Centers for Disease Control and Prevention. CDC twenty four seven. Saving Lives, Protecting People
Centers for Disease Control & Prevention. CDC twenty four seven. Saving Lives, Protecting People
Volume 30, Number 3—March 2024 CME ACTIVITY - Synopsis
Molecular Epidemiology of Underreported Emerging Zoonotic Pathogen Streptococcus suis in Europe
Article và Appendix
Jaime Brizuela
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).
Introduction
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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.
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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.; Glaxo
Smith
Kline.
Authors
Jaime Brizuela, MRes; Thomas J. Roodsant, Ph
D; Qureisha Hasnoe, MSc; Boas C.L. Van der Putten, Ph
D; Jana Kozakova, MD; Hans-Christian Slotved, Ph
D, DMSc; Mark van der Linden, Ph
D; Ilse G.A. De Beer-Schuurman, BSc; Ewa Sadowy, Ph
D, MD; Juan Antonio Sáez-Nieto, Ph
D; Victoria J. Chalker, Ph
D; Kees C.H. Van der Ark, Ph
D; Constance Schultsz, Ph
D, MD.
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 lớn increase insight into the molecular epidemiology of human S. Suis infections in Europe. To lớn procure data, we surveyed 7 reference laboratories & performed a systematic đánh giá 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 và 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 tư vấn 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 và sepsis (1). Human S. Suis infections occur both through direct tương tác with infected pigs and consumption of undercooked contaminated pork (2). Human S. Suis infections have become endemic in đất nước thái lan and Vietnam, driven by consumption of traditional raw pork dishes (1), và S. Suis has caused multiple outbreaks in humans with high levels of illness & death in china and vương quốc nụ cười (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 tài khoản 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, và 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 và 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 khổng lồ increase insight into the epidemiology of human S. Suis infections in Europe & 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 đứng đầu pig-rearing countries in Europe, performed a systematic literature review and explored the gray literature (social media, news accounts, & government reports). In addition, we reconstructed a representative phylogeny of zoonotic S. Suis isolates in Europe.
This study was not reviewed by an ethics reviews 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 lớn 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).
Survey
We contacted national reference laboratories in 10 countries in Europe (Czech Republic, Denmark, France, Germany, Hungary, Italy, the Netherlands, Poland, Spain, & the United Kingdom) that included S. Suis infections within their scope. We asked those laboratories khổng lồ 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 lớn complete a questionnaire collecting patient metadata và bacterial typing và metadata. Anonymized patient metadata were age, sex, clinical signs, & occupation. Bacterial typing encompassed serotype, sequence type (ST), và 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 cốt truyện their isolates for further genomic analysis (Appendix).
Systematic review
We performed a systematic reviews according to PRISMA (Preferred Reporting Items for Systematic đánh giá and Meta-Analyses) guidelines (14) lớn identify cases of human S. Suis infections in Europe in articles published from 1990 (survey start date) through 2022. We screened Pub
Med, website of Science, and Scopus for key terms—S. Suis, human, và ≥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) và 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 & 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 lớn avoid duplication, we excluded from the systematic reviews isolates reported in both the survey & 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. Lớn identify additional cases, we performed a broad scan of gray literature lớn 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) và the Google news section using the terms S. Suis, infection, và 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, và the United Kingdom for reports on zoonotic bacterial infections related khổng lồ human S. Suis infections. To lớn 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 & 21 previously sequenced) và 7 from the systematic đánh giá (Appendix Figure 1). We used MLST version 2.19.0 (https://github.com/tseemann/mlst) with the Pub
MLST database (https://pubmlst.org) to lớn type the MLST profiles of the draft genomes. We submitted profiles for novel STs lớn Pub
MLST. We performed in silico serotyping by feeding processed Illumina reads into the S. Suis serotyping pipeline (15). We reconstructed a bộ vi xử lý core genome single-nucleotide polymorphism (SNP) phylogeny and using Panaroo version 1.3.0 (16) to reconstruct the pangenome và align the chip 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 mã sản phẩm with the flag “-fconst” to lớn include the constant sites from SNP-sites. We investigated the presence of 46 accessory genes previously found lớn 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 & coverage of 80%. We visualized the resulting gen presence/absence matrix in Phandango (19,20). Raw Illumina sequences can be found in the National Center for Biotechnology Information Short Read Archive (Bio
Project PRJNA853715). Genome assemblies have been deposited in Gen
Bank và are available under the same Bio
Project number (Appendix Table 7).
