Presence of integrons and their correlation with multidrug resistance in Salmonella enterica serovar Typhimurium: Exploratory systematic review

Nancy Yaneth Flórez , Claudia Silva, José Miguel Villarreal, Magdalena Wiesner, .

Keywords: Salmonella Typhimurium, drug resistance, multiple, genomic islands, integrons, public health

Abstract

In Salmonella enterica serovar Typhimurium (Typhimurium), multidrug resistance is associated with integrons carrying resistance genes dispersed by mobile genetic elements. This exploratory systematic review sought to identify integron types and their resistance genes in multidrug resistance Typhimurium isolates. We used Medline, PubMed, SciELO, ScienceDirect, Redalyc, and Google Scholar as motor searchers for articles in Spanish or English published between 2012 and 2020, including the keywords “integrons”, “antibiotic resistance”, and “Salmonella Typhimurium”. We included 38 articles reporting multidrug resistance up to five antibiotic families.
Class 1 integrons with aadA2 and blaPSE-1 gene cassettes were predominant, some probably related to the Salmonella genomic island 1. We did not find studies detailing class 1 and 2 integrons in the same isolate, nor class 3 integrons reported. The presence of integrons largely explains the resistance profiles found in isolates from different sources in 15 countries.

Downloads

Download data is not yet available.
  • Nancy Yaneth Flórez Grupo de Microbiología, Dirección de Investigación en Salud Pública, Instituto Nacional de Salud, Bogotá, D. C., Colombia; Doctorado en Ciencias de la Salud, Facultad de Medicina, Universidad Antonio Nariño, Bogotá, D. C., Colombia https://orcid.org/0000-0003-3389-6483
  • Claudia Silva Instituto de Biotecnología, Universidad Nacional Autónoma de México, Cuernavaca, México https://orcid.org/0000-0003-0104-8412
  • José Miguel Villarreal Grupo de Bioquímica y Biología Molecular de las Micobacterias, Facultad de Ciencias, Universidad Nacional de Colombia, Bogotá, D. C., Colombia; Grupo de Investigación en Enfermedades Infecciosas, Facultad de Medicina, Universidad Nacional de Colombia, Bogotá, D. C., Colombia https://orcid.org/0000-0002-7974-2263
  • Magdalena Wiesner Grupo de Microbiología, Dirección de Investigación en Salud Pública, Instituto Nacional de Salud, Bogotá, D. C., Colombia https://orcid.org/0000-0002-6220-5322

References

Center for Disease Control and Prevention. CDC yellow book 2020: Health information for international travel. Brunette GW, Nemhauser JB, editors. New York: Oxford University Press; 2019. https://doi.org/10.1093/med/9780190928933.001.0001

World Health Organization, Food and Agriculture Organization of the United Nations. INFOSAN activity report 2018-2019. World Health Organization, editor. Geneva: World Health Organization; 2020. p. 76.

McQuiston JR, Herrera-Leon S, Wertheim BC, Doyle J, Fields PI, Tauxe RV, et al. Molecular phylogeny of the salmonellae: Relationships among Salmonella species and subspecies determined from four housekeeping genes and evidence of lateral gene transfer events. J Bacteriol. 2008;190:7060-7. https://doi.org/10.1128/JB.01552-07

Organización Mundial de la Salud. Salmonella (no tifoidea). 2018. Fecha de consulta: 21 de agosto de 2019. Disponible en: https://www.who.int/es/news-room/fact-sheets/detail/salmonella-%28non-typhoidal%29

Rabsch W, Andrews HL, Kingsley RA, Prager R, Tschäpe H, Adams LG, et al. Salmonella enterica serotype Typhimurium and its host-adapted variants. Infect Immun. 2002;70:2249-55. https://doi.org/10.1128/IAI.70.5.2249-2255.2002

Leekitcharoenphon P, Hendriksen RS, Le Hello S, Weill F-X, Baggesen DL, Jun S-R, et al. Global genomic epidemiology of Salmonella enterica serovar Typhimurium DT104. Appl Environ Microbiol. 2016;82:2516-26. https://doi.org/10.1128/AEM.03821-15

Kingsley RA, Msefula CL, Thomson NR, Kariuki S, Holt KE, Gordon MA, et al. Epidemic multiple drug resistant Salmonella Typhimurium causing invasive disease in sub-Saharan Africa have a distinct genotype. Genome Res. 2009;19:2279-87. https://doi.org/10.1101/gr.091017.109

Wang X, Biswas S, Paudyal N, Pan H, Li X, Fang W, et al. Antibiotic resistance in Salmonella Typhimurium isolates recovered from the food chain through national antimicrobial resistance monitoring system between 1996 and 2016. Front Microbiol. 2019;10:985. https://doi.org/10.3389/fmicb.2019.00985

Deng Y, Bao X, Ji L, Chen L, Liu J, Miao J, et al. Resistance integrons: Class 1, 2 and 3 integrons. Ann Clin Microbiol Antimicrob. 2015;14:45. https://doi.org/10.1186/s12941-015-0100-6

