High Microbiological Spectrum Resistance Rates in Urine Isolates From Jalisco, Mexico. A Retrospective Study and Literature Review

iMedPub Journals
2015
International Archives of Medicine
http://journals.imed.pub
Section: Microbiology
ISSN: 1755-7682
Vol. 8 No. 148

doi: 10.3823/1747
High Microbiological Spectrum Resistance Rates in

Urine Isolates from Jalisco, Mexico.
A Retrospective Study and Literature Review
Original
Maria G. Zavala-Cerna1, Nicole Macriz-Romero2, Juan F. Santoscoy-Gutierrez2, Leza Naydich1,

Fernando A. Santoscoy-Tovar3, Jose A. Rueda-Cruz3, Olivia Torres-Bugarin1,
Dennis Spalla Morris1, Isidro G. Zavala-Trujillo4
Abstract
Background: Urinary tract infections (UTIs) are a major public health
problem worldwide. In Latin America, most UTIs are treated without
bacteriological identification. Our aim was to examine resistance rates
to commonly prescribed antibiotics, focusing on cases from Jalisco,
Mexico; and additionally to conduct a review of the literature to search
for resistance patterns in other countries of Latin America.
1 School of Medicine, Universidad

Autonoma de Guadalajara PC 45129
Jal. Mxico.
2Facultad de Medicina de la Universidad
Autnoma de Guadalajara PC 45129,
Jal. Mxico.
3Microbiology Department, Unidad
de Patologa Clnica, Guadalajara PC
44650, Jal. Mxico.
4Infectious Disease Division, Hospital
ngel Leao, Universidad Autnoma
de Guadalajara, Guadalajara PC 45200,
Jal. Mxico.
Methods: Retrospective analysis of urine cultures from ambulatory

and hospitalized patients taken from Nov 2012-Nov 2013; susceptibility testing and minimal inhibitory concentration (MIC) was done by
microdilution methodology. For literature search, we reviewed different data bases and included papers in English and Spanish, published
from 2007-2014, representative from the Latin America region.
Results: We obtained 1.206 consecutive samples from outpatient

and inpatient facilities, including adult and pediatric subjects. The
most frequent isolate in all groups was ESBL-producing E. coli with
high resistance rates for ampicillin, TMP-SMX, and ciprofloxacin. In
the literature review we found 15 papers related to resistance rates
of commonly prescribed antibiotics.
Conclusions: The information summarized in this article supports

the finding that resistance rates to commonly prescribed antimicrobial
agents are increasing worldwide. As such, this study challenges the
rationale behind empiric use of antibiotics, emphasizing the need,
whenever possible, to perform urine cultures before initiating antimicrobial treatment.
Under License of Creative Commons Attribution 3.0 License
Contact information:
Maria G. Zavala-Cerna.
Research Professor at Immunology
Department, School of Medicine.
Address: Universidad Autonoma de
Guadalajara ,Av. Patria 1201, Lomas del
Valle Zapopan, Jal. Mexico 45129. 52 333
6488824 . Ext.33152.
g_zavala_78@hotmail.com
Keywords
Antimicrobial resistance;
E. coli; Extended spectrum
beta lactamases; Urine culture.
This article is available at: www.intarchmed.com and www.medbrary.com
ISSN: 1755-7682 J
Background
Urinary tract infections (UTIs) are a major public
health problem in terms of morbidity and financial cost, exceeding that of chronic renal failure
[1]. UTIs have been reported to affect up to 150
million individuals annually worldwide [1-3] and
contribute to >30% of health-care facility associated infections, as annually reported by acute care
hospitals [4]. UTIs are one of the most common
bacterial infections occurring in children and the
most common bacterial infection diagnosed in
women [2, 5, 6]. Prompt recognition and correct
antimicrobial management can relieve symptoms
and prevent more serious sequelae, such as progressive kidney damage [5, 6]. Most UTIs (85%)
are caused by Escherichia coli (E. Coli) and Staphylococcus saprophyticus (10%), with Klebsiella
pneumoniae and the Proteus species accounting
for the majority of the remaining etiologic agents
[1]. In up to 95% of UTI cases, treatment is prescribed without bacteriological identification, even
in the presence of severe symptoms, the choice
of treatment relies on local epidemiologic data
coupled with empirical selection of antibiotics based upon the patients age and gender [2]. Commonly, urine samples are sent for microbiological
evaluation only following treatment failure, or in
presence of recurrent or relapsing infection [1].
Because most UTIs are generally treated empirically, the selection of antimicrobial agent should be
determined not only by the most common pathogen, but also from consideration of risk factors
that may alter that pathogens typical susceptibility
profile. One such risk factor is the production of
extended spectrum beta lactamases [5, 7]. The
acquisition of such beta lactamases may be related
to changes in the bacterial genome by mutation
or acquisition by horizontal transfer of extrachromosomal genetic material [8, 9].
Successful invasion of the urinary tract by bacteria depends on bacterial virulence, inoculum size,
defense mechanisms in the host, and for women,
2015
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hormone effects and changes in the genital microbiota due to female anatomical characteristics
[10, 11]. In cases of community-acquired (CA)
UTIs (defined as those acquired prior to any hospital admission or more than 10 days after any
hospital discharge) [12] the knowledge of local
antimicrobial susceptibility profiles of common
uropathogens is essential for prudent, empiric
treatment [1]. Treatment of UTIs generally includes -lactam antibiotics, fluoroquinolones, nitrofurantoin or trimethoprim/sulfametoxazole (TMP/
SMX). Treatment varies according to patient age
and gender, pathogen implicated, course of disease, and the anatomical area of the urinary tract
involved [3, 13]. While these drugs are successful
in resolving some UTIs, resistance to commonly
prescribed antimicrobial agents is a matter of increasing concern. For example, fluoroquinolone
resistance has been reported in various countries
[3], and evidence provides an association between
quinolone resistance and increased rates for prescription in the community [14]. Indeed, in the span
of a decade (1997-2007), fluoroquinolone use in
Latin America has dramatically increased, with
consumption rates having doubled or tripled during this period in some countries [15, 16]; more
importantly, a strong trend indicating increased
resistance can be seen worldwide. Because of this
emerging resistance problem, empiric treatments
are likely to become less effective, particularly in
an outpatient setting where patient follow-up
may be limited or nonexistent [7]. Thus, given the
changing spectrum of microorganisms involved
in the development of UTIs and the emergence
of acquired microbial agent resistance, there is a
heightened need for more rigorous patient screening to guide empiric therapy [2]. Additionally, local data regarding pathogen susceptibility profiles
with respect to antimicrobial agents coupled with
knowledge of common UTI risk factors in a particular locale is expected to lead to better tailoring
and more effective empiric treatment protocols
ISSN: 1755-7682
[3]. Our aim was to examine resistance rates of

