JCM Accepts, published online ahead of print on 18 June 2008 J. Clin. Microbiol. doi:10.1128/JCM.01008-08 Copyright © 2008, American Society for Microbiology and/or the Listed Authors/Institutions. All Rights Reserved.
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High rate of Intestinal Colonization with Extended Spectrum
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ß-Lactamases Producing Organisms in Household Contacts of Infected
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Community Patients
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Aránzazu Valverde,1,2 Fabio Grill,3 Teresa M. Coque,1,2 Vicente Pintado3,
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Fernando Baquero,1,2 Rafael Cantón,1,2* and Javier Cobo3
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Servicio de Microbiología,1 CIBER en Epidemiología y Salud Pública (CIBERESP),2
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and Servicio de Enfermedades Infecciosas3. Hospital Universitario Ramón y Cajal.
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28034-Madrid. Spain
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Running title. ESBL fecal colonization in family groups
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Key words: ESBL, Escherichia coli, household contacts, fecal carriage
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*Corresponding author: R. Cantón. Servicio de Microbiología. Hospital
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Universitario Ramón y Cajal. 28034-Madrid. Spain. Phone: +34913368330; FAX:
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+34913368809; e-mail:
[email protected]
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Fecal carriage with extended-spectrum ß-lactamase (ESBL)-organisms was
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detected in 70% of index cases (n=40) with community-acquired infections due to
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ESBL-producers and reached 16.7% in household contacts (n=54). Sixty-six
27
percent of ESBL-organisms from index cases were indistinguishable (PFGE) when
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compared with household isolates. Community-patients and their households
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represent a reservoir for ESBL-producers, increasing dispersal of resistance in
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healthy people.
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Extended spectrum ß-lactamase (ESBL) producing organisms have dramatically
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increased worldwide (2,22). This has been associated with efficient dispersion of
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specific clones and plasmids harbouring blaESBL genes (5,6,20). In addition, co-
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resistance to non-ß-lactam antibiotics may have fuelled persistence of ESBL-producing
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isolates, a fact that has been demonstrated in intensive care units (17,19,23). A
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threatening epidemiological problem is the dispersal of ESBL-organisms to healthy
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people in the community, which might depend on the frequency of ESBL-fecal carriers
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as well as their presence in the food chain (15,18,30).
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In a previous study, we demonstrated that nearly 12% of hospitalized patients might
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carry ESBL-producing isolates in the intestinal compartment (32). This colonization has
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been associated with a high risk for developing an infection due to ESBL-producers
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(23,25). This has been scarcely studied in community patients and to a lesser extent in
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healthy subjects (24,32). Moreover, there is little information about the pathways of the
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intestinal colonization. This has been investigated in hospitalized patients and recently
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in outpatients involved in food-borne outbreaks (9,15). In the present study, we
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analysed the fecal carriage with ESBL-producing isolates in a group of patients with
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community-acquired infections (CAIs) due to these organisms and the corresponding
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status of the people living with them (household contacts).
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From April 2004 to June 2005 a total of 299 patients presented an infection or
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colonization process due to an ESBL-producing organism in our institution. Fifty-six
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percent were outpatients and 95% of them had a urinary tract infection. Forty clinical
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samples from 40 patients (index cases, ICs) with CAIs (37 urinary tract infections, 2
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bacteremia, and one soft tissue infection) due to an ESBL-producing E. coli (n=39) or
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Klebsiella pneumoniae (n=1) isolates and fecal samples (one per IC) were studied. Only
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ICs that positively agree to participate in the study and submitted fecal samples were
3
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enrolled. Thirty-four of the 40 ICs (mean age 63.6 years, range 2-96) were females. In
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addition, 54 fecal samples from 54 household contacts of 29 IC recovered within two-
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weeks of IC enrolment were also studied. The number of household contacts for each IC
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ranged from only one to 7 (mean 2 household per patient). The ethical committee
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approved the study and signed informed consents were obtained.
