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Cirugía y cirujanos

On-line version ISSN 2444-054XPrint version ISSN 0009-7411

Cir. cir. vol.87 n.2 Ciudad de México Mar./Apr. 2019  Epub Nov 29, 2021

https://doi.org/10.24875/ciru.18000494 

Original articles

Antibiotic resistance: Microbiological profile of urinary tract infections in Mexico

Resistencia a antibióticos: Perfil microbiológico de las infecciones de vías urinarias en México

Erick Sierra-Díaz1  * 

Cesar J. Hernández-Ríos1 

Alejandro Bravo-Cuellar2 

1Departamento de Urología, UMAE Hospital de Especialidades Centro Medico Nacional de Occidente. Instituto Mexicano del Seguro Social, Guadalajara, Jalisco, México

2Departamento de Inmunología, Centro de Investigación Biomédica de Occidente. Instituto Mexicano del Seguro Social, Guadalajara, Jalisco, México


Abstract

Objective:

The objective of this study was to describe the prevalence, microbiological profile, bacterial resistance, and the sensitivity to antibiotics of microorganisms causing urinary tract infection (UTI) at a single-site tertiary referral hospital in the western region of Mexico.

Methods:

A total of 5895 culture samples processed at the microbiology laboratory from August 1, 2014, to July 31, 2015, were analyzed.

Results:

A total of 5895 samples for urine cultures (UC) were collected, of which 3363 were taken in women (57.05%) and 2532 in men (42.95%). A prevalence of 24% was calculated. From 1444 positive UC, 1512 microorganisms were isolated; the major etiological agent was Escherichia coli, representing 67.28% followed by Pseudomonas with 7.12%. With respect to fungi, Candida glabrata was found as the most common agent. Susceptibility to daptomycin and linezolid was 100%, and meropenem, 91.4%. Highest antimicrobial resistance was found for ampicillin (77.47%) and moxifloxacin (72.89%). Nearly 49% of E. coli strains and 27% of Klebsiella pneumoniae strains showed extended-spectrum beta-lactamase (ESBL) production.

Conclusions:

Bacterial UTI persists as one of the most common infections affecting all age groups and both genders. As in other countries, E. coli ranks first in Mexico, with 67.28%, and nearly 50% of the strains produce ESBL.

KEY WORDS Urinary tract infections; Antibiotic sensitivity and resistance; Extended-spectrum beta-lactamase-producing bacteria

Resumen

Objetivo:

Describir la prevalencia, el perfil microbiológico, la resistencia y la sensibilidad a los antibióticos de microorganismos causantes de infecciones de vías urinarias en un centro de referencia de tercer nivel en el occidente de México.

Método:

Se realizó un estudio transversal que incluyó 5895 urocultivos procesados en el laboratorio de microbiología del 1 de agosto de 2014 al 31 de julio de 2015.

Resultados:

De los 5895 urocultivos, 3363 correspondieron a mujeres (57.05%) y 2532 a varones (42.95%). De los 1444 resultados positivos, se aislaron 1512 microorganismos (prevalencia del 24%); el más común fue Escherichia coli, con un 67.28%, seguido por Pseudomonas con un 7.12%. Candida glabrata se reportó como el patógeno fúngico más frecuente. De manera general, la sensibilidad a la daptomicina y al linezolid fue del 100%, y al meropenem fue del 91.4%. La resistencia más alta se reportó para ampicilina y moxifloxacino (77.47 y 72.89%, respetivamente). Cerca del 49% y del 27% de las cepas de E. coli y Klebsiella pneumoniae mostraron producción de betalactamasas de espectro extendido.

Conclusiones:

Las infecciones de vías urinarias persisten como una de las formas más habituales de infección y afectan a todos los grupos de edad. En México, al igual que en otros países, E. coli se coloca en primer lugar de frecuencia, con el 67.28%.

