed-days).


To the best of the authors' knowledge, this is the first report from the ICUs of the largest teaching hospital in northwestern Iran. The result of this study highlighted the important key role of rational prescription of antibiotics. This matter becomes more important when it concerns the emergence of antimicrobial resistance produced by gram-negative bacilli and MRSA strains (Giske et al., 2008; De Kraker et al., 2011; Resch, Wilke, Fink, 2009; Mulvey, Simor, 2009). Hence, the detection of antimicrobial resistance patterns in every hospital plays an important role in the management of infections.

Hospital-acquired infections are life-threatening conditions that involve patients, especially those admitted to ICUs. Respiratory pathogens are responsible for about one-third of ICU infections (Garner et al., 1998; Flanders, Collard, Saint, 2006). In the present study, the most common site of infection was the respiratory tract (51.7 %); this result is in agreement with other studies conducted indifferent countries including Turkey (38.8 %) (Gunseren et al., 1999), India (29.7%) (Orrett, 2002), Oman (65%) (Al-Lawati, Crouch, Elhag, 2000), Italy (91%) (Bassetti et al., 2012), the United States (54.4%) (Streit et al., 2004), and a separate report from Iran (70.6%) (Mohammadtaheri et al., 2010).

The SENTRY Antimicrobial Surveillance Program which included 25 ICUs in Europe (1997-1998) and North America (2001) reported S. aureusas the most common pathogen in developed countries followed by P. aeruginosa and E. coli (Streit et al., 2004; Fluit et al., 2001). However, this pattern in developing countries such as Brazil (Mendes et al., 2005), Turkey (Kucukates, 2005), Iran (Mohammadtaheri et al., 2010), and other Middle Eastern countries were documented as Pseudomonas and Acinetobacter (Aly, Al-Mousa, Al Asar, 2008; Bayram, Balci, 2006). In the present study, Enterobacter aerogenes followed by E. coli and P. aeruginosa were the organisms most frequently recovered from ICUs. In a Serbian report, Enterobacter strains were the bacteria most commonly isolated from ICUs (Djordjevic et al., 2012).

In the current study, Escherichia coli (36.2%) and Enterobacter aerogenes (52.7%) were the isolates most commonly found in urinary and respiratory tracts. These findings are in agreement with those of the study conducted by Streit et al. in North America (Streit et al., 2004). However, in a report from Oman, Escherichia coli and Pseudomonas aeruginosa were the pathogens most commonly found in the urinary and respiratory tracts of ICU patients (Al-Lawati, Crouch, Elhag, 2000). Whereas, Klebsiella and Pseudomonas were the microorganisms most commonly found in the urine of patients admitted to the ICU of Imam Khomeini Hospital in Tehran (Hadadi et al., 2008).

In the current study, 86.2% of microorganisms isolated from urine were gram-negative bacteria. This finding is in line with a 2003 NNIS study that showed the highest rates of gram-negative infections to be in urine (Gaynes, Edwards, 2005).

The most common gram-positive organisms recovered from the ICUs in this study were S. aureus followed by S. epidermidis. This result is in agreement with the findings of Mohammadtaheri et al. (2010) and Khalili et al. (2012) in their studies conducted in ICU and infectious ward settings in Iran. ().

In the present study, MRSA made up 87.5% of all S.aureus isolates. This rate is higher than those reported from Canada (CAN-ICU study) (22.3%) (Zhanel et al., 2008), Europe (39%) (Fridkin, 2001), and the USA (55%) (Styers et al., 2006), but it is comparable with the report from Turkey (82%) (Bayram, Balci, 2006). Also, the rate of MRSA in the current study is lower than that report separately from Iran (96.2%) (Mohammadtaheri et al., 2010).

All MRSA isolates in the current study were susceptible to vancomycin; this is in line with the report from Iran and the CAN-ICU study (Mohammadtaheri et al., 2010; Khalili et al., 2012; Zhanel et al., 2008). The other active agent against MRSA was trimethoprim-sulfamethoxazole (46.7%); this result is similar to that of Mohammadtaheri et al. (51.9%) (Mohammadtaheriet al., 2010), but it is far from that of the CAN-ICU study (11.7%) (Zhanel et al., 2008).

Currently, MRSA is an emerging problem associated with a higher rate of mortality and increased durations of hospitalization and healthcare costs (Giskeet al., 2008; De Kraker et al., 2011).This higher rate of MRSA should raise the concerns of health authorities and lead to a larger battle against the propagation of infections.