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Fecal samples were screened for ESBL-producers as previously described (32).
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Bacterial identification was performed by standard methods and CLSI microdilution (4)
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for susceptibility pattern. ESBL characterization was performed by PCR and sequencing
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(6,32,33). Population structure was established by PFGE (32). In addition, phylogenetic
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groups among E. coli isolates were identified by a multiplex PCR (3).
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Twenty-eight out of 40 ICs (70%, CI95%:53.4-83.4) and 9 out of 54 household
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contacts (16.7%; CI95%:6.7-26.1) presented fecal carriage with ESBL-producing E.
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coli isolates (Figure 1). Moreover, 9 ICs out of 29 had at least one colonized household
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contact (31.0%; CI 95%:14.2-47.9). This figure increased (42.1%; CI 95%:19.9-64.3) in
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the subset of household contacts of ICs with fecal carriage (8/19). In contrast, only one
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household contact (1/10, 10%; CI95%:0-28.6) within the subset of those from ICs with
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negative fecal carriage, presented an intestinal colonization of ESBL-producing E. coli
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(Figure 1).
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Characteristics of ESBL-producing isolates from ICs and their corresponding
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household contacts are shown in tables 1 and 2. Seventy-two percent (21/29) of ICs
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presented E. coli clinical isolates with the same PFGE type as those from their fecal
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samples. Moreover, PFGE analysis revealed an indistinguishable pattern among ESBL-
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producing E. coli from ICs (clinical sample or fecal sample) and their corresponding
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household contacts in 66% (6/9) of isolates.
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Overall, ESBL characterization revealed a predominance of CTX-M-14 (57%) and
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SHV-12 (18.6%), the emergence of ESBLs belonging to CTX-M-1 group (7.1%), and a
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small representation of TEM (5.7%) enzymes. This distribution is in agreement with the
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epidemiological situation of ESBL-producing isolates from the community at the time
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of enrollment in our study (2,27,31). It is of note that 2 ICs and 2 household contacts
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were colonized with two different ESBL-producing isolates.
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The present study demonstrates a high rate (70%) of intestinal colonization in
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patients with CAI due to ESBL-producing organisms. The presence of these pathogens
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in the bowel is considered as a risk factor for suffering infections with these bacteria
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(28). Moreover, it can explain the high rates of isolation of ESBL-producing organisms
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in certain anatomic locations (i.e. abdominal and urinary tract infections), than in others
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where there is not a clear implication of endogenous microbiota (28). It is of note that
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our 70% figure is similar to that found in hospitalized patients under high antimicrobial
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selective pressure (17,23). Around 50% of our patients received antimicrobial treatment
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(18 patients) or medical extrahospitalary assistance (22 patients) at least two months
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before ESBL infections which have been defined as risk factors for colonization with
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these pathogens (28).
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An important finding was the high rate (16.7%) of intestinal colonization in
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households of patients suffering CAI with ESBL-producing organisms. This figure is
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higher than that previously found by our group in the same geographic area (3.7%,
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p=0.004, Chi square test) and in other countries (range, 1.7% to 13.1%) in healthy
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individuals (13,21,26,32). These values were even higher (42.1%) in the subset of
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household contacts of ICs with fecal carriage. Despite of potential limitation of our study
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due to the small sample size, these results revealed the importance of the intestinal
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colonization as a reservoir for transmission of resistant bacteria and its potential role as
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traffickers in antibiotic resistance genes (14,29). This has been studied in the
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nosocomial setting where it is generally assumed that for every patient with a clinically
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significant infection with an ESBL-producing organism at least one other patient exists
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in the same unit with intestinal colonization with an ESBL-producer (9,17,22). Data
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from the community remain scarce. It has been shown that methicillin-resistant
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Staphylococcus aureus or vancomycin-resistant enterococci may be acquired from
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different family members (1,10,11) and there is no information contradicting this
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suspicion with ESBL pathogens.