PALABRAS CLAVE Infección de vías urinarias; Sensibilidad y resistencia a antibióticos; Bacterias productoras de betalactamasas de espectro extendido

Introduction

The increasing rate of antibiotic resistance in uropathogens, especially in Escherichia coli and Klebsiella pneumoniae as the most common etiologic agents of urinary tract infections (UTI), leads to difficulties in selecting adequate empirical therapy and achieving treatment success1. Since sulfonamide and penicillin were introduced into clinical use in the 1930s and 1940s, respectively, people was motivated by the illusion that infectious diseases were totally controlled by antibiotics. The widespread use of antibiotics, however, imposes strong selection pressure for the development of antibiotic resistance, a major, present-day public health problem2. In recent years, the problem has worsened due to the emergence of extended-spectrum beta-lactamases (ESBL), which mediate resistance to b-lactam antimicrobials, especially the third-generation cephalosporins among these organisms. Genes responsible for ESBL production arise by point mutation at the active site of the earlier b-lactamases and are usually plasmid mediated. In addition, ESBL-positive and Gram-negative bacteria often carry genes that confer high levels of resistance to many other antibiotics3.

A summary of several international surveillance systems that have reported uropathogenic E. coli resistance to selected antibiotics in North and South America and Europe reports that there is considerable local variation in resistance. Resistance to ampicillin and trimethoprim ranges from 80% and 61% in Mexico to 33% and 9% in Quebec. In Mexico, resistance to ciprofloxacin has been reported at 72%4.

There are many reports in the literature describing the epidemiology of bacterial resistance; however, the microbiologic profile varies from place to place. At our institution, there are no reports on antibiotic resistance and susceptibility trends. The aim of this study was to examine the epidemiological data obtained from isolated bacteria in urine samples from patients at our hospital over a 1-year period. Data included the susceptibility, resistance, and prevalence of ESBL-producing bacteria and fungi.

Methods

A cross-sectional study was carried out with results from urine samples obtained from hospitalized and outpatients at the Western National Medical Center in Jalisco, Mexico, from August 2014 to July 2015. Samples were processed and analyzed in the Hospital's Microbiology Laboratory. The presence of †105 colony-forming units/mL in urine culture (UC) media was considered significant for UTI. Isolated bacteria and antibiotic susceptibility were identified by standard laboratory techniques or an automated system (Vitek, Biomerieux®) as required.

Inadequate urine samples were excluded from the study: those not processed 1 h after collection, insufficient urine, or urine that was not well labeled. Results with more than 3 pathogens were also excluded.

The Microsoft Excel® program was utilized to analyze data to obtain demographic data from patients such as gender and age (averages and ranges). The prevalence and percentages of sensitivity and resistance were calculated with basic arithmetic operations. The study was approved by the Institutional Ethics Committee with registration number R-2015-1310-185.

Results

Demographic characteristics

A cross-sectional study was conducted with the objective of describing prevalence, microbiological profile, susceptibility, and resistance to antibiotics in UTI. A total of 5895 UC results were collected. Among the results analyzed, 3363 were of women (57.05%) and 2532 men (42.95%). Mean age was 53 years, with a range of 15-102 years. Of the UC performed, 24.5% (n = 1444) were positive. Based on the total number of patients and the number of positive cases, a prevalence of 24% was calculated. From 3363 UC performed in women, 25.9% (n = 872) were positive; for the group of men, 22.5% (n = 572) were positive of a total of 2532 UC.

Microbiological profile

A total of 1512 bacteria and fungi were isolated; two microorganisms were isolated in 68 samples. The most common etiological agent was E. coli representing 67.2% (n = 983), and with regard to isolated fungi, Candida glabrata was reported as the most common agent. Table 1 reveals the distribution and percentages of isolated etiologic microorganisms.

