2013-1-hashemi

JRHS 2013; 13(1): 75-80

Copyright © Journal of Research in Health Sciences

The Prevalence of Antibiotic Resistance of Enterobacteriaceae Strains Isolated In Community- and Hospital-Acquired Infections in Teaching Hospitals of Hamadan, West of Iran

Seyyed Hamid Hashemi (MD)a, Farzaneh Esna-Ashari (MD)b*, Shahrzad Tavakoli (MD)c, Mojgan Mamani (MD)a

a Department of Infectious Diseases, School of Medicine, Hamadan University of Medical Science, Hamadan, Iran

b Department of Community Medicine, School of Medicine, Hamadan University of Medical Science, Hamadan, Iran

c Department of Infectious Diseases, School of Medicine, Hamadan University of Medical Science, Hamadan, Iran

* Correspondence: Farzaneh Esna-Ashari (MD), E-mail1: esnaashari_f@umsha.ac.ir, E-mail2: esna_f@yahoo.com

Received: 13 November 2012, Revised: 09 December 2012, Accepted: 16 January 2013, Available online: 23 January 2013

Abstract

Background: The prevalence of antimicrobial resistance among Enterobacteriaceae is increasing worldwide. Identification of pathogens and their resistance to antimicrobials is mandatory for successful empiric antibiotic treatment. The aim of this study was to investigate the prevalence of antimicrobial resistance of Enterobacteriaceae isolated from hospital-acquired and community-acquired infections.

Methods: In a descriptive-comparative study, during 2010, all clinical isolates of Enterobacteriaceae and their antibiograms from laboratories of Sina and Bessat Hospitals, Hamadan, west of Iran were included. Hospital-acquired infections were identified by records from infection-control units. A questionnaire containing information about demographic characteristics, source of specimen, kind of Enterobacteriaceae and their antimicrobial resistance was filled for each patient. Data were analysed using SPSS.

Results: A total of 574 samples were collected, out of which the most prevalent pathogens were Escherichia coli and Klebsiella pneumoniae. Almost all isolates of Enterobacteriaceae were resistant to ampicillin (98.8%), and the least resistance was to piperacillin (3.7%). In addition, most isolates were resistant to cefazolin, cefixime, and co-trimoxazole. Among third generation cephalosporins, the highest resistance to ceftriaxone and the least resistance to ceftizoxime were observed. 19.3% of isolates were resistant to imipenem. In terms of fluroquinolones, nosocomial infections and community acquired infections were resisitant to ciprofloxacin 33% and 4.1% respectively. The rate of resistance in nosocomial infections was higher than that of community-acquired infections.

Conclusion: The prevalence of multidrug resistant Enterobacteriaceae is increasing both in community-acquired and hospital-acquired infections. Because of propable increasing resistance to fluoroquinolones and newer betalactams, reassessment of resistance of Enterobacteriaceae must continue in future years.

Keywords: Enterobacteriaceae, Antimicrobial resistance, Nosocmial infection

Introduction

Enterobacteriaceae is a large and heterogeneous family of gram-negative, facultative anaerobic, enteric bacilli whose normal place is in gastrointestinal tract of human and animals. Drug resistance in enteric bacilli is largely attributed to the vast transfer of resistance plasmids among different genera of Enterobacteriaceae. Today, in many regions of the world; about half of Shigella species are resistant to numerous drugs. The Salmonella carried by animals also is resistant especially against drugs (particularly tetracycline) used in animal foods. Use of drugs in animal foods leads to faster growth of animals, however, this is associated with an increase in drug-resistant intestinal organisms in fecal flora of farm workers 1.

Plasmids carrying drug resistance genes are observed in many gram-negative bacteria of normal flora. Extensive use of antimicrobial drugs, especially in hospitalized patients, has resulted in inhibition of drug-sensitive organisms in intestinal flora and sustained presence and growth of drug-resistant bacteria including Enterobacter, Klebsiella, Proteus, Pseudomonas, Serratia, and fungi. Such organisms make various problems especially for patients with immunodeficiency and granulocytopenia. Closed environment of hospitals makes transfer of these resistant organisms easier through aerosols and direct contact from personnel 2.

Contamination and infection in medical environments are among the important public health problems of the present century 2. Over recent years, on one hand, application of new treatment methods has saved lives, and on the other hand, it has had many fatal consequences by making the ground for nosocomial resistant infections 2,3. In addition to increased mortality, nosocomial infections lead to an increase in hospitalization period, tasks of medical staff, taking medications, and consequently, considerable increase in treatment costs 4.

