Rapid DNA Detection of Salmonella enterica Typhimurium and Heidelberg from Poultry Samples
Abstract
:1. Introduction
2. Materials and Methods
2.1. Bacterial Isolates
2.2. Clinical/Environmental Poultry Flock Samples
2.3. DNA Extraction and Multiplex Real-Time PCRs
3. Results
3.1. Analysis of Salmonella Isolates
3.2. Analysis of Clinical/Environmental Poultry Flock Samples
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- WHO (World Health Organization). Salmonella. Available online: https://www.who.int/westernpacific/health-topics/salmonella (accessed on 31 May 2021).
- Issenhuth-Jeanjean, S.; Roggentin, P.; Mikoleit, M.; Guibourdenche, M.; de Pinna, E.; Nair, S.; Fields, P.I.; Weill, F.X. Supplement 2008-2010 (no. 48) to the White-Kauffmann-Le Minor scheme. Res. Microbiol. 2014, 165, 526–530. [Google Scholar] [CrossRef]
- Switt, A.I.; Soyer, Y.; Warnick, L.D.; Wiedmann, M. Emergence, distribution, and molecular and phenotypic characteristics of Salmonella enterica serotype 4,5,12:i:-. Foodborne. Pathog. Dis. 2009, 6, 407–415. [Google Scholar] [CrossRef]
- Nisar, M.; Kassem, I.I.; Rajashekara, G.; Goyal, S.M.; Lauer, D.; Voss, S.; Nagaraja, K.V. Genotypic relatedness and antimicrobial resistance of Salmonella Heidelberg isolated from chickens and turkeys in the midwestern United States. J. Vet. Diagn. Investig. 2017, 29, 370–375. [Google Scholar] [CrossRef]
- Reis, R.O.D.; Souza, M.N.; Cecconi, M.C.P.; Timm, L.; Ikuta, N.; Simon, D.; Wolf, J.M.; Lunge, V.R. Increasing prevalence and dissemination of invasive nontyphoidal Salmonella serotype Typhimurium with multidrug resistance in hospitalized patients from southern Brazil. Braz. J. Infect. Dis. 2018, 22, 424–432. [Google Scholar] [CrossRef] [PubMed]
- Kipper, D.; Mascitti, A.K.; De Carli, S.; Carneiro, A.M.; Streck, A.F.; Fonseca, A.S.K.; Ikuta, N.; Lunge, V.R. Emergence, Dissemination and Antimicrobial Resistance of the Main Poultry-Associated Salmonella Serovars in Brazil. Vet. Sci. 2022, 9, 405. [Google Scholar] [CrossRef] [PubMed]
- Sun, H.; Wan, Y.; Du, P.; Bai, L. The Epidemiology of Monophasic Salmonella Typhimurium. Foodborne Pathog. Dis. 2020, 17, 87–97. [Google Scholar] [CrossRef] [PubMed]
- Souza, A.I.S.; Saraiva, M.M.S.; Casas, M.R.T.; Oliveira, G.M.; Cardozo, M.V.; Benevides, V.P.; Barbosa, F.O.; Freitas Neto, O.C.; Almeida, A.M.; Berchieri, A., Jr. High occurrence of β-lactamase-producing Salmonella Heidelberg from poultry origin. PLoS ONE 2020, 15, e0230676. [Google Scholar] [CrossRef] [PubMed]
- Kipper, D.; Orsi, R.H.; Carroll, L.M.; Mascitti, A.K.; Streck, A.F.; Fonseca, A.S.K.; Ikuta, N.; Tondo, E.C.; Wiedmann, M.; Lunge, V.R. Recent Evolution and Genomic Profile of Salmonella enterica Serovar Heidelberg Isolates from Poultry Flocks in Brazil. Appl. Environ. Microbiol. 2021, 87, e0103621. [Google Scholar] [CrossRef] [PubMed]
- Velge, P.; Cloeckaert, A.; Barrow, P. Emergence of Salmonella epidemics: The problems related to Salmonella enterica serotype Enteritidis and multiple antibiotic resistance in other major serotypes. Vet. Res. 2005, 36, 267–288. [Google Scholar] [CrossRef] [PubMed]
- OIE; World Organization for Animal Health. OIE Terrestrial Manual 2010; Salmonellosis: Paris, France, 2010; Chapter 2.9.9. [Google Scholar]
- Lee, K.M.; Runyon, M.; Herrman, T.J.; Phillips, R.; Hsieh, J. Review of Salmonella detection and identification methods: Aspects of rapid emergency response and food safety. Food Control 2015, 47, 264–276. [Google Scholar] [CrossRef]
- MAPA. Instrução Normativa Nº 193, de 19 de Setembro de 1994; Ministério da Agricultura, Pecuária e Abastecimento, MAPA: Brasília, DF, Brazil, 1994.
