Plasmid mechanisms of resistance to quinolones, beta-lactams and colistin in Salmonella enterica. Paraguay 2020-2021

Authors

DOI:

https://doi.org/10.18004/mem.iics/1812-9528/2023.e21122313

Keywords:

Salmonella, resistance, antimicrobials, plasmid

Abstract

Bacteria can develop antimicrobial resistance mechanisms, those acquired and transmissible being the most significant due to the potential for dissemination. The emergence of Salmonella enterica with resistance to third-generation cephalosporins, quinolones, and colistin represents a progressive threat. The objective was to determine antimicrobial resistance and the presence of plasmid resistance mechanisms to quinolones, β-lactams, and colistin in Salmonella isolates from integrated surveillance of enteropathogens. Five hundred and one strains of Salmonella spp. collected between 2020 and 2021 were studied by the enteropathogen network of the Laboratorio Central de Salud Publica (Central Public Health Laboratory). Research was conducted on the resistance to third-generation cephalosporins, quinolones, and colistin, isolated from humans, foodstuffs, animals for consumption, and the environment. The strains studied exhibited resistance to tetracycline (32.5%), nalidixic acid (29%), ampicillin (13.2%), nitrofurantoin (11.6%), third-generation cephalosporins (7.2%), cotrimoxazole (5.8%), and ciprofloxacin (2.2%). Eighteen percent (90/501) presented plasmid-transferable resistance, 111 genes were detected (71 strains with one gene, 17 strains with two genes, and 2 strains with three different genes). Qnr B: 41.1% (37/90), mcr-1: 38.9% (35/90), CMY: 23.3% (21/90), CTX-M: 16.7% (15/90), and Qnr S: 3.3% (3/90). Heidelberg was the predominant serovar in chicken samples and the largest carrier of CMY and mcr-1 resistance genes. The detection of genes in foodstuffs and animals for consumption, which can be easily transmitted to humans, is a cause for alarm and highlights the importance of continuing to strengthen multisectoral and multidisciplinary surveillance.

Downloads

Download data is not yet available.

References

Daza Pérez RM. Resistencia bacteriana a antimicrobianos: su importancia en la toma de decisiones en la práctica diaria. Inf Ter Sis Nac Salud. 1998; 22(3):57-67

Álvarez-Hernández DA, Garza-Mayén GS, Vázquez-López R. Quinolonas: Perspectivas actuales y mecanismos de resistencia. Rev Chilena infectol. 2015 Oct; 32(5): 499-504. doi:10.4067/S0716-0182015000600002.

González-Torralba A, García-Esteban C, Alós JI. Enteropatógenos y antibióticos. Enferm Infecc Microbiol Clín. 2018; 36(1): 47-54. doi: 10.1016/j.eimc.2015.06.015

Moura Q, Fernandes MR, Silva KC, Monte DF, Esposito F, Dropa M, et al. Virulent nontyphoidal Salmonella producing CTX-M and CMY-2 β-lactamases from livestock, food and human infection, Brazil. Virulence. 2018; 9(1):281-286. doi: 10.1080/21505594.2017.1279779

Navarro F, Calvo J, Cantón R, Fernández-Cuenca F, Mirelis B. Detección fenotípica de mecanismos de resistencia en microorganismos gramnegativos. Enferm Infecc Microbiol Clín . 2011 ;29(7): 524-534. doi: 10.1016/j.eimc.2011.03.011

Pallecchi L, Bartoloni A, Fiorelli C, Mantella A, Di Maggio T, Gamboa H, et al. Rapid Dissemination and Diversity of CTX-M Extended-Spectrum β-Lactamase Genes in Commensal Escherichia coli Isolates from Healthy Children from Low-Resource Settings in Latin America. Antimicrob Agents Chemother. 2007; 51(8): 2720-5. doi: 10.1128/AAC.00026-07

Sennati S, Santella G, Di Conza J, Pallecchi L, Pino M, Ghiglione B, et al. Changing Epidemiology of Extended-Spectrum β-Lactamases in Argentina: Emergence of CTX-M-15. Antimicrob Agents Chemother . 2012; 56(11): 6003-5. doi: 10.1128/AAC.00745-12

