Skip to main content
SpringerLink
Log in

Virulence potential of Salmonella 1,4, [5],12:i:- strains isolated during decades from different sources in the Southeast region of Brazil

  • Clinical Microbiology - Research Paper
  • Published:
Brazilian Journal of Microbiology Aims and scope Submit manuscript

Abstract

Salmonella 1,4, [5],12:i:- is one of the most prevalent serovars associated with gastroenteritis in several countries, including Brazil. However, few studies have analyzed the virulence potential of this variant in this country. Therefore, this study aimed to characterize S. 1,4, [5],12:i:- strains isolated in Southeast Brazil. To this end, 113 S. 1,4, [5],12:i:- strains isolated from different sources between 1983 and 2020 were analyzed. For all strains, the frequencies of 11 virulence genes were investigated using PCR and the molecular typing was performed using pulsed-field gel electrophoresis (PFGE). Furthermore, 40 strains isolated from human and non-human sources were characterized by survival under acid and oxidative stress, and virulence analysis in Galleria mellonella was performed for 20 selected strains. All virulence genes were detected in more than 91% of the strains. The studied strains were grouped into four clusters using PFGE. Most strains were present in one cluster, named PFGE-A, with a genetic similarity of ≥ 79.5%. All 40 strains survived acid stress after 10 min and 1 h of exposure. Under oxidative stress, all 40 strains survived after 10 min, and 36 survived after 1 h of exposure. In the G. mellonella assay, nine isolates from non-human sources and six isolates from human showed high-to-intermediate virulence profiles. In conclusion, the pathogenic potential of the strains studied was corroborated by the high frequency of all the virulence genes identified. The PFGE results suggested that most strains belonged to one main cluster that has been prevailing in the São Paulo State, Brazil. The S. 1,4, [5],12:i:- strains isolated from human and non-human sources successfully survived the unfavorable conditions in the human gastrointestinal tract. Finally, strains isolated from non-human sources showed a higher proportion of isolates with high to intermediate virulence profiles in G. mellonella than in human isolates, suggesting a possible difference between isolates from different origins.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

Data availability

Please contact the authors Giovana do Nascimento Pereira or Juliana Pfrimer Falcão for data requests.

References

  1. World Health Organization (2020) The top 10 causes of death. https://www.who.int/news-room/fact-sheets/detail/the-top-10-causes-of-death#:~:text=The%20top%20global%20causes%20of,birth%20asphyxia%20and%20birth%20trauma%2C. Accessed 20 November 2022

  2. GBD (2016) Diarrhoeal Disease Collaborators (2018). Estimates of the global, regional, and national morbidity, mortality, and etiologies of diarrhoea in 195 countries: a systematic analysis for the Global Burden of Disease Study 2016. Lancet Infect Dis 18:1211–1228. https://doi.org/10.1016/S1473-3099(18)30362-1

    Article  Google Scholar 

  3. Woh PY, Yeung MPS, Goggins WB, Lo N, Wong KT, Chow V, Chau KY, Fung K, Chen Z, Ip M (2021) Genomic epidemiology of multidrug-resistant Nontyphoidal Salmonella in young children hospitalized for gastroenteritis. Microbiol Spectr 9:e0024821. https://doi.org/10.1128/Spectrum.00248-21

    Article  PubMed  Google Scholar 

  4. Ehuwa O, Jaiswal AK, Jaiswal S (2021) Salmonella, food safety and food handling practices. Foods 10:907. https://doi.org/10.3390/foods10050907

    Article  PubMed  PubMed Central  Google Scholar 

  5. Rincón-Gamboa SM, Poutou-Piñales RA, Carrascal-Camacho AK (2021) Antimicrobial resistance of non-typhoid Salmonella in meat and meat products. Foods 10:1731. https://doi.org/10.3390/foods10081731

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Sun H, Wan Y, Du P, Bai L (2020) The epidemiology of monophasic Salmonella typhimurium. Foodborne Pathog Dis 17:87–97. https://doi.org/10.1089/fpd.2019.2676

