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Distribution of bacterial uropathogens and their susceptibility patterns over 12year (20012013) West Bank, Palestine

Ahmad M. Zaid
Medicare-Medipal laboratoriesRamallah, West Bank, Palestine National Authority. * Correspondence:

kilani@medipal.ps

Background. The increased emergence of new resistant strains in most human

pathogens has become one of the most serious global health threat. Empirical treatment of urinary tract infections (UTIs) has become difcult in many parts of world. Therefore, local susceptibility patterns of uropathogens is of great importance to achieve cure and reduce the misuse of empirical antibiotics. This study presents the incidence of uropathogens and their antimicrobial susceptibility patterns in West bank of Palestine .

Methods. A total of 16,883 urine culture samples were included in this retrospective study. The incidence of recovered uropathogens was estimated over 12-year in the examined urine samples, as well as the sex and age groups of the patients. Antimicrobial susceptibility was performed for all identied bacterial isolates.

Results. A total of 6.539 /16,883 (38.7% ) urine culture samples showed signicant bacterial growth. The common isolates were E. coli, coagulase negative Staphylococci, Streptococcus spp, S aureus, and Klebsiella spp, and their frequencies were 47%, 19.6%, 18.4%, 4.9%, 2.9%, respectively. Gram positive uropathogens showed susceptibility towards amoxi/clav, cefuroxime ,cephalothin , culpha /trimethoprim, nitrofurantoin, ciprooxacin, ooxacin and noroxacin as follow: 83.9%, 80.1%, 70.1%, 36.6%, 65.1, 57.6%, 51.6%, 47.8%, respectively. While Gram negative uropathogens were susceptible to ciprooxacin, ooxacin, noroxacin, cefuroxim, nitrofurantoin, sulpha/trimethoprim, nalidixic acid, and amoxi/clav 76.1%, 71.8%, 72.9%, 64%, 67.5%, 48.7%, 57.6%, 42.1%, respectively.

Conclusions. This retrospective study shows high rates of antimicrobial resistance This article is available from: www.iajaa.org
to all commonly used anti-urinary tract infection drugs, and demonstrates the importance to monitor the incidence of common uropathogens and their antimicrobial susceptibility patterns before starting treatment.

Introduction
Urinary tract infections (UTIs) have an estimated occurrence of 150 million infections each year worldwide (1). In the USA, UTIs account for more than 7 million outpatient visits annually. Total costs for management of UTIs exceed one billion dollars in USA (2). Gram negative aerobic bacteria represent the majority of uncomplicated UTIs, with E. coli incidence rate (70-95%) , while the most commonly isolated gram positive aerobic bacteria are coagulase negative staphylococci accounts for around 5 to 10% (3-4). Under License of Creative Commons Attribution 3.0 License

Most pathogens of the urinary tract are coming from fecal normal ora that colonize the peri-urethral area and vagina in females. Due to continuous and increased emergence of new bacterial resistance strains, antimicrobial susceptibility patterns of uropathogens are of great importance for successful treatment of UTIs. Local data on antimicrobial susceptibility patterns is becoming more necessary in countries where there is antimicrobial abuse especially when these: drugs can be obtained without medical prescription from pharmacies (5).

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To our best knowledge, few local data on antimicrobial susceptibility patterns and epidemiology of uropathogens among Palestinian population were reported. A recent published study showed limited data from one local area (6). This study investigated large numbers of cultured UTI specimens which have been received over the last 12 years covering the whole Palestinian population of West Bank region.

24-48 hours at 37oC. After incubation, the urine cultures considered to be negative when bacterial growth was lower than 103 CFU/mL; positive when pure growth was higher than 105 CFU/mL. Growth of more than one type of bacteria was considered contamination and neglected . Identication of bacterial isolates was based on the Gram staining characteristics of the bacteria, appearance of colonies on agar, Catalase test, Oxidase test, Staphylase test and their biochemical prole including Triple Sugar Iron (TSI), Sulphour-Indole-Mannitol (SIM), Urease, Citrate, Methyl-Red (MR) and VogesProskauer (VP).