Partridge SR, Kwong SM, Firth N, Jensen SO. Mobile genetic elements associated with antimicrobial resistance. Clin Microbiol Rev. 2018;31. https://doi.org/10.1128/CMR.00088-17

Okoro CK, Kingsley RA, Connor TR, Harris SR, Parry CM, Al-Mashhadani MN, et al. Intracontinental spread of human invasive Salmonella Typhimurium pathovariants in sub-Saharan Africa. Nat Genet. 2012;44:1215-21. https://doi.org/10.1038/ng.2423

Monte DFM, Sellera FP, Lopes R, Keelara S, Landgraf M, Greene S, et al. Class 1 integronborne cassettes harboring blaCARB-2 gene in multidrug-resistant and virulent Salmonella Typhimurium ST19 strains recovered from clinical human stool samples, United States. PLoS ONE. 2020;15:e0240978. https://doi.org/10.1371/journal.pone.0240978

Maldonado NA, Múnera MI, López JA, Sierra P, Robledo CG, Robledo J, et al. Tendencias de la resistencia a antibióticos en Medellín y municipios del Área Metropolitana entre 2007-2012: resultados de seis años de vigilancia. Biomédica. 2014;34:433-46. https://doi.org/10.7705/biomedica.v34i3.1658

Instituto Nacional de Salud. Informe de Vigilancia por Laboratorio de Salmonella spp.: “Colombia 1997-2018.” Bogotá: Instituto Nacional de Salud; 2019. p. 25.

Ministerio de Salud y Protección Social. Plan Nacional de Respuesta a la resistencia a los antimicrobianos. Plan estratégico. Bogotá: Minsalud; 2018.

Arksey H, O’Malley L. Scoping studies: Towards a methodological framework. Int J Soc Res Methodol. 2005;8:19-32. https://doi.org/10.1080/1364557032000119616

Peters MDJ, Godfrey CM, Khalil H, McInerney P, Parker D, Soares CB. Guidance for conducting systematic scoping reviews. Int J Evid Based Healthc. 2015;13:141-6. https://doi.org/10.1097/XEB.0000000000000050

National Center for Emerging and Zoonotic Infectious Diseases (NCEZID), Division of Foodborne, Waterborne, and Environmental Diseases (DFWED). Glossary of Terms Related to Antibiotic Resistance | NARMS | CDC [Internet]. National Antimicrobial Resistance Monitoring System for Enteric Bacteria (NARMS). 2019. Fecha de consulta: 29 de octubre de 2023. Disponible en: https://www.cdc.gov/narms/resources/glossary.html

Rodríguez EC, Díaz-Guevara P, Moreno J, Bautista A, Montaño L, Realpe ME, et al. Laboratory surveillance of Salmonella enterica from human clinical cases in Colombia 2005-2011. Enferm Infecc Microbiol Clin. 2017;35:417-25. https://doi.org/10.1016/j.eimc.2016.02.023

Moher D, Liberati A, Tetzlaff J, Altman DG, PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. PLoS Med. 2009;6:e1000097. https://doi.org/10.1371/journal.pmed.1000097

Akinyemi KO, Ajoseh SO. Factors contributing to the emergence and spread of antibiotics resistance in salmonella species. In: Mares M, editor. Current topics in salmonella and salmonellosis. InTech; 2017. https://doi.org/10.5772/67701

Dessie HK, Bae DH, Lee YJ. Characterization of integrons and their cassettes in Escherichia coli and Salmonella isolates from poultry in Korea. Poult Sci. 2013;92:3036-43. https://doi.org/10.3382/ps.2013-03312

Roberts MC, Schwarz S. Tetracycline and phenicol resistance genes and mechanisms: Importance for agriculture, the environment, and humans. J Environ Qual. 2016;45:576-92. https://doi.org/10.2134/jeq2015.04.0207

Roberts MC. Tetracycline resistance determinants: Mechanisms of action, regulation of expression, genetic mobility, and distribution. FEMS Microbiol Rev. 1996;19:1-24. https://doi.org/10.1111/j.1574-6976.1996.tb00251.x

White PA, McIver CJ, Rawlinson WD. Integrons and gene cassettes in the enterobacteriaceae. Antimicrob Agents Chemother. 2001;45:2658-61. https://doi.org/10.1128/AAC.45.9.2658-2661.2001

Leverstein-van Hall MA, Blok HEM, Donders RT, Paauw A, Fluit AC, Verhoef J. Multidrug resistance among Enterobacteriaceae is strongly associated with the presence of integrons and is independent of species or isolate origin. J Infect Dis. 2003;187:251-9. https://doi.org/10.1086/345880

Jia C, Wang Z, Huang C, Teng L, Zhou H, An H, et al. Mobilome-driven partitions of the resistome in Salmonella. mSystems. 2023;e0088323. https://doi.org/10.1128/msystems.00883-23