    Article  PubMed  Google Scholar 

  7. Qin X, Yang M, Cai H, Liu Y, Gorris L, Aslam MZ, Jia K, Sun T, Wang X, Dong Q (2022) Antibiotic resistance of Salmonella typhimurium monophasic variant 1,4,[5],12:i:-in China: A systematic review and meta-analysis. Antibiotics 11:532. https://doi.org/10.3390/antibiotics11040532

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Fernandes SA, Tavechio AT, Ghilardi ÂCR, de Almeida EA, da Silva JML, Camargo CH, Tiba-Casas MR (2022) Salmonella enterica serotypes from human and nonhuman sources in Sao Paulo State, Brazil, 2004–2020. Rev Inst Med Trop Sao Paulo 64:10–19. https://doi.org/10.1590/S1678-9946202264066

    Article  Google Scholar 

  9. Jiang L, Wang P, Song X, Zhang H, Ma S, Wang J, Li W, Lv R, Liu X, Ma S, Yan J, Zhou H, Huang D, Cheng Z, Yang C, Feng L, Wang L (2021) Salmonella Typhimurium reprograms macrophage metabolism via T3SS effector SopE2 to promote intracellular replication and virulence. Nat Commun 12:879. https://doi.org/10.1038/s41467-021-21186-4

    Article  CAS  PubMed  Google Scholar 

  10. Akritidou T, Akkermans S, Gaspari S, Azraini ND, Smet C, Van de Wiele T, Van Impe JFM (2022) Effect of gastric pH and bile acids on the survival of Listeria monocytogenes and Salmonella Typhimurium during simulated gastrointestinal digestion. Innov Food Sci Emerg Technol 82:103161. https://doi.org/10.1016/j.ifset.2022.103161

    Article  CAS  Google Scholar 

  11. Sibinelli-Sousa S, de Araújo-Silva AL, Hespanhol JT, Bayer-Santos E (2022) Revisiting the steps of Salmonella gut infection with a focus on antagonistic interbacterial interactions. FEBS J 289:4192–4211. https://doi.org/10.1111/febs.16211

    Article  CAS  PubMed  Google Scholar 

  12. Gu D, Xue H, Yuan X, Yu J, Xu X, Huang Y, Li M, Zhai X, Pan Z, Zhang Y, Jiao X (2021) Genome-wide identification of genes involved in acid stress resistance of Salmonella Derby. Genes (Basel) 12:476. https://doi.org/10.3390/genes12040476

    Article  CAS  PubMed  Google Scholar 

  13. Nikiema MEM, Kakou-ngazoa S, Ky BA, Sylla A, Bako E, Addablah AYA, Ouoba JB, Sampo E, Gnada K, Zongo O, Traoré KA, Sanou A, Bonkoungou IJO, Ouédraogo R, Barro N, Sangaré L (2021) Characterization of virulence factors of Salmonella isolated from human stools and street food in urban areas of Burkina Faso. BMC Microbiol 21:338. https://doi.org/10.1186/s12866-021-02398-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Zhao S, Li C, Hsu CH, Tyson GH, Strain E, Tate H, Tran TT, Abbott J, McDermott PF (2020) Comparative genomic analysis of 450 strains of Salmonella enterica isolated from diseased animals. Genes (Basel) 11:2–16. https://doi.org/10.3390/genes11091025

    Article  CAS  Google Scholar 

  15. Wang W, Chen J, Shao X, Huang P, Zha J, Ye Y (2021) Occurrence and antimicrobial resistance of Salmonella isolated from retail meats in Anhui, China. Food Sci Nutr 9:4701–4710. https://doi.org/10.1002/fsn3.2266

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Lou L, Zhang P, Piao R, Wang Y (2019) Salmonella pathogenicity island 1 (SPI-1) and its complex regulatory network. Front Cell Infect Microbiol 9:1–12. https://doi.org/10.3389/fcimb.2019.00270

    Article  CAS  Google Scholar 

  17. Almeida F, Pitondo-Silva A, Oliveira MA, Falcão JP (2013) Molecular epidemiology and virulence markers of Salmonella Infantis isolated over 25 years in São Paulo State, Brazil. Infect Genet Evol 19:145–151. https://doi.org/10.1016/j.meegid.2013.07.004

