Phenotypic analyses of Salmonella enterica serovar Enteritidis strains isolated in the pre- and post-epidemic period in

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BACTERIAL AND FUNGAL PATHOGENESIS - RESEARCH PAPER

Phenotypic analyses of Salmonella enterica serovar Enteritidis strains isolated in the pre- and post-epidemic period in Brazil Fábio Campioni 1 & Carolina Nogueira Gomes 1 & Dália dos Prazeres Rodrigues 2 & Alzira Maria Morato Bergamini 3 & Juliana Pfrimer Falcão 1 Received: 6 May 2020 / Accepted: 17 October 2020 # Sociedade Brasileira de Microbiologia 2020

Abstract Salmonella Enteritidis has caused, since the 1980s, a sustained epidemic of human infections in many countries. This study analyzed S. Enteritidis strains isolated before and after the epidemic period in Brazil regarding their capacities to survive to acid, oxidative, and high-temperature stresses, and capacity to grow in egg albumen. Moreover, the ability to invade human epithelial cells (Caco-2) and to survive inside human (U937) and chicken (HD11) macrophages was checked. Post-epidemic strains showed a better ability to survive after 10 min under acid stress at 37 °C (P ≤ 0.05). However, both groups of strains showed similar ability to survive after 1 h under acid stress at 37 °C and at 42 °C independently of the time of exposure. Similar ability was verified in both groups of strains regarding oxidative stress, growth in egg albumen, high-temperature stress, invasion to Caco-2 cells, and invasion and survival in macrophages. In conclusion, post-epidemic S. Enteritidis strains showed a better ability to survive under the acid stress found in the stomach, which might be an advantage to reach the intestine and colonize chickens and humans. However, both groups of strains did not differ significantly in the majority of the phenotypic tests analyzed in this study. Keywords Salmonella Enteritidis . Epidemic . Stress . Cell invasion . Macrophage survival

Introduction Salmonella enterica serovar Enteritidis (S. Enteritidis) is a major Salmonella serovar causing, since the 1980s, a sustained epidemic of human infections in several countries linked mostly to the consumption of raw or undercooked chicken or eggs, becoming one of the top Salmonella serovars isolated in the globe [1]. Responsible Editor: Cristiano Gallina Moreira * Juliana Pfrimer Falcão [email protected] 1

Departamento de Análises Clínicas, Toxicológicas e Bromatológicas, Faculdade de Ciências Farmacêuticas de Ribeirão Preto - USP, Av. do Café, s/n. Bloco S – Sala 41, Ribeirão Preto, SP 14040-903, Brazil

2

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

3

Laboratório de Microbiologia de Alimentos, Instituto Adolfo Lutz – Centro de Laboratórios Regionais - Ribeirão Preto VI, Rua Minas 877, Ribeirão Preto, SP 14085-410, Brazil

The precise date of the epidemic beginning is not known, as well as the exact reasons have not been well established. However, the existence of a S. Enteritidis epidemic clone, harboring genes for chicken colonization, has been shown in some countries [2–5]. In Brazil, the introduction of an epidemic clone was noticed a

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