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Antimicrobial Resistance and Sensitivity among Isolates of Klebsiella pneumoniae from Hospital Patients in Turkey.



Klebsiella pneumoniae bacteria are significant agents of urinary system infections, upper respiratory tract infections and nosocomial infections. The aim of this study was to determine the antibiotic resistance to K. pneumoniae strains isolated in Microbiology Laboratory of different hospitals in Kahramanmaras between 2006-2007. Urine, vaginal fluid, wound, cerebrospinal fluid, blood, which send from various clinics were inoculated both Mac Conkey agar and Eosin Methylen Blue (EMB) agar. Twenty two K. pneumoniae were tested. Antibiotic resistance was determined by agar disc diffusion method using Mueller-Hinton agar according to Clinical and Laboratory Standards Institute recommendations and the production of b- lactamase was detected with the iodometric slide test. The Multiple antibiotic resistance (MAR) index values among 22 K. pneumoniae isolates were calculated.

The results indicated that resistance rate of antibiotics was in the range of 95% Penicillin (PEN), 82% Amoxicillin (AMO), 77% Cefazolin (CEF), 59% Ceftriaxone (CEFT) and Tetracyclin (TET), 46% Gentamicin (GEN), 32% Nitrofurantoin (NIT), 27% Cefoxitin (CEFX and Ofloxacin (OFL), 23% Streptomycin (STR), 19% Chloramfenicol (CHL) and 9% Meropenem (MER). Among 22 isolates of K. pneumoniae 13 (59 %) showed beta lactamase activity especially isolated from urine, while 9 (41%) showed no beta lactamase activity. Out of 22 isolates, 18 (82%) isolates showed Multiple Antibiotic Resistance against four to ten antibiotics. (c) 2011 Friends Science Publishers

Key Words: K. pneumoniae; Antibiotic resistance; Beta lactamase activity


Klebsiella pneumoniae strains are opportunistic pathogen and have been associated with various ailments such as urinary tract infection, septicemia, respiratory tract infection, wound infection, and diarrhea (Khadri et al.,2007).

Klebsiella pneumoniae is resistant to a number of antibiotics mainly extended-spectrum cephalosporin's and penicillin's due to acquisition of plasmid that encode for the production of extended spectrum beta lactamases (ESBL) especially TEM and SHV enzymes have been described worlwide (Lopes et al., 2005). Resistance of this species to third generation cephalosporins was first described in the early 1980s and a linear increase in resistance has occured since 1986 (Burwen et al., 1994; Monnet et al., 1997). These enzymes are derivatives of common b lactamases that have undergone one or more amino acid substitutions near the active site of the enzyme, thus increasing the affinity and the hydrolytic ability of enzyme for third-generation cephalosporins and monobactams (Jacoby and Medeiros, 1991). Genes encoding these enzymes are generally located in transferable plasmids, which are often such as aminoglycosides (Ferna'ndez-Rodri'guez et al., 1992).

In this study we determined the status of antimicrobial resistance, underlying conditions and determination of K. pneumoniae isolates with beta-lactamase production from patients, multiple antibiotic resistance index and also treatment of infections based on K. pneumoniae, which antibiotics could be better.


Isolation of bacterial strains and identification: Twenty two isolates were collected from hospital patients in Kahramanmaras between 2006-2007 and recorded at specimens. Mac Conkey agar and EMBagar (Eosin Metilen Blue) agar used for K. pneumoniae isolation. Isolates were considered to be presumptive Klebsiella spp. gram-negative bacill, mucoid colonies and lactose positive. Confirmation of isolates was performed by using classic chemical tests (motility test, ure hydrolysis, acid production from mannitol, production of H2S, IMVIC (Indol, Metil Red, Voges-Proskauer and Citrate), (Lassen, 1975; Krieg and Holt,1984).

Antibiotic resistance activity: Antibiotic resistance was determined by an agar disc diffusion test (Bauer et al., 1966) using Mueller-Hinton agar (Difco) according to Clinical and

Laboratory Standards Institute (CLSI, 2005) recommendations. Twelve different antibiotics were used. For antibiotic resistance determination, the isolates were grown in Luria- Bertani (LB) broth until the turbidity equal to the 0.5 Mc Farland standart. Cultures were swabbed on to the Mueller-Hinton agar and all isolates were tested against Meropenem (MER, 10 ug/mL), Amoxicillin (AMO, 20 ug/mL), Penicilin (PEN, 10 ug/mL), Nitrofrantoin (NIT, 300 ug/mL), Cefazolin (CEF, 30 ug/mL), Cefoxitin (CEFX, 30 ug/mL), Ceftriaxone (CEFT, 30 ug/mL), Gentamicin (GEN, 10 ug/mL), Tetracycline (TET, 30 ug/mL), Streptomycine (STR, 10 ug/mL), Chloramfenicol (CHL, 30 ug/mL), Oflaxain (OFL, 5 ug/mL). The isolates those grown in inoculation were evaluated as resistant and the others were evaluated as susceptible (CLSI.2005). The antibiotic discs were dispensed sufficiently separated from each other so as to avoid overlapping of inhibition zones.