According to previous studies performed in Iranian hospitals, Enterobacteriaceae isolated from nosocomial infections were mostly resistant to ampicillin and cotrimoxazole and more than 70% of the isolates were resistant to one of the third-generation cephalosporins 5, 6.

Given the increased prevalence of antibiotic resistance and also inappropriate and uncontrolled use of antibiotics by hospitalized and other patients, it is necessary to determine and compare the prevalence of antibiotic resistance in nosocomial and community-acquired infections in order to take required actions toward control of antibiotic resistance.

The present study was conducted to determine the frequency of antibiotic resistance of Enterobacteriaceae isolated from nosocomial and community-acquired infections in Hamadan, west of Iran.

Methods

In this descriptive-comparative study conducted in April 2010- April 2011 (a full year), all clinical samples with positive culture for Enterobacteriaceae along with their antibiogram results were requested from laboratories of Sina and Besat hospitals in Hamadan.

According to the possible source of infection, samples from one or more sites including blood, urine, sputum, wound srcretion, tracheal secretion, cerebrospinal fluid, joint fluid, or stool were obtained. Enterobacteriacea strains were identified by standard microbiological methods, but specific species using standard biochemical methods7. Antimicrobial susceptibility testing was performed by Kirby-Bauer disk diffusion method according to the guidelines of the Clinical and Laboratory Standards Institute 8. The following antibiotic disks were used: ampicillin (10 µg), cefazolin (30 μg), cefotamime (30 µg), ceftriaxone (30 µg), ceftizoxime (30 μg), ceftazidime (30 μg), cefixime (5 µg), gentamicin (10 µg), amikacin (30 μg), imipenem (30 μg), piperacillin (100 μg), cotrimoxazole (25 µg), nalidixic acid (30 µg), ciprofloxacin(5 µg) , and nitrofurantoin (30 µg) (Padtan Teb Co., Iran). Strains showing resistance to at least three antibiotics were considered as multidrug resistant (MDR).

The collected information contained origin of sample, admission ward, species of the pathogenic Enterobacteriaceae, and antibiogram results of the samples. Cases with nosocomial infection were requested from hospitals' infection control unit in order to determine the type of infections (nosocomial or community-acquired infections). The obtained data were recorded in the questionnaire. Nosocomial infections refer to clinically significant infections which occur due to the hospitalization process of patients. The infections which were manifested clinically after 48 hours of hospitalization were considered as hospital-acquired (nosocomial) infections 9. Patients who went to clinics, emergency rooms, and physician offices and had positive culture for Enterobacteriaceae were included in the study as the community-acquired infections.

The data were analyzed using SPSS software. The qualitative variables were described using percentage frequency distribution and the groups were compared using Chi-square test. Percentages were used for description of antibiotic resistance with respect to Enterobacteriaceae strains. Chi square test was done for comparing the prevalence of antibiotic resistance among hospital and community acquired infections. P values less than 0.05 were considered significant.

Results

Totally, 574 samples were collected from 505 patients, of which, 303 samples (52.8%) and 271 samples (47.2%) were in nosocomial infection and community-acquired infection groups, respectively.

Based on their origin, the collected samples contained urine (69.3%), tracheal secretions (19.3%), blood (6.6%), wound infection (2.8%), sputum (0.9%), stool (0.3%), cerebrospinal fluid (0.3%), and joint fluid (0.3%).

Most of the samples were collected from emergency rooms and ICUs (144 samples (25.1%) from emergency rooms and 143 samples (24.9%) from ICUs, in that order) and the fewest samples were from Dermatology Ward (1 sample).

Among the 574 strains of Enterobacteriaceae, E. coli was the most prevalent species (70.6%). In the order of prevalence, other species of Enterobacteriaceae included 84 cases of Klebsiella spp. (14.6%), 45 cases of Proteus spp. (7.8%), 17 cases of Enterobacter spp. (3%), 12 cases of Serratia spp. (2.1%), two cases of Shigella spp. (0.3%), two cases of Morganella spp. (0.3%), and one case of Salmonella spp. (0.2%).