    Article  PubMed  Google Scholar 

  18. Hur J, Choi YY, Park JH, Jeon BW, Lee HS, Kim AR, Lee JH (2011) Antimicrobial resistance, virulence-associated genes, and pulsed-field gel electrophoresis profiles of Salmonella enterica subsp. enterica serovar Typhimurium isolated from piglets with diarrhea in Korea. Can J Vet Res 75:49–56

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Shah DH, Zhou X, Addwebi T, Davis MA, Orfe L, Call DR, Guard J, Besser TE (2011) Cell invasion of poultry-associated Salmonella enterica serovar enteritidis isolates is associated with pathogenicity, motility and proteins secreted by the type III secretion system. Microbiology 157:1428–1445. https://doi.org/10.1099/mic.0.044461-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Seribelli AA, Cruz MF, Vilela FP, Frazão MR, Paziani MH, Almeida F, Medeiros MIC, Rodrigues DDP, Kress MR vo. Z, Allard MW, Falcão JP (2020) Phenotypic and genotypic characterization of Salmonella Typhimurium isolates from humans and foods in Brazil. PLoS One 15:e0237886. https://doi.org/10.1371/journal.pone.0237886

  21. Pereira T, de Barros P, Fugisaki L, Rossoni R, Ribeiro F, de Menezes R, Junqueira J, Scorzoni L (2018) Recent advances in the use of Galleria mellonella model to study immune responses against human pathogens. J Fungi 4:128. https://doi.org/10.3390/jof4040128

    Article  CAS  Google Scholar 

  22. Vilela FP, Gomes CN, Paziani MH, Braz VS, Rodrigues D dos P, Costa RG, Tiba-Casas MR, Kress MR von Z, Falcão JP, Campioni F (2020) Virulence traits and expression of bstA, fliC and sopE2 in Salmonella Dublin strains isolated from humans and animals in Brazil. Infect Genet Evol 80:104193. https://doi.org/10.1016/j.meegid.2020.104193

  23. Marin C, Chinillac MC, Cerdà-Cuéllar M, Montoro-Dasi L, Sevilla-Navarro S, Ayats T, Marco-Jimenez F, Vega S (2020) Contamination of pig carcass with Salmonella enterica serovar Typhimurium monophasic variant 1,4[5],12:i:- originates mainly in live animals. Sci Total Environ 703:134609. https://doi.org/10.1016/j.scitotenv.2019.134609

    Article  CAS  PubMed  Google Scholar 

  24. Murase T, Ozaki H, Phuektes P, Angkititrakul S (2018) Genotypic and phenotypic characterization of Salmonella enterica subsp. enterica serovar Typhimurium monophasic variants isolated in Thailand and Japan. J Vet Med Sci 80:1839–1846. https://doi.org/10.1292/jvms.18-0510

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Olive DM, Bean P (1999) Principles and applications of methods for DNA-based typing of microbial organisms. J Clin Microbiol 37:1661–1669. https://doi.org/10.1128/JCM.37.6.1661-1669.1999

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. 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. https://doi.org/10.1017/S0950268814000491

    Article  CAS  PubMed  Google Scholar 

  27. Sambrook J, Russel WD (2001) Molecular Cloning: a laboratory manual. Cold Spring Harbor Laboratory, New York

    Google Scholar 

  28. Falcão JP, Falcão DP, Pitondo-Silva A, Malaspina AC, Brocchi M (2006) Molecular typing and virulence markers of Yersinia enterocolitica strains from human, animal and food origins isolated between 1968 and 2000 in Brazil. J Med Microbiol 55:1539–1548. https://doi.org/10.1099/jmm.0.46733-0

    Article  CAS  PubMed  Google Scholar 

  29. Ribot EM, Fair MA, Gautom R, Cameron DN, Hunter SB, Swaminathan B, Barrett TJ (2006) Standardization of Pulsed-Field Gel Electrophoresis Protocols for the Subtyping of Escherichia coli O157:H7, Salmonella, and Shigella for PulseNet. Foodborne Pathog and Dis 3:59–67. https://doi.org/10.1089/fpd.2006.3.59

    Article  CAS  Google Scholar 

  30. Hunter PR, Gaston MA (1988) Numerical index of the discriminatory ability of typing systems: an application of Simpson’s index of diversity. J Clin Microbiol 26:2465–2466. https://doi.org/10.1128/jcm.26.11.2465-2466.1988

