Porphyromonas gingivalis‐derived lipopolysaccharide causes excessive hepatic lipid accumulation via activating NF‐κB and JNK signaling pathways
Background Porphyromonas gingivalis is the main pathogen of periodontal disease affecting over half of the worldwide adult population. Recent studies have shown that P. gingivalis is related to the development of non‐alcoholic fatty liver disease (NAFLD), a global major chronic liver disease, especi...
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| Veröffentlicht in: | Oral diseases 2019-10, Vol.25 (7), p.1789-1797 |
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| creator | Ding, Lu‐yang Liang, Li‐zong Zhao, Yong‐xu Yang, Ya‐nan Liu, Feng Ding, Qiu‐rong Luo, Li‐jun |
| description | Background
Porphyromonas gingivalis is the main pathogen of periodontal disease affecting over half of the worldwide adult population. Recent studies have shown that P. gingivalis is related to the development of non‐alcoholic fatty liver disease (NAFLD), a global major chronic liver disease, especially in developed countries. However, how P. gingivalis contributes to the pathogenesis of NAFLD has not been fully clarified. We aimed to conduct a preliminary exploration of the underlying mechanism of P. gingivalis infection in the development of NAFLD.
Methods
Human hepatocellular cells HepG2 were incubated with/without oleic acid (OA) and tested for lipid accumulation upon stimulation by lipopolysaccharide (LPS) derived from P. gingivalis or Escherichia coli. Intracellular lipid droplet formation was analyzed and quantified by Oil Red O staining. The involvement of signaling pathway molecules and pro‐inflammatory cytokines related to NF‐κB and MAPKs were examined with Western blot and quantitative real‐time PCR (qRT‐PCR) analyses and further evaluated with inhibitor treatment and RNA interference.
Results
HepG2 cells accumulated more intracellular lipids when stimulated with P. gingivalis LPS, as compared to cells treated with E. coli LPS or control. Further pathway analysis demonstrated that after stimulation with P. gingivalis LPS, cells displayed significantly upregulated MyD88 expression, increased phosphorylation of p65 and JNK, and more release of pro‐inflammatory cytokines, such as IL‐1, IL‐8, and TNF‐α. In addition, suppression of phosphorylation of p65 and JNK by inhibitors and RNA interference resulted in a reduction in lipid accumulation upon P. gingivalis LPS treatment.
Conclusions
These results suggest that P. gingivalis‐derived LPS may contribute to intracellular lipid accumulation and inflammatory reaction of HepG2 cells via the activation of NF‐κB and JNK signaling pathways. This study offers a possible explanation to the functional involvement of P. gingivalis infection in the pathological progression of NAFLD. These findings may help design new treatment strategies in NAFLD. |
| doi_str_mv | 10.1111/odi.13153 |
| format | Article |
| fullrecord | <record><control><sourceid>proquest_cross</sourceid><recordid>TN_cdi_proquest_miscellaneous_2254503313</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>2254503313</sourcerecordid><originalsourceid>FETCH-LOGICAL-c3533-98b8ade72247290aa412d0ea36024f4148962f37ecab65d70239aab1da92607d3</originalsourceid><addsrcrecordid>eNp1kU1uFDEQRi0EIiGw4ALIEhtYdGK7-ncJgUAgSliAxK5VY3tmHHW3G9f0hN5xBBachkNwCE5ChQkskPDGVvnpVak-IR5qdaj5HEUXDjXoAm6JfV0qnanaFLf5DUWeFQY-7ol7RJdK6aoBc1fsgTY11KXeF9_exTSu5xT7OCDJVRhWYYtdoJ9fvjqfwtY72YUxjrGbCa1dYwrOS4sTeZL-s_VEDMm1H3ET7DUbnGRw6qeOK3GQ24Bc2LB2w3Z5fsLqH9-fSxycfHP-VlJYDdyRv1ixvsKZ7os7S-zIP7i5D8SHk5fvj19nZxevTo-fnWUWCoCsqRc1Ol8Zk1emUYi5Nk55hFKZfJnrvG5Ks4TKW1yUhauUgQZxoR02plSVgwPxZOcdU_w0edq0fSDruw4HHydqjSnyQgFoYPTxP-hlnBLPzRSoUpUVr5yppzvKpkiU_LIdU-gxza1W7XVULUfV_o6K2Uc3xmnRe_eX_JMNA0c74Cp0fv6_qb14cbpT_gICh6JP</addsrcrecordid><sourcetype>Aggregation Database</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2306067825</pqid></control><display><type>article</type><title>Porphyromonas gingivalis‐derived lipopolysaccharide causes excessive hepatic lipid accumulation via activating NF‐κB and JNK signaling pathways</title><source>MEDLINE</source><source>Wiley Journals</source><creator>Ding, Lu‐yang ; Liang, Li‐zong ; Zhao, Yong‐xu ; Yang, Ya‐nan ; Liu, Feng ; Ding, Qiu‐rong ; Luo, Li‐jun</creator><creatorcontrib>Ding, Lu‐yang ; Liang, Li‐zong ; Zhao, Yong‐xu ; Yang, Ya‐nan ; Liu, Feng ; Ding, Qiu‐rong ; Luo, Li‐jun</creatorcontrib><description>Background