Sensitivity of the grown Enterobacteriaceae was assessed for 15 antibiotics which were effective against Gram-negative bacteria including ampicillin, amikacin, ceftriaxone, cefazolin, ceftizoxime, ceftazidime, cefixim, cefotaxime, ciprofloxacin, nitrofurantoin, gentamicin, imipenem, nalidixic acid, cotrimoxazole, and piperacillin. Frequency of antibiotic resistance in all samples is shown in Figure 1. The highest resistance and the lowest resistance were observed in ampicillin (99.8%) and piperacillin (3.7%), respectively.

Types of antibiotic resistance of Enterobacteriaceae are shown in Table 1 for community-acquired and nosocomial infections separately. In both groups of infections, ampicillin and piperacillin showed the highest and the lowest resistance, as well. Of those types of antibiotic resistance, only the antibiotic resistance to ampicillin of nosocomial infection group was not significantly different from that of community-acquired infection group, however, other cases of antibiotic resistance of one group were significantly different from those of other group(P<0.001).

As Table 2 indicates, in nosocomial infections, resistance against all antibiotics for isolated samples from ICU Ward were significantly higher than isolated from Emergency Ward (P<0.001) except for ampicillin.

Tables 3 and 4 show antibiotic resistance according to infectious organism in nosocomial and community-acquired infections. Accordingly, more than 20% of nosocomial and community-acquired E. coli species were resistant to 14 and 8 types of antibiotics respectively. Twenty-five percent of the nosocomial Proteous species were resistant to 12 types of antibiotics and 20% of the community-acquired ones were resistant to 10 types of antibiotics. Eight percent of the community-acquired Klebsiella and more than 29% of the nosocomial species were resistant to 8 types and 13 types of antibiotics respectively.

In terms of nosocomial Enterobacter species there was more than 30% resistance to 11 types of antibiotics and communityacquired species were resistant to 8 types of antibiotics.

Figure 1: Frequency distribution of antibiotic resistance in enterobacteriaceae isolated in teaching hospital of Hamadan

Table 1: The prevalence of antibiotic resistance by source of infections (hospital and community acquired infections)

Table 2: The prevalence of antibiotic resistance in nosocomial infections by the ward of admission (ICU & Emergency Wards)

Table 3: The prevalence of antibiotic resistance by Entrobacteriace strains in nosocomial infections

Table 4: The prevalence of antibiotic resistance by Entrobacteriace strains in community acquired infections

Discussion

In this study, the most prevalent bacteria in Enterobacteriaceae family in nosocomial and community-acquired infections were E. coli and Klebsiella spp. The Enterobacteriaceae family with E. coli on the top has been known as the most prevalent agent of urinary tract infection (UTI), bacteremia, and sepsis and it is also among the prevalent agents of intra-abdominal and genital region infections. The Enterobacteriaceae species play a major role in most community-acquired infections with origins from urogenital system, lungs, gastrointestinal tract, bed sores, surgical wounds, and venous catheters 10,11 . In this study, almost all isolated species of Enterobacteriacea (98.8%) were resistant to ampicillin and they were least resistant (3.7%) to piperacillin. Moreover, most species were resistant to cefazolin, cefixime, and cotrimoxazole. The resistance against nitrofurantoin was rather high. Among the third-generation cephalosporins, the highest resistance was observed against ceftriaxone and the least resistance was observed against ceftizoxime. The resistance against aminoglycosides, ciprofloxacinand imipenem was high. In most of the cases, the resistance of Enterobacteriaceae in nosocomial infection was greater than that in community-acquired infections. In this manner, our findings about the higher resistance rates of Enterobacteriacea isolates from ICUs compared to those from emergency rooms is explained by the fact that almost all isolates from ICUs have nosocomial origin. Conversely, most bacteria isolates from emergency room patients are community-acquired.

In this study, the high sensitivity of Enterobacteriaceae to ceftizoxime and less sensitivity to ceftriaxone may be due to routine and extensive use of ceftriaxone in outpatients and inpatients and also limited use of ceftizoxime. Despite the availability of ceftizoxime, it has not been much received by physicians due to its higher dose and shorter half-life as compared to ceftriaxone.

In recent years, many studies have reported the increasing resistance of Enterobacteriaceae to ampicillin, cotrimoxazole and first-generation cephalosporins. The resistance to third-generation cephalosporins has also been increasing, though less than the first-generation, in many countries. Currently, among the beta-lactam antibiotics, carbapenems are the most effective drugs 12 .

