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Relationship between inflammation, the gut microbiota, and metabolic osteoarthritis development: studies in a rat model
Summary Osteoarthritis (OA) may result from intrinsic inflammation related to metabolic disturbance. Obesity-associated inflammation is triggered by lipopolysaccharide (LPS) derived from the gut microbiota. However, the relationship between gut microbiota, LPS, inflammation, and OA remain unclear. O...
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Published in: | Osteoarthritis and cartilage 2015-11, Vol.23 (11), p.1989-1998 |
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container_end_page | 1998 |
container_issue | 11 |
container_start_page | 1989 |
container_title | Osteoarthritis and cartilage |
container_volume | 23 |
creator | Collins, K.H Paul, H.A Reimer, R.A Seerattan, R.A Hart, D.A Herzog, W |
description | Summary Osteoarthritis (OA) may result from intrinsic inflammation related to metabolic disturbance. Obesity-associated inflammation is triggered by lipopolysaccharide (LPS) derived from the gut microbiota. However, the relationship between gut microbiota, LPS, inflammation, and OA remain unclear. Objective To evaluate the associations between gut microbiota, systemic LPS levels, serum and local inflammatory profiles, and joint damage in a high fat/high sucrose diet induced obese rat model. Methods 32 rats were randomized to a high fat/high sucrose diet (diet-induced obese (DIO), 40% fat, 45% sucrose, n = 21) or chow diet group (12% fat, 3.7% sucrose n = 11) for 28 weeks. After a 12-week obesity induction period, DIO animals were stratified into Obesity Prone (DIO-P, top 33% by change in body mass, n = 7), and Obesity Resistant groups (DIO-R, bottom 33%, n = 7). At sacrifice, joints were scored using a Modified Mankin Criteria. Blood and synovial fluid analytes, serum LPS, and fecal gut microbiota were analyzed. Results DIO animals had greater Modified Mankin scores than chow animals ( P = 0.002). There was a significant relationship ( r = 0.604, p = 0.001) between body fat, but not body mass, and Modified Mankin score. Eighteen synovial fluid and four serum analytes were increased in DIO animals. DIO serum LPS levels were increased compared to chow ( P = 0.031). Together, Lactobacillus species (spp.) and Methanobrevibacter spp. abundance had a strong predictive relationship with Modified Mankin Score ( r2 = 0.5, P |
doi_str_mv | 10.1016/j.joca.2015.03.014 |
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Obesity-associated inflammation is triggered by lipopolysaccharide (LPS) derived from the gut microbiota. However, the relationship between gut microbiota, LPS, inflammation, and OA remain unclear. Objective To evaluate the associations between gut microbiota, systemic LPS levels, serum and local inflammatory profiles, and joint damage in a high fat/high sucrose diet induced obese rat model. Methods 32 rats were randomized to a high fat/high sucrose diet (diet-induced obese (DIO), 40% fat, 45% sucrose, n = 21) or chow diet group (12% fat, 3.7% sucrose n = 11) for 28 weeks. After a 12-week obesity induction period, DIO animals were stratified into Obesity Prone (DIO-P, top 33% by change in body mass, n = 7), and Obesity Resistant groups (DIO-R, bottom 33%, n = 7). At sacrifice, joints were scored using a Modified Mankin Criteria. Blood and synovial fluid analytes, serum LPS, and fecal gut microbiota were analyzed. Results DIO animals had greater Modified Mankin scores than chow animals ( P = 0.002). There was a significant relationship ( r = 0.604, p = 0.001) between body fat, but not body mass, and Modified Mankin score. Eighteen synovial fluid and four serum analytes were increased in DIO animals. DIO serum LPS levels were increased compared to chow ( P = 0.031). Together, Lactobacillus species (spp.) and Methanobrevibacter spp. abundance had a strong predictive relationship with Modified Mankin Score ( r2 = 0.5, P < 0.001). Conclusions Increased OA in DIO animals is associated with greater body fat, not body mass. The link between gut microbiota and adiposity-derived inflammation and metabolic OA warrants further investigation.