BRIEF RESEARCH REPORT published: 08 December 2021 doi: 10.3389/fmed.2021.792233 Clinical and Epidemiological Characteristics of Streptococcus suis Infections in Catalonia, Spain Javier Díez de los Ríos 1 , Esteban Reynaga 2*, Merce García-Gonzàlez 3 , Jordi Càmara 4 , Carmen Ardanuy 4 , Jordi Cuquet 5 , Maria D. Quesada 6 , Marian Navarro 7 , Anna Vilamala 7 , Noemi Párraga-Niño 8 , Sara Quero 8,9,10 , Alba Romero 2 , Rosa M. Benítez 2 , Edited by: Jacint Altimiras 11 and Maria Luisa Pedro-Botet 2,9,12 on behalf of Study Group for S. suis Jiufeng Sun, Guangdong Provincial Center for 1 Department of Internal Medicine, Hospital Universitari Vic, Barcelona, Spain, 2 Department of Infectious Diseases, Hospital Disease Control and Prevention, China Universitari Germans Trias i Pujol, Badalona, Spain, 3 Department of Microbiology, Hospital Universitari Arnau de Vilanova, Reviewed by: Lleida, Spain, 4 Department of Microbiology, Hospital Universitari Bellvitge-IDIBELL, Barcelona, Spain, 5 Department of Internal Anusak Kerdsin, Medicine, Hospital Universitari Granollers, Barcelona, Spain, 6 Department of Microbiology, Hospital Universitari Germans Kasetsart University, Thailand Trias i Pujol, Badalona, Spain, 7 Department of Microbiology, Hospital Universitari Vic, Barcelona, Spain, 8 Infectious Diseases Zhenwen Zhou, Unit, Fundació Institut d’Investigació Germans Trias i Pujol, Barcelona, Spain, 9 CIBER de Enfermedades Respiratorias, Guangzhou Medical University, China CIBERES, Madrid, Spain, 10 Institut d’Investigació i Innovació Parc Taulí, Sabadell, Spain, 11 Department of Epidemiology, Hospital Universitari Vic, Barcelona, Spain, 12 Department of Medicine, Universitat Autònoma de Barcelona, Barcelona, Spain *Correspondence: Esteban Reynaga eareynaga.germanstrias@gencat.cat Introduction: Streptococcus suis (S. suis) is a human zoonotic pathogen of occupational origin, with infection acquired through contact with live pigs or pig meat. Specialty section: This article was submitted to Pig farming is one of Catalonia’s biggest industries and as a result this region of Spain Infectious Diseases – Surveillance, has one of the highest density pig populations per km2 . The aim of our study was to Prevention and Treatment, describe the infections caused by S. suis occurring in that area over a 9-year period. a section of the journal Frontiers in Medicine Materials and Methods: A retrospective, multi-center study was carried out by Received: 10 October 2021 searching records from 15 hospitals in Catalonia for the period between 2010 and 2019. Accepted: 18 November 2021 Published: 08 December 2021 Results: Over the study period altogether nine cases of S. suis infection were identified Citation: in five hospitals, with five of these cases occurring in the 2018–2019 period. The mean Díez de los Ríos J, Reynaga E, age of patients was 48 ± 8.9 years and all of them were males. Five patients (55.6%) García-Gonzàlez M, Càmara J, Ardanuy C, Cuquet J, Quesada MD, worked in pig farms. The most frequent manifestation of infection was meningitis (5 Navarro M, Vilamala A, cases; 55.6%) followed by septic arthritis (3 cases; 33.3%). None of the patients died Párraga-Niño N, Quero S, Romero A, at 30 days; nonetheless, 4 developed hearing loss as a long-term complication. Benítez RM, Altimiras J and Pedro-Botet ML (2021) Clinical and Conclusion: The most commonly identified S. suis infection was meningitis. Over 50% Epidemiological Characteristics of Streptococcus suis Infections in of the episodes occurred in the last 2 years and have affected pig farm workers. Further Catalonia, Spain. surveillance is needed in order to know its prevalence. Front. Med. 8:792233. doi: 10.3389/fmed.2021.792233 Keywords: Streptococcus suis, pig farm workers, meningitis, septic arthritis, Spain Frontiers in Medicine | www.frontiersin.org 1 December 2021 | Volume 8 | Article 792233 Díez de los Ríos et al. S. suis Infection, Spain INTRODUCTION covering the period between January 2010 and December 2019. Of the 15 Catalan hospitals participating in the study, 11 were Streptococcus suis (S. suis) is a primary commensal of pigs, located in the province of Barcelona, three in the province of commonly colonizing