Skip to main content
Log in

Characterization of antimicrobial resistance in Salmonella enterica strains isolated from Brazilian poultry production

  • Original Paper
  • Published:
Antonie van Leeuwenhoek Aims and scope Submit manuscript

Abstract

Antimicrobial resistance profiles and presence of resistance determinants and integrons were evaluated in Salmonella enterica strains from Brazilian poultry. The analysis of 203 isolates showed that those from the poultry environment (88 isolates) were significantly more resistant to antimicrobials than isolates from other sources, particularly those isolated from poultry by-product meal (106 isolates). Thirty-seven isolates were resistant to at least three antimicrobial classes. Class 1 integrons were detected in 26 isolates, and the analysis of the variable region between the 5′ conserved segment (CS) and 3′ CS of each class 1 integron-positive isolate showed that 13 contained a typical 3′ CS and 14 contained an atypical 3′ CS. One Salmonella Senftenberg isolate harbored two class 1 integrons, showing both typical and atypical 3′ CSs. The highest percentage of resistance was found to sulfonamides, and sul genes were detected in the majority of the resistant isolates. Aminoglycoside resistance was detected in 50 isolates, and aadA and aadB were present in 28 and 32 isolates, respectively. In addition, strA and strB were detected in 78.1 and 65.6 % isolates resistant to streptomycin, respectively. Twenty-one isolates presented reduced susceptibility to β-lactams and harbored bla TEM, bla CMY, and/or bla CTX-M. Forty isolates showed reduced susceptibility to tetracycline, and most presented tet genes. These results highlight the importance of the environment as a reservoir of resistant Salmonella, which may enable the persistence of resistance determinants in the poultry production chain, contributing, therefore, to the debate regarding the impacts that antimicrobial use in animal production may exert in human health.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Aarestrup FM, Lertworapreecha M, Evans MC, Bangtrakulnonth A, Chalermchaikit T, Hendriksen RS, Wegener HC (2003) Antimicrobial susceptibility and occurrence of resistance genes among Salmonella enterica serovar Weltevreden from different countries. J Antimicrob Chemother 52:715–718

    Article  CAS  PubMed  Google Scholar 

  • ABEF (2011) Relatório anual. http://www.ubabef.com.br/publicacoes. Accessed June 2014

  • Anjum MF, Choudhary S, Morrison V, Snow LC, Mafura M, Slickers P, Ehricht R, Woodward MJ (2011) Identifying antimicrobial resistance genes of human clinical relevance within Salmonella isolated from food animals in Great Britain. J Antimicrob Chemother 66:550–559

    Article  CAS  PubMed  Google Scholar 

  • Antunes P, Machado J, Sousa JC, Peixe L (2005) Dissemination of sulfonamide resistance genes (sul1, sul2, and sul3) in Portuguese Salmonella enterica strains and relation with integrons. Antimicrob Agents Chemother 49:836–839

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bush K, Jacoby GA (2010) Updated functional classification of beta-lactamases. Antimicrob Agents Chemother 54:969–976

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Campioni F, Zoldan MM, Falcão JP (2014) Characterization of Salmonella enteritidis strains isolated from poultry and farm environments in Brazil. Epidemiol Infect 142:1403–1410

    Article  CAS  PubMed  Google Scholar 

  • Carlson SA, Bolton LF, Briggs CE, Hurd HS, Sharma VK, Fedorka-Cray PJ, Jones BD (1999) Detection of multiresistant Salmonella typhimurium DT104 using multiplex and fluorogenic PCR. Mol Cell Probes 13:213–222

    Article  CAS  PubMed  Google Scholar 

  • CDC (2013) National Center for Emerging and Zoonotic Infectious Diseases. http://www.cdc.gov/salmonella/general/diagnosis.html. Accessed June 2014

  • Chuanchuen R, Padungtod P (2009) Antimicrobial resistance genes in Salmonella enterica isolates from poultry and swine in Thailand. J Vet Med Sci 71:1349–1355

    Article  CAS  PubMed  Google Scholar 

  • Chuanchuen R, Koowatananukul C, Khemtong S (2008a) Characterization of class 1 integrons with unusual 3′ conserved region from Salmonella enterica isolates. Southeast Asian J Trop Med Public Health 39:419–424

    CAS  PubMed  Google Scholar 

  • Chuanchuen R, Pathanasophon P, Khemtong S, Wannaprasat W, Padungtod P (2008b) Susceptibilities to antimicrobials and disinfectants in Salmonella isolates obtained from poultry and swine in Thailand. J Vet Med Sci 70:595–601

