Prevalence, genetic characterization and virulence genes of sorbitol-fermenting Escherichia coli O157:H- and E. coli O157:H7 isolated from retail beef

Sorbitol-fermenting (SF) Escherichia coli O157:H- strains have emerged as important pathogens and have been associated with a higher incidence of progression to hemolytic–uremic syndrome (HUS) than non-sorbitol fermenting (NSF) E. coli O157:H7. The present study was carried out to determine the prev...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:International journal of food microbiology 2013-08, Vol.165 (3), p.295-301
Hauptverfasser: Sallam, Khalid Ibrahim, Mohammed, Mahmoud Ahmed, Ahdy, Asmaa Mohammed, Tamura, Tomohiro
Format: Artikel
Sprache:eng
Schlagworte:
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
container_end_page 301
container_issue 3
container_start_page 295
container_title International journal of food microbiology
container_volume 165
creator Sallam, Khalid Ibrahim
Mohammed, Mahmoud Ahmed
Ahdy, Asmaa Mohammed
Tamura, Tomohiro
description Sorbitol-fermenting (SF) Escherichia coli O157:H- strains have emerged as important pathogens and have been associated with a higher incidence of progression to hemolytic–uremic syndrome (HUS) than non-sorbitol fermenting (NSF) E. coli O157:H7. The present study was carried out to determine the prevalence of SF E. coli O157:H- and NSF E. coli O157:H7 strains in retail beef products in Mansoura, Egypt. The contamination rates with rfbEO157-positive E. coli O157 strains were 26.7% (8/30), 10% (3/30) and 3.7% (1/27) in ground beef, beef burger, and fresh beef samples, respectively with an overall mean of 13.8% (12/87) among all meat products tested. SF E. coli O157:H- were the most dominant among the isolated O157 strains. Of the fifteen O157 strains isolated, 11 (73.3%) were SF E. coli O157:H-, while the remaining 4 (26.7%) were NSF E. coli O157:H7. The 11 SF O157H- strains were genetically positive for sfpA gene. Restriction fragment length polymorphism (RFLP) analysis for fliC gene demonstrated a similar pattern for both SF and NSF O157 isolates. PCR assays verified the existence of stx1 gene in 7 (46.7%) and stx2 gene in 13 (86.7%) of the 15 O157 strains isolated. Unexpectedly, two of the 15 O157 strains isolated were negative for Shiga toxin genes. The eae gene was identified in all of the 15 O157 strains except in one NSF O157:H7 strain. EHEC-hlyA gene was detected in 14 (93.3%) of the 15 O157 isolates, nonetheless only 11 strains showed enterohemolytic phenotype on blood agar. A combination of the four virulence genes, stx1, stx2, eae and EHEC-hlyA were detected in 7 (46.7%) strains, while six (40%) strains were positive for stx2, eae and hlyA genes. This is the first record for isolation of E. coli O157: H- in Egypt as well as in the African continent. •This is the first record for isolation of E. coli O157:H- in the African continent.•We identified many sorbitol-fermenting E. coli O157:H- that contained stx1 gene.•We detected two non-Shiga toxigenic O157 strains that lacked stx1 and stx2.•SF E. coli O157:H- was the most dominant among the isolated O157 strains from beef.