Table I: Prevalence of the antibiotic resistance and beta lactamase production among 22 clinical K. pneumoniae isolates

Antibiotics###Beta lactamase activity


Pen Tet###+

Pen OfI###-

Amo Pen###+

Amo Pen Cef Cefx###+

Amo Pen Nit Cef###+

Amo Pen CefCefl###-

Amo Pen Cef Ceft###-

Amo Pen Nit Tet OfI###+

Amo CefCefx Gent OfI###-

Amo Pen Cef Ceft Gent Tet###+

Pen Cef Ceft Gent Tet Str###-

Amo Pen CefCeft Gent Tet###-

Amo Pen Nit Cef Ceft Tet Chl###+

Mer Amo Pen Nit Cef Cefk Ceft###+

Amo Pen Cef Cefx Ceft Gent Tet###+

Amo Pen Nit CefCefI Tet Str###-

Amo Pen Nit Cef Ceft Gent Tet Oil###-

Mer Amo Pen Cef Cefx Ceft Gent Tet###+

Amo Pen Cef Cef't Gent Tet Str Chl###+

Amo Pen Cef Cell Gent Tet Str Chl Ofi###+

Amo Pen Nit Cef Ceft Gent Tet Str Chl Ofi###+

There are many local studies about antimicrobial resistance and sensitivity among K. pneumoniae in Turkey like ours (Halit et al., 1999; Gonlugur et al., 2004; YUksel et al., 2006; Aladag and Durak, 2009; Albayrak and Kaya, 2009) and other countries (Jones et al., 2004; Aiyegoro et al., 2007; Jean et al., 2009; Romanus et al., 2009).

Among the beta lactam antibiotics, penicillin resistance rate (95%) was the highest and amoxicillin resistance rate was 82% in the present study (Table II). Aladag and Durak (2009) has shown penicillin resistance rate 100% to K. pneumoniae isolated from urinary system infections. In their study, bacterial suspectibility to all antimicrobial agents was determined according to criteria of the National Committee for Clinical Laboratory Standarts by means of agar disc diffusion test like ours. A high resistance of beta lactam antibiotics is due to penisilinase coded by R factor inhibited it. (Sawai et al., 1973). Generally urine isolates were resistant to only penicillin. Blood isolates were resistant to penicillin and amoxicillin. Cerebro Spinal Fluid (CSF) isolates were resistant to penicillin and cefazolin. Beta lactams were showed high resistance in this study.

Among the Cephalosporins group, as for the cefazolin resistance rate, it has been 77% (Table II). It was the highest in cephalosporins group. In Turkey, Sesli-Cetin et al. (2007) reported that cefazolin suspectibility rate has been 31.4%. K. pneumoniae isolated from intensive care unit. Gonlugur et al. (2004) has shown cefazolin suspectibility rate 64.3% to Klebsiella spp isolated from a Turkish university hospital by disc diffusion method. Our result was different from that reported by Jean et al. (2009) who also reported that K. pneumoniae showed a resistance of 31% to cefazoline. In their study, a total of 574 Enterobacteriaceae isolates recovered from various clinical samples. E. coli, K. pneumoniae, Enterobacter cloaceae, Serratia marcescens, Citrobacter freundii, Morganella moragnii, Proteus mirabilis were tested 18 antimicrobial agents by the broth microdilution method. It can be suggested that difference of the method can be affect resistance's percentage of bacteria.

Table II: Antibiotic resistance of 22 isolates K. pneumoniae strains according to the disc diffusion

Antibiotic group:###Antibiotics###Resistance (%)

Beta-Lactams:###Penicilin (PEN),Amoxicillin (AMO), Meropenem (MER)###95%, 82%, 9%

Nitrofrantoins:###Nitrofrantoin (NIT)###32%

Cephalosporins:###Cefazolin(CEF), Ceftriaxone(CEFT), Cefoxitin(CEFX)###77%, 59%, 27%

Aminoglycosides:###Gentamycin (GEN), Streptomycine (STR)###46%, 23%

Tetracyclines:###Tetracycline (TET)###59%

Macrolides:###Chloramphenicol (CHL),###19%

Quinolones:###Ofloxacin (OFL)###27%

Table III: Multiple Antibiotic resistance index of 22 K. pneumoniae strains

Source of isolates###Total Isolates###Multiple Antibiotic Resistance Index (MAR)

Urine###15###0.08, 0.17(3 isl) 0.33((2 isl), 0.42(3 isl), 0.58(3 isl), 0.66, 0.75, 0.83

Blood###3###0.5, 0.58, 0.66

Vaginal Fluid###1###0.33

Cerebrospinal Fluid###2###0.66


Among the Cephalosporins group, as for the ceftriaxone resistance rate, it has been 59% (Table II). Ceftriaxone resistance rate has reported from 0.6% to 79.6% in different studies (Karlowsky et al., 2002; Jones et al., 2004; Al-Zahrani and Akhtar, 2005; Romanus et al., 2009). Shukla et al. (2004) reported that K. pneumoniae showed a resistance of 62.5% to ceftriaxone among the different clinical isolates.

