Staff Publications

Staff Publications

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    'Staff publications' contains references to publications authored by Wageningen University staff from 1976 onward.

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Clonal expansion of a virulent Streptococcus suis serotype 9 lineage distinguishable from carriage subpopulations
Willemse, Niels ; Ark, Kees C.H. van der; Stockhofe-Zurwieden, Norbert ; Smith, Hilde ; Picavet, Daisy I. ; Solt-Smits, Conny van; Wisselink, Henk J. ; Schultsz, Constance ; Greeff, Astrid de - \ 2019
Scientific Reports 9 (2019)1. - ISSN 2045-2322

Streptococcus suis is a porcine pathogen, causing severe invasive infections. S. suis serotype 9 is increasingly causing disease in Dutch and Chinese pig herds, but it is unknown whether all serotype 9 isolates are equally virulent and markers that can identify virulent strains are not available. Therefore, discrimination between virulent isolates and carriage isolates typically not associated with disease, is currently not possible. We collected tonsillar S. suis isolates from 6 herds not previously diagnosed with S. suis infections, and clinical S. suis isolates of previously diseased pigs. We confirmed the virulence of a virulent type strain and one representative clinical isolate, and the lack of virulence of two carriage isolates, in a pig infection model. Phylogenetic analysis of whole genome sequences of 124 isolates resulted in 10 groups, of which two were almost uniquely populated by clinical isolates. The population structure of S. suis serotype 9 appears highly diverse. However, analysis of the capsule loci sequences showed variation in a single region which fully correlated with a virulent genotype. Transmission electron microscopy suggested differences in capsule thickness between carriage and clinical genotypes. In conclusion, we found that that the S. suis serotype 9 population in the Netherlands is diverse. A distinct virulence-associated lineage was identified and could be discriminated based on the capsule locus sequence. Whilst the difference in virulence cannot be directly attributed to the DNA sequence, the correlation of capsule locus sequence with virulence could be used in the development of diagnostic tests to identify potential virulent S. suis serotype 9 in pigs.

Limited contribution of non-intensive chicken farming to ESBL-producing Escherichia coli colonization in humans in Vietnam : an epidemiological and genomic analysis
Nguyen, Vinh Trung ; Jamrozy, Dorota ; Matamoros, Sébastien ; Carrique-Mas, Juan J. ; Ho, Huynh Mai ; Thai, Quoc Hieu ; Nguyen, Thi Nhu Mai ; Wagenaar, Jaap A. ; Thwaites, Guy ; Parkhill, Julian ; Schultsz, Constance ; Ngo, Thi Hoa - \ 2019
Journal of Antimicrobial Chemotherapy 74 (2019)3. - ISSN 0305-7453 - p. 561 - 570.

OBJECTIVES: To investigate the risk of colonization with ESBL-producing Escherichia coli (ESBL-Ec) in humans in Vietnam associated with non-intensive chicken farming. METHODS: Faecal samples from 204 randomly selected farmers and their chickens, and from 306 age- and sex-matched community-based individuals who did not raise poultry were collected. Antimicrobial usage in chickens and humans was assessed by medicine cabinet surveys. WGS was employed to obtain a high-resolution genomic comparison between ESBL-Ec isolated from humans and chickens. RESULTS: The adjusted prevalence of ESBL-Ec colonization was 20.0% (95% CI 10.8%-29.1%) and 35.2% (95% CI 30.4%-40.1%) in chicken farms and humans in Vietnam, respectively. Colonization with ESBL-Ec in humans was associated with antimicrobial usage (OR = 2.52, 95% CI = 1.08-5.87) but not with involvement in chicken farming. blaCTX-M-55 was the most common ESBL-encoding gene in strains isolated from chickens (74.4%) compared with blaCTX-M-27 in human strains (47.0%). In 3 of 204 (1.5%) of the farms, identical ESBL genes were detected in ESBL-Ec isolated from farmers and their chickens. Genomic similarity indicating recent sharing of ESBL-Ec between chickens and farmers was found in only one of these farms. CONCLUSIONS: The integration of epidemiological and genomic data in this study has demonstrated a limited contribution of non-intensive chicken farming to ESBL-Ec colonization in humans in Vietnam and further emphasizes the importance of reducing antimicrobial usage in both human and animal host reservoirs.