urine isolates to commonly prescribed antibiotics,
focusing on cases in Jalisco, Mexico; additionally
to conduct a review of the literature to search
for resistance patterns in other countries of Latin
America.
Methods
We conducted a retrospective analysis of data from
the microbiology laboratory at Unidad de Patologa Clnica (UPC), in Guadalajara, Jalisco, Mexico,
which is a reference laboratory in Mexico certified
by the College of American Pathologists in the Laboratory Accreditation Program since 2000.
All microbiological reports on bacterial pathogens
between November 2012 and November 2013 from
the state of Jalisco were included in this study.
Sample collection
In all cases, urine was collected by either clean catch
method or bladder catheterization; samples were
conserved at room temperature for no more than 2
hours before they were analyzed. Samples analyzed
contained >25 white blood cells per microliter, and
resulted in only one pathogenic micro-organism
with counts of >100,000 colony forming units per
milliliter. The decision to perform a urine culture was
made by the attending physicians.
Microbiological Analyses
Standard techniques were used for culture and
identification of pathogens [17]. Non-susceptibility testing and minimal inhibitory concentration
(MIC) was performed by microdilution methodology [MicroScan panels (Siemens, Sacramento, CA,
USA)]. Inhibition for each isolate was defined as
susceptible, intermediate or resistant, according to
the guidelines of the Clinical and Laboratory Standards Institute (CLSI) [18]. Antimicrobials tested
were amikacin, ampicillin, ampicillin/sulbactam,
amoxicillin/clavulanate (AMOX/CALV), cefotaxime, cefoxitin, ceftazidime, ceftriaxone, cefuroxime, ciprofloxacin, chloramphenicol, ertapenem,
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gentamycin, imipenem, levofloxacin, meropenem,

piperacillin, piperacillin/tazobactam (PIP/TAZ), tetracycline, ticarcilin/clavulanate, tigecyclin, nitrofurantoin, trimetropim/sulfametoxazole (TMP/SMX)
and tobramycin.
MicroScan panels comprise dehydrated panels for
microdilution antibiotic susceptibility. Those used
for ESBL detection which contains combinations of
ceftazidime or cefotaxime plus -lactamase inhibitors have received Food and Drug Administration
approval; and in studies of large numbers of ESBLproducing isolates, they have appeared to be highly
reliable.
Screening for ESBL producers

We used the LabPro software which is capable
of identifying ESBL strains by phenotypic conformation with ceftazidime, ceftazidime/clavulanate,
cefotaxime and cefotaxime/clavulanate, as recommended by the CLSI [19]. Growth at or above the
screening antibiotic concentration was suspicious
of ESBL production and an indication for the organism to be tested by a phenotypic confirmatory
test.
The phenotype confirmatory test for ESBL production was performed with use of MicroScan
panels using ceftazidime (0.25-128 g/mL), ceftazidime plus clavulanic acid (0.25/4 - 128/4 g/mL),
cefotaxime (0.25-64 g/mL), or cefotaxime plus
clavulanic acid (0.25/4 - 64/4 g/mL), against the
isolates, phenotypic confirmation of ESBL producers was considered as 3 twofold serial-dilution
decreases in minimum inhibitory concentration
(MIC) of either cephalosporin in the presence of
clavulanic acid compared to its MIC when tested
alone.
Study groups
Children and adults were assessed separately. Four
(4) groups were established for this purpose: 1) Outpatient adults (OA), 2) Inpatient adults (IA), 3) Outpatient Pediatric (OP) and 4) Inpatient Pediatric (IP).
2015
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Statistics
For descriptive purposes, mean and standard deviation calculations were used for nominal variables
and proportions for categorical variables. GraphPad
Prism (5th version) software was used for statistical
analysis and figure design.
84.9% of the cases (90) were outpatients (OP) and