</description><identifier>ISSN: 1063-4584</identifier><identifier>EISSN: 1522-9653</identifier><identifier>DOI: 10.1016/j.joca.2015.03.014</identifier><identifier>PMID: 26521745</identifier><language>eng</language><publisher>England: Elsevier Ltd</publisher><subject>Adiposity - physiology ; Animals ; Disease Models, Animal ; Disease Progression ; Gastrointestinal Microbiome ; Gut microbiota and osteoarthritis ; Inflammation - complications ; Inflammation - metabolism ; Inflammation - pathology ; Inflammation and osteoarthritis ; Male ; Metabolic osteoarthritis ; Obesity - complications ; Obesity - metabolism ; Obesity - pathology ; Obesity and inflammation ; Osteoarthritis - etiology ; Osteoarthritis - metabolism ; Osteoarthritis - pathology ; Rat model osteoarthritis ; Rats ; Rats, Sprague-Dawley ; Rheumatology</subject><ispartof>Osteoarthritis and cartilage, 2015-11, Vol.23 (11), p.1989-1998</ispartof><rights>Osteoarthritis Research Society International</rights><rights>2015 Osteoarthritis Research Society International</rights><rights>Copyright © 2015 Osteoarthritis Research Society International. Published by Elsevier Ltd. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c521t-1f3faaaad1d1c7b80faa399c1f61f95e801020183ad94583d07e8916da16da6c3</citedby><cites>FETCH-LOGICAL-c521t-1f3faaaad1d1c7b80faa399c1f61f95e801020183ad94583d07e8916da16da6c3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26521745$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Collins, K.H</creatorcontrib><creatorcontrib>Paul, H.A</creatorcontrib><creatorcontrib>Reimer, R.A</creatorcontrib><creatorcontrib>Seerattan, R.A</creatorcontrib><creatorcontrib>Hart, D.A</creatorcontrib><creatorcontrib>Herzog, W</creatorcontrib><title>Relationship between inflammation, the gut microbiota, and metabolic osteoarthritis development: studies in a rat model</title><title>Osteoarthritis and cartilage</title><addtitle>Osteoarthritis Cartilage</addtitle><description>Summary Osteoarthritis (OA) may result from intrinsic inflammation related to metabolic disturbance. Obesity-associated inflammation is triggered by lipopolysaccharide (LPS) derived from the gut microbiota. However, the relationship between gut microbiota, LPS, inflammation, and OA remain unclear. Objective To evaluate the associations between gut microbiota, systemic LPS levels, serum and local inflammatory profiles, and joint damage in a high fat/high sucrose diet induced obese rat model. Methods 32 rats were randomized to a high fat/high sucrose diet (diet-induced obese (DIO), 40% fat, 45% sucrose, n = 21) or chow diet group (12% fat, 3.7% sucrose n = 11) for 28 weeks. After a 12-week obesity induction period, DIO animals were stratified into Obesity Prone (DIO-P, top 33% by change in body mass, n = 7), and Obesity Resistant groups (DIO-R, bottom 33%, n = 7). At sacrifice, joints were scored using a Modified Mankin Criteria. Blood and synovial fluid analytes, serum LPS, and fecal gut microbiota were analyzed. Results DIO animals had greater Modified Mankin scores than chow animals ( P = 0.002). There was a significant relationship ( r = 0.604, p = 0.001) between body fat, but not body mass, and Modified Mankin score. Eighteen synovial fluid and four serum analytes were increased in DIO animals. DIO serum LPS levels were increased compared to chow ( P = 0.031). Together, Lactobacillus species (spp.) and Methanobrevibacter spp. abundance had a strong predictive relationship with Modified Mankin Score ( r2 = 0.5, P < 0.001). Conclusions Increased OA in DIO animals is associated with greater body fat, not body mass. The link between gut microbiota and adiposity-derived inflammation and metabolic OA warrants further investigation.