Studies in early last decade showed that the Enterobacteriaceae resistance in nosocomial infections is higher than that in community-acquired infections 13-15 , especially in case of Klebsiella bacteremia which is more prevalent and causes higher mortality in nosocomial infections and is also more resistant to cephalosporins and ciprofloxacin 14-16 . However, the resistance to the above antibiotics in community-acquired infections is increasing parallel to that in nosocomial infections 17-18.

Two studies by Tsai et al. in 2010 and Wollheim et al. In 2011, considered the appearance of E. coli and Klebsiella producing extended-spectrum beta-lactamase (ESBL) and their release among different species of Enterobacteriaceae as the cause of resistant nosocomial infections and increase in mortality 19,20 .

A review by Pitout et al. and a study on the course of Enterobacteriaceae resistance in Europe by Hawser et al. reported that the Enterobacteriaceae infection producing ESBL was increasing in recent decade both in hospitals and in communities and this has led to the fact that the empirical treatment's guidelines are not effective in community-acquired infections and require further reviews 21-22. Given that most of the resistant species of Enterobacteriaceae are sensitive to carbapenems, physicians may use carbapenems as an empirical treatment for severe community-acquired urinary tract infection in near future 23 .

According to the previous reports from different hospitals in Iran, ESBL producing Enterobacteriaceae have been common in the last decade 24-27. Indeed, resistance to carbapenems has been uncommon. Only 58.4% of Klebsiella pneumoniae isolates were sensitive to imipenem 28. In the present study, resistance to imipenem was 19.3% which showed that the resistance to carbapenems in Iran is increasing faster than in European countries and that the uncontrolled use of this antibiotic warns about further resistance in near future. In the United States, carbapenem-resistant Enterobacteriaceae have been reported more commonly over the last years. The emergence of carbapenemase has contributed to an increased prevalence of carbapenem-resistant Enterobacteriaceae 29 . Studies performed in some Asian, African, and South American countries also have shown the global increase in MDR Enterobacteriaceae 30-32.

In a study from Kuwait in 2004, those species of Enterobacteriaceae causing community-acquired UTI showed increased resistance to ciprofloxacin and gentamicin 33. Another study from Kuwait in 2009, showed the increased resistance of those species of Enterobacteriaceae causing nosocomial and community-acquired UTI to ciprofloxacin and piperacillin. In the above study, the multidrug resistance of E. coli and Klebsiella was observed in one third of both nosocomial and community-acquired infections. The ESBL producing species in nosocomial infections were more than those in community-acquired infections and the highest sensitivity was observed against carbapenems, piperacillin/tazobactam, and nitrofurantoin 30.

In a study by Khanfar in Saudi Arabia in 2009, all isolated types of E. coli and Klebsiella were sensitive to imipenem, however, the highest resistance was observed against ciprofloxacin and aminoglycosides 31. The studies performed on community-acquired UTI in Senegal, Mexico, Madagascar, and Nicaragua have shown increased Enterobacteriaceae resistance in community-acquired infections especially against cotrimoxazole and ciprofloxacin 32,34-36 .

In general, various studies have shown that the prevalence of MDR Enterobacteriaceae in nosocomial and community-acquired infections is increasing in Iran and different parts of the world.

Conclusion

The Enterobacteriaceae resistance to quinolones and carbapenems and its multidrug resistance in nosocomial and community-acquired infections are increasing in our region. To overcome these problems, the trend of Enterobacteriaceae resistance must be continually reassessed in future years due to the probable increase in resistance to new beta-lactams and quinolones.

In order to use antibiotics properly, awareness of epidemiological information on antibiotic resistance is helpful. Moreover appropriate guidelines for empirical treatment of community-acquired infections can prevent uncontrolled use of antibiotics and reduce the increasing process of antibiotic resistance in future.

Acknowledgments

The authors appreciate the authorities of infection control units of the hospitals and microbiology laboratory of Sina Hospital for their cooperation in providing required information.

Conflict of interest statement

There was no conflict of interest for authors in this project. 

Funding

No financial support was provided.