Table 1 Etiologic agents 

Microorganism n (%)
Isolated bacteria 1461 (96.63)
Escherichia coli 983 (67.28)
Pseudomonas 104 (7.12)
Klebsiella 94 (6.43)
Enterococcus 88 (6.02)
Proteus 45 (3.08)
Staphylococcus 29 (1.98)
Acinetobacter baumanii 28 (1.92)
Enterobacter 25 (1.71)
Morganella morganii 19 (1.30)
Citrobacter freundii 18 (1.30)
Providentia 13 (0.89)
Streptococcus 7 (0.48)
Others 8(0.55)
Isolated fungi 51 (3.37)
Candida glabrata 18 (35.29)
Candida albicans 11 (21.57)
Candida krusei 9 (17.65)
Trichorosporon beigelli 8 (15.69)
Others 4 (7.84)

Of 1512 isolated pathogens, 96.63% were bacterial agents (n = 1461) and 3.37% fungi (n = 51). Of 1461 isolated bacteria, Escherichia coli showed 67.28% (n = 983) followed by Pseudomonas and Klebsiella.

Of 51 fungi isolated, C. glabrata was the most common (35.29%), followed by Candida albicans, Candida krusei, and Trichosporon beigelii.

Sensitivity and resistance to antibiotics

The sensitivity and resistance of isolated microorganisms were reviewed for 34 antibiotics, highlighting daptomycin and linezolid, both with 100% sensitivity. Carbapenems were tested in >1300 cases, reporting sensitivities of >90%. Table 2 details the number of tests conducted by antibiotic and sensitivity percentage for the microorganisms.

Table 2 Susceptibility to antimicrobials 

Antimicrobial Total Susceptible (%) Antimicrobial Total Susceptible (%)
Daptomycin 124 124 (100.00) Cefotaxime 1335 595 (44.57)
Linezolid 124 124 (100.00) Cefazolin 1232 543 (44.07)
Meropenem 1364 1247 (91.42) Ceftriaxone 1364 599 (43.91)
Imipenem 1336 1220 (91.32) Cefuroxime 1307 556 (42.54)
Cefotetan 1203 1092 (90.77) Trimethoprim/sulfamethoxazole 1260 467 (37.06)
Vancomycin 117 105 (89.74) Synercid 117 43 (36.75)
Amikacin 1335 1163 (87.12) Levofloxacine 1459 412 (28.24)
Piperacilin/tazobactam 1307 989 (75.67) Amoxicillin/clavulanic acid 29 8 (27.59)
Gentamicin 1348 769 (57.05) Moxifloxacin 1210 317 (26.20)
Ticarcilline/clavulanic acid 1335 744 (55.73) Ampicillin/sulbactam 1260 330 (26.19)
Cefepime 1364 698 (51.17) Ciprofloxacin 1452 374 (25.76)
Aztreonam 1307 582 (44.53) Ampicillin 1327 276 (20.80)
Ceftazidime 1364 608 (44.57)

Similarly, antibiotic resistance was determined. Observed data demonstrated that ampicillin, moxifloxacin, and levofloxacin exhibited resistances in >70% in >1200 cases. Table 3 reports the details of antibiotic resistance.

Table 3 Resistance to antimicrobials 

Antimicrobial Total Resistant (%) Antimicrobial Total Resistant (%)
Ampicillin 1327 1028 (77.47) Gentamicin 1348 640 (47.48)
Moxifloxacin 1210 882 (72.89) Cefepime 1364 649 (47.58)
Ciprofloxacin 1452 1058 (72.87) Cefuroxime 1307 617 (47.21)
Amoxicilin/clavulanic acid 29 21 (72.41) Ticarcilline/clavulanic acid 1335 203 (15.21)
Levofloxacin 1459 1012 (69.36) Vancomycin 117 12 (10.26)
Trimethoprim/sulfamethoxazole 1260 792 (62.86) Amikacin 1335 136 (10.19)
Cefazolin 1232 659 (53.49) Imipenem 1336 113 (8.46)
Ampicillin/sulbactam 1260 643 (51.03) Meropenem 1364 101 (7.40)
Cefotaxime 1335 674 (50.49) Piperacilin/tazobactam 1307 75 (5.74)
Ceftriaxone 1364 672 (49.27) Cefotetan 1203 37 (3.08)
Aztreonam 1307 623 (47.67) Daptomycin 124 0 (0.00)
Ceftazidime 1364 649 (47.58) Linezolid 124 0 (0.00)

As mentioned earlier, E. coli was the most prevalent pathogen. Table 4 lists antibiotic sensitivity and resistance to E. coli.