</description><subject>Adiposity - physiology</subject><subject>Animals</subject><subject>Disease Models, Animal</subject><subject>Disease Progression</subject><subject>Gastrointestinal Microbiome</subject><subject>Gut microbiota and osteoarthritis</subject><subject>Inflammation - complications</subject><subject>Inflammation - metabolism</subject><subject>Inflammation - pathology</subject><subject>Inflammation and osteoarthritis</subject><subject>Male</subject><subject>Metabolic osteoarthritis</subject><subject>Obesity - complications</subject><subject>Obesity - metabolism</subject><subject>Obesity - pathology</subject><subject>Obesity and inflammation</subject><subject>Osteoarthritis - etiology</subject><subject>Osteoarthritis - metabolism</subject><subject>Osteoarthritis - pathology</subject><subject>Rat model osteoarthritis</subject><subject>Rats</subject><subject>Rats, Sprague-Dawley</subject><subject>Rheumatology</subject><issn>1063-4584</issn><issn>1522-9653</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><recordid>eNp9kUtv1TAQhSNERR_wB1ggL1k0YSa-zk0QQkJVC0iVkHisLceecB2c-GI7rfrv63ALCxa1ZHksnzny-aYoXiJUCNi8GavRa1XVgKICXgFunhQnKOq67BrBn-YaGl5uRLs5Lk5jHAGAI8Kz4rhuRI3bjTgpbr-SU8n6Oe7snvWUbolmZufBqWn683DO0o7YzyWxyerge-uTOmdqNmyipHrvrGY-JvIqpF2wyUZm6Iac3080p7cspsVYitmTKRZUtvGG3PPiaFAu0ouH86z4cXX5_eJTef3l4-eLD9elzj9MJQ58UHkZNKi3fQv5xrtO49Dg0AlqASHnb7kyXQ7KDWyp7bAxat2N5mfF64PvPvjfC8UkJxs1Oadm8kuUuK07LrJFnaX1QZpTxhhokPtgJxXuJIJcgctRrsDlClwClxl4bnr14L_0E5l_LX8JZ8G7g4ByyhtLQUZtadZkbCCdpPH2cf_3_7VrZ2erlftFdxRHv4Q585MoYy1BfltHvk4cBUArRMfvAbuzqI8</recordid><startdate>20151101</startdate><enddate>20151101</enddate><creator>Collins, K.H</creator><creator>Paul, H.A</creator><creator>Reimer, R.A</creator><creator>Seerattan, R.A</creator><creator>Hart, D.A</creator><creator>Herzog, W</creator><general>Elsevier Ltd</general><scope>6I.</scope><scope>AAFTH</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></search><sort><creationdate>20151101</creationdate><title>Relationship between inflammation, the gut microbiota, and metabolic osteoarthritis development: studies in a rat model</title><author>Collins, K.H ; Paul, H.A ; Reimer, R.A ; Seerattan, R.A ; Hart, D.A ; Herzog, W</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c521t-1f3faaaad1d1c7b80faa399c1f61f95e801020183ad94583d07e8916da16da6c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Adiposity - physiology</topic><topic>Animals</topic><topic>Disease Models, Animal</topic><topic>Disease Progression</topic><topic>Gastrointestinal Microbiome</topic><topic>Gut microbiota and osteoarthritis</topic><topic>Inflammation - complications</topic><topic>Inflammation - metabolism</topic><topic>Inflammation - pathology</topic><topic>Inflammation and osteoarthritis</topic><topic>Male</topic><topic>Metabolic osteoarthritis</topic><topic>Obesity - complications</topic><topic>Obesity - metabolism</topic><topic>Obesity - pathology</topic><topic>Obesity and inflammation</topic><topic>Osteoarthritis - etiology</topic><topic>Osteoarthritis - metabolism</topic><topic>Osteoarthritis - pathology</topic><topic>Rat model