15.1% (16) were inpatients (IP). Age and gender
comparisons from each of the four analysis groups
are set forth in Table 1.
Table 1. D
emographic characteristics of the study
population.
Ethics
Adults (n= 1100)
The present study was registered and approved by

the ethics committee of the Hospital Angel Leao,
Universidad Autnoma de Guadalajara and patient
data was managed anonymously to protect privacy.
Literature review
Female sex
(%)
We reviewed data from the available medical literature. A systematic search of papers was performed from data bases PUBMED, Clinical Key Elsevier,
and ProQuest. We used the following search terms:
Urine culture, Uropathogenic E. coli, ESBL,
Antimicrobial resistance and Latin America. We
included all papers that fall into the scope of the
present review written in English and Spanish, obtained with dates from 2007 through 2014.
Results
Study population
A total of 1.206 positive consecutive samples were
analyzed from the following five metropolitan zones
located in the state of Jalisco, Mexico: 1) Metropolitan zone of Guadalajara (Guadalajara, Ixtlahuacan,
Tlaquepaque, Tonal, Tlajomulco, and Zapopan), 2)
Metropolitan zone of Puerto Vallarta (Bahia de Banderas), 3) Metropolitan zone of Tepatitln (Tepatitln and Arandas), 4) Metropolitan zone of Ocotln
(Ocotln and Poncitln) and 5) Metropolitan zone
of Autln (Autln de Navarro).
The proportion of adults (n=1100) was higher
compared to children < 18 years of age (n=106).
Among adults, 91.5% of the cases (1,006) corresponded to outpatients (OA), and 8.5% of the cases
(94) were inpatients (IA). In the pediatric population
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Pediatric (n= 106)
OA
IA
OP
IP
n (%)
1006 (91.5)
94 (8.5)
90 (84.9)
16 (15.1)
Age
(meanSD)
60.419.7 62.321.3
5.34.3
2.21.9
86.7
70.6
82.7
49.5
OA outpatient adults, IA inpatient adults, OP outpatient

pediatric, IP inpatient pediatric, SD standard deviation.
Microbiologic spectrum
The most frequent bacterial isolate in this study
was ESBL-producing E. coli. The overall incidence of
this pathogen was 68.3% (824/1.206), with similar proportions amongst the four analysis groups:
OA (69.5%), IA (72.4%), OP (53.3%) and IP (50%);
followed by non-producing ESBL E. coli. Table 2
provides the most frequently found pathogens in
urine cultures.
Antibiotic resistance
In line with the determination that the most common bacterial isolate found was ESBL-producing
E. coli, elevated rates of resistance in this bacteria were likewise found in adult outpatients/
inpatients to commonly prescribed drugs like
ampicilline/sulbactam (100/100%), ceftriaxone (66.1/72.1%), trimethoprim sulfametoxazole
(TMP/SMX) (64.8/55.9%) and to ciprofloxacin
(85.7/92.6%). These elevated resistance rates were
also found in children, from both inpatients/outpatients: ampicillin/sulbactam (100/100%), ceftriaxone (54.2/37.5%), TMP/SMX (72.9/62.5%),
and ciprofloxacin (60.4/50.0%). With respect to
non-ESBL E. coli, resistance rates were significant
2015
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Table 2. Frequencies of pathogens found in urine

cultures among different groups.
Adults (n= 1100)
OA
IA
(n=1006) (n=94)
n (%)
700(69.5) 68 (72.4)
Pediatric (n= 106)

OP
IP
(n= 90)
(n= 16 )
n (%)
48 (53.3) 8 (50.0)
ESBL E. coli
Non-ESBL
251 (25.0) 19(20.2) 33 (36.7) 4 (25.0)
E. coli
Klebsiella
10 (1.0)
2 (2.1)
1 (1.1)
2 (12.4)
ozanae
Klebsiella
15 (1.5)
2 (2.1)
1 (1.1)
0 (0)
pneumoniae
Morganella
19 (1.9)
2 (2.1)
2 (2.2)
1 (6.3)
morgani
Proteus
11 (1.1)
1 (1.1)
5 (5.6)
1 (6.3)
mirabilis
OA outpatient adults, IA inpatient adults, OP outpatient
pediatric, IP inpatient pediatric, SD standard deviation.
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but not as elevated as those for ESBL-producing E.

coli, except for a significant proportion of isolates
that were found to be resistant to ciprofloxacin
in adults (47.8-47.4%) and, to a lesser extent,
in children (15.2-25%). Conversely, susceptibility
rates within E. coli isolates (both ESBL and nonESBL producers) were >95% for carbapenems
and >69% for nitrofurantoin. A complete appreciation of the antimicrobial resistance from ESBL
E. coli and non-ESBL E. coli is set forth in Figure
1. More detailed information on ESBL and nonESBL E. coli, Klebsiella, Morganella, and Proteus
bacteria is provided in the Table 4 for adults and
Table 5 for the pediatric group.
Figure 1: A
ntimicrobial resistance of extended spectrum beta lactamases (ESBL) and non-ESBL E. coli to most
common prescribing drugs for urinary tract infections treatment.
Amikacin (AMK), gentamicin (GEN), ampicillin sulbactam (AMP/SUL), ampicillin (AMP), cefuroxime (CEF), ciprofloxacin (CIPRO), levofloxacin (LEVO),
trimethoprim sulfametoxazole (TMP/SMX) and nitrofurantoin (NITRO).
ISSN: 1755-7682 J
Literature review
We found 15 different studies performed in Latin
America from 2007-2014; in Mexico, data regarding
the epidemiology of ESBL-producing enterobacteriaceae, most specifically, ESBL-producing E. coli, is
scarce, in both outpatient and inpatient settings.
After reviewing studies performed in Latin America,
we confirmed the presence of high resistance rates
to commonly prescribed antimicrobial agents. Table
3 summarizes different studies results performed in
different countries from America with resistance rates of E. coli isolated from urine cultures. Infections
comprising resistant E. coli are typically associated
with increased age of patient, hospitalization, recent
antibiotic use, chronic medical conditions, surgery,
and immunosuppression. The high resistance rates
reported in Mexico, as well as those from other
studies in this region, demonstrate a need to better
characterize pathogenic isolates in UTI cases.
Discussion
There is a recognized significant challenge with antimicrobial resistance among important gram-negative organisms including E. coli worldwide [20].
In recent years, extended-spectrum -lactamases
(ESBLs) have increased in type and frequency, such
as enterobacteriaceae and carbapenemases, which
have resulted in a worldwide dissemination of such
extended spectrum -lactamases producing strains
[21]; production of extended spectrum -lactamases
(ESBLs) is currently a matter of increasing global
concern [5, 22]. Ruppe and Cols identified that the
occurrence of UTI caused by ESBL E. coli in women
who were not exposed to antibiotics was linked to
the relative amount of fecal ESBL E. coli [23].
Results from our study echoes previous reports
finding the main causative organism of UTIs to be
E. coli [24]. But perhaps most importantly, we found
an even higher proportion of E. coli producers of
ESBL in the isolates examined in here. This finding
corresponds with previous studies not only in the
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Latin American region [15], but also from the Asia/