doi_str_mv 10.1016/j.ijfoodmicro.2013.05.024
format Article
fullrecord <record><control><sourceid>proquest_cross</sourceid><recordid>TN_cdi_proquest_miscellaneous_1500778338</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><els_id>S0168160513002717</els_id><sourcerecordid>1412161651</sourcerecordid><originalsourceid>FETCH-LOGICAL-c454t-f48f30a0df382da6731ff9326de1fd7bbdd2a57291e9a3ea2e8031eba318a5983</originalsourceid><addsrcrecordid>eNqNkU2P0zAQhi0EYkvhLyBzQOJAgj_iOOG2qgqLtNJygLM1scdbV0m82Gkl-CH8XtIPYI89WRo974xnHkLecFZyxusP2zJsfYxuCDbFUjAuS6ZKJqonZMEb3RayqtlTspjZpuA1U1fkRc5bxpiSkj0nV0I2TCrNF-T314R76HG0-J7e44hTsNRuIIGdMIVfMIU4Uhgd3Ye0O3JHLNPoaY6pC1PsC49pwHEK4z1dZ7uZg3YTgNrYB3rHlf54Uxx7rMvHNU1Djj1M6KhPcaAJJwg97RD9S_LMQ5_x1fldku-f1t9WN8Xt3ecvq-vbwlaqmgpfNV4yYM7LRjioteTet1LUDrl3uuucE6C0aDm2IBEEzntz7EDyBlTbyCV5d-r7kOKPHebJDCFb7HsYMe6y4YoxrRspL0CrSh7OysUFKBe85rXiM9qe0Nlkzgm9eUhhgPTTcGYOss3WPJJtDrINU2aWPWdfn8fsugHdv-RfuzPw9gxAttD7BKMN-T-na6GbmV2S1YnD-dT7gMlkGw6qXUhoJ-NiuOA7fwBxCM20</addsrcrecordid><sourcetype>Aggregation Database</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>1412161651</pqid></control><display><type>article</type><title>Prevalence, genetic characterization and virulence genes of sorbitol-fermenting Escherichia coli O157:H- and E. coli O157:H7 isolated from retail beef</title><source>MEDLINE</source><source>Access via ScienceDirect (Elsevier)</source><creator>Sallam, Khalid Ibrahim ; Mohammed, Mahmoud Ahmed ; Ahdy, Asmaa Mohammed ; Tamura, Tomohiro</creator><creatorcontrib>Sallam, Khalid Ibrahim ; Mohammed, Mahmoud Ahmed ; Ahdy, Asmaa Mohammed ; Tamura, Tomohiro</creatorcontrib><description>Sorbitol-fermenting (SF) Escherichia coli O157:H- strains have emerged as important pathogens and have been associated with a higher incidence of progression to hemolytic–uremic syndrome (HUS) than non-sorbitol fermenting (NSF) E. coli O157:H7. The present study was carried out to determine the prevalence of SF E. coli O157:H- and NSF E. coli O157:H7 strains in retail beef products in Mansoura, Egypt. The contamination rates with rfbEO157-positive E. coli O157 strains were 26.7% (8/30), 10% (3/30) and 3.7% (1/27) in ground beef, beef burger, and fresh beef samples, respectively with an overall mean of 13.8% (12/87) among all meat products tested. SF E. coli O157:H- were the most dominant among the isolated O157 strains. Of the fifteen O157 strains isolated, 11 (73.3%) were SF E. coli O157:H-, while the remaining 4 (26.7%) were NSF E. coli O157:H7. The 11 SF O157H- strains were genetically positive for sfpA gene. Restriction fragment length polymorphism (RFLP) analysis for fliC gene demonstrated a similar pattern for both SF and NSF O157 isolates. PCR assays verified the existence of stx1 gene in 7 (46.7%) and stx2 gene in 13 (86.7%) of the 15 O157 strains isolated. Unexpectedly, two of the 15 O157 strains isolated were negative for Shiga toxin genes. The eae gene was identified in all of the 15 O157 strains except in one NSF O157:H7 strain. EHEC-hlyA gene was detected in 14 (93.3%) of the 15 O157 isolates, nonetheless only 11 strains showed enterohemolytic phenotype on blood agar. A combination of the four virulence genes, stx1, stx2, eae and EHEC-hlyA were detected in 7 (46.7%) strains, while six (40%) strains were positive for stx2, eae and hlyA genes. This is the first record for isolation of E. coli O157: H- in Egypt as well as in the African continent. •This is the first record for isolation of E. coli O157:H- in the African continent.•We identified many sorbitol-fermenting E. coli O157:H- that contained stx1 gene.•We detected two non-Shiga toxigenic O157 strains that lacked stx1 and stx2.•SF E. coli O157:H- was the most dominant among the isolated O157 strains from beef.