the tonsils and nasal cavities of these Girona and one in the province of Lleida. The epidemiological animals (1). This bacterium can also infect other mammals such and clinical characteristics of all patients reported to have been as wild boar and birds (2). infected by S. suis were retrospectively recorded in a database. It is considered a human zoonotic pathogen of mainly Invasive S. suis infection was defined by the isolation of S. suis occupational origin and was first reported in Denmark in 1968 from a normally sterile site (blood, cerebrospinal fluid, synovial (3). S. suis is classified into 35 serotypes with serotype two being fluid, seminal fluid) in a patient with signs and symptoms the most virulent. It is frequently isolated both in swine and in of infection. humans (4). Two S. suis infections previously described as sporadic cases Occupational exposition is a frequent antecedent in human (2), were included in this analysis. infection. There are 5 major groups of workers exposed to S. The study was approved by the Ethics Committee of the suis infection: pig farmers, slaughterhouse workers, butchers and Hospital Universitari de Vic; need for informed consent was meat handlers, veterinarians and wild boar hunters (1). Other waived (No. 2021163). factors such as alcoholism, corticosteroid or immunosuppressive therapy, diabetes, splenectomy and gastrointestinal tumors may increase the risk of human infection (5). Bacterial Identification and Antibiotic Catalonia is the region of Spain with the biggest pig industry Susceptibility Testing and thus represents one of the highest density pig populations The identification of S. suis isolates was done using either the per km2 in the country. Of the four provinces making up the Vitek-2 (Biomèrieux R ) or the MALDI-TOF (Bruker Daltonics) Autonomous Region of Catalonia (Lleida, Barcelona, Tarragona commercial system. The antimicrobial susceptibility test was and Girona), Barcelona (including the Osona region, with around performed through microdilution using commercially available 1,000 pigs/km2 ) (6) and Lleida are the two provinces with the Vitek-2 (Biomèrieux R ) or MicroScan (Beckman) systems. The highest density of pigs per km2 (Figure 1) (7). results were interpreted according to by the European Committee Given this high density, it was felt of interest to examine on Antimicrobial Susceptibility Testing (EUCAST) criteria (8). the frequency and characteristics of S. suis invasive infections in humans in this geographic area. Statistical Analysis For the qualitative variables, the percentages for each of MATERIALS AND METHODS the different categories were calculated. For the quantitative variables, the mean, median and standard deviation were A retrospective, observational multi-center study of invasive S. calculated. The IBM R SPSS R Statistics programme version 26 suis infections was carried out by examining hospital records was used to perform the statistical analysis. FIGURE 1 | Map of the autonomous region of Catalonia in Spain showing the number of S. suis invasive infections, the density of pigs/km2 and the population/km2 by province. Frontiers in Medicine | www.frontiersin.org 2 December 2021 | Volume 8 | Article 792233 Díez de los Ríos et al. S. suis Infection, Spain FIGURE 2 | Distribution of cases of S. suis infections reported in Catalonia 2010–2019 by year (A) and by month (B). RESULTS Five patients were treated with ceftriaxone, one patient with ceftriaxone plus clindamycin, two patients with penicillin and Nine cases of S. suis infections were detected at five hospitals, one patient with erythromycin. The mean duration of treatment of which four were in the province of Barcelona and one in was 25.8 ± 25.5 days. the province of Lleida. Of these nine cases, four (44.5%) were detected in the 2011–2014 period and five (55.5%) in the 2018- 2019 period (Figure 2A). DISCUSSION Likewise, five cases occurred in summer while the remaining four cases occurred in autumn and winter (Figure 2B). Despite being a leading pig producer in Europe, few S. suis The mean age of the nine patients was 48 ± 8.9 years and infections have been reported in Spain (5). In this study we the patients were all male. Charlson