Tetracycline resistance was 59% (Table II). Resistance patterns of K. pneumoniae revealed that 88.5% to tetracycline (Romanus et al., 2009). In a similar study, all K. pneumoniae isolates were higly resistant to tetracycline 100% (Okonko et al., 2009). Our results are similar to that reported by Ahmed et al. (2000) who also reported that K. pneumoniae showed a resistance of 61% to tetracycline. In their study, a total of 155 common pathogenic bacteria were recovered from patients with diarrhea and 362 common bacterial organisms were recovered from patients with urinary tract infections. E. coli, K. pneumoniae, Proteus mirabilis, Enterobacter, Acinetobacter and Pseudomonas species were isolates obtained from this study.

Among the aminoglycosides, as for the gentamicin resistance rate, it was 46% (Table II). In Turkey, some researchers have reported gentamycin resistance rate from 15.2% to 77.9% (Urbarli et al., 2001; Yilmaz et al., 2005). Our results are in complyance with previous research. In Trinidad Orrett (2004) it showed gentamicin resistance rate was 16.7% among the K. pneumoniae isolated from intensive care unit. Gentamycin resistance rate change according to region. For example, while in westren Nigeria, Okonko et al (2009) reported that gentamicin resistance rate was 100%, In south-western Nigeria Okesola and Makanjula (2009) reported that 48.4%.

Resistance rate of nitrofurantoin was 32% in the present study (Table II). Romanus et al. (2009) reported that 31.2% nitrofurantoin resistance rate was like ours. In their study, a total of 300 clinical isolates of K. pneumoniae were isolated from 100 blood samples, 100 sputum samples, 100 urine samples. The isolates were subjected to susceptibility testing using agar disc diffusion test of determining antimicrobial susceptibility and the results were interpreted as per National Committee for Clinical Laboratory Standarts (NCCLS) recommendations like ours. Ay et al. (2003) reported that nitrofurantoin resistance rate was 48% and 30% among the K. pneumoniae isolated from urine samples. YUksel et al. (2006) reported that nitrofurantoin could be included as a reasonable alternative in the empirical treatment of lower urinary tract infections in older children.

Taking into account the total number of clinical isolates in the present study period only 27% of the K. pneumoniae species isolated were resistant to cefoxitin (Table II). Goldstein et al. (1995) reported 2.8% cefoxitin resistance rate of K. pneumoniae isolated in community. In Turkey, Toroglu et al. (2005) reported that cefoxitin resistance rate was from 0% to 100% to Klebsiella sp isolated from Aksu river. Durmaz et al. (1997) have shown that out of 93 Klebsiella sp., 20 were resistant to cefoxitin.

Among the Quinolones group, ofloxacin resistance rate was 27% K. pneumoniae isolated from clinical samples (Table II). In Turkey, Ozbilge et al. (2004) reported that ofloxacin resistance rate was 6% K. pneumoniae isolated from urine samples. Aiyegoro et al. (2007) reported that all Klebsiella spp showed sensitivity to ofloxacin. Okonko et al. (2009) reported that K. pneumoniae showed 0% resistance to ofloxacin. Durak et al. (2007) also reported that K. pneumoniae showed a resistance of 25% to ofloxacin among the clinical isolates. In their study, the sensitivities of total 103 bacteria strains consisting of 52 Gram negative (E. coli, Proteus spp, Pseudomonas aeruginosa, K. pneumoniae) and 51 Gram positive (Stpahylococcus aureus, Streptococcus pyogenes) bacteria isolated and identified from different patient material against to ofloxacin were determined by disc diffusion method.

Durak et al. (2007) reported that ofloxacin is more effective to Gram negative strains than Gram positive bacteria and an increase on the number of resistant strains.

Taking into account the total number of clinical isolates in the present study period only 23% of the K. pneumoniae species isolated were resistant to streptomycin (Table II). Okonko et al. (2009) reported streptomycin resistance rate of 100% to K. pneumoniae isolated from clinical samples. Aladag and Durak (2007) also reported that Klebsiella spp showed a resistance of 22,4% to streptomycin, using the method similar to ours.