Khan MA, Lemmens N, Riera E, Blonk T, Goedhart J, Van Belkum A, et al. Dominance of CTX-M-2 and CTX-M-56 among extended-spectrum β-lactamases produced by Klebsiella pneumoniae and Escherichia coli isolated in hospitals in Paraguay. J Antimicrob Chemother.2009; 64(6): 1330-2. doi: 10.1093/jac/dkp382

Guillén R, Velázquez G, Lird G, Espínola C, Laconich M, Carpinelli L, et al. Detección molecular de belactamasas de espectro extendido (BLEE) en enterobacterias aisladas en Asunción. Mem Inst Investig Cienc Salud. 2016; 14(1): 8-16. https://revistascientificas.una.py/index.php/RIIC/article/view/1839

Bevan ER, Jones AM, Hawkey PM. Global epidemiology of CTX-M β-lactamases: temporal and geographical shifts in genotype. J Antimicrob Chemother . 2017; 72(8):2145-55. doi: 10.1093/jac/dkx146

Martínez Rojas DDV. Betalactamasas tipo AmpC: Generalidades y métodos para detección fenotípica. Rev Soc Ven Microbiol. 2009; 29(2):78-83. http://www.redalyc.org/exportarcita.oa?id=199414957003

Cejas D, Vignoli R, Quinteros M, Marino R, Callejo R, Betancor L, et al. First detection of CMY-2 plasmid mediated ß-lactamase in Salmonella Heidelberg in South America. Rev Argent Microbiol. 2014; 46(1):30-33. doi: 10.1016/S0325-7541(14)70044-6

Tijerino Ayala A, Bolaños Acuña HM, Acuña Calvo MT, Vargas Morales JL, Campos Chacón E. Emergencia de β-lactamasa AmpC plasmídica del grupo CMY-2 en Shigella sonnei y Salmonella spp. en Costa Rica, 2003-2015. Rev Panam Salud Publica. 2016; 40(1):70-75.

Van den Berg RR, Dissel S, Rapallini MLBA, van der Weijden CC, Wit B, Heymans R. Characterization and whole genome sequencing of closely related multidrug-resistant Salmonella enterica serovar Heidelberg isolates from imported poultry meat in the Netherlands. PLoS One. 2019; 14(7): e0219795. doi: 10.1371/journal.pone.0219795

Seral C, Gude M, Castillo F. Emergencia de β-lactamasas AmpC plasmídicas (pAmpC ó cefamicinasas): origen, importancia, detección y alternativas terapéuticas. Rev Esp Quimioter 2012; 25: 89-99.

Azargun R, Gholizadeh P, Sadeghi V, Hosainzadegan H, Tarhriz V, Memar MY, et al. Molecular mechanisms associated with quinolone resistance in Enterobacteriaceae: review and update. Trans R Soc Trop Med Hyg. 2020;114(10): 770-781. doi: 10.1093/trstmh/traa041

Barreiros de Souza R, Magnani M, Rocha Moreira de Oliveira T C. Mecanismos de resistência às quinolonas em Salmonella spp. Semina: Ciências Agrárias 2010;31(2):413-427. https://www.redalyc.org/articulo.oa?id=445744096014

Toribio L, Sevilla C, Gonzales-Escalante E. Marcadores de resistencia plasmídica a quinolonas qnr en aislamientos clínicos de enterobacterias productoras de betalactamasas CTX-M en Lima, Perú. Rev Peru Med Exp Salud Publica. 2019; 36(2): 265-9. doi: http://dx.doi.org/10.17843/rpmesp.2019.362.3960

Rodríguez-Martínez JM, Cano ME, Velasco C, Martínez-Martínez L, Pascual A. Plasmid-mediated quinolone resistance: an update. J Infect Chemother. 2011; 17(2): 149-82. doi: 10.1007/s10156-010-0120-2

Albornoz E, Lucero C, Romero G, Quiroga MP, Rapoport M, Guerriero L, et al. Prevalence of Plasmid-Mediated Quinolone Resistance Genes in Clinical Enterobacteria from Argentina. Microb Drug Resist. 2017;23(2):177-87. doi: 10.1089/mdr.2016.0033