Material and methods

This retrospective study is based on data obtained from the records of 11 centers of Medicare-Medipal laboratories. Data included 16,883 urine culture samples investigated over twelve years period (April 2001, to March 2013).

Antimicrobial susceptibility test

All bacterial isolates were tested for their susceptibility to antimicrobials using modied Kirby-Bauer technique and guidelines used in England (7).The antimicrobials diffusion discs were obtained from (Bioanalyse, Yenimahalle ,Ankara / Turkey). Antimicrobials tested were the following: amikacin, amoxicillin-clavulanic acid, ampicillin, cefaclor, cexime, cefotaxime, ceftazidime, ceftriaxone, cephlexin, cephalothin, cip rooxacin,ooxacin,cotrimoxazole, gentamicin, nalidixic acid, noroxacin, sulphamethoxazole-trimethoprim (SXT) and nitrofurantoin. Furthermore, other antibiotics were used less frequently and were mentioned in table 1.

Urine Culture and identication of bacterial isolates

Most specimens were mid-stream clean catch urine collected upon request of examining physician, and not all cultured samples were examined for urinalysis. Urine samples were cultured on both 5% blood agar and MacConkeys culture plates. Inoculation of plates was done by using one micro liter disposable calibrated loops. Plates were incubated for

Table 1. Distribution of antimicrobial susceptibility for the main uropathogens.

Antibiotics Amox / Clav Cefaclor Cexime Cefotaxime Ceftazidime Ceftriaxone Cefuroxime Cephalexin Cephalothin Ciprooxacin Gentamycin Nalidixic Acid Nitrofurantoin Ooxacin Sulpha../Trime.. E . coli No.(%)* 2571(43) 1755(44) 666(72.1) 408(75.2) 1638(79.7) 1164(79.3) 2386(66.1) 1465(29.9) 702(16.4) 1534(77) 475(71.2) 1923(59.9) 2477(74.4) 425(73.2) 2488(49.3) Streptococcus spp. No.(%) 1028(91.1) 720(64.7) 313(33.2) 60(70) 442(50.9) 440(77.7) 1018(85.3) 602(51.2) 250(73.2) 575(55.1) 61(52.5) 212(7.5) 894(61.9) 173(46.2) 976(30.5) C.N.S No.(%) 1077(79.1) 801(61) 286(10.8) 76(57.9) 491(25.9) 520(55.2) 1071(76.4) 713(59.6) 262(69.8) 557(60.5) 79(79.7) 258(8.1) 968(67.5) 175(52.6) 1083(40.7) S .aureus No.(%) 278(76.3) 165(60) 52(7.7) 31(71) 100(28) 86(59.3) 227(74.9) 153(49) 85(61.2) 173(56.1) 51(70.6) 83(6) 226(69.5) 69(62.3) 242(46.7) Proteus spp. No.(%) 116(60.3) 85(50.6) 27(88.9) 22(77.3) 76(85.5) 55(90.9) 97(71.1) 62(40.3) 22(27.3) 68(76.5) 26(57.7) 81(34.6) 107(8.4) 18(72.2) 107(29) Klebsiella spp. No.(%) 148(31.8) 124(54.8) 54(72.2) 21(81) 112(78.6) 76(77.6) 160(58.8) 94(47.9) 22(18.2) 92(76.1) 24(58.3) 90(62.2) 154(43.5) 26(69.2) 160(53.1)

* No(%): Total number and percentage of each bacteria isolates

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IBM-SPSS software (version 17 for Windows) was used to calculate the frequencies, cross-tables, and risk estimations.

Result
A total number of 6,539/ 16,883 (38.7% ) was positive for a signicant and pure bacterial growth from urine samples over the 12-year period. The distribution of bacterial isolates is shown in gure 1 .Gram negative isolates accounted for 3627 (57.1%), while Gram positive isolates accounted for 2730 (42.9%). E. coli represented the vast majority of gram negative bacterial isolates (83.2%), followed by Klebsiella spp. (5.1%), Proteus spp. (3.6%), Pseudomonas spp.(3.4%), Citrobacter spp. (1.8%), Enterobacter spp. (1.6%), and other less frequent uropathogens. Gram positive bacterial isolates are dominated by coagulase negative staphylococci (CNS) (46%), followed by Streptococci spp. (42.3 %), and S. aureus (11.5%). Figure 2 shows the distribution of gender and uropathogen isolates. There is a signicant in the incidence (P < 0.05) of E. coli( 50.7% vs 46.1%), Citrobacter spp .