index scores were 0 (55.6%), describe a series of cases of invasive S. suis infections in an area 1 (22.2%), and 2 (22.2%). None of the patients were under of high swine density in Spain. corticosteroid or other immunosuppressive treatment at the time In our series, invasive S. suis infections occurred more of infection. frequently in summer. These data coincide with those reported Five patients (55.5%) worked in pig farms and only one patient in Wangkaew et al. (9) and suggest that S. suis infections could be had a pet (a cat). Four patients (44.4%) had handled meat in the related to high ambient temperatures. previous week; one of them being a wild boar hunter who had Although the number of cases is low, most of them occurred suffered a wild boar bite and another was a butcher. in the last 2 years suggesting surveillance of a putative increase The most frequent manifestation of infection was meningitis in the future. However, it could be partially explained by S. suis (5; 55.5%), followed by septic arthritis (3; 33.3%) and there was misidentification in the past as reported by other authors (10). one case each of native mitral valve endocarditis complicated by Several studies have demonstrated that S. suis infection an ischemic stroke, periprosthetic infection of total hip prosthesis in humans is associated with occupational or environmental and orchitis. exposure to live pigs or pig meat (1). In fact, in a series study The most frequent symptoms were fever (8 cases; 88.8%) and published in the Netherlands, 93% of those infected by S. suis headache (5 cases; 55.5%). Three patients (33.3%) presented with were pig farmers, abattoir workers or butchers, or had occasional septic shock. contact with pigs or pork products (11). Similarly, six (66.6%) None of the patients died at 30 days; nonetheless, four patients of the patients in the present study were farmers or butchers, developed hearing loss as a long-term complication (one of them the remaining three being residents of areas with an unusually also developed ataxia). high density of pigs (Lleida and the Osona region of Barcelona), Table 1 shows the clinical and epidemiological characteristics although they did not have any direct contact with farms. of each case, as well as the antibiotic treatment and the outcome. S. suis infections have mostly been reported in Asian countries, All of S. suis strains were susceptible to 3rd generation especially Thailand, Vietnam and China (12). Infections cephalosporins, vancomycin and rifampicin, 88.9% described have included meningitis, infective endocarditis, to penicillin and fluoroquinolones, respectively and sepsis syndrome, arthritis, pneumonia, endophthalmitis and 71.4% to trimethoprim-sulfamethoxazole. Most strains spondylodiscitis (9). Recently Kerdsin et al. analyzed genotypic were resistant to erythromycin and clindamycin (both diversity in multiple S suis infections. The authors observed 88.9%). Table 2 shows the MICs of S. suis to the that in 83.7% of meningitis cases the clonal complex CC1 antibiotics tested. was isolated followed by CC104 (14.9%), Sepsis could be Frontiers in Medicine | www.frontiersin.org 3 December 2021 | Volume 8 | Article 792233 Frontiers in Medicine | www.frontiersin.org Díez de los Ríos et al. TABLE 1 | Clinical and epidemiological characteristics of cases of S. suis Infection. Case 1 Case 2 Case 3 Case 4 Case 5 Case 6 Case 7 Case 8 Case 9 Age 57 48 47 48 63 50 42 63 37 Sex Male Male Male Male Male Male Male Male Male Farm worker No No No Yes Yes No Yes Yes Yes Handled meat in Not known Yes Yes (butcher) Yes Not known No Yes Not known No previous week Pets Cat Not known Not known No Not known No No Not known No Underlying Alcoholism No No Hypertension, No No No Alcoholism Prosthetic hip condition Glomerulonephritis Charlson Index 1 0 0 0 2 1 0 2 0 Immunosuppressive No No No No No No No No No treatment Symptoms Fever, Fever, Fever, Fever, Fever Haematospermia Fever, Fever Fever headache headache headache headache, headache encephalitis Type of infection Meningitis, Meningitis, Meningitis Meningitis Native mitral Orchitis Meningitis Septic arthritis Prosthesis hip septic arthritis septic arthritis valve infection endocarditis