Iglesias-Osores S. Uso de colistina en el sector pecuario: necesidad de una prohibición global. Acta Med Peru. 2020; 37(1): 114-5. doi: https://doi.org/10.35663/amp.2020.371.898

Melgarejo Touchet NL. Resistencia a colistina en enterobacterales. Rev salud publica Parag. diciembre de 2022; 12(2): 48-61. doi: 10.18004/rspp.diciembre.48

Liu YY, Wang Y, Walsh TR, Yi LX, Zhang R, Spencer J, et al. Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: a microbiological and molecular biological study. Lancet Infect Dis. 2016; 16(2):161-8. doi: 10.1016/S1473-3099(15)00424-7

Poirel L, Jayol A, Nordmann P. Polymyxins: Antibacterial Activity, Susceptibility Testing, and Resistance Mechanisms Encoded by Plasmids or Chromosomes. Clin Microbiol Rev. 2017;30(2):557-596. doi: 10.1128/CMR.00064-16

Grimont P, Weill FX. Antigenic formulae of the salmonella servovars. 9° Ed. WHO Collaborating Center for Reference and Research on Salmonella. Institut Pasteur.2007;1-166.

Díaz O G, Rosadio A R, Marcelo M G, Chero O A, Jiménez A R, Reyna W I, et al. Evaluación de una Técnica de PCR-Múltiple para la Detección Rápida de Salmonella Typhimurium y Enteritidis en Cuyes (Cavia porcellus) Naturalmente Infectados. Rev Inv Vet Perú. 2017; 28(3): 713-722. doi: 10.15381/rivep.v28i3.13361

CLSI. Clinical & Laboratory Standards Institute. [citado 9 de julio de 2023]. M100Ed33 | Performance Standards for Antimicrobial Susceptibility Testing, 33rd Edition. Disponible en: https://clsi.org/standards/products/microbiology/documents/m100/

INEI-ANLIS. Servicio Antimicrobianos. Protocolos Colistín | antimicrobianos.com.arantimicrobianos.com.ar [Internet]. [citado 9 de julio de 2023]. Disponible en: Disponible en: http://antimicrobianos.com.ar/2017/09/protocolos-colistin/

INEI-ANLIS. Servicio Antimicrobianos. Protocolos de métodos moleculares | antimicrobianos.com.arantimicrobianos.com.ar [Internet]. [citado 9 de julio de 2023]. Disponible en: Disponible en: http://antimicrobianos.com.ar/category/protocolos-de-metodos-moleculares/

Newcombe RG. Two-sided confidence intervals for the single proportion: comparison of seven methods. Stat Med. 1998; 17(8): 857-872. doi: 10.1002/(SICI)1097-0258(19980430)17:8<857::AID-SIM777>3.0.CO;2-E

Ortiz F, Weiler N, Alvarez M, Orrego MV, Kawabata A, Riera E, et al. Resistencia a múltiples antibióticos en serovariedades de Salmonella aisladas de muestras clínicas y alimentos. Mem Inst Investig Cienc Salud. 2021; 19(1): 37-47. doi: 10.18004/mem.iics/1812-9528/2021.019.01.37

Puig Peña Y, Leyva Castillo V, Tejedor Arias R, Illnait Zaragoz MT, Ferrer Márquez Y, Camejo Jardines A. Susceptibilidad antimicrobiana y serovariedades de Salmonella aisladas en carnes y productos cárnicos. Rev haban cienc méd. 2021;20(2): e3894. Disponible en: http://www.revhabanera.sld.cu/index.php/rhab/article/view/3894

Quino W, Hurtado CV, Meza AM, Zamudio ML, Gavilan RG, Quino W, et al. Patrones de resistencia a los antimicrobianos en serovares de Salmonella enterica en Perú, 2012-2015. Rev Chilena Infectol. 2020; 37(4): 395-401. doi: 10.4067/S0716-10182020000400395