References

  1. Brooks GF, Carroll KC, Butel JS, Morse SA. Jawetz, Melnick & Adelbergs Medical Microbiology. 24th ed. New York: McGraw-Hill; 2007.
  2. Coello R, Gastmeier P, de Boer AS. Surveillance of hospital-acquired infection in England, Germany, and The Netherlands: will international comparison of rates be possible? Infect Control Hosp Epidemiol. 2001; 22:393-397.
  3. Zinner SH. Changing epidemiology of infections in patients with neutropenia and cancer: emphasis on gram-positive and resistant bacteria. Clin Infect Dis. 1999; 29:490-494.
  4. Vayalumkal JV, Streitenberger L, Wray R, Goldman C, Freeman R, Drews S et al .Survey of isolation practices at a tertiary care pediatric hospital. Am J Infect Control. 2007;35:207-211.
  5. Aminzadeh Z, Zare-Dehabadi M, Gachkar L, Shah-Hoseini H. Frequency of gram-negative bacilli and their antimicrobial resistance patterns in Loghman Hospital. Iran J Infect Trop Dis. 2006; 10:27-33.
  6. Hashemi SH, Mamani M, Jamal-Omidi S, Niayesh A. Nosocomial bacterial infections and their antimicrobial resistance patterns in university hospitals of Hamadan, Iran. J Res Health Sci. 2010;10(1):54-58.
  7. Forbes BA, Sahm DF, Weissfeld AS. Bailey & Scotts Diagnostic Microbiology. 12th ed. Philadelphia: Elsevier Mosby; 2007.
  8. CLSI. Performance standards for antimicrobial susceptibility testing. 18th informational supplement. Wayne, PA: Clinical and Laboratory Standards Institute; 2008.
  9. Ducel G, Fobry J, Nicolle L. Prevention of hospital-cquired infections: a practical guide. 2nd ed, Geneva: WHO; 2002.
  10. Hadadi A, Rasoulinejad M, Maleki Z, Yonesian M, Shirani A, Kourorian Z. Antimicrobial resistance pattern of gram-negative bacilli of nosocomial origin at 2 university hospital in Iran. Diagn Microbiol Infect Dis. 2008;60:301-305.
  11. Shanthi M, Sekar U. Extended spectrum beta lactamase producing Escherichia coli and Klebsiella pneumoniae: risk factors for infection and impact of resistance on outcomes. J Assoc Physicians India. 2010;58 Suppl:41-44.
  12. Kunz AN, Brook I. Emerging resistant gram-negative aerobic bacilli in hospital-acquired infections. Chemotherapy. 2010;56:492-500.
  13. Tsay R, Siu LK, Fung CP, Chang FY. Characteristics of bacteremia between community-acquired and nosocomial Klebsiella pneumoniae infection. Arch Intern Med. 2002;162:1021-1027.
  14. Yinnon AM, Butnaru A, Raveh D, Jerassy Z, Rudensky B. Klebsiella bacteraemia: community versus nosocomial infection. QJM. 1996; 89:933-941.
  15. Wang Z, Ji W, Guo HB, Tao YZ, Ding YF. Comparative studies on the composition and antibiotic-resistance of pathogenic bacteria between children with community-acquired and hospital-acquired pneumonia. Zhonghua Yu Fang Yi Xue Za Zhi. 2011;45:211-216.
  16. Kang CI, Kim SH, Bang JW, Kim HB, Kim NJ, Kim EC, et al. Community-acquired versus nosocomial klebsiella pneumonia bacteremia: clinical features, treatment outcomes, and clinical implication of antimicrobial resistance. J Korean Med Sci. 2006;21:816-822.
  17. Cagnacci S, Gualco L, Debbia E, Schito GC, Marchese A. European emergence of ciprofloxacin-resistant Escherichia coli clonal groups O25:H4-ST 131 and O15:K52:H1 causing community-acquired uncomplicated cystitis. J Clin Microbiol. 2008;46:2605-2612.
  18. Woodford N, Ward ME, Kaufmann ME, Turton J, Fagan EJ, James D et al. Community and hospital spread of Escherichia coli producing CTX-M extended-spectrum b-lactamases in the UK. J Antimicrobial Chemother .2004;54:735-743.
  19. Tsai SS, Huang JC, Chen ST, Sun JH, Wang CC, Lin SF, et al. Characteristics of Klebsiella pneumoniae bacteremia in community-acquired and nosocomial infections in diabetic patients. Chang Gung Med J. 2010;33:532-539.
  20. Wollheim C, Guerra IM, Conte VD, Hoffman SP, Schreiner FJ, Delamare AP, et al. Nosocomial and community infections due to class A extended-spectrum β-lactamase (ESBLA)-producing Escherichia coli and Klebsiella spp. in southern Brazil. Braz J Infect Dis .2011;15(2):138-143.
  21. Pitout JD, Laupland KB. Extended-spectrum β-lactamase-producing enterobacteriaceae: an emerging public-health concern. Lancet Infect Dis. 2008;8:159-166.
  22. Hawser SP, Bouchillon SK, Hoban DJ, Badal RE, Cantón R, Baquero F. Incidence and antimicrobial susceptibility of Escherichia coli and Klebsiella pneumoniae with extended-spectrum-lactamases in community- and hospital-associated intra-abdominal infections in Europe: results of the 2008 study for monitoring antimicrobial resistance trends. Antimicrob Agents Chemother. 2010;54:3043-3046.
  23. Pitout JD. Infections with extended-spectrum beta-lactamase-producing enterobacteriaceae: changing epidemiology and drug treatment choices. Drugs. 2010;70:313-333.
  24. Feizabadi MM, Etemadi G, Yadegarinia D, Rahmati M, Shabanpoor S, Bokaei S. Antibiotic-resistance patterns and frequency of extended-spectrum beta-lactamase-producing isolates of Klebsiella pneumoniae in Tehran. Med Sci Monit. 2006;12(11):362-365.
  25. Mirsalehian A, Akbari Nakhjavani F, Peymani A.,Jabal Ameli Fereshteh,Mirafshar S.M.,Hamidian M. Frequency of extended spectrum b-lactamase producing Enterobacteriaceae in intensive care units. Tehran University Medical Journal. 2007;65(1):33-38.