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Patient-to-patient transmission has been demonstrated with ESBL-producing K.
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pneumoniae isolates in the nosocomial setting (7,17,23). In the community, this
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landscape might have also been produced with E. coli (6,8,9,16). In our study, up to
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66% of isolates from ICs and their corresponding households had an indistinguishable
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PFGE pattern. Epidemic plasmids might be responsible for this situation. This
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possibility was studied in different CTX-M-14 producing clones (Valverde et al,
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unpublished data). We cannot rule out a common source as we do not investigate
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ESBL-producing organisms in food or domestic pets. Both have been involved in the
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spread of these pathogens and their corresponding blaESBL genes (12,15,30).
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In summary, high rates of intestinal colonization with ESBL-producing organisms in
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community patients infected with these isolates was observed. Household contacts of
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these patients had high rates of intestinal colonization with ESBL-producing organisms,
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higher than that in outpatients and the general population (32). These results highlight
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that community patients and their households represent a clear reservoir for these
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organisms and the corresponding blaESBL genes. This fact increases the risk of
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dissemination of such organisms to normal healthy people and facilitates the acquisition
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of resistance mechanisms by susceptible bacteria.
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A. Valverde is supported by CIBER-ESP (Network Center for Biomedical Research in
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Epidemiology and Public Health) from Instituto Carlos III, Ministerio de Sanidad y
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Consumo of Spain. F. Grill was supported by “Red Española de Investigación en
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Patología Infecciosa” (REIPI-ISCIII-C03/14) from Instituto Carlos III, Ministerio de
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Sanidad y Consumo of Spain. This study was partially supported by research grants
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from the Ministerio de Sanidad y Consumo, Instituto de Salud Carlos III (PI040162),
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DeReMicrobiana Project of the Madrid Autonomous Community, and the European
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Commission (LSHM-CT-2003-503335).
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We thank Azucena Rollán for her excellent technical work.
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TABLE 1. Characteristics of ESBL-producing isolates from clinical and fecal samples
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of index cases with no household contacts E. coli
Index case IC1
IC2
IC4
IC11
Sample
Organism
Urine
E.coli
CV3C
A
Fecal
E.coli
CV3HC
A
Urine
E.coli
CV12C
D
Fecal
E.coli
CV12C
D
Urine
E.coli
CV16C
Fecal
E.coli
CV16C
Urine
E.coli
CV37C
E C
IC16
IC18
IC19
E.coli
CV39C
E.coli
CTX-M-14 CTX-M-14
CTX-M-14
CV40C
A
CTX-M-14
E.coli
CV40C
A
CTX-M-14
E.coli
CV52C
A
CTX-M-14
Fecal
E.coli
CV52C
A
CTX-M-14
Urine
E.coli
CV59C
B1
CTX-M-14
Fecal
E.coli
CV59C
B1
CTX-M-14
Urine
E.coli
CV77C
B1
CTX-M-14
Fecal
E.coli
CV77C
B1
CTX-M-14
Urine
E.coli
CV80C
B1
CTX-M-14
Fecal
E.coli
CV80HC
B1
CTX-M-14
C A
CV39C
D
CTX-M-14
D
Urine
E.coli
A
CTX-M-14
CTX-M-14
Fecal
IC15
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D E CTX-M-14
D
Urine
CV37HC
A
CTX-M-14
CTX-M-14
Urine
E.coli
CTX-M-14
D
Fecal
IC13
ESBL phylogroup
Fecal
IC12
PFGE
255 256 257 258 259 260 261 12
262
TABLE 1 (cont.) E. coli Index case
Sample
Organism
PFGE
ESBL phylogroup
IC7
IC10
IC17
IC20
Urine
E.coli
CV20C
D
CTX-M-14
Fecal
E.coli
CV20S
D
SHV-2
Urine
E.coli
CV29C
B1
Fecal
E.coli
CV29C
B1
Urine
E.coli
CV70C
Fecal
E.coli
CV70C
Urine
E.coli
CV86C
E.coli
CV86C
E.coli
CV14O
E.coli
E C
Fecal
IC3
CV14H-Da
B1
SHV-12
E.coli
CV17S
B1
SHV-12
E.coli
CV17S
B1
SHV-12
Urine
E.coli
CV24S
A
SHV-12
Fecal
E.coli
CV24S
A
SHV-12
Urine
K. pneumoniae
CV18O
-
TEM-4
Fecal
E.coli
CV18H-Da
B1
SHV-12
Urine
E.coli
CV41T
A
TEM-39
Fecal
E.coli
CV41T
A
TEM-39
Urine
E.coli
CV28C
D
CTX-M-32
Fecal
E.coli
CV28C
D
CTX-M-32
C A IC9
263
a.