</description><identifier>ISSN: 0168-1605</identifier><identifier>EISSN: 1879-3460</identifier><identifier>DOI: 10.1016/j.ijfoodmicro.2013.05.024</identifier><identifier>PMID: 23803571</identifier><identifier>CODEN: IJFMDD</identifier><language>eng</language><publisher>Amsterdam: Elsevier B.V</publisher><subject>Agar ; Animals ; Beef ; Biological and medical sciences ; Cattle ; Egypt ; Escherichia coli ; Escherichia coli O157 - genetics ; Escherichia coli O157 - isolation &amp; purification ; Escherichia coli O157 - pathogenicity ; Food industries ; Food Microbiology ; Fundamental and applied biological sciences. Psychology ; Meat - microbiology ; Meat and meat product industries ; O157:H7 ; Polymerase Chain Reaction ; Shiga Toxin - genetics ; Sorbitol - metabolism ; Sorbitol-fermenting ; Virulence Factors - genetics ; Virulence genes</subject><ispartof>International journal of food microbiology, 2013-08, Vol.165 (3), p.295-301</ispartof><rights>2013</rights><rights>2014 INIST-CNRS</rights><rights>Copyright © 2013. Published by Elsevier B.V.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c454t-f48f30a0df382da6731ff9326de1fd7bbdd2a57291e9a3ea2e8031eba318a5983</citedby><cites>FETCH-LOGICAL-c454t-f48f30a0df382da6731ff9326de1fd7bbdd2a57291e9a3ea2e8031eba318a5983</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.ijfoodmicro.2013.05.024$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,780,784,3550,27924,27925,45995</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&amp;idt=27627880$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23803571$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Sallam, Khalid Ibrahim</creatorcontrib><creatorcontrib>Mohammed, Mahmoud Ahmed</creatorcontrib><creatorcontrib>Ahdy, Asmaa Mohammed</creatorcontrib><creatorcontrib>Tamura, Tomohiro</creatorcontrib><title>Prevalence, genetic characterization and virulence genes of sorbitol-fermenting Escherichia coli O157:H- and E. coli O157:H7 isolated from retail beef</title><title>International journal of food microbiology</title><addtitle>Int J Food Microbiol</addtitle><description>Sorbitol-fermenting (SF) Escherichia coli O157:H- strains have emerged as important pathogens and have been associated with a higher incidence of progression to hemolytic–uremic syndrome (HUS) than non-sorbitol fermenting (NSF) E. coli O157:H7. The present study was carried out to determine the prevalence of SF E. coli O157:H- and NSF E. coli O157:H7 strains in retail beef products in Mansoura, Egypt. The contamination rates with rfbEO157-positive E. coli O157 strains were 26.7% (8/30), 10% (3/30) and 3.7% (1/27) in ground beef, beef burger, and fresh beef samples, respectively with an overall mean of 13.8% (12/87) among all meat products tested. SF E. coli O157:H- were the most dominant among the isolated O157 strains. Of the fifteen O157 strains isolated, 11 (73.3%) were SF E. coli O157:H-, while the remaining 4 (26.7%) were NSF E. coli O157:H7. The 11 SF O157H- strains were genetically positive for sfpA gene. Restriction fragment length polymorphism (RFLP) analysis for fliC gene demonstrated a similar pattern for both SF and NSF O157 isolates. PCR assays verified the existence of stx1 gene in 7 (46.7%) and stx2 gene in 13 (86.7%) of the 15 O157 strains isolated. Unexpectedly, two of the 15 O157 strains isolated were negative for Shiga toxin genes. The eae gene was identified in all of the 15 O157 strains except in one NSF O157:H7 strain. EHEC-hlyA gene was detected in 14 (93.3%) of the 15 O157 isolates, nonetheless only 11 strains showed enterohemolytic phenotype on blood agar. A combination of the four virulence genes, stx1, stx2, eae and EHEC-hlyA were detected in 7 (46.7%) strains, while six (40%) strains were positive for stx2, eae and hlyA genes. This is the first record for isolation of E. coli O157: H- in Egypt as well as in the African continent. •This is the first record for isolation of E. coli O157:H- in the African continent.•We identified many sorbitol-fermenting E. coli O157:H- that contained stx1 gene.•We detected two non-Shiga toxigenic O157 strains that lacked stx1 and stx2.•SF E. coli O157:H- was the most dominant among the isolated O157 strains from beef.