In the present investigation, the resistance rate of pathogens to imipenem was documented in more than 80% of isolates; this rate is higher than those of Belgium (13%) (Glupczynski et al., 2001), Poland (8%) (Patzer, Dzierzanowska,Turner, 2002), and Turkey (20.8%) (Kucukates, 2005).

Recent data from Iran revealed that the resistance of microorganisms to imipenem has increased. The susceptibility rates of pathogens to imipenem in earlier studies from Iran were about 98% and 87.5% in 2006 and 2008, respectively (Vessal et al., 2006; Hadadi et al., 2008). In 2010, however, the authors of the current study reported the decline of these rates to 2-37% and 19%, respectively (Mohammadtaheri et al., 2010). Accordingly, it may be concluded that the appearance of pathogens resistant to imipenem is increasing in Iran with the passing of time and consumption of the drug.

Antimicrobial resistance to ciprofloxacin was documented in 65% of cases. This rate in reports from Iran, Turkey, and Belgium was 76%, 29%, and 21%, respectively (Kucukates, 2005; Hadadi et al., 2008; Glupczynski et al., 2001).

The overall resistance rate of antimicrobials was higher in the current study than in other reports (Gunseren et al., 1999; Mendes et al., 2005; Styers et al., 2006; Patzer, Dzierzanowska, Turner, 2002; Gonlugur et al., 2004; Karlowsky et al., 2003). Moreover, the resistance rate to cephalosporins (79.5%-87.8%) was comparable to that in Iran (Hadadiet al., 2008), but higher than reported in foreign studies (Gunseren et al., 1999; Al-Lawati, Crouch, Elhag, 2000; Glupczynski et al., 2001; Patzer, Dzierzanowska,Turner, 2002; Gonlugur et al., 2004; Karlowsky et al., 2003; Meric et al., 2005).

Current results also showed that 25.8% of Acinetobacter, 20% of Klebsiella, and 16.6% of Pseudomonas were an MDR gram-negative pathogen. In one study from Turkey from 2000 to 2002, 45.4% of Acinetobacters and 37.7% of P. aeruginosa isolates were MDR (Yaman et al., 2004). In another study conducted in Iran, 80% of Acinetobacter and 59% of Klebsiella isolates were MDR (Hadadi et al., 2008). In the Karlowsky et al. (2003) study, among Acinetobacter isolates, the MDR rate was 11.6-24.2%.

MDR gram-negative bacilli-related infections have become a major, rising problem (Thomson, Bonomo, 2005). Despite the growth of MDR strains, very few antimicrobials have been developed to combat these infections (Rubinstein, Vaughan, 2005). The growing body of evidence also proves the development of resistant gram-negative infections without adequate therapeutic options (Falagas et al., 2005). Moreover, MDR gram-negative infections are associated with increased mortality rates, extended durations of hospitalization, and higher healthcare costs (Bergman et al., 2006).

At the end, the results of the present study showed a higher rate of antimicrobial resistance patterns in the ICUs of the largest referral tertiary teaching hospital in northwestern Iran. The irrational use of antibiotics reported in this study may partially justify these results. Therefore, detecting and managing bacterial resistance should be given more attention by clinicians as an important part of any infection control program. Additionally, the development of antibiotic stewardship programs in hospitals, encouragement of rational antibiotic use, and national and local antibacterial surveillances and control programs are recommended to reduce the development of resistant strains and encourage the successful management of infections.

This study has some limitations. Because of its retrospective design, access to clinicians and a medical menu was not possible. Therefore, a clinical judgment about the administration of antibiotics in some cases was not applicable.


This study showed a higher rate of bacterial resistance in the ICUs of a tertiary teaching hospital in Iran. Due to the emergence of resistant microorganisms in ICUs and considering the critical condition of patients in such a setting, more surveillance and control of the use of antibiotics is needed to combat infections.


The authors would like to thank Student Research Committee of Tabriz University of Medical Science and Imam Reza hospital staffs for supporting this study.


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FUNDING/SUPPORT None declared.

Received: July 18, 2014; Accepted: May 17, 2016

*Correspondence: T. Entezari-Maleki. Cardiovascular Research Center, Faculty of Pharmacy. Tabriz University of Medical Sciences, Tabriz, Iran, Daneshgah Street, 55617, Tabriz, Iran. E-mail:


The authors declare no conflicts of interest.


All authors contributed to the content, drafting, critical revision and approval of this manuscript. We confirm all patient/personal identifiers have been removed or disguised so the patient/person(s) described are not identifiable and cannot be identified by analyzing the details of these cases.

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