Carbapenemase-Encoding Genes and Colistin Resistance in Gram-Negative Bacteria During the COVID-19 Pandemic in Mexico: Results from the Invifar Network
Restricted accessResearch articleFirst published online June, 2023
Carbapenemase-Encoding Genes and Colistin Resistance in Gram-Negative Bacteria During the COVID-19 Pandemic in Mexico: Results from the Invifar Network
In this study, we report the carbapenemase-encoding genes and colistin resistance in Escherichia coli, Klebsiella pneumoniae, Acinetobacter baumannii, and Pseudomonas aeruginosa in the second year of the COVID-19 pandemic. Clinical isolates included carbapenem-resistant K. pneumoniae, carbapenem-resistant E. coli, carbapenem-resistant A. baumannii, and carbapenem-resistant P. aeruginosa. Carbapenemase-encoding genes were detected by PCR. Carbapenem-resistant K. pneumoniae and carbapenem-resistant E. coli isolates were analyzed using the Rapid Polymyxin NP assay. mcr genes were screened by PCR. Pulsed-field gel electrophoresis and whole-genome sequencing were performed on representative isolates. A total of 80 carbapenem-resistant E. coli, 103 carbapenem-resistant K. pneumoniae, 284 carbapenem-resistant A. baumannii, and 129 carbapenem-resistant P. aeruginosa isolates were recovered. All carbapenem-resistant E. coli and carbapenem-resistant K. pneumoniae isolates were included for further analysis. A selection of carbapenem-resistant A. baumannii and carbapenem-resistant P. aeruginosa strains was further analyzed (86 carbapenem-resistant A. baumannii and 82 carbapenem-resistant P. aeruginosa). Among carbapenem-resistant K. pneumoniae and carbapenem-resistant E. coli isolates, the most frequent gene was blaNDM (86/103 [83.5%] and 72/80 [90%], respectively). For carbapenem-resistant A. baumannii, the most frequently detected gene was blaOXA-40 (52/86, 60.5%), and for carbapenem-resistant P. aeruginosa, was blaVIM (19/82, 23.2%). For carbapenem-resistant A. baumannii, five indistinguishable pulsotypes were detected. Circulation of K. pneumoniae New Delhi metallo-β-lactamase (NDM) and E. coli NDM was detected in Mexico. High virulence sequence types (STs), such as K. pneumoniae ST307, E. coli ST167, P. aeruginosa ST111, and A. baumannii ST2, were detected. Among K. pneumoniae isolates, 18/101 (17.8%) were positive for the Polymyxin NP test (two, 11.0% positive for the mcr-1 gene, and one, 5.6% with disruption of the mgrB gene). All E. coli isolates were negative for the Polymyxin NP test. In conclusion, K. pneumoniae NDM and E. coli NDM were detected in Mexico, with the circulation of highly virulent STs. These results are relevant in clinical practice to guide antibiotic therapies considering the molecular mechanisms of resistance to carbapenems.
Get full access to this article
View all access options for this article.
References
1.
LangfordBJ, SoM, RaybardhanS, et al.Bacterial co-infection and secondary infection in patients with COVID-19: A living rapid review and meta-analysis. Clin Microbiol Infect, 2020; 26(12):1622–1629; doi: 10.1016/j.cmi.2020.07.016
2.
LansburyL, LimB, BaskaranV, et al.Co-infections in people with COVID-19: A systematic review and meta-analysis. J Infect, 2020; 81(2):266–275; doi: 10.1016/j.jinf.2020.05.046
3.
Palacios-BaenaZR, GiannellaM, ManisseroD, et al.Risk factors for carbapenem-resistant Gram-negative bacterial infections: A systematic review. Clin Microbiol Infect, 2021; 27(2):228–235; doi: 10.1016/j.cmi.2020.10.016
4.
LoganLK, WeinsteinRA. The epidemiology of carbapenem-resistant Enterobacteriaceae: The impact and evolution of a global menace. J Infect Dis, 2017; 215(Suppl 1):S28–S36; doi: 10.1093/infdis/jiw282
5.
WongD, NielsenTB, BonomoRA, et al.Clinical and pathophysiological overview of Acinetobacter infections: A century of challenges. Clin Microbiol Rev, 2017; 30(1):409–447; doi: 10.1128/CMR.00058-16
6.