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Fang FC, Libby SJ, Buchmeier NA, Loewen PC, Switala J, Harwood J, Guiney DG (1992) The alternative σ factor KatF (RpoS) regulates Salmonella virulence. Proc Natl Acad Sci U S A 89:11978–11982.https://doi.org/10.1073/pnas.89.24.11978

  32. Renwick J, Daly P, Reeves EP, Kavanagh K (2006) Susceptibility of larvae of Galleria mellonella to infection by Aspergillus fumigatus is dependent upon stage of conidial germination. Mycopathologia 161:377–384. https://doi.org/10.1007/s11046-006-0021-1

    Article  PubMed  Google Scholar 

  33. Seixas R, Santos TR, Machado J, Tavares L, Bernardo F, Semedo-Lemsaddek T, Oliveira M (2016) Phenotypic and molecular characterization of Salmonella 1,4,[5],12:i:- R-Type ASSuT isolates from humans, animals, and environment in Portugal, 2006–2011. Foodborne Pathog Dis 13:633–641. https://doi.org/10.1089/fpd.2016.2156

    Article  CAS  PubMed  Google Scholar 

  34. Barilli E, Bacci C, Villa ZS, Merialdi G, D’Incau M, Brindani F, Vismarra A (2018) Antimicrobial resistance, biofilm synthesis and virulence genes in Salmonella isolated from pigs bred on intensive farms. Ital J Food Saf 7:131–137. https://doi.org/10.4081/ijfs.2018.7223

    Article  CAS  Google Scholar 

  35. Zheng D, Ma K, Du J, Zhou Y, Wu G, Qiao X, Wang Y, Ni Y, Fu J, Huo X (2021) Characterization of human origin Salmonella serovar 1,4,[5],12:i:- in Eastern China, 2014 to 2018. Foodborne Pathog Dis 18:790–797. https://doi.org/10.1089/fpd.2021.0008

    Article  CAS  PubMed  Google Scholar 

  36. Long L, You L, Wang D, Wang M, Wang J, Bai G, Li J, Wei X, Li S (2022) Highly prevalent MDR, frequently carrying virulence genes and antimicrobial resistance genes in Salmonella enterica serovar 4,[5],12:i:- isolates from Guizhou Province. China PLoS One 17:e0266443. https://doi.org/10.1371/journal.pone.0266443

    Article  CAS  PubMed  Google Scholar 

  37. Moura Q, Fernandes MR, Silva KC, Monte DF, Esposito F, Dropa M, Noronha C, Moreno AM, Landgraf M, Negrão FJ, Lincopan N (2018) Virulent nontyphoidal Salmonella producing CTX-M and CMY-2 β-lactamases from livestock, food and human infection, Brazil. Virulence 9:281–286. https://doi.org/10.1080/21505594.2017.1279779

    Article  CAS  PubMed  Google Scholar 

  38. Almeida F, Medeiros MIC, dos Rodrigues D, P, Falcão JP, (2015) Genotypic diversity, pathogenic potential and the resistance profile of Salmonella Typhimurium strains isolated from humans and food from 1983 to 2013 in Brazil. J Med Microbiol 64:1395–1407. https://doi.org/10.1099/jmm.0.000158

    Article  CAS  PubMed  Google Scholar 

  39. Seribelli AA, da Silva P, Frazão MR, Kich JD, Allard MW, Falcão JP (2021) Phylogenetic relationship and genomic characterization of Salmonella Typhimurium strains isolated from swine in Brazil. Infect Genet Evol 93:104977. https://doi.org/10.1016/j.meegid.2021.104977

    Article  CAS  PubMed  Google Scholar 

  40. Mandilara G, Sideroglou T, Chrysostomou A, Rentifis I, Papadopoulos T, Polemis M, Tzani M, Tryfinopoulou K, Mellou K (2021) The rising burden of salmonellosis caused by monophasic Salmonella typhimurium (1,4,[5],12:i:-) in Greece and new food vehicles. Antibiotics 10:185. https://doi.org/10.3390/antibiotics10020185

