Sobrevivência de Salmonella enterica às condições gástricas simuladas in vitro: papel dos fatores de adesão e resistência antibacteriana

Autores

  • Jhennifer Arruda Schmiedt Universidade Federal do Paraná
  • Emanoelli Aparecida Rodrigues dos Santos Universidade Estadual Paulista https://orcid.org/0000-0001-6011-3232
  • Leonardo Ereno Tadielo Universidade Estadual Paulista
  • Tatiane Barbosa Coitinho Universidade Federal do Paraná
  • Carolina Dias Rodrigues Universidade Federal do Paraná
  • Luiz Gustavo Bach Universidade Federal do Paraná https://orcid.org/0000-0002-0913-8538
  • Taís Luana Pinto Universidade Federal do Paraná
  • Juliano Gonçalves Pereira Universidade Estadual Paulista
  • Vanessa Mendonça Soares Universidade Estadual Paulista
  • Thiago Henrique Bellé Universidade Federal do Paraná https://orcid.org/0000-0002-9462-6666
  • Vinicius Cunha Barcellos Universidade Federal do Paraná https://orcid.org/0000-0002-9404-3460
  • Luciano dos Santos Bersot Universidade Federal do Paraná https://orcid.org/0000-0001-7013-5574

DOI:

https://doi.org/10.18593/evid.32846

Palavras-chave:

Microrganismos resistentes, Beta-lactamases, Biofilme, Tolerância gastrointestinal, Cortes cárneos, Frango de corte

Resumo

O estudo tem como objetivo verificar a capacidade de adesão e formação de biofilme de isolados de Salmonella spp. produtores de enzimas beta-lactamases de espectro estendido (ESBL), bem como a resistência de isolados produtores ou não de ESBL, frente às condições gástricas e intestinais simuladas in vitro. Foram utilizados 18 isolados de Salmonella spp. obtidos de cortes de frangos congelados produzidos no Estado do Paraná, Brasil. Os isolados produtores de ESBL foram avaliados de forma fenotípica e genotípica quanto a capacidade de adesão e formação de biofilme em lâminas de polipropileno. Além disso, todos os isolados foram submetidos a avaliação in vitro de resistência às condições gástricas e intestinais e após as simulações, realizadas contagens das células sobreviventes. Com relação à adesão e formação de biofilme, 13 isolados apresentaram essa capacidade. Quanto a tolerância às condições gástricas e intestinais, a quantificação de Salmonella spp. diminuiu (p<0,05) conforme a passagem do trato gastrointestinal. Em relação a comparação de isolados produtores e não produtores de ESBL, não houve diferença (p>0,05) na taxa de sobrevivência total. Os resultados demonstram que, apesar da diminuição da contagem de microrganismos conforme a passagem simulada pelos sucos gástricos e intestinais, a taxa de sobrevivência média total dos isolados de Salmonella spp. foi alta, o que permite inferir que os isolados possuem a capacidade de sobreviver às condições gastrointestinais simuladas, e ainda sim permaneceram em número capaz de causar infecção.

Downloads

Não há dados estatísticos.

Referências

Majowicz SE, Musto J, Scallan E, Angulo FJ, Kirk M, O'Brien SJ, et al. The global burden of nontyphoidal Salmonella gastroenteritis. Clin Infect Dis. 2010;50(6):882-89.

Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson MA, Roy SL, et al. Foodborne illness acquired in the United States – major pathogens. Emerging Infect Dis. 2011;17(1):7.

EFSA and ECDC – European Food Safety Authority and European Centre for Disease Prevention and Control. The European Union One Health 2018 Zoonoses Report. EFSA Journal. 2019;17(12):e05926.

Brasil. Ministério da Saúde. Secretaria de Vigilância em Saúde. Departamento de Vigilância das Doenças Transmissíveis. Coordenação Geral de Doenças Transmissíveis. Surtos de doenças transmitidas por alimentos no Brasil: informe 2018. Brasília: Ministério da Saúde; 2019. [citado em 2023 Jun 5]. Disponível em: https://portalarquivos2.saude.gov.br/images/pdf/2019/fevereiro/15/Apresenta----o-Surtos-DTA--Fevereiro-2019.pdf

Coburn B, Grassl GA, Finlay BB. Salmonella, the host and disease: a brief review. Immunol Cell Biol. 2007;85(2):112-18.

Chen HM, Wang Y, Su LH, Chiu CH. Nontyphoid Salmonella infection: microbiology, clinical features, and antimicrobial therapy. Pediatr Neonatol. 2013;54(3):147-52.