- MAPA. Instrução Normativa Nº 78, de 03 de Novembro de 2003; Ministério da Agricultura, Pecuária e Abastecimento, MAPA: Brasília, DF, Brazil, 2003.
- MAPA. Instrução Normativa Nº 20, de 21 de Outubro de 2016; Ministério da Agricultura, Pecuária e Abastecimento, MAPA: Brasília, DF, Brazil, 2016.
- Grimont, P.A.; Weil, F.X. Antigenic Formulae of the Salmonella Serovars, 9th ed.; WHO Collaborating Centre for Reference and Research on Salmonella; Institut Pasteur: Paris, France, 2007; pp. 1–167. [Google Scholar]
- Souza, M.N.; Lehmann, F.K.M.; De Carli, S.; Kipper, D.; Fonseca, A.S.K.; Ikuta, N.; Lunge, V.R. Molecular detection of Salmonella serovars Enteritidis, Heidelberg and Typhimurium directly from pre-enriched poultry samples. Br. Poult. Sci. 2019, 60, 388–394. [Google Scholar] [CrossRef] [PubMed]
- Gast, R.K. Paratyphoid infections. In Diseases of Poultry, 12th ed.; Blackwell Publishing: Ames, IA, USA, 2008; pp. 636–655. [Google Scholar]
- Deng, X.; Shariat, N.; Driebe, E.M.; Roe, C.C.; Tolar, B.; Trees, E.; Keim, P.; Zhang, W.; Dudley, E.G.; Fields, P.I.; et al. Comparative analysis of subtyping methods against a whole-genome-sequencing standard for Salmonella enterica serotype Enteritidis. J. Clin. Microbiol. 2015, 53, 212–218. [Google Scholar] [CrossRef] [PubMed]
- Maurischat, S.; Baumann, B.; Martin, A.; Malorny, B. Rapid detection and specific differentiation of Salmonella enterica subsp. enterica Enteritidis, Typhimurium and its monophasic variant 4,[5],12:i:- by real-time multiplex PCR. Int. J. Food Microbiol. 2015, 193, 8–14. [Google Scholar] [CrossRef] [PubMed]
- Park, S.H.; Ricke, S.C. Development of multiplex PCR assay for simultaneous detection of Salmonella genus, Salmonella subspecies I, Salm. Enteritidis, Salm. Heidelberg and Salm. Typhimurium. J. Appl. Microbiol. 2015, 118, 152–160. [Google Scholar] [CrossRef] [PubMed]
- Zhang, S.; Yin, Y.; Jones, M.B.; Zhang, Z.; Deatherage Kaiser, B.L.; Dinsmore, B.A.; Fitzgerald, C.; Fields, P.I.; Deng, X. Salmonella serotype determination utilizing high-throughput genome sequencing data. J. Clin. Microbiol. 2015, 53, 1685–1692. [Google Scholar] [CrossRef]
- L Plym, F.; Wierup, M. Salmonella contamination: A significant challenge to the global marketing of animal food products. Rev. Sci. Tech. 2006, 25, 541–554. [Google Scholar]
- MAPA. Instrução Normativa Nº 62, de 26 de Agosto de 2003. In Anexo–Métodos Analíticos Oficiais para Análises Microbiológicas para Controle de Produtos de Origem Animal e Água–Capítulo XV–Pesquisa Salmonella; Ministério da Agricultura, Pecuária e Abastecimento, MAPA: Brasília, DF, Brazil, 2003. [Google Scholar]
- Soumet, C.; Ermel, G.; Fach, P.; Colin, P. Evaluation of different DNA extraction procedures for the detection of Salmonella from chicken products by polymerase chain reaction. Lett. Appl. Microbiol. 1994, 19, 294–298. [Google Scholar] [CrossRef]
- Morasi, R.M.; da Silva, A.Z.; Nuñez, K.V.M.; Dantas, S.T.A.; Faganello, C.; Juliano, L.C.B.; Tiba-Casas, M.R.; Pantoja, J.C.F.; Amarante, A.F.; Júnior, A.F.; et al. Overview of antimicrobial resistance and virulence factors in Salmonella spp. isolated in the last two decades from chicken in Brazil. Food Res. Int. 2022, 162, 111955. [Google Scholar] [CrossRef]
- Ferrari, R.G.; Rosario, D.K.A.; Cunha-Neto, A.; Mano, S.B.; Figueiredo, E.E.S.; Conte-Junior, C.A. Worldwide Epidemiology of Salmonella Serovars in Animal-Based Foods: A Meta-analysis. Appl. Environ. Microbiol. 2019, 85, e00591-19. [Google Scholar] [CrossRef]
