Geographical, Temporal and Host-Species Distribution of Potentially Human-Pathogenic Group B Streptococcus in Aquaculture Species in Southeast Asia

Group B Streptococcus (GBS) is a major pathogen of humans and aquatic species. Fish have recently been recognized as the source of severe invasive foodborne GBS disease, caused by sequence type (ST) 283, in otherwise healthy adults in Southeast Asia. Thailand and Vietnam are among the major aquaculture producers in Southeast Asia, with GBS disease reported in fish as well as frogs in both countries. Still, the distribution of potentially human-pathogenic GBS in aquaculture species is poorly known. Using 35 GBS isolates from aquatic species in Thailand collected from 2007 to 2019 and 43 isolates from tilapia collected in Vietnam in 2018 and 2019, we have demonstrated that the temporal, geographical, and host-species distribution of GBS ST283 is broader than previously known, whereas the distribution of ST7 and the poikilothermic lineage of GBS are geographically restricted. The gene encoding the human GBS virulence factor C5a peptidase, scpB, was detected in aquatic ST283 from Thailand but not in ST283 from Vietnam or in ST7 from either country, mirroring current reports of GBS strains associated with human sepsis. The observed distribution of strains and virulence genes is likely to reflect a combination of spill-over, host adaptation through the gain and loss of mobile genetic elements, and current biosecurity practices. The plastic nature of the GBS genome and its importance as a human, aquatic, and potentially foodborne pathogen suggests that active surveillance of GBS presence and its evolution in aquaculture systems may be justified.

[1]  S. Madhi,et al.  Group B streptococcus infection during pregnancy and infancy: estimates of regional and global burden , 2022, The Lancet. Global health.

[2]  P. Palittapongarnpim,et al.  Genomic epidemiology of Streptococcus agalactiae ST283 in Southeast Asia , 2022, Scientific reports.

[3]  T. V. Van Boeckel,et al.  Twenty-year trends in antimicrobial resistance from aquaculture and fisheries in Asia , 2021, Nature Communications.

[4]  S. Chen,et al.  GBS-SBG - GBS Serotyping by Genome Sequencing , 2021, bioRxiv.

[5]  Risk profile - Group B Streptococcus (GBS) –​ Streptococcus agalactiae sequence type (ST) 283 in freshwater fish , 2021 .

[6]  M. Brouwer,et al.  Prevalence of group B streptococcal colonization in the healthy non-pregnant population: A systematic review and meta-analysis. , 2021, Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases.

[7]  Dhitiwat Changpradub,et al.  Clinical manifestations and prognostic factors for Streptococcus agalactiae bacteremia among nonpregnant adults in Thailand. , 2021, Journal of infection and chemotherapy : official journal of the Japan Society of Chemotherapy.

[8]  T. V. Van Boeckel,et al.  Global trends in antimicrobial use in aquaculture , 2020, Scientific Reports.

[9]  C. Choresca,et al.  Isolation and molecular characterization of streptococcal species recovered from clinical infections in farmed Nile tilapia (Oreochromis niloticus) in the Philippines. , 2020, Journal of fish diseases.

[10]  R. Zadoks,et al.  Development and Application of a Prophage Integrase Typing Scheme for Group B Streptococcus , 2020, Frontiers in Microbiology.

[11]  I. Hirono,et al.  Cytotoxicity of Streptococcus agalactiae secretory protein on tilapia cultured cells. , 2020, Journal of fish diseases.

[12]  M. Ip,et al.  Multidrug-Resistant Streptococcus agalactiae Strains Found in Human and Fish with High Penicillin and Cefotaxime Non-Susceptibilities , 2020, Microorganisms.

[13]  R. Zadoks,et al.  Community-acquired Group B streptococcal meningitis in adults. , 2020, The Journal of infection.

[14]  Charles C. Zhou,et al.  Investigation of Streptococcus agalactiae using pcsB‐based LAMP in milk, tilapia and vaginal swabs in Haikou, China , 2020, Journal of applied microbiology.

