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Volume 30, Number 3—March 2024
CME ACTIVITY - Synopsis

Molecular Epidemiology of Underreported Emerging Zoonotic Pathogen Streptococcus suis in Europe

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Methods
Results
Discussion
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Author affiliations: Amsterdam University Medical Center, University of Amsterdam, Amsterdam, the Netherlands (J. Brizuela, T.J. Roodsant, Q. Hasnoe, B.C.L. van der Putten, I.G.A de Beer-Schuurman, K.C.H. van der Ark, C. Schultsz); National Institute for Public Health, Prague, Czech Republic (J. Kozakova); Statens Serum Institut, Copenhagen, Denmark (H.-C. Slotved); University Hospital RWTH Aachen, Aachen, Germany (M. van der Linden); National Medicines Institute, Warsaw, Poland (E. Sadowy); Carlos III Health Institute, Madrid, Spain (J.A. Sáez-Nieto); UK Health Security Agency, London, UK (V.J. Chalker).

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Introduction

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Release date: February 22, 2024; Expiration date: February 22, 2025
Learning Objectives

Upon completion of this activity, participants will be able to:

  • Assess the worldwide epidemiology of Streptococcus suis.

  • Distinguish the most common serotype of S. suis associated with zoonotic infection.

  • Analyze clinical syndromes associated with infection with S. suis.

  • Evaluate genetic characteristics of S. suis isolates in the current study.

CME Editor

Tony Pearson-Clarke, MS, Technical Writer/Editor, Emerging Infectious Diseases. Disclosure: Tony Pearson-Clarke, MS, has no relevant financial relationships.

CME Author

Charles P. Vega, MD, Health Sciences Clinical Professor of Family Medicine, University of California, Irvine School of Medicine, Irvine, California. Disclosure: Charles P. Vega, MD, has the following relevant financial relationships: consultant or advisor for Boehringer Ingelheim Pharmaceuticals, Inc.; GlaxoSmithKline.

Authors

Jaime Brizuela, MRes; Thomas J. Roodsant, PhD; Qureisha Hasnoe, MSc; Boas C.L. van der Putten, PhD; Jana Kozakova, MD; Hans-Christian Slotved, PhD, DMSc; Mark van der Linden, PhD; Ilse G.A. de Beer-Schuurman, BSc; Ewa Sadowy, PhD, MD; Juan Antonio Sáez-Nieto, PhD; Victoria J. Chalker, PhD; Kees C.H. van der Ark, PhD; Constance Schultsz, PhD, MD.

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Abstract

Streptococcus suis, a zoonotic bacterial pathogen circulated through swine, can cause severe infections in humans. Because human S. suis infections are not notifiable in most countries, incidence is underestimated. We aimed to increase insight into the molecular epidemiology of human S. suis infections in Europe. To procure data, we surveyed 7 reference laboratories and performed a systematic review of the scientific literature. We identified 236 cases of human S. suis infection from those sources and an additional 87 by scanning gray literature. We performed whole-genome sequencing to type 46 zoonotic S. suis isolates and combined them with 28 publicly available genomes in a core-genome phylogeny. Clonal complex (CC) 1 isolates accounted for 87% of typed human infections; CC20, CC25, CC87, and CC94 also caused infections. Emergence of diverse zoonotic clades and notable severity of illness in humans support classifying S. suis infection as a notifiable condition.

Streptococcus suis is an opportunistic bacterial porcine pathogen that can cause severe disease in humans, most commonly meningitis and sepsis (1). Human S. suis infections occur both through direct contact with infected pigs and consumption of undercooked contaminated pork (2). Human S. suis infections have become endemic in Thailand and Vietnam, driven by consumption of traditional raw pork dishes (1), and S. suis has caused multiple outbreaks in humans with high levels of illness and death in China and Thailand (3). In Europe, S. suis infections are considered an occupational hazard, mainly occurring among persons with skin lesions working closely with pigs or pork products (1). Human infections in Europe account for ≈10% of the global prevalence, but incidence in Europe is likely underestimated because S. suis infections are not a notifiable disease (4). Togo, Madagascar, Chile, and Indonesia have recently reported zoonotic S. suis infections, meaning all continents except Antarctica have now reported human infections (1,5–8).