- Fernandes, S.A.; Paterson, D.L.; Ghilardi-Rodrigues, A.C.; Adams-Haduch, J.M.; Tavechio, A.T.; Doi, Y. CTX-M-2-producing Salmonella Typhimurium isolated from pediatric patients and poultry in Brazil. Microb. Drug Resist. 2009, 15, 317–321. [Google Scholar] [CrossRef]
- Seribelli, A.A.; Cruz, M.F.; Vilela, F.P.; Frazão, M.R.; Paziani, M.H.; Almeida, F.; Medeiros, M.I.C.; Rodrigues, D.D.P.; Kress, M.R.V.Z.; Allard, M.W.; et al. Phenotypic and genotypic characterization of Salmonella Typhimurium isolates from humans and foods in Brazil. PLoS ONE 2020, 15, e0237886. [Google Scholar] [CrossRef]
- Seribelli, A.A.; da Silva, P.; Frazão, M.R.; Kich, J.D.; Allard, M.W.; Falcão, J.P. Phylogenetic relationship and genomic characterization of Salmonella Typhimurium strains isolated from swine in Brazil. Infect. Genet. Evol. 2021, 93, 104977. [Google Scholar] [CrossRef] [PubMed]
- Foley, S.L.; Lynne, A.M. Food animal-associated Salmonella challenges: Pathogenicity and antimicrobial resistance. J. Anim. Sci. 2008, 86, E173–E187. [Google Scholar] [CrossRef]
- Han, J.; Lynne, A.M.; David, D.E.; Tang, H.; Xu, J.; Nayak, R.; Kaldhone, P.; Logue, C.M.; Foley, S.L. DNA sequence analysis of plasmids from multidrug resistant Salmonella enterica serotype Heidelberg isolates. PLoS ONE 2012, 7, e51160. [Google Scholar] [CrossRef]
- Chittick, P.; Sulka, A.; Tauxe, R.V.; Fry, A.M. A summary of national reports of foodborne outbreaks of Salmonella Heidelberg infections in the United States: Clues for disease prevention. J. Food Prot. 2006, 69, 1150–1153. [Google Scholar] [CrossRef]
- Pulido-Landínez, M.; Sánchez-Ingunza, R.; Guard, J.; Pinheiro do Nascimento, V. Assignment of serotype to Salmonella enterica isolates obtained from poultry and their environment in southern Brazil. Lett. Appl. Microbiol. 2013, 57, 288–294. [Google Scholar] [CrossRef]
- Núncio, A.S.P.; Webber, B.; Pottker, E.S.; Cardoso, B.; Esposito, F.; Fontana, H.; Lincopan, N.; Girardello, R.; Pilotto, F.; Dos Santos, L.R.; et al. Genomic characterization of multidrug-resistant Salmonella Heidelberg E2 strain isolated from chicken carcass in southern Brazil. Int. J. Food Microbiol. 2022, 379, 109863. [Google Scholar] [CrossRef] [PubMed]
- Sielski Galvão Soares, L.; Casella, T.; Kawagoe, E.K.; Benetti Filho, V.; Omori, W.P.; Nogueira, M.C.L.; Wagner, G.; Rodrigues de Oliveira, R.; Stahlhofer, S.R.; Antunes Ferreira, F.; et al. Phenotypic and genotypic characterization of antibiotic resistance of Salmonella Heidelberg in the South of Brazil. Int. J. Food Microbiol. 2023, 391–393, 110151. [Google Scholar] [CrossRef] [PubMed]
- Silveira, L.; Nunes, A.; Pista, Â.; Isidro, J.; Belo Correia, C.; Saraiva, M.; Batista, R.; Castanheira, I.; Machado, J.; Gomes, J.P. Characterization of Multidrug-Resistant Isolates of Salmonella enterica Serovars Heidelberg and Minnesota from Fresh Poultry Meat Imported to Portugal. Microb. Drug Resist. 2021, 27, 87–98. [Google Scholar] [CrossRef] [PubMed]
- Bugarel, M.; Tudor, A.; Loneragan, G.H.; Nightingale, K.K. Molecular detection assay of five Salmonella serotypes of public interest: Typhimurium, Enteritidis, Newport, Heidelberg, and Hadar. J. Microbiol. Methods 2017, 134, 14–20. [Google Scholar] [CrossRef]
- CDC, Centers for Disease Control and Prevention. National Enteric Disease Surveillance: Salmonella Annual Report, 2013; National Center for Emerging and Zoonotic Infectious Diseases: Atlanta, GA, USA, 2016.
