Fecal Carriage of Enterobacteriaceae Producing Extended-Spectrum Beta-Lactamases in Hospitalized Patients and Healthy Community Volunteers in Burkina Faso

Abstract

Extended-spectrum β-lactamase-producing Enterobacteriaceae (ESBL-PE) have been described worldwide, but few reports focused on Burkina Faso. To assess the prevalence of digestive carriage of such bacteria in the community and in the hospital, 214 fecal samples, 101 from healthy volunteers and 113 from hospitalized patients without digestive pathology, were collected in Bobo Dioulasso, Burkina Faso economic capital, during July and August 2014. Stool samples were screened using ESBL agar plates. Strains were identified by mass spectrometry using the Biotyper MALDI-TOF. ESBL production was confirmed with the double-disc synergy test. Susceptibility was tested using the disk diffusion method on Müller-Hinton agar. The main ESBL genes were detected using multiplex PCR and bidirectional gene sequencing. Escherichia coli phylogenetic groups were identified using a PCR-based method. During the study period, prevalence of subjects with fecal ESBL-PE was 32% (69/214), 22% among healthy volunteers and 42% among inpatients. All but two ESBL, CTX-M-15 and ESBL-PE, were mostly E. coli (78%). Among the 60 ESBL-producing E. coli strains, 26% belonged to phylogenetic group D, 23.3% to group A, 20% to group B1, 6.6% to group B2, and 3.3% to the ST131 clone. Univariate analysis showed that history of hospitalization and previous antibiotic use were risk factors associated with ESBL-PE fecal carriage. In Burkina Faso, the prevalence of both healthy subjects from the community and hospitalized patients with fecal ESBL-PE is alarmingly high. This feature should be taken into consideration by both general practitioners and hospital doctors with regard to empirical treatments of infections, notably urinary tract infections.

Introduction

Extended-spectrum β-lactamases (ESBL) hydrolyze a wide range of β-lactam antibiotics, including second- and third-generation cephalosporins.^1,2 Furthermore, ESBL-producing enterobacterial (ESBL-PE) isolates that produce new ESBL families (especially CTX-M enzymes) are associated with resistance to fluoroquinolones and aminoglycosides and have been detected worldwide. This might limit the available treatment options and increase the likelihood of empiric treatment failure.^3,4

Digestive tract is the main reservoir of Enterobacteriaceae causing infections whatever their onset (community or hospital).⁵ Therefore, knowing the prevalence of subjects with digestive tract carriage of ESBL-PE in the community and among hospitalized patients is a manner to predict the involvement of such bacteria in infections and their level of transmission. From this point of view, the situation is particularly dramatic in Africa where subjects with ESBL-PE digestive tract carriage range from 10% to 50% and is higher than 60% in the case of ESBL-producing Escherichia coli.^6,7 In Burkina Faso, a low-income country of West Africa, nothing is known about the digestive tract carriage of ESBL-producing Enterobacteriaceae both among inpatients and healthy subjects. The objective of the present study was to assess the prevalence of patients hospitalized at the Souro Sanou University Hospital and healthy volunteers living in the city of Bobo Dioulasso with digestive tract carriage of ESBL-PE, and to characterize the ESBL produced as well as the genetic background of the E. coli producing these enzymes.

Materials and Methods

Patients, specimen collection, and ethical clearance

This study was conducted in Bobo Dioulasso, Burkina Faso economical capital with a population of about 1 million inhabitants. During July and August 2014, 214 fecal samples were collected from 101 healthy volunteers in the community and 113 patients who were hospitalized at the Souro Sanou University Hospital for more than 48 hr (people with digestive pathologies were excluded from the study). Souro Sanou University Hospital is the major healthcare and referral center for Burkina Faso southern and western regions. It has 521 beds distributed in different specialized (medicine, surgery, gynecology, obstetrics, and pediatrics) acute care units. Each participant was interviewed by health professionals using a home-made standardized questionnaire to record the following data: age, gender, antibiotic treatment during the past 3 months, and any hospital stays in the previous year. The study was approved by the Souro Sanou University Hospital board (Authorization No. MS/SG/CHUSS/DG/DL 2014-171, July 2, 2014). Informed written consent was obtained from all subjects and at least one parent for each child before enrollment.