Streptococcal Adhesin P (SadP) contributes to Streptococcus suis adhesion to the human intestinal epithelium
Ferrando, Maria Laura ; Willemse, Niels ; Zaccaria, Edoardo ; Pannekoek, Yvonne ; Ende, Arie van der; Schultsz, Constance - \ 2017
PLoS ONE 12 (2017)4. - ISSN 1932-6203

Background Streptococcus suis is a zoonotic pathogen, causing meningitis and septicemia. We previously demonstrated that the gastrointestinal tract (GIT) is an entry site for zoonotic S. suis infection. Here we studied the contribution of Streptococcal adhesin Protein (SadP) to hostpathogen interaction at GIT level. Methods SadP expression in presence of Intestinal Epithelial Cells (IEC) was compared with expression of other virulence factors by measuring transcript levels using quantitative Real Time PCR (qRT-PCR). SadP variants were identified by phylogenetic analysis of complete DNA sequences. The interaction of SadP knockout and complementation mutants with IEC was tested in vitro. Results Expression of sadP was significantly increased in presence of IEC. Sequence analysis of 116 invasive strains revealed five SadP sequence variants, correlating with genotype. SadP1, present in zoonotic isolates of clonal complex 1, contributed to binding to both human and porcine IEC and translocation across human IEC. Antibodies against the globotriaosylceramide Gb3/CD77 receptor significantly inhibited adhesion to human IEC. Conclusion SadP is involved in the host-pathogen interaction in the GIT. Differences between SadP variants may determine different affinities to the Gb3/CD77 host-receptor, contributing to variation in adhesion capacity to host IEC and thus to S. suis zoonotic potential.