Pacific region (where India, China and Thailand reported the highest prevalence rates of ESBL-producing E. coli: 79.0%, 55.0% and 50.8% respectively
[25]). In contrast, the results from this study differ
from those conducted in other parts of the world,
mainly North America and Europe; for example, in a
study performed in Scotland on enterobacteriaceae
isolates, only 7.5% of the isolates were phenotypically confirmed ESBL producers [26]. Nevertheless,
Kassakian et al [27] recently reported an increase in
the prevalence of community-acquired and healthcare-associated infections in the U.S. due to ESBLproducing bacteria, particularly urinary tract infections due to ESBL-producing E. coli, with notably
high resistance rates to ciprofloxacin (95%). Thus,
further study of ESBL-producing enterobacterieae,
particularly ESBL-producing E. coli, continues to appear highly warranted.
The discrepancies encountered in different parts
of the world may be attributed to antimicrobial
distribution practices. This especially holds true in
countries that forego prescriptions altogether and
permit sales of such drugs over-the-counter. For
example, the practice in Mxico was to sell antimicrobials over-the-counter until 2010, at which time
physician prescriptions became a requirement. Importantly, some studies have identified international
travel as a risk factor for the colonization by and infection with resistant E. coli [6, 22, 28]. This finding
highlights the importance of recognizing resistance
patterns in different parts of the world, particularly
in places where tourism attracts many international
travelers.
ESBL are beta-lactamases that hydrolyze extended spectrum cephalosporins with an oxyimino
side chain [6]. Community acquisition of ESBLproducing E. coli was first reported in Ireland in
1998, where an ESBL producing nalidixic acidresistant uropathogenic E. coli strain was isolated
from an elderly patient who did not have a recent
history of hospitalization. Since then, ESBL-produThis article is available at: www.intarchmed.com and www.medbrary.com
2015
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Table 3. Resistance rates (%) in E. coli isolates from urine cultures in different countries of America since 2007.
PIP/TAZ
TMP/SMX
Nitrofurantoin
Imipenem
Meropenem
19
72
MEX
[32]
2007
66
MEX
[33]
2007
59.2
13.2
MEX
[34]
2009
50
55
19
71
66
29.7
13.4
27.6
56.5
8.2
13.4
6.8
14.1
17.2
7.5
43.5
26.4
49.0
71.7
5.6
72.4
41.4
79.3
96.5
51.7
66.7
33.3
66.7
66.7
83.3
83.3
83.3
100
50.0
Amikacin
Ampicillin
AMP/SUL
AMOX/CLAV
Cephazolin
Cephalothin
Cefuroxime
Cefoxitin
Cefotaxime
Ceftriaxone
Ceftazidime
Cefepime
Ciprofloxacin
4th
Pediatric
PUC
80
40
30
17
18
27
Uncomplicated
UTIs
73
23
28
2.5
67.2
13.9
35.6
14.3
3.5
24.7
Outpatients
71
39
24
14
10
Inpatients
83
61
36
16
19
non-ESBL
ESBL
non-ESBL
ESBL
non-ESBL
ESBL
Patients
ICU
PUC
Inpatients Outpatients Uncomplicated

UTIs
PCU
PUC
Outpatients
PUC
4th
Reference
Gatifloxacin
1st
Country Year
Levofloxacin
Quinolones
2nd
3rd
Norfloxacin
Cephalosporins
2do
3rd
MEX
[35]
2010
MEX
2012
MEX
2012
[36]
MEX
2012
2015
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Cefotaxime
Ceftriaxone
Ceftazidime
Cefepime
Ciprofloxacin
Norfloxacin
Levofloxacin
Gatifloxacin
PIP/TAZ
TMP/SMX
Nitrofurantoin
Imipenem
Meropenem
40.8
40.8
14.6
54.4
MEX
[37]
2013
100
100
48
100
100
98
96
MEX
[14]
2013
13.9
0.9
7.7
72.0
21.1
COL
[38]
2007
5.6
1.1
1.1
1.1
22.5
9.4
39.2
1.8
31.6
8.5
5.6
2.8
2.8
2.8
37.6
13
0.6
44.6
1.7
43.9
12.2
9.5
2.4
2.4
2.4
34.1
26.8
46.3
57.4
38.3
44.7
38.9
16.3
33.2
21.3
Outpatients
Inpatients
100
PUC
2.9
90.6
Outpatients
Inpatients
ICU
Cephalothin
AMOX/CLAV
-
Cephazolin
AMP/SUL
44.4
Ampicillin
Amikacin
85
CA
UTIs
4th
Reference
Cefoxitin
21.5
4th
Country Year
Cefuroxime
8.6
37
PUC
Quinolones
2nd
3rd
17.7
1st
40
Outpatients
PUC
Patients
Cephalosporins
2do
3rd
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COL
[39]
2009
BRA
[40]
2014
USA
[41][
2013
GUA
CA UTI
1.4
29.3
10.8
2.5
8.3 46.3
2.9 58.6 2.5
0
2011
ECU
CA UTI
0.9
72
27
8
29
9
3
41
57
7
[42]
2007
CHI
CA UTI
7.5 53.6
31.8
5.6
19.6
6.4 29.6
4
0
0
2009
Complicated and
NIC
18.6
45.5
[43]
2.3 61.4
20.5
31.8
38.6 7.0
uncomplicated UTI
2010
Mexico (Mex), Colombia (Col), Guatemala (GUA), Chile (CHI), Nicaragua (NIC), Ecuador (ECU), Brazil (BRA), Positive urine cultures (PUC), urinary tract infection (UTI), trymetroprim
sulfametoxazole (TMP/SMX) ampicillin sulbactam (AMP/SUL), amoxicillin clavulanate (AMOX/CLAV), piperacilin tazobactam (PIP/TAZ), Emergency department (ED), Centers for
Disease Control and Prevention (CDC), Intensive care unit (ICU), Extended spectrum beta lactamases (ESBL), community acquired (CA).
ED
17.6
27.5
2015
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Table 4. A
ntimicrobial activity against Gram-negative organisms collected
from urine samples in adults from Jalisco, Mexico.
Organism/
antimicrobials
ESBL E. coli n (%)
Amikacin
Gentamicin
Ampicillin/
Sulbactam
Ampicillin
Amoxicilline/
Clavulanate
Ceftazidime
Cefuroxime
Ceftriaxone
Ciprofloxacin
Levofloxacin
Imipenem
Ertapenem
Meropenem
Piperacillin
Piperacillin/
Tazobactam
TMP/SMX
Nitrofurantoin
Non-ESBL E. coli
n (%)
Amikacin
Adult population (n=1100)

