Berberine protects liver from ethanol-induced oxidative stress and steatosis in mice

•BBR prevented liver injury and mitochondrial oxidative damage induced by binge ethanol.•BBR reduced lipid peroxidation and CYP2E1 induction under the condition of chronic ethanol exposure.•BBR reduced hepatosteatosis partially through restoring PPARα/PGC-1α and HNF4α/MTTP pathways. Alcohol consumpt...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:Food and chemical toxicology 2014-12, Vol.74, p.225-232
Hauptverfasser: Zhang, Pengcheng, Ma, Dongshen, Wang, Yongchen, Zhang, Miao, Qiang, Xiaoyan, Liao, Min, Liu, Xie, Wu, Hui, Zhang, Yubin
Format: Artikel
Sprache:eng
Schlagworte:
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
container_end_page 232
container_issue
container_start_page 225
container_title Food and chemical toxicology
container_volume 74
creator Zhang, Pengcheng
Ma, Dongshen
Wang, Yongchen
Zhang, Miao
Qiang, Xiaoyan
Liao, Min
Liu, Xie
Wu, Hui
Zhang, Yubin
description •BBR prevented liver injury and mitochondrial oxidative damage induced by binge ethanol.•BBR reduced lipid peroxidation and CYP2E1 induction under the condition of chronic ethanol exposure.•BBR reduced hepatosteatosis partially through restoring PPARα/PGC-1α and HNF4α/MTTP pathways. Alcohol consumption is customary in many cultures and it is a common human behavior worldwide. Binge ethanol and chronic alcohol consumption, two usual drinking patterns of human beings, produce a state of oxidative stress in liver and disturb the liver function. However, a safe and effective therapy for alcoholic liver disease in humans is still elusive. This study identified the natural product berberine as a potential agent for treating or preventing ethanol-induced liver injury. We demonstrated that berberine attenuated oxidative stress resulted from binge drinking in liver by reducing hepatic lipid peroxidation, glutathione exhaust and mitochondrial oxidative damage. Furthermore, berberine also prevented the oxidative stress and macrosteatosis in response to chronic ethanol exposure in mice. Either the total cytochrome P450 2E1 or the mitochondria-located cytochrome P450 2E1, which is implicated in ethanol-mediated oxidative stress, was suppressed by berberine. On the other hand, berberine significantly blunted the lipid accumulation in liver due to chronic alcohol consumption, at least partially, through restoring peroxisome proliferator-activated receptor α/peroxisome proliferator-activated receptor-gamma Co-activator-1α and hepatocyte nuclear factor 4α/microsomal triglyceride transfer protein pathways. These findings suggested that berberine could serve as a potential agent for preventing or treating human alcoholic liver disease.
doi_str_mv 10.1016/j.fct.2014.10.005
format Article
fullrecord <record><control><sourceid>proquest_cross</sourceid><recordid>TN_cdi_proquest_miscellaneous_1660078933</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><els_id>S027869151400427X</els_id><sourcerecordid>1660078933</sourcerecordid><originalsourceid>FETCH-LOGICAL-c515t-306dd0075ae4a214cefff26de3892509b4345a0bc215999f345b60e9b897dad23</originalsourceid><addsrcrecordid>eNqNkU2PFCEQhonRuLOjP8CL4WLipUc-Ghriyd24arKJl_VMaCgik_5YKWaj_14mM-rN7AkKnqq8qYeQV5ztOOP63X6XQt0JxvtW7xhTT8iGm0F2Wir-lGyYGEynLVcX5BJxzxgb-KCfkwuheqWMsRtydwVlhJIXoPdlrRAq0ik_QKGprDOF-t0v69TlJR4CRLr-zNHX9k-xFkCkfontCr6umJHmhc45wAvyLPkJ4eX53JJvNx_vrj93t18_fbn-cNsFxVXtJNMxtkzKQ-8F7wOklISOII0Vitmxl73ybAyCK2ttatWoGdjR2CH6KOSWvD3NbdF_HACrmzMGmCa_wHpAx7Vu442V8hGoEnLQwjwG7Ye2ctMWvSX8hIayIhZI7r7k2ZdfjjN3VOT2rilyR0XHp6ao9bw-jz-MM8S_HX-cNODNGfAY_JSKX0LGf5xlkht-5N6fOGgrfshQHIYMS9OUS_Po4pr_E-M31Wmthg</addsrcrecordid><sourcetype>Aggregation Database</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>1647014887</pqid></control><display><type>article</type><title>Berberine protects liver from ethanol-induced oxidative stress and steatosis in mice</title><source>MEDLINE</source><source>ScienceDirect Journals (5 years ago - present)</source><creator>Zhang, Pengcheng ; Ma, Dongshen ; Wang, Yongchen ; Zhang, Miao ; Qiang, Xiaoyan ; Liao, Min ; Liu, Xie ; Wu, Hui ; Zhang, Yubin</creator><creatorcontrib>Zhang, Pengcheng ; Ma, Dongshen ; Wang, Yongchen ; Zhang, Miao ; Qiang, Xiaoyan ; Liao, Min ; Liu, Xie ; Wu, Hui ; Zhang, Yubin</creatorcontrib><description>•BBR prevented liver injury and mitochondrial oxidative damage induced by binge ethanol.•BBR reduced lipid peroxidation and CYP2E1 induction under the condition of chronic ethanol exposure.•BBR reduced hepatosteatosis partially through restoring PPARα/PGC-1α and HNF4α/MTTP pathways. Alcohol consumption is customary in many cultures and it is a common human behavior worldwide. Binge ethanol and chronic alcohol consumption, two usual drinking patterns of human beings, produce a state of oxidative stress in liver and disturb the liver function. However, a safe and effective therapy for alcoholic liver disease in humans is still elusive. This study identified the natural product berberine as a potential agent for treating or preventing ethanol-induced liver injury. We demonstrated that berberine attenuated oxidative stress resulted from binge drinking in liver by reducing hepatic lipid peroxidation, glutathione exhaust and mitochondrial oxidative damage. Furthermore, berberine also prevented the oxidative stress and macrosteatosis in response to chronic ethanol exposure in mice. Either the total cytochrome P450 2E1 or the mitochondria-located cytochrome P450 2E1, which is implicated in ethanol-mediated oxidative stress, was suppressed by berberine. On the other hand, berberine significantly blunted the lipid accumulation in liver due to chronic alcohol consumption, at least partially, through restoring peroxisome proliferator-activated receptor α/peroxisome proliferator-activated receptor-gamma Co-activator-1α and hepatocyte nuclear factor 4α/microsomal triglyceride transfer protein pathways. These findings suggested that berberine could serve as a potential agent for preventing or treating human alcoholic liver disease.</description><identifier>ISSN: 0278-6915</identifier><identifier>EISSN: 1873-6351</identifier><identifier>DOI: 10.1016/j.fct.2014.10.005</identifier><identifier>PMID: 25455889</identifier><identifier>CODEN: FCTOD7</identifier><language>eng</language><publisher>Oxford: Elsevier Ltd</publisher><subject>Addictive behaviors ; Adult and adolescent clinical studies ; Alcoholic liver disease ; Alcoholism ; Alcoholism and acute alcohol poisoning ; Alcohols ; Animals ; Apoptosis - drug effects ; Berberine ; Berberine - pharmacology ; Binge Drinking - pathology ; Biological and medical sciences ; Central Nervous System Depressants - antagonists &amp; inhibitors ; Central Nervous System Depressants - toxicity ; Consumption ; Cytochromes P450 ; Ethanol ; Ethanol - antagonists &amp; inhibitors ; Ethanol - toxicity ; Ethyl alcohol ; Fatty Liver, Alcoholic - prevention &amp; control ; Food toxicology ; Lipid Metabolism - drug effects ; Lipids ; Liver ; Liver Diseases, Alcoholic - prevention &amp; control ; Male ; Medical sciences ; Mice ; Mice, Inbred ICR ; Mitochondria, Liver - drug effects ; Mitochondrial Swelling - drug effects ; Oxidative stress ; Oxidative Stress - drug effects ; Protective Agents - pharmacology ; Psychology. Psychoanalysis. Psychiatry ; Psychopathology. Psychiatry ; Signal Transduction - drug effects ; Steatosis ; Stresses ; Toxicology</subject><ispartof>Food and chemical toxicology, 2014-12, Vol.74, p.225-232</ispartof><rights>2014 Elsevier Ltd</rights><rights>2015 INIST-CNRS</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c515t-306dd0075ae4a214cefff26de3892509b4345a0bc215999f345b60e9b897dad23</citedby><cites>FETCH-LOGICAL-c515t-306dd0075ae4a214cefff26de3892509b4345a0bc215999f345b60e9b897dad23</cites><orcidid>0000-0002-5586-6763</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.fct.2014.10.005$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,780,784,3548,27923,27924,45994</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&amp;idt=29031819$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25455889$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Zhang, Pengcheng</creatorcontrib><creatorcontrib>Ma, Dongshen</creatorcontrib><creatorcontrib>Wang, Yongchen</creatorcontrib><creatorcontrib>Zhang, Miao</creatorcontrib><creatorcontrib>Qiang, Xiaoyan</creatorcontrib><creatorcontrib>Liao, Min</creatorcontrib><creatorcontrib>Liu, Xie</creatorcontrib><creatorcontrib>Wu, Hui</creatorcontrib><creatorcontrib>Zhang, Yubin</creatorcontrib><title>Berberine protects liver from ethanol-induced oxidative stress and steatosis in mice</title><title>Food and chemical toxicology</title><addtitle>Food Chem Toxicol</addtitle><description>•BBR prevented liver injury and mitochondrial oxidative damage induced by binge ethanol.•BBR reduced lipid peroxidation and CYP2E1 induction under the condition of chronic ethanol exposure.•BBR reduced hepatosteatosis partially through restoring PPARα/PGC-1α and HNF4α/MTTP pathways. Alcohol consumption is customary in many cultures and it is a common human behavior worldwide. Binge ethanol and chronic alcohol consumption, two usual drinking patterns of human beings, produce a state of oxidative stress in liver and disturb the liver function. However, a safe and effective therapy for alcoholic liver disease in humans is still elusive. This study identified the natural product berberine as a potential agent for treating or preventing ethanol-induced liver injury. We demonstrated that berberine attenuated oxidative stress resulted from binge drinking in liver by reducing hepatic lipid peroxidation, glutathione exhaust and mitochondrial oxidative damage. Furthermore, berberine also prevented the oxidative stress and macrosteatosis in response to chronic ethanol exposure in mice. Either the total cytochrome P450 2E1 or the mitochondria-located cytochrome P450 2E1, which is implicated in ethanol-mediated oxidative stress, was suppressed by berberine. On the other hand, berberine significantly blunted the lipid accumulation in liver due to chronic alcohol consumption, at least partially, through restoring peroxisome proliferator-activated receptor α/peroxisome proliferator-activated receptor-gamma Co-activator-1α and hepatocyte nuclear factor 4α/microsomal triglyceride transfer protein pathways. These findings suggested that berberine could serve as a potential agent for preventing or treating human alcoholic liver disease.</description><subject>Addictive behaviors</subject><subject>Adult and adolescent clinical studies</subject><subject>Alcoholic liver disease</subject><subject>Alcoholism</subject><subject>Alcoholism and acute alcohol poisoning</subject><subject>Alcohols</subject><subject>Animals</subject><subject>Apoptosis - drug effects</subject><subject>Berberine</subject><subject>Berberine - pharmacology</subject><subject>Binge Drinking - pathology</subject><subject>Biological and medical sciences</subject><subject>Central Nervous System Depressants - antagonists &amp; inhibitors</subject><subject>Central Nervous System Depressants - toxicity</subject><subject>Consumption</subject><subject>Cytochromes P450</subject><subject>Ethanol</subject><subject>Ethanol - antagonists &amp; inhibitors</subject><subject>Ethanol - toxicity</subject><subject>Ethyl alcohol</subject><subject>Fatty Liver, Alcoholic - prevention &amp; control</subject><subject>Food toxicology</subject><subject>Lipid Metabolism - drug effects</subject><subject>Lipids</subject><subject>Liver</subject><subject>Liver Diseases, Alcoholic - prevention &amp; control</subject><subject>Male</subject><subject>Medical sciences</subject><subject>Mice</subject><subject>Mice, Inbred ICR</subject><subject>Mitochondria, Liver - drug effects</subject><subject>Mitochondrial Swelling - drug effects</subject><subject>Oxidative stress</subject><subject>Oxidative Stress - drug effects</subject><subject>Protective Agents - pharmacology</subject><subject>Psychology. Psychoanalysis. Psychiatry</subject><subject>Psychopathology. Psychiatry</subject><subject>Signal Transduction - drug effects</subject><subject>Steatosis</subject><subject>Stresses</subject><subject>Toxicology</subject><issn>0278-6915</issn><issn>1873-6351</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkU2PFCEQhonRuLOjP8CL4WLipUc-Ghriyd24arKJl_VMaCgik_5YKWaj_14mM-rN7AkKnqq8qYeQV5ztOOP63X6XQt0JxvtW7xhTT8iGm0F2Wir-lGyYGEynLVcX5BJxzxgb-KCfkwuheqWMsRtydwVlhJIXoPdlrRAq0ik_QKGprDOF-t0v69TlJR4CRLr-zNHX9k-xFkCkfontCr6umJHmhc45wAvyLPkJ4eX53JJvNx_vrj93t18_fbn-cNsFxVXtJNMxtkzKQ-8F7wOklISOII0Vitmxl73ybAyCK2ttatWoGdjR2CH6KOSWvD3NbdF_HACrmzMGmCa_wHpAx7Vu442V8hGoEnLQwjwG7Ye2ctMWvSX8hIayIhZI7r7k2ZdfjjN3VOT2rilyR0XHp6ao9bw-jz-MM8S_HX-cNODNGfAY_JSKX0LGf5xlkht-5N6fOGgrfshQHIYMS9OUS_Po4pr_E-M31Wmthg</recordid><startdate>20141201</startdate><enddate>20141201</enddate><creator>Zhang, Pengcheng</creator><creator>Ma, Dongshen</creator><creator>Wang, Yongchen</creator><creator>Zhang, Miao</creator><creator>Qiang, Xiaoyan</creator><creator>Liao, Min</creator><creator>Liu, Xie</creator><creator>Wu, Hui</creator><creator>Zhang, Yubin</creator><general>Elsevier Ltd</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>7U7</scope><scope>C1K</scope><scope>7X8</scope><scope>7TB</scope><scope>8FD</scope><scope>F28</scope><scope>FR3</scope><orcidid>https://orcid.org/0000-0002-5586-6763</orcidid></search><sort><creationdate>20141201</creationdate><title>Berberine protects liver from ethanol-induced oxidative stress and steatosis in mice</title><author>Zhang, Pengcheng ; Ma, Dongshen ; Wang, Yongchen ; Zhang, Miao ; Qiang, Xiaoyan ; Liao, Min ; Liu, Xie ; Wu, Hui ; Zhang, Yubin</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c515t-306dd0075ae4a214cefff26de3892509b4345a0bc215999f345b60e9b897dad23</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Addictive behaviors</topic><topic>Adult and adolescent clinical studies</topic><topic>Alcoholic liver disease</topic><topic>Alcoholism</topic><topic>Alcoholism and acute alcohol poisoning</topic><topic>Alcohols</topic><topic>Animals</topic><topic>Apoptosis - drug effects</topic><topic>Berberine</topic><topic>Berberine - pharmacology</topic><topic>Binge Drinking - pathology</topic><topic>Biological and medical sciences</topic><topic>Central Nervous System Depressants - antagonists &amp; inhibitors</topic><topic>Central Nervous System Depressants - toxicity</topic><topic>Consumption</topic><topic>Cytochromes P450</topic><topic>Ethanol</topic><topic>Ethanol - antagonists &amp; inhibitors</topic><topic>Ethanol - toxicity</topic><topic>Ethyl alcohol</topic><topic>Fatty Liver, Alcoholic - prevention &amp; control</topic><topic>Food toxicology</topic><topic>Lipid Metabolism - drug effects</topic><topic>Lipids</topic><topic>Liver</topic><topic>Liver Diseases, Alcoholic - prevention &amp; control</topic><topic>Male</topic><topic>Medical sciences</topic><topic>Mice</topic><topic>Mice, Inbred ICR</topic><topic>Mitochondria, Liver - drug effects</topic><topic>Mitochondrial Swelling - drug effects</topic><topic>Oxidative stress</topic><topic>Oxidative Stress - drug effects</topic><topic>Protective Agents - pharmacology</topic><topic>Psychology. Psychoanalysis. Psychiatry</topic><topic>Psychopathology. Psychiatry</topic><topic>Signal Transduction - drug effects</topic><topic>Steatosis</topic><topic>Stresses</topic><topic>Toxicology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Zhang, Pengcheng</creatorcontrib><creatorcontrib>Ma, Dongshen</creatorcontrib><creatorcontrib>Wang, Yongchen</creatorcontrib><creatorcontrib>Zhang, Miao</creatorcontrib><creatorcontrib>Qiang, Xiaoyan</creatorcontrib><creatorcontrib>Liao, Min</creatorcontrib><creatorcontrib>Liu, Xie</creatorcontrib><creatorcontrib>Wu, Hui</creatorcontrib><creatorcontrib>Zhang, Yubin</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>Toxicology Abstracts</collection><collection>Environmental Sciences and Pollution Management</collection><collection>MEDLINE - Academic</collection><collection>Mechanical &amp; Transportation Engineering Abstracts</collection><collection>Technology Research Database</collection><collection>ANTE: Abstracts in New Technology &amp; Engineering</collection><collection>Engineering Research Database</collection><jtitle>Food and chemical toxicology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Zhang, Pengcheng</au><au>Ma, Dongshen</au><au>Wang, Yongchen</au><au>Zhang, Miao</au><au>Qiang, Xiaoyan</au><au>Liao, Min</au><au>Liu, Xie</au><au>Wu, Hui</au><au>Zhang, Yubin</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Berberine protects liver from ethanol-induced oxidative stress and steatosis in mice</atitle><jtitle>Food and chemical toxicology</jtitle><addtitle>Food Chem Toxicol</addtitle><date>2014-12-01</date><risdate>2014</risdate><volume>74</volume><spage>225</spage><epage>232</epage><pages>225-232</pages><issn>0278-6915</issn><eissn>1873-6351</eissn><coden>FCTOD7</coden><abstract>•BBR prevented liver injury and mitochondrial oxidative damage induced by binge ethanol.