Zoonotic transmission of mcr-1 colistin resistance gene from small-scale poultry farms, Vietnam
Trung, Nguyen Vinh ; Matamoros, Sébastien ; Carrique-Mas, Juan J. ; Nghia, Nguyen Huu ; Nhung, Nguyen Thi ; Chieu, Tran Thi Bich ; Mai, Ho Huynh ; Rooijen, Willemien van; Campbell, James ; Wagenaar, Jaap A. ; Hardon, Anita ; Mai, Nguyen Thi Nhu ; Hieu, Thai Quoc ; Thwaites, Guy ; Jong, Menno D. de; Schultsz, Constance ; Hoa, Ngo Thi - \ 2017
Emerging Infectious Diseases 23 (2017)3. - ISSN 1080-6040 - p. 529 - 532.
We investigated the consequences of colistin use in backyard chicken farms in Vietnam by examining the prevalence of mcr-1 in fecal samples from chickens and humans. Detection of mcr-1-carrying bacteria in chicken samples was associated with colistin use and detection in human samples with exposure to mcr-1-positive chickens.
Non-Typhoidal Salmonella Colonization in Chickens and Humans in the Mekong Delta of Vietnam
Trung, N.V. ; Carrique-Mas, J.J. ; Nghia, N.H. ; Tu, L.T.P. ; Mai, H.H. ; Tuyen, H.T. ; Campbell, J. ; Nhung, N.T. ; Nhung, H.N. ; Minh, P.V. ; Chieu, T.T.B. ; Hieu, T.Q. ; Mai, N.T.N. ; Baker, S. ; Wagenaar, J.A. ; Hoa, N.T. ; Schultsz, C. - \ 2017
Zoonoses and Public Health 64 (2017)2. - ISSN 1863-1959 - p. 94 - 99.
antimicrobial resistance - chickens - colonization - humans - Non-typhoidal Salmonella - Vietnam
Salmonellosis is a public health concern in both the developed and developing countries. Although the majority of human non-typhoidal Salmonella enterica (NTS) cases are the result of foodborne infections or person-to-person transmission, NTS infections may also be acquired by environmental and occupational exposure to animals. While a considerable number of studies have investigated the presence of NTS in farm animals and meat/carcasses, very few studies have investigated the risk of NTS colonization in humans as a result of direct animal exposure. We investigated asymptomatic NTS colonization in 204 backyard chicken farms, 204 farmers and 306 matched individuals not exposed to chicken farming, in southern Vietnam. Pooled chicken faeces, collected using boot or handheld swabs on backyard chicken farms, and rectal swabs from human participants were tested. NTS colonization prevalence was 45.6%, 4.4% and 2.6% for chicken farms, farmers and unexposed individuals, respectively. Our study observed a higher prevalence of NTS colonization among chicken farmers (4.4%) compared with age-, sex- and location- matched rural and urban individuals not exposed to chickens (2.9% and 2.0%). A total of 164 chicken NTS strains and 17 human NTS strains were isolated, and 28 serovars were identified. Salmonella Weltevreden was the predominant serovar in both chickens and humans. NTS isolates showed resistance (20–40%) against tetracycline, chloramphenicol, sulfamethoxazole-trimethoprim and ampicillin. Our study reflects the epidemiology of NTS colonization in chickens and humans in the Mekong delta of Vietnam and emphasizes the need of larger, preferably longitudinal studies to study the transmission dynamics of NTS between and within animal and human host populations.
Colonization of Enteroaggregative Escherichia coli and Shiga toxin-producing Escherichia coli in chickens and humans in southern Vietnam
Trung, Nguyen Vinh ; Nhung, Hoang Ngoc ; Carrique-Mas, Juan J. ; Mai, Ho Huynh ; Tuyen, Ha Thanh ; Campbell, James ; Nhung, Nguyen Thi ; Minh, Pham Van; Wagenaar, Jaap A. ; Mai, Nguyen Thi Nhu ; Hieu, Thai Quoc ; Schultsz, Constance ; Hoa, Ngo Thi - \ 2016
BMC Microbiology 16 (2016)1. - ISSN 1471-2180
Chicken - E. coli - EAEC - Humans - STEC - Vietnam

Background: Enteroaggregative (EAEC) and Shiga-toxin producing Escherichia coli (STEC) are a major cause of diarrhea worldwide. E. coli carrying both virulence factors characteristic for EAEC and STEC and producing extended-spectrum beta-lactamase caused severe and protracted disease during an outbreak of E. coli O104:H4 in Europe in 2011. We assessed the opportunities for E. coli carrying the aggR and stx genes to emerge in 'backyard' farms in south-east Asia. Results: Faecal samples collected from 204 chicken farms; 204 farmers and 306 age- and gender-matched individuals not exposed to poultry farming were plated on MacConkey agar plates with and without antimicrobials being supplemented. Sweep samples obtained from MacConkey agar plates without supplemented antimicrobials were screened by multiplex PCR for the detection of the stx1, stx2 and aggR genes. One chicken farm sample each (0.5 %) contained the stx1 and the aggR gene. Eleven (2.4 %) human faecal samples contained the stx1 gene, 2 samples (0.4 %) contained stx2 gene, and 31 (6.8 %) contained the aggR gene. From 46 PCR-positive samples, 205 E. coli isolates were tested for the presence of stx1, stx2, aggR, wzx O104 and fliC H4 genes. None of the isolates simultaneously contained the four genetic markers associated with E. coli O104:H4 epidemic strain (aggR, stx2, wzx O104 and fliC H4 ). Of 34 EAEC, 64.7 % were resistant to 3rd-generation cephalosporins. Conclusion: These results indicate that in southern Vietnam, the human population is a more likely reservoir of aggR and stx gene carrying E. coli than the chicken population. However, conditions for transmission of isolates and/or genes between human and animal reservoirs resulting in the emergence of highly virulent E. coli strains are still favorable, given the nature of'backyard' farms in Vietnam.