(1.5% vs 0.9%), and Pseudomonas spp. (2.9% vs 1.8%) in males compared to females, but a signicant incidence (P < 0.05) was observed in females than males due to infection with Streptococci spp. (18.9 vs 16.4%), Klebsiellaspp(3.1% vs 1.9%), & coagulase negative staphylococci (20.1% vs 17.3%) . The results of antimicrobial susceptibility patterns of uropathogen isolates are shown in table 1.

Discussions
This study shows generally that the results of bacterial isolates from urine cultures are much similar to other recent ndings published in the neighboring country of Jordan (8-10). Escherichia coli is still the leading uropathogen, with overall (47%) of all bacteria isolated from urine samples obtained from patients suspected to have UTI. Also, E .coli represented (83.2%) of all Gram negative isolates, and its incidence was signicantly higher among males than females ( 50.7% vs 46.1%). This result is different than ndings reported from Turkey and Jordan ( 3,8,9), where women more often develop urinary tract infections due to E.coli. However, it is important to note that most of our patients developed community ac-

Figure1. Distribution of bacteria isolates detected in urine cultures

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Figure 2. Gender distribution of uropathogen isolates.

quired urinary tract infection . Remarkable high incidence of E.coli was found among children (62.1%) and elderly (55.2%) when compared to other age groups. The present study demonstrates that the incidence rate of coagulase negative staphylococci (CNS)(19.6%) was common among females (20.1%) and similar to many other studies worldwide ( 3,11,12 ). Young adults and adolescents females had the highest incidence rates of CNS isolates (24.8%, 23.3%), respectively. Moreover, the incidence rate of Streptococcus species (18.4) was slightly higher among females than males (18.9 vs. 16.4%). The same observation is noticed with CNS which caused more UTIs among females compared to males (20.1% vs. 17.3%) especially among sexually active young persons. While the incidence rate of S.aureus (4.9%) was much similar among males and females (5.5% vs 4.8%). These results may reect the fact that UTI is remarkably increased among sexually young active age groups as reported by Vincent et al. (12 ). The incidence rates of Klebsiella spp., Enterobacter spp., and Pseudomonas spp. as cause of UTIs in this study were low and similar to many other studies (9-10). It is well established that these bacteria spp. are often associated with hospitalized patients and cause complicated cystitis and pyelonephritis (13). These three species are often associated with hospitalized patients and less with community acquired UTI. Age groups

also did not show signicant difference in incidence of these organisms among males and females as indicted by other studies (5,14). Other bacterial isolates were found in(<1%) including citrobacter spp., Pantoea spp., Acinetobacter spp., Serratia spp . In general, all bacterial isolates from urine culture samples showed the lowest susceptibility in vitro to ampicillin (28.3%), while imipenem has the highest activity (93.8%). However, imipenem used mainly in hospitalized patients. Gram positive bacteria showed better susceptibility rates in vitro to commonly used drugs in UTIs such as amoxi/Clav , cefuroxime and nitrofuratoin, whereas less susceptibility rate was detected against ciprooxacin, sulpha/trimethoprim and cephalexin ( Table 1). The results of this study demonstrated that E.coli isolates have the lowest susceptibility to the following drugs: amoxi/clav, cephalexin, cephalothin, and sulpha/trime ( Table 1). While E.coli was moderately susceptible to ciprooxacin, nitrofuratoin, cefuroxime and nalidixic Acid, ( Table 1). The low susceptibility to amoxi/clav and sulpha/trimethoprim in this study is similar to the results reported from Jordan and other Middle East countries (8,9,10,15,16). The other Gram-negative isolates (Klebsiella spp., Enterobacter spp., Proteus spp., Citrobacter spp. and Pseudomonas spp.) showed more resistance Under License of Creative Commons Attribution 3.0 License

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to antibiotics and mostly were multidrug resistance ( Table 1). In conclusion, this study suggests that further periodic multi center surveys are needed to control the spectrum of antimicrobial resistance in common clinical bacterial isolates in our region, since such available local data will help physicians to select the proper empiric therapy in treatment of UTIs and other infections and contribute to control the misuse of antimicrobial agents.