</description><subject>Agar</subject><subject>Animals</subject><subject>Beef</subject><subject>Biological and medical sciences</subject><subject>Cattle</subject><subject>Egypt</subject><subject>Escherichia coli</subject><subject>Escherichia coli O157 - genetics</subject><subject>Escherichia coli O157 - isolation &amp; purification</subject><subject>Escherichia coli O157 - pathogenicity</subject><subject>Food industries</subject><subject>Food Microbiology</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Meat - microbiology</subject><subject>Meat and meat product industries</subject><subject>O157:H7</subject><subject>Polymerase Chain Reaction</subject><subject>Shiga Toxin - genetics</subject><subject>Sorbitol - metabolism</subject><subject>Sorbitol-fermenting</subject><subject>Virulence Factors - genetics</subject><subject>Virulence genes</subject><issn>0168-1605</issn><issn>1879-3460</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkU2P0zAQhi0EYkvhLyBzQOJAgj_iOOG2qgqLtNJygLM1scdbV0m82Gkl-CH8XtIPYI89WRo974xnHkLecFZyxusP2zJsfYxuCDbFUjAuS6ZKJqonZMEb3RayqtlTspjZpuA1U1fkRc5bxpiSkj0nV0I2TCrNF-T314R76HG0-J7e44hTsNRuIIGdMIVfMIU4Uhgd3Ye0O3JHLNPoaY6pC1PsC49pwHEK4z1dZ7uZg3YTgNrYB3rHlf54Uxx7rMvHNU1Djj1M6KhPcaAJJwg97RD9S_LMQ5_x1fldku-f1t9WN8Xt3ecvq-vbwlaqmgpfNV4yYM7LRjioteTet1LUDrl3uuucE6C0aDm2IBEEzntz7EDyBlTbyCV5d-r7kOKPHebJDCFb7HsYMe6y4YoxrRspL0CrSh7OysUFKBe85rXiM9qe0Nlkzgm9eUhhgPTTcGYOss3WPJJtDrINU2aWPWdfn8fsugHdv-RfuzPw9gxAttD7BKMN-T-na6GbmV2S1YnD-dT7gMlkGw6qXUhoJ-NiuOA7fwBxCM20</recordid><startdate>20130801</startdate><enddate>20130801</enddate><creator>Sallam, Khalid Ibrahim</creator><creator>Mohammed, Mahmoud Ahmed</creator><creator>Ahdy, Asmaa Mohammed</creator><creator>Tamura, Tomohiro</creator><general>Elsevier B.V</general><general>Elsevier</general><scope>IQODW</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>7QL</scope><scope>7QO</scope><scope>7T7</scope><scope>7U7</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>P64</scope><scope>RC3</scope></search><sort><creationdate>20130801</creationdate><title>Prevalence, genetic characterization and virulence genes of sorbitol-fermenting Escherichia coli O157:H- and E. coli O157:H7 isolated from retail beef</title><author>Sallam, Khalid Ibrahim ; Mohammed, Mahmoud Ahmed ; Ahdy, Asmaa Mohammed ; Tamura, Tomohiro</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c454t-f48f30a0df382da6731ff9326de1fd7bbdd2a57291e9a3ea2e8031eba318a5983</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Agar</topic><topic>Animals</topic><topic>Beef</topic><topic>Biological and medical sciences</topic><topic>Cattle</topic><topic>Egypt</topic><topic>Escherichia coli</topic><topic>Escherichia coli O157 - genetics</topic><topic>Escherichia coli O157 - isolation &amp; purification</topic><topic>Escherichia coli O157 - pathogenicity</topic><topic>Food industries</topic><topic>Food Microbiology</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Meat - microbiology</topic><topic>Meat and meat product industries</topic><topic>O157:H7</topic><topic>Polymerase Chain Reaction</topic><topic>Shiga Toxin - genetics</topic><topic>Sorbitol - metabolism</topic><topic>Sorbitol-fermenting</topic><topic>Virulence Factors - genetics</topic><topic>Virulence genes</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Sallam, Khalid Ibrahim</creatorcontrib><creatorcontrib>Mohammed, Mahmoud Ahmed</creatorcontrib><creatorcontrib>Ahdy, Asmaa Mohammed</creatorcontrib><creatorcontrib>Tamura, Tomohiro</creatorcontrib><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Toxicology Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><jtitle>International journal of food microbiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Sallam, Khalid Ibrahim</au><au>Mohammed, Mahmoud Ahmed</au><au>Ahdy, Asmaa Mohammed</au><au>Tamura, Tomohiro</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Prevalence, genetic characterization and virulence genes of sorbitol-fermenting Escherichia coli O157:H- and E. coli O157:H7 isolated from retail beef</atitle><jtitle>International journal of food microbiology</jtitle><addtitle>Int J Food Microbiol</addtitle><date>2013-08-01</date><risdate>2013</risdate><volume>165</volume><issue>3</issue><spage>295</spage><epage>301</epage><pages>295-301</pages><issn>0168-1605</issn><eissn>1879-3460</eissn><coden>IJFMDD</coden><abstract>Sorbitol-fermenting (SF) Escherichia coli O157:H- strains have emerged as important pathogens and have been associated with a higher incidence of progression to hemolytic–uremic syndrome (HUS) than non-sorbitol fermenting (NSF) E. coli O157:H7. The present study was carried out to determine the prevalence of SF E. coli O157:H- and NSF E. coli O157:H7 strains in retail beef products in Mansoura, Egypt. The contamination rates with rfbEO157-positive E. coli O157 strains were 26.7% (8/30), 10% (3/30) and 3.7% (1/27) in ground beef, beef burger, and fresh beef samples, respectively with an overall mean of 13.8% (12/87) among all meat products tested. SF E. coli O157:H- were the most dominant among the isolated O157 strains. Of the fifteen O157 strains isolated, 11 (73.3%) were SF E. coli O157:H-, while the remaining 4 (26.7%) were NSF E. coli O157:H7. The 11 SF O157H- strains were genetically positive for sfpA gene. Restriction fragment length polymorphism (RFLP) analysis for fliC gene demonstrated a similar pattern for both SF and NSF O157 isolates. PCR assays verified the existence of stx1 gene in 7 (46.7%) and stx2 gene in 13 (86.7%) of the 15 O157 strains isolated. Unexpectedly, two of the 15 O157 strains isolated were negative for Shiga toxin genes. The eae gene was identified in all of the 15 O157 strains except in one NSF O157:H7 strain. EHEC-hlyA gene was detected in 14 (93.3%) of the 15 O157 isolates, nonetheless only 11 strains showed enterohemolytic phenotype on blood agar. A combination of the four virulence genes, stx1, stx2, eae and EHEC-hlyA were detected in 7 (46.7%) strains, while six (40%) strains were positive for stx2, eae and hlyA genes. This is the first record for isolation of E. coli O157: H- in Egypt as well as in the African continent. •This is the first record for isolation of E. coli O157:H- in the African continent.•We identified many sorbitol-fermenting E. coli O157:H- that contained stx1 gene.•We detected two non-Shiga toxigenic O157 strains that lacked stx1 and stx2.•SF E. coli O157:H- was the most dominant among the isolated O157 strains from beef.</abstract><cop>Amsterdam</cop><pub>Elsevier B.V</pub><pmid>23803571</pmid><doi>10.1016/j.ijfoodmicro.2013.05.024</doi><tpages>7</tpages></addata></record>
fulltext fulltext
identifier ISSN: 0168-1605
ispartof International journal of food microbiology, 2013-08, Vol.165 (3), p.295-301
issn 0168-1605
1879-3460
language eng
recordid cdi_proquest_miscellaneous_1500778338
source MEDLINE; Access via ScienceDirect (Elsevier)
subjects Agar
Animals
Beef
Biological and medical sciences
Cattle
Egypt
Escherichia coli
Escherichia coli O157 - genetics
Escherichia coli O157 - isolation & purification
Escherichia coli O157 - pathogenicity
Food industries
Food Microbiology
Fundamental and applied biological sciences. Psychology
Meat - microbiology
Meat and meat product industries
O157:H7
Polymerase Chain Reaction
Shiga Toxin - genetics
Sorbitol - metabolism
Sorbitol-fermenting
Virulence Factors - genetics
Virulence genes
title Prevalence, genetic characterization and virulence genes of sorbitol-fermenting Escherichia coli O157:H- and E. coli O157:H7 isolated from retail beef
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-30T20%3A53%3A29IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_cross&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Prevalence,%20genetic%20characterization%20and%20virulence%20genes%20of%20sorbitol-fermenting%20Escherichia%20coli%20O157:H-%20and%20E.%20coli%20O157:H7%20isolated%20from%20retail%20beef&rft.jtitle=International%20journal%20of%20food%20microbiology&rft.au=Sallam,%20Khalid%20Ibrahim&rft.date=2013-08-01&rft.volume=165&rft.issue=3&rft.spage=295&rft.epage=301&rft.pages=295-301&rft.issn=0168-1605&rft.eissn=1879-3460&rft.coden=IJFMDD&rft_id=info:doi/10.1016/j.ijfoodmicro.2013.05.024&rft_dat=%3Cproquest_cross%3E1412161651%3C/proquest_cross%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1412161651&rft_id=info:pmid/23803571&rft_els_id=S0168160513002717&rfr_iscdi=true