A model of ruminal volatile fatty acid absorption kinetics and rumen epithelial blood flow in lactating Holstein cows

Ruminal absorption of volatile fatty acids (VFA) is quantitatively the most important nutrient flux in cattle. Historically, VFA absorption models have been derived primarily from ruminal variables such as chemical composition of the fluid, volume, and pH. Recently, a mechanistic model incorporated...

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Veröffentlicht in:Journal of dairy science 2012-06, Vol.95 (6), p.2919-2934
Hauptverfasser: Storm, A.C., Kristensen, N.B., Hanigan, M.D.
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description Ruminal absorption of volatile fatty acids (VFA) is quantitatively the most important nutrient flux in cattle. Historically, VFA absorption models have been derived primarily from ruminal variables such as chemical composition of the fluid, volume, and pH. Recently, a mechanistic model incorporated the control of VFA absorption from epithelial surface area of the reticulorumen. In the present study, we hypothesized that ruminal absorption of VFA was controlled through epithelial permeability to VFA and rumen epithelial capillary blood flow. The objective of the study was to construct a model of VFA exchange across the rumen wall that incorporates epithelial blood flow as a driving force for ruminal VFA removal. The bidirectional fluxes between the ruminal and epithelial pool of VFA were assumed mass action driven, given that passive diffusion of nonionized VFA is the dominant transmembrane VFA flux. Parameter estimates were derived by fitting the model to observed data. The model provided reliable unbiased estimates of ruminal VFA absorption and rumen epithelial blood flow. Blood flow was modeled using an equation that considered the effect of butyrate and dietary crude protein intake per kilogram of body weight. The rate constants related to the flux from ruminal fluid to epithelium were in the order isobutyrate < acetate < propionate < butyrate (0.32±0.02, 0.72±0.2, 0.91±0.06, and 0.97±0.02 /h, respectively). The rate constants for fluxes of isobutyrate, acetate, propionate, and butyrate from the rumen epithelium to the ruminal fluid, relative to the pool size of the epithelium, were 4.78, 10.6, 13.4, and 14.3 /h, respectively. Ruminal concentrations of acetate, propionate, butyrate, and isobutyrate were predicted with root mean square prediction errors as percentage of the observed means (RMSPE) of 5.86, 5.75, 11.3, and 4.12, respectively. The epithelial blood flow was predicted with 26.3% RMSPE. Sensitivity analyses indicated that when ruminal butyrate concentration increased from 4.0 to 37.4mmol/L, blood flow of the epithelium increased 47% and the ruminal disappearance rate of propionate increased 11%. The concentration gradient of propionate between ruminal fluid and epithelium was no more than 3:1 and increased with increasing blood flow. In conclusion, a dynamic model based on rumen epithelial blood flow and bidirectional fluxes of VFA between ruminal fluid and epithelium gave unbiased predictions with low residual error of ruminal VFA absorption
doi_str_mv 10.3168/jds.2011-4239
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Historically, VFA absorption models have been derived primarily from ruminal variables such as chemical composition of the fluid, volume, and pH. Recently, a mechanistic model incorporated the control of VFA absorption from epithelial surface area of the reticulorumen. In the present study, we hypothesized that ruminal absorption of VFA was controlled through epithelial permeability to VFA and rumen epithelial capillary blood flow. The objective of the study was to construct a model of VFA exchange across the rumen wall that incorporates epithelial blood flow as a driving force for ruminal VFA removal. The bidirectional fluxes between the ruminal and epithelial pool of VFA were assumed mass action driven, given that passive diffusion of nonionized VFA is the dominant transmembrane VFA flux. Parameter estimates were derived by fitting the model to observed data. The model provided reliable unbiased estimates of ruminal VFA absorption and rumen epithelial blood flow. Blood flow was modeled using an equation that considered the effect of butyrate and dietary crude protein intake per kilogram of body weight. The rate constants related to the flux from ruminal fluid to epithelium were in the order isobutyrate &lt; acetate &lt; propionate &lt; butyrate (0.32±0.02, 0.72±0.2, 0.91±0.06, and 0.97±0.02 /h, respectively). The rate constants for fluxes of isobutyrate, acetate, propionate, and butyrate from the rumen epithelium to the ruminal fluid, relative to the pool size of the epithelium, were 4.78, 10.6, 13.4, and 14.3 /h, respectively. Ruminal concentrations of acetate, propionate, butyrate, and isobutyrate were predicted with root mean square prediction errors as percentage of the observed means (RMSPE) of 5.86, 5.75, 11.3, and 4.12, respectively. The epithelial blood flow was predicted with 26.3% RMSPE. Sensitivity analyses indicated that when ruminal butyrate concentration increased from 4.0 to 37.4mmol/L, blood flow of the epithelium increased 47% and the ruminal disappearance rate of propionate increased 11%. The concentration gradient of propionate between ruminal fluid and epithelium was no more than 3:1 and increased with increasing blood flow. In conclusion, a dynamic model based on rumen epithelial blood flow and bidirectional fluxes of VFA between ruminal fluid and epithelium gave unbiased predictions with low residual error of ruminal VFA absorption under washed rumen conditions. The model indicates that the effect of varying epithelial blood flow on the control of ruminal VFA absorption is related to the concentration gradient of individual VFA between ruminal fluid and epithelial blood. Epithelial blood flow may be an important determinant of ruminal absorption of VFA, a result that has not been evaluated on independent data.