Host-pathogen interaction at the intestinal mucosa correlates with zoonotic potential of Streptococcus suis

Maria Laura Ferrando, Astrid De Greeff, W.J.M. Van Rooijen, Norbert Stockhofe-Zurwieden, Jens Nielsen, P.J. Wichgers Schreur, Yvonne Pannekoek, Annet Heuvelink, Arie Van Der Ende, Hilde Smith, Constance Schultsz*

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

25 Citations (Scopus)

Abstract

Streptococcus suis has emerged as an important cause of bacterial meningitis in adults. The ingestion of undercooked pork is a risk factor for human S. suis serotype 2 (SS2) infection. Here we provide experimental evidence indicating that the gastrointestinal tract is an entry site of SS2 infection. Methods. We developed a noninvasive in vivo model to study oral SS2 infection in piglets.We compared in vitro interaction of S. suis with human and porcine intestinal epithelial cells (IEC). Results. Two out of 15 piglets showed clinical symptoms compatible with S. suis infection 24-48 hours after ingestion of SS2. SS2 was detected in mesenteric lymph nodes of 40% of challenged piglets. SS2 strains isolated from patients showed significantly higher adhesion to human IEC compared to invasive strains isolated from pigs. In contrast, invasive SS9 strains showed significantly higher adhesion to porcine IEC. Translocation across human IEC, which occurred predominately via a paracellular route, was significantly associated with clonal complex 1, the predominant zoonotic genotype. Adhesion and translocation were dependent on capsular polysaccharide production. Conclusions. SS2 should be considered a food-borne pathogen. S. suis interaction with human and pig IEC correlates with S. suis serotype and genotype, which can explain the zoonotic potential of SS2.

Original languageEnglish
Pages (from-to)95-105
JournalThe Journal of Infectious Diseases
Volume212
Issue number1
DOIs
Publication statusPublished - 2015

Fingerprint

Streptococcus suis
Host-Pathogen Interactions
Zoonoses
Intestinal Mucosa
Epithelial Cells
Swine
Infection
Eating
Genotype
Serogroup
Bacterial Meningitides
Polysaccharides
Gastrointestinal Tract
Lymph Nodes

Keywords

  • clonal complex
  • intestinal translocation
  • piglets.
  • serotype
  • Streptococcus suis
  • tight junctions
  • zoonotic infections

Cite this

Ferrando, Maria Laura ; De Greeff, Astrid ; Van Rooijen, W.J.M. ; Stockhofe-Zurwieden, Norbert ; Nielsen, Jens ; Wichgers Schreur, P.J. ; Pannekoek, Yvonne ; Heuvelink, Annet ; Van Der Ende, Arie ; Smith, Hilde ; Schultsz, Constance. / Host-pathogen interaction at the intestinal mucosa correlates with zoonotic potential of Streptococcus suis. In: The Journal of Infectious Diseases. 2015 ; Vol. 212, No. 1. pp. 95-105.
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title = "Host-pathogen interaction at the intestinal mucosa correlates with zoonotic potential of Streptococcus suis",
abstract = "Streptococcus suis has emerged as an important cause of bacterial meningitis in adults. The ingestion of undercooked pork is a risk factor for human S. suis serotype 2 (SS2) infection. Here we provide experimental evidence indicating that the gastrointestinal tract is an entry site of SS2 infection. Methods. We developed a noninvasive in vivo model to study oral SS2 infection in piglets.We compared in vitro interaction of S. suis with human and porcine intestinal epithelial cells (IEC). Results. Two out of 15 piglets showed clinical symptoms compatible with S. suis infection 24-48 hours after ingestion of SS2. SS2 was detected in mesenteric lymph nodes of 40{\%} of challenged piglets. SS2 strains isolated from patients showed significantly higher adhesion to human IEC compared to invasive strains isolated from pigs. In contrast, invasive SS9 strains showed significantly higher adhesion to porcine IEC. Translocation across human IEC, which occurred predominately via a paracellular route, was significantly associated with clonal complex 1, the predominant zoonotic genotype. Adhesion and translocation were dependent on capsular polysaccharide production. Conclusions. SS2 should be considered a food-borne pathogen. S. suis interaction with human and pig IEC correlates with S. suis serotype and genotype, which can explain the zoonotic potential of SS2.",
keywords = "clonal complex, intestinal translocation, piglets., serotype, Streptococcus suis, tight junctions, zoonotic infections",
author = "Ferrando, {Maria Laura} and {De Greeff}, Astrid and {Van Rooijen}, W.J.M. and Norbert Stockhofe-Zurwieden and Jens Nielsen and {Wichgers Schreur}, P.J. and Yvonne Pannekoek and Annet Heuvelink and {Van Der Ende}, Arie and Hilde Smith and Constance Schultsz",
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Host-pathogen interaction at the intestinal mucosa correlates with zoonotic potential of Streptococcus suis. / Ferrando, Maria Laura; De Greeff, Astrid; Van Rooijen, W.J.M.; Stockhofe-Zurwieden, Norbert; Nielsen, Jens; Wichgers Schreur, P.J.; Pannekoek, Yvonne; Heuvelink, Annet; Van Der Ende, Arie; Smith, Hilde; Schultsz, Constance.