An emerging zoonotic clone in the Netherlands provides clues to virulence and zoonotic potential of Streptococcus suis
Willemse, N. ; Howell, K.J. ; Weinert, L.A. ; Heuvelink, A. ; Pannekoek, Y. ; Wagenaar, J.A. ; Smith, H.E. ; Ende, A. Van Der; Schultsz, C. - \ 2016
Scientific Reports 6 (2016). - ISSN 2045-2322

Streptococcus suis is a zoonotic swine pathogen and a major public health concern in Asia, where it emerged as an important cause of bacterial meningitis in adults. While associated with food-borne transmission in Asia, zoonotic S. suis infections are mainly occupational hazards elsewhere. To identify genomic differences that can explain zoonotic potential, we compared whole genomes of 98 S. suis isolates from human patients and pigs with invasive disease in the Netherlands, and validated our observations with 18 complete and publicly available sequences. Zoonotic isolates have smaller genomes than non-zoonotic isolates, but contain more virulence factors. We identified a zoonotic S. suis clone that diverged from a non-zoonotic clone by means of gene loss, a capsule switch, and acquisition of a two-component signalling system in the late 19th century, when foreign pig breeds were introduced. Our results indicate that zoonotic potential of S. suis results from gene loss, recombination and horizontal gene transfer events.

Prevalence and risk factors for carriage of antimicrobial-resistant Escherichia coli on household and small-scale chicken farms in the Mekong Delta of Vietnam
Nguyen, Vinh Trung ; Carrique-Mas, Juan J. ; Ngo, Thi Hoa ; Ho, Huynh Mai ; Ha, Thanh Tuyen ; Campbell, James I. ; Nguyen, Thi Nhung ; Hoang, Ngoc Nhung ; Pham, Van Minh ; Wagenaar, Jaap A. ; Hardon, Anita ; Thai, Quoc Hieu ; Schultsz, Constance - \ 2015
Journal of Antimicrobial Chemotherapy 70 (2015)7. - ISSN 0305-7453 - p. 2144 - 2152.
Antimicrobial resistance - Antimicrobial use - Poultry - Treatment incidence

Objectives: To describe the prevalence of antimicrobial resistance among commensal Escherichia coli isolates on household and small-scale chicken farms, common in southern Vietnam, and to investigate the association of antimicrobial resistance with farming practices and antimicrobial usage. Methods: We collected data on farming and antimicrobial usage from 208 chicken farms. E. coli was isolated from boot swab samples using MacConkey agar (MA) and MA with ceftazidime, nalidixic acid or gentamicin. Isolates were tested for their susceptibility to 11 antimicrobials and for ESBL production. Risk factor analyses were carried out, using logistic regression, at both the bacterial population and farm levels. Results: E. coli resistant to gentamicin, ciprofloxacin and third-generation cephalosporins was detected on 201 (96.6%), 191 (91.8%) and 77 (37.0%) of the farms, respectively. Of the 895 E. coli isolates, resistance to gentamicin, ciprofloxacin and third-generation cephalosporins was detected in 178 (19.9%), 291 (32.5%) and 29 (3.2%) of the isolates, respectively. Ciprofloxacin resistance was significantly associated with quinolone usage (OR = 2.26) and tetracycline usage (OR = 1.70). ESBL-producing E. coli were associated with farms containing fish ponds (OR = 4.82). Conclusions: Household and small farms showed frequent antimicrobial usage associated with a high prevalence of resistance to the most commonly used antimicrobials. Given the weak biocontainment, the high prevalence of resistant E. coli could represent a risk to the environment and to humans.

Host-pathogen interaction at the intestinal mucosa correlates with zoonotic potential of Streptococcus suis
Ferrando, Maria Laura ; Greeff, Astrid De; Rooijen, W.J.M. Van; Stockhofe-Zurwieden, Norbert ; Nielsen, Jens ; Wichgers Schreur, P.J. ; Pannekoek, Yvonne ; Heuvelink, Annet ; Ende, Arie Van Der; Smith, Hilde ; Schultsz, Constance - \ 2015
The Journal of Infectious Diseases 212 (2015)1. - ISSN 0022-1899 - p. 95 - 105.
clonal complex - intestinal translocation - piglets. - serotype - Streptococcus suis - tight junctions - zoonotic infections

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.