Outpatients (n=1006)
Inpatients (n=94)
n
%
n
%
S
I
R
S
I
700 (69.5)
68 (72.4)
700
41.7
49.6
8.7
68
36.7
51.5
700
19.9
18.3
61.2
68
14.7
17.6
11.8
67.7
700
100
68
100
700
0.7
0.1
99.2
68
1.5
4.4
94.1
275
23.6
46.2
30.2
34
20.6
44.1
35.3
700
700
700
700
700
700
425
425
700
25.7
8.0
31.6
13.4
14.7
99.4
98.8
99.8
0.6
15.4
15.0
2.3
0.9
5.4
0.3
0.9
0.2
0.6
58.9
77.0
66.1
85.7
79.9
0.3
0.2
0
98.8
68
68
68
68
68
68
34
34
68
14.7
8.8
25.0
7.4
10.3
98.5
100
100
1.5
19.1
10.3
2.9
0
2.9
0
0
0
2.9
66.2
80.9
72.1
92.6
86.8
1.5
0
0
95.6
699
23.3
28.6
48.1
68
11.7
26.5
61.8
699
698
34.2
81.9
1.0
6.6
64.8
11.5
68
68
41.2
69.1
2.9
8.8
55.9
22.1
251 (25.0)
251
74.5
24.7
19 (20.2)
0.8
19
73.7
21.1
5.3
Organism/
antimicrobials
Gentamicin
Ampicillin/
Sulbactam
Ampicillin
Amoxicillin/
Clavulanate
Ceftazidime
Cefuroxime
Ceftriaxone
Ciprofloxacin
Levofloxacin
Imipenem
Ertapenem
Meropenem
Piperacillin
Piperacillin/
Tazobactam
TMP/SMX
Nitrofurantoin

Inpatients (n=94)
n
%
n
%
S
I
R
S
I
R
251
55.4
22.7
21.9
19
63.2
10.5
26.3
251
100
19
100
251
2.8
3.2
94.0
19
100
81
7.4
25.9
3.7
60.0
40.0
251
251
251
251
251
251
170
170
251
89.6
67.3
91.6
47.4
51.0
97.2
94.7
97.6
1.2
2.8
23.5
2.8
4.8
17.1
1.2
2.4
0
6.0
7.6
9.2
5.6
47.8
31.9
1.6
2.9
2.4
92.8
19
19
19
19
19
19
14
14
19
84.2
57.9
84.2
52.6
52.6
94.7
92.9
92.9
0
10.5
21.1
5.3
0
10.5
0
0
0
10.5
5.3
21.1
10.5
47.4
36.8
5.3
7.1
7.1
89.5
251
53.0
33.0
14.0
19
57.9
26.3
15.8
251
251
27.1
82.1
0
9.6
72.9
8.4
19
19
21.1
78.9
0
0
78.9
21.1
Klebsiella ozanae
n (%)
Amikacin
Gentamicin
Ampicillin/
Sulbactam
Ampicillin
AMOX/CLAV
Vol. 8 No. 148

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10 (1.0)
2 (2.1)
10
10
50.0
40.0
50.0
10.0
0
50.0
2
2
50.0
100.0
50.0
0
0
0
10
100
100
10
10
0
30.0
0
30.0
100
40.0
2
2
0
0
0
100
100
0
2015
ISSN: 1755-7682
Organism/
antimicrobials
Ceftazidime
Cefuroxime
Ceftriaxone
Ciprofloxacin
Levofloxacin
Imipenem
Piperacillin
Piperacillin/
Tazobactam
TMP/SMX
Nitrofurantoin
Klebsiella
pneumonie n (%)
Amikacin
Gentamicin
Ampicillin/
sulbactam
Ampicillin
Amoxicillin/
Clavulanate
Ceftazidime
Cefuroxime
Ceftriaxone
Ciprofloxacin
Levofloxacin
Imipenem
10
n
10
10
10
10
10
10
10

