Dietary Intake of Proteins and Calories Is Inversely Associated With The Oxidation State of Plasma Thiols in End-Stage Renal Disease Patients

Objectives Oxidative stress contributes to the pathogenesis of protein-energy wasting in maintenance hemodialysis (MHD) patients, but knowledge of specific effectors and mechanisms remains fragmented. Aim of the study was to define whether and how food intake is involved in the causal relationship b...

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Veröffentlicht in:Journal of renal nutrition 2015-11, Vol.25 (6), p.494-503
Hauptverfasser: Fanti, Paolo, MD, Giustarini, Daniela, PhD, Rossi, Ranieri, PhD, Cunningham, Sue E.D., RD, PhD, Folli, Franco, MD, PhD, Khazim, Khaled, MD, Cornell, John, PhD, Matteucci, Elena, MD, Bansal, Shweta, MD
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container_end_page 503
container_issue 6
container_start_page 494
container_title Journal of renal nutrition
container_volume 25
creator Fanti, Paolo, MD
Giustarini, Daniela, PhD
Rossi, Ranieri, PhD
Cunningham, Sue E.D., RD, PhD
Folli, Franco, MD, PhD
Khazim, Khaled, MD
Cornell, John, PhD
Matteucci, Elena, MD
Bansal, Shweta, MD
description Objectives Oxidative stress contributes to the pathogenesis of protein-energy wasting in maintenance hemodialysis (MHD) patients, but knowledge of specific effectors and mechanisms remains fragmented. Aim of the study was to define whether and how food intake is involved in the causal relationship between oxidative stress and protein-energy wasting. Methods Seventy-one adult MHD patients and 24 healthy subjects (control) were studied cross-sectionally with analyses of diet record and of oxidative stress, as measured by a battery of plasma thiols including the protein sulfhydryl (-SH) group (PSH) levels (a marker of total protein–SH reducing capacity), the protein thiolation index (PTI, the ratio between disulfide, i.e., oxidized and reduced –SH groups in proteins), low molecular mass (LMM) thiols, LMM disulfides, and mixed LMM-protein disulfides. In addition, interleukin-6 (IL-6), albumin, C-reactive protein, and neutrophil gelatinase-associated lipocalin (NGAL) were measured as markers of inflammation. Results The patients showed low energy (22.0 ± 8.4 kcal/kg/day) and adequate protein (1.0 ± 0.4 g/kg/day) intakes, high levels of cystine (CySS; patients vs. control: 113.5 [90.9-132.8] vs. 68.2 [56.2-75.7] μM), cysteinylated proteins (CySSP; 216.0 [182.8-254.0] vs. 163.5 [150.0-195.5] μM), and high PTI (0.76 [0.61-0.88] vs. 0.43 [0.40-0.54]; P  
doi_str_mv 10.1053/j.jrn.2015.06.003
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Aim of the study was to define whether and how food intake is involved in the causal relationship between oxidative stress and protein-energy wasting. Methods Seventy-one adult MHD patients and 24 healthy subjects (control) were studied cross-sectionally with analyses of diet record and of oxidative stress, as measured by a battery of plasma thiols including the protein sulfhydryl (-SH) group (PSH) levels (a marker of total protein–SH reducing capacity), the protein thiolation index (PTI, the ratio between disulfide, i.e., oxidized and reduced –SH groups in proteins), low molecular mass (LMM) thiols, LMM disulfides, and mixed LMM-protein disulfides. In addition, interleukin-6 (IL-6), albumin, C-reactive protein, and neutrophil gelatinase-associated lipocalin (NGAL) were measured as markers of inflammation. Results The patients showed low energy (22.0 ± 8.4 kcal/kg/day) and adequate protein (1.0 ± 0.4 g/kg/day) intakes, high levels of cystine (CySS; patients vs. control: 113.5 [90.9-132.8] vs. 68.2 [56.2-75.7] μM), cysteinylated proteins (CySSP; 216.0 [182.8-254.0] vs. 163.5 [150.0-195.5] μM), and high PTI (0.76 [0.61-0.88] vs. 0.43 [0.40-0.54]; P  &lt; .001 in all comparisons). In patients, variation of CySSP was explained by a standard regression model (R = 0.775; P  = .00001) that included significant contributions of protein intake (β = −0.361), NGAL (β = 0.387), age (β = 0.295), and albumin (β = 0.457). In the same model, variation of PTI (R = 0.624; P  = .01) was explained by protein intake (β = −0.384) and age (β = 0.326) and NGAL (β = 0.311). However, when PSH was entered as dependent variable (R = 0.730; P  = .0001), only serum albumin (β = 0.495) and age (β = −0.280), but not dietary intake or NGAL, contributed to the model. Conclusions In MHD, markers of thiol oxidation including CySSP and PTI show independent association with dietary intake and NGAL, whereas PSH, a marker of thiol-reducing capacity, did not associate with these same variables. The mechanism(s) responsible for inverse association between oxidative stress and food intake in MHD remain undefined.</description><identifier>ISSN: 1051-2276</identifier><identifier>EISSN: 1532-8503</identifier><identifier>DOI: 10.1053/j.jrn.2015.06.003</identifier><identifier>PMID: 26235932</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Acute-Phase Proteins ; Adult ; Aged ; Aged, 80 and over ; Biomarkers - blood ; C-Reactive Protein - metabolism ; Case-Control Studies ; Cross-Sectional Studies ; Diet Records ; Dietary Proteins - administration &amp; dosage ; Energy Intake ; Female ; Humans ; Interleukin-6 - blood ; Kidney Failure, Chronic - blood ; Kidney Failure, Chronic - therapy ; Lipocalin-2 ; Lipocalins - blood ; Male ; Middle Aged ; Nephrology ; Oxidative Stress ; Proto-Oncogene Proteins - blood ; Renal Dialysis ; Serum Albumin - metabolism ; Sulfhydryl Compounds - blood ; Sulfhydryl Compounds - chemistry ; Young Adult</subject><ispartof>Journal of renal nutrition, 2015-11, Vol.25 (6), p.494-503</ispartof><rights>National Kidney Foundation, Inc.</rights><rights>2015 National Kidney Foundation, Inc.</rights><rights>Copyright © 2015 National Kidney Foundation, Inc. Published by Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c576t-796b862b31cb3c85f6ee09cd53554161ae3776c1bf1a3d55e20cb9b8375692cf3</citedby><cites>FETCH-LOGICAL-c576t-796b862b31cb3c85f6ee09cd53554161ae3776c1bf1a3d55e20cb9b8375692cf3</cites><orcidid>0000-0003-4929-5316 ; 0000-0002-6065-9013 ; 0000-0001-8037-7825 ; 0000-0001-6872-007X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1053/j.jrn.2015.06.003$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>230,314,780,784,885,3550,27924,27925,45995</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26235932$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Fanti, Paolo, MD</creatorcontrib><creatorcontrib>Giustarini, Daniela, PhD</creatorcontrib><creatorcontrib>Rossi, Ranieri, PhD</creatorcontrib><creatorcontrib>Cunningham, Sue E.D., RD, PhD</creatorcontrib><creatorcontrib>Folli, Franco, MD, PhD</creatorcontrib><creatorcontrib>Khazim, Khaled, MD</creatorcontrib><creatorcontrib>Cornell, John, PhD</creatorcontrib><creatorcontrib>Matteucci, Elena, MD</creatorcontrib><creatorcontrib>Bansal, Shweta, MD</creatorcontrib><title>Dietary Intake of Proteins and Calories Is Inversely Associated With The Oxidation State of Plasma Thiols in End-Stage Renal Disease Patients</title><title>Journal of renal nutrition</title><addtitle>J Ren Nutr</addtitle><description>Objectives Oxidative stress contributes to the pathogenesis of protein-energy wasting in maintenance hemodialysis (MHD) patients, but knowledge of specific