European Food Safety Authority (EFSA); European Centre for Disease Prevention and Control (ECDC). The European Union Summary Report on Antimicrobial Resistance in zoonotic and indicator bacteria from humans, animals and food in 2020/2021. EFSA J. 2023 Mar 6;21(3): e07867. doi: 10.2903/j.efsa.2023.7867

Dos Reis RO, Cecconi MC, Timm L, Souza MN, Ikuta N, Wolf JM, et al. Salmonella isolates from urine cultures: serotypes and antimicrobial resistance inhospital settings. Braz J Microbiol. 2019 Apr; 50(2): 445-448. doi: 10.1007/s42770-019-00052-y

Lee S, Park N, Yun S, Hur E, Song J, Lee H, et al. Presence of plasmid-mediated quinolone resistance (PMQR) genes in non-typhoidal Salmonella strains with reduced susceptibility to fluoroquinolones isolated from human salmonellosis in Gyeonggi-do, South Korea from 2016 to 2019. Gut Pathog. 2021;13(1):35. doi: 10.1186/s13099-021-00431-7

Pribul BR, Festivo ML, Souza MMS, Rodrigues Ddos P. Characterization of quinolone resistance in Salmonella spp. isolates from food products and human samples in Brazil. Braz J Microbiol. 2016;47(1):196-201. doi: 10.1016/j.bjm.2015.04.001

Melgarejo-Touchet N, Busignani S, Dunjo P, Brítez M, Weiler N, Orrego V, et al. Resistencia antimicrobiana en Escherichia coli de muestras cecales de bovinos para carne faenados en frigoríficos de la zona del arroyo Mburicao, Asunción-Paraguay. Año 2021. Mem Inst Investig Cienc Salud. 2022; 20(3):51-9. doi: 10.18004/mem.iics/1812-9528/2022.020.03.51

Doublet B, Praud K, Nguyen-Ho-Bao T, Argudín MA, Bertrand S, Butaye P, et al. Extended-spectrum β-lactamase- and AmpC β-lactamase-producing D-tartrate-positive Salmonella enterica serovar Paratyphi B from broilers and human patients in Belgium, 2008-10. J Antimicrob Chemother . 2014; 69(5): 1257-64. doi: 10.1093/jac/dkt504

Kwon BR, Wei B, Cha SY, Shang K, Zhang JF, Jang HK, et al. Characterization of Extended-Spectrum Cephalosporin (ESC) Resistance in Salmonella Isolated from Chicken and Identification of High Frequency Transfer of blaCMY-2 Gene Harboring Plasmid In Vitro and In Vivo. Animals (Basel). 2021; 11(6):1778. doi: 10.3390/ani11061778

Depoorter P, Persoons D, Uyttendaele M, Butaye P, De Zutter L, Dierick K, et al. Assessment of human exposure to 3rd generation cephalosporin resistant E. coli (CREC) through consumption of broiler meat in Belgium. Int J Food Microbiol. 2012; 159(1): 30-8. doi: 10.1016/j.ijfoodmicro.2012.07.026

Melo RT, Galvão NN, Guidotti-Takeuchi M, Peres PABM, Fonseca BB, Profeta R, et al. Molecular Characterization and Survive Abilities of Salmonella Heidelberg Strains of Poultry Origin in Brazil. Front Microbiol. 2021; 12: 674147. doi: 10.3389/fmicb.2021.674147

Aravena C, Valencia B, Villegas A, Ortega M, Fernández R A, Araya R P, et al. Caracterización de cepas clínicas y ambientales de Salmonella enterica subsp. enterica serovar Heidelberg aisladas en Chile. Rev Med Chil. 2019; 147(1): 24-33. doi: 10.4067/S0034-98872019000100024

Rau RB, Ribeiro AR, dos Santos A, Barth AL. Antimicrobial resistance of Salmonella from poultry meat in Brazil: results of a nationwide survey. Epidemiol Infect. 2021; 149: e228. doi: 10.1017/S0950268821002156