S. suis is classified into 29 distinct serotypes based on its capsular polysaccharide, as well as 27 novel serotypes based on novel capsular polysaccharide loci. In addition, sporadic infections caused by serotypes 4, 5, 7, 9, 16, 21, 24, and 31 have been reported (3,9–11). S. suis genotypes are classified on the basis of sequence types (STs) determined through multilocus sequence typing (MLST), which are grouped into clonal complexes (CCs) (12). CC1 with a serotype 2 capsule is the main lineage causing human infections and has expanded worldwide (3). Emerging zoonotic lineages, such as CC20, which emerged from CC16 in the Netherlands after acquiring a serotype 2 capsule, have also been described (13).

We aimed to increase insight into the epidemiology of human S. suis infections in Europe and to assess the bacterial population structure and diversity of zoonotic S. suis clades (1). We assessed the frequency of human S. suis infections in Europe through a survey of reference laboratories in top pig-rearing countries in Europe, performed a systematic literature review and explored the gray literature (social media, news accounts, and government reports). In addition, we reconstructed a representative phylogeny of zoonotic S. suis isolates in Europe.

This study was not reviewed by an ethics review board, because it was based on anonymized surveillance data. In accordance with Dutch law, approval from a medical ethics committee was not deemed necessary because case-patients were not subject to any actions or rules of conduct. We did not obtain informed consent because our data collection processes were exempted under exceptions formulated in the Dutch Implementation of the European General Data Protection Regulation Act (2016/679).

Methods

Survey

We contacted national reference laboratories in 10 countries in Europe (Czech Republic, Denmark, France, Germany, Hungary, Italy, the Netherlands, Poland, Spain, and the United Kingdom) that included S. suis infections within their scope. We asked those laboratories to retrospectively collect data on cases of human S. suis infection during 1990–2018 because most human S. suis infections have been reported since 1990. We asked participating laboratories to complete a questionnaire collecting patient metadata and bacterial typing and metadata. Anonymized patient metadata were age, sex, clinical signs, and occupation. Bacterial typing encompassed serotype, sequence type (ST), and available whole-genome sequences. Bacterial metadata were date of isolation, source of isolation, and method of identification. In addition, we requested in the questionnaire that reference laboratories share their isolates for further genomic analysis (Appendix).

Systematic Review

We performed a systematic review according to PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) guidelines (14) to identify cases of human S. suis infections in Europe in articles published from 1990 (survey start date) through 2022. We screened PubMed, Web of Science, and Scopus for key terms—S. suis, human, and ≥1 country in Europe (as defined by the World Health Organization)—in the titles or abstracts of articles published before April 1, 2022 (Appendix). We removed duplicate references by using Zotero version 6.0.8 (https://www.zotero.org) and manual checking. We included studies containing data on human S. suis isolates or case reports describing human S. suis infections in Europe; we extracted patient and bacterial metadata for further analysis. We excluded studies that did not include data on zoonotic S. suis isolates or human infections, reported isolates not collected in Europe, did not publish original data, were published before 1990, or lacked information on the origin of isolates (Figure 1). To avoid duplication, we excluded from the systematic review isolates reported in both the survey and an article; in addition, if an isolate appeared in multiple articles, we included data only from the original article.

Grey Literature Search

Because S. suis is not a notifiable disease, there are no guidelines for reporting such infections. To identify additional cases, we performed a broad scan of gray literature to capture cases of human S. suis infections in Europe not identified in the scientific literature or the survey. However, we distinguished cases we identified in the survey, literature review, and official reports from unreported cases (all other cases). We searched X (previously Twitter) and the Google news section using the terms S. suis, infection, and human in Dutch, English, French, German, Italian, Portuguese, and Spanish. To complement those data, we scanned ministry of health websites from France, Germany, Italy, the Netherlands, Portugal, Spain, and the United Kingdom for reports on zoonotic bacterial infections related to human S. suis infections. To avoid duplication, we compared metadata, when available, with isolate data from the survey and systematic review.

In Silico Typing and Phylogenetic Analysis

We included 74 genomes for whole-genome sequencing (WGS) analysis, 67 from the survey (46 sequenced during this investigation and 21 previously sequenced) and 7 from the systematic review (Appendix Figure 1). We used MLST version 2.19.0 (https://github.com/tseemann/mlst) with the PubMLST database (https://pubmlst.org) to type the MLST profiles of the draft genomes. We submitted profiles for novel STs to PubMLST. We performed in silico serotyping by feeding processed Illumina reads into the S. suis serotyping pipeline (15). We reconstructed a core genome single-nucleotide polymorphism (SNP) phylogeny and using Panaroo version 1.3.0 (16) to reconstruct the pangenome and align the core genome. We calculated the number of constant sites in the core genome alignment with SNP-sites version 2.5.1 (17) using the flag “-C.” We reconstructed the maximum-likelihood (ML) phylogeny by running IQ-TREE version 2.0.3 (18) with 1,000 bootstraps and used the general time-reversible plus gamma model with the flag “-fconst” to include the constant sites from SNP-sites. We investigated the presence of 46 accessory genes previously found to be overrepresented in zoonotic isolates (human-pig prevalence ratio >2) using ABRicate (https://github.com/tseemann/abricate) with a custom database and a minimum protein identity and coverage of 80%. We visualized the resulting gene presence/absence matrix in Phandango (19,20). Raw Illumina sequences can be found in the National Center for Biotechnology Information Short Read Archive (BioProject PRJNA853715). Genome assemblies have been deposited in GenBank and are available under the same BioProject number (Appendix Table 7).

Results

Geographic Distribution of Reported Human S. suis Infections across Europe, 1990–2022

Of 10 reference laboratories invited to participate in the survey, 7 laboratories (Spain, Germany, Netherlands, Denmark, Czech Republic, Poland, and United Kingdom) responded and reported 107 unique cases of human S. suis infections (Appendix Table 2). In the systematic review, of 119 screened titles and abstracts, we selected 53 articles mentioning human S. suis infections in Europe for full-text reading. In addition, we included 29 studies identified by screening reference lists (Figure 1). In total, we extracted data from 129 cases of human S. suis infections reported in 69 research articles (Figure 1; Appendix Table 3). Combining both sources, we identified 236 unique cases of human S. suis infections across Europe during 1990–2022. Germany, Spain, and the Netherlands, the top pig-rearing countries in Europe (21), reported 114/236 (48%) of the cases (Figure 2). Furthermore, 203/236 (86%) of the reported cases originated from just 8 countries (Germany, Spain, the Netherlands, Denmark, Hungary, France, Poland, and the Czech Republic), 6 of which participated in the survey study; sporadic cases reported from 8 additional countries in Europe completed the dataset.

Epidemiology of Human S. suis Infections in Europe

Most patients were middle-aged men (Table 1). Of patients with a reported clinical syndrome, meningitis was the main clinical syndrome observed in both the survey (59/71 [83%]) and systematic review (59/86 [68%]), followed by sepsis, which affected 15/71 (21%) in the survey and 21/86 (24%) in the systematic review. Additional clinical signs and symptoms included hearing loss (n = 22), endocarditis (n = 6), and spondylodiscitis (n = 3); 11 patients died. Patient occupation was described as a potential risk factor in 19 cases in the survey and 72 cases in the systematic review (Table 1). Most infections, 78/92 (85%) in the survey and 43/48 (90%) in the systematic review, were caused by serotype 2 isolates, followed by serotype 14 isolates (Table 2). Most isolates (76/87 [78%] in the survey and 14/16 [88%] in the systematic review) belonged to zoonotic lineage CC1. In addition, 11/87 (13%) infections in the survey and 1 in the systematic review were caused by CC20 lineage isolates.

