Omega-3 polyunsaturated fatty acids in critically ill patients with acute respiratory distress syndrome: A systematic review and meta-analysis

•Omega-3 polyunsaturated fatty acids have been administered to ARDS patients, mostly by enteral route with contradictory results.•Enteral immunomodulatory diets with fish oils may be associated with an improvement in early and late PaO2-to-FiO2 ratio in ARDS, although a clinical and statistically si...

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Veröffentlicht in:Nutrition (Burbank, Los Angeles County, Calif.) Los Angeles County, Calif.), 2019-05, Vol.61, p.84-92
Hauptverfasser: Langlois, Pascal L., D'Aragon, Fréderick, Hardy, Gil, Manzanares, William
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D'Aragon, Fréderick
Hardy, Gil
Manzanares, William
description •Omega-3 polyunsaturated fatty acids have been administered to ARDS patients, mostly by enteral route with contradictory results.•Enteral immunomodulatory diets with fish oils may be associated with an improvement in early and late PaO2-to-FiO2 ratio in ARDS, although a clinical and statistically significant heterogeneity exists.•The treatment effect seems to be greatest in those trials published before 2011 that provided an immunomodulatory formula with fish oils administered as a continuous infusion.•Further well-powered clinical trials aimed at evaluating whether modulating pathophysiology of ARDS patients with omega-3 could improve morbidity and mortality are warranted. Acute respiratory distress syndrome (ARDS) is characterized by an acute inflammatory response in the lung parenchyma leading to severe hypoxemia. Because of its anti-inflammatory and immunomodulatory properties, omega-3 polyunsaturated fatty acids (ω-3 PUFA) have been administered to ARDS patients, mostly by the enteral route, as immune-enhancing diets with eicosapentaenoic acid, γ-linolenic acid, and antioxidants. However, clinical benefits of ω-3 PUFAs in ARDS patients remain unclear because clinical trials have found conflicting results. Considering the most recent randomized controlled trials (RCTs) and recent change in administration strategies, the aim of this updated systematic review and meta-analysis was to evaluate clinical benefits of ω-3 PUFA administration on gas exchange and clinical outcomes in ARDS patients. We searched for RCTs conducted in intensive care unit (ICU) patients with ARDS comparing the administration of ω-3 PUFAs to placebo. The outcomes assessed were PaO2-to-FiO2 ratio evaluated early (3–4 d) and later (7–8 d), mortality, ICU and hospital length of stay (LOS), length of mechanical ventilation (MV), and infectious complications. Two independent reviewers assessed eligibility, risk of bias, and abstracted data. Data were pooled using a random effect model to estimate the relative risk or weighted mean difference (WMD). Twelve RCTs (n = 1280 patients) met our inclusion criteria. Omega-3 PUFAs administration was associated with a significant improvement in early PaO2-to-FiO2 ratio (WMD = 49.33; 95% confidence interval [CI] 20.88–77.78; P = 0.0007; I2 = 69%), which persisted at days 7 to 8 (WMD = 27.87; 95% CI 0.75–54.99; P = 0.04; I2 = 57%). There was a trend in those receiving ω-3 PUFA toward reduced ICU LOS (P = 0.08) and duration of MV (P = 0.06), whereas m
doi_str_mv 10.1016/j.nut.2018.10.026
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Acute respiratory distress syndrome (ARDS) is characterized by an acute inflammatory response in the lung parenchyma leading to severe hypoxemia. Because of its anti-inflammatory and immunomodulatory properties, omega-3 polyunsaturated fatty acids (ω-3 PUFA) have been administered to ARDS patients, mostly by the enteral route, as immune-enhancing diets with eicosapentaenoic acid, γ-linolenic acid, and antioxidants. However, clinical benefits of ω-3 PUFAs in ARDS patients remain unclear because clinical trials have found conflicting results. Considering the most recent randomized controlled trials (RCTs) and recent change in administration strategies, the aim of this updated systematic review and meta-analysis was to evaluate clinical benefits of ω-3 PUFA administration on gas exchange and clinical outcomes in ARDS patients. We searched for RCTs conducted in intensive care unit (ICU) patients with ARDS comparing the administration of ω-3 PUFAs to placebo. The outcomes assessed were PaO2-to-FiO2 ratio evaluated early (3–4 d) and later (7–8 d), mortality, ICU and hospital length of stay (LOS), length of mechanical ventilation (MV), and infectious complications. Two independent reviewers assessed eligibility, risk of bias, and abstracted data. Data were pooled using a random effect model to estimate the relative risk or weighted mean difference (WMD). Twelve RCTs (n = 1280 patients) met our inclusion criteria. Omega-3 PUFAs administration was associated with a significant improvement in early PaO2-to-FiO2 ratio (WMD = 49.33; 95% confidence interval [CI] 20.88–77.78; P = 0.0007; I2 = 69%), which persisted at days 7 to 8 (WMD = 27.87; 95% CI 0.75–54.99; P = 0.04; I2 = 57%). There was a trend in those receiving ω-3 PUFA toward reduced ICU LOS (P = 0.08) and duration of MV (P = 0.06), whereas mortality, hospital LOS, and infectious complications remained unchanged. Continuous enteral infusion was associated with reduced mortality (P = 0.02), whereas analysis restricted to enteral administration either with or without bolus found improved early PaO2 and FiO2 (P = 0.001) and MV duration (P = 0.03). Trials at higher risk of bias had a significant reduction in mortality (P = 0.04), and improvement in late PaO2-to-FiO2 ratio (P = 0.003). In critically ill patients with ARDS, ω-3 PUFAs in enteral immunomodulatory diets may be associated with an improvement in early and late PaO2-to-FiO2 ratio, and statistical trends exist for an improved ICU LOS and MV duration. Considering these results, administering ω-3 PUFAs appears a reasonable strategy in ARDS.</description><identifier>ISSN: 0899-9007</identifier><identifier>ISSN: 1873-1244</identifier><identifier>EISSN: 1873-1244</identifier><identifier>DOI: 10.1016/j.nut.2018.10.026</identifier><identifier>PMID: 30703574</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Acute respiratory distress syndrome ; Antioxidants ; Antioxidants - therapeutic use ; Bias ; Clinical trials ; Confidence intervals ; Critical Illness - therapy ; Diet ; Eicosapentaenoic acid ; Eicosapentaenoic Acid - analogs &amp; derivatives ; Eicosapentaenoic Acid - therapeutic use ; Enteral Nutrition - methods ; Fatty acids ; Fatty Acids, Omega-3 - administration &amp; dosage ; Fish oil ; Fish oils ; gamma-Linolenic Acid - therapeutic use ; Gas exchange ; Humans ; Hypoxemia ; Immunomodulation ; Inflammation ; Inflammatory response ; Length of Stay - statistics &amp; numerical data ; Linolenic acid ; Lungs ; Mechanical ventilation ; Medical research ; Meta-analysis ; Mortality ; Omega-3 ; Parenchyma ; Patients ; Polyunsaturated fatty acids ; Randomized Controlled Trials as Topic ; Respiration, Artificial - statistics &amp; numerical data ; Respiratory distress syndrome ; Respiratory Distress Syndrome - therapy ; Review ; Statistical analysis ; Systematic review ; Treatment Outcome ; Upgrading ; Ventilation ; Ventilators</subject><ispartof>Nutrition (Burbank, Los Angeles County, Calif.), 2019-05, Vol.61, p.84-92</ispartof><rights>2018 Elsevier Inc.</rights><rights>Copyright © 2018 Elsevier Inc. All rights reserved.</rights><rights>Copyright Elsevier Limited May 2019</rights><rights>2018 Elsevier Inc. All rights reserved. 2018 Elsevier Inc.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c480t-c80bc774a4b1a97fde8d33433118baed4433ea6783e56b386eb8810b9dc51c4e3</citedby><cites>FETCH-LOGICAL-c480t-c80bc774a4b1a97fde8d33433118baed4433ea6783e56b386eb8810b9dc51c4e3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.proquest.com/docview/2191338090?pq-origsite=primo$$EHTML$$P50$$Gproquest$$H</linktohtml><link.rule.ids>230,314,780,784,885,3550,27924,27925,45995,64385,64387,64389,72469</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30703574$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Langlois, Pascal L.</creatorcontrib><creatorcontrib>D'Aragon, Fréderick</creatorcontrib><creatorcontrib>Hardy, Gil</creatorcontrib><creatorcontrib>Manzanares, William</creatorcontrib><title>Omega-3 polyunsaturated fatty acids in critically ill patients with acute respiratory distress syndrome: A systematic review and meta-analysis</title><title>Nutrition (Burbank, Los Angeles County, Calif.)</title><addtitle>Nutrition</addtitle><description>•Omega-3 polyunsaturated fatty acids have been administered to ARDS patients, mostly by enteral route with contradictory results.•Enteral immunomodulatory diets with fish oils may be associated with an improvement in early and late PaO2-to-FiO2 ratio in ARDS, although a clinical and statistically significant heterogeneity exists.•The treatment effect seems to be greatest in those trials published before 2011 that provided an immunomodulatory formula with fish oils administered as a continuous infusion.•Further well-powered clinical trials aimed at evaluating whether modulating pathophysiology of ARDS patients with omega-3 could improve morbidity and mortality are warranted. Acute respiratory distress syndrome (ARDS) is characterized by an acute inflammatory response in the lung parenchyma leading to severe hypoxemia. Because of its anti-inflammatory and immunomodulatory properties, omega-3 polyunsaturated fatty acids (ω-3 PUFA) have been administered to ARDS patients, mostly by the enteral route, as immune-enhancing diets with eicosapentaenoic acid, γ-linolenic acid, and antioxidants. However, clinical benefits of ω-3 PUFAs in ARDS patients remain unclear because clinical trials have found conflicting results. Considering the most recent randomized controlled trials (RCTs) and recent change in administration strategies, the aim of this updated systematic review and meta-analysis was to evaluate clinical benefits of ω-3 PUFA administration on gas exchange and clinical outcomes in ARDS patients. We searched for RCTs conducted in intensive care unit (ICU) patients with ARDS comparing the administration of ω-3 PUFAs to placebo. The outcomes assessed were PaO2-to-FiO2 ratio evaluated early (3–4 d) and later (7–8 d), mortality, ICU and hospital length of stay (LOS), length of mechanical ventilation (MV), and infectious complications. Two independent reviewers assessed eligibility, risk of bias, and abstracted data. Data were pooled using a random effect model to estimate the relative risk or weighted mean difference (WMD). Twelve RCTs (n = 1280 patients) met our inclusion criteria. Omega-3 PUFAs administration was associated with a significant improvement in early PaO2-to-FiO2 ratio (WMD = 49.33; 95% confidence interval [CI] 20.88–77.78; P = 0.0007; I2 = 69%), which persisted at days 7 to 8 (WMD = 27.87; 95% CI 0.75–54.99; P = 0.04; I2 = 57%). There was a trend in those receiving ω-3 PUFA toward reduced ICU LOS (P = 0.08) and duration of MV (P = 0.06), whereas mortality, hospital LOS, and infectious complications remained unchanged. Continuous enteral infusion was associated with reduced mortality (P = 0.02), whereas analysis restricted to enteral administration either with or without bolus found improved early PaO2 and FiO2 (P = 0.001) and MV duration (P = 0.03). Trials at higher risk of bias had a significant reduction in mortality (P = 0.04), and improvement in late PaO2-to-FiO2 ratio (P = 0.003). In critically ill patients with ARDS, ω-3 PUFAs in enteral immunomodulatory diets may be associated with an improvement in early and late PaO2-to-FiO2 ratio, and statistical trends exist for an improved ICU LOS and MV duration. Considering these results, administering ω-3 PUFAs appears a reasonable strategy in ARDS.</description><subject>Acute respiratory distress syndrome</subject><subject>Antioxidants</subject><subject>Antioxidants - therapeutic use</subject><subject>Bias</subject><subject>Clinical trials</subject><subject>Confidence intervals</subject><subject>Critical Illness - therapy</subject><subject>Diet</subject><subject>Eicosapentaenoic acid</subject><subject>Eicosapentaenoic Acid - analogs &amp; derivatives</subject><subject>Eicosapentaenoic Acid - therapeutic use</subject><subject>Enteral Nutrition - methods</subject><subject>Fatty acids</subject><subject>Fatty Acids, Omega-3 - administration &amp; dosage</subject><subject>Fish oil</subject><subject>Fish oils</subject><subject>gamma-Linolenic Acid - therapeutic use</subject><subject>Gas exchange</subject><subject>Humans</subject><subject>Hypoxemia</subject><subject>Immunomodulation</subject><subject>Inflammation</subject><subject>Inflammatory response</subject><subject>Length of Stay - statistics &amp; numerical data</subject><subject>Linolenic acid</subject><subject>Lungs</subject><subject>Mechanical ventilation</subject><subject>Medical research</subject><subject>Meta-analysis</subject><subject>Mortality</subject><subject>Omega-3</subject><subject>Parenchyma</subject><subject>Patients</subject><subject>Polyunsaturated fatty acids</subject><subject>Randomized Controlled Trials as Topic</subject><subject>Respiration, Artificial - statistics &amp; numerical data</subject><subject>Respiratory distress syndrome</subject><subject>Respiratory Distress Syndrome - therapy</subject><subject>Review</subject><subject>Statistical analysis</subject><subject>Systematic review</subject><subject>Treatment Outcome</subject><subject>Upgrading</subject><subject>Ventilation</subject><subject>Ventilators</subject><issn>0899-9007</issn><issn>1873-1244</issn><issn>1873-1244</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>8G5</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>GUQSH</sourceid><sourceid>M2O</sourceid><recordid>eNp9kctuFDEQRS0EIpPAB7BBltiw6cFue7ptWKAoCg8pUjawtqrtmsQj9wPbnah_gm_GrQkRsGDlKvvcK1ddQl5xtuWMN-8O22HO25pxVfotq5snZMNVKypeS_mUbJjSutKMtSfkNKUDY4zrRj8nJ4K1TOxauSE_r3u8gUrQaQzLPCTIc4SMju4h54WC9S5RP1AbffYWQlioD4FOkD0OOdF7n28LNWekEdPki3iMC3U-5dInmpbBxbHH9_S81CljX5S2sHce7ykMjvaYoYIBwpJ8ekGe7SEkfPlwnpHvny6_XXyprq4_f704v6qsVCxXVrHOtq0E2XHQ7d6hckJIIThXHaCTpURoWiVw13RCNdgpxVmnnd1xK1GckY9H32nuenS2zBIhmCn6HuJiRvDm75fB35qb8c7wdYe14sXh7YNDHH_MmLLpfbIYAgw4zsnUvNWyFg2XBX3zD3oY51gmXinNhVBMs0LxI2XjmFLE_eNvODNr3OZgStxmjXu9KnEXzes_x3hU_M63AB-OAJZllpVHk2wJzqLzEW02bvT_sf8FnVG_OQ</recordid><startdate>20190501</startdate><enddate>20190501</enddate><creator>Langlois, Pascal L.</creator><creator>D'Aragon, Fréderick</creator><creator>Hardy, Gil</creator><creator>Manzanares, William</creator><general>Elsevier Inc</general><general>Elsevier Limited</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>3V.</scope><scope>7RQ</scope><scope>7RV</scope><scope>7TS</scope><scope>7U7</scope><scope>7X7</scope><scope>7XB</scope><scope>88C</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>8G5</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AN0</scope><scope>ASE</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FPQ</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>GUQSH</scope><scope>HCIFZ</scope><scope>K6X</scope><scope>K9.</scope><scope>KB0</scope><scope>LK8</scope><scope>M0S</scope><scope>M0T</scope><scope>M1P</scope><scope>M2O</scope><scope>M7P</scope><scope>MBDVC</scope><scope>NAPCQ</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>Q9U</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20190501</creationdate><title>Omega-3 polyunsaturated fatty acids in critically ill patients with acute respiratory distress syndrome: A systematic review and meta-analysis</title><author>Langlois, Pascal L. ; 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numerical data</topic><topic>Linolenic acid</topic><topic>Lungs</topic><topic>Mechanical ventilation</topic><topic>Medical research</topic><topic>Meta-analysis</topic><topic>Mortality</topic><topic>Omega-3</topic><topic>Parenchyma</topic><topic>Patients</topic><topic>Polyunsaturated fatty acids</topic><topic>Randomized Controlled Trials as Topic</topic><topic>Respiration, Artificial - statistics &amp; numerical data</topic><topic>Respiratory distress syndrome</topic><topic>Respiratory Distress Syndrome - therapy</topic><topic>Review</topic><topic>Statistical analysis</topic><topic>Systematic review</topic><topic>Treatment Outcome</topic><topic>Upgrading</topic><topic>Ventilation</topic><topic>Ventilators</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Langlois, Pascal L.</creatorcontrib><creatorcontrib>D'Aragon, Fréderick</creatorcontrib><creatorcontrib>Hardy, Gil</creatorcontrib><creatorcontrib>Manzanares, William</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Career &amp; 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Acute respiratory distress syndrome (ARDS) is characterized by an acute inflammatory response in the lung parenchyma leading to severe hypoxemia. Because of its anti-inflammatory and immunomodulatory properties, omega-3 polyunsaturated fatty acids (ω-3 PUFA) have been administered to ARDS patients, mostly by the enteral route, as immune-enhancing diets with eicosapentaenoic acid, γ-linolenic acid, and antioxidants. However, clinical benefits of ω-3 PUFAs in ARDS patients remain unclear because clinical trials have found conflicting results. Considering the most recent randomized controlled trials (RCTs) and recent change in administration strategies, the aim of this updated systematic review and meta-analysis was to evaluate clinical benefits of ω-3 PUFA administration on gas exchange and clinical outcomes in ARDS patients. We searched for RCTs conducted in intensive care unit (ICU) patients with ARDS comparing the administration of ω-3 PUFAs to placebo. The outcomes assessed were PaO2-to-FiO2 ratio evaluated early (3–4 d) and later (7–8 d), mortality, ICU and hospital length of stay (LOS), length of mechanical ventilation (MV), and infectious complications. Two independent reviewers assessed eligibility, risk of bias, and abstracted data. Data were pooled using a random effect model to estimate the relative risk or weighted mean difference (WMD). Twelve RCTs (n = 1280 patients) met our inclusion criteria. Omega-3 PUFAs administration was associated with a significant improvement in early PaO2-to-FiO2 ratio (WMD = 49.33; 95% confidence interval [CI] 20.88–77.78; P = 0.0007; I2 = 69%), which persisted at days 7 to 8 (WMD = 27.87; 95% CI 0.75–54.99; P = 0.04; I2 = 57%). There was a trend in those receiving ω-3 PUFA toward reduced ICU LOS (P = 0.08) and duration of MV (P = 0.06), whereas mortality, hospital LOS, and infectious complications remained unchanged. Continuous enteral infusion was associated with reduced mortality (P = 0.02), whereas analysis restricted to enteral administration either with or without bolus found improved early PaO2 and FiO2 (P = 0.001) and MV duration (P = 0.03). Trials at higher risk of bias had a significant reduction in mortality (P = 0.04), and improvement in late PaO2-to-FiO2 ratio (P = 0.003). In critically ill patients with ARDS, ω-3 PUFAs in enteral immunomodulatory diets may be associated with an improvement in early and late PaO2-to-FiO2 ratio, and statistical trends exist for an improved ICU LOS and MV duration. Considering these results, administering ω-3 PUFAs appears a reasonable strategy in ARDS.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>30703574</pmid><doi>10.1016/j.nut.2018.10.026</doi><tpages>9</tpages><oa>free_for_read</oa></addata></record>
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identifier ISSN: 0899-9007
ispartof Nutrition (Burbank, Los Angeles County, Calif.), 2019-05, Vol.61, p.84-92
issn 0899-9007
1873-1244
1873-1244
language eng
recordid cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_10019281
source MEDLINE; Access via ScienceDirect (Elsevier); ProQuest Central UK/Ireland
subjects Acute respiratory distress syndrome
Antioxidants
Antioxidants - therapeutic use
Bias
Clinical trials
Confidence intervals
Critical Illness - therapy
Diet
Eicosapentaenoic acid
Eicosapentaenoic Acid - analogs & derivatives
Eicosapentaenoic Acid - therapeutic use
Enteral Nutrition - methods
Fatty acids
Fatty Acids, Omega-3 - administration & dosage
Fish oil
Fish oils
gamma-Linolenic Acid - therapeutic use
Gas exchange
Humans
Hypoxemia
Immunomodulation
Inflammation
Inflammatory response
Length of Stay - statistics & numerical data
Linolenic acid
Lungs
Mechanical ventilation
Medical research
Meta-analysis
Mortality
Omega-3
Parenchyma
Patients
Polyunsaturated fatty acids
Randomized Controlled Trials as Topic
Respiration, Artificial - statistics & numerical data
Respiratory distress syndrome
Respiratory Distress Syndrome - therapy
Review
Statistical analysis
Systematic review
Treatment Outcome
Upgrading
Ventilation
Ventilators
title Omega-3 polyunsaturated fatty acids in critically ill patients with acute respiratory distress syndrome: A systematic review and meta-analysis
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-12-30T10%3A02%3A42IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Omega-3%20polyunsaturated%20fatty%20acids%20in%20critically%20ill%20patients%20with%20acute%20respiratory%20distress%20syndrome:%20A%20systematic%20review%20and%20meta-analysis&rft.jtitle=Nutrition%20(Burbank,%20Los%20Angeles%20County,%20Calif.)&rft.au=Langlois,%20Pascal%20L.&rft.date=2019-05-01&rft.volume=61&rft.spage=84&rft.epage=92&rft.pages=84-92&rft.issn=0899-9007&rft.eissn=1873-1244&rft_id=info:doi/10.1016/j.nut.2018.10.026&rft_dat=%3Cproquest_pubme%3E2179423614%3C/proquest_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2191338090&rft_id=info:pmid/30703574&rft_els_id=S0899900718305501&rfr_iscdi=true