Diaz D, Hernandez-Carreño PE, Velazquez DZ, Chaidez-Ibarra MA, Montero-Pardo A, Martinez-Villa FA, et al. Prevalence, main serovars and anti-microbial resistance profiles of non-typhoidal Salmonella in poultry samples from the Americas: A systematic review and meta-analysis. Transbound Emerg Dis. 2022; 69(5): 2544-58. doi: 10.1111/tbed.14362

Alikhan NF, Moreno LZ, Castellanos LR, Chattaway MA, McLauchlin J, Lodge M, et al. Dynamics of Salmonella enterica and antimicrobial resistance in the Brazilian poultry industry and global impacts on public health. PLoS Genet. 2022; 18(6): e1010174. doi: 10.1371/journal.pgen.1010174

Silva KC, Fontes LC, Moreno AM, Astolfi-Ferreira CS, Ferreira AJP, Lincopan N. Emergence of Extended-Spectrum-β-Lactamase CTX-M-2-Producing Salmonella enterica Serovars Schwarzengrund and Agona in Poultry Farms. Antimicrob Agents Chemother. 2013; 57(7): 3458-9. doi: 10.1128/AAC.05992-11

Fernandes SA, Camargo CH, Francisco GR, Bueno MFC, Garcia DO, Doi Y, et al. Prevalence of Extended-Spectrum β-Lactamases CTX-M-8 and CTX-M-2-Producing Salmonella Serotypes from Clinical and Nonhuman Isolates in Brazil. Microb Drug Resist. 2017; 23(5):580-9. doi: 10.1089/mdr.2016.0085

Granda A, Riveros M, Martínez-Puchol S, Ocampo K, Laureano-Adame L, Corujo A, et al. Presence of Extended-Spectrum β-lactamase, CTX-M-65 in Salmonella enterica serovar Infantis Isolated from Children with Diarrhea in Lima, Peru. J Pediatr Infect Dis. 2019; 14(4):194-200. doi: 10.1055/s-0039-1685502

Di Marcantonio L, Romantini R, Marotta F, Chiaverini A, Zilli K, Abass A, et al. The Current Landscape of Antibiotic Resistance of Salmonella Infantis in Italy: The Expansion of Extended-Spectrum Beta-Lactamase Producers on a Local Scale. Front Microbiol. 2022; 13:812481. doi: 10.3389/fmicb.2022.812481

Brown AC, Chen JC, Watkins LKF, Campbell D, Folster JP, Tate H, et al. CTX-M-65 Extended-Spectrum β-Lactamase-Producing Salmonella enterica Serotype Infantis, United States1. Emerg Infect Dis. 2018; 24 (12): 2284-2291. doi: 10.3201/eid2412.180500

Bertani AM de J, Cunha MPV, de Carvalho E, Araújo LT, dos Santos CA, Amarante AF, et al. Genomic characterization of a multi-drug resistant, CTX-M-65-producing clinical isolate of Salmonella Infantis isolated in Brazil. Microbes Infect. 2022;24(5):104972. doi: 10.1016/j.micinf.2022.104972

Fortini D, Owczarek S, Dionisi AM, Lucarelli C, Arena S, Carattoli A, et al. Colistin Resistance Mechanisms in Human Salmonella enterica Strains Isolated by the National Surveillance Enter-Net Italia (2016-2018). Antibiotics (Basel). 2022; 11(1): 102. doi: 10.3390/antibiotics11010102

Lentz SAM, Dalmolin TV, Barth AL, Martins AF. mcr-1 Gene in Latin America: How Is It Disseminated Among Humans, Animals, and the Environment? Front Public Health. 2021; 9: 648940. doi: 10.3389/fpubh.2021.648940

Melgarejo Touchet N, Martínez M, Franco R, Falcón M, Busignani S, Espínola C, et al. Resistencia plasmídica a colistin por el gen mcr-1 en Enterobacteriaceae en Paraguay. Rev salud publica Parag. 2018;8(1):44-8. Disponible en: https://revistas.ins.gov.py/index.php/rspp/article/view/58

Mendes Oliveira VR, Paiva MC, Lima WG. Plasmid-mediated colistin resistance in Latin America and Caribbean: A systematic review. Travel Med Infect Dis. 2019; 31: 101459. doi: 10.1016/j.tmaid.2019.07.015. Epub 2019 Jul 20. PMID: 31336179