Year of isolation was collected for only 44/129 (34%) isolates from cases in the systematic review (Appendix Table 3). Nonetheless, average number of cases per year in the systematic review and survey increased after 1999, from 2.7 during 1990–1999 to 5.7 during 2000–2009 and 5.0 during 2010–2019 (Appendix Figure 2). Moreover, we calculated crude estimates of S. suis incidence in the at-risk population in 6 (Czech Republic, Germany, Hungary, the Netherlands, Poland, and Spain) countries with >5 cases reported in the survey or literature review during 2005–2013. We defined the population at risk as the proportion of the agricultural census involved in pig specialized holdings with a 10% upper margin to account for butchers, hunters, slaughterhouse workers, lorry drivers, and meat factory workers. Incidence range in the at-risk population for those 6 countries during 2005–2013 averaged 0.161–4.945 cases/100,000 persons; Poland had the lowest incidence and the Netherlands the highest (Appendix Table 6).

Scan of Grey Literature

Because no centralized surveillance system exists for human S. suis infection and the disease is not notifiable in any country in Europe, the number of infections in Europe has likely been underestimated. We scanned gray literature in search of cases not identified through either the survey or systematic review. Public Health England (now the UK Health Security Agency) included human S. suis infections in their annual zoonosis official reports collected from the Veterinary Diagnostic Analysis database of the Animal and Plant Health Agency (22). During 1991–2017, those reports recorded 61 human S. suis infections in the United Kingdom, 10 times the number of cases identified from the survey and systematic review combined (6 cases). However, those 61 cases might overlap with cases from the survey and systematic review because neither metadata nor identification method were provided (Appendix Table 4). The Netherlands Reference Laboratory for Bacterial Meningitis surveyed 57 medical microbiology laboratories in the Netherlands during 2013 with the aim of identifying cases not reported to the reference laboratory and collected an additional 25 unique cases isolated during 1990–2011 (Appendix Table 5) (23). We also found 1 case of S. suis meningitis in a butcher in Spain that was reported through X (24).

Population Structure of Zoonotic S. suis in Europe

To study the population structure of zoonotic S. suis isolates in Europe, we reconstructed a core-genome SNP phylogeny of 74 strains from 10 different countries (Figure 3). We identified 5 novel STs, 1660, 1602, 1663, 1707, and 1708. Most strains were part of the major zoonotic clade CC1, which has spread across Europe; >1 strain from each country included in the phylogeny was CC1. Most of the CC1 strains had a serotype 2 capsule, and a small subset possessed the structurally similar serotype 14 capsule (25). We distinguished 2 subclades within CC1 in a genome-wide SNP phylogeny (Appendix Figure 3). The other zoonotic clades appeared to be more geographically restricted. For example, most of the CC20 strains were isolated in the Netherlands, where the lineage is thought to have emerged (13). Two additional CC20 strains were isolated in Germany, forming a serotype 5 outgroup to clonal CC20 serotype 2 strains from the Netherlands. All CC25 strains were recovered in the Czech Republic. The 3 ST25 serotype 2 strains had only 73–116 SNPs across their core genomes, whereas the ST29 strain differed from the ST25 strains by 4,353–4,416 SNPs and had a serotype 7 capsule. Strains from the CC87 clade were identified in Germany and the Czech Republic and possessed a serotype 2 capsule. The 3 strains from Germany were ST19 and highly similar (81–118 SNPs), whereas the strain from the Czech Republic had novel ST1660 and differed from the ST19 clade by 9,411–9,434 SNPs.

CC1 and CC20 Isolates and Genes Associated with Zoonotic Potential

Overall, strains from clades CC1 and CC20 had a higher number of accessory genes overrepresented in zoonotic isolates than did strains from lineages CC25, CC87, and CC94 (Figure 4). Most genes associated with zoonoses were present in >1 of the lineages; only the 2-component signal transduction system nisK/R and the fimbria-like adhesin sssP1 genes were absent from the dataset (Figure 4). Of note, despite its role in adhesion and virulence being extensively studied, muramidase-related protein (mrp) was absent from the CC20 clade (26). Factor H binding protein (fhb), associated with binding factor H and increased translocation across the blood/brain barrier (27), was present only in CC1 strains. Differences could be observed within CC1 sublineages; 1 subclade had an additional factor H binding protein (fhbp). Last, suilysin (sly), a pore-forming hemolysin with a clear role in pathogenesis (20), was present in all clades except CC25, which instead carried the hyaluronate lysin A (hylA), associated with reduced virulence (Figure 4) (28).