    Bazzaz BS, Naderinasab M, Mohamadpoor AH, Farshadzadeh Z, Ahmadi S, Yousefi F. The prevalence of extended-spectrum beta-lactamase-producing Escherichia coli and Klebsiella pneumoniae among clinical isolates from a general hospital in Iran. Acta Microbiol Immunol Hung. 2009;56(1):89-99.

  26. Mansouri S, Abbasi S. Prevalence of multiple drug resistant clinical isolates of extended-spectrum beta- lactamase producing Enterobacteriaceae in Southeast Iran. Iran J Med Sci. 2010;35(2):101-108.
  27. Khourshidi A, Sharif AR. Imipenem resistance among gram-negative and gram-positive bacteria in hospitalized patients. Iranian J Publ Health 2010;39(2):110-113.
  28. Gupta N, Limbago BM, Patel JB, Kallen AJ. Carbapenem-resistant Enterobacteriaceae: epidemiology and prevention. Clin Infect Dis. 2011;53(1):60-67.
  29. Benwan K, Sweih N, Rotimi VO. Etiology and antibiotic susceptibility patterns of community- and hospital-acquired urinary tract infections in a general hospital in Kuwait. Med Princ Pract. 2010;19:440-446.
  30. Khanfar HS, Bindayna KM, Senok AC, Botta GA. Extended spectrum beta-lactamases (ESBL) in Escherichia coli and Klebsiella pneumoniae: trends in the hospital and community settings. J Infect Dev Ctries .2009; 3:295-299.
  31. Sire JM, Nabeth P, Perrier-Gros-Claude JD, Bahsoun I, Siby T, Macondo EA, et al. Antimicrobial resistance in outpatient Escherichia coli urinary isolates in Dakar, Senegal. J Infect Dev Ctries. 2007;1(3):263-268.
  32. Dimitrov TS, Udo EE, Emara M, Awni F, Passadilla R. Etiology and Antibiotic Susceptibility Patterns of Community-Acquired Urinary Tract Infections in a Kuwait Hospital. Med Princ Pract. 2004;13:334-339.
  33. Arredondo-García JL, Amábile-Cuevas CF. High resistance prevalence towards ampicillin, co-trimoxazole and ciprofloxacin, among uropathogenic Escherichia coli isolates in Mexico City. J Infect Developing Countries. 2008;2:350-353.
  34. Randrianirina F, Soares JL, Carod JF, Ratsima E, Thonnier V, Combe P, et al. Antimicrobial resistance among uropathogens that cause community-acquired urinary tract infections in Antananarivo, Madagascar. J Antimicrob Chemother. 2007;59:309-312.
  35. Bours PHA, Polak R, Hoepelman AIM, Delgado E, Jarquin A, Matute AJ. Increasing resistance in community-acquired urinary tract infections in Latin America, five years after the implementation of national therapeutic guidelines. Int J Infect Dis. 2010;14:e770-e777.


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