    Article  PubMed  Google Scholar 

  • CLSI (2008) Performance standards for antimicrobial disk and dilution susceptibility test for bacteria isolate from animals. Approved Standard CLSI Documents M31-A3. CLSI, Wayne, PA

  • CLSI (2013) Performance standards for antimicrobial susceptibility testing; 23nd Informational Supplement. Approved Standard CLSI Documents M100-S23. CLSI, Wayne, PA

  • Collignon P, Powers JH, Chiller TM, Aidara-kane A, Aarestrup FM (2009) World health organization ranking of antimicrobials according to their importance in human medicine: a critical step for developing risk management strategies for the use of antimicrobial in food production animals. Clin Infect Dis 49:132–141

    Article  CAS  PubMed  Google Scholar 

  • Costa RG, Festivo ML, Araujo MS, Reis EMF, Lázaro NS, Rodrigues DP (2013) Antimicrobial susceptibility and serovars of Salmonella circulating in commercial poultry carcasses and poultry products in Brazil. J Food Prot 76:2011–2017

    Article  CAS  PubMed  Google Scholar 

  • Dionisi AM, Lucarelli C, Benedetti I, Owczarek S, Luzzi I (2011) Molecular characterization of multidrug-resistant Salmonella enterica serotype Infantis from humans, animals and the environment in Italy. Int J Antimicrob Agents 38:384–389

    Article  CAS  PubMed  Google Scholar 

  • Edelstein M, Pimkin M, Palagin I, Edelstein I, Stratchounski L (2003) Prevalence and molecular epidemiology of CTX-M extended-spectrum β-lactamase-producing Escherichia coli and Klebsiella pneumonia in Russian hospitals. Antimicrob Agents Chemother 47:3724–3732

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Firoozeh F, Zahraei-Salehi T, Shahcheraghi F, Karimi V, Aslani MM (2012) Characterization of class I integrons among Salmonella enterica serovar Enteritidis isolated from humans and poultry. FEMS Immunol Med Microbiol 64:237–243

    Article  CAS  PubMed  Google Scholar 

  • Frana TS, Carlson SA, Griffith RW (2001) Relative distribution and conservation of genes encoding aminoglycoside-modifying enzymes in Salmonella enterica serotype Typhimurium phage type DT104. Appl Environ Microbiol 67:445–448

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Frye JG, Jackson CR (2013) Genetic mechanisms of antimicrobial resistance identified in Salmonella enterica, Escherichia coli, and Enterococcus spp. isolated from U.S. food animals. Front Microbiol 4:135

    Article  PubMed Central  PubMed  Google Scholar 

  • Ge B, LaFon PC, Carter PJ, McDermott SD, Abbott J, Glenn A, Ayers SL, Friedman SL, Paige JC, Wagner DD, Zhao S, McDermott PF, Rasmussen MA (2013) Retrospective analysis of Salmonella, Campylobacter, Escherichia coli, and Enterococcus in animal feed ingredients. Foodborne Pathog Dis 10:684–691

    Article  CAS  PubMed  Google Scholar 

  • Gebreyes WA, Thakur S (2005) Multidrug-resistant Salmonella enterica serovar Muenchen from pigs and humans and potential interserovar transfer of antimicrobial resistance. Antimicrob Agents Chemother 49:503–511

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Glenn LM, Lindsey RL, Folster JP, Pecic G, Boerlin P, Gilmour MW, Harbottle H, Zhao S, McDermott PF, Fedorka-Cray PJ, Frye JG (2013) Antimicrobial resistance genes in multidrug-resistant Salmonella enterica isolated from animals, retail meats, and humans in the United States and Canada. Microb Drug Resist 19:175–184

    Article  CAS  PubMed  Google Scholar 

  • Grape M, Sundström L, Kronvall G (2003) Sulphonamide resistance gene sul3 found in Escherichia coli isolates from human sources. J Antimicrob Chemother 52:1022–1024

    Article  CAS  PubMed  Google Scholar 

  • Han J, Lynne AM, David DE, Tang H, Xu J, Nayak R, Kaldhone P, Logue CM, Foley SL (2012) DNA sequence analysis of plasmids from multidrug resistant Salmonella enterica serotype Heidelberg isolates. PLoS ONE 7:1–8

    Google Scholar 

  • Hofacre CL, White DG, Maurer JJ, Morales C, Lobsinger C, Hudson C (2001) Characterization of antibiotic-resistant bacteria in rendered animal products. Avian Dis 45:953–961

    Article  CAS  PubMed  Google Scholar 

  • Hur J, Kim JH, Park JH, Lee YJ, Lee JH (2011) Molecular and virulence characteristics of multi-drug resistant Salmonella Enteritidis strains isolated from poultry. Vet J 189:306–311