- RASFF, Rapid Alert System for Food and Feed. The Rapid Alert System for Food and Feed-2013 Annual Report; The Europian Union: Luxembourg, 2014. [Google Scholar]
- Waldman, J.; Souza, M.N.; Fonseca, A.S.K.; Ikuta, N.; Lunge, V.R. Direct detection of Salmonella from poultry samples by DNA isothermal amplification. Br. Poult. Sci. 2020, 61, 653–659. [Google Scholar] [CrossRef]
- Cheng, C.Y.; Chi, J.R.; Lin, S.R.; Chou, C.C.; Huang, C.C. Rapid quantification of Salmonella Typhimurium inoculated to meat products by real-time PCR. Acta Vet. Hung. 2009, 57, 25–38. [Google Scholar] [CrossRef] [PubMed]
- McCarthy, N.; Reen, F.J.; Buckley, J.F.; Frye, J.G.; Boyd, E.F.; Gilroy, D. Sensitive and rapid molecular detection assays for Salmonella enterica serovars Typhimurium and Heidelberg. J. Food Prot. 2009, 72, 2350–2357. [Google Scholar] [CrossRef] [PubMed]
- Prendergast, D.M.; Hand, D.; Nί Ghallchóir, E.; McCabe, E.; Fanning, S.; Griffin, M.; Egan, J.; Gutierrez, M. A multiplex real-time PCR assay for the identification and differentiation of Salmonella enterica serovar Typhimurium and monophasic serovar 4,[5],12:i:-. Int. J. Food Microbiol. 2013, 166, 48–53. [Google Scholar] [CrossRef]
Serological Profile (n) | Antigenic Formula | S. enterica qPCR | Heidelberg qPCR | Typhimurium qPCR | Partial WKL ¹ Scheme (n) | SHTAmp qPCR (n) |
---|---|---|---|---|---|---|
Poli O; OMA; O:4; O:5; O:12; H:r and H:2 (57) | 1,4,[5]12:r:1,2 | + | + | - | Heidelberg (57) | Heidelberg (57) |
Poli O; OMA; O:4; O:5; O:12; H:i and H:2 (21) | 1,4,[5]12:i:1,2 | + | - | + | Typhimurium (21) | Typhimurium (21) |
Poli O, OMB; O:8; H:z10 e H:enx (1) | 6,8:z10:e,n,x | + | - | - | Hadar (1) | Negative (1) |
Poli O; OMA; O:21; H:e,n,x; H:b (2) | 21:b:e,n,x | + | - | - | Minnesota (2) | Negative (2) |
Poli O; OMA; O:4; H:E; H:h e H:enz15 (1) | 1,4,[5]12:e,h:e,n,z15 | + | - | - | Sandiego (1) | Negative (1) |
Poli O; OMA; O:4; O:12; O:27; H:d and H:7 (1) | 1,4,12,27:d:1,7 | + | - | - | Schwarzengrund (1) | Negative (1) |
Poli O; OMA; O:4; O:5; O:12; H:i (4) | 1,4,[5],12:i:- | + | - | + | Salmonella spp. (4) | Typhimurium (4) |
Poli O; OMA; O:4; O:5; O:12; H:2 (5) | 1,4,[5],12:-:1,2 | + | - | + | Salmonella spp. (5) | Typhimurium (5) |
Poli O; OMA; O:4; O:5; O:12; H:2 (2) | 1,4,[5],12:-:1,2 | + | - | - | Salmonella spp. (2) | Negative (2) |
Poli O; OMA; O:4; O:5; O:12; H:2 (9) | 1,4,[5],12:-:1,2 | + | + | - | Salmonella spp. (9) | Heidelberg (9) |
Poli O; OMA; O:4; H:2 (4) | 1,4:-:1,2 | + | + | - | Salmonella spp. (4) | Heidelberg (4) |
Poli O; OMA; O:4; H:2, H:r (3) | 1,4:r:1,2 | + | + | - | Salmonella spp. (3) | Heidelberg (3) |