effectors and mechanisms remains fragmented. Aim of the study was to define whether and how food intake is involved in the causal relationship between oxidative stress and protein-energy wasting. Methods Seventy-one adult MHD patients and 24 healthy subjects (control) were studied cross-sectionally with analyses of diet record and of oxidative stress, as measured by a battery of plasma thiols including the protein sulfhydryl (-SH) group (PSH) levels (a marker of total protein–SH reducing capacity), the protein thiolation index (PTI, the ratio between disulfide, i.e., oxidized and reduced –SH groups in proteins), low molecular mass (LMM) thiols, LMM disulfides, and mixed LMM-protein disulfides. In addition, interleukin-6 (IL-6), albumin, C-reactive protein, and neutrophil gelatinase-associated lipocalin (NGAL) were measured as markers of inflammation. Results The patients showed low energy (22.0 ± 8.4 kcal/kg/day) and adequate protein (1.0 ± 0.4 g/kg/day) intakes, high levels of cystine (CySS; patients vs. control: 113.5 [90.9-132.8] vs. 68.2 [56.2-75.7] μM), cysteinylated proteins (CySSP; 216.0 [182.8-254.0] vs. 163.5 [150.0-195.5] μM), and high PTI (0.76 [0.61-0.88] vs. 0.43 [0.40-0.54]; P  &lt; .001 in all comparisons). In patients, variation of CySSP was explained by a standard regression model (R = 0.775; P  = .00001) that included significant contributions of protein intake (β = −0.361), NGAL (β = 0.387), age (β = 0.295), and albumin (β = 0.457). In the same model, variation of PTI (R = 0.624; P  = .01) was explained by protein intake (β = −0.384) and age (β = 0.326) and NGAL (β = 0.311). However, when PSH was entered as dependent variable (R = 0.730; P  = .0001), only serum albumin (β = 0.495) and age (β = −0.280), but not dietary intake or NGAL, contributed to the model. Conclusions In MHD, markers of thiol oxidation including CySSP and PTI show independent association with dietary intake and NGAL, whereas PSH, a marker of thiol-reducing capacity, did not associate with these same variables. The mechanism(s) responsible for inverse association between oxidative stress and food intake in MHD remain undefined.</description><subject>Acute-Phase Proteins</subject><subject>Adult</subject><subject>Aged</subject><subject>Aged, 80 and over</subject><subject>Biomarkers - blood</subject><subject>C-Reactive Protein - metabolism</subject><subject>Case-Control Studies</subject><subject>Cross-Sectional Studies</subject><subject>Diet Records</subject><subject>Dietary Proteins - administration &amp; dosage</subject><subject>Energy Intake</subject><subject>Female</subject><subject>Humans</subject><subject>Interleukin-6 - blood</subject><subject>Kidney Failure, Chronic - blood</subject><subject>Kidney Failure, Chronic - therapy</subject><subject>Lipocalin-2</subject><subject>Lipocalins - blood</subject><subject>Male</subject><subject>Middle Aged</subject><subject>Nephrology</subject><subject>Oxidative Stress</subject><subject>Proto-Oncogene Proteins - blood</subject><subject>Renal Dialysis</subject><subject>Serum Albumin - metabolism</subject><subject>Sulfhydryl Compounds - blood</subject><subject>Sulfhydryl Compounds - chemistry</subject><subject>Young Adult</subject><issn>1051-2276</issn><issn>1532-8503</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9UtFqFDEUHUSxtfoBvkh-YMbcpMnMIBTKtupCocVWfAyZ5E4309mkJOnS_Qj_2ayrRX0QAgmce84l55yqegu0ASr4-6mZom8YBdFQ2VDKn1WHIDirO0H58_KmAmrGWnlQvUppohRAdOxldcAk46Ln7LD6fuYw67glS5_1HZIwkqsYMjqfiPaWLPQcosNEluX4DcaE85acphSM0xkt-ebyityskFw-OquzC55c54L8VJp1WuuCujAn4jw597Yu6C2SL-j1TM5cQp2QXBUi-pxeVy9GPSd88-s-qr5-PL9ZfK4vLj8tF6cXtRGtzHXby6GTbOBgBm46MUpE2hsruBDHIEEjb1tpYBhBcysEMmqGfuh4K2TPzMiPqpO97v3DsEZryu6oZ3Uf3bp4oYJ26m_Eu5W6DRt1LKEHgCIAewETQ0oRxycuULXLRk2qZKN22SgqVcmmcN79ufSJ8TuMMvBhP4Dl6xuHUSVTbDFoXUSTlQ3uv_In_7DN7Lwzer7DLaYpPMRieVKgElNUXe_KsesGiNILxjj_AezEto8</recordid><startdate>20151101</startdate><enddate>20151101</enddate><creator>Fanti, Paolo, MD</creator><creator>Giustarini, Daniela, PhD</creator><creator>Rossi, Ranieri, PhD</creator><creator>Cunningham, Sue