In: The Journal of Infectious Diseases, Vol. 212, No. 1, 2015, p. 95-105.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - Host-pathogen interaction at the intestinal mucosa correlates with zoonotic potential of Streptococcus suis

AU - Ferrando, Maria Laura

AU - De Greeff, Astrid

AU - Van Rooijen, W.J.M.

AU - Stockhofe-Zurwieden, Norbert

AU - Nielsen, Jens

AU - Wichgers Schreur, P.J.

AU - Pannekoek, Yvonne

AU - Heuvelink, Annet

AU - Van Der Ende, Arie

AU - Smith, Hilde

AU - Schultsz, Constance

PY - 2015

Y1 - 2015

N2 - Streptococcus suis has emerged as an important cause of bacterial meningitis in adults. The ingestion of undercooked pork is a risk factor for human S. suis serotype 2 (SS2) infection. Here we provide experimental evidence indicating that the gastrointestinal tract is an entry site of SS2 infection. Methods. We developed a noninvasive in vivo model to study oral SS2 infection in piglets.We compared in vitro interaction of S. suis with human and porcine intestinal epithelial cells (IEC). Results. Two out of 15 piglets showed clinical symptoms compatible with S. suis infection 24-48 hours after ingestion of SS2. SS2 was detected in mesenteric lymph nodes of 40% of challenged piglets. SS2 strains isolated from patients showed significantly higher adhesion to human IEC compared to invasive strains isolated from pigs. In contrast, invasive SS9 strains showed significantly higher adhesion to porcine IEC. Translocation across human IEC, which occurred predominately via a paracellular route, was significantly associated with clonal complex 1, the predominant zoonotic genotype. Adhesion and translocation were dependent on capsular polysaccharide production. Conclusions. SS2 should be considered a food-borne pathogen. S. suis interaction with human and pig IEC correlates with S. suis serotype and genotype, which can explain the zoonotic potential of SS2.

AB - Streptococcus suis has emerged as an important cause of bacterial meningitis in adults. The ingestion of undercooked pork is a risk factor for human S. suis serotype 2 (SS2) infection. Here we provide experimental evidence indicating that the gastrointestinal tract is an entry site of SS2 infection. Methods. We developed a noninvasive in vivo model to study oral SS2 infection in piglets.We compared in vitro interaction of S. suis with human and porcine intestinal epithelial cells (IEC). Results. Two out of 15 piglets showed clinical symptoms compatible with S. suis infection 24-48 hours after ingestion of SS2. SS2 was detected in mesenteric lymph nodes of 40% of challenged piglets. SS2 strains isolated from patients showed significantly higher adhesion to human IEC compared to invasive strains isolated from pigs. In contrast, invasive SS9 strains showed significantly higher adhesion to porcine IEC. Translocation across human IEC, which occurred predominately via a paracellular route, was significantly associated with clonal complex 1, the predominant zoonotic genotype. Adhesion and translocation were dependent on capsular polysaccharide production. Conclusions. SS2 should be considered a food-borne pathogen. S. suis interaction with human and pig IEC correlates with S. suis serotype and genotype, which can explain the zoonotic potential of SS2.

KW - clonal complex

KW - intestinal translocation

KW - piglets.

KW - serotype

KW - Streptococcus suis

KW - tight junctions

KW - zoonotic infections

U2 - 10.1093/infdis/jiu813

DO - 10.1093/infdis/jiu813

M3 - Article

VL - 212

SP - 95

EP - 105

JO - The Journal of Infectious Diseases

JF - The Journal of Infectious Diseases

SN - 0022-1899

IS - 1

ER -