Multilocus Sequence Typing and Staphylococcal Protein A Typing Revealed Novel and Diverse Clones of Methicillin-Resistant Staphylococcus aureus in Seafood and the Aquatic Environment

Methicillin-resistant Staphylococcus aureus (MRSA) has been a global health concern since the 1960s, and isolation of this pathogen from food-producing animals has been increasing. However, little information is available on the prevalence of MRSA and its clonal characteristics in seafood and the aq...

Full description

Saved in:
Bibliographic Details
Published inJournal of food protection Vol. 80; no. 3; pp. 476 - 481
Main Authors Murugadas, V, Toms, C Joseph, Reethu, Sara A, Lalitha, K V
Format Journal Article
LanguageEnglish
Published United States 01.03.2017
Subjects
Online AccessGet full text

Cover

Loading…
Abstract Methicillin-resistant Staphylococcus aureus (MRSA) has been a global health concern since the 1960s, and isolation of this pathogen from food-producing animals has been increasing. However, little information is available on the prevalence of MRSA and its clonal characteristics in seafood and the aquatic environment. In this study, 267 seafood and aquatic environment samples were collected from three districts of Kerala, India. Staphylococcal protein A (spa) typing and multilocus sequence typing (MLST) was performed for 65 MRSA strains isolated from 20 seafood and aquatic environment samples. The MRSA clonal profiles were t657-ST772, t002-ST5, t334-ST5, t311-ST5, t121-ST8, t186-ST88, t127-ST1, and two non-spa assignable strains. Whole spa gene sequence analysis along with MLST confirmed one strain as t711-ST6 and another as a novel MRSA clone identified for the first time in seafood and the aquatic environment with a t15669 spa type and a new MLST profile of ST420-256-236-66-82-411-477. The MRSA strains were clustered into five clonal complexes based on the goeBURST algorithm, indicating high diversity among MRSA strains in seafood and the aquatic environment. The novel clone formed a separate clonal complex with matches to three loci. This study recommends large-scale spa typing and MLST of MRSA isolates from seafood and the aquatic environment to determine the prevalence of new MRSA clones. This monitoring process can be useful for tracing local spread of MRSA isolates into the seafood production chain in a defined geographical area.
AbstractList Methicillin-resistant Staphylococcus aureus (MRSA) has been a global health concern since the 1960s, and isolation of this pathogen from food-producing animals has been increasing. However, little information is available on the prevalence of MRSA and its clonal characteristics in seafood and the aquatic environment. In this study, 267 seafood and aquatic environment samples were collected from three districts of Kerala, India. Staphylococcal protein A (spa) typing and multilocus sequence typing (MLST) was performed for 65 MRSA strains isolated from 20 seafood and aquatic environment samples. The MRSA clonal profiles were t657-ST772, t002-ST5, t334-ST5, t311-ST5, t121-ST8, t186-ST88, t127-ST1, and two non-spa assignable strains. Whole spa gene sequence analysis along with MLST confirmed one strain as t711-ST6 and another as a novel MRSA clone identified for the first time in seafood and the aquatic environment with a t15669 spa type and a new MLST profile of ST420-256-236-66-82-411-477. The MRSA strains were clustered into five clonal complexes based on the goeBURST algorithm, indicating high diversity among MRSA strains in seafood and the aquatic environment. The novel clone formed a separate clonal complex with matches to three loci. This study recommends large-scale spa typing and MLST of MRSA isolates from seafood and the aquatic environment to determine the prevalence of new MRSA clones. This monitoring process can be useful for tracing local spread of MRSA isolates into the seafood production chain in a defined geographical area.
Author Toms, C Joseph
Reethu, Sara A
Murugadas, V
Lalitha, K V
Author_xml – sequence: 1
  givenname: V
  surname: Murugadas
  fullname: Murugadas, V
  organization: MFB Division, ICAR-Central Institute of Fisheries Technology, CIFT Junction, Willingdon Island, Matsyapuri P.O., Cochin-682 029, Kerala, India
– sequence: 2
  givenname: C Joseph
  surname: Toms
  fullname: Toms, C Joseph
  organization: MFB Division, ICAR-Central Institute of Fisheries Technology, CIFT Junction, Willingdon Island, Matsyapuri P.O., Cochin-682 029, Kerala, India
– sequence: 3
  givenname: Sara A
  surname: Reethu
  fullname: Reethu, Sara A
  organization: MFB Division, ICAR-Central Institute of Fisheries Technology, CIFT Junction, Willingdon Island, Matsyapuri P.O., Cochin-682 029, Kerala, India
– sequence: 4
  givenname: K V
  surname: Lalitha
  fullname: Lalitha, K V
  organization: MFB Division, ICAR-Central Institute of Fisheries Technology, CIFT Junction, Willingdon Island, Matsyapuri P.O., Cochin-682 029, Kerala, India
BackLink https://www.ncbi.nlm.nih.gov/pubmed/28207309$$D View this record in MEDLINE/PubMed
BookMark eNpVkc1O3DAUha2Kqgy0b1BVXnYTsJ3EiZejKRQQtIihUneW49x0jDx2sJ1R58V4PjzAVOrqLu455_58R-jAeQcIfabkpCppfUpKzgrC2r8nD8NYUF4wTt6hGRVVVQgimgM020t-H6KjGB8IIUww_gEdspaRpiRihp5uJpuM9XqKeAmPEzgN-H47GvcHK9fjZVLjapv7Xmtl8W3wCYzD873mDjagLPT4h9-AfbF8MxsIEfDC5oUj9gO-gbQy2lhrXHEH0cSkXPovOk9XU4BccvgS1OB9_xKWVoDnj5NKRuMztzHBuzW49BG9H5SN8OmtHqNf52f3i4vi-uf3y8X8utAVFamouqGrG6LqKl8smGiaUnMOgg2EgyKa6poq0nSs4h3vWT3UmlFQWrQ11NCR8hh9fc0dg8_PiUmuTdRgrXLgpyhpy4XgomnLLK1epTr4GAMMcgxmrcJWUiJ3xOQOh9zhkFfnt5JymYll25e3CVO3hv6faY-ofAazuphe
CitedBy_id crossref_primary_10_11150_kansenshogakuzasshi_94_186
crossref_primary_10_1016_j_foodcont_2018_02_045
crossref_primary_10_1089_fpd_2017_2336
crossref_primary_10_1016_j_jgar_2018_10_005
crossref_primary_10_1007_s13213_019_01484_5
crossref_primary_10_1111_1750_3841_14915
crossref_primary_10_1111_1758_2229_12995
crossref_primary_10_1128_spectrum_00342_22
Cites_doi 10.4236/aim.2016.66039
10.1186/1471-2180-12-64
10.1128/JCM.00113-06
10.1128/JCM.00071-08
10.1128/JCM.37.11.3556-3563.1999
10.4315/0362-028X-73.12.2285
10.1128/JCM.42.11.4947-4955.2004
10.1016/j.ijfoodmicro.2007.04.006
10.1016/j.fm.2015.04.007
10.1016/j.foodcont.2006.12.007
10.1016/j.vetmic.2010.02.004
10.1016/j.mib.2007.08.003
10.1099/jmm.0.017632-0
10.1128/JCM.43.10.5150-5157.2005
10.1093/jac/dki372
10.1128/JCM.42.2.792-799.2004
10.1111/jam.12186
10.1016/j.ijfoodmicro.2012.03.022
10.1128/JCM.00941-09
10.1128/AAC.47.12.3926-3934.2003
10.1111/lam.12304
10.1016/j.nmni.2015.05.003
10.1111/j.1574-6968.2008.01482.x
10.1111/j.1469-0691.2009.03110.x
10.1093/jac/dkl394
10.1111/j.1574-6968.2010.02151.x
10.1007/BF01586186
10.1128/JCM.01599-07
10.1186/1471-2180-14-63
10.1016/j.mib.2012.08.003
10.1016/S0966-842X(99)01609-1
10.3201/eid1507.080652
10.1128/JCM.38.3.1008-1015.2000
ContentType Journal Article
DBID CGR
CUY
CVF
ECM
EIF
NPM
AAYXX
CITATION
7X8
DOI 10.4315/0362-028x.jfp-16-260
DatabaseName Medline
MEDLINE
MEDLINE (Ovid)
MEDLINE
MEDLINE
PubMed
CrossRef
MEDLINE - Academic
DatabaseTitle MEDLINE
Medline Complete
MEDLINE with Full Text
PubMed
MEDLINE (Ovid)
CrossRef
MEDLINE - Academic
DatabaseTitleList MEDLINE
Database_xml – sequence: 1
  dbid: NPM
  name: PubMed
  url: https://proxy.k.utb.cz/login?url=http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed
  sourceTypes: Index Database
– sequence: 2
  dbid: EIF
  name: MEDLINE
  url: https://proxy.k.utb.cz/login?url=https://www.webofscience.com/wos/medline/basic-search
  sourceTypes: Index Database
DeliveryMethod fulltext_linktorsrc
Discipline Economics
Public Health
Agriculture
EISSN 1944-9097
EndPage 481
ExternalDocumentID 10_4315_0362_028X_JFP_16_260
28207309
Genre Research Support, Non-U.S. Gov't
Journal Article
GroupedDBID ---
-~X
..I
0R~
0SF
29K
3V.
53G
5GY
7RQ
7WY
7X2
7X7
7XC
883
88E
88I
8C1
8FE
8FH
8FI
8FJ
8FL
8R4
8R5
A8Z
AAHBH
AAIKC
AALRI
AAMNW
AAVBQ
AAXUO
ABCQX
ABDNZ
ABUWG
ACGOD
ACYGS
ADBBV
ADNWM
ADVLN
AEILP
AENEX
AFJKZ
AFKRA
AFRAH
AHMBA
AI.
AITUG
AKRWK
ALIPV
ALMA_UNASSIGNED_HOLDINGS
AMRAJ
ATCPS
AZQEC
BENPR
BEZIV
BHPHI
BPHCQ
BVXVI
CCPQU
CGR
CUY
CVF
D-I
DWQXO
EBS
ECM
EDH
EHX
EIF
EJD
F5P
FDB
FRNLG
FRP
FYUFA
GNUQQ
GROUPED_ABI_INFORM_COMPLETE
GROUPED_DOAJ
HCIFZ
HZ~
IAG
IAO
IGS
INH
INR
K60
K6~
L7B
M0F
M0K
M1P
M2P
NPM
O9-
OK1
P2P
PATMY
PQBIZ
PQBZA
PQQKQ
PROAC
PSQYO
PYCSY
Q2X
SJN
SV3
UBH
VH1
WH7
Y3D
ZE2
ZT4
~KM
AAYXX
CITATION
7X8
ID FETCH-LOGICAL-c419t-4bfb570a54282929773c66e92f06ea0c1c51a07b246b6d25f5c21eac985e5eb03
ISSN 0362-028X
IngestDate Fri Oct 25 07:27:55 EDT 2024
Thu Sep 26 20:04:43 EDT 2024
Sat Sep 28 08:17:22 EDT 2024
IsDoiOpenAccess false
IsOpenAccess true
IsPeerReviewed true
IsScholarly true
Issue 3
Keywords Staphylococcal protein A type diversity
t15669
Nontypeable
Seafood and aquatic environment
Methicillin-resistant Staphylococcus aureus
Language English
LinkModel OpenURL
MergedId FETCHMERGED-LOGICAL-c419t-4bfb570a54282929773c66e92f06ea0c1c51a07b246b6d25f5c21eac985e5eb03
Notes ObjectType-Article-1
SourceType-Scholarly Journals-1
ObjectType-Feature-2
content type line 23
OpenAccessLink https://doi.org/10.4315/0362-028x.jfp-16-260
PMID 28207309
PQID 1869969783
PQPubID 23479
PageCount 6
ParticipantIDs proquest_miscellaneous_1869969783
crossref_primary_10_4315_0362_028X_JFP_16_260
pubmed_primary_28207309
PublicationCentury 2000
PublicationDate 2017-03-00
20170301
PublicationDateYYYYMMDD 2017-03-01
PublicationDate_xml – month: 03
  year: 2017
  text: 2017-03-00
PublicationDecade 2010
PublicationPlace United States
PublicationPlace_xml – name: United States
PublicationTitle Journal of food protection
PublicationTitleAlternate J Food Prot
PublicationYear 2017
References Koreen (10.4315/0362-028X.JFP-16-260_bb0090) 2004; 42
Enright (10.4315/0362-028X.JFP-16-260_bb0065) 1999; 7
Shopsin (10.4315/0362-028X.JFP-16-260_bb0160) 1999; 37
U.S. Food and Drug Administration (10.4315/0362-028X.JFP-16-260_bb0175) 2001
Sergelidis (10.4315/0362-028X.JFP-16-260_bb0150) 2014; 59
Boye (10.4315/0362-028X.JFP-16-260_bb0035) 2011; 314
Normanno (10.4315/0362-028X.JFP-16-260_bb0130) 2015; 51
Frenay (10.4315/0362-028X.JFP-16-260_bb0070) 1996; 15
Ruppitsch (10.4315/0362-028X.JFP-16-260_bb0145) 2006; 44
Kluytmans (10.4315/0362-028X.JFP-16-260_bb0085) 2010; 16
Arakere (10.4315/0362-028X.JFP-16-260_bb0015) 2009; 292
Strommenger (10.4315/0362-028X.JFP-16-260_bb0170) 2008; 46
Votintseva (10.4315/0362-028X.JFP-16-260_bb0185) 2014; 14
Atyah (10.4315/0362-028X.JFP-16-260_bb0020) 2010; 144
Brown (10.4315/0362-028X.JFP-16-260_bb0040) 2005; 56
Shambat (10.4315/0362-028X.JFP-16-260_bb0155) 2012; 12
Denis (10.4315/0362-028X.JFP-16-260_bb0055) 2009; 15
Kumar (10.4315/0362-028X.JFP-16-260_bb0095) 2016; 6
Mediavilla (10.4315/0362-028X.JFP-16-260_bb0100) 2012; 15
Visnuvinayagam (10.4315/0362-028X.JFP-16-260_bb0180) 2015; 36
Normanno (10.4315/0362-028X.JFP-16-260_bb0125) 2007; 117
Nadig (10.4315/0362-028X.JFP-16-260_bb0120) 2010; 59
Bouchiat (10.4315/0362-028X.JFP-16-260_bb0030) 2015; 7
Enright (10.4315/0362-028X.JFP-16-260_bb0060) 2000; 38
Mitra (10.4315/0362-028X.JFP-16-260_bb0110) 2013; 114
Huss (10.4315/0362-028X.JFP-16-260_bb0080) 1988
Aires de Sousa (10.4315/0362-028X.JFP-16-260_bb0010) 2005; 43
Zhang (10.4315/0362-028X.JFP-16-260_bb0190) 2004; 42
Hammad (10.4315/0362-028X.JFP-16-260_bb0075) 2012; 156
Mellmann (10.4315/0362-028X.JFP-16-260_bb0105) 2007; 46
Clinical and Laboratory Standards Institute (10.4315/0362-028X.JFP-16-260_bb0045) 2014
De Lencastre (10.4315/0362-028X.JFP-16-260_bb0050) 2007; 10
Robinson (10.4315/0362-028X.JFP-16-260_bb0140) 2003; 47
Simon (10.4315/0362-028X.JFP-16-260_bb0165) 2007; 18
Rhee (10.4315/0362-028X.JFP-16-260_bb0135) 2010; 73
Baum (10.4315/0362-028X.JFP-16-260_bb0025) 2009; 47
Moodley (10.4315/0362-028X.JFP-16-260_bb0115) 2006; 58
References_xml – volume: 6
  start-page: 399
  year: 2016
  ident: 10.4315/0362-028X.JFP-16-260_bb0095
  article-title: Incidence of methicillin-resistant staphylococci in fresh seafood
  publication-title: Adv. Microbiol
  doi: 10.4236/aim.2016.66039
  contributor:
    fullname: Kumar
– volume: 12
  start-page: 64
  year: 2012
  ident: 10.4315/0362-028X.JFP-16-260_bb0155
  article-title: Clonal complexes and virulence factors of Staphylococcus aureus from several cities in India
  publication-title: BMC Microbiol
  doi: 10.1186/1471-2180-12-64
  contributor:
    fullname: Shambat
– year: 2014
  ident: 10.4315/0362-028X.JFP-16-260_bb0045
  contributor:
    fullname: Clinical and Laboratory Standards Institute
– volume: 44
  start-page: 2442
  year: 2006
  ident: 10.4315/0362-028X.JFP-16-260_bb0145
  article-title: Classifying spa types in complexes improves interpretation of typing results for methicillin-resistant Staphylococcus aureus
  publication-title: J. Clin. Microbiol
  doi: 10.1128/JCM.00113-06
  contributor:
    fullname: Ruppitsch
– volume: 46
  start-page: 2805
  year: 2007
  ident: 10.4315/0362-028X.JFP-16-260_bb0105
  article-title: Characterization of clonal relatedness among the natural population of Staphylococcus aureus strains by using spa sequence typing and the BURP (based upon repeat patterns) algorithm
  publication-title: J. Clin. Microbiol
  doi: 10.1128/JCM.00071-08
  contributor:
    fullname: Mellmann
– volume: 37
  start-page: 3556
  year: 1999
  ident: 10.4315/0362-028X.JFP-16-260_bb0160
  article-title: Evaluation of protein A gene polymorphic region DNA sequencing for typing of Staphylococcus aureus strains
  publication-title: J. Clin. Microbiol
  doi: 10.1128/JCM.37.11.3556-3563.1999
  contributor:
    fullname: Shopsin
– volume: 73
  start-page: 2285
  year: 2010
  ident: 10.4315/0362-028X.JFP-16-260_bb0135
  article-title: Emergence and characterization of foodborne methicillin-resistant Staphylococcus aureus in Korea
  publication-title: J. Food Prot
  doi: 10.4315/0362-028X-73.12.2285
  contributor:
    fullname: Rhee
– volume: 42
  start-page: 4947
  year: 2004
  ident: 10.4315/0362-028X.JFP-16-260_bb0190
  article-title: New quadriplex PCR assay for detection of methicillin and mupirocin resistance and simultaneous discrimination of Staphylococcus aureus from coagulase-negative staphylococci
  publication-title: J. Clin. Microbiol
  doi: 10.1128/JCM.42.11.4947-4955.2004
  contributor:
    fullname: Zhang
– year: 1988
  ident: 10.4315/0362-028X.JFP-16-260_bb0080
  contributor:
    fullname: Huss
– volume: 117
  start-page: 219
  year: 2007
  ident: 10.4315/0362-028X.JFP-16-260_bb0125
  article-title: Methicillin-resistant Staphylococcus aureus (MRSA) in foods of animal origin product in Italy
  publication-title: Int. J. Food Microbiol
  doi: 10.1016/j.ijfoodmicro.2007.04.006
  contributor:
    fullname: Normanno
– volume: 51
  start-page: 51
  year: 2015
  ident: 10.4315/0362-028X.JFP-16-260_bb0130
  article-title: Methicillin-resistant Staphylococcus aureus (MRSA) in slaughtered pigs and abattoir workers in Italy
  publication-title: Food Microbiol
  doi: 10.1016/j.fm.2015.04.007
  contributor:
    fullname: Normanno
– volume: 18
  start-page: 1565
  year: 2007
  ident: 10.4315/0362-028X.JFP-16-260_bb0165
  article-title: Prevalence of enterotoxigenic Staphylococcus aureus in fishery products and fish processing factory workers
  publication-title: Food Control
  doi: 10.1016/j.foodcont.2006.12.007
  contributor:
    fullname: Simon
– volume: 144
  start-page: 502
  year: 2010
  ident: 10.4315/0362-028X.JFP-16-260_bb0020
  article-title: First report of methicillin-resistant Staphylococcus aureus from cage-cultured tilapia (Oreochromis niloticus)
  publication-title: Vet. Microbiol
  doi: 10.1016/j.vetmic.2010.02.004
  contributor:
    fullname: Atyah
– volume: 10
  start-page: 428
  year: 2007
  ident: 10.4315/0362-028X.JFP-16-260_bb0050
  article-title: Antibiotic resistant Staphylococcus aureus: a paradigm of adaptive power
  publication-title: Curr. Opin. Microbiol
  doi: 10.1016/j.mib.2007.08.003
  contributor:
    fullname: De Lencastre
– volume: 59
  start-page: 815
  year: 2010
  ident: 10.4315/0362-028X.JFP-16-260_bb0120
  article-title: Epidemic meticillin-resistant Staphylococcus aureus (EMRSA-15) variants detected in healthy and diseased individuals in India
  publication-title: J. Med. Microbiol
  doi: 10.1099/jmm.0.017632-0
  contributor:
    fullname: Nadig
– volume: 43
  start-page: 5150
  year: 2005
  ident: 10.4315/0362-028X.JFP-16-260_bb0010
  article-title: Comparison of genetic backgrounds of methicillin-resistant and -susceptible Staphylococcus aureus isolates from Portuguese hospitals and the community
  publication-title: J. Clin. Microbiol
  doi: 10.1128/JCM.43.10.5150-5157.2005
  contributor:
    fullname: Aires de Sousa
– volume: 56
  start-page: 1000
  year: 2005
  ident: 10.4315/0362-028X.JFP-16-260_bb0040
  article-title: Guidelines for the laboratory diagnosis and susceptibility testing of methicillin-resistant Staphylococcus aureus (MRSA)
  publication-title: J. Antimicrob. Chemother
  doi: 10.1093/jac/dki372
  contributor:
    fullname: Brown
– volume: 42
  start-page: 792
  year: 2004
  ident: 10.4315/0362-028X.JFP-16-260_bb0090
  article-title: spa Typing method for discriminating among Staphylococcus aureus isolates: implications for use of a single marker to detect genetic micro- and macrovariation
  publication-title: J. Clin. Microbiol
  doi: 10.1128/JCM.42.2.792-799.2004
  contributor:
    fullname: Koreen
– volume: 114
  start-page: 1604
  year: 2013
  ident: 10.4315/0362-028X.JFP-16-260_bb0110
  article-title: Staphylococcus aureus spa type t267, clonal ancestor of bovine subclinical mastitis in India
  publication-title: J. Appl. Microbiol
  doi: 10.1111/jam.12186
  contributor:
    fullname: Mitra
– volume: 156
  start-page: 286
  year: 2012
  ident: 10.4315/0362-028X.JFP-16-260_bb0075
  article-title: Occurrence and characteristics of methicillin-resistant and -susceptible Staphylococcus aureus and methicillin-resistant coagulase-negative staphylococci from Japanese retail ready-to-eat raw fish
  publication-title: Int. J. Food Microbiol
  doi: 10.1016/j.ijfoodmicro.2012.03.022
  contributor:
    fullname: Hammad
– volume: 47
  start-page: 3624
  year: 2009
  ident: 10.4315/0362-028X.JFP-16-260_bb0025
  article-title: Non-spa-typeable clinical Staphylococcus aureus strains are naturally occurring protein A mutants
  publication-title: J. Clin. Microbiol
  doi: 10.1128/JCM.00941-09
  contributor:
    fullname: Baum
– volume: 47
  start-page: 3926
  year: 2003
  ident: 10.4315/0362-028X.JFP-16-260_bb0140
  article-title: Evolutionary models of the emergence of methicillin-resistant Staphylococcus aureus
  publication-title: Antimicrob. Agents Chemother
  doi: 10.1128/AAC.47.12.3926-3934.2003
  contributor:
    fullname: Robinson
– volume: 59
  start-page: 500
  year: 2014
  ident: 10.4315/0362-028X.JFP-16-260_bb0150
  article-title: Isolation of methicillin-resistant Staphylococcus spp. from ready-to-eat fish products
  publication-title: Lett. Appl. Microbiol
  doi: 10.1111/lam.12304
  contributor:
    fullname: Sergelidis
– volume: 7
  start-page: 15
  year: 2015
  ident: 10.4315/0362-028X.JFP-16-260_bb0030
  article-title: Epidemiology of Staphylococcus aureus in Bangalore, India: emergence of the ST217 clone and high rate of resistance to erythromycin and ciprofloxacin in the community
  publication-title: New Microbes New Infect
  doi: 10.1016/j.nmni.2015.05.003
  contributor:
    fullname: Bouchiat
– volume: 292
  start-page: 141
  year: 2009
  ident: 10.4315/0362-028X.JFP-16-260_bb0015
  article-title: A novel type-III staphylococcal cassette chromosome mec (SCCmec) variant among Indian isolates of methicillin-resistant Staphylococcus aureus
  publication-title: FEMS Microbiol. Lett
  doi: 10.1111/j.1574-6968.2008.01482.x
  contributor:
    fullname: Arakere
– volume: 16
  start-page: 11
  year: 2010
  ident: 10.4315/0362-028X.JFP-16-260_bb0085
  article-title: Methicillin-resistant Staphylococcus aureus in food products: cause for concern or case for complacency?
  publication-title: Clin. Microbiol. Infect
  doi: 10.1111/j.1469-0691.2009.03110.x
  contributor:
    fullname: Kluytmans
– volume: 36
  start-page: 571
  year: 2015
  ident: 10.4315/0362-028X.JFP-16-260_bb0180
  article-title: Status on methicillin resistant and multiple drug resistant Staphylococcus aureus in fishes of Cochin and Mumbai coast, India
  publication-title: J. Environ. Biol
  contributor:
    fullname: Visnuvinayagam
– volume: 58
  start-page: 1118
  year: 2006
  ident: 10.4315/0362-028X.JFP-16-260_bb0115
  article-title: spa Typing of methicillin-resistant Staphylococcus aureus isolated from domestic animals and veterinary staff in the UK and Ireland
  publication-title: J. Antimicrob. Chemother
  doi: 10.1093/jac/dkl394
  contributor:
    fullname: Moodley
– volume: 314
  start-page: 101
  year: 2011
  ident: 10.4315/0362-028X.JFP-16-260_bb0035
  article-title: Variations in spa types found in consecutive MRSA isolates from the same patients
  publication-title: FEMS Microbiol. Lett
  doi: 10.1111/j.1574-6968.2010.02151.x
  contributor:
    fullname: Boye
– volume: 15
  start-page: 60
  year: 1996
  ident: 10.4315/0362-028X.JFP-16-260_bb0070
  article-title: Molecular typing of methicillin-resistant Staphylococcus aureus on the basis of protein A gene polymorphism
  publication-title: Eur. J. Clin. Microbiol. Infect. Dis
  doi: 10.1007/BF01586186
  contributor:
    fullname: Frenay
– year: 2001
  ident: 10.4315/0362-028X.JFP-16-260_bb0175
  contributor:
    fullname: U.S. Food and Drug Administration
– volume: 46
  start-page: 574
  year: 2008
  ident: 10.4315/0362-028X.JFP-16-260_bb0170
  article-title: spa Typing of Staphylococcus aureus as a frontline tool in epidemiological typing
  publication-title: J. Clin. Microbiol
  doi: 10.1128/JCM.01599-07
  contributor:
    fullname: Strommenger
– volume: 14
  start-page: 63
  year: 2014
  ident: 10.4315/0362-028X.JFP-16-260_bb0185
  article-title: Prevalence of Staphylococcus aureus protein A (spa) mutants in the community and hospitals in Oxfordshire
  publication-title: BMC Microbiol
  doi: 10.1186/1471-2180-14-63
  contributor:
    fullname: Votintseva
– volume: 15
  start-page: 588
  year: 2012
  ident: 10.4315/0362-028X.JFP-16-260_bb0100
  article-title: Global epidemiology of community-associated methicillin resistant Staphylococcus aureus (CA-MRSA)
  publication-title: Curr. Opin. Microbiol
  doi: 10.1016/j.mib.2012.08.003
  contributor:
    fullname: Mediavilla
– volume: 7
  start-page: 482
  year: 1999
  ident: 10.4315/0362-028X.JFP-16-260_bb0065
  article-title: Multilocus sequence typing
  publication-title: Trends Microbiol
  doi: 10.1016/S0966-842X(99)01609-1
  contributor:
    fullname: Enright
– volume: 15
  start-page: 1098
  year: 2009
  ident: 10.4315/0362-028X.JFP-16-260_bb0055
  article-title: Methicillin-resistant Staphylococcus aureus ST398 in swine farm personnel, Belgium
  publication-title: Emerg. Infect. Dis
  doi: 10.3201/eid1507.080652
  contributor:
    fullname: Denis
– volume: 38
  start-page: 1008
  year: 2000
  ident: 10.4315/0362-028X.JFP-16-260_bb0060
  article-title: Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus
  publication-title: J. Clin. Microbiol
  doi: 10.1128/JCM.38.3.1008-1015.2000
  contributor:
    fullname: Enright
SSID ssj0002926
Score 2.2949386
Snippet Methicillin-resistant Staphylococcus aureus (MRSA) has been a global health concern since the 1960s, and isolation of this pathogen from food-producing animals...
SourceID proquest
crossref
pubmed
SourceType Aggregation Database
Index Database
StartPage 476
SubjectTerms Animals
India
Methicillin
Methicillin-Resistant Staphylococcus aureus - isolation & purification
Microbial Sensitivity Tests
Multilocus Sequence Typing
Seafood
Staphylococcal Infections - epidemiology
Staphylococcal Protein A
Title Multilocus Sequence Typing and Staphylococcal Protein A Typing Revealed Novel and Diverse Clones of Methicillin-Resistant Staphylococcus aureus in Seafood and the Aquatic Environment
URI https://www.ncbi.nlm.nih.gov/pubmed/28207309
https://search.proquest.com/docview/1869969783
Volume 80
hasFullText 1
inHoldings 1
isFullTextHit
isPrint
link http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV1Lj9MwELa6uwdACEF5lcfKSNwqlyS13eZYSlerBaqq7Eq9RU7irISgLW2yQvwwrvw1ZvxIW9RKwCWq8hhH_b6MZ8YzY0Je4yTGg6LP-rlKGY9Ul8W55IzrTAQqwvYkGND_OJbnV_xiJmaNxq-trKWqTDvZj711Jf-DKpwDXLFK9h-QrYXCCfgN-MIREIbjX2FsqmdhNqrW8M3blOg2OJa-7hAMSfgT4foiQyQm2JIBwxv-nqm-QTMxb48XN9q2DHhn0jR0e_gFe_ib_BiNGfEYlZmzqV6juTkvd0TD6Kpa6cpk1n7SqsBGyT4xc_CtMj1hR5uCugP2sHnMtY3YSg4AJlTXKld-13YfFLchonoJw68baXjdyoe6N4HaD-hu2LWt906KC3XA9FnnenW0Vc8x5ywObEav1992JyjH0-6WMuZ2Z5k_JwkwmUw_DawXA-vqe-dzsWShZJHd2GCLN8uvhjjglaIijDdTZp3I6C8dkZMINB2o2JO3o_FkWhsDURxJW7GJw77ZNyj2o3Zido2jAx6PsXwu75N7DiI6sPx7QBp63iR3Btcr17ZFN8ktX9--bpK7NhJMbYHbQ_Jzw1LqWUotAymwhO6ylDqW0oG_x7OUGpaaRxxLqWUpXRR0L0vpLkupZSkF4Y6lRhiwlDqW0i2WPiJXZ6PL4Tlzu4WwjIdxyXhapKIXKMExOSACv6abSanjqAikVkEWZiJUQS-NuExlHolCZFEIZkfcF1roNOg-JsdzeOunhBZxADZCnMkikzzUIgUfoS8lTmAh74m8RZiHKVnapjAJONOIcIIIJ4DwLLk4myShTADhFnnlsUxAe-OSnJrrRbVOcEO4WGL4tUWeWJBriZ4Uzw5eeU5ubz6TF-S4XFX6JdjIZXpKjnqzHhz7w_DUcfI3XrLDMw
link.rule.ids 315,783,787,27936,27937,31732,33279,33757
linkProvider ProQuest
openUrl ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Multilocus+Sequence+Typing+and+Staphylococcal+Protein+A+Typing+Revealed+Novel+and+Diverse+Clones+of+Methicillin-Resistant+Staphylococcus+aureus+in+Seafood+and+the+Aquatic+Environment&rft.jtitle=Journal+of+food+protection&rft.au=Murugadas%2C+V&rft.au=Toms%2C+C+Joseph&rft.au=Reethu%2C+Sara+A&rft.au=Lalitha%2C+K+V&rft.date=2017-03-01&rft.eissn=1944-9097&rft.volume=80&rft.issue=3&rft.spage=476&rft_id=info:doi/10.4315%2F0362-028x.jfp-16-260&rft_id=info%3Apmid%2F28207309&rft.externalDocID=28207309
thumbnail_l http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=0362-028X&client=summon
thumbnail_m http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=0362-028X&client=summon
thumbnail_s http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=0362-028X&client=summon