Diagnostic sample Blood culture, Blood culture, Blood culture, CSF Blood culture Seminal fluid CSF Blood culture, Synovial fluid CSF CSF CSF synovial fluid Skin lesion No Yes (wild boar No No No No Yes No Yes 4 bite) Septic shock Yes Yes No Yes No No No No No Days ICU 16 15 No 8 No No No No No Endotracheal Yes Yes No Yes No No No No No intubation Definitive antibiotic Ceftriaxone Ceftriaxone Ceftriaxone Penicillin Penicillin Erythromycin Ceftriaxone Ceftriaxone Ceftriaxone + Clindamycin Dexamethasone Yes Not known Not known No No No Yes No No Mortality No No No No No No No No No Sequelae Hearing loss, Hearing loss No Hearing loss No No Hearing loss No No ataxia December 2021 | Volume 8 | Article 792233 CSF, Cerebrospinal fluid; ICU, Intensive Care Unit. S. suis Infection, Spain Díez de los Ríos et al. S. suis Infection, Spain TABLE 2 | Antibiotic MICs of Streptococcus suis. Antimicrobials Case 1 Case 2 Case 3 Case 4 Case 5 Case 6 Case 7 Case 8 Case 9 Penicillin <0.03 <0.03 0.06 <0.03 0.023 0.5c <0.06 0.047 0.064 Cefotaxime 0.12 <0.06 0.12 <0.06 <0.03 <0.06 0.5 0.125 <0.06 Levofloxacin 0.5 0.5 0.5 0.5 <0.25 8 <0.25 0.5 0.19 Erythromycin >4b >4 >1 >4 >4 <0.12 >8 >0.5 >4 Clindamycin >4 >4 >1 >0.5 >4 0.5 >1 >0.5 <0.25 SXTa >2 <0.5 <0.5 <0.5 >2 <0.5 <1 0.25 <0.5 Rifampicin <0.25 <0.25 <0.5 <0.5 <0.5 <0.5 <0.06 <0.5 <0.5 Vancomycin <0.5 <0.5 1 <0.5 0.25 0.5 0.25 0.5 0.5 a SXT,trimethoprim-sulfamethoxazole. b Numbers in boldface indicate resistance values according to EUCAST. c Non-penicillin-susceptible. associated with isolates belonging to all CCs and two singletons fail to adequately diagnose the infection. Several molecular (ST235 and ST236). CC1 isolates also accounted for 47.7% biological techniques have been developed for diagnosis, but of the sepsis cases, followed by those of CC104 (37.3%). they are not suitable for small hospitals or for field diagnostics. Infective endocarditis was mainly caused by CC1 isolates. Nakayama et al. (18) developed the immunochromatographic Septic arthritis cases were caused by CC1 isolates, whereas banding (ICS) technique against S. suis serotype 2 to detect CC104 and CC233/379 isolates were associated with spontaneous S. suis antigens in urine and could be a good option for peritonitis. Serotype two (94.6%) was predominant, followed rapid diagnosis. by serotype 14 (4.5%) (13). In Europe, the Netherlands is one Antimicrobial resistance is a major health problem; data of the countries with the highest density of pigs, and cases of suggest an increasing and alarming contribution of S. suis to meningitis in humans caused by S. suis have been described this global threat (19). Bamphensin et al. (20) analyzed 448 (11). In our series meningitis was the most commonly of S. S. suis isolates recovered from human infections in Thailand suis infection and was frequently complicated by long-term and characterized them for their antimicrobial susceptibility. A hearing loss. Hearing loss occurred in 80% of our patients, total of 37 (8.2%) showed intermediate resistance to penicillin. similar to the rate described in patients with S. suis meningitis Isolates belonging to serotype 2 ST233 were the most common in the Netherlands (86%) (11), although higher than data strain type associated with penicillin non-susceptibility. Serotype reported for Vietnam (50%) (12). The role of dexamethasone in 14 (ST105) and serotype 24 (ST221 and ST234) were also preventing hearing loss after S. suis meningitis is controversial found to be intermediately resistant to penicillin. In our study, (11, 14). one (11%) patient had an infection due to penicillin-non- It should be noted that a patient with haematospermia was susceptible S. suis in 2019. Although just one case out of nine, diagnosed with orchitis. In this particular case, neither contact we must be aware of an eventual increase of cases caused with animals nor meat consumption nor any other risk factor for by S suis penicillin non-susceptibility strains in the future in S. suis infection was detected, although the patient lived in an area Catalonia, Spain. with a high density of pig farms. The present study has several limitations, mainly due Mortality from invasive S. suis infections is high. to