Detection of ESBL-PE isolates and antibiotic susceptibility testing

Briefly, 0.5 g of each fresh stool sample was suspended in 5 ml of sterile saline and 100 μl aliquots were plated on ESBL agar plates (bioMérieux, Marcy-l'Etoile, France) and were examined after 24 and 48 hr of incubation at 37°C. Each distinct morphotype of colonies that grew on ESBL agar plates was studied. Species identification was performed by Matrix-Assisted Laser Desorption–Ionization Time-of-Flight (MALDI-TOF) Mass Spectrometry (Bruker Daltonics, Bremen, Germany). All Enterobacteriaceae isolates were screened for ESBL production using the double-disc synergy test.⁸ In all positive isolates, antimicrobial susceptibility was tested by using the disk diffusion method on Müller-Hinton agar for the following antibiotics: amoxicillin, amoxicillin–clavulanic acid, aztreonam, cefepime, cefotaxime, cefpirome, cefpodoxime, cefoxitin, ceftazidime, cephalothin, moxalactam, piperacillin, piperacillin–tazobactam, ticarcillin, ticarcillin–clavulanic acid, imipenem, nalidixic acid, ciprofloxacin, levofloxacin, ofloxacin, amikacin, gentamicin, netilmicin, tobramycin, fosfomycin, chloramphenicol, tetracycline, and trimethoprim–sulfamethoxazole. Results were interpreted following the European Committee on Antimicrobial Susceptibility Testing (EUCAST) clinical breakpoints (Version 5.0) (www.eucast.org/clinical_breakpoints/).

Molecular identification of ESBL genes

DNA was extracted from single colonies in a final volume of 100 μl of distilled water by incubation at 95°C for 10 min, followed by a centrifugation step. Multiplex PCR was used to identify strains harboring bla_CTX-M genes that encode different CTX-M variants (i.e., CTX-M group 1, 2, 8, 9, and 25) as well as the bla_TEM, bla_SHV, and bla_OXA-like genes, as previously described.⁹ DNA samples from reference strains carrying bla_CTX-M, bla_TEM, bla_SHV, or bla_OXA-like were used as positive controls. PCR products were separated by electrophoresis on 1.5% agarose gels containing ethidium bromide at 100 V for 80 min. A 100 bp DNA ladder (Promega, Fitchburg, WI) was used for size estimation. All specific PCR products were purified using the ExoSAP-IT PCR Clean-up Kit (GE Healthcare, Piscataway, NJ) and bidirectional sequencing was performed on a 3100 ABI Prism Genetic Analyzer (Applied Biosystems, Foster City, CA). Sequence alignment and analysis were performed using the BLAST program available at the National Center for Biotechnology Information (www.ncbi.nlm.nih.gov).

Detection of E. coli phylogenetic groups and sequence type 131 clone

To determine the phylogenetic group of the ESBL-producing E. coli isolates, we used the PCR-based method described by Clermont et al.¹⁰ For strains assigned to the B2 phylogenetic group, the presence of E. coli sequence type (ST) 131 was determined using an O25b-specific PCR method with pabB and trpA (control) allele-specific primers, as previously described.¹¹

Statistical analysis

Data were analyzed with Epi Info version 3.5.3 (Centers for Disease Control and Prevention, Atlanta, GA). Conditional logistic regression analysis was used for the univariate analysis of risk factors and odds ratio with 95% confidence intervals. A p < 0.05 was considered to be statistically significant.

Results

Prevalence and risk factors of ESBL-PE fecal carriage

During the study period, 214 subjects (101 healthy volunteers and 113 hospitalized patients) with a mean age of 21.9 ± 7.1 years were enrolled (Table 1). Among the healthy volunteers, 6 (6%) were hospitalized in the previous year and 22 (22%) received antibiotics, within the 3 months before inclusion in the study, such as β-Lactams (n = 9/22, 41%), fluoroquinolones (n = 7/22, 32%), or other unspecified antibiotics (n = 6/22, 27%). Among the hospitalized patients, 21 (18.5%) were also hospitalized in the previous year and 58 (51%) received antibiotics, within the 3 months before sampling, such as β-Lactams (n = 36/58, 62%), fluoroquinolones (n = 13/58, 22%), or other antibiotics (n = 9/58, 16%) (Table 1). The previous use of antibiotics and prior hospitalization were different for both populations (p < 0.005) (Table 2). Among the 214 stool samples, 69 (32% [26–39%]) grew on selective ESBL agar; 47 of these samples were from inpatients (42% [33–51%] of 113) and 22 from healthy volunteers (22% [15–31%] of 101) (p = 0.002). ESBL production by these 69 samples was confirmed with the double-disk synergy test and by PCR. When taking into account the unit where the enrolled patients were hospitalized, we found that 65% (19/29) of patients enrolled from medicine wards were ESBL-PE carriers, 47% (14/30) from surgery wards, 28% (8/29) from gynecology/obstetrics ward, and 24% (6/25) from the pediatric department. Univariate analysis did not identify any specific factor associated with ESBL-PE fecal carriage in the hospitalized population (Table 3). Conversely, in the healthy controls, previous use of antibiotics and anterior hospitalization were risk factors for ESBL-PE carriage (p < 0.05) (Table 3).

Table 1.

Demographic Characteristics, Prevalence of ESBL-PE Fecal Carriage in the Study Population

Variables	Healthy volunteers (n = 101)	Inpatients (n = 113)	Total (n = 214)
Age, years, mean (SD)	18.5 (12.5)	25.9 (18.8)	21.9 (7.1)
Males, n (%)	47 (46)	46 (40.7)	93 (43)
ESBL-PE carriers, n (%)	22 (22)	47 (42)	69 (32)
Hospitalization duration, days, mean (SD)	—	10.3 (11.2)	—
Previous hospitalization (in the last year), n (%)
Yes	6 (6)	21 (18.5)	27 (12.6)
No	95 (94)	92 (81.5)	187 (87.4)
Antibiotic treatment (in last 3 months), n (%)
Yes	22 (22)	58 (51)	80 (37.4)
No	45 (44)	37 (33)	82 (38.3)
Not known	34 (34)	18 (16)	52 (24.3)
Used antibiotics, n (%)
β-Lactams	9 (41)	36 (62)	45 (21)
Fluoroquinolones	7 (32)	13 (22)	20 (9.3)
Other antibiotics^a	6 (27)	9 (16)	15 (7)

Tetracycline, doxycycline, trimethoprim–sulfamethoxazole, erythromycin, clindamycin, and gentamicin.

SD, standard deviation.

Table 2.

Univariate Analysis of Antibiotic Use and Previous Hospitalization Among Outpatients and Inpatients

Risk factors	Outpatients (n = 101)	Inpatients (113)	Odds ratio (95% CI)	P
Previous use of antibiotics
Yes/no	22/45	58/37	0.31 (0.16–0.60)	<0.001
Previous hospitalization
Yes/no	6/95	21/92	0.27 (0.10–0.71)	0.005

Table 3.

Analysis of Risk Factors for ESBL-PE Fecal Carriage in the Study Population

	Outpatients (n = 101)				Inpatients (n = 113)
Covariate	ESBL-positive (n = 22)	ESBL-negative (n = 79)	Odds ratio (95% CI)	P	ESBL-positive (n = 47)	ESBL-negative (n = 66)	Odds ratio (95% CI)	P
Age, years, mean (SD)	21.6 (14.5)	17.6 (11.8)		0.24	25.8 (15.4)	26 (21.7)		0.95
Male gender	7	40	0.46 (0.16–1.24)	0.12	16	29	0.62 (0.29–1.34)	0.28
Hospitalization duration, days, mean (SD)					12.1 (14.1)	8.9 (8.35)		0.09
Antibiotic use (last 3 months)
Yes/no	15/4	7/41	20.47 (5.5–95.23)	<0.001	23/15	35/22	0.96 (0.41–2.23)	0.93
Anterior hospitalization (in last year)
Yes/no	5/17	1/78	23 (2.51–209.17)	<0.001	9/38	12/54	1.01 (0.39–2.65)	0.89

Characterization of and associated resistance in ESBL-PE isolates

From the 69 ESBL-positive samples, 77 different ESBL-PE isolates were identified by MALDI-TOF Mass Spectrometry: E. coli was the main enterobacterial species (60/77: 78%), followed by Klebsiella pneumoniae (16/77: 21%) and Enterobacter cloacae (1/77: 1%). Among the healthy volunteers, 21/101 had an ESBL-producing E. coli among whom three had also an ESBL-producing K. pneumoniae isolate, and one had an ESBL-producing K. pneumoniae. The three healthy volunteers who carried both ESBL-producing E. coli and K. pneumoniae isolates were hospitalized during the previous year. Among the hospitalized patients, 47/113 had ESBL-producing isolates: 34 an E coli isolate, 7 a K. pneumoniae isolate, 1 an E. cloacae isolate, and 5 both an E. coli isolate and a K. pneumoniae isolate.

The susceptibility pattern of the ESBL-producing strains is summarized in Figure 1. ESBL-producing isolates from healthy volunteers were more frequently resistant to chloramphenicol and fluoroquinolones, while isolates from inpatients showed higher resistance rates to tetracyclines and aminoglycosides. Most samples from both populations were also resistant to sulfamethoxazole–trimethoprim. All isolates were susceptible to imipenem.

FIG. 1.

Percentage of antimicrobial resistance of the ESBL-PE samples from healthy volunteers (n = 22) and hospitalized patients (n = 47). ESBL-PE, extended-spectrum β-lactamase-producing Enterobacteriaceae.

β-Lactamase production characterization

ESBL-positive strains harbored genes encoding CTX-M group 1 enzymes [CTX-M-15: 75/77 (98%)], CTX-M group 9 enzymes [CTX-M-14:1/77 (1%)], or SHV enzymes [SHV-12: 1/77 (1%)]. The bla_CTX-M-15 gene was detected alone in 15 isolates (20%) or in association with other β-lactamase genes: bla_OXA-1 and bla_TEM-1 in 8 isolates (10.6%), bla_TEM-1 and bla_SHV-1 in 4 (5.3%), bla_OXA-1 and bla_SHV-1 in 8 (10.6%), bla_TEM-1 alone in 15 (20%), bla_OXA-1 alone in 23 (30.6%), and bla_SHV-1 alone in 2 (2.6%). The bla_CTX-M-14 gene was associated with the bla_OXA-1 gene while bla_SHV-12 was detected alone. The bla_CTX-M-15 gene was found in 59 E. coli strains, 15 K. pneumoniae isolates and the single E. cloacae strain. The bla_CTX-M-14 gene was detected in one E. coli strain (healthy volunteer) and bla_SHV-12 in one K. pneumoniae isolate (healthy volunteer) (Table 4).

Table 4.

Characterization of the ESBL-PE Strains Isolated from Healthy Volunteers and Hospitalized Patients

	No. of ESBL producers (%)	All detected genes	ESBL genes	Other β-lactamase genes
Healthy volunteers (n = 22 ESBL-positive samples)
Escherichia coli	21 (84)	CTX-M, TEM, OXA-1-like (2)^a	CTX-M-15 (2)^a	TEM-1, OXA-1 (2)^a
		CTX-M, TEM (1)	CTX-M-15 (1)	TEM-1 (1)
		CTX-M, OXA-1-like (11)	CTX-M-15 (10)	OXA-1 (10)
		CTX-M-14 (1)	OXA-1 (1)
		CTX-M (6)	CTX-M-15 (6)
		CTX-M, SHV (1)	CTX-M-15 (1)	SHV-1 (1)
Klebsiella pneumoniae	4 (16)	CTX-M, SHV, OXA-1-like (1)	CTX-M-15 (1)	SHV-1, OXA-1 (1)
		CTX-M, TEM (1)	CTX-M-15 (1)	TEM-1 (1)
		CTX-M (1)	CTX-M-15 (1)
		SHV (1)	SHV-12 (1)
Hospitalized patients (n = 47 ESBL-positive samples)
E. coli	39 (75)	CTX-M, TEM, OXA-1-like (6)	CTX-M-15 (6)	TEM-1, OXA-1 (6)
		CTX-M, TEM (12)	CTX-M-15 (12)	TEM-1 (12)
		CTX-M, OXA-1-like (13)	CTX-M-15 (13)	OXA-1 (13)
		CTX-M, SHV, OXA-1-like (2)	CTX-M-15 (2)	SHV-11, OXA-1 (2)
		CTX-M (6)	CTX-M-15 (6)
K. pneumoniae	12 (23)	CTX-M, SHV, OXA-1-like (5)	CTX-M-15 (5)	SHV-1, OXA-1 (5)
		CTX-M, SHV, TEM (3)	CTX-M-15 (3)	TEM-1, SHV-1 (3)
		CTX-M, SHV (1)	CTX-M-15 (1)	SHV-1 (1)
		CTX-M, TEM (1)	CTX-M-15 (1)	TEM-1 (1)
		CTX-M (2)	CTX-M-15 (2)
Enterobacter cloacae	1 (2)	CTX-M, SHV, TEM (1)	CTX-M-15 (1)	SHV-1, TEM-1 (1)

Number of samples.

E. coli phylogenetic groups and ST131 clone

The phylogenetic group analysis indicated that the 60 ESBL-positive E. coli isolates were distributed in six phylogenetic groups: D (18/60), A (14/60), B1 (12/60), C (8/60), B2 (4/60), F (3/60), and one unknown.

Group B1 E. coli isolates were only detected from hospitalized patients, while group D isolates were mostly from healthy volunteers (12 out of 18). The ST131 clone was found only in healthy volunteers (Table 5).

Table 5.

Phylogenetic Group Assignment of the 60 ESBL-Producer E. Coli Strains Classified According to the β-Lactamase Production

Detected genes	A	B1	B2	C	D	F	Unknown	ST131
Healthy volunteers (n = 21 E. coli isolates)
CTX-M, TEM, OXA-1-like (n = 2 samples)	2	—	—	—	—	—	—	—
CTX-M, TEM (n = 1 sample)	—	—	1	—	—	—	—	1
CTX-M, OXA-1-like (n = 11 samples)	2	—	2	—	7	—	—
CTX-M (n = 6 samples)	—	—	1	—	5	—	—	1
CTX-M, SHV (n = 1 sample)	1	—	—	—	—	—	—	—
Hospitalized patients (n = 39 E. coli isolates)
CTX-M, TEM (n = 4 samples)	1	1	—	—	1	1	—	—
CTX-M (n = 2 samples)	1	1	—	—	—	—	—	—
CTX-M, OXA-1-like (n = 4 samples)	1	—	—	—	3	—	—	—
CTX-M, TEM, OXA-1-like (n = 2 samples)	—	2	—	—	—	—	—	—
CTX-M, TEM (n = 6 samples)	2	1	—	2	—	1	—	—
CTX-M (n = 2 samples)	—	2	—	—	—	—	—	—
CTX-M, OXA-1-like (n = 3 samples)	2	1	—	—	—	—	—	—
CTX-M, TEM, OXA-1-like (n = 2 samples)	—	—	—	2	—	—	—	—
CTX-M, TEM (n = 2 samples)	—	—	—	2	—	—	—	—
CTX-M (n = 2 samples)	—	2	—	—	—	—	—	—
CTX-M, OXA-1-like (n = 6 samples)	2	1	—	—	2	1	—	—
CTX-M, TEM, OXA-1-like (n = 2 samples)	—	—	—	2	—	—	—	—
CTX-M, SHV, OXA-1-like (n = 2 samples)	—	1	—	—	—	—	1	—

Discussion

In this study, we investigated the prevalence of healthy community volunteers and hospitalized patients with intestinal carriage of ESBL-PE in Burkina Faso. Overall, we found a prevalence of fecal ESBL-PE carriage of 32%, which is much higher than what is observed in the countries in the North, and particularly in Europe, where fecal carriage rates range from 0.6% to 11.6%.^12–14 However, our results are consistent with data from various countries of Sub-Saharan Africa: 16–55% in Cameroon^7,15 and 31% in Niger.¹⁶ This geographical difference is underlined by studies reporting that the antibiotic resistance level in low-income countries is dramatically increasing, mainly as a consequence of hygiene policy failure, poor drug quality, antibiotic misuse, and lack of surveillance programs.^12,17,18 In our study, the prevalence of fecal carriage was significantly higher in hospitalized patients compared with community volunteers (42% vs. 22%, p = 0.02), in agreement with previous work^7,15 showing that inpatients are more exposed to strong selective pressure of antibiotics or bacterial transmission. Nevertheless, the proportion of ESBL-PE fecal carriage in healthy volunteers was also high, suggesting that ESBL-producing isolates can spread in the community beyond the hospital environment (nosocomial infections), thus potentially increasing the seriousness of community-acquired infections.

Our risk factor analysis showed that in the community, previous hospital stays during the last year and antibiotic use within the last 3 months are high risk factors of ESBL-PE fecal carriage, differently from what was reported by Rodriguez-Bano et al. in Spain and Wu et al. in Hong Kong.^19,20 This discrepancy could be explained by the different clinical practices in these three countries. Indeed in Burkina Faso, like in many less wealthy countries, the number of physicians, microbiologists, and epidemiologists who can guide/supervise appropriate diagnostic testing, treatment, and control of infectious diseases is insufficient. Moreover, in Burkina Faso, antibiotics can be purchased over the counter without medical prescription. Patients may buy only a few tablets of an antibiotic because of limited availability of money. Moreover, patients may begin an antimicrobial regimen and stop it when they feel better, before the end of the treatment, to save the remaining tablets for another time. All these reasons can explain why prior hospitalization or previous antibiotic use can be serious risk factors of ESBL-PE fecal carriage in low- and middle-income countries, as previously highlighted by studies in Madagascar²¹ and in rural Thai communities.²² In the present study, ESBL producers were mainly E. coli and K. pneumoniae strains in hospitalized patients. Lonchel et al. in Cameroon and Zhang et al. in China reported a more important diversity of ESBL-PE species (e.g., Enterobacter spp. and Citrobacter spp.).^15,23 Nevertheless, in all reports, E. coli was the most frequently identified species during colonization by ESBL-PE.^15,23,24 Importantly, all these bacteria that transit in the human intestine can become resistant through horizontal gene exchanges.²⁵