Inpatients (n=94)
%
n
%
S
I
R
S
I
50.0
30.0
20.0
2
50.0
0
30.0
10.0
60.0
2
50.0
0
50.0
10.0
40.0
2
50.0
0
40.0
10.0
50.0
2
0
0
50.0
10.0
40.0
2
0
0
100
0
0
2
100.0
0
0
0
100
2
0
0
Organism/
antimicrobials
R
50.0
50.0
50.0
100.0
100.0
0
100.0
10
30.0
40.0
30.0
50.0
50.0
10
10
20.0
20.0
10.0
40.0
70.0
40.0
2
2
0
50.0
50.0
0
50.0
50.0
15 (1.5)
2 (2.1)
15
10
80.0
40.0
20.0
10.0
0
50.0
2
2
50.0
50.0
50.0
50.0
0
0
15
100
100.0
15
100
100.0
15
20.0
46.7
33.3
100.0
15
15
15
15
15
15
60.0
13.3
40.0
33.3
53.3
93.3
13.3
26.7
0
13.4
6.7
0
26.7
60.0
60.0
53.3
40.0
6.7
2
2
2
2
2
2
50.0
0
50.0
0
0
100.0
0
0
0
50.0
50.0
0
50.0
100.0
50.0
50.0
50.0
0
Piperacillin
Piperacillin/
Tazobactam
TMP/SMX
Nitrofurantoin

Inpatients (n=94)
n
%
n
%
S
I
R
S
I
R
15
0
6.7
93.3
2
0
50.0
50.0
15
20.0
40.0
40.0
50.0
50.0
15
15
13.3
6.7
6.7
20.0
80.0
73.3
2
2
0
0
50.0
0
50.0
100.0
Morganella
morgani n (%)
Amikacin
Gentamicin
Ampicillin/
sulbactam
Ampicillin
Amoxicillin/
Clavulanate
Ceftazidime
Cefuroxime
Ceftriaxone
Ciprofloxacin
Levofloxacin
Imipenem
Piperacillin
Piperacillin/
Tazobactam
TMP/SMX
Nitrofurantoin
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19 (1.9)
2 (2.1)
19
19
47.4
21.1
42.1
26.3
10.5
52.6
2
2
0
50.0
100.0
0
0
50.0
19
100
100.0
19
100
100.0
19
100
100.0
19
19
19
19
19
19
19
10.5
0
31.6
42.1
42.1
31.6
5.3
10.5
0
52.6
5.3
31.6
47.4
5.3
79.0
100
15.8
52.6
26.3
21.0
89.5
2
2
2
2
2
2
2
0
0
50.0
0
100.0
0
0
0
0
0
100.0
0
50.0
0
100.0
100.0
50.0
0
0
50.0
100.0
19
36.8
42.1
21.1
50.0
50.0
19
19
21.1
0
0
26.3
78.9
73.7
2
2
0
50.0
0
0
100.0
50.0
2015
ISSN: 1755-7682
Organism/
antimicrobials

Inpatients (n=94)
n
%
n
%
S
I
R
S
I
Table 5. A
ntimicrobial activity against Gram-negative organisms collected
from urine samples in children from Jalisco (2012-2013).
R
Proteus mirabilis
11 (1.1)
1 (1.1)
n (%)
Amikacin
11
36.4
63.6
0
1
0
100.0
0
Gentamicin
11
18.2
27.3
54.5
1
0
100.0
0
Ampicillin/
11
0
0
100
1
0
0
100.0
sulbactam
Ampicillin
10
10.0
0
90.0
1
0
0
100.0
Amoxicillin/
11
18.2
0
81.8
1
0
0
100.0
Clavulanate
Ceftazidime
11
18.2
36.4
45.4
1
0
0
100.0
Cefuroxime
11
27.3
27.3
45.4
1
0
0
100.0
Ceftriaxone
11
81.8
9.1
9.1
1
0
100.0
0
Levofloxacin
11
45.4
18.2
36.4
1
100.0
0
0
Imipenem
11
36.4
9.1
54.5
1
100.0
0
0
Piperacillin
11
0
0
100
1
0
0
100.0
Piperacillin/
11
45.4
36.4
18.2
1
0
100.0
0
Taxobactam
TMP/SMX
11
9.1
9.1
81.8
1
0
0
100.0
Nitrofurantoin
11
0
18.2
81.2
1
0
0
100.0
Sensible (S), Intermediate (I), Resistant (R), Trympetroprim sulfametoxazol (TMP/SMX)
Vol. 8 No. 148

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Organism/
antimicrobials
ESBL E. coli n (%)
Amikacin
Gentamicin
Ampicillin/
sulbactam
Ampicillin
Amoxicillin/
Clavulanate
Ceftazidime
Cefuroxime
Ceftriaxone
Ciprofloxacin
Levofloxacin
Imipenem
Ertapenem
Meropenem
Piperacillin
Piperacillin/
Tazobactam
TMP/SMX
Nitrofurantoin
Non-ESBL E. coli
n(%)
Amikacin
Gentamicin
48
48
Pediatric population (n=106)