Discussion

Despite having caused multiple outbreaks with high levels of illness and death in the past decade and reports of new zoonotic lineages arising on different continents, S. suis remains largely excluded from disease surveillance programs (29). Although neither carriage in healthy humans nor human-to-human transmission of S. suis have been reported to date, systematic surveillance is needed to follow the evolutionary trends of this pathogen in humans and pigs, the main reservoir from which zoonotic lineages emerge (2).

Our study included some potential sources of bias. Differences in number of cases between countries should not be attributed only to the size of pig populations. Other factors, such as government policy and disease monitoring and reporting, could contribute to observed differences in reported human S. suis cases between countries. For instance, although France has one of the largest pig populations in Europe, only 7 human cases have been reported. In contrast, although they have smaller pig populations, the Czech Republic reported 18 and Poland 22 cases (Figure 2) (30). The distribution of clinical symptoms aligns with previous regional and global estimates (1). However, clinical data gathered in the survey were potentially biased toward reporting meningitis because several of the surveyed laboratories are reference laboratories for bacterial meningitis (Table 1) (1). The systematic review yielded diverse article types (e.g., case reports, surveillance studies) and inconsistent quality of reported metadata. Often, year of isolation and bacterial typing was absent, making it difficult to establish meaningful time trends in the emergence of zoonotic S. suis in Europe. Finally, the time frames of the survey, 1990–2018, and systematic review, 1990–2022, were not identical.

The serotype 2 capsule is linked with zoonotic S. suis infections, and most worldwide S. suis cases are caused by serotype 2 (4). While investigating the emergence of the zoonotic clade CC20, 1 study (13) proposed that capsule-switching events leading to acquisition of a serotype 2 capsule may be necessary for pathogenic porcine strains to become zoonotic. We observed hints of capsule-switching events, with the CC20 strains from Germany carrying serotype 5 capsule instead of serotype 2, potentially representing an intermediate step in the emergence of zoonotic CC20 from CC16 (13). Furthermore, zoonotic strains from CC87 and CC94 lineages were serotype 2, whereas most porcine CC87 strains described in the literature carried a serotype 8 capsule; porcine CC94 strains displayed a wide range of capsules, serotypes 3, 7, and 23 being the most common (31). However, the low number of samples collected for CC25, CC87, and CC94 in our study and the fact that they were collected more than a decade ago make it difficult to conclude whether or not these CCs are emerging as zoonotic lineages or are geographically restricted (Appendix Tables 2, 3).

The presence of genes associated with zoonotic potential varied across lineages. Differences in the accessory genome of the zoonotic S. suis population, with some well-studied virulence factors such as sly, mrp, and fhb missing from certain pathogenic clades, suggest that, although individual genes might contribute to virulence and zoonotic potential, those genes are not individually essential for S. suis to infect humans (20,26,27) (Figure 4). Moreover, simply because a gene is overrepresented in zoonotic isolates does not mean it plays an active role in zoonotic potential, and its role in zoonosis should be explored experimentally. For example, some genes, such as zmp and sp1, more common in human than porcine S. suis isolates, have been shown not to be critical for virulence (32,33), and others, such as igdE and ideS, only play a role in evading porcine, not human, immune response (34,35).

Estimated cumulative prevalence of human S. suis infection is substantially higher in southeastern Asia than Europe and the epidemiology of human S. suis infections differs significantly between continents (1). In Europe, skin injuries and abrasions are thought to be the main point of entry for S. suis (3), whereas in countries in southeastern Asia with a tradition of raw pork product consumption, the intestinal tract is a notable entry point for infection (2,36). Differences in exposure routes have led to differences in epidemiology; multiple foodborne human S. suis outbreaks with high levels of illness and death have occurred in southeastern Asia in the past 2 decades (36,37). In Thailand, educational campaigns targeted toward at-risk populations have been shown to reduce incidence of human infections (36). Educational campaigns in Europe should be tailored to the different at-risk populations there. Our crude estimates of incidence of S. suis human infections in the population at risk for the Czech Republic, Germany, Hungary, the Netherlands, Poland, and Spain are comparable to the incidence of other pathogens causing similar infections in the general population (Appendix). Our estimated incidence in the population at risk for S. suis, range 0.161–4.945 cases/100,000 persons across the different countries, was generally higher (except in Poland) than population-wide incidence for Neisseria meningitidis (0.42–1.09) and lower than that of S. pneumoniae (1.52–14.86) reported by the European Centre for Disease Prevention and Control (38) (Appendix Table 6).