Porphyromonas gingivalis is the main pathogen of periodontal disease affecting over half of the worldwide adult population. Recent studies have shown that P. gingivalis is related to the development of non‐alcoholic fatty liver disease (NAFLD), a global major chronic liver disease, especially in developed countries. However, how P. gingivalis contributes to the pathogenesis of NAFLD has not been fully clarified. We aimed to conduct a preliminary exploration of the underlying mechanism of P. gingivalis infection in the development of NAFLD.
Methods
Human hepatocellular cells HepG2 were incubated with/without oleic acid (OA) and tested for lipid accumulation upon stimulation by lipopolysaccharide (LPS) derived from P. gingivalis or Escherichia coli. Intracellular lipid droplet formation was analyzed and quantified by Oil Red O staining. The involvement of signaling pathway molecules and pro‐inflammatory cytokines related to NF‐κB and MAPKs were examined with Western blot and quantitative real‐time PCR (qRT‐PCR) analyses and further evaluated with inhibitor treatment and RNA interference.
Results
HepG2 cells accumulated more intracellular lipids when stimulated with P. gingivalis LPS, as compared to cells treated with E. coli LPS or control. Further pathway analysis demonstrated that after stimulation with P. gingivalis LPS, cells displayed significantly upregulated MyD88 expression, increased phosphorylation of p65 and JNK, and more release of pro‐inflammatory cytokines, such as IL‐1, IL‐8, and TNF‐α. In addition, suppression of phosphorylation of p65 and JNK by inhibitors and RNA interference resulted in a reduction in lipid accumulation upon P. gingivalis LPS treatment.
Conclusions
These results suggest that P. gingivalis‐derived LPS may contribute to intracellular lipid accumulation and inflammatory reaction of HepG2 cells via the activation of NF‐κB and JNK signaling pathways. This study offers a possible explanation to the functional involvement of P. gingivalis infection in the pathological progression of NAFLD. These findings may help design new treatment strategies in NAFLD.</description><identifier>ISSN: 1354-523X</identifier><identifier>EISSN: 1601-0825</identifier><identifier>DOI: 10.1111/odi.13153</identifier><identifier>PMID: 31283861</identifier><language>eng</language><publisher>Denmark: Wiley Subscription Services, Inc</publisher><subject>Adult ; Bacteroidaceae Infections ; Blotting, Western ; Cell activation ; Cytokines ; Dentistry ; Fatty liver ; Gum disease ; Humans ; Inflammation ; Intracellular ; JNK ; Lipids ; Lipopolysaccharides ; Liver diseases ; MAP Kinase Signaling System ; MyD88 protein ; NF-kappa B ; NF‐κB ; Non-alcoholic Fatty Liver Disease - microbiology ; Non-alcoholic Fatty Liver Disease - pathology ; non‐alcoholic fatty liver disease ; Oleic acid ; Periodontal diseases ; periodontitis ; Periodontitis - microbiology ; Phosphorylation ; Population studies ; Porphyromonas gingivalis ; Porphyromonas gingivalis - isolation & purification ; Real-Time Polymerase Chain Reaction ; RNA-mediated interference ; Signal transduction ; Tumor necrosis factor</subject><ispartof>Oral diseases, 2019-10, Vol.25 (7), p.1789-1797</ispartof><rights>2019 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd. All rights reserved</rights><rights>2019 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd. All rights reserved.