[15]  W. Paveenkittiporn,et al.  Streptococcus agalactiae infections and clinical relevance in adults, Thailand. , 2020, Diagnostic microbiology and infectious disease.

[16]  Christopher Beaudoin,et al.  Producing polished prokaryotic pangenomes with the Panaroo pipeline , 2020, Genome Biology.

[17]  S. Boonyayatra,et al.  Phenotypic and genotypic characterization of Streptococcus spp. isolated from tilapia (Oreochromis spp.) cultured in river-based cage and earthen ponds in Northern Thailand. , 2020, Journal of fish diseases.

[18]  C. Rodkhum,et al.  Comparative genomics inferred two distinct populations of piscine pathogenic Streptococcus agalactiae, serotype Ia ST7 and serotype III ST283, in Thailand and Vietnam. , 2019, Genomics.

[19]  Jennifer Lu,et al.  Improved metagenomic analysis with Kraken 2 , 2019, Genome Biology.

[20]  C. Town,et al.  Population Gene Introgression and High Genome Plasticity for the Zoonotic Pathogen Streptococcus agalactiae , 2019, Molecular biology and evolution.

[21]  P. Newton,et al.  One hypervirulent clone, sequence type 283, accounts for a large proportion of invasive Streptococcus agalactiae isolated from humans and diseased tilapia in Southeast Asia , 2019, PLoS neglected tropical diseases.

[22]  R. Guy,et al.  Group B Streptococcus in surgical site and non-invasive bacterial infections worldwide: A systematic review and meta-analysis. , 2019, International journal of infectious diseases : IJID : official publication of the International Society for Infectious Diseases.

[23]  H. Figueiredo,et al.  Streptococcus agalactiae Sequence Type 283 in Farmed Fish, Brazil , 2019, Emerging infectious diseases.

[24]  Keith A Jolley,et al.  Open-access bacterial population genomics: BIGSdb software, the PubMLST.org website and their applications , 2018, Wellcome open research.

[25]  The State of World Fisheries and Aquaculture 2020 , 2018, The State of World Fisheries and Aquaculture.

[26]  S. Beatson,et al.  Microevolution of Streptococcus agalactiae ST-261 from Australia Indicates Dissemination via Imported Tilapia and Ongoing Adaptation to Marine Hosts or Environment , 2018, Applied and Environmental Microbiology.

[27]  L. Ng,et al.  Group B Streptococcus Infections Caused by Improper Sourcing and Handling of Fish for Raw Consumption, Singapore, 2015–2016 , 2017, Emerging infectious diseases.

[28]  H. Figueiredo,et al.  Large-scale genomic analyses reveal the population structure and evolutionary trends of Streptococcus agalactiae strains in Brazilian fish farms , 2017, Scientific Reports.

[29]  H. Figueiredo,et al.  Large-scale genomic analyses reveal the population structure and evolutionary trends of Streptococcus agalactiae strains in Brazilian fish farms , 2017, Scientific Reports.

[30]  W. Schaffner,et al.  Short-read whole genome sequencing for determination of antimicrobial resistance mechanisms and capsular serotypes of current invasive Streptococcus agalactiae recovered in the USA. , 2017, Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases.

[31]  Christopher W. Wong,et al.  2015 Epidemic of Severe Streptococcus agalactiae Sequence Type 283 Infections in Singapore Associated With the Consumption of Raw Freshwater Fish: A Detailed Analysis of Clinical, Epidemiological, and Bacterial Sequencing Data. , 2017, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[32]  R. Lin,et al.  Group B Streptococcus Sequence Type 283 Disease Linked to Consumption of Raw Fish, Singapore , 2016, Emerging infectious diseases.

[33]  C. Chu,et al.  Genetic and pathogenic difference between Streptococcus agalactiae serotype Ia fish and human isolates , 2016, BMC Microbiology.

[34]  D. Crook,et al.  Capsular Typing Method for Streptococcus agalactiae Using Whole-Genome Sequence Data , 2016, Journal of Clinical Microbiology.