Anyanwu MU, Jaja IF, Nwobi OC. Occurrence and Characteristics of Mobile Colistin Resistance (mcr) Gene-Containing Isolates from the Environment: A Review. Int J Environ Res Public Health. 2020; 17(3): 1028. doi: 10.3390/ijerph17031028

INEI_ANLIS. Servicio Antimicrobianos. Alerta mcr-1. INEI-ANLIS. Servicio Antimicrobianos. Alerta epidemiológica: Emergencia de resistencia plasmídica (transferible) a colistina/polimixina B mcr-1 en Argentina. Boletín informativo No 3. Febrero 2016. Disponible en http://antimicrobianos.com.ar/2016/02/alertaepidemiologico-emergencia-de-resistenciaplasmidica-transferible-a-colistinapolimixina-b-mcr1-en-argentina/

Fernandes MR, Moura Q, Sartori L, Silva KC, Cunha MP, Esposito F, et al. Silent dissemination of colistin-resistant Escherichia coli in South America could contribute to the global spread of the mcr-1 gene. Euro Surveill. 2016; 21(17). doi: 10.2807/1560-7917.ES.2016.21.17.30214

Sennati S, Di Pilato V, Riccobono E, Di Maggio T, Villagran AL, Pallecchi L, et al. Citrobacter braakii carrying plasmid-borne mcr-1 colistin resistance gene from ready-to-eat food from a market in the Chaco region of Bolivia. J Antimicrob Chemother. 2017; 72(7): 2127-2129. doi: 10.1093/jac/dkx078

Saavedra SY, Diaz L, Wiesner M, Correa A, Arévalo SA, Reyes J, et al. Genomic and Molecular Characterization of Clinical Isolates of Enterobacteriaceae Harboring mcr-1 in Colombia, 2002 to 2016. Antimicrob Agents Chemother. 2017; 61(12): e00841-17. doi: 10.1128/AAC.00841-17

Garza-Ramos U, Tamayo-Legorreta E, Arellano-Quintanilla DM, Rodriguez-Medina N, Silva-Sanchez J, Catalan-Najera J, et al. Draft Genome Sequence of a Multidrug- and Colistin-Resistant mcr-1-Producing Escherichia coli Isolate from a Swine Farm in Mexico. Genome Announc. 2018; 6(10): e00102-18. doi: 10.1128/genomeA.00102-18

Legarraga P, Wozniak A, Prado S, Estrella L, García P, Legarraga P, et al. Primera comunicación en Chile de la detección del gen mcr-1 en un aislado clínico de Escherichia coli resistente a colistín. Rev Chilena Infectol. 2018;35(4):453-4. doi: 10.4067/s0716-10182018000400453

Delgado-Blas JF, Ovejero CM, Abadia-Patiño L, Gonzalez-Zorn B. Coexistence of mcr-1 and blaNDM-1 in Escherichia coli from Venezuela. Antimicrob Agents Chemother. 2016; 60(10):6356-8. doi: 10.1128/AAC.01319-16

Sia CM, Greig DR, Day M, Hartman H, Painset A, Doumith M, et al. The characterization of mobile colistin resistance (mcr) genes among 33 000 Salmonella enterica genomes from routine public health surveillance in England. Microb Genom. 2020; 6(2): e000331. doi: 10.1099/mgen.0.000331

Published

2023-10-19

How to Cite

Ortiz, F., Weiler, N., Álvarez, M., Orrego, V., Martínez, J., Melgarejo, N., … González, M. (2023). Plasmid mechanisms of resistance to quinolones, beta-lactams and colistin in Salmonella enterica. Paraguay 2020-2021. Memorias Del Instituto De Investigaciones En Ciencias De La Salud, 21(1). https://doi.org/10.18004/mem.iics/1812-9528/2023.e21122313

Issue

Section

Articulos Originales

Similar Articles

<< < 1 2 3 4 5 > >> 

You may also start an advanced similarity search for this article.

Most read articles by the same author(s)

1 2 > >>