    Article  PubMed  Google Scholar 

  • Jana S, Deb JK (2006) Molecular understanding of aminoglycoside action and resistance. Appl Microbiol Biotechnol 70:140–150

  • Jong A, Smet A, Ludwig C, Stephan B, Graef E, Vanrobaeys M, Haesebrouck F (2014) Antimicrobial susceptibility of Salmonella isolates from healthy pigs and chickens (2008–2011). Vet Microbiol 171:298–306

    Article  PubMed  Google Scholar 

  • Kempf I, Roux AL, Perrin-Guvomard A, Mourand G, Devendec LL, Bougeard S, Richez P, Pottier GL, Etarradossi N (2013) Effect of in-feed paromomycin supplementation on antimicrobial resistance of enteric bacteria in turkeys. Vet J 198:398–403

    Article  CAS  PubMed  Google Scholar 

  • Kerrn MB, Klemmensen T, Frimodt-Moller N, Espersen F (2001) Susceptibility of Danish Escherichia coli strains isolated from urinary tract infections and bacteraemia, and distribution of sul genes conferring sulphonamide resistance. J Antimicrob Chemother 50:513–516

    Article  Google Scholar 

  • Kim S, Kim SH, Kim J, Shin JH, Lee BK, Park MS (2011) Occurrence and distribution of various genetic structures of class 1 and class 2 integrons in Salmonella enterica isolates from foodborne disease patients in Korea for 16 years. Foodborne Pathog Dis 8:319–324

    Article  CAS  PubMed  Google Scholar 

  • Laanen M, Persoons D, Ribbens S, Jong E, Callens B, Strubbe M, Maes D, Dewulf J (2013) Relationship between biosecurity and production/antimicrobial treatment characteristics in pig herds. Vet J 198:508–512

    Article  CAS  PubMed  Google Scholar 

  • Lee MF, Chen YH, Peng CF (2009) Molecular characterization of class 1 integrons in Salmonella enterica serovar Choleraesuis isolates from southern Taiwan. Int J Antimicrob Agents 33:219–222

    Google Scholar 

  • Li X, Bethune LA, Jia Y, Lovell RA, Proescholdt TA, Benz SA, Schell TC, Kaplan G, McChesney DG (2012) Surveillance of Salmonella prevalence in animal feeds and characterization of the Salmonella isolates by serotyping and antimicrobial susceptibility. Foodborne Pathog Dis 9:692–698

    Article  CAS  PubMed  Google Scholar 

  • Machado E, Coque TM, Cantón R, Sousa JC, Peixe L (2013) Commensal Enterobacteriaceae as reservoirs of extended-spectrum beta-lactamases, integrons, and sul genes in Portugal. Front Microbiol 4:1–7

    Article  CAS  Google Scholar 

  • Madsen L, Aarestrup FM, Olsen JE (2000) Characterisation of streptomycin resistance determinants in Danish isolates of Salmonella Typhimurium. Vet Microbiol 75:73–82

    Article  CAS  PubMed  Google Scholar 

  • MAPA (1998) Circular DFPA N° 047/98. http://www.agricultura.gov.br. Accessed June 2014

  • MAPA (2003) Instrução Normativa n° 09. http://www.agricultura.gov.br. Accessed June 2014

  • MAPA (2009) Instrução Normativa n° 26. http://www.agricultura.gov.br. Accessed June 2014

  • MAPA (2012) Instrução Normativa n° 14. http://www.agricultura.gov.br. Accessed June 2014

  • Mohd-Zain Z, Kamsani NH, Ahmad N (2013) Molecular insights of co-trimoxazol resistance genes in Haemophilus influenzae isolated in Malaysia. Trop Biomed 30:584–590

    CAS  PubMed  Google Scholar 

  • Molbak K (2005) Human health consequences of antimicrobial drug-resistant Salmonella and other foodborne pathogens. Clin Infect Dis 41:1613–1620

    Article  PubMed  Google Scholar 

  • Oliveira SD, Santos LR, Schuch DMT, Silva AB, Salle CTP, Canal CW (2002) Detection and identification of salmonellas from poultry-related samples by PCR. Vet Microbiol 87:25–35

    Article  CAS  PubMed  Google Scholar 

  • Oliveira SD, Flores FS, Santos LR, Brandelli A (2005) Antimicrobial resistance in Salmonella enteritidis strains isolated from broiler carcasses, food, human and poultry-related samples. Int J Food Microbiol 97:297–305

    Article  Google Scholar 

  • Rademaker JLW, de Bruijin FJ (1997) Characterization and classification of microbes by REP-PCR genomic fingerprinting and computer-assisted pattern analysis. In: Caetano-Anolles G, Gresshoff PM (eds) DNA markers: protocols, applications, and overviews. Wiley-VCH, New York, pp 151–171

    Google Scholar 

  • Rodríguez I, Martín MC, Mendoza MC, Rodicio MR (2006) Class 1 and class 2 integrons in non-prevalent serovars of Salmonella enterica: structure and association with transposons and plasmids. J Antimicrob Chemother 58:1124–1132

    Article  PubMed  Google Scholar 

  • Sapkota AR, Lefferts LY, McKenzie S, Walker P (2007) What do we feed to food-production animals? A review of animal feed ingredients and their potential impacts on human health. Environ Health Perspect 115:663–670

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sapkota AR, Kinney EL, George A, Hulet RM, Cruz-Cano R, Schwab KJ, Zhang G, Joseph SW (2014) Lower prevalence of antibiotic-resistant Salmonella on large-scale U.S. conventional poultry farms that transitioned to organic practices. Sci Total Environ 476–477:387–392

    Article  PubMed  Google Scholar 

  • Schwarz S, Kehrenberg C, Walsh TR (2001) Use of antimicrobial agents in veterinary medicine and food animal production. Int J Antimicrob Agents 17:431–437

    Article  CAS  PubMed  Google Scholar 

  • Skold O (2001) Resistance to trimethoprim and sulfonamides. Vet Res 32:261–273

    Article  CAS  PubMed  Google Scholar 

  • Su J, Shi L, Yang L, Xiao Z, Li X, Yamasaki S (2006) Analysis of integrons in clinical isolates of Escherichia coli in China during the last six years. FEMS Microbiol Lett 254:75–80

    Article  CAS  PubMed  Google Scholar 

  • Van TTH, Nguyen HNK, Smooker PM, Coloe PJ (2012) The antibiotic resistance characteristics of non-typhoidal Salmonella enterica isolated from food-producing animals, retail meat and humans in South East Asia. Int J Food Microbiol 154:98–106

    Article  CAS  PubMed  Google Scholar 

  • Wannaprasat W, Padungtod P, Chuanchuen R (2011) Class 1 integrons and virulence genes in Salmonella enterica isolates from pork and humans. Int J Antimicrob Agents 37:457–461

    Article  CAS  PubMed  Google Scholar 

  • White PA, McIver CJ, Deng YM, Rawlinson WD (2000) Characterization of two new gene cassettes, aadA5 and dfrA17. FEMS Microbiol Lett 182:265–269

    Article  CAS  PubMed  Google Scholar 

  • White PA, McIver CJ, Rawlinson WD (2001) Integrons and gene cassettes in the Enterobacteriaceae. Antimicrob Agents Chemother 45:2658–2661

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • WHO (2013) Salmonella (non-typhoidal). http://www.who.int/mediacentre/factsheets/fs139/en. Accessed June 2014

  • Winokur PL, Vonstein DL, Hoffman LJ, Uhlenhopp EK (2001) Evidence for transfer of CMY-2 AmpC β-lactamase plasmids between Escherichia coli and Salmonella isolates from food animals and humans. Antimicrob Agents Chemother 45:2716–2722

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yau S, Liu X, Djordjevic SP, Hall RM (2010) RSF1010-like plasmids in australian Salmonella enterica serovar Typhimurium and origin of their sul2-strA-strB antibiotic resistance gene cluster. Microb Drug Resist 16:249–252

    Article  CAS  PubMed  Google Scholar 

  • Yu CY, Chou SJ, Yeh CM, Chao M-R, Huang KC, Chang YF, Chiou CS, Weill FX, Chiu CH, Chu CH, Chu C (2008) Prevalence and characterization of multidrug-resistant (Type ACSSuT) Salmonella enterica serovar Typhimurium strains in isolates from four gosling farms and a hatchery farm. J Clin Microbiol 46:522–526

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors thank the Laboratório Porto Belo for supplying the majority of the Salmonella spp. used in this study. S. P. Mattiello received a scholarship from Probolsas/PUCRS.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sílvia D. Oliveira.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mattiello, S.P., Drescher, G., Barth, V.C. et al. Characterization of antimicrobial resistance in Salmonella enterica strains isolated from Brazilian poultry production. Antonie van Leeuwenhoek 108, 1227–1238 (2015). https://doi.org/10.1007/s10482-015-0577-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10482-015-0577-1

Keywords

Navigation