osteoarthritis</topic><topic>Rats</topic><topic>Rats, Sprague-Dawley</topic><topic>Rheumatology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Collins, K.H</creatorcontrib><creatorcontrib>Paul, H.A</creatorcontrib><creatorcontrib>Reimer, R.A</creatorcontrib><creatorcontrib>Seerattan, R.A</creatorcontrib><creatorcontrib>Hart, D.A</creatorcontrib><creatorcontrib>Herzog, W</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</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><jtitle>Osteoarthritis and cartilage</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Collins, K.H</au><au>Paul, H.A</au><au>Reimer, R.A</au><au>Seerattan, R.A</au><au>Hart, D.A</au><au>Herzog, W</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Relationship between inflammation, the gut microbiota, and metabolic osteoarthritis development: studies in a rat model</atitle><jtitle>Osteoarthritis and cartilage</jtitle><addtitle>Osteoarthritis Cartilage</addtitle><date>2015-11-01</date><risdate>2015</risdate><volume>23</volume><issue>11</issue><spage>1989</spage><epage>1998</epage><pages>1989-1998</pages><issn>1063-4584</issn><eissn>1522-9653</eissn><abstract>Summary Osteoarthritis (OA) may result from intrinsic inflammation related to metabolic disturbance. Obesity-associated inflammation is triggered by lipopolysaccharide (LPS) derived from the gut microbiota. However, the relationship between gut microbiota, LPS, inflammation, and OA remain unclear. Objective To evaluate the associations between gut microbiota, systemic LPS levels, serum and local inflammatory profiles, and joint damage in a high fat/high sucrose diet induced obese rat model. Methods 32 rats were randomized to a high fat/high sucrose diet (diet-induced obese (DIO), 40% fat, 45% sucrose, n = 21) or chow diet group (12% fat, 3.7% sucrose n = 11) for 28 weeks. After a 12-week obesity induction period, DIO animals were stratified into Obesity Prone (DIO-P, top 33% by change in body mass, n = 7), and Obesity Resistant groups (DIO-R, bottom 33%, n = 7). At sacrifice, joints were scored using a Modified Mankin Criteria. Blood and synovial fluid analytes, serum LPS, and fecal gut microbiota were analyzed. Results DIO animals had greater Modified Mankin scores than chow animals ( P = 0.002). There was a significant relationship ( r = 0.604, p = 0.001) between body fat, but not body mass, and Modified Mankin score. Eighteen synovial fluid and four serum analytes were increased in DIO animals. DIO serum LPS levels were increased compared to chow ( P = 0.031). Together, Lactobacillus species (spp.) and Methanobrevibacter spp. abundance had a strong predictive relationship with Modified Mankin Score ( r2 = 0.5, P < 0.001). Conclusions Increased OA in DIO animals is associated with greater body fat, not body mass. The link between gut microbiota and adiposity-derived inflammation and metabolic OA warrants further investigation.</abstract><cop>England</cop><pub>Elsevier Ltd</pub><pmid>26521745</pmid><doi>10.1016/j.joca.2015.03.014</doi><tpages>10</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Adiposity - physiology Animals Disease Models, Animal Disease Progression Gastrointestinal Microbiome Gut microbiota and osteoarthritis Inflammation - complications Inflammation - metabolism Inflammation - pathology Inflammation and osteoarthritis Male Metabolic osteoarthritis Obesity - complications Obesity - metabolism Obesity - pathology Obesity and inflammation Osteoarthritis - etiology Osteoarthritis - metabolism Osteoarthritis - pathology Rat model osteoarthritis Rats Rats, Sprague-Dawley Rheumatology |
title | Relationship between inflammation, the gut microbiota, and metabolic osteoarthritis development: studies in a rat model |
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