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Dionisi AM, Graziani C, Lucarelli C, Filetici E, Villa L, Owczarek S, Caprioli A, Luzzi I (2009) Molecular characterization of multidrug-resistant strains of Salmonella enterica serotype typhimurium and monophasic variant (S. 4,[5],12:i:–) isolated from human infections in Italy. Foodborne Pathog Dis 6:711–717. https://doi.org/10.1089/fpd.2008.0240

    Article  CAS  PubMed  Google Scholar 

  42. Meneguzzi M, Pissetti C, Rebelatto R, Trachsel J, Kuchiishi SS, Reis AT, Guedes RMC, Leão JA, Reichen C, Kich JD (2021) Re-emergence of salmonellosis in hog farms: Outbreak and bacteriological characterization. Microorganisms 9:947. https://doi.org/10.3390/microorganisms9050947

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Possebon FS, Tiba Casas MR, Nero LA, Yamatogi RS, Araújo JP, Pinto JP de NA (2020) Prevalence, antibiotic resistance, PFGE and MLST characterization of Salmonella in swine mesenteric lymph nodes. Prev Vet Med 179:105024. https://doi.org/10.1016/j.prevetmed.2020.105024

  44. Mourão J, Rebelo A, Ribeiro S, Peixe L, Novais C, Antunes P (2020) Atypical Non-H2S-Producing monophasic Salmonella typhimurium ST3478 strains from chicken meat at processing stage are adapted to diverse stresses. Pathogens 9:701. https://doi.org/10.3390/pathogens9090701

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Wessels K, Rip D, Gouws P (2021) Salmonella in chicken meat: consumption, outbreaks, characteristics, current control methods and the potential of bacteriophage use. Foods 10:1742. https://doi.org/10.3390/foods10081742

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Álvarez-Ordóñez A, Fernández A, Bernardo A, López M (2009) A comparative study of thermal and acid inactivation kinetics in fruit juices of Salmonella enterica serovar typhimurium and Salmonella enterica serovar senftenberg grown at acidic conditions. Foodborne Pathog Dis 6:1147–1155. https://doi.org/10.1089/fpd.2009.0313

    Article  CAS  PubMed  Google Scholar 

  47. Hsu C-Y, Wu Y-L, Lin H-C, Lin M-Y, Chou S-H, Shiau C-W, Chiu H-C (2021) A novel dibenzoxazepine attenuates intracellular Salmonella typhimurium oxidative stress resistance. Microbiol Spectr 9:e01519-e1521. https://doi.org/10.1128/Spectrum.01519-21

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Westerman TL, Bogomolnaya L, Andrews-Polymenis HL, Sheats MK, Elfenbein JR (2018) The Salmonella type-3 secretion system-1 and flagellar motility influence the neutrophil respiratory burst. PLoS One 13:e0203698. https://doi.org/10.1371/journal.pone.0203698

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Briones AC, Lorca D, Cofre A, Cabezas CE, Krüger GI, Pardo-Esté C, Baquedano MS, Salinas CR, Espinoza M, Castro-Severyn J, Remonsellez F, Hidalgo AA, Morales EH, Saavedra CP (2022) Genetic regulation of the ompX porin of Salmonella Typhimurium in response to hydrogen peroxide stress. Biol Res 55:8. https://doi.org/10.1186/s40659-022-00377-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Calderón IL, Morales E, Caro NJ, Chahúan CA, Collao B, Gil F, Villarreal JM, Ipinza F, Mora GC, Saavedra CP (2011) Response regulator ArcA of Salmonella enterica serovar Typhimurium downregulates expression of OmpD, a porin facilitating uptake of hydrogen peroxide. Res Microbiol 162:214–222. https://doi.org/10.1016/j.resmic.2010.11.001

    Article  CAS  PubMed  Google Scholar 

  51. Morales EH, Calderón IL, Collao B, Gil F, Porwollik S, McClelland M, Saavedra CP (2012) Hypochlorous acid and hydrogen peroxide-induced negative regulation of Salmonella enterica serovar Typhimurium ompW by the response regulator ArcA. BMC Microbiol 12:63. https://doi.org/10.1186/1471-2180-12-63

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Seribelli AA, Ribeiro TRM, da Silva P, Martins IM, Vilela FP, Medeiros MIC, Peronni KC, da Silva Junior WA, Moreira CG, Falcão JP (2021) Salmonella Typhimurium ST313 isolated in Brazil revealed to be more invasive and inflammatory in murine colon compared to ST19 strains. J Microbiol 59:861–870. https://doi.org/10.1007/s12275-021-1082-z

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This study was supported by a research grant from the São Paulo Research Foundation (FAPESP) (Proc. 2019/19338–8 and 2022/07013–0) under the supervision of JPF and the Coordination of Improvement of Higher Education Personnel (CAPES) – Finance Code 001. During the course of this study, GNP was supported by a fellowship from CAPES 88887.523672/2020–00. JPF received a productive fellowship from the National Council for Scientific and Technological Development (CNPq: Proc.304399/2018–3 and 304803/2021–9).

Author information

Authors and Affiliations

  1. Departamento de Análises Clínicas, Toxicológicas E Bromatológicas, Faculdade de Ciências Farmacêuticas de Ribeirão Preto – USP, Av. Do Café, S/N°, Ribeirão Preto, SP, 14040-903, Brasil

    Giovana do Nascimento Pereira, Amanda Aparecida Seribelli, Carolina Nogueira Gomes, Felipe Pinheiro Vilela, Ludmilla Tonani, Márcia Regina von Zeska Kress & Juliana Pfrimer Falcão

  2. Departamento de Biologia Celular E Molecular E Bioagentes Patogênicos, Faculdade de Medicina de Ribeirão Preto - USP, Av. Do Café, S/N°, Ribeirão Preto, SP, 14040-903, Brasil

    Amanda Aparecida Seribelli

  3. Instituto Adolfo Lutz – IAL, Av. Dr. Arnaldo, 355, São Paulo, SP, 01246-000, Brasil

    Monique Ribeiro Tiba-Casas

  4. Instituto Adolfo Lutz – IAL, R. Minas, 877, Ribeirão Preto, SP, 14085-410, Brasil

    Marta Inês Cazentini Medeiros

  5. Fundação Oswaldo Cruz – FIOCRUZ, Pavilhão Rocha Lima, Av. Brasil, 4365, Rio de Janeiro, RJ, 21040-900, Brasil

    Dália dos Prazeres Rodrigues

Authors
  1. Giovana do Nascimento Pereira
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Amanda Aparecida Seribelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Carolina Nogueira Gomes
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Felipe Pinheiro Vilela
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ludmilla Tonani
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Monique Ribeiro Tiba-Casas
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Marta Inês Cazentini Medeiros
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Dália dos Prazeres Rodrigues
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Márcia Regina von Zeska Kress
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Juliana Pfrimer Falcão
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Giovana do Nascimento Pereira wrote the manuscript and did the methodologies and analyses. Amanda Aparecida Seribelli and Carolina Nogueira Gomes helped with methodologies of acid and oxidative stresses and analyses. Felipe Pinheiro Vilela helped with methodologies of Galleria mellonella and analyses. Ludmilla Tonani helped with Galleria mellonella assay. Monique Ribeiro Tiba-Casas, Marta Inês Cazentini Medeiros, and Dália dos Prazeres Rodrigues provided the strains. Marcia Regina von Zeska Kress helped with Galleria mellonella assay. Juliana Pfrimer Falcão reviewed and edited the manuscript, got funding aid and supervised the work at University of Sao Paulo.

Corresponding author

Correspondence to Juliana Pfrimer Falcão.

Ethics declarations

Ethics approval

Ethical approval was granted from the Ethics Committee of the School of Pharmaceutical Sciences of Ribeirão Preto – USP. CAAE 42889721.1.0000.5403.

Consent to participate

All authors read and approved the manuscript.

Consent for publication

All authors read and approved the manuscript.

Competing interests

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Responsible Editor: Luis Augusto Nero

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 17 KB)

Supplementary file2 (DOCX 37 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pereira, G.d.N., Seribelli, A.A., Gomes, C.N. et al. Virulence potential of Salmonella 1,4, [5],12:i:- strains isolated during decades from different sources in the Southeast region of Brazil. Braz J Microbiol 54, 2827–2843 (2023). https://doi.org/10.1007/s42770-023-01145-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42770-023-01145-5

Keywords

Search

Navigation