Table 4 Susceptibility of antimicrobials for Escherichia coli 

Antimicrobial S (%) I (%) R (%) Antimicrobial S (%) I (%) R (%)
Imipenem 99.69 0.00 0.31 Ceftriaxone 48.93 1.42 49.64
Meropenem 99.49 0.10 0.41 Cefazoline 45.37 1.63 53.00
Cefotetan 97.25 0.92 1.83 Tobramycin 47.30 10.17 42.52
Amikacin 95.02 2.85 2.14 Cefuroxime 43.64 3.15 53.20
Piperacilin/tazobactam 87.49 8.14 4.37 Trimethoprim/sulfamethoxazole 35.30 0.00 64.70
Ticarcilline/clavulanic acid 63.17 28.38 8.44 Ampicillin/sulbactam 23.70 24.52 51.78
Gentamicin 56.26 0.61 43.13 Levofloxacin 20.45 1.93 77.62
Cefepime 49.95 0.00 50.05 Moxifloxacin 20.45 0.71 78.84
Cefotaxime 49.64 0.71 49.64 Ciprofloxacin 19.94 0.51 79.55
Ceftazidime 49.44 0.10 50.46 Ampicillin 16.89 0.51 82.60
Aztreonam 49.24 0.92 49.85

S: sensible, I: intermediate, R: resistant

Pseudomonas aeruginosa was isolated as the second most common pathogen. It was also observed that the sensitivity index was <35% for the antibiotics tested. Table 5 records the sensitivity and resistance percentage of antibiotics tested for P. aeruginosa, while table 6 registers ESBL-producing bacteria.

Table 5 Susceptibility of antimicrobials for Pseudomonas 

Antimicrobial Susceptible (%) Intermediate (%) Resistant (%)
Cefepime 34.62 0.00 65.38
Meropenem 31.73 0.96 67.31
Imipenem 26.92 0.96 72.12
Gentamicin 25.96 1.92 72.12
Tobramycin 25.00 0.96 74.04
Amikacin 22.12 4.81 73.08
Ciprofloxacin 17.31 0.00 82.69
Levofloxacio 17.31 1.92 80.77
Piperacilin/tazobactam 2.88 88.46 8.65
Aztreonam 0.96 32.69 66.35
Ceftriaxone 0.00 18.27 81.73
Ceftazidime 0.00 31.73 68.27
Cefotaxime 0.00 18.27 81.73
Ticarcilline/clavulanic acid 0.00 32.69 67.31

Table 6 Bacteria producing β actamases of extended spectrum 

Bacteria n (%) Global percentage
Escherichia coli 477/983 (48.52) 29.07
Klebsiella pneumonie 23/94 (27.38) 1.40
Klebsiella oxytoca 1/94 (10.00) 0.06
Proteus mirabilis 2/45 (4.44) 0.12

Discussion

Escherichia coli is the most prevalent facultative Gram-negative bacillus among human fecal flora, usually inhabiting the colon as the innocuous commensal. UTI comprises the most common form of extraintestinal E. coli infection, and E. coli is the most common cause of UTI. At some point during their lives, at least 12% of men and 10-20% of women experience an acute symptomatic UTI, and an even greater number develop asymptomatic bacteriuria5. The susceptibility of uropathogens to various antibiotics or antibiogram profiling may aid in improving the treatment of UTI without any delay. However, there are many microorganisms responsible for UTI. Among these, some with a high rate of resistant ESBL species have gained much attention6. In 2011, Molina-López et al.7 analyzed antimicrobial, serotypes, and phylogenetic groups among strains of E. coli isolated from outpatients with UTI in Mexico City. Among the 29 identified serotypes, the most frequent was 025:H4 (21.2%), which has been associated with multidrug resistance and a high virulence potential.