Geographic Distribution of Reported Human S. Suis Infections across Europe, 1990–2022
Of 10 reference laboratories invited to lớn participate in the survey, 7 laboratories (Spain, Germany, Netherlands, Denmark, Czech Republic, Poland, & United Kingdom) responded and reported 107 quality cases of human S. Suis infections (Appendix Table 2). In the systematic review, of 119 screened titles và 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 quality cases of human S. Suis infections across Europe during 1990–2022. Germany, Spain, và 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 reviews (59/86 <68%>), followed by sepsis, which affected 15/71 (21%) in the survey & 21/86 (24%) in the systematic review. Additional clinical signs và symptoms included hearing loss (n = 22), endocarditis (n = 6), và spondylodiscitis (n = 3); 11 patients died. Patient occupation was described as a potential risk factor in 19 cases in the survey và 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 và 14/16 <88%> in the systematic review) belonged to lớn 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 reviews (Appendix Table 3). Nonetheless, average number of cases per year in the systematic đánh giá and survey increased after 1999, from 2.7 during 1990–1999 khổng lồ 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 đánh giá 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 trương mục for butchers, hunters, slaughterhouse workers, lorry drivers, và 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 & 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 tìm kiếm 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 & 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 và systematic review combined (6 cases). However, those 61 cases might overlap with cases from the survey & 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 khổng lồ the reference laboratory và collected an additional 25 chất lượng 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, và 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 khổng lồ have emerged (13). Two additional CC20 strains were isolated in Germany, forming a serotype 5 outgroup khổng lồ 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 bộ vi xử lý core genomes, whereas the ST29 strain differed from the ST25 strains by 4,353–4,416 SNPs & had a serotype 7 capsule. Strains from the CC87 clade were identified in Germany và the Czech Republic and possessed a serotype 2 capsule. The 3 strains from Germany were ST19 & highly similar (81–118 SNPs), whereas the strain from the Czech Republic had novel ST1660 và differed from the ST19 clade by 9,411–9,434 SNPs.
CC1 and CC20 Isolates & Genes Associated with Zoonotic Potential
Overall, strains from clades CC1 & CC20 had a higher number of accessory genes overrepresented in zoonotic isolates than did strains from lineages CC25, CC87, & CC94 (Figure 4). Most genes associated with zoonoses were present in >1 of the lineages; only the 2-component signal transduction system nis
K/R & the fimbria-like adhesin sss
P1 genes were absent from the dataset (Figure 4). Of note, despite its role in adhesion và 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 & 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 (hyl
A), associated with reduced virulence (Figure 4) (28).
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 lớn date, systematic surveillance is needed khổng lồ follow the evolutionary trends of this pathogen in humans và 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 khổng lồ the form size of pig populations. Other factors, such as government policy and disease monitoring & reporting, could contribute to lớn 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 và 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 reviews yielded diverse article types (e.g., case reports, surveillance studies) và inconsistent quality of reported metadata. Often, year of isolation & bacterial typing was absent, making it difficult lớn 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 lớn acquisition of a serotype 2 capsule may be necessary for pathogenic porcine strains lớn 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, và 23 being the most common (31). However, the low number of samples collected for CC25, CC87, and CC94 in our study & the fact that they were collected more than a decade ago make it difficult lớn 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, & fhb missing from certain pathogenic clades, suggest that, although individual genes might contribute to lớn virulence và zoonotic potential, those genes are not individually essential for S. Suis lớn 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, và 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 lớn be critical for virulence (32,33), và others, such as igd
E & ide
S, 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 & abrasions are thought khổng lồ 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 & 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 khổng lồ reduce incidence of human infections (36). Educational campaigns in Europe should be tailored to lớn 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 lớn 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 và Control (38) (Appendix Table 6).
Furthermore, we found evidence of underreporting in the Netherlands; 25 cases were not reported lớn 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 nhận xét combined (22) because the survey và systematic reviews 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 trung quốc in 2005 và 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 và comparable khổng lồ 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 và evolutionary trends và better detect potential human-to-human transmission.
Streptococcus suis (S. Suis) is a gram-positive bacterial pathogen in pigs which can cause serious infections in human including meningitis, and septicaemia resulting in serious complications. There were discrepancies between different data và little is known concerning associated risk factors of S. Suis. A systematic đánh giá and meta-analysis was conducted to investigate on S. Suis infection risk factors in human. We searched eight relevant databases using the Me
SH terms “Streptococcus suis” OR “Streptococcus suis and infection” limited in human with no time nor language restriction. Out of 4,999 articles identified, 32 và 3 studies were included for systematic nhận xét and meta-analysis respectively with a total of 1,454 Streptococcus suis cases reported. S. Suis patients were generally adult males và the elderly. The mean age ranged between 37 to lớn 63 years. Meningitis was the most common clinical manifestation, & deafness was the most common sequelae found among survivors followed by vestibular dysfunction. Infective endocarditis was also noted as among the most common clinical presentations associated with high mortality rate in a few studies. Meta-analyses categorized by type of control groups (community control, và non-S. Suis sepsis) were done among 850 participants in 3 studies. The combined odd ratios for studies using community control groups và non-S. Suis sepsis as controls respectively were 4.63 (95% CI 2.94–7.29) và 78.00 (95% CI 10.38–585.87) for raw pork consumption, 4.01 (95% CI 2.61–6.15) & 3.03 (95% CI 1.61–5.68) for exposure khổng lồ pigs or pork, 11.47, (95% CI 5.68–23.14) and 3.07 (95% CI 1.81–5.18) for pig-related occupation và 3.56 (95% CI 2.18–5.80) and 5.84 (95% CI 2.76–12.36) for male sex. The results were found khổng lồ be significantly associated with S. Suis infection và there was non-significant heterogeneity. History of skin injury & underlying diseases were noted only a small percentage in most studies. Setting up an effective screening protocol & public health interventions would be effective khổng lồ enhance understanding about the disease.
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