E.D., RD, PhD</creator><creator>Folli, Franco, MD, PhD</creator><creator>Khazim, Khaled, MD</creator><creator>Cornell, John, PhD</creator><creator>Matteucci, Elena, MD</creator><creator>Bansal, Shweta, MD</creator><general>Elsevier 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>5PM</scope><orcidid>https://orcid.org/0000-0003-4929-5316</orcidid><orcidid>https://orcid.org/0000-0002-6065-9013</orcidid><orcidid>https://orcid.org/0000-0001-8037-7825</orcidid><orcidid>https://orcid.org/0000-0001-6872-007X</orcidid></search><sort><creationdate>20151101</creationdate><title>Dietary Intake of Proteins and Calories Is Inversely Associated With The Oxidation State of Plasma Thiols in End-Stage Renal Disease Patients</title><author>Fanti, Paolo, MD ; Giustarini, Daniela, PhD ; Rossi, Ranieri, PhD ; Cunningham, Sue E.D., RD, PhD ; Folli, Franco, MD, PhD ; Khazim, Khaled, MD ; Cornell, John, PhD ; Matteucci, Elena, MD ; Bansal, Shweta, MD</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c576t-796b862b31cb3c85f6ee09cd53554161ae3776c1bf1a3d55e20cb9b8375692cf3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Acute-Phase Proteins</topic><topic>Adult</topic><topic>Aged</topic><topic>Aged, 80 and over</topic><topic>Biomarkers - blood</topic><topic>C-Reactive Protein - metabolism</topic><topic>Case-Control Studies</topic><topic>Cross-Sectional Studies</topic><topic>Diet Records</topic><topic>Dietary Proteins - administration &amp; dosage</topic><topic>Energy Intake</topic><topic>Female</topic><topic>Humans</topic><topic>Interleukin-6 - blood</topic><topic>Kidney Failure, Chronic - blood</topic><topic>Kidney Failure, Chronic - therapy</topic><topic>Lipocalin-2</topic><topic>Lipocalins - blood</topic><topic>Male</topic><topic>Middle Aged</topic><topic>Nephrology</topic><topic>Oxidative Stress</topic><topic>Proto-Oncogene Proteins - blood</topic><topic>Renal Dialysis</topic><topic>Serum Albumin - metabolism</topic><topic>Sulfhydryl Compounds - blood</topic><topic>Sulfhydryl Compounds - chemistry</topic><topic>Young Adult</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Fanti, Paolo, MD</creatorcontrib><creatorcontrib>Giustarini, Daniela, PhD</creatorcontrib><creatorcontrib>Rossi, Ranieri, PhD</creatorcontrib><creatorcontrib>Cunningham, Sue E.D., RD, PhD</creatorcontrib><creatorcontrib>Folli, Franco, MD, PhD</creatorcontrib><creatorcontrib>Khazim, Khaled, MD</creatorcontrib><creatorcontrib>Cornell, John, PhD</creatorcontrib><creatorcontrib>Matteucci, Elena, MD</creatorcontrib><creatorcontrib>Bansal, Shweta, MD</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Journal of renal nutrition</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Fanti, Paolo, MD</au><au>Giustarini, Daniela, PhD</au><au>Rossi, Ranieri, PhD</au><au>Cunningham, Sue E.D., RD, PhD</au><au>Folli, Franco, MD, PhD</au><au>Khazim, Khaled, MD</au><au>Cornell, John, PhD</au><au>Matteucci, Elena, MD</au><au>Bansal, Shweta, MD</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Dietary Intake of Proteins and Calories Is Inversely Associated With The Oxidation State of Plasma Thiols in End-Stage Renal Disease Patients</atitle><jtitle>Journal of renal nutrition</jtitle><addtitle>J Ren Nutr</addtitle><date>2015-11-01</date><risdate>2015</risdate><volume>25</volume><issue>6</issue><spage>494</spage><epage>503</epage><pages>494-503</pages><issn>1051-2276</issn><eissn>1532-8503</eissn><abstract>Objectives Oxidative stress contributes to the pathogenesis of protein-energy wasting in maintenance hemodialysis (MHD) patients, but knowledge of specific effectors and mechanisms remains fragmented. Aim of the study was to define whether and how food intake is involved in the causal relationship between oxidative stress and protein-energy wasting. Methods Seventy-one adult MHD patients and 24 healthy subjects (control) were studied cross-sectionally with analyses of diet record and of oxidative stress, as measured by a battery of plasma thiols including the protein sulfhydryl (-SH) group (PSH) levels (a marker of total protein–SH reducing capacity), the protein thiolation index (PTI, the ratio between disulfide, i.e., oxidized and reduced –SH groups in proteins), low molecular mass (LMM) thiols, LMM disulfides, and mixed LMM-protein disulfides. In addition, interleukin-6 (IL-6), albumin, C-reactive protein, and neutrophil gelatinase-associated lipocalin (NGAL) were measured as markers of inflammation. Results The patients showed low energy (22.0 ± 8.4 kcal/kg/day) and adequate protein (1.0 ± 0.4 g/kg/day) intakes, high levels of cystine (CySS; patients vs. control: 113.5 [90.9-132.8] vs. 68.2 [56.2-75.7] μM), cysteinylated proteins (CySSP; 216.0 [182.8-254.0] vs. 163.5 [150.0-195.5] μM), and high PTI (0.76 [0.61-0.88] vs. 0.43 [0.40-0.54]; P  &lt; .001 in all comparisons). In patients, variation of CySSP was explained by a standard regression model (R = 0.775; P  = .00001) that included significant contributions of protein intake (β = −0.361), NGAL (β = 0.387), age (β = 0.295), and albumin (β = 0.457). In the same model, variation of PTI (R = 0.624; P  = .01) was explained by protein intake (β = −0.384) and age (β = 0.326) and NGAL (β = 0.311). However, when PSH was entered as dependent variable (R = 0.730; P  = .0001), only serum albumin (β = 0.495) and age (β = −0.280), but not dietary intake or NGAL, contributed to the model. Conclusions In MHD, markers of thiol oxidation including CySSP and PTI show independent association with dietary intake and NGAL, whereas PSH, a marker of thiol-reducing capacity, did not associate with these same variables. The mechanism(s) responsible for inverse association between oxidative stress and food intake in MHD remain undefined.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>26235932</pmid><doi>10.1053/j.jrn.2015.06.003</doi><tpages>10</tpages><orcidid>https://orcid.org/0000-0003-4929-5316</orcidid><orcidid>https://orcid.org/0000-0002-6065-9013</orcidid><orcidid>https://orcid.org/0000-0001-8037-7825</orcidid><orcidid>https://orcid.org/0000-0001-6872-007X</orcidid><oa>free_for_read</oa></addata></record>
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subjects Acute-Phase Proteins
Adult
Aged
Aged, 80 and over
Biomarkers - blood
C-Reactive Protein - metabolism
Case-Control Studies
Cross-Sectional Studies
Diet Records
Dietary Proteins - administration & dosage
Energy Intake
Female
Humans
Interleukin-6 - blood
Kidney Failure, Chronic - blood
Kidney Failure, Chronic - therapy
Lipocalin-2
Lipocalins - blood
Male
Middle Aged
Nephrology
Oxidative Stress
Proto-Oncogene Proteins - blood
Renal Dialysis
Serum Albumin - metabolism
Sulfhydryl Compounds - blood
Sulfhydryl Compounds - chemistry
Young Adult
title Dietary Intake of Proteins and Calories Is Inversely Associated With The Oxidation State of Plasma Thiols in End-Stage Renal Disease Patients
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