The uropathogenic strains expressed resistance rates as high as 83% for ampicillin and the lowest resistance rate was for meropenem, with 0.85%7. Our work does not identify the serotypes; however, we can add that 67.28% of isolated bacteria were E. coli, finding the highest index of resistance for ampicillin, with a percentage similar to the resistance reported by Molina-López et al. (83 vs. 82.6%)7. With regard to quinolones and trimethoprim/sulfamethoxazole, our study reported higher resistances.

In another study reported in 2015 by Paniagua-Contreras et al. in Mexico, nearly 48% of E. coli strains were resistant to cephalothin, 97.4% to ampicillin, and 72.7% for cefotaxime; of 188 isolated strains, 96.9% were resistant to at least 3-11 of the antimicrobials studied8.

Miranda-Estrada et al. reported, in 2015, an analysis performed on 107 isolates of E. coli at two locations in Mexico. Resistance to ampicillin and trimethoprim/sulfamethoxazole was 92.5 and 70.1%, respectively9.

López-Banda et al. analyzed antibiotic resistance in 108 isolated E. coli obtained from 2008 to 2010 in Mexico City. Approximately 20% of the isolates registered the presence of b-lactamases. The authors did not report a statistical relationship between multiresistance and phylogenetic group10.

Table 7 presents the comparison of our work with the aforementioned studies conducted in Mexico.

Table 7 Antibiotic resistance in Mexico 

Antibiotics Molina-Lopez et al.7 (n = 119) (%) Paniagua-Contreras et al.8 (n =194) (%) Miranda-Estrada et al.9 (n =107) (%) López-Banda et al.10 (n =108) (%) Sierra-Diaz (n =983) (%)
Ampicillin 83.70 97.4 92.5 55.7 82.6
Ciprofloxacin 56 - 45.8 62.3 79.5
Moxifloxacin - - - 52.6 78.84
Levofloxacin - - - 60.2 77.62
Trimethoprim/sulfamethoxazole 56.40 66 70.1 65.1 64.7
Cefuroxime 15 - 62.6 1.8 53.2
Ceftriaxone 10.20 48.9 18.7 0 49.64
Ceftazidime 9 - 57 0 50.46
Cefotaxime - 72.7 57 0 49.64
Cefepime 7.60 - 15.9 0 50.05
Amikacin 1.70 14.4 14 6.5 2.14
Cefotetan - - - 1.6 1.83
Meropenem 0.85 - - 0 0.41
Imipenem - - - 1.9 0.31

With regard to data on resistance to antibiotics in North America, Foxman4 presented a review in 2010. Table 8 demonstrated the comparison of our study with that reported by Foxman.

Table 8 Antibiotic resistance in North America 

Antibiotic Foxman4 (%) Sierra-Diaz (%)


Canada USA Mexico Mexico
Ampicillin 33 - 80 77.47
Trimethoprim/sulfamethoxazol 9 - 61 62.86
Quinolones 0 5-10 72 71.7a

aAverage: Moxifloxacin, 72.89%; Ciprofloxacin, 72.87%, and Levofloxacin, 69.36%.

The Antimicrobial Resistance Epidemiological Survey on Cystitis study was conducted in nine countries in Europe, as well as in Brazil, to determine the susceptibility of the major uropathogens circulating in the communities of these geographic areas11. The authors reported that not all sites exhibited the same susceptibility profile, with some countries less affected by resistance problems than others. In Germany, Hungary, Poland, and the Netherlands, > 90% of strains were susceptible to fosfomycin, mecillinam, nitrofurantoin, and ciprofloxacin. Susceptibility rates varied widely among countries for ampicillin (32.7-65.5%), amoxicillin/clavulanic acid (51.9-93.5%), cefuroxime (73-93%), and trimethoprim/sulfamethoxazole (54.5-87.8%)12.