</description><identifier>ISSN: 0022-0302</identifier><identifier>EISSN: 1525-3198</identifier><identifier>DOI: 10.3168/jds.2011-4239</identifier><identifier>PMID: 22612930</identifier><identifier>CODEN: JDSCAE</identifier><language>eng</language><publisher>New York, NY: Elsevier Inc</publisher><subject>Absorption ; acetates ; Acetates - analysis ; Animal productions ; Animals ; Apraxia, Ideomotor ; Biological and medical sciences ; blood ; blood flow ; body weight ; butyrates ; Butyrates - analysis ; Cattle ; cows ; crude protein ; dairy cow ; Epithelium - metabolism ; Epithelium - physiology ; epithelium blood flow ; equations ; Fatty Acids, Volatile - metabolism ; Female ; Food industries ; Fundamental and applied biological sciences. Psychology ; Holstein ; Isobutyrates - analysis ; lactation ; Lactation - physiology ; Milk and cheese industries. Ice creams ; Models, Biological ; permeability ; prediction ; Propionates - analysis ; propionic acid ; protein intake ; Rumen - blood supply ; Rumen - metabolism ; Rumen - physiology ; rumen epithelium ; ruminal volatile fatty acid kinetics ; surface area ; Terrestrial animal productions ; Vertebrates ; volatile fatty acid model ; volatile fatty acids</subject><ispartof>Journal of dairy science, 2012-06, Vol.95 (6), p.2919-2934</ispartof><rights>2012 American Dairy Science Association</rights><rights>2015 INIST-CNRS</rights><rights>Copyright © 2012 American Dairy Science Association. Published by Elsevier Inc. 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Historically, VFA absorption models have been derived primarily from ruminal variables such as chemical composition of the fluid, volume, and pH. Recently, a mechanistic model incorporated the control of VFA absorption from epithelial surface area of the reticulorumen. In the present study, we hypothesized that ruminal absorption of VFA was controlled through epithelial permeability to VFA and rumen epithelial capillary blood flow. The objective of the study was to construct a model of VFA exchange across the rumen wall that incorporates epithelial blood flow as a driving force for ruminal VFA removal. The bidirectional fluxes between the ruminal and epithelial pool of VFA were assumed mass action driven, given that passive diffusion of nonionized VFA is the dominant transmembrane VFA flux. Parameter estimates were derived by fitting the model to observed data. The model provided reliable unbiased estimates of ruminal VFA absorption and rumen epithelial blood flow. Blood flow was modeled using an equation that considered the effect of butyrate and dietary crude protein intake per kilogram of body weight. The rate constants related to the flux from ruminal fluid to epithelium were in the order isobutyrate &lt; acetate &lt; propionate &lt; butyrate (0.32±0.02, 0.72±0.2, 0.91±0.06, and 0.97±0.02 /h, respectively). The rate constants for fluxes of isobutyrate, acetate, propionate, and butyrate from the rumen epithelium to the ruminal fluid, relative to the pool size of the epithelium, were 4.78, 10.6, 13.4, and 14.3 /h, respectively. Ruminal concentrations of acetate, propionate, butyrate, and isobutyrate were predicted with root mean square prediction errors as percentage of the observed means (RMSPE) of 5.86, 5.75, 11.3, and 4.12, respectively. The epithelial blood flow was predicted with 26.3% RMSPE. Sensitivity analyses indicated that when ruminal butyrate concentration increased from 4.0 to 37.4mmol/L, blood flow of the epithelium increased 47% and the ruminal disappearance rate of propionate increased 11%. The concentration gradient of propionate between ruminal fluid and epithelium was no more than 3:1 and increased with increasing blood flow. In conclusion, a dynamic model based on rumen epithelial blood flow and bidirectional fluxes of VFA between ruminal fluid and epithelium gave unbiased predictions with low residual error of ruminal VFA absorption under washed rumen conditions. The model indicates that the effect of varying epithelial blood flow on the control of ruminal VFA absorption is related to the concentration gradient of individual VFA between ruminal fluid and epithelial blood. Epithelial blood flow may be an important determinant of ruminal absorption of VFA, a result that has not been evaluated on independent data.</description><subject>Absorption</subject><subject>acetates</subject><subject>Acetates - analysis</subject><subject>Animal productions</subject><subject>Animals</subject><subject>Apraxia, Ideomotor</subject><subject>Biological and medical sciences</subject><subject>blood</subject><subject>blood flow</subject><subject>body weight</subject><subject>butyrates</subject><subject>Butyrates - analysis</subject><subject>Cattle</subject><subject>cows</subject><subject>crude protein</subject><subject>dairy cow</subject><subject>Epithelium - metabolism</subject><subject>Epithelium - physiology</subject><subject>epithelium blood flow</subject><subject>equations</subject><subject>Fatty Acids, Volatile - metabolism</subject><subject>Female</subject><subject>Food industries</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Holstein</subject><subject>Isobutyrates - analysis</subject><subject>lactation</subject><subject>Lactation - physiology</subject><subject>Milk and cheese industries. Ice creams</subject><subject>Models, Biological</subject><subject>permeability</subject><subject>prediction</subject><subject>Propionates - analysis</subject><subject>propionic acid</subject><subject>protein intake</subject><subject>Rumen - blood supply</subject><subject>Rumen - metabolism</subject><subject>Rumen - physiology</subject><subject>rumen epithelium</subject><subject>ruminal volatile fatty acid kinetics</subject><subject>surface area</subject><subject>Terrestrial animal productions</subject><subject>Vertebrates</subject><subject>volatile fatty acid model</subject><subject>volatile fatty acids</subject><issn>0022-0302</issn><issn>1525-3198</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2012</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp10c9vFCEUB3BiNHZbPXpVLia9TH38mtk5No1akyYetGfCwJtKZWEFpk3_e5nsqidPhJfPