One hypervirulent clone, sequence type 283, accounts for a large proportion of invasive Streptococcus agalactiae isolated from humans and diseased tilapia in Southeast Asia.
Adolescent
Adult
Aged
Aged, 80 and over
Animals
Asia, Southeastern
/ epidemiology
Child
Child, Preschool
Female
Fish Diseases
/ epidemiology
Foodborne Diseases
/ epidemiology
Genotype
Humans
Infant
Infant, Newborn
Male
Middle Aged
Molecular Epidemiology
Multilocus Sequence Typing
Phylogeny
Pregnancy
Streptococcal Infections
/ epidemiology
Streptococcus agalactiae
/ classification
Tilapia
Whole Genome Sequencing
Young Adult
Journal
PLoS neglected tropical diseases
ISSN: 1935-2735
Titre abrégé: PLoS Negl Trop Dis
Pays: United States
ID NLM: 101291488
Informations de publication
Date de publication:
06 2019
06 2019
Historique:
received:
09
01
2019
accepted:
29
04
2019
entrez:
28
6
2019
pubmed:
28
6
2019
medline:
28
11
2019
Statut:
epublish
Résumé
In 2015, Singapore had the first and only reported foodborne outbreak of invasive disease caused by the group B Streptococcus (GBS; Streptococcus agalactiae). Disease, predominantly septic arthritis and meningitis, was associated with sequence type (ST)283, acquired from eating raw farmed freshwater fish. Although GBS sepsis is well-described in neonates and older adults with co-morbidities, this outbreak affected non-pregnant and younger adults with fewer co-morbidities, suggesting greater virulence. Before 2015 ST283 had only been reported from twenty humans in Hong Kong and two in France, and from one fish in Thailand. We hypothesised that ST283 was causing region-wide infection in Southeast Asia. We performed a literature review, whole genome sequencing on 145 GBS isolates collected from six Southeast Asian countries, and phylogenetic analysis on 7,468 GBS sequences including 227 variants of ST283 from humans and animals. Although almost absent outside Asia, ST283 was found in all invasive Asian collections analysed, from 1995 to 2017. It accounted for 29/38 (76%) human isolates in Lao PDR, 102/139 (73%) in Thailand, 4/13 (31%) in Vietnam, and 167/739 (23%) in Singapore. ST283 and its variants were found in 62/62 (100%) tilapia from 14 outbreak sites in Malaysia and Vietnam, in seven fish species in Singapore markets, and a diseased frog in China. GBS ST283 is widespread in Southeast Asia, where it accounts for a large proportion of bacteraemic GBS, and causes disease and economic loss in aquaculture. If human ST283 is fishborne, as in the Singapore outbreak, then GBS sepsis in Thailand and Lao PDR is predominantly a foodborne disease. However, whether transmission is from aquaculture to humans, or vice versa, or involves an unidentified reservoir remains unknown. Creation of cross-border collaborations in human and animal health are needed to complete the epidemiological picture.
Sections du résumé
BACKGROUND
In 2015, Singapore had the first and only reported foodborne outbreak of invasive disease caused by the group B Streptococcus (GBS; Streptococcus agalactiae). Disease, predominantly septic arthritis and meningitis, was associated with sequence type (ST)283, acquired from eating raw farmed freshwater fish. Although GBS sepsis is well-described in neonates and older adults with co-morbidities, this outbreak affected non-pregnant and younger adults with fewer co-morbidities, suggesting greater virulence. Before 2015 ST283 had only been reported from twenty humans in Hong Kong and two in France, and from one fish in Thailand. We hypothesised that ST283 was causing region-wide infection in Southeast Asia.
METHODOLOGY/PRINCIPAL FINDINGS
We performed a literature review, whole genome sequencing on 145 GBS isolates collected from six Southeast Asian countries, and phylogenetic analysis on 7,468 GBS sequences including 227 variants of ST283 from humans and animals. Although almost absent outside Asia, ST283 was found in all invasive Asian collections analysed, from 1995 to 2017. It accounted for 29/38 (76%) human isolates in Lao PDR, 102/139 (73%) in Thailand, 4/13 (31%) in Vietnam, and 167/739 (23%) in Singapore. ST283 and its variants were found in 62/62 (100%) tilapia from 14 outbreak sites in Malaysia and Vietnam, in seven fish species in Singapore markets, and a diseased frog in China.
CONCLUSIONS
GBS ST283 is widespread in Southeast Asia, where it accounts for a large proportion of bacteraemic GBS, and causes disease and economic loss in aquaculture. If human ST283 is fishborne, as in the Singapore outbreak, then GBS sepsis in Thailand and Lao PDR is predominantly a foodborne disease. However, whether transmission is from aquaculture to humans, or vice versa, or involves an unidentified reservoir remains unknown. Creation of cross-border collaborations in human and animal health are needed to complete the epidemiological picture.
Identifiants
pubmed: 31246981
doi: 10.1371/journal.pntd.0007421
pii: PNTD-D-19-00013
pmc: PMC6597049
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, P.H.S.
Systematic Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
e0007421Subventions
Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : Medical Research Council
ID : G1001787
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/P007201/1
Pays : United Kingdom
Déclaration de conflit d'intérêts
I have read the journal's policy and the authors of this manuscript have the following competing interests: SLC and TB are named applicants on a patent for the ST83-specific PCR test used in this study.
Références
PLoS Comput Biol. 2014 Apr 10;10(4):e1003537
pubmed: 24722319
J Fish Dis. 2012 Mar;35(3):173-86
pubmed: 22324342
Front Microbiol. 2019 Jan 23;10:10
pubmed: 30728810
Emerg Infect Dis. 2019 Apr;25(4):776-779
pubmed: 30882311
Front Microbiol. 2017 Mar 28;8:499
pubmed: 28400757
PLoS Comput Biol. 2015 Feb 12;11(2):e1004041
pubmed: 25675341
J Clin Microbiol. 2009 Apr;47(4):1143-8
pubmed: 19158264
Emerg Infect Dis. 2016 Dec;22(12):2097-2103
pubmed: 27869599
J Clin Microbiol. 2010 Apr;48(4):1261-9
pubmed: 20181908
J Fish Dis. 2015 Dec;38(12):1083-7
pubmed: 25643734
Bioinformatics. 2009 Jul 15;25(14):1754-60
pubmed: 19451168
Clin Infect Dis. 2018 Aug 31;67(6):854-860
pubmed: 29509833
Antimicrob Agents Chemother. 2014;58(1):212-20
pubmed: 24145532
J Clin Microbiol. 2002 Jan;40(1):216-26
pubmed: 11773119
Vet Microbiol. 2016 Feb 29;184:64-72
pubmed: 26854346
Int J Infect Dis. 2013 Sep;17(9):e777-80
pubmed: 23453715
BMC Bioinformatics. 2010 Dec 10;11:595
pubmed: 21143983
J Clin Microbiol. 2007 Oct;45(10):3224-9
pubmed: 17699641
Genome Med. 2014 Nov 20;6(11):90
pubmed: 25422674
J Clin Microbiol. 2008 Apr;46(4):1285-91
pubmed: 18287314
Emerg Infect Dis. 2016 Nov;22(11):1970-1973
pubmed: 27767904
J Clin Microbiol. 2004 May;42(5):2161-7
pubmed: 15131184
Aust N Z J Med. 2000 Aug;30(4):462-5
pubmed: 10985511
J Dairy Sci. 2017 Nov;100(11):9294-9297
pubmed: 28918144
Genome Biol. 2004;5(2):R12
pubmed: 14759262
J Clin Microbiol. 2011 Oct;49(10):3652-5
pubmed: 21865428
Nat Commun. 2014 Aug 04;5:4544
pubmed: 25088811
J Clin Rheumatol. 2014 Mar;20(2):74-8
pubmed: 24561409
Emerg Infect Dis. 2017 Dec;23(12):
pubmed: 29148967
Ann Epidemiol. 2007 Nov;17(11):854-62
pubmed: 17689259
J Clin Microbiol. 2011 Aug;49(8):2911-8
pubmed: 21697333
Ecohealth. 2015 Sep;12(3):480-9
pubmed: 25561382
mBio. 2010 Aug 24;1(3):
pubmed: 20824105
J Clin Microbiol. 2003 Jun;41(6):2530-6
pubmed: 12791877
J Appl Microbiol. 2017 Jun;122(6):1497-1507
pubmed: 28295891
Clin Infect Dis. 2017 May 15;64(suppl_2):S145-S152
pubmed: 28475781
Euro Surveill. 2018 May;23(21):
pubmed: 29845930
J Fish Dis. 2013 Aug;36(8):735-9
pubmed: 23347250
Mol Biol Evol. 2012 Aug;29(8):1969-73
pubmed: 22367748
J Antimicrob Chemother. 2010 Sep;65(9):1907-14
pubmed: 20584746
Am J Trop Med Hyg. 2014 Aug;91(2):384-8
pubmed: 24980495
Clin Microbiol Infect. 2018 Aug;24(8):923-925
pubmed: 29655956
J Fish Dis. 2016 Jan;39(1):13-29
pubmed: 25399660
J Mammary Gland Biol Neoplasia. 2011 Dec;16(4):357-72
pubmed: 21968538
Emerg Infect Dis. 2016 Nov;22(11):1974-1977
pubmed: 27767905
Emerg Infect Dis. 2016 Oct;22(10):1800-3
pubmed: 27648702
J Clin Microbiol. 2005 Aug;43(8):3727-33
pubmed: 16081902
J Med Microbiol. 2008 Nov;57(Pt 11):1369-76
pubmed: 18927414
Am J Trop Med Hyg. 2009 Aug;81(2):190-4
pubmed: 19635868
J Dairy Sci. 2015 Oct;98(10):6913-24
pubmed: 26233443
Clin Infect Dis. 2014 May;58(9):1211-8
pubmed: 24647013
Nucleic Acids Res. 2012 Dec;40(22):11189-201
pubmed: 23066108
Front Microbiol. 2018 Jul 10;9:1482
pubmed: 30042741
J Clin Microbiol. 2009 Mar;47(3):800-3
pubmed: 19109468
J Med Microbiol. 2016 Mar;65(3):247-254
pubmed: 26701807
BMC Microbiol. 2013 Feb 18;13:41
pubmed: 23419028
Transbound Emerg Dis. 2012 Aug;59(4):369-75
pubmed: 22146014
PLoS One. 2010 Mar 10;5(3):e9490
pubmed: 20224823
Appl Environ Microbiol. 2018 Aug 1;84(16):
pubmed: 29915111
J Clin Microbiol. 2015 Sep;53(9):2919-26
pubmed: 26135871
PLoS One. 2013 Jul 10;8(7):e67755
pubmed: 23874442
Genome Announc. 2016 Mar 24;4(2):
pubmed: 27013037
Genome Announc. 2015 Oct 22;3(5):
pubmed: 26494662
J Clin Microbiol. 2012 Apr;50(4):1219-27
pubmed: 22219307
Nucleic Acids Res. 2012 Jan;40(1):e6
pubmed: 22064866
PLoS One. 2018 Dec 10;13(12):e0208990
pubmed: 30532177
Environ Pollut. 2014 Aug;191:8-16
pubmed: 24780637
J Clin Microbiol. 2006 Nov;44(11):4252-4
pubmed: 17005749
Sci Rep. 2017 Oct 19;7(1):13538
pubmed: 29051505
Clin Microbiol Infect. 2016 Apr;22(4):379.e9-379.e16
pubmed: 26691681
BMC Bioinformatics. 2009 Dec 15;10:421
pubmed: 20003500