CTX-M-9
SHV-12
Fecal
IC14
CTX-M-9
B1
Urine
IC6
A
CTX-M-9
CTX-M-9
Fecal
IC8
D
CTX-M-9
D
Urine
IC5
D E
T P D
CTX-M-9
PFGE pattern degradated.
264
13
265
TABLE 2. Characteristics of ESBL-producing E. coli isolates from all samples of index
266
cases and fecal samples from positive ESBL-household contacts
Family
Household contacta
Index case
group (no. of household
Sample
PFGE
Phylogroup
ESBL
Urine
CV5C
D
CTX-M-14
Fecal
CV5C
D
CTX-M-14
Urine
CV34C
A
CTX-M-14
Fecal
b
-
b
-
b
Urine
CV61C
B1
CTX-M-14
Fecal
CV61C
B1
CTX-M-14
Urine
CV64C
A
CTX-M-14
Fecal
CV64C
B1
CTX-M-14
Urine
CV81C
A
CTX-M-14
Fecal
CV81C
A
CTX-M-14
Urine
CV92C
B1
CTX-M-14
Fecal
CV92HC
A
CTX-M-14
PFGE
Phylogroup
contacts) FG1 (1 )
FG2 (1)
FG4 (1)
FG5 (1)
FG7 (1)
E C
C A FG8 (1)
FG9 (1)
FG3 (1)
FG6 (1)
D E
CV5C
D
CTX-M-14
A
CTX-M-14
B1
CTX-M-14
CV64C
B1
CTX-M-14
CV82C
D
CTX-M-14
CV93.1
A
TEM-52
CV93.2
A
TEM-52
CV94S
D
SHV-12
CV44C
A
CTX-M-14
CV68C
D
CTX-M-1
CV69C
D
CTX-M-14
T P -
Urine
CV94S
D
SHV-12
Fecal
CV94S
D
SHV-12
Urine
CV44S
D
SHV-12
Fecal
CV44S
D
SHV-12
CV44C
A
CTX-M-14
Urine
CV68C
D
CTX-M-1
Fecal
CV68C
D
CTX-M-1
267
a.
Isolates of household contacts were obtained from fecal samples;
268
b.
No positive ESBL fecal sample was obtained
269 270 271 272 14
ESBL
CV36C
CV61C
273
FIG 1. Index cases with fecal carriage of ESBL-producing organism and their
274
corresponding household contacts
Index cases: 40
Index case carriage (-): 12
With household contacts: 10
Household contacts carriage (+): 1
D E
Index case carriage (+): 28
Without household contacts: 2
Household contacts carriage (-): 15
With household contacts: 19
T P
Household contacts carriage (+): 8
E C Household contact: 54
C A
Without household contacts: 9
Household contacts carriage (-): 30
Index case: Patient with ESBL-Producing Organism Infection
Index Case Carriage (+) : Patient with ESBL-Producing Organism Infection and fecal positive ESBL culture Household contacts Carriage (+) : Household contacts with positive ESBL-Producing Organism in fecal sample
275
15