Aknowledgments
I would like to express my sincere thanks for Dr. Bashar Karmi, Mr. Ibrahim Salhi and Mrs. Ola abu-Kishik for their excellent help, motivation and encouragement to get this study done.

References
1. Stamm, W E, Norrby RS. Urinary tract infections: disease panorama and challenges. J Infect Dis 2001; 183: S1-4. 2. Richards DA,Toop LJ,Chambers ST,Sutherland MG,Harris BH,Ikram RB,Jones MR,McGeoch GR,Peddie B. Antibiotic resistance in uncomplicated urinary tract infection: problems with interpreting cumulative resistance rates from local community laboratories. N Z Med J 2002;115(1146): 12-14. 3. Cetin M,Ucar E,Guven O,Ocak S. Community-acquired urinary tract infections in Southern Turkey: etiology and antimicrobial resistance. Clin Nephrol 2009;71(1): 30-35. 4. Hooton, T M. The current management strategies for communityacquired urinary tract infection. Infect Dis Clin North Am 2003;17(2): 303-332. 5. Bosch FJ,van Vuuren C,Joubert G. Antimicrobial resistance patterns in outpatient urinary tract infections:the constant need to revise prescribing habits. S Afr Med J 2011;101(5): 328-31.

6. Abu-Taha SA, W,Sweileh MW. Antibiotic resistance of bacterial strains isolated from patients with community-acquired urinary tract infections: an exploratory study in Palestine. Curr Clin Pharmacol 2011;6(4): 304-307. 7. Practice in Tropical Countries (Part 2). Cheesbrough M, District Laboratory, Cambridge, 2002. University Press: Cambridge, UK. 8. Nimri L, Batchoun R. Community-acquired urinary tract infections in a rural area in Jordan: Predominant uropathogens, and their antimicrobial resistance. Webmed Central Microbiology 2011;12:19. 9. Shehabi A A , Mahafzah M A, Khalili K. Antimicrobial resistance and plasmid proles of urinary Escherichia coli isolates from Jordanian patients. East Mediterr Health J 2004; 10(3): 322-328. 10. Murshidi, M S, Farah B N.Urinary tract infections in adult and adolescent males of a developing community: pattern, bacteriology and genito-urinary predisposing factors. Arch Esp Urol 2002;55(10): 288-293. 11. Harrington RD, Hooton, MT.Urinary tract infections risk factors and gender. J Gend Specif Med 2000;3(8):27-34. 12. Vincent CR, Thomas TL, Reyes L, White CL, Canales BK, Brown MB. Symptoms and risk factors associated with rst urinary tract infection in college age women: a prospective cohort study. J Urol 2013;189(3): 904-910. 13. Ronald A. The etiology of urinary tract infection: traditional and emerging pathogens. Am J Med 2002;8(113): 14S-19S. 14. Mishra MP, Debata NK, Padhy RN, Rosenthal VD. Surveillance of multidrug resistant uropathogenic bacteria in hospitalized patients in Indian. Asian Pac J Trop Biomed 2013; 3(4): 315-324.15. Al-Mardeni RI,Batarseh A,Omaish L,Shraideh M,Batarseh B,Unis N. Empirical treatment for pediatric urinary tract infection and resistance patterns of uropathogens, in Queen Alia hospital and prince AIsha military center--Jordan. Saudi J Kidney Dis Transpl 2009;20(1): 135-139. 16. Karem H, Alzoubi, NJ S, Bader M. Al-Sadi MB, Saafan A. Al-Saf AS, Abuirjeie A N. Antibiotic Consumption and Development of Resistance among Gram-Negative Bacilli in Hospitalized Patients of King Abdullah University Hospital (KAUH) in North Jordan. Jordan Journal of Pharmaceutical Sciences 2008; 1(1): 65-70.

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