Latest developments on Streptococcus suis: an emerging zoonotic pathogen: part 1
Segura, M. ; Zheng, H. ; Greeff, A. de; Gao, G.F. ; Grenier, D. ; Jiang, Y. ; Chengping, L. ; Maskell, D. ; Oishi, K. ; Okura, M. ; Osawa, R. ; Schultsz, C. ; Schwerk, C. ; Sekizaki, T. ; Smith, H. ; Srimanote, P. ; Takamatsu, D. ; Tang, J. ; Tenenbaum, T. ; Tharavichitkul, P. ; Hoa, N.T. ; Valentin-Weigand, P. ; Wells, J.M. ; Wertheim, H. ; Zhu, B. ; Xu, J. ; Gottschalk, M. - \ 2014
Future Microbiology 9 (2014)4. - ISSN 1746-0913 - p. 441 - 444.
serotype-2 - thailand - infection - diversity
The first international workshop on Streptococcus suis, which is an important swine pathogen and emerging zoonotic agent, took place in Beijing, jointly organized by the Faculty of Veterinary Medicine, University of Montreal, Canada and the National Institute for Communicable Disease Control and Prevention, China CDC. The aim of the meeting was to gather together, for the first time, more than 80 researchers working on S. suis, from countries including China, Canada, Japan, The Netherlands, Germany, Thailand, the UK and Vietnam. This article, the first of a two-part report on this First International Workshop, reviews current aspects of the epidemiology and population genomics of S. suis, covers public health concerns and discusses questions about S. suis serotyping and molecular diagnostics.
Latest developments on Streptococcus suis: an emerging zoonotic pathogen: part 2
Segura, M. ; Zheng, H. ; Greeff, A. de; Gao, G.F. ; Gremier, D. ; Jiang, Y. ; Chengping, L. ; Maskell, D. ; Oishi, K. ; Okura, M. ; Osawa, R. ; Schultsz, C. ; Schwerk, C. ; Sekizaki, T. ; Smith, H. ; Srimanote, P. ; Takamatsu, D. ; Tang, J. ; Tenenbaum, T. ; Tharavichitkul, P. ; Hoa, N.T. ; Valentin-Weigand, P. ; Wells, J.M. ; Wertheim, H. ; Zhu, B. ; Xu, J. ; Gottschalk, M. - \ 2014
Future Microbiology 9 (2014)5. - ISSN 1746-0913 - p. 587 - 591.
cerebrospinal fluid barrier - plexus epithelial-cells - in-vitro - bacterial interactions - swine pathogen - serotype-2 - infection - diversity - virulence - release
This second and final chapter of the report on the First International Workshop on Streptococcus suis follows on from Part 1, published in the April 2014, volume 9, issue 4 of Future Microbiology. S. suis is a swine pathogen and a zoonotic agent afflicting people in close contact with infected pigs or pork meat. Although sporadic cases of human infections had been reported worldwide, deadly S. suis outbreaks emerged in Asia. The severity of the disease underscores the lack of knowledge on the virulence and zoonotic evolution of this human-infecting agent. The pathogenesis of the infection, interactions with host cells and new avenues for treatments were among the topics discussed during the First International Workshop on S. suis (China 2013).
Genetic diversity of Streptococcus suis isolates as determined by comparative genome hybridization
Greeff, A. de; Wisselink, H.J. ; Bree, F.M. de; Schultsz, C. ; Baums, C.G. ; Ngo Thi, Hoa ; Stockhofe-Zurwieden, N. ; Smith, H.E. - \ 2011
BMC Microbiology 11 (2011). - ISSN 1471-2180 - 15 p.
germ-free pigs - hyaluronate lyase - capsular type-2 - binding protein - virulence - identification - serotype-2 - strains - expression - purification
