Molecular Characterization of Carbapenemase-Producing Escherichia coli and Salmonella in children with diarrhea in rural Burkina Faso.

doi:10.21203/rs.3.rs-19069/v1

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Molecular Characterization of Carbapenemase-Producing Escherichia coli and Salmonella in children with diarrhea in rural Burkina Faso.

https://doi.org/10.21203/rs.3.rs-19069/v1

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Background In recent years, Carbapenemase-producing Enterobacteriaceae (CPE) resistance to antibiotics has dramatically increased leading to limitations of their treatment options. In the present study, we investigated the occurrence of carbapenemase-producing Escherichia coli and Salmonella in rural Burkina Faso, using bacterial strains obtained from previous studies.

Results Diarrheagenic Escherichia coli (DEC) strains was identified using 16-plex Polymerase Chain Reaction (PCR), whereas antibiotic susceptibility was realized using the disk diffusion method. Furthermore, multiplex PCR assays were used to characterize bla KPC, bla VIM and bla IMP genes in carbapenemase-producing E . coli and Salmonella . The study highlighted high resistance rates of the identified bacteria to common antibiotics. Likewise, two strains of E . coli were imipenem resistant with Carbapenemase-encoding genes. The genes detected were Klebsiella pneumoniae carbapenemase (KPC), Verona integrin-encoded metallo-β-lactamase (VIM) and Imipenemase (IMP-2) reaching a rate of 40% each. However, no Carbapenemase-encoding genes were detected in Salmonella isolates.

Conclusions This study showed that for a real-time infection control and prompt application of antimicrobial chemotherapy, characterization of carbapenemase-producing Enterobacteriaceae in patients is crucial.

Drug Discovery, Design, & Development

Antibiotics

Carbapenemase-Producing Enterobacteriaceae

children

Burkina Faso

New antimicrobial resistance mechanisms are emerging and spreading globally, hampering our ability to effectively treat common infectious diseases. This has extended illness, disability and increased death rates [1]. As a result, antimicrobial resistance represents a major challenge for public health worldwide. One of the most worrying threat is the emergence and rapid dissemination of carbapenem resistant Gram-negative bacteria, following the spread of carbapenemase-producing Enterobacteriaceae (CPE) [2, 3]. In bacteria of animal and human origins, beta-lactam resistance, which includes resistance to extended-spectrum beta-lactams, has now been increasingly observed [4]. In Enterobacteriaceae, the carbapenemases have been previously classified into the three following classes : class A [ie K. pneumoniae carbapenemase (KPC) enzymes], Class B [ie metallo-beta-lactamases (MBL)] including New Delhi metallo-β-lactamase (NDM), Verona integrin-encoded metallo-β-lactamase (VIM), Imipenemase (IMP), and Class D [ie oxacillinase (OXA)-48 and related variants] [5–7]. Enterobacteriaceae can be resistant to carbapenems through intrinsic or acquired mechanisms. The intrinsic mechanisms can occur by (a) production of chromosomal carbapenemases from the group of class A serine carbapenemases [8] or (b) efflux pumps or (c) reduction in outer membrane permeability through porin loss [9].

The acquired resistance is a plasmid-mediated mechanism through which the mobile carbapenemases are easily transmitted between bacteria (Table 1; [10]).

Table 1

The plasmid-mediated mechanisms of resistance [10]
Type of mechanism of resistance	Examples
(a) Carbapenemases	(1) Class A serine carbapenemases
	Klebsiella pneumoniae carbapenamse (KPC)
	Guiana extended spectrum (GES)
	(2) Class B metallo-β-lactamases (MBLs)
	Verona integron-encoded metallo-β-lactamase (VIM)
	Active on imipenem (IMP)
	Sao Paulo metallo-β-lactamase (SPM)
	Seoul imipenemase (SIM)
	German imipenemase (GIM)
	New Delhi metallo-β-lactamase (NDM)
	(3) Class D serine carbapenemases
	OXA β-lactamases (e.g. OXA-48 and variants)
(b) Amp-C beta-lactamase OR extended spectrum beta-lactamase (ESBL) production along with efflux pumps or porin loss

The recent spread of CPE is one of the major public health threats worldwide [11] because carbapenems are among the main stay of therapy for treating severe infections directly related to multidrug-resistant bacteria producing extended-spectrum β-lactamases (ESBLs) [12]. Carbapenemases are defined as β-lactamases that hydrolyze almost all beta-lactam antibiotics. According to some recent studies, the most prevalent carbapenemases in Enterobacteriaceae are bla_KPC (Ambler class A), bla_VIM, bla_IMP, bla_NDM (class B) and bla_OXA-48 like (class D) [11, 13]. Although several studies reported the occurrence of carbapenemases producing bacteria in Africa [12], to our best knowledge, no study focusing on the molecular characterization of carbapenemase-producing E. coli and Salmonella has been undertaken in Burkina Faso. Therefore, the objective of the present study was to carry out a molecular characterization of Carbapenemase-Producing Escherichia coli and Salmonella isolates recovered from children in two rural hospitals in Burkina Faso.

Bacterial strains

Bacterial strains were obtained from our previous studies [14, 15] conducted in Gourcy and Boromo municipalities (Fig. 1). The 16-plex PCR was used to detect simultaneously 16 genes from the five main pathogroups of E. coli (enterohemoragic E. coli: EHEC, enteropathogenic E. coli: EPEC, enteroaggregative E. coli: EAEC, enteroinvasive E. coli: EIEC and enterotoxigenic E. coli: ETEC) as described by Antikainen et al. [16]. The genes investigated and primers used are listed in Table 2 [16–18]. A questionnaire was used to collect demographic information (e.g., age and sex) of each patient).

Table 2

Oligonucleotides primers used for multiplex PCR reaction
Pathotype	Target gene	Primer sequence (5' to 3')	Size (bp)	[C] (µM)	Reference
Typical EPEC	bfpB	MP3-bfpB-F: GACACCTCATTGCTGAAGTCG	910	0.1	[18]
Typical EPEC	bfpB	MP3-bfpB-R:CCAGAACACCTCCGTTATGC	910	0.1	[18]
EHEC and EPEC	eaeA	eae-F:TCAATGCAGTTCCGTTATCAGTT	482	0.1	[18]
	eaeA	eae-R:GTAAAGTCCGTTACCCCAACCTG	482	0.1	[18]
	escV	MP3-escV-F:ATTCTGGCTCTCTTCTTCTTTATGGCTG	544	0.4	[18]
	escV	MP3-escV-R:CGTCCCCTTTTACAAACTTCATCGC	544	0.4	[18]
	Ent	ent-F:TGGGCTAAAAGAAGACACACTG	629	0.4	[18]
	Ent	ent-R:CAAGCATCCTGATTATCTCACC	629	0.4	[18]
EHEC	EHEC-hly	hlyEHEC-F: TTCTGGGAAACAGTGACGCACATA	688	0.1	[17]
	EHEC-hly	hlyEHEC-R: TCACCGATCTTCTCATCCCAATG	688	0.1	[17]
	Stx1	MP4-stx1A-F:CGATGTTACGGTTTGTTACTGTGACAGC	244	0.2	[18]
	Stx1	MP4-stx1A-R:AATGCCACGCTTCCCAGAATTG	244	0.2	[18]
	Stx2	MP3-stx2AF:GTTTTGACCATCTTCGTCTGATTATTGAG	324	0.4	[18]
	Stx2	MP3-stx2A-R:AGCGTAAGGCTTCTGCTGTGAC	324	0.4	[18]
EAEC	astA	MP-astA-F TGCCATCAACACAGTATATCCG	102	0.4	[18]
	astA	MP2-astA-R ACGGCTTTGTAGTCCTTCCAT	102	0.4	[18]
	aggR	MP2-aggR-F:ACGCAGAGTTGCCTGATAAAG	400	0.2	[18]
	aggR	MP2-aggR-R:AATACAGAATCGTCAGCATCAGC	400	0.2	[18]
	Pic	MP2-pic-F:AGCCGTTTCCGCAGAAGCC	1111	0.2	[18]
	Pic	MP2-pic-R:AAATGTCAGTGAACCGACGATTGG	1111	0.2	[18]
EIEC	invE	MP2-invE-F:CGATAGATGGCGAGAAATTATATCCCG	766	0.2	[18]
	invE	MP2-invE-R:CGATCAAGAATCCCTAACAGAAGAATCAC	766	0.2	[18]
	ipaH	ipaH-F: GAAAACCCTCCTGGTCCATCAGG	437	0.1	[19]
	ipaH	ipaH-R:GCCGGTCAGCCACCCTCTGAGAGTAC	437	0.1	[19]
ETEC	elt	MP2-LT-F: GAACAGGAGGTTTCTGCGTTAGGTG	655	0.1	[18]
	elt	MP2-LT-R: CTTTCAATGGCTTTTTTTTGGGAGTC	655	0.1	[18]
	estA	MP4-STIa-F : CCTCTTTTAGYCAGACARCTGAATCASTTG	157	0.4	[18]
	estA	MP4-STIa-R : CAGGCAGGATTACAACAAAGTTCACAG	157	0.4	[18]
	estB	MP2-STI-F : TGTCTTTTTCACCTTTCGCTC	171	0.2	[18]
	estB	MP2-STI-R CGGTACAAGCAGGATTACAACAC	171	0.2	[18]
E. coli	uidA	MP2-uidA-F:ATGCCAGTCCAGCGTTTTTGC	1487	0.2	[19]
E. coli	uidA	MP2-uidA-R:AAAGTGTGGGTCAATAATCAGGAAGTG	1487	0.2	[19]

Antimicrobial susceptibility testing and ESBL production

Antibiotic susceptibility was determined on Mueller–Hinton agar using the standard disc diffusion procedure as described by the European Committee of Antimicrobial Susceptibility Testing (EUCAST) [19]. Nineteen antibiotics belonging to 7 different families were tested : amoxicillin (25 µg), amoxicillin-clavulanic acid (20/10 µg), ceftriaxone (30 µg), cefotaxime (30 µg), cefepime (30 µg), cefixime (10 µg), piperacillin (75 µg), piperacillin-tazobactam (100 + 10 µg), imipenem (10 µg), tetracycline (30 µg), chloramphenicol (30 µg), trimethoprim-sulfametoxazole (1.25 ± 23.75 µg), aztreonam (30 µg), colistin sulfate (50 µg), ciprofloxacin (5 µg), nalidixic acid (30 µg), gentamycin (15 µg), netilmicin (10 µg) and tobramycin (10 µg) (Bio-Rad, France). The diameters of the antibiotic sensitivity halos were recorded according to the recommendations of EUCAST. Intermediary (I) susceptibility of pathovars was classified as resistant (R). A double synergy test was used for ESBL-producing strains testing. This consisted of placing discs (2–3 cm diameter) of ceftriaxone and cefotaxime around an amoxicillin-clavulanic acid disc on the bacterial plate.

Detection of antibiotic resistance genes

DNA for PCR analysis was extracted from the isolates using the heat lysis method [20]. A loopful of bacterial growth from Mueller Hinton agar (Liofilchem, Italy) plate was suspended in 1 ml of sterile water, and the mixture was boiled for 10 min at + 100 °C and centrifuged for 10 min at 12000 rpm at + 4 °C. The obtained supernatant was collected and used for PCR reactions. Multiplex PCR assays were carried out using oligonucleotides (Table 3) to detect the presence of genes of the bla_KPC, bla_VIM and bla_IMP types in carbapenemase-producing E. coli and Salmonella strains [21, 22].

Table 3

Oligonucleotides used to amplify carbapenemases genes
Primer name	Target	Primers sequence (5'to3')	Size (bp)	Reference
KPC- F KPC-R	bla_KPC	GCT CAG GCG CAA CTG TAA G	300	[21]
KPC- F KPC-R	bla_KPC	AGC ACA GCG GCA GCA AGA AAG	300	[21]
VIM- F VIM-R	bla_VIM	CAG ATT GCC GAT GGT GTT TGG	390	[22]
VIM- F VIM-R	bla_VIM	AGG TGG GCC ATT CAG CCA GA	390	[22]
IMP- F IMP-R	bla_IMP	GGA ATA GAG TGG CTT AAT TCTC	232	[22]
IMP- F IMP-R	bla_IMP	GTG ATG CGT CYC CAA YTT CAC T	232	[22]

About2.5 µl of supernatant were added to 22.5 µl reaction mixture containing 5U of Taq DNA polymerase (Accu Power, Korea), deoxyribonucleic triphosphate (10 mM), buffer GC (10X), MgCl2 (25 mM), and PCR primers (10 µM). We performed PCR conditions as followed: 5 min at + 94 °C, followed by 35 amplification cycles of + 94 °C for 30 s, 59 ± 4 °C for 60 s and + 72 °C for 60 s with a final extension of + 72 °C for 10 min on a thermal cycler (Gene Amp 9700, Applied Biosystems). Our reaction products were separated by electrophoresis in (1.5% weight/volume) agarose gel, stained with a Redsafe solution (Prolabo, France) and visualized under ultraviolet (UV) light (Gel Logic 200).

Bacterial isolates

Of the 275 stool samples, about five isolates were confirmed as E. coli strains: 3 EAEC (60%), and 2 atypical EPEC (40%). Nine Salmonella isolates were detected belonging to the following serotypes: Salmonella Poona, S. Typhimurium, S. Ouakam, S. Virchow, S. Duisburg and S. Hvittingfoss.

Antimicrobial resistance

The identified E. coli trains were 100% resistant to amoxicillin-clavulanic acid, amoxicillin and tetracycline; 80% resistant to trimetoprim-sulfametoxazol, colistin-sulfate and piperacillin; 60% resistant to cefotaxim, ceftriaxone, aztreonam, cefixime and cefepime. Whereas, resistance to chloramphenicol was shown in 40% of isolates. Antimicrobial susceptibility testing revealed that two E. coli strains were imipenem–resistant.

The Salmonella trains were 100% resistant to amoxicillin, 89% to amoxicillin-clavulanic acid, 67% to tetracycline, cefixime and cefepime; 56% resistant to ceftriaxone, cefotaxim and colistin-sulfate, 30–50% resistant to aztreonam, trimetoprim-sulfametoxazol and piperacillin while no resistance was shown to imipenem (Fig. 2). Thus, global prevalences of carbapenemase-producing E. coli and Salmonella enterica in the study children were 1.81% and 0%, respectively.

Carbapenemase genes

The carbapenemase genes have been reported in two strains (one atypical EPEC and one EAEC) which were resistant to imipenem. Each of these two isolates carried the following genes: bla_KPC, bla_VIM and bla_IMP−2. No carbapenemase genes were detected in Salmonella isolates (Table 4). All five strains were isolated in children of one year old while the sex distribution was 4/5 (80%) for male and 1/5 (20%) for female. The five E. coli isolates were carbapenemase and ESBL-producing strains (Table 4).

Table 4

Carbapenemase-producing Enterobacteriaceae
Code (E. coli pathovars)	Sex	Age (year)	Carbapenemase genes + ESBL phenotypes	Carbapenemase genes			Total N (%)
Code (E. coli pathovars)	Sex	Age (year)	Carbapenemase genes + ESBL phenotypes	bla_KPC	bla_VIM	bla_IMP−2	Total N (%)
025 B (EAEC)	M	1	-/+	-	-	-	0 (0)
039B (EAEC)	F	1	-/+	-	-	-	0 (0)
043B (Atypical EPEC)	M	1	+/+	+	+	+	3 (50)
044B (EAEC)	M	1	+/+	+	+	+	3 (50)
046B (Atypical EPEC)	M	1	-/+	-	-	-	0 (0)
Code (S. serovars)
084B (S. Duisburg)	M	3	-/+	-	-	-	0 (0)
057B (S. Poona)	M	2	-/-	-	-	-	0 (0)
066B (S. Typhimurium)	M	1	-/-	-	-	-	0 (0)
068B (S. Typhimurium)	M	2	-/+	-	-	-	0 (0)
078B (S. Ouakam)	M	1	-/-	-	-	-	0 (0)
063G (S. Hvittingfoss)	F	1	-/+	-	-	-	0 (0)
087G (S. Poona)	F	1	-/+	-	-	-	0 (0)
112G1 (S. Virchow)	F	3	-/-	-	-	-	0 (0)
112G2 (S. Virchow)	F	3	-/-	-	-	-	0 (0)

Increasing numbers of antibiotic-resistant Enterobacteriaceae are responsible of serious problems in infection control. This phenomenon also contributes to the global spread of carbapenemase- producing bacteria becoming therefore especially worrisome [23]. Indeed, it is a major public health concern, mainly within communities. Our study reported for the first time the occurrence of carbapenemase-producing E. coli in children with diarrhea in rural settings of Burkina Faso.

The isolated strains were mainly resistant to amoxicillin-clavulanic acid, amoxicillin, tetracycline, trimetoprim-sulfametoxazol, colistin-sulfate, piperacillin, cefotaxime, ceftriaxone, aztreonam, cefixime and cefepime (between 60% and 100%). Particularly, two E. coli harbored resistance patterns to imipenem. In contrast, no resistance to imipenem was observed in Salmonella strains. Similar results concerning E. coli resistance to imipenem were reported in India [12]. Susceptibility to netilmicin and ciprofloxacin appears to follow the general trend observed elsewhere in the world.

Our finding on overall prevalence of E. coli harboring carbapenemase genes in the 275 children was 1.81%. This result is similar to 2.5% reported in pets in Africa [3] suggesting that bacteria producing carbapenemase are currently spreading among these pets [3] and because of the proximity between humans and animals, these bacteria can contaminate humans. Indeed, animals could be reservoirs of gene transmission to humans. For example, it has been shown that poultry flocks contribute to the global dissemination of Salmonella Kentucky ST198-X1-SGI1CIP-R strain in developing countries [24]. Since subsistence, farming and animal husbandry are the primary economic activities for the local populations in Boromo and Gourcy, the spread of these bacteria poses serious health concerns.

Oatherwises, we detected no carbapenemase genes in Salmonella strains. This is expected because carbapenemase-producing Salmonella strains are rarely isolated. In contrast, resistance to carbapenems was observed in CIP-R Salmonella KentuckyX1-ST198-SGI1 isolates in which carbapenemases blaVIM − 2 and blaOXA − 48 have been detected [24].

Three main genes were detected in E. coli strains: Klebsiella pneumoniae carbapenemase (KPC), Verona integrin-encoded metallo-β-lactamase (VIM) and Imipenemase (IMP-2) with a rate of 40% each. To our best of knowledge, this is the first report of bla_KPC gene in E. coli in Burkina Faso. However, KPC producers have been described, mostly from nosocomial K. pneumoniae isolates, and E. coli strains in Israel but also from other enterobacterial species [25]. As K. pneumoniae was identified extensively worldwide, a study suggested that it may have contributed to the spread of the blaKPC genes [26].

As far as the class B metallo-β-lactamases (MBLs) is concerned, our results corroborate the existing reports. Endemicity of VIM- and IMP-type enzymes has been reported in Greece, Taiwan and Japan [27, 8], although outbreaks and single reports of VIM and IMP producers have been shown in many other countries [27].

It has been shown that carbapenemases can hydrolyze almost all β-lactams, and are easily transferable among enterobacterial species [28]. These genes are found in multidrug-resistant isolates consistent with the result found in the present study [28]. Therefore, its spread in Enterobacteriaceae is a public health issue. For example, invasive infections by carbapenem-resistant strains have been found to be associated with high morbidity and mortality rates [29].

Otherwises, several risk factors of colonization and infection with carbapenemase-producing Enterobacteriaceae (CPE) including severe underlying illness, prolonged hospital stay, the presence of invasive medical devices, and antibiotic use have been shown. [30–33]. According to previous studies, CPE have been associated with adverse clinical and economic outcomes such as increased mortality, increased length of stay, setting up an effective therapy scheme, decreased functional status on discharge, and increased cost of health care [34–37]. Young children (those under one year old) were severely infected with carbapenem-resistant E. coli. This is a matter of public health issues because the emergence of MBL-producing bacteria greatly limits treatment options [38]. The most frequent MBLs reported to date belong to the VIM and IMP types and have been described extensively worldwide [39].

To conclude, infections by carbapenem-resistant bacteria are difficult to treat successfully. This study highlights the need for rapid identification of MBL-producing Gram-negative species both for appropriate treatment and for timely implementation of infection control measures. In developing countries like Burkina Faso, phenotypic methods may be useful for routine detection of carbapenemase production, particularly when PCR is not available.

CPE: Carbapenemase-producing Enterobacteriaceae; DEC: Diarrheagenic Escherichia coli; KPC: Klebsiella pneumoniae Carbapenemase; VIM: Verona integron‑encoded metallo-β-lactamase; IMP: Imipenemase; NDM: New Delhi metallo-β-lactamase; ESBLs: extended-spectrum β-lactamases; EHEC: enterohemoragic E. coli; EPEC: enteropathogenic E. coli; EAEC: enteroaggregative E. coli; EIEC: enteroinvasive E. coli; ETEC: enterotoxigenic E. coli.

Acknowledgements

We thank the "Réseau de Recherche sur les Maladies Entériques à Potentiel Épidémique en Afrique de l’Ouest (REMENTA)" for assistance with PCR reagents, the "Centre National de Recherche et de Formation sur le Paludisme (CNRFP)/Ouagadougou, Burkina Faso" and the "Centre National de Référence pour les Antibiotiques (CNR-Antibiotiques)/Institut Pasteur de Côte d'Ivoire" for technical support.

Authors' contributions

Conceptualization, R.D, A.G-S and N.B; Methodology, R.D, A.K₁ and I.S; Original draft preparation, R.D; Writing-Review and Editing, R.D, A.K₁, I.S, W.A.D.K. All authors have read and approved the final manuscript.

Funding

No funding was received for this study.

Availability of data and materials

Not applicable.

Ethics approval and consent to participate

Permission to conduct the study was obtained from the hospital authorities of Burkina Faso, and informed verbal consent was obtained from the parents/guardians of every child before sample collection. The National Ethical Committee (s) of Burkina Faso (N ° 2009-39) approved the study protocol.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Author details

Laboratory of Molecular Biology, Epidemiology and Surveillance of Bacteria and Viruses Transmitted by Food/Center for Research in Biological, Food and Nutritional Sciences/Graduate School of Science and Technology/University Joseph KI-ZERBO, 03 BP 7021 Ouagadougou 03, Burkina Faso.
Training and Research Unit in Applied Sciences and Technologies/University of Dedougou, BP 176 Dedougou, Burkina Faso.
National Centre for Research and Training on Malaria, 01 BP 2208 Ouagadougou 01, Burkina Faso.
Institute of Sciences, 01 BP 1757 Ouagadougou 01, Burkina Faso.
Molecular Biology Platform, Pasteur Institute of Abidjan, Ivory Coast,01 BP 490 Abidjan 01.
Laboratory of Biological and Medical Analyzes, Pasteur Institute of Dakar, Dakar, Senegal.
Faculty of Medicine, Pharmacy and Odontology, University of Cheikh Anta DIOP of Dakar, Senegal.
Laboratory of Bacteriology-Virology, Unit of Antibiotics, Natural Substances and Surveillance of Resistance of Microorganisms to Antimicrobials/ Pasteur Institute of Abidjan, Ivory Coast, 01 BP 490 Abidjan 01.
Laboratory of Bacteriology-Virology/Unit of Training and Research of Medical Sciences/University Felix Houphouet BOIGNY, 01 BP V34 Abidjan 01, Ivory Coast.
Unit of Experimental Bacteriology, Pasteur Institute of Dakar, 36 avenue Pasteur, BP 220, Dakar, Senegal.

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Molecular Characterization of Carbapenemase-Producing Escherichia coli and Salmonella in children with diarrhea in rural Burkina Faso.

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Abstract

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Background

Methods

Bacterial strains

Antimicrobial susceptibility testing and ESBL production

Detection of antibiotic resistance genes

Results

Bacterial isolates

Antimicrobial resistance

Carbapenemase genes

Discussion

Abbreviations

Declarations

References

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