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

Nadi ZR, Salehi TZ, Tamai IA, Sillanpaa M, Dallal MMS. Evaluation of antibiotic resistance and prevalence of common Salmonella enterica serovars isolated from foodborne outbreaks. Microchem Journal. 2020;155:104660.

Wang H, Ye K, Wei X, Cao J, Xu X, Zhou G. Occurrence, antimicrobial resistance and biofilm formation of Salmonella isolates from a chicken slaughter plant in China. Food Control. 2013;33(2):378-84.

Dar MA, Ahmad SM, Bhat SA, Ahmed R, Urwat U, Mumtaz PT, et al. Salmonella Typhimurium in poultry: a review. Worlds Poult Sci J. 2017;73(2):345-54.

Voss-Rech D, Kramer B, Silva VS, Rebelatto R, Abreu PG, Coldebella A, et al. Longitudinal study reveals persistent environmental Salmonella Heidelberg in Brazilian broiler farms. Vet Microbiol. 2019; 233:118-23.

Kottwitz LBM, Oliveira TCRM, Alcocer I, Farah SMSS, Abrahão WSM, Rodrigues DP. Avaliação epidemiológica de surtos de salmonelose ocorridos no período de 1999 a 2008 no Estado do Paraná, Brasil. Acta Sci Health Sci. 2010;32:9-15.

Mendonça, EP. Características de virulência, resistência e diversidade genética de sorovares de Salmonella com impacto na saúde pública, isolados de frangos de corte no Brasil [tese de Doutorado]. Uberlândia: Universidade Federal de Uberlândia; 2016. 131 p.

Perin AP, Martins BTF, Barreiros MAB, Yamatogi RS, Nero LA, Bersot LS. Occurrence, quantification, pulse types, and antimicrobial susceptibility of Salmonella sp. isolated from chicken meat in the state of Paraná, Brazil. Braz J Microbiol. 2019;51(1):335-45.

Lejeune P. Biofilms – Dependent Regulation of Gene Expression. In: Wilson M, Devine D, organizators. Medical Implications of Biofilms. Cambridge: Cambridge University Press; 2003. p. 3-17.

Oliveira DCV. Produção de biofilme por Salmonella sp. isolada de frango [dissertação de mestrado]. Botucatu: Instituto de Biociências de Botucatu, Universidade Estadual Paulista; 2011. 75 p.

Carattoli A. Plasmids and the spread of resistance. Int J Med Microbiol. 2013;303(6-7):298-304.

Sirsat SA, Burkholder KM, Muthaiyan A, Dowd SE, Bhunia AK, Ricke SC. Effect of sublethal heat stress on Salmonella Typhimurium virulence. J Appl Microbiol. 2011;110(3):813-22.

Smith JL. The role of gastric acid in preventing foodborne disease and how bacteria overcome acid conditions. J Food Prot. 2003;66(7):1292-1303.

Berk PA, De Jonge R, Zwietering MH, Abee T, Kieboom, J. Acid resistance variability among isolates of Salmonella enterica serovar Typhimurium DT104. J Appl Microbiol. 2005;99(4):859-866.

Howden CW, Hunt RH. Relationship between gastric secretion and infection. Gut. 1987;28(1):96.

McDonald SW, MacFarlane NG. The mouth, stomach and intestines. Anaesth Intensive Care Med. 2018;19(3):128-32.

Crum-Cianflone NF. Salmonellosis and the gastrointestinal tract: more than just peanut butter. Curr Gastroenterol Rep. 2008;10(4):424-31.

Tadielo LE, Bellé TH, Santos EAR, Schmiedt JA, Cerqueira-Cézar CK, Nero LA, et al. Pure and mixed biofilms formation of Listeria monocytogenes and Salmonella Typhimurium on polypropylene surfaces. LWT – Food Sci and Technol. 2022;162:113469.

Poimenidou SV, Chrysadakou M, Tzakoniati A, Bikouli VC, Nychas GJ, Skandamis PN. Variability of Listeria monocytogenes strains in biofilm formation on stainless steel and polystyrene materials and resistance to peracetic acid and quaternary ammonium compounds. Int J Food Microbiol. 2016;237:164-71.

Dias RC, Santos BC, Santos LF, Vieira MA, Yamatogi, RS, Mondelli AL, et al. Diarrheagenic Escherichia coli pathotypes investigation revealed atypical enteropathogenic E. coli as putative emerging diarrheal agents in children living in Botucatu, São Paulo State, Brazil. APMIS. 2016;124(4):299–308.

Oliveira DCV, Fernandes Júnior A, Kaneno R, Silva MG, Araújo Júnior JP, Silva NCC, et al. Ability of Salmonella spp. to Produce Biofilm Is Dependent on Temperature and Surface Material. Foodborne Pathog Dis. 2014;11(6):478-83.