Background Streptococcus suis is a zoonotic pathogen that causes infections in young piglets. S. suis is a heterogeneous species. Thirty-three different capsular serotypes have been described, that differ in virulence between as well as within serotypes.Results In this study, the correlation between gene content, serotype, phenotype and virulence among 55 S. suis strains was studied using Comparative Genome Hybridization (CGH). Clustering of CGH data divided S. suis isolates into two clusters, A and B. Cluster A isolates could be discriminated from cluster B isolates based on the protein expression of extracellular factor (EF). Cluster A contained serotype 1 and 2 isolates that were correlated with virulence. Cluster B mainly contained serotype 7 and 9 isolates. Genetic similarity was observed between serotype 7 and serotype 2 isolates that do not express muramidase released protein (MRP) and EF (MRP-EF-), suggesting these isolates originated from a common founder. Profiles of 25 putative virulence-associated genes of S. suis were determined among the 55 isolates. Presence of all 25 genes was shown for cluster A isolates, whereas cluster B isolates lacked one or more putative virulence genes. Divergence of S. suis isolates was further studied based on the presence of 39 regions of difference. Conservation of genes was evaluated by the definition of a core genome that contained 78% of all ORFs in P1/7.Conclusions In conclusion, we show that CGH is a valuable method to study distribution of genes or gene clusters among isolates in detail, yielding information on genetic similarity, and virulence traits of S. suis isolates.
Rapid Evolution of Virulence and Drug Resistance in the Emerging Zoonotic Pathogen Streptococcus suis
Holden, M.T.G. ; Hauser, H. ; Sanders, M. ; Hoa Ngo, Thi ; Cherevach, I. ; Cronin, A. ; Goodhead, I. ; Mungall, K. ; Quail, M.A. ; Price, C. ; Rabbinowitsch, E. ; Sharp, S. ; Croucher, N. ; Chieu, Tran Bich ; Nguyen, Thi Hoang Mai ; To, Song Diep ; Nguyen, Tran Chinh ; Kehoe, M. ; Leigh, J.A. ; Ward, P.N. ; Dowson, C.G. ; Whatmore, A.M. ; Chanter, N. ; Iversen, P. ; Gottschalk, M. ; Slater, J.D. ; Smith, H.E. ; Spratt, B.G. ; Jianguo, Xu ; Changyun, Ye ; Bentley, S. ; Barrell, B.G. ; Schultsz, C. ; Maskell, D.J. ; Parkhill, J. - \ 2009
PLoS ONE (2009). - ISSN 1932-6203 - 7 p.
Background - Streptococcus suis is a zoonotic pathogen that infects pigs and can occasionally cause serious infections in humans. S. suis infections occur sporadically in human Europe and North America, but a recent major outbreak has been described in China with high levels of mortality. The mechanisms of S. suis pathogenesis in humans and pigs are poorly understood. Methodology/Principal Findings - The sequencing of whole genomes of S. suis isolates provides opportunities to investigate the genetic basis of infection. Here we describe whole genome sequences of three S. suis strains from the same lineage: one from European pigs, and two from human cases from China and Vietnam. Comparative genomic analysis was used to investigate the variability of these strains. S. suis is phylogenetically distinct from other Streptococcus species for which genome sequences are currently available. Accordingly, ~40% of the ~2 Mb genome is unique in comparison to other Streptococcus species. Finer genomic comparisons within the species showed a high level of sequence conservation; virtually all of the genome is common to the S. suis strains. The only exceptions are three ~90 kb regions, present in the two isolates from humans, composed of integrative conjugative elements and transposons. Carried in these regions are coding sequences associated with drug resistance. In addition, small-scale sequence variation has generated pseudogenes in putative virulence and colonization factors. Conclusions/Significance - The genomic inventories of genetically related S. suis strains, isolated from distinct hosts and diseases, exhibit high levels of conservation. However, the genomes provide evidence that horizontal gene transfer has contributed to the evolution of drug resistance.
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