•BBR reduced lipid peroxidation and CYP2E1 induction under the condition of chronic ethanol exposure.•BBR reduced hepatosteatosis partially through restoring PPARα/PGC-1α and HNF4α/MTTP pathways. Alcohol consumption is customary in many cultures and it is a common human behavior worldwide. Binge ethanol and chronic alcohol consumption, two usual drinking patterns of human beings, produce a state of oxidative stress in liver and disturb the liver function. However, a safe and effective therapy for alcoholic liver disease in humans is still elusive. This study identified the natural product berberine as a potential agent for treating or preventing ethanol-induced liver injury. We demonstrated that berberine attenuated oxidative stress resulted from binge drinking in liver by reducing hepatic lipid peroxidation, glutathione exhaust and mitochondrial oxidative damage. Furthermore, berberine also prevented the oxidative stress and macrosteatosis in response to chronic ethanol exposure in mice. Either the total cytochrome P450 2E1 or the mitochondria-located cytochrome P450 2E1, which is implicated in ethanol-mediated oxidative stress, was suppressed by berberine. On the other hand, berberine significantly blunted the lipid accumulation in liver due to chronic alcohol consumption, at least partially, through restoring peroxisome proliferator-activated receptor α/peroxisome proliferator-activated receptor-gamma Co-activator-1α and hepatocyte nuclear factor 4α/microsomal triglyceride transfer protein pathways. These findings suggested that berberine could serve as a potential agent for preventing or treating human alcoholic liver disease.</abstract><cop>Oxford</cop><pub>Elsevier Ltd</pub><pmid>25455889</pmid><doi>10.1016/j.fct.2014.10.005</doi><tpages>8</tpages><orcidid>https://orcid.org/0000-0002-5586-6763</orcidid></addata></record>
fulltext fulltext
identifier ISSN: 0278-6915
ispartof Food and chemical toxicology, 2014-12, Vol.74, p.225-232
issn 0278-6915
1873-6351
language eng
recordid cdi_proquest_miscellaneous_1660078933
source MEDLINE; ScienceDirect Journals (5 years ago - present)
subjects Addictive behaviors
Adult and adolescent clinical studies
Alcoholic liver disease
Alcoholism
Alcoholism and acute alcohol poisoning
Alcohols
Animals
Apoptosis - drug effects
Berberine
Berberine - pharmacology
Binge Drinking - pathology
Biological and medical sciences
Central Nervous System Depressants - antagonists & inhibitors
Central Nervous System Depressants - toxicity
Consumption
Cytochromes P450
Ethanol
Ethanol - antagonists & inhibitors
Ethanol - toxicity
Ethyl alcohol
Fatty Liver, Alcoholic - prevention & control
Food toxicology
Lipid Metabolism - drug effects
Lipids
Liver
Liver Diseases, Alcoholic - prevention & control
Male
Medical sciences
Mice
Mice, Inbred ICR
Mitochondria, Liver - drug effects
Mitochondrial Swelling - drug effects
Oxidative stress
Oxidative Stress - drug effects
Protective Agents - pharmacology
Psychology. Psychoanalysis. Psychiatry
Psychopathology. Psychiatry
Signal Transduction - drug effects
Steatosis
Stresses
Toxicology
title Berberine protects liver from ethanol-induced oxidative stress and steatosis in mice
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-13T06%3A32%3A47IST&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=Berberine%20protects%20liver%20from%20ethanol-induced%20oxidative%20stress%20and%20steatosis%20in%20mice&rft.jtitle=Food%20and%20chemical%20toxicology&rft.au=Zhang,%20Pengcheng&rft.date=2014-12-01&rft.volume=74&rft.spage=225&rft.epage=232&rft.pages=225-232&rft.issn=0278-6915&rft.eissn=1873-6351&rft.coden=FCTOD7&rft_id=info:doi/10.1016/j.fct.2014.10.005&rft_dat=%3Cproquest_cross%3E1660078933%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=1647014887&rft_id=info:pmid/25455889&rft_els_id=S027869151400427X&rfr_iscdi=true