its retrospective design. The unavailability of serotypes Eighty-four out of the 659 cases with S. suis infection and the shortness of the series make it difficult to draw diagnosed in Thailand were fatal (12.7%), of which 21 significant conclusions. cases were attributed to meningitis, 62 cases to sepsis, and In summary, invasive S. suis infections are rare in one case was to infective endocarditis (13). As we have Spain, although there appears to have been an increase noted, none of the patients in our series died, and all in recent years. While most of the patients had a history the patients with meningitis survived. Compared to other of contact with live pigs or pig meat, this was not always causes of meningitis in an age-matched population, the the case. Meningitis was the most prevalent clinical number of lethal cases of S. suis meningitis is relatively manifestation and hearing loss was a common and low (15). This may be due to the fact that the majority of serious complication. people infected with S. suis are healthy adults with a low comorbidity score. STUDY GROUP FOR S. suis Early detection of human S. suis infection is crucial, as rapid progression of symptoms, such as sepsis or septic shock, is one of Rafel Perez Vidal (Hospital de Sant Joan de Déu, Manresa), the risk factors for high mortality (16, 17). However, traditional Lorena Gaviria (Hospital de Cerdanya, Puigcerdà), Goretti diagnostic methods are routine and complex, and sometimes Sauca-Subias (Hospital de Mataró), Carme Gallès (Hospital Frontiers in Medicine | www.frontiersin.org 5 December 2021 | Volume 8 | Article 792233 Díez de los Ríos et al. S. suis Infection, Spain de Blanes), Josefa Perez (CATLAB Hospital de Terrassa AUTHOR CONTRIBUTIONS and Hospital Mutua de Terrassa), Oriol Gasch (Hospital Universitari Parc Taulí, Sabadell), Alex Soriano (Hospital All authors listed in the contributors’ affiliations meet the ICMJE Clinic de Barcelona, Barcelona) Vicents Brito (Hospital Sant Authorship Criteria, that is, they contributed substantially to Boi de Llobregat), Nieves Larrosa (Hospital Universitari Vall the study’s conception and design, the acquisition of data, the d’Hebron, Barcelona). drafting of the article, its critical review, and the final approval of the manuscript. DATA AVAILABILITY STATEMENT SUPPLEMENTARY MATERIAL Requests to access the data analyzed in this The Supplementary Material for this article can be found study should be directed to Esteban Reynaga, online at: https://www.frontiersin.org/articles/10.3389/fmed. eareynaga.germanstrias@gencat.cat. 2021.792233/full#supplementary-material REFERENCES 14. Nguyen TH, Tran TH, Thwaites G, Ly VC, Dinh XS, Ho Dang TN, et al. Dexamethasone in Vietnamese adolescents and adults with bacterial 1. Dutkiewicz J, Sroka J, Zajac V, Wasiński B, Cisak E, Sawczyn A, et al. meningitis. N Engl J Med. (2007) 357:243–40. doi: 10.1056/NEJMoa070852 Streptococcus suis: a re-emerging pathogen associated with occupational 15. Bohr V, Hansen B, Jessen O, Johnsen N, Kjersem H, Kristensen HS, et al. exposure to pigs or pork products. Part I–Epidemiology. Ann Agric Environ Eight hundred and seventy-five cases of bacterial meningitis. Part I of a Med. (2017) 24:683–95. doi: 10.26444/aaem/79813 three-part series: clinical data, prognosis, and the role of specialised hospital 2. Fernández-Aguilar X, Gottschalk M, Aragon V, Càmara J, Ardanuy C, Velarde departments. J Infect. (1983) 7:21–30. doi: 10.1016/S0163-4453(83)90894-0 R, et al. Urban wild boars and risk for zoonotic Streptococcus suis, Spain. Emerg 16. Wangsomboonsiri W, Luksananun T, Saksornchai S, Ketwong K, Infect Dis. (2018) 24:1083–6. doi: 10.3201/eid2406.171271 Sungkanuparph S. Streptococcus suis infection and risk factors for mortality. J 3. Perch B, Kristjansen P, Skadhauge K. Group R streptococci pathogenic for Infect. (2008) 57:392–6. doi: 10.1016/j.jinf.2008.08.006 man: two cases of meningitis and one fatal case of sepsis. Acta Pathol Microbiol 17. Rayanakorn A, Katip W, Goh BH, Oberdorfer P, Lee LH. Clinical Scand. (1968) 74:69–76. doi: 10.1111/j.1699-0463.1968.tb03456.x manifestations and risk factors of Streptococcus suis mortality among northern 4. Feng Y, Zhang H, Wu Z, Wang S, Cao M, Hu D, et al. Streptococcus suis thai population: retrospective 13-year cohort study. Infect Drug Resist. (2019) infection: an emerging/reemerging challenge of bacterial infectious diseases? 