[35]  C. Rodkhum,et al.  Genomic comparison between pathogenic Streptococcus agalactiae isolated from Nile tilapia in Thailand and fish-derived ST7 strains. , 2015, Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases.

[36]  A. von Haeseler,et al.  IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies , 2014, Molecular biology and evolution.

[37]  C. Buchrieser,et al.  Streptococcus agalactiae clones infecting humans were selected and fixed through the extensive use of tetracycline , 2014, Nature Communications.

[38]  Justin Zobel,et al.  SRST2: Rapid genomic surveillance for public health and hospital microbiology labs , 2014, bioRxiv.

[39]  V. Barbe,et al.  Reductive evolution in Streptococcus agalactiae and the emergence of a host adapted lineage , 2013, BMC Genomics.

[40]  R. Zadoks,et al.  Human Streptococcus agalactiae strains in aquatic mammals and fish , 2013, BMC Microbiology.

[41]  I. Margarit,et al.  Emergence and Global Dissemination of Host-Specific Streptococcus agalactiae Clones , 2010, mBio.

[42]  M. Zamri-Saad,et al.  Pathological changes in red tilapias (Oreochromis spp.) naturally infected by Streptococcus agalactiae. , 2010, Journal of comparative pathology.

[43]  W. Schaffner,et al.  Increasing burden of invasive group B streptococcal disease in nonpregnant adults, 1990-2007. , 2009, Clinical infectious diseases : an official publication of the Infectious Diseases Society of America.

[44]  P. Klesius,et al.  Human Streptococcus agalactiae Isolate in Nile Tilapia (Oreochromis niloticus) , 2009, Emerging infectious diseases.

[45]  C. Iregui,et al.  Streptococcosis on a red tilapia, Oreochromis sp., farm: a case study. , 2009, Journal of fish diseases.

[46]  Joyce J. Evans,et al.  Phylogenetic relationships among Streptococcus agalactiae isolated from piscine, dolphin, bovine and human sources: a dolphin and piscine lineage associated with a fish epidemic in Kuwait is also associated with human neonatal infections in Japan. , 2008, Journal of medical microbiology.

[47]  AlsharapySamer Ahmed,et al.  Molecular investigation of Streptococcus agalactiae isolates from environmental samples and fish specimens during a massive fish kill in Kuwait Bay. , 2008, Pakistan journal of biological sciences : PJBS.

[48]  F. Kong,et al.  Identification of a Streptococcus agalactiae Serotype III Subtype 4 Clone in Association with Adult Invasive Disease in Hong Kong , 2006, Journal of Clinical Microbiology.

[49]  J. Qasem,et al.  Isolation of Streptococcus agalactiae from cultured silver pomfret, Pampus argenteus (Euphrasen), in Kuwait. , 2004, Journal of fish diseases.

[50]  Philippe Glaser,et al.  Multilocus Sequence Typing System for Group B Streptococcus , 2003, Journal of Clinical Microbiology.

[51]  P. Klesius,et al.  Characterization of β‐haemolytic Group B Streptococcus agalactiae in cultured seabream, Sparus auratus L., and wild mullet, Liza klunzingeri (Day), in Kuwait , 2002 .

[52]  F. Kong,et al.  Serotype Identification of Group B Streptococci by PCR and Sequencing , 2002, Journal of Clinical Microbiology.

[53]  K. Chow,et al.  Group B streptococcal meningitis in adults: recent increase in Southeast Asia. , 2000, Australian and New Zealand journal of medicine.

[54]  R. Thune,et al.  A NON-HEMOLYTIC, GROUP B STREPTOCOCCUS INFECTION OF CULTURED BULLFROGS, RANA CATESBEIANA, IN BRAZIL , 1983, Journal of wildlife diseases.

[55]  D. Ryder,et al.  Streptococcus agalactiae Multilocus sequence type 261 is associated with mortalities in the emerging Ghanaian tilapia industry. , 2018, Journal of fish diseases.