European Food Safety Authority, European Centre for Disease Prevention and Control. The European Union One Health 2019 zoonoses report. EFSA J. 2021;19:e06406. https://doi.org/10.2903/j.efsa.2021.6406

Simpson KMJ, Hill-Cawthorne GA, Ward MP, Mor SM. Diversity of Salmonella serotypes from humans, food, domestic animals and wildlife in New South Wales, Australia. BMC Infect Dis. 2018;18:623. https://doi.org/10.1186/s12879-018-3563-1

Lammie SL, Hughes JM. Antimicrobial resistance, food safety, and one health: The need for convergence. Annu Rev Food Sci Technol. 2016;7:287-312. https://doi.org/10.1146/annurev-food-041715-033251

World Health Organization. Global antimicrobial resistance surveillance system (GLASS) report: Early implementation 2017-2018. Geneva: World Health Organization; 2018. p. 164.

Anderson ES. Drug resistance in Salmonella Typhimurium and its implications. BMJ. 1968;3:333-9. https://doi.org/10.1136/bmj.3.5614.333

Huyan J, Tian Z, Zhang Y, Zhang H, Shi Y, Gillings MR, et al. Dynamics of class 1 integrons in aerobic biofilm reactors spiked with antibiotics. Environ Int. 2020;140:105816. https://doi.org/10.1016/j.envint.2020.105816

World Health Organization. Critically important antimicrobials for human medicine. 5th rev. Geneva: World Health Organization; 2017.

World Health Organization. Critically important antimicrobials for human medicine. 6th revision. Geneva: World Health Organization; 2019.

Guerra B, Soto S, Cal S, Mendoza MC. Antimicrobial resistance and spread of class 1 integrons among Salmonella serotypes. Antimicrob Agents Chemother. 2000;44:2166-9. https://doi.org/10.1128/AAC.44.8.2166-2169.2000

Madec JY, Doublet B, Ponsin C, Cloeckaert A, Haenni M. Extended-spectrum β-lactamase blaCTX-M-1 gene carried on an IncI1 plasmid in multidrug-resistant Salmonella enterica serovar Typhimurium DT104 in cattle in France. J Antimicrob Chemother. 2011;66:942-4. https://doi.org/10.1093/jac/dkr014

Gallardo F, Ruiz J, Soto SM, Jiménez de Anta MT, Vila J. Distintos mecanismos de resistencia asociados a integrones en aislamientos clínicos de Salmonella Typhimurium. Rev Esp Quimioter. 2003;16:398-402.

Partridge SR, Tsafnat G, Coiera E, Iredell JR. Gene cassettes and cassette arrays in mobile resistance integrons. FEMS Microbiol Rev. 2009;33:757-84. https://doi.org/10.1111/j.1574-6976.2009.00175.x

Pulecio-Santos S, Bermúdez-Duarte P, Suárez Alfonso MC. Susceptibilidad antimicrobiana de aislamientos de Salmonella enterica obtenidos del pre-beneficio y de porcinos en Colombia. Rev Salud Pública. 2015;17:106-19. https://doi.org/10.15446/rsap.v17n1.45716

O’Mahony R, Quinn T, Drudy D, Walsh C, Whyte P, Mattar S, et al. Antimicrobial resistance in nontyphoidal Salmonella from food sources in Colombia: Evidence for an unusual plasmid-localized class 1 integron in serotypes Typhimurium and Anatum. Microb Drug Resist. 2006;12:269-77. https://doi.org/10.1089/mdr.2006.12.269

Flórez-Delgado NY, Ubillus EN, Pérez-Sepúlveda B, Ospina-Ríos EL, Carrascal-Camacho AK, Chamorro-Tobar IC, et al. Class 1 integrons in clinical and swine industry isolates of Salmonella Typhimurium from Colombia, dating 1997 to 2017. J Med Microbiol. 2023;72. https://doi.org/10.1099/jmm.0.001704

Balsalobre LC, Dropa M, Matté MH. An overview of antimicrobial resistance and its public health significance. Braz J Microbiol. 2014;45:1-5. https://doi.org/10.1590/S1517-83822014005000033

Organización Mundial de la Salud. Lista OMS de antimicrobianos de importancia crítica para la medicina humana (lista OMS de AIC). Geneva: OMS; 2019. p. 2.

How to Cite
1.
Flórez NY, Silva C, Villarreal JM, Wiesner M. Presence of integrons and their correlation with multidrug resistance in Salmonella enterica serovar Typhimurium: Exploratory systematic review. Biomed. [Internet]. 2024 May 30 [cited 2026 Jan. 12];44(2):258-76. Available from: https://revistabiomedicaorg.biteca.online/index.php/biomedica/article/view/6816

Some similar items:

Published
2024-05-30
Section
Topic review

Altmetric

Article metrics
Abstract views
Galley vies
PDF Views
HTML views
Other views
Crossref Cited-by logo
Escanea para compartir
QR Code