12:3955–65. doi: 10.2147/IDR.S233326 Virulence. (2014) 5:477–97. doi: 10.4161/viru.28595 18. Nakayama T, Zhao J, Takeuchi D, Kerdsin A, Chiranairadul P, Areeratana P, 5. Gómez-Zorrilla S, Ardanuy C, Lora-Tamayo J, Cámara J, García-Somoza D, et al. Colloidal gold-based immunochromatographic strip test compromising Peña C, et al. Streptococcus suis infection and malignancy in man, Spain. Emerg optimised combinations of anti-S. suis capsular polysaccharide polyclonal Infect Dis. (2014) 20:1067–8. doi: 10.3201/eid2006.131167 antibodies for detection of Streptococcus suis. Biosens Bioelectron. (2014) 6. Reynaga E, Navarro M, Vilamala A, Roure P, Quintana M, Garcia-Nuñez M, 60:175–9. doi: 10.1016/j.bios.2014.03.074 et al. Prevalence of colonization by methicillin-resistant Staphylococcus aureus 19. Segura M. Streptococcus suis research: progress and ST398 in pigs and pig farm workers in an area of Catalonia, Spain. BMC Infect challenges. Pathogens. (2020) 9:707. doi: 10.3390/pathogens90 Dis. (2016) 16:1–8. doi: 10.1186/s12879-016-2050-9 90707 7. Idescat (Institut D’EStadística de CATalunya): Anuari estadístic de Catalunya. 20. Bamphensin N, Chopjitt P, Hatrongjit R, Boueroy P, Fittipaldi N, Agricultura, ramaderia i pesca. Ramaderia. Explotacions ramaderes. Gottschalk M, et al. Non-Penicillin-Susceptible Streptococcus suis Isolated Per espècies. Comarques, àmbits i provincies. Explotacions. Catalunya: from Humans. Pathogens. (2021) 10:1178. doi: 10.3390/pathogens100 Departament d’Agricultura, Ramaderia, Pesca, Alimentació i Medi natural. 91178 Available online at: https://www.idescat.cat/pub/?id=aec&n=452&lang=es (accessed June 15, 2021). Conflict of Interest: The authors declare that the research was conducted in the 8. The European Committee on Antimicrobial Susceptibility Testing absence of any commercial or financial relationships that could be construed as a (EUCAST). Breakpoint Tables Interpretation of MICs and Zone Diameters. potential conflict of interest. EUCAST (2020). 9. Wangkaew S, Chaiwarith R, Tharavichitkul P, Supparatpinyo K. Streptococcus Publisher’s Note: All claims expressed in this article are solely those of the authors suis infection: a series of 41 cases from Chiang Mai University Hospital. J Infect. (2006) 52:455–60. doi: 10.1016/j.jinf.2005.02.012 and do not necessarily represent those of their affiliated organizations, or those of 10. Schultsz C, Van Dijk D, Wagenaar JA, Van der Ende A. Zoonotische infecties the publisher, the editors and the reviewers. Any product that may be evaluated in met Streptococcus suis in Nederland. Infect Bull. (2013) 9:280–4. this article, or claim that may be made by its manufacturer, is not guaranteed or 11. van Samkar A, Brouwer MC, Schultsz C, van der Ende A, van de Beek D. endorsed by the publisher. Streptococcus suis meningitis in the Netherlands. J Infect. (2015) 71:602–4. doi: 10.1016/j.jinf.2015.07.001 Copyright © 2021 Díez de los Ríos, Reynaga, García-Gonzàlez, Càmara, Ardanuy, 12. Kerdsin A, Akeda Y, Takeuchi D, Dejsirilert S, Gottschalk M, Oishi Cuquet, Quesada, Navarro, Vilamala, Párraga-Niño, Quero, Romero, Benítez, K. Genotypic diversity of Streptococcus suis strains isolated from Altimiras and Pedro-Botet. This is an open-access article distributed under the terms humans in Thailand. Eur J Clin Microbiol Infect Dis. (2018) 37:917–25. of the Creative Commons Attribution License (CC BY). The use, distribution or doi: 10.1007/s10096-018-3208-8 reproduction in other forums is permitted, provided the original author(s) and the 13. Mai NTH, Hoa NT, Nga TVT, Linh LD, Chau TTH, Sinh DX, et al. copyright owner(s) are credited and that the original publication in this journal Streptococcus suis meningitis in adults in Vietnam. Clin Infect Dis. (2008) is cited, in accordance with accepted academic practice. No use, distribution or 46:659–67. doi: 10.1086/527385 reproduction is permitted which does not comply with these terms. Frontiers in Medicine | www.frontiersin.org 6 December 2021 | Volume 8 | Article 792233