</rights><rights>Copyright © 2019 John Wiley & Sons A/S</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3533-98b8ade72247290aa412d0ea36024f4148962f37ecab65d70239aab1da92607d3</citedby><cites>FETCH-LOGICAL-c3533-98b8ade72247290aa412d0ea36024f4148962f37ecab65d70239aab1da92607d3</cites><orcidid>0000-0002-3374-2858</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fodi.13153$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fodi.13153$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,780,784,1417,27924,27925,45574,45575</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31283861$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Ding, Lu‐yang</creatorcontrib><creatorcontrib>Liang, Li‐zong</creatorcontrib><creatorcontrib>Zhao, Yong‐xu</creatorcontrib><creatorcontrib>Yang, Ya‐nan</creatorcontrib><creatorcontrib>Liu, Feng</creatorcontrib><creatorcontrib>Ding, Qiu‐rong</creatorcontrib><creatorcontrib>Luo, Li‐jun</creatorcontrib><title>Porphyromonas gingivalis‐derived lipopolysaccharide causes excessive hepatic lipid accumulation via activating NF‐κB and JNK signaling pathways</title><title>Oral diseases</title><addtitle>Oral Dis</addtitle><description>Background
Porphyromonas gingivalis is the main pathogen of periodontal disease affecting over half of the worldwide adult population. Recent studies have shown that P. gingivalis is related to the development of non‐alcoholic fatty liver disease (NAFLD), a global major chronic liver disease, especially in developed countries. However, how P. gingivalis contributes to the pathogenesis of NAFLD has not been fully clarified. We aimed to conduct a preliminary exploration of the underlying mechanism of P. gingivalis infection in the development of NAFLD.
Methods
Human hepatocellular cells HepG2 were incubated with/without oleic acid (OA) and tested for lipid accumulation upon stimulation by lipopolysaccharide (LPS) derived from P. gingivalis or Escherichia coli. Intracellular lipid droplet formation was analyzed and quantified by Oil Red O staining. The involvement of signaling pathway molecules and pro‐inflammatory cytokines related to NF‐κB and MAPKs were examined with Western blot and quantitative real‐time PCR (qRT‐PCR) analyses and further evaluated with inhibitor treatment and RNA interference.
Results
HepG2 cells accumulated more intracellular lipids when stimulated with P. gingivalis LPS, as compared to cells treated with E. coli LPS or control. Further pathway analysis demonstrated that after stimulation with P. gingivalis LPS, cells displayed significantly upregulated MyD88 expression, increased phosphorylation of p65 and JNK, and more release of pro‐inflammatory cytokines, such as IL‐1, IL‐8, and TNF‐α. In addition, suppression of phosphorylation of p65 and JNK by inhibitors and RNA interference resulted in a reduction in lipid accumulation upon P. gingivalis LPS treatment.
Conclusions
These results suggest that P. gingivalis‐derived LPS may contribute to intracellular lipid accumulation and inflammatory reaction of HepG2 cells via the activation of NF‐κB and JNK signaling pathways. This study offers a possible explanation to the functional involvement of P. gingivalis infection in the pathological progression of NAFLD. These findings may help design new treatment strategies in NAFLD.</description><subject>Adult</subject><subject>Bacteroidaceae Infections</subject><subject>Blotting, Western</subject><subject>Cell activation</subject><subject>Cytokines</subject><subject>Dentistry</subject><subject>Fatty liver</subject><subject>Gum disease</subject><subject>Humans</subject><subject>Inflammation</subject><subject>Intracellular</subject><subject>JNK</subject><subject>Lipids</subject><subject>Lipopolysaccharides</subject><subject>Liver diseases</subject><subject>MAP Kinase Signaling System</subject><subject>MyD88 protein</subject><subject>NF-kappa B</subject><subject>NF‐κB</subject><subject>Non-alcoholic Fatty Liver Disease - microbiology</subject><subject>Non-alcoholic Fatty Liver Disease - pathology</subject><subject>non‐alcoholic fatty liver disease</subject><subject>Oleic acid</subject><subject>Periodontal diseases</subject><subject>periodontitis</subject><subject>Periodontitis - microbiology</subject><subject>Phosphorylation</subject><subject>Population studies</subject><subject>Porphyromonas gingivalis</subject><subject>Porphyromonas gingivalis - isolation & purification</subject><subject>Real-Time Polymerase Chain Reaction</subject><subject>RNA-mediated interference</subject><subject>Signal transduction</subject><subject>Tumor necrosis factor</subject><issn>1354-523X</issn><issn>1601-0825</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kU1uFDEQRi0EIiGw4ALIEhtYdGK7-ncJgUAgSliAxK5VY3tmHHW3G9f0hN5xBBachkNwCE5ChQkskPDGVvnpVak-IR5qdaj5HEUXDjXoAm6JfV0qnanaFLf5DUWeFQY-7ol7RJdK6aoBc1fsgTY11KXeF9_exTSu5xT7OCDJVRhWYYtdoJ9fvjqfwtY72YUxjrGbCa1dYwrOS4sTeZL-s_VEDMm1H3ET7DUbnGRw6qeOK3GQ24Bc2LB2w3Z5fsLqH9-fSxycfHP-VlJYDdyRv1ixvsKZ7os7S-zIP7i5D8SHk5fvj19nZxevTo-fnWUWCoCsqRc1Ol8Zk1emUYi5Nk55hFKZfJnrvG5Ks4TKW1yUhauUgQZxoR02plSVgwPxZOcdU_w0edq0fSDruw4HHydqjSnyQgFoYPTxP-hlnBLPzRSoUpUVr5yppzvKpkiU_LIdU-gxza1W7XVULUfV_o6K2Uc3xmnRe_eX_JMNA0c74Cp0fv6_qb14cbpT_gICh6JP</recordid><startdate>201910</startdate><enddate>201910</enddate><creator>Ding, Lu‐yang</creator><creator>Liang, Li‐zong</creator><creator>Zhao, Yong‐xu</creator><creator>Yang, Ya‐nan</creator><creator>Liu, Feng</creator><creator>Ding, Qiu‐rong</creator><creator>Luo, Li‐jun</creator><general>Wiley Subscription Services, Inc</general><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>7QP</scope><scope>K9.</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-3374-2858</orcidid></search><sort><creationdate>201910</creationdate><title>Porphyromonas gingivalis‐derived lipopolysaccharide causes excessive hepatic lipid accumulation via activating NF‐κB and JNK signaling pathways</title><author>Ding, Lu‐yang ; Liang, Li‐zong ; Zhao, Yong‐xu ; Yang, Ya‐nan ; Liu, Feng ; Ding, Qiu‐rong ; Luo, Li‐jun</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3533-98b8ade72247290aa412d0ea36024f4148962f37ecab65d70239aab1da92607d3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Adult</topic><topic>Bacteroidaceae Infections</topic><topic>Blotting, Western</topic><topic>Cell activation</topic><topic>Cytokines</topic><topic>Dentistry</topic><topic>Fatty liver</topic><topic>Gum disease</topic><topic>Humans</topic><topic>Inflammation</topic><topic>Intracellular</topic><topic>JNK</topic><topic>Lipids</topic><topic>Lipopolysaccharides</topic><topic>Liver diseases</topic><topic>MAP Kinase Signaling System</topic><topic>MyD88 protein</topic><topic>NF-kappa B</topic><topic>NF‐κB</topic><topic>Non-alcoholic Fatty Liver Disease - microbiology</topic><topic>Non-alcoholic Fatty Liver Disease - pathology</topic><topic>non‐alcoholic fatty liver disease</topic><topic>Oleic acid</topic><topic>Periodontal diseases</topic><topic>periodontitis</topic><topic>Periodontitis - microbiology</topic><topic>Phosphorylation</topic><topic>Population studies</topic><topic>Porphyromonas gingivalis</topic><topic>Porphyromonas gingivalis - isolation & purification</topic><topic>Real-Time Polymerase Chain Reaction</topic><topic>RNA-mediated interference</topic><topic>Signal transduction</topic><topic>Tumor necrosis factor</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Ding, Lu‐yang</creatorcontrib><creatorcontrib>Liang, Li‐zong</creatorcontrib><creatorcontrib>Zhao, Yong‐xu</creatorcontrib><creatorcontrib>Yang, Ya‐nan</creatorcontrib><creatorcontrib>Liu, Feng</creatorcontrib><creatorcontrib>Ding, Qiu‐rong</creatorcontrib><creatorcontrib>Luo, Li‐jun</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>MEDLINE - Academic</collection><jtitle>Oral diseases</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Ding, Lu‐yang</au><au>Liang, Li‐zong</au><au>Zhao, Yong‐xu</au><au>Yang, Ya‐nan</au><au>Liu, Feng</au><au>Ding, Qiu‐rong</au><au>Luo, Li‐jun</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Porphyromonas gingivalis‐derived lipopolysaccharide causes excessive hepatic lipid accumulation via activating NF‐κB and JNK signaling pathways</atitle><jtitle>Oral diseases</jtitle><addtitle>Oral Dis</addtitle><date>2019-10</date><risdate>2019</risdate><volume>25</volume><issue>7</issue><spage>1789</spage><epage>1797</epage><pages>1789-1797</pages><issn>1354-523X</issn><eissn>1601-0825</eissn><abstract>Background
Porphyromonas gingivalis is the main pathogen of periodontal disease affecting over half of the worldwide adult population. Recent studies have shown that P. gingivalis is related to the development of non‐alcoholic fatty liver disease (NAFLD), a global major chronic liver disease, especially in developed countries. However, how P. gingivalis contributes to the pathogenesis of NAFLD has not been fully clarified. We aimed to conduct a preliminary exploration of the underlying mechanism of P. gingivalis infection in the development of NAFLD.
Methods
Human hepatocellular cells HepG2 were incubated with/without oleic acid (OA) and tested for lipid accumulation upon stimulation by lipopolysaccharide (LPS) derived from P. gingivalis or Escherichia coli. Intracellular lipid droplet formation was analyzed and quantified by Oil Red O staining. The involvement of signaling pathway molecules and pro‐inflammatory cytokines related to NF‐κB and MAPKs were examined with Western blot and quantitative real‐time PCR (qRT‐PCR) analyses and further evaluated with inhibitor treatment and RNA interference.
Results
HepG2 cells accumulated more intracellular lipids when stimulated with P. gingivalis LPS, as compared to cells treated with E. coli LPS or control. Further pathway analysis demonstrated that after stimulation with P. gingivalis LPS, cells displayed significantly upregulated MyD88 expression, increased phosphorylation of p65 and JNK, and more release of pro‐inflammatory cytokines, such as IL‐1, IL‐8, and TNF‐α. In addition, suppression of phosphorylation of p65 and JNK by inhibitors and RNA interference resulted in a reduction in lipid accumulation upon P. gingivalis LPS treatment.
Conclusions
These results suggest that P. gingivalis‐derived LPS may contribute to intracellular lipid accumulation and inflammatory reaction of HepG2 cells via the activation of NF‐κB and JNK signaling pathways. This study offers a possible explanation to the functional involvement of P. gingivalis infection in the pathological progression of NAFLD. These findings may help design new treatment strategies in NAFLD.</abstract><cop>Denmark</cop><pub>Wiley Subscription Services, Inc</pub><pmid>31283861</pmid><doi>10.1111/odi.13153</doi><tpages>9</tpages><orcidid>https://orcid.org/0000-0002-3374-2858</orcidid></addata></record> |
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| subjects | Adult Bacteroidaceae Infections Blotting, Western Cell activation Cytokines Dentistry Fatty liver Gum disease Humans Inflammation Intracellular JNK Lipids Lipopolysaccharides Liver diseases MAP Kinase Signaling System MyD88 protein NF-kappa B NF‐κB Non-alcoholic Fatty Liver Disease - microbiology Non-alcoholic Fatty Liver Disease - pathology non‐alcoholic fatty liver disease Oleic acid Periodontal diseases periodontitis Periodontitis - microbiology Phosphorylation Population studies Porphyromonas gingivalis Porphyromonas gingivalis - isolation & purification Real-Time Polymerase Chain Reaction RNA-mediated interference Signal transduction Tumor necrosis factor |
| title | Porphyromonas gingivalis‐derived lipopolysaccharide causes excessive hepatic lipid accumulation via activating NF‐κB and JNK signaling pathways |
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