In terms of E. coli bacterial resistance specifically, there are reports from other countries13-15. Table 9 shows the analysis and the comparison with our results.

Table 9 E. Coli resistance reported in other countries 

Antibiotics Abujnah et al.3 (Libya) (n = 208) (%) ARESC et al.11 (Europe and Brazil) (n =2315) (%) Can et al.12 (Turkey) (n = 294) (%) Sohail et al.13 (Pakistan) (n = 244) (%) Mamuye et al.14 (Ethiopia) (n = 85) (%) Yilmaz et al.15 (Turkey) (n = 8975) (%) Sierra-Diaz (Mexico) (n = 983) (%)
Ampicillin 69.2 48.3 - - 79.2 66.9 82.6
Ciprofloxacin 23.1 8.1 39 82 54.7 49.9 79.5
Levofloxacin 19.2 - - 82 - 77.62
Trimethoprim/sulfamethoxazole 37 29.4 44 78 22.6 20 64.7
Cefuroxime - 2.4 25 80 - 30.9 53.2
Ceftriaxone 6.7 - - 71 45.3 28 49.64
Ceftazidime 6.7 - - 71 - 14.9 50.46
Cefepime 6.3 - - 71 - 12 50.05
Amikacin 0 - - 91 - 0.3 2.14
Meropenem 0.5 - 0 3 - 0 0.41
Imipenem 0.5 - 0 3 - 0 0.31

Table 10 compares susceptibility profiles between our results and those of other countries16-18 regarding general uropathogens.

Table 10 Uropathogens susceptibility comparison between Mexico and other countries 

Antibiotics Mubanga et al.16 (Lesotho) (n = 200) (%) Stefaniuk et al.17 (Poland) (n = 381) (%) Osthoff et al.18 (Australia) (n = 200) (%) Hernandez & Sierra (Mexico) (n = 983) (%)
Ampicillin - 38.6 - 20.8
Ciprofloxacin 95.1 60.8 70 25.76
Trimethoprim/sulfamethoxazole 32.5 60.2 53 37.06
Cefuroxime - 82.1 - 42.54
Ceftazidime - 88.2 - 44.57
Cefotaxime - 86.5 - 44.57
Cefepime - 91.1 - 51.17
Amikacin - 96 - 87.12
Meropenem - 100 100 91.42

Our study sheds light on useful data including those antibiotics such as daptomycin and linezolid may be effective in the treatment of multidrug-resistant cases because they exhibited no bacteria resistance. Other medications with a low index of resistance comprised cefotetan, piperacillin/tazobactam, and carbapenems with resistance percentages <10. However, it is prudent to analyze the tables of the results obtained in this study at the time of the empirical treatment indicated, due to that the majority of antimicrobial drugs available for oral administration presented resistance percentages of >50 for the majority of the pathogens isolated.

Conclusions

With the described results, it is possible to define an overall panorama of resistance and susceptibility to antibiotics in our working area. This study may also be submitted as a national projection due to the results reported, and it can be concluded that the spectrum of sensitivity and resistance of uropathogenic bacteria to antibiotics coincides partially with those reported by other sources of information at national and international levels. In addition, it is clear that there is more resistance to antibiotics, in general, in our study population, as in other national studies, compared with other countries. Data tables can be useful for the judicious use of antibiotics in our unit.

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FundingThe author(s) received no specific funding for this work. This work was funded by the Instituto Mexicano del Seguro Social. There was no external funding.

Received: May 30, 2018; Accepted: August 14, 2018

*Correspondence: Erick Sierra-Díaz, Tarascos, 3473-240*, Fraccionamiento Monraz, C.P. 44670, Guadalajara, Jalisco, México E-mail: erksland@hotmail.com

Conflicts of interest

The authors declare that they have no conflicts of interest.

Creative Commons License Instituto Nacional de Cardiología Ignacio Chávez. Published by Permanyer. This is an open access article under the CC BY-NC-ND license