Poli O; OMA; O:4; H:r (2) | 1,4:r:- | + | + | - | Salmonella spp. (2) | Heidelberg (2) |
Poli O; OMA; O:4; O:12 (5) | 1,4,12:-:- | + | + | - | Salmonella spp. (5) | Heidelberg (5) |
Poli O; OMA; O:4; O:5; O:12 (7) | 1,4,[5]12:-:- | + | + | - | Salmonella spp. (7) | Heidelberg (7) |
Poli O; OMA; O:4 (3) | 1,4:-:- | + | + | - | Salmonella spp. (3) | Heidelberg (3) |
Poli O, O:4 (1) | 1,4:-:- | + | + | - | Salmonella spp. (1) | Heidelberg (1) |
Poli O, O:5 (1) | 1,[5]:-:- | + | + | - | Salmonella spp. (1) | Heidelberg (1) |
Poli O (9) | -:-:- | + | + | - | Salmonella spp. (9) | Heidelberg (9) |
Poli O (3) | -:-:- | + | - | - | Salmonella spp. (3) | Negative (3) |
Poli O; OMA; O:4; O:5; O:12; H:r (2) | 1,4,[5],12:r:- | + | - | - | Salmonella spp. (2) | Negative (2) |
Poli O; OMA; O:4; H:e (1) | 1,4:e:- | + | - | - | Salmonella spp. (1) | Negative (1) |
Poli O; OMA; O:4; O:12; O:27 (2) | 1,4,12,27:-:- | + | - | - | Salmonella spp. (2) | Negative (2) |
Poli O; OMA; O:4; O:12; O:27, H:r (1) | 1,4,12,27:r:- | + | - | - | Salmonella spp. (1) | Negative (1) |
Antigenic Formula | S. enterica qPCR | Heidelberg qPCR | Typhimurium qPCR | WKLM ¹ Scheme Result (n) | SHTAmp qPCR (n) |
---|---|---|---|---|---|
3,10[15][15,34]:e,h:1,6 | + | - | - | Anatum (1) | Negative (1) |
1,4,12,27:l,v:1,7 | + | - | - | Bredeney (1) | Negative (1) |
1,9,12:g,m:- | + | - | - | Enteritidis (8) | Negative (8) |
1,9,12:-:- | + | - | - | Gallinarum (8) | Negative (8) |
1,4,[5]12:r:1,2 | + | + | - | Heidelberg (6) | Heidelberg (6) |
1,4,12,27:d:1,7 | + | - | - | Schwarzengrund (2) | Negative (2) |
6,7,14:z29:[1,2,7] | + | - | - | Tennessee (1) | Negative (1) |
1,4,[5]12:i:1,2 | + | - | + | Typhimurium (3) | Typhimurium (3) |
Missing data | + | - | - | Salmonella spp. (4) | Negative (4) |
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Mathias, J.B.; Souza, M.N.; Kipper, D.; Fonseca, A.S.K.; Lunge, V.R.; Ikuta, N. Rapid DNA Detection of Salmonella enterica Typhimurium and Heidelberg from Poultry Samples. Poultry 2024, 3, 47-56. https://doi.org/10.3390/poultry3010005
Mathias JB, Souza MN, Kipper D, Fonseca ASK, Lunge VR, Ikuta N. Rapid DNA Detection of Salmonella enterica Typhimurium and Heidelberg from Poultry Samples. Poultry. 2024; 3(1):47-56. https://doi.org/10.3390/poultry3010005
Chicago/Turabian StyleMathias, Joana Bittencourt, Margarida Neves Souza, Diéssy Kipper, André Salvador Kazantzi Fonseca, Vagner Ricardo Lunge, and Nilo Ikuta. 2024. "Rapid DNA Detection of Salmonella enterica Typhimurium and Heidelberg from Poultry Samples" Poultry 3, no. 1: 47-56. https://doi.org/10.3390/poultry3010005