Bäumler AJ, Heffron F. Identification and sequence analysis of lpfABCDE, a putative fimbrial operon of Salmonella Typhimurium. J. Bacteriol. 1995;177(8):2087-97.

Collinson SK, Emody L, Trust TJ, Kay WW. Thin aggregative fimbriae from diarrheagenic Escherichia coli. J. Bacteriol. 1992;174(13):4490-95.

Halatsi K, Oikonomou I, Lambiri M, Mandilara G, Vatopoulos A, Kyriacou A. PCR detection of Salmonella spp. using primers targeting the quorum sensing gene sdiA. FEMS Microbiol Lett. 2006;259(2):201-07.

Skyberg JA, Logue CM, Nolan LK. Virulence genotyping of Salmonella spp. with multiplex PCR. Avian Dis. 2006;50(1):77-81.

Santos KMO, Vieira ADS, Buriti FCA, Nascimento JCF, Melo MES, Bruno LM, et al. Artisanal coalho cheeses as source of beneficial Lactobacillus plantarum and Lactobacillus rhamnosus strains. Dairy Sci Technol. 2015;95(2):209-230.

Wang H, Ye K, Wei X, Cao J, Xu X, Zhou G. Occurrence, antimicrobial resistance and biofilm formation of Salmonella isolates from a chicken slaughter plant in China. Food Control. 2013;33(2):378-384.

Barnhart MM, Chapman MR. Curli biogenesis and function. Annu Ver Microbiol. 2006;60:131-47.

Borsoi A, Santin E, Santos LR, Salle CTP, Moraes HLS, Nascimento VP. Inoculation of newly hatched broiler chicks with two Brazilian isolates of Salmonella Heidelberg strains with different virulence gene profiles, antimicrobial resistance, and pulsed field gel electrophoresis patterns to intestinal changes evaluation. Poult Sci. 2009;88(4):750-58.

Morente EO, Fernández-Fuentes MA, Burgos MJG, Abriouel H, Pulido RP, Gálvez A. Biocide tolerance in bacteria. Int J Food Microbiol. 2013;162(1),13-25.

Poole K. Efflux pumps as antimicrobial resistance mechanisms. Ann Med. 2007;39(3):162-76.

Jiang X, Yu T, Liang Y, Ji S, Guo X, Ma J, et al. Efflux pump-mediated benzalkonium chloride resistance in Listeria monocytogenes isolated from retail food. Int J Food Microbiol. 2016;217:141-45.

Weston N, Sharma P, Ricci V, Piddock LJV. Regulation of the AcrAB-TolC efflux pump in Enterobacteriaceae. Res Microbiol. 2018;169(7-8):425-31.

Lee SHI, Cappato LP, Corassin CH, Cruz AGD, Oliveira CAFD. Effect of peracetic acid on biofilms formed by Staphylococcus aureus and Listeria monocytogenes isolated from dairy plants. J Dairy Sci. 2016;99(3):2384-90.

Akinbobola AB, Sherry L, Mckay WG, Ramage G, Williams C. Tolerance of Pseudomonas aeruginosa in in-vitro biofilms to high-level peracetic acid disinfection. J Hosp Infec. 2017;97(2):162-68.

Haubert L, Zehetmeyr ML, Pereira YMN, Kroning IS, Maia DSV, Sehn CP, et al. Tolerance to benzalkonium chloride and antimicrobial activity of Butia odorata Barb. Rodr. extract in Salmonella spp. isolates from food and food environments. Food Res Int. 2019;116:652-59.

Bai AJ, Rai VR. Bacterial quorum sensing and food industry. Compr Rev Food Sci Food Saf. 2011;10(3):183-93.

Hiller CC, Lucca V, Carvalho D, Borsoi A, Borges KA, Furian TQ, et al. Influence of catecholamines on biofilm formation by Salmonella Enteritidis. Microb Pathog. 2019;130:54-58.

Cantón R, Ruiz-Garbajosa P. Co-resistance: an opportunity for the bacteria and resistance genes. Curr Opin Pharmacol. 2011;11(5):477-85.

Paul D, Chakraborty R, Mandal SM. Biocides and health-care agents are more than just antibiotics: Inducing cross to co-resistance in microbes. Ecotoxicol Environ Saf. 2019;174:601-10.

Silva N, Carvalho I, Currie C, Sousa M, Igrejas G, Poeta P. Extended‐Spectrum‐β‐Lactamase and Carbapenemase‐Producing Enterobacteriaceae in Food‐Producing Animals in Europe: An Impact on Public Health?. In: Capelo-Martínez JL, Igrejas G, organizators. Antibiotic Drug Resistence. Hoboken: John Wiley & Sons; 2019. p. 261-73.