Furthermore, we found evidence of underreporting in the Netherlands; 25 cases were not reported to the Netherlands Reference Laboratory for Bacterial Meningitis or described in published articles (23). The United Kingdom was the only country where human S. suis infections were included in official government reports. Those UK reports contained 10 times as many cases within the same timeframe than UK cases from the survey and systematic review combined (22) because the survey and systematic review did not capture many unpublished cases. This finding suggest that the number of cases collected in other countries through the survey might also be underestimated. We observed an increase in reported cases after 1999 (Appendix Figure 2); however, this increase could have been caused by heightened awareness after a severe outbreak in China in 2005 and by more precise bacterial identification techniques (37). Moreover, in Thailand, a country where S. suis is a notifiable disease, reported infections have increased in the past few years (10).

In conclusion, despite not being a notifiable disease in Europe, novel zoonotic S. suis lineages, including multidrug-resistant lineages, have been detected recently both in Europe and worldwide (13,29). Moreover, our likely underestimated incidence estimates suggest that risk for S. suis infection for the at-risk population is greater than that of N. meningitidis and comparable to that of S. pneumoniae in the general population. Given the severity of the disease it causes, we propose making S. suis infections notifiable in Europe to improve surveillance of emerging zoonotic lineages and evolutionary trends and better detect potential human-to-human transmission.

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Acknowledgments

Our work was funded by the European Union Horizon 2020 grant 727966 (PIGSs).

Author contributions: conceptualization: K.A. and C.S.; data curation: J.B., T.R., Q.H., B.P., J.K., H.C.S., I.B.S., E.S., J.A.S., and V.C.; formal analysis: J.B., B.P., and Q.H.; funding acquisition: C.S.; investigation: J.B., B.P., and Q.H.; methodology: J.B., T.R., Q.H., B.P., K.A., and C.S.; project administration: K.A., C.S., and J.B.; resources: C.S.; software: C.S.; supervision: T.R., B.P., K.A., C.S.; validation: J.B.; visualization: J.B.; writing- original draft: J.B.; writing- reviewing and editing: J.B., T.R., H.Q., B.P., J.K., H.C.S., I.B.S., E.S., J.A.S., V.C., K.A., and C.S.

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Article Title: 
Molecular Epidemiology of Underreported Emerging Zoonotic Pathogen Streptococcus suis in Europe
CME Questions

  • Streptococcus suis is endemic in which of the following countries?

    • Vietnam and Thailand

    • Germany and Spain

    • Tanzania and Kenya

    • Ecuador and Colombia

  • Which serotype of S. suis is associated with the greatest proportion of zoonotic infections historically as well as in the current study?

    • Serotype 2

    • Serotype 4

    • Serotype 7

    • Serotype 9

  • What was the main clinical syndrome associated with S. suis infections in the current study?

    • Endocarditis

    • Sepsis

    • Enteritis

    • Meningitis

  • Which of the following statements regarding genetic characteristics of S. suis isolates in the current study is most accurate?

    • Most strains were part of the major zoonotic clade CC20

    • Strains from clades CC1 and CC20 had more accessory genes overrepresented in zoonotic isolates

    • All pathogenic clades featured the sly, mrp, and fhb genes

    • Overrepresented genes generally increased zoonotic potential

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Cite This Article

DOI: 10.3201/eid3003.230348

Original Publication Date: February 22, 2024

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Jaime Brizuela, Amsterdam UMC location University of Amsterdam, Department of Medical Microbiology and Infection Prevention, Meibergdreef 9, Amsterdam, the Netherlands

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Page updated: February 22, 2024
Page reviewed: February 22, 2024
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