In our study, bla_CTX-M-15 was the most frequently detected ESBL-encoding gene (98% of isolates), as previously reported in Cameroon (96% of isolates), Indonesia (94.5%), and Tunisia (91%).^7,26,27 bla_SHV-12, which was previously reported in Cameroon,^15,28 was detected in a single K. pneumoniae isolate. The SHV-12 enzyme has evolved from SHV-1 and has been detected in different Enterobacteriaceae species in other African countries.^29,30 Nevertheless CTX-M-type ESBL, especially CTX-M-15, remain dominant worldwide, except in Asia where ESBL epidemiology shows specific characteristics, with the predominance of CTX-M-9 and 14.^23,31 ESBL-encoding genes are carried by plasmids, thus facilitating their transfer between different bacterial species both in hospitals and in the community.^32,33 Most of these plasmids typically carry resistance genes also to other drugs, such as aminoglycosides and fluoroquinolones.³⁴ Accordingly, in our study, CTX-M-15 producers also showed high-level resistance to non-β-lactams, such as aminoglycosides and tetracycline in hospitalized patients and chloramphenicol and fluoroquinolones in the community volunteers. Most ESBL-PE samples from both populations were also resistant to sulfamethoxazole–trimethoprim. The high resistance level to chloramphenicol, sulfamethoxazole–trimethoprim, and fluoroquinolones was probably due to easy access and a large and uncontrolled use in the community. Concerning the level of resistance to tetracycline in hospitalized patients, except for an extensive use in hospitals, other risk factors have not been identified.

In Burkina Faso, like in many low-income countries, there are no restrictions on the use of antibiotics. Many of our patients and healthy volunteers had a history of broad-spectrum antibiotic consumption. Some antibiotics were prescribed by medical professionals, while others were not. Based on this irrational antibiotic use, we hypothesize that the high prevalence of fecal carriage of ESBL-PE that are resistant also to non-β-lactam antibiotics is caused by the strong drug-selective pressure on bacterial populations that live in the human intestine, generally in good intelligence with their host,³⁵ and not to an epidemic-resistant clone. The E. coli phylogenetic group assignment supports this hypothesis. Indeed, the 60 ESBL-producing E. coli isolates belonged to six of the eight different phylogenetic groups recently described by Clermont et al.¹⁰ Moreover, most isolates were assigned to the commensal groups A and B1. This finding contrasts with previous studies that associated the dissemination of CTX-M-15-producing isolates with the spread of the epidemic ST131 E. coli strain belonging to group B2.^36–38 In the present study, only four isolates were assigned to group B2 and only two belonged to the epidemic ST131 clone, indicating that this clone is less represented in fecal ESBL-producing E. coli. Similar results were reported in Tunisia, Libya, and Spain.^39–41 Besides group A, B1, and B2, some ESBL-producing E. coli isolates belonged also to three other phylogenetic groups associated with CTX-M-15 dissemination: the virulent extraintestinal group D, previously found in a similar study in France,⁴² and groups C and E, usually described in urinary tract infections.⁴³ This important genetic diversity among CTX-M producers in Burkina Faso suggests that horizontal plasmid transfer has played a more important role than clonal expansion in the community and hospital environments. Molecular epidemiology investigations, including multilocus sequence typing and variable number of tandem repeats analysis, two powerful tools for the genetic characterization of Enterobacteriaceae, are needed to complete this study.^44,45 This genetic characterization of Enterobacteriaceae (sensitive and resistant to antibiotics) population in Burkina Faso will enhance our understanding of epidemiology and the circulation of these bacteria within and between hospitalized patients and community populations in this country.

In summary, this first study on ESBL carriage among intestinal isolates in Burkina Faso shows that ESBL-PE intestinal carriage by asymptomatic humans in Burkina Faso is high. The characterization of β-lactamase-encoding genes highlights an important dissemination of the ESBL CTX-M-15 without clonal dissemination. History of hospitalization and previous antibiotic use are risk factors in the community. Public health efforts should focus on educating the population and healthcare professionals on the proper use of antibiotics.

Footnotes

Acknowledgments

Preliminary results were presented at the 35th Réunion Interdisciplinaire de Chimiothérapie Anti-Infectieuse (RICAI) in 2015 (Communication No. 338). The authors thank Elisabetta Andermarcher for assistance in preparing and editing the article.

Disclosure Statement

No competing financial interests exist.

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