Poole TL, Callaway TR, Norman KN, Scott HM, Loneragan GH, Ison SA, et al. Transferability of antimicrobial resistance from multidrug-resistant Escherichia coli isolated from cattle in the USA to E. coli and Salmonella Newport recipients. J Glob Antimicrob Resist. 2017;11:123-32.

Harakeh S, Azhar E, Almasaudi S, Kissoyan KB, Fadlallah S, Tanelian A, et al. Effects of a specific nutrient combination on ESBL resistance. Saudi J Biol Sci. 2019;26(7):1576-80.

Kücken D, Feucht HH, Kaulfers PM. Association of qacE and qacE Δ1 with multiple resistance to antibiotics and antiseptics in clinical isolates of Gram-negative bacteria. FEMS Microbiol Lett. 2000;183(1):95-98.

Chapman JS. Biocide resistance mechanisms. Int Biodeterior Biodegrad. 2003;51(2):133-38.

Long M, Lai H, Deng W, Zhou K, Li B, Liu S, et al. Disinfectant susceptibility of different Salmonella serotypes isolated from chicken and egg production chains. J Appl Microbiol. 2016;121(3):672-81.

Shah J, Desai PT, Chen D, Stevens JR, Weimer BC. Preadaptation to cold stress in Salmonella enterica serovar Typhimurium increases survival during subsequent acid stress exposure. Appl Environ Microbiol. 2013;79(23):7281-89.

Álvarez-Ordóñez A, Begley M, Prieto M, Messens W, López M, Bernardo A, et al. Salmonella spp. survival strategies within the host gastrointestinal tract. Microbiol. 2011;157(12):3268-81.

Dykhuizen RS, Frazer R, Duncan C, Smith CC, Golden M, Benjamin N, et al. Antimicrobial effect of acidified nitrite on gut pathogens: importance of dietary nitrate in host defense. Antimicrob Agents Chemother. 1996;40(6):1422-25.

Mikkelsen LL, Naughton PJ, Hedemann MS, Jensen BB. Effects of physical properties of feed on microbial ecology and survival of Salmonella enterica serovar Typhimurium in the pig gastrointestinal tract. Appl Environ Microbiol. 2004;70(6):3485-92.

Melo ANF, Souza GT, Schaffne D, Oliveira TCM, Maciel JF, Souza EL, et al. Changes in thermo-tolerance and survival under simulated gastrointestinal conditions of Salmonella Enteritidis PT4 and Salmonella Typhimurium PT4 in chicken breast meat after exposure to sequential stresses. Int J Food Microbiol. 2017;251:15-23.

Yang Y, Khoo WJ, Zheng Q, Chung HJ, Yuk HG. Growth temperature alters Salmonella Enteritidis heat/acid resistance, membrane lipid composition and stress/virulence related gene expression. Int J Food Microbiol. 2014;172:102-109.

Gunn JS. Mechanisms of bacterial resistance and response to bile. Microbes Infect. 2000;2(8):907-13.

Merritt ME, Donaldson JR. Effect of bile salts on the DNA and membrane integrity of enteric bacteria. J Med Microbiol. 2009;58(12):1533-41.

Pradhan D, Negi VD. Stress-induced adaptations in Salmonella: a ground for shaping its Pathogenesis. Microbiological research. 2019;229:126311.

Van Velkinburgh JC, Gunn JS. PhoP-PhoQ-regulated loci are required for enhanced bile resistance in Salmonella spp. Infect and Immun. 1999;67(4):1614-22.

McKnight, GM, Duncan CW, Liefert C, Golden MH. Dietary nitrate in man: friend or foe?. Br J Nutr. 1999;81:349-58.

Xu J, Xu X, Verstraete W. The bactericidal effect and chemical reactions of acidified nitrite under conditions simulating the stomach. J Appl Microbiol. 2001;90(4):523-529.

Downloads

Publicado

30-11-2023

Como Citar

Schmiedt, J. A., Santos, E. A. R. dos, Tadielo, L. E., Coitinho, T. B., Rodrigues, C. D., Bach, L. G., Pinto, T. L., Pereira, J. G., Soares, V. M., Bellé, T. H., Barcellos, V. C., & Bersot, L. dos S. (2023). Sobrevivência de Salmonella enterica às condições gástricas simuladas in vitro: papel dos fatores de adesão e resistência antibacteriana. Evidência, 23(2), 129–144. https://doi.org/10.18593/evid.32846

Edição

Seção

Biociências