Macrolides antibiotics like chloramfenicol resistance rate was 19% in the present study (Table II). Okonko et al. (2009) reported chloramphenicol resistance rate of 100% in Abekuta, South western Nigeria. In a different study, the extended spectrum beta lactamase (ESBL) producing Klebsiella spp strains isolated from urinary system infections were determined to be 21% resistant to chloramphenicol (Kim et al., 2005). In Turkey, Aladag and Durak (2009) reported 17.8% chloramfenicol resistance rate among the ESBL producing K. pneumoniae and 20% chloramfenicol resistance rate among the non ESBL producing K. pneumoniae. Our results were similar to that reported by Aladag and Durak (2007) who also reported that K. pneumoniae showed a resistance 17.8% and 20% resistance to chloramphenicol. All samples strains of susceptibility of antibiotics were determined by using disc diffusion method as we did.

Among the beta lactam antibiotics, resistance rate of meropenem has been 9% in the present study (Table II). Carbapenems are the drugs of choice for many infections caused by gram negative and gram positive bacteria (Nicolau, 2008; Shah, 2008). In our results, it was the lowest. Ay et al. (2003) reported that Klebsiella has the highest resistance among the bacteria isolated from urine samples. Imipenem antibiotics, third generation cephalosporins, kinolon and aminoglycozid have the most sensitive antibiotics Klebsiella (Ay et al., 2003). Al-Zahrani and Akhtar (2005) reported that K. pneumoniae showed highest susceptibility to meropenem (94.4%), which corroborates with the previous reports (Ay et al., 2003; Al- Zahrani and Akhtar, 2005; Ullah et al., 2009).

Among the isolates, 59% (13/22) were found to be beta-lactamase producers. There was no correlation between b lactamase production and resistance to the used antibiotics. The reason for this is that many isolates were determined to be b-lactamase negative in spite of their resistance to some of the antibiotics. On the other hand, some isolates were determined to be both b-lactamase positive and resistant to some antibiotics (Toroglu et al., 2005). Some researchers reported that extended spectrum b- lactamase in K. pneumoniae. It reported that from 10.4% to 66.7% among K. pneumoniae isolated from different samples (Kader and Kumar, 2004; Kolar et al., 2006; Aladag and Durak, 2009; Albayrak and Kaya, 2009; Kaskatepe and Yildiz, 2009).

In recent years, due to selection pressure of antibiotics in hospital enviroment multiple resistance to antibiotics has been seen in the enteric organisms. This is more so with K.pneumoniae (Eisentein, 1995). This organisms has been resistant to aminoglycosides beta lactams, fluoroquinolones and to other antibiotics and has the greatest ability to receive and disseminate resistant factors (French et al., 1997). The presence of antimicrobial agents at low concentration through leaching or continued usage lead to the development of drug resistant isolates and multiple antibiotic resistance (MAR) in bacteria and reduced efficiency of antibiotic treatment for human and animal diseases (Tendencia and De la Pena, 2001). In present study, both vaginal fluid and wound samples showed 0.33 the MAR index value. Among the K. pneumoniae strains isolated from Urine, the lowest MAR index value was 0.08, the highest MAR index value was 0.83.

In present study, the MAR indexes of K. pneumoniae were from 0.33 to 0.83. MAR index were given Table III. Out of 22 isolates, 18 (82%) isolates showed Multiple Antibiotic Resistance four to ten antibiotics. Some researchers found that multiple antibiotic resistance (MAR) index value were from 75 to 88.3% among K. pneumoniae isolates (Shukla et al., 2004; Manandhar et al. 2006). Our results were similiar to Shukla et al. (2004). In their study, 88.3% (106) of the isolates were found to be resistant to at least one of the 3rd Generation antibiotics (3GC) (cefotaxime, ceftazidime and ceftriaxone) and 72% of the isolates were resistant to all the 3GC tested.

Further studies need to be carried out to determine especially those, which haven't been studied on are resistant to K. pneumoniae. K. pneumoniae isolated from different clinical samples need to be tested to find out whether they produce b lactamase or not. While dealing with K. pneumoniae infections, extended spectrum antibiotics might be avoided. Before using the antibiotics, antibiotic sensitivity test should be done. Following usage of antibiotics and identification of antibiotics resistance evolution are vital for a good treatment.


It is suggested that meropenem, chloramphenicol and streptomycin could be better for treatment of infections based on K. pneumoniae according to the present study. Penicilin and amoxicillin were non-advisible antibiotics for K. pneumoniae infections according to the MAR results. Furthermore, K. pneumoniae infections is a serious opportunistic pathogens. There was no compatibility between b-lactamase production and antibiotic resistance.


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Author:Toroglu, Sevil; Keskin, Dilek
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Date:Dec 31, 2011
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