Download PDF
J Pediatr Infect Dis 2019; 14(04): 194-200
DOI: 10.1055/s-0039-1685502
Original Article
Georg Thieme Verlag KG Stuttgart · New York

Presence of Extended-Spectrum β-lactamase, CTX-M-65 in Salmonella enterica serovar Infantis Isolated from Children with Diarrhea in Lima, Peru

Ana Granda
1   Department of Pediatrics, Instituto de Medicina Tropical “Alexander von Humboldt,” Universidad Peruana Cayetano Heredia, Lima, Perú
,
Maribel Riveros
1   Department of Pediatrics, Instituto de Medicina Tropical “Alexander von Humboldt,” Universidad Peruana Cayetano Heredia, Lima, Perú
,
Sandra Martínez-Puchol
2   ISGlobal, Hospital Clinic, Universitat de Barcelona, Barcelona, Spain
,
Karen Ocampo
1   Department of Pediatrics, Instituto de Medicina Tropical “Alexander von Humboldt,” Universidad Peruana Cayetano Heredia, Lima, Perú
,
Laura Laureano-Adame
3   Food Research Center, Nutreco, Toledo, Spain
,
Alfredo Corujo
3   Food Research Center, Nutreco, Toledo, Spain
,
Isabel Reyes
4   Unidad de investigación pediátrica, Hospital de Emergencias Pediátricas, Lima, Perú
,
Joaquim Ruiz 
2   ISGlobal, Hospital Clinic, Universitat de Barcelona, Barcelona, Spain
,
Theresa J. Ochoa
1   Department of Pediatrics, Instituto de Medicina Tropical “Alexander von Humboldt,” Universidad Peruana Cayetano Heredia, Lima, Perú
5   Center for Infectious Diseases, University of Texas Health Science Center at Houston, Houston, TX, United States
› Author Affiliations Funding J. R. was supported by the I3 program of the Ministerio de Economia y Competitividad, Spain (grant number: CES11/012). ISGlobal is a member of the CERCA Programme, Generalitat de Catalunya.
Further Information

Publication History

17 July 2018

07 March 2019

Publication Date:
20 April 2019 (online)

   Permissions and Reprints

Abstract

Gastroenteritis in children is a serious condition in many parts of the world. Salmonella enterica is one of the causes of the disease. In this study, 280 fecal samples from children with diarrhea in four hospitals in Lima, Peru, were collected between September 2012 and March 2013. Salmonella was detected in 26 of the samples. Serotyping demonstrated that 25 of the isolates were S. enterica Infantis, and one isolate was S. enterica Typhimurium. Repetitive extragenic palindromic–polymerase chain reaction analysis suggests that all S. Infantis belong to the same clone. All but one of the S. Infantis isolates exhibited an extended-spectrum β-lactamase phenotype as they harbored bla CTX-M 65. Two strains also carried bla TEM-1. Nine of the isolates were resistant to azithromycin and two to ciprofloxacin. This study demonstrates that a multidrug-resistant S. Infantis clone carrying bla CTX-M 65 was circulating among children in Lima, Peru. The development of molecular epidemiology studies in Salmonella-causing diarrhea or other pathologies in Lima and in other areas will be useful to determine the permanence, geographical spread, and clinical implications of this clone.

Keywords

extended-spectrum β-lactamases - Salmonella enterica serovar Infantis - diarrhea
 

  • References

  • 1 Majowicz SE, Musto J, Scallan E. , et al; International Collaboration on Enteric Disease ‘Burden of Illness’ Studies. The global burden of nontyphoidal Salmonella gastroenteritis. Clin Infect Dis 2010; 50 (06) 882-889
    CrossrefPubMedGoogle Scholar
  • 2 Liu L, Oza S, Hogan D. , et al. Global, regional, and national causes of under-5 mortality in 2000-15: an updated systematic analysis with implications for the Sustainable Development Goals. Lancet 2016; 388 (10063): 3027-3035
    CrossrefPubMedGoogle Scholar
  • 3 Tapalski D, Hendriksen RS, Hasman H, Ahrens P, Aarestrup FM. Molecular characterisation of multidrug-resistant Salmonella enterica serovar Typhimurium isolates from Gomel region, Belarus. Clin Microbiol Infect 2007; 13 (10) 1030-1033
    CrossrefPubMedGoogle Scholar
  • 4 Aviv G, Rahav G, Gal-Mor O. Horizontal transfer of the Salmonella enterica Serovar Infantis resistance and virulence plasmid pESI to the gut microbiota of warm-blooded hosts. MBio 2016; 7 (05) e01395-e01416
    PubMedGoogle Scholar
  • 5 Almeida F, Pitondo-Silva A, Oliveira MA, Falcão JP. Molecular epidemiology and virulence markers of Salmonella Infantis isolated over 25 years in São Paulo State, Brazil. Infect Genet Evol 2013; 19: 145-151
    CrossrefPubMedGoogle Scholar
  • 6 Cartelle Gestal M, Zurita J, Paz Y Mino A, Ortega-Paredes D, Alcocer I. Characterization of a small outbreak of Salmonella enterica serovar Infantis that harbour CTX-M-65 in Ecuador. Braz J Infect Dis 2016; 20 (04) 406-407
    CrossrefPubMedGoogle Scholar
  • 7 Hendriksen RS, Vieira AR, Karlsmose S. , et al. Global monitoring of Salmonella Serovar distribution from the world health organization global foodborne infections network country data bank: results of quality assured laboratories from 2001 to 2007. Foodborne Pathog Dis 2011; 8 (08) 887-900
    CrossrefPubMedGoogle Scholar
  • 8 Gonzales Escalante E. Incremento de aislamientos de Salmonella spp. productora de β-lactamasas de espectro extendido en pacientes pediátricos del Instituto Nacional de Salud del Niño. Rev Peru Med Exp Salud Publica 2015; 32 (03) 605-607
    CrossrefPubMedGoogle Scholar
  • 9 Del Pozo L, Silva N, Valencia A. , et al. Estudio de un brote intrahospitalario por Salmonella Typhimurium productora de beta-lactamasa de espectro extendido SHV-5. An Fac Med Lima 2006; 67 (04) 318-326
    PubMedGoogle Scholar
  • 10 World Health Organization (WHO) Drug-resistant Salmonella. 2005 Fact sheet No 139. Available at: http://www.who.int/mediacentre/factsheets/fs139/en/
    PubMed
  • 11 Tipper DJ, Strominger JL. Mechanism of action of penicillins: a proposal based on their structural similarity to acyl-D-alanyl-D-alanine. Proc Natl Acad Sci U S A 1965; 54 (04) 1133-1141
    CrossrefPubMedGoogle Scholar
  • 12 Cantón R, González-Alba JM, Galán JC. CTX-M enzymes: origin and diffusion. Front Microbiol 2012; 3: 110
    PubMedGoogle Scholar
  • 13 Mikoleit M. Biochemical identification of Salmonella and Shigella using an abbreviated panel of tests. WHO Global Foodborne Infections Network. (Protocol Number: 2010GFNLAB001) Enteric Diseases Laboratory Branch Centers for Disease Control and Prevention Atlanta, GA USA; 2015
    PubMed
  • 14 Pusterla N, Byrne BA, Hodzic E, Mapes S, Jang SS, Magdesian KG. Use of quantitative real-time PCR for the detection of Salmonella spp. in fecal samples from horses at a veterinary teaching hospital. Vet J 2010; 186 (02) 252-255
    CrossrefPubMedGoogle Scholar
  • 15 Clinical and Laboratory Standards Institute (CLSI) Performance Standards for Antimicrobial Susceptibility Testing; Twenty-seven Informational Supplement. 2017 CLSI Document M100-S27Wayne PA: Clinical and Laboratory Standards Institute. Available at: http://file.qums.ac.ir/repository/mmrc/clsi%202017.pdf
    PubMed
  • 16 Bauer AW, Kirby WM, Sherris JC, Turck M. Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol 1966; 45 (04) 493-496
    CrossrefPubMedGoogle Scholar
  • 17 Jarlier V, Nicolas MH, Fournier G, Philippon A. Extended broad-spectrum β-lactamases conferring transferable resistance to newer β-lactam agents in Enterobacteriaceae: hospital prevalence and susceptibility patterns. Rev Infect Dis 1988; 10 (04) 867-878
    CrossrefPubMedGoogle Scholar
  • 18 Belaaouaj A, Lapoumeroulie C, Caniça MM. , et al. Nucleotide sequences of the genes coding for the TEM-like -lactamases IRT-1 and IRT-2 (formerly called TRI-1 and TRI-2). FEMS Microbiol 1994; 120 (1–2): 75-80
    PubMedGoogle Scholar
  • 19 Pitout JD, Thomson KS, Hanson ND, Ehrhardt AF, Moland ES, Sanders CC. β-Lactamases responsible for resistance to expanded-spectrum cephalosporins in Klebsiella pneumoniae, Escherichia coli, and Proteus mirabilis isolates recovered in South Africa. Antimicrob Agents Chemother 1998; 42 (06) 1350-1354
    CrossrefPubMedGoogle Scholar
  • 20 Batchelor M, Hopkins KL, Threlfall EJ. , et al. Characterization of AmpC-mediated resistance in clinical Salmonella isolates recovered from humans during the period 1992 to 2003 in England and Wales. J Clin Microbiol 2005; 43 (05) 2261-2265
    CrossrefPubMedGoogle Scholar
  • 21 Jouini A, Vinué L, Slama KB. , et al. Characterization of CTX-M and SHV extended-spectrum beta-lactamases and associated resistance genes in Escherichia coli strains of food samples in Tunisia. J Antimicrob Chemother 2007; 60 (05) 1137-1141
    CrossrefPubMedGoogle Scholar
  • 22 Palma N, Pons MJ, Gomes C. , et al. Resistance to quinolones, cephalosporins and macrolides in Escherichia coli causing bacteraemia in Peruvian children. J Glob Antimicrob Resist 2017; 11: 28-33
    CrossrefPubMedGoogle Scholar
  • 23 Vila J, Marcos MA, Jimenez de Anta MT. A comparative study of different PCR-based DNA fingerprinting techniques for typing of the Acinetobacter calcoaceticus-A. baumannii complex. J Med Microbiol 1996; 44 (06) 482-489
    CrossrefPubMedGoogle Scholar
  • 24 Zamudio ML, Meza A, Bailón H, Martinez-Urtaza J, Campos J. Experiencias en la vigilancia epidemiológica de agentes patógenos transmitidos por alimentos a través de electroforesis en campo pulsado (PFGE) en el Perú. Rev Peru Med Exp Salud Publica 2011; 28 (01) 128-135
    CrossrefPubMedGoogle Scholar
  • 25 Miller T, Prager R, Rabsch W, Fehlhaber K, Voss M. Epidemiological relationship between Salmonella Infantis isolates of human and broiler origin. Lohmann Inf 2010; 45 (02) 27-31
    PubMedGoogle Scholar
  • 26 Di Conza JA, Mollerach ME, Gutkind GO, Ayala JA. Dos aislamientos de Salmonella infantis multirresistentes se comportan como hipoinvasivos pero con elevada proliferación intracelular. Rev Argent Microbiol 2012; 44 (02) 69-74
    PubMedGoogle Scholar
  • 27 Merino L, Ruiz J, Alonso J, Via J. . Resistencia antimicrobiana y epidemiología molecular en cepas de Salmonella enterica serovar Enteritidis aisladas en las provincias de Chaco y Corrientes (Argentina). Comunicaciones científicas y tecnológicas. Universidad Nacional del Nordeste Resumen; 2005 :M-020
    PubMed
  • 28 Hohmann EL. Nontyphoidal salmonellosis. Clin Infect Dis 2001; 32 (02) 263-269
    CrossrefPubMedGoogle Scholar
  • 29 Silva C, Betancor L, García C. , et al; SalmoIber CYTED Network. Characterization of Salmonella enterica isolates causing bacteremia in Lima, Peru, using multiple typing methods. PLoS One 2017; 12 (12) e0189946
    CrossrefPubMedGoogle Scholar
  • 30 García C. Resistencia antibiótica en el Perú y América Latina. Acta Méd Peruana 2012; 29 (02) 99-103
    PubMedGoogle Scholar
  • 31 Ruiz J. Mechanisms of resistance to quinolones: target alterations, decreased accumulation and DNA gyrase protection. J Antimicrob Chemother 2003; 51 (05) 1109-1117
    CrossrefPubMedGoogle Scholar
  • 32 Ruiz J, Castro D, Goñi P, Santamaria JA, Borrego JJ, Vila J. Analysis of the mechanism of quinolone resistance in nalidixic acid-resistant clinical isolates of Salmonella serotype Typhimurium. J Med Microbiol 1997; 46 (07) 623-628
    CrossrefPubMedGoogle Scholar
  • 33 Malorny B, Schroeter A, Guerra B, Helmuth R. Incidence of quinolone resistance in strains of Salmonella isolated from poultry, cattle and pigs in Germany between 1998 and 2001. Vet Rec 2003; 153 (21) 643-648
    CrossrefPubMedGoogle Scholar
  • 34 Fàbrega A, Soto SM, Ballesté-Delpierre C, Fernández-Orth D, Jiménez de Anta MT, Vila J. Impact of quinolone-resistance acquisition on biofilm production and fitness in Salmonella enterica . J Antimicrob Chemother 2014; 69 (07) 1815-1824
    CrossrefPubMedGoogle Scholar
  • 35 Le Hello S, Bekhit A, Granier SA. , et al. The global establishment of a highly-fluoroquinolone resistant Salmonella enterica serotype Kentucky ST198 strain. Front Microbiol 2013; 4: 395
    PubMedGoogle Scholar
  • 36 Rossolini GM, D'Andrea MM, Mugnaioli C. The spread of CTX-M-type extended-spectrum beta-lactamases. Clin Microbiol Infect 2008; 14 (Suppl. 01) 33-41
    CrossrefPubMedGoogle Scholar
  • 37 Pallecchi L, Malossi M, Mantella A. , et al. Detection of CTX-M-type beta-lactamase genes in fecal Escherichia coli isolates from healthy children in Bolivia and Peru. Antimicrob Agents Chemother 2004; 48 (12) 4556-4561
    CrossrefPubMedGoogle Scholar
  • 38 Pallecchi L, Bartoloni A, Fiorelli C. , 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 (08) 2720-2725
    CrossrefPubMedGoogle Scholar
  • 39 Colquechagua Aliaga F, Sevilla Andrade C, Gonzales Escalante E. Enterobacterias productoras de betalactamasas de espectro extendido en muestras fecales en el Instituto Nacional de Salud del Niño, Perú. Rev Peru Med Exp Salud Publica 2015; 32 (01) 26-32
    CrossrefPubMedGoogle Scholar
  • 40 Riccobono E, Di Pilato V, Di Maggio T. , et al. Characterization of IncI1 sequence type 71 epidemic plasmid lineage responsible for the recent dissemination of CTX-M-65 extended-spectrum β-lactamase in the Bolivian Chaco region. Antimicrob Agents Chemother 2015; 59 (09) 5340-5347
    CrossrefPubMedGoogle Scholar