Outpatients (n=90)
Inpatients (n=16)
%
n
%
S
I
R
S
I
48 (53.3)
8 (50.0)
85.4
10.4
4.2
8
50.0
37.5
25.0
18.8
56.2
8
12.5
12.5
R
12.5
75.0
48
100.0
100.0
48
2.1
97.9
100.0
48
31.3
68.7
37.5
25.0
37.5
48
48
48
48
48
48
2
2
48
47.9
27.1
43.8
39.6
41.7
100.0
100.0
100.0
0
8.3
8.3
2.1
0
4.2
0
0
0
6.3
43.8
64.6
54.2
60.4
54.2
0
0
0
93.7
8
8
8
8
8
8
0
0
8
25.0
12.5
50.0
50.0
50.0
87.5
0
12.5
25.0
12.5
0
0
0
0
62.5
62.5
37.5
50.0
50.0
12.5
100.0
48
43.8
22.9
33.3
25.0
25.0
50.0
48
48
25.0
85.4
2.1
2.1
72.9
12.5
8
8
37.5
87.5
0
0
62.5
12.5
33 (36.7)
33
33
97.0
39.4
3.0
54.5
4 (25.0)
0
6.1
4
4
75.0
0
25.0
100.0
0
0
11
2015
ISSN: 1755-7682
Organism/
antimicrobials
Ampicillin/
sulbactam
Ampicillin
Amoxicillin/
Clavulanate
Ceftazidime
Cefuroxime
Ceftriaxone
Ciprofloxacin
Levofloxacin
Imipenem
Ertapenem
Meropenem
Piperacillin
Piperacillin/
Tazobactam
TMP/SMX
Nitrofurantoin
Klebsiella ozanae
n(%)
Amikacin
Gentamicin
Ampicillin/
sulbactam
Ampicillin
Amoxicillin/
Clavulanate
12

Outpatients (n=90)
Inpatients (n=16)
%
n
%
S
I
R
S
I
Organism/
antimicrobials
R
33
100.0
100.0
33
3.0
97.0
100.0
32
43.8
56.2
50.0
50.0
33
33
33
33
33
33
1
1
33
100.0
94.0
100.0
84.8
84.9
100.0
100.0
100.0
0
0
3.0
0
0
3.0
0
0
0
0
0
3.0
0
15.2
12.1
0
0
0
100.0
4
4
4
4
4
4
0
0
4
100.0
100.0
100.0
75.0
75.0
100.0
0
0
0
0
0
25.0
0
0
0
0
0
25.0
0
0
100.0
33
69.7
24.2
6.1
75.0
25.0
33
33
9.1
93.9
0
0
90.9
6.1
4
4
0
100.0
0
0
100.0
0
1 (1.1)
2 (12.4)
1
1
100.0
0
0
100.0
0
0
2
2
100.0
50.0
0
50.0
0
0
100.0
100.0
100.0
100.0
100.0
50.0
50.0
Ceftazidime
Cefuroxime
Ceftriaxone
Ciprofloxacin
Levofloxacin
Imipenem
Piperacillin
Piperacillin/
Tazobactam
TMP/SMX
Nitrofurantoin
Klebsiella
pneumonie n(%)
Amikacin
Getamicin
Ampicillin/
sulbactam
Ampicillin
Amoxicillin/
Clavulanate
Ceftazidime
Cefuroxime
Ceftriaxone
Ciprofloxacin
Levofloxacin
Imipenem
Piperacillin
1
1
1
1
1
1
1
Vol. 8 No. 148

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Outpatients (n=90)
Inpatients (n=16)
%
n
%
S
I
R
S
I
R
100.0
0
0
2
100.0
0
0
100.0
0
0
2
50.0
0
50.0
100.0
0
0
2
100.0
0
0
100.0
0
0
2
100.0
0
0
100.0
0
0
2
100.0
0
0
100.0
0
0
2
100.0
0
0
0
0
100.0
2
0
0
100.0
100.0
100.0
1
1
0
100.0
0
0
100.0
0
2
2
50.0
50.0
0
0
50.0
50.0
1 (1.1)
0 (0)
1
1
100.0
0
0
0
0
100.0
0
0
100.0
100.0
100.0
1
1
1
1
1
1
1
0
0
0
0
100.0
100.0
0
0
0
0
0
0
0
0
100.0
100.0
100.0
100.0
0
0
100.0
0
0
0
0
0
0
0
ISSN: 1755-7682
Organism/
antimicrobials
Piperacillin/
Tazobactam
TMP/SMX
Nitrofurantoin
Morganella
morgani n(%)
Amikacin
Gentamicin
Ampicillin/
sulbactam
Ampicillin
Amoxicillin/
Clavulanate
Ceftazidime
Cefuroxime
Ceftriaxone
Ciprofloxacin
Levofloxacin
Imipenem
Piperacillin
Piperacillin/
Tazobactam
TMP/SMX
Nitrofurantoin

Outpatients (n=90)
Inpatients (n=16)
%
n
%
S
I
R
S
I
Organism/
antimicrobials
R
100.0
1
1
0
0
0
100.0
100.0
0
0
0
2 (2.2)
1 (6.3)
2
2
50.0
50.0
50.0
50.0
0
0
1
1
0
0
100.0
100.0
0
0
100.0
100.0
100.0
100.0
100.0
100.0
2
2
2
2
2
2
2
0
0
50.0
100.0
100.0
0
0
0
0
50.0
0
0
0
0
100.0
100.0
0
0
0
100.0
100.0
1
1
1
1
1
1
1
0
0
0
100.0
100.0
0
0
0
0
100.0
0
0
0
0
100.0
100.0
0
0
0
100.0
100.0
50.0
50.0
100.0
50.0
0
50.0
100.0
100.0
0
100.0
2015
Vol. 8 No. 148
doi: 10.3823/1747

Outpatients (n=90)
Inpatients (n=16)
%
n
%
S
I
R
S
I
Proteus mirabilis
5 (5.6)
1 (6.3)
n (%)
Amikacin
5
80.0
20.0
0
1
100.0
0
0
Gentamicin
5
20.0
60.0
20.0
1
0
100.0
0
Ampicillin/
5
0
0
100.0
1
0
0
100.0
sulbactam
Ampicillin
5
0
0
100.0
1
0
0
100.0
Amoxicillin/
5
0
0
100.0
1
0
100.0
0
Clavulanate
Ceftazidime
5
0
40.0
60.0
1
0
0
100.0
Cefuroxime
5
0
0
100.0
1
0
100.0
0
Ceftriaxone
5
40.0
40.0
20.0
1
100.0
0
0
Ciprofloxacin
5
60.0
0
40.0
1
100.0
0
0
Levofloxacin
5
80.0
20.0
0
1
100.0
0
0
Imipenem
5
80.0
0
20.0
1
0
0
100.0
Piperacillin
5
40.0
0
60.0
1
0
0
100.0
Piperacillin/
5
60.0
0
40.0
1
0
0
100.0
Tazobactam
TMP/SMX
5
0
0
100.0
1
100.0
0
0
Sensible (S), Intermediate (I), Resistant (R), Trympetroprim sulfametoxazole (TMP/SMX).
13
ISSN: 1755-7682 J
cing E. coli have been increasingly reported [2,

27]. Over the last two decades, the proportion of
community-acquired ESBL-producing E. coli strains
with resistance to first-line antimicrobial agents,
such as ampicillin, cephalosporins, TMP-SMX, and
fluoroquinolones have increased globally, further
complicating the management of UTI infections
[2]. While -lactamases may be chromosomally
encoded and universally present in a species or
plasmid mediated, the main type of commonly
found ESBL in Klebsiella and Escherichia coli are
SHV-1 and SHV-2 enzymes (for sulphydral variable type 1). The second largest group of ESBLs
are CTX-M enzymes. Indeed E. coli that produce
CTX-M enzymes have been identified as a cause of UTIs, mainly in the community setting [29].
Various reports suggest that CTX-M-type ESBLs
may now be the most frequently encountered
ESBL worldwide [30].
Currently, in order to establish diagnosis, a presence of 1,000 to 10,000 colony-forming units
(CFU)/mL is required [4]. Accordingly, physicians
are encouraged to avoid prescribing antibiotics
to patients with low-colony-count urine specimens, in order to decrease unnecessary exposure
to antibiotics that may lead to the development
of multidrug-resistant bacteria and other negative
antibiotic-related conditions and side effects [4].
Furthermore, fluoroquinolones are no longer the
first line of treatment in cases of uncomplicated
cystitis or pyelonephritis, according to both the
Infectious Diseases Society of America (IDSA) and
the medical guidelines published by the European
Society for Microbiology and Infectious Diseases
(ESCMID) [31].
The knowledge of specific risk factors for resistance development should help guide the selection of the appropriate antibiotic treatment
and assist in the designing of appropriate control
programs to reduce morbidity and costs related
to UTIs worldwide, emphasizing the need to perform urine cultures before initiating antimicrobial
14
2015
Vol. 8 No. 148
doi: 10.3823/1747
treatment. This report will ideally encourage a

more scientific and measured use of antibiotics
which is of utmost importance, not only for patients who live in Mexico and Latin America, but
also for travelers whom have acquired infections
during their visits to these countries.
Our study has several potential limitations; the
lack of data on clinical information, including previous antimicrobial treatments and recurrence of
infection rates, due to study design, may result in
information bias, although it is unlikely that this
would result in differential bias. Furthermore, the
antibiotic fosfomycin was not analyzed herein based on urine culture susceptibility tests that generally indicate low resistance rates for this drug. A
follow-up study, incorporating additional information via informed consent permission, would be
useful to establish associations between risk factors and resistance rates to specific antimicrobials.
Such findings may, in turn, elucidate an alternative
treatment option for uncomplicated cystitis caused by ESBL-producing E. coli infection, to minimize the current indicated use of carbapenems,
which may better be reserved for more severe
infections, in order to preserve its low resistance
profile.
Conclusion
Data analyzed in this review is relevant to Mexico,
Latin America and patients worldwide who have
contracted UTIs while traveling to Mexico and other
parts of Latin America, before returning to their
home country. Additionally this study supports the
need for improved education of health care workers
regarding the use of antimicrobials as part of an
international antibiotic stewardship program. Taken
together, these suggested changes may not only
benefit patients with UTIs, but may also go a long
way to reduce the presence of antimicrobial agent
resistant bacteria generally.
ISSN: 1755-7682
Acknowledgments
Special thanks to Ricardo Del Castillo, Dean of the
School of Medicine for his constant support to institutional research activities.
Thanks to Unidad de Patologia Clinica for their
contribution in the elaboration of the present study.
Conflict of interest statement

All authors declare that they do not have a commercial or other association that might pose a conflict
of interest.
There was no financial support for the present
study.
Authors' contributions
All authors made substantial contributions to conception and design of the manuscript.
MZC and IZT participated in the conception and
design of the study.
NMR, FSG, JRC and DM participated in the acquisition and analysis of the data.
MZC, LN, IZT, OTB and FST participated in the
analysis and interpretation of the data.
MZC performed the statistical analysis.
All authors were involved in drafting of the manuscript or revising it critically for important intellectual content and gave final approval of the version
to be published.
Footnote
Part of the information from this study was presented in the XXXIX Congreso Anual de la Asociacin
Mexicana de Infectologa y Microbiologia Clnica,
AC, in Acapulco, Guerrero, Mexico on May 2831, 2014. Published in Enfermedades Infecciosas y
Microbiologia 2014, 34:S51. Abstract number A72
ISSN-1870-1388.
2015
Vol. 8 No. 148
doi: 10.3823/1747
References
1. Sood, S. and R. Gupta, Antibiotic resistance pattern of
community acquired uropathogens at a tertiary care hospital in
jaipur, rajasthan. Indian J Community Med, 2012. 37(1): p. 3944.
2. Aboderin OA, A.A., Odetoyin BW, Lamikanra A,, Antimicrobial
resistance in Escherichia coli strains from urinary tract infections.
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