MiriagouV, CornagliaG, EdelsteinM, et al.Acquired carbapenemases in Gram-negative bacterial pathogens: Detection and surveillance issues. Clin Microbiol Infect, 2010; 16(2):112–122; doi: 10.1111/j.1469-0691.2009.03116.x
7.
RolainJM, ParolaP, CornagliaG. New Delhi metallo-beta-lactamase (NDM-1): Towards a new pandemia?. Clin Microbiol Infect, 2010; 16(12):1699–1701; doi: 10.1111/j.1469-0691.2010.03385.x
8.
NoriP, SzymczakW, PuiusY, et al.Emerging co-pathogens: New Delhi metallo-beta-lactamase producing Enterobacterales infections in New York City COVID-19 patients. Int J Antimicrob Agents, 2020; 56(6):106179; doi: 10.1016/j.ijantimicag.2020.106179
9.
Ambler RP. The structure of beta-lactamases. Philos Trans R Soc Lond B Biol Sci, 1980; 289(1036):321–331; doi: 10.1098/rstb.1980.0049
NordmannP, NaasT, PoirelL. Global spread of Carbapenemase-producing Enterobacteriaceae. Emerg Infect Dis, 2011; 17(10):1791–1798; doi: 10.3201/eid1710.110655
12.
Hammoudi HalatD, Ayoub MoubareckC. The current burden of Carbapenemases: Review of significant properties and dissemination among Gram-negative bacteria. Antibiotics (Basel), 2020; 9(4):186; doi: 10.3390/antibiotics9040186
13.
CuiX, ZhangH, DuH. Carbapenemases in Enterobacteriaceae: Detection and antimicrobial therapy. Front Microbiol, 2019; 10:1823; doi: 10.3389/fmicb.2019.01823
14.
SafaviM, BostanshirinN, HajikhaniB, et al.Global genotype distribution of human clinical isolates of New Delhi metallo-β-lactamase-producing Klebsiella pneumoniae: A systematic review. J Glob Antimicrob Resist, 2020; 23:420–429; doi: 10.1016/j.jgar.2020.10.016
15.
JeannotK, BolardA, PlésiatP. Resistance to polymyxins in Gram-negative organisms. Int J Antimicrob Agents, 2017; 49(5):526–535; doi:10.1016/j.ijantimicag.2016.11.029
16.
BialvaeiAZ, Samadi KafilH. Colistin, mechanisms and prevalence of resistance. Curr Med Res Opin, 2015; 31(4):707–721; doi: 10.1185/03007995.2015.1018989
17.
ZayyadH, Eliakim-RazN, LeiboviciL, et al.Revival of old antibiotics: Needs, the state of evidence and expectations. Int J Antimicrob Agents, 2017; 49(5):536–541; doi: 10.1016/j.ijantimicag.2016.11.021
18.
MlynarcikP, KolarM. Molecular mechanisms of polymyxin resistance and detection of mcr genes. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub, 2019; 163(1):28–38; doi: 10.5507/bp.2018.070
19.
GogryFA, SiddiquiMT, SultanI, et al.Current update on intrinsic and acquired colistin resistance mechanisms in Bacteria. Front Med (Lausanne), 2021; 8:677720; doi: 10.3389/fmed.2021.677720
20.
Rodríguez-SantiagoJ, Cornejo-JuárezP, Silva-SánchezJ, et al.Polymyxin resistance in Enterobacterales: Overview and epidemiology in the Americas. Int J Antimicrob Agents, 2021; 58(5):106426; doi: 10.1016/j.ijantimicag.2021.106426
21.
CLSI. M100-S30. Performance Standards for Antimicrobial Susceptibility Testing; Twenty-Second Informational Supplement. Clinical and Laboratory Standars Institute: Wayne, PA; 2020.
22.
BogaertsP, Rezende de CastroR, de MendonçaR, et al.Validation of carbapenemase and extended-spectrum β-lactamase multiplex endpoint PCR assays according to ISO 15189. J Antimicrob Chemother, 2013; 68(7):1576–1582; doi: 10.1093/jac/dkt065
23.
HongSS, KimK, HuhJY, et alJ. Multiplex PCR for rapid detection of genes encoding class A carbapenemases. Ann Lab Med, 2012; 32(5):359–361; doi: 10.3343/alm.2012.32.5.359
Pérez-PérezFJ, HansonND. Detection of plasmid-mediated AmpC beta-lactamase genes in clinical isolates by using multiplex PCR. J Clin Microbiol, 2002; 40(6):2153–2162; doi: 10.1128/jcm.40.6.2153–2162.2002
26.
BrinkAJ, CoetzeeJ, CorcoranC, et al.Emergence of OXA-48 and OXA-181 carbapenemases among Enterobacteriaceae in South Africa and evidence of in vivo selection of colistin resistance as a consequence of selective decontamination of the gastrointestinal tract. J Clin Microbiol, 2013; 51(1):369–372; doi: 10.1128/JCM.02234-12
27.
NordmannP, JayolA, PoirelL. Rapid detection of polymyxin resistance in Enterobacteriaceae. Emerg Infect Dis, 2016; 22(6):1038–1043; doi: 10.3201/eid2206.151840
28.
Rodríguez-SantiagoJ, Rodríguez-MedinaN, Tamayo-LegorretaEM, et al.Molecular and genomic insights of mcr-1-producing Escherichia coli isolates from piglets. Antibiotics (Basel), 2022; 11(2):157; doi: 10.3390/antibiotics11020157
29.
CannatelliA, D'AndreaMM, GianiT, et al.In vivo emergence of colistin resistance in Klebsiella pneumoniae producing KPC-type carbapenemases mediated by insertional inactivation of the PhoQ/PhoP mgrB regulator. Antimicrob Agents Chemother, 2013; 57(11):5521–5526; doi: 10.1128/AAC.01480-13
TenoverFC, ArbeitRD, GoeringRV, et al.Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: Criteria for bacterial strain typing. J Clin Microbiol, 1995; 33(9):2233–2239.
32.
BarriosH, Garza-RamosU, Reyna-FloresF, et al.Isolation of carbapenem-resistant NDM-1-positive Providencia rettgeri in Mexico. J Antimicrob Chemother, 2013; 68(8):1934–1936; doi: 10.1093/jac/dkt124
33.
Bocanegra-IbariasP, Garza-GonzálezE, Morfín-OteroR, et al.Molecular and microbiological report of a hospital outbreak of NDM-1-carrying Enterobacteriaceae in Mexico. PLoS One, 2017; 12(6):e0179651; doi: 10.1371/journal.pone.0179651
34.
Aquino-AndradeA, Merida-VieyraJ, Arias de la GarzaE. Carbapenemase-producing Enterobacteriaceae in Mexico: Report of seven non-clonal cases in a pediatric hospital. BMC Microbiol, 2018; 18(1):38; doi: 10.1186/s12866-018-1166-z
35.
Garza-GonzálezE, Bocanegra-IbariasP, Rodríguez-NoriegaE, et al.Molecular investigation of an outbreak associated with total parenteral nutrition contaminated with NDM-producing Leclercia adecarboxylata. BMC Infect Dis, 2021; 21(1):235; doi: 10.1186/s12879-021-05923-0
36.
Garza-GonzálezE, Bocanegra-IbariasP, Bobadilla-Del-ValleM, et al.Drug resistance phenotypes and genotypes in Mexico in representative gram-negative species: Results from the infivar network. PLoS One, 2021; 16(3):e0248614; doi:10.1371/journal.pone.0248614
VillaL, FeudiC, FortiniD, et al.Diversity, virulence, and antimicrobial resistance of the KPC-producing. Microb Genom, 2017; 3(4):e000110; doi: 10.1099/mgen.0.000110
39.
WyresKL, HoltKE. Klebsiella pneumoniae population genomics and antimicrobial-resistant clones. Trends Microbiol, 2016; 24(12):944–956; doi: 10.1016/j.tim.2016.09.007
40.
SchauflerK, NowakK, DüxA, et al.Clinically relevant ESBL-producing. Front Microbiol, 2018; 9:150; doi: 10.3389/fmicb.2018.00150
41.
LongSW, OlsenRJ, EagarTN, et al.Population genomic analysis of 1,777 extended-spectrum beta-lactamase-producing. mBio, 2017; 8(3):e00489-17; doi: 10.1128/mBio.00489-17
42.
BaekEH, KimSE, KimS, et al.Successful control of an extended-spectrum beta-lactamase-producing Klebsiella pneumoniae ST307 outbreak in a neonatal intensive care unit. BMC Infect Dis, 2020; 20(1):166; doi: 10.1186/s12879-020-4889-z
43.
KimJO, SongSA, YoonEJ, et al.Outbreak of KPC-2-producing Enterobacteriaceae caused by clonal dissemination of Klebsiella pneumoniae ST307 carrying an IncX3-type plasmid harboring a truncated Tn4401a. Diagn Microbiol Infect Dis, 2017; 87(4):343–348; doi: 10.1016/j.diagmicrobio.2016.12.012
44.
BoonstraMB, SpijkermanDCM, Voor In ‘t HoltAF, et al.An outbreak of ST307 extended-spectrum beta-lactamase (ESBL)-producing. Infect Control Hosp Epidemiol, 2020; 41(1):31–36; doi: 10.1017/ice.2019.304
45.
Bocanegra-IbariasP, Garza-GonzálezE, Padilla-OrozcoM, et al.The successful containment of a hospital outbreak caused by NDM-1-producing Klebsiella pneumoniae ST307 using active surveillance. PLoS One, 2019; 14(2):e0209609; doi: 10.1371/journal.pone.0209609
46.
LuB, LinC, LiuH, et al.Molecular characteristics of Klebsiella pneumoniae isolates from outpatients in Sentinel Hospitals, Beijing, China, 2010–2019. Front Cell Infect Microbiol, 2020; 10:85; doi: 10.3389/fcimb.2020.00085
47.
CarattoliA, BertiniA, VillaL, et al.Identification of plasmids by PCR-based replicon typing. J Microbiol Methods, 2005; 63(3):219–228; doi: 10.1016/j.mimet.2005.03.018
48.
Flores-ValdezM, AresMA, Rosales-ReyesR, et al.Whole genome sequencing of pediatric. Front Microbiol, 2021; 12:711577; doi: 10.3389/fmicb.2021.711577
49.
BartualSG, SeifertH, HipplerC, et al.Development of a multilocus sequence typing scheme for characterization of clinical isolates of Acinetobacter baumannii. J Clin Microbiol, 2005; 43(9):4382–4390; doi: 10.1128/JCM.43.9.4382–4390.2005
50.
DiancourtL, PassetV, NemecA, et al.The population structure of Acinetobacter baumannii: Expanding multiresistant clones from an ancestral susceptible genetic pool. PLoS One, 2010; 5(4):e10034; doi:10.1371/journal.pone.0010034
51.
GaiarsaS, Batisti BiffignandiG, EspositoEP, et al.Comparative analysis of the two. Front Microbiol, 2019; 10:930; doi:10.3389/fmicb.2019.00930
52.
WarethG, LindeJ, HammerP, et al.Molecular characterization of German. Pathogens, 2021; 10(6):60690; doi:10.3390/pathogens10060690
53.
EjazH, AhmadM, YounasS, et al.Molecular epidemiology of extensively-drug resistant. Infect Drug Resist, 2021; 14:1931–1939; doi: 10.2147/IDR.S310478
54.
AbdollahiA, AliramezaniA, SalehiM, et al.Co-infection of ST2. BMC Infect Dis, 2021; 21(1):927. doi: 10.1186/s12879-021-06642-2
55.
MeshkatZ, SalimizandH, AminiY, et al.Detection of efflux pump genes in multiresistant Acinetobacter baumannii ST2 in Iran. Acta Microbiol Immunol Hung, 2021; 68(2):113–120; doi: 10.1556/030.2021.01314
56.
NogbouND, RamashiaM, NkawaneGM, et al.Whole-genome sequencing of a colistin-resistant. Antibiotics (Basel), 2022; 11(5):594; doi: 10.3390/antibiotics11050594
57.
Mancilla-RojanoJ, OchoaSA, Reyes-GrajedaJP, et al.Molecular epidemiology of Acinetobacter calcoaceticus-Acinetobacter baumannii complex isolated from children at the Hospital Infantil de México Federico Gómez. Front Microbiol, 2020; 11:576673; doi: 10.3389/fmicb.2020.576673
58.
CurranB, JonasD, GrundmannH, et al.Development of a multilocus sequence typing scheme for the opportunistic pathogen Pseudomonas aeruginosa. J Clin Microbiol, 2004; 42(12):5644–5649; doi:10.1128/JCM.42.12.5644–5649.2004
59.
YooJS, YangJW, KimHM, et al.Dissemination of genetically related IMP-6-producing multidrug-resistant Pseudomonas aeruginosa ST235 in South Korea. Int J Antimicrob Agents, 2012; 39(4):300–304; doi: 10.1016/j.ijantimicag.2011.11.018
60.
HrabákJ, CervenáD, IzdebskiR, et al.Regional spread of Pseudomonas aeruginosa ST357 producing IMP-7 metallo-β-lactamase in Central Europe. J Clin Microbiol, 2011; 49(1):474–475; doi: 10.1128/JCM.00684-10
OliverA, MuletX, López-CausapéC, et al.The increasing threat of Pseudomonas aeruginosa high-risk clones. Drug Resist Updat, 2015; 21–22:41–59; doi: 10.1016/j.drup.2015.08.002
63.
KossowA, KampmeierS, WillemsS, et al.Control of multidrug-resistant Pseudomonas aeruginosa in allogeneic hematopoietic stem cell transplant recipients by a novel bundle including remodeling of sanitary and water supply systems. Clin Infect Dis, 2017; 65(6):935–942; doi: 10.1093/cid/cix465
64.
Molina-MoraJA, Chinchilla-MonteroD, García-BatánR, et al.Genomic context of the two integrons of ST-111 Pseudomonas aeruginosa AG1: A VIM-2-carrying old-acquaintance and a novel IMP-18-carrying integron. Infect Genet Evol, 2021; 89:104740; doi: 10.1016/j.meegid.2021.104740
65.
PapagiannitsisCC, VerraA, GalaniV, et al.Unravelling the features of success of VIM-producing ST111 and ST235. Microorganisms, 2020; 8(12):1884; doi: 10.3390/microorganisms8121884
66.
ZhangL, TanFC, StrasfeldL, et al.Long-term dominance of Carbapenem-non-susceptible. Front Cell Infect Microbiol, 2022; 12:904602; doi: 10.3389/fcimb.2022.904602
67.
LiX, FuY, ShenM, et al.Dissemination of blaNDM-5 gene via an IncX3-type plasmid among non-clonal Escherichia coli in China. Antimicrob Resist Infect Control, 2018; 7:59; doi: 10.1186/s13756-018-0349-6
68.
GiufrèM, ErricoG, AccogliM, et al.Emergence of NDM-5-producing Escherichia coli sequence type 167 clone in Italy. Int J Antimicrob Agents, 2018; 52(1):76–81; doi: 10.1016/j.ijantimicag.2018.02.020
69.
RamadanH, GuptaSK, SharmaP, et al.Circulation of emerging NDM-5-producing Escherichia coli among humans and dogs in Egypt. Zoonoses Public Health, 2020; 67(3):324–329; doi: 10.1111/zph.12676
70.
EndimianiA, BrilhanteM, BernasconiOJ, et al.Employees of Swiss veterinary clinics colonized with epidemic clones of carbapenemase-producing Escherichia coli. J Antimicrob Chemother, 2020; 75(3):766–768; doi: 10.1093/jac/dkz470
71.
ChakrabortyT, SadekM, YaoY, et al.Cross-border emergence of Escherichia coli producing the Carbapenemase NDM-5 in Switzerland and Germany. J Clin Microbiol, 2021; 59(3):e02238-20; doi: 10.1128/JCM.02238-20
72.
LiJ, WangJ, YangY, et al.Etiology and antimicrobial resistance of secondary bacterial infections in patients hospitalized with COVID-19 in Wuhan, China: A retrospective analysis. Antimicrob Resist Infect Control, 2020; 9(1):153; doi: 10.1186/s13756-020-00819-1
73.
Garza-GonzálezE, Morfín-OteroR, Mendoza-OlazaránS, et al.A snapshot of antimicrobial resistance in Mexico. Results from 47 centers from 20 states during a six-month period. PLoS One, 2019; 14(3):e0209865; doi: 10.1371/journal.pone.0209865
74.
López-JácomeLE, Fernández-RodríguezD, Franco-CendejasR, et al.Increment antimicrobial resistance during the COVID-19 pandemic: Results from the Invifar Network. Microb Drug Resist, 2021; doi: 10.1089/mdr.2021.0231
75.
Merida-VieyraJ, De Colsa-RaneroA, Arzate-BarbosaP, et al.First clinical isolate of Escherichia coli harboring mcr-1 gene in Mexico. PLoS One, 2019; 14(4):e0214648; doi: 10.1371/journal.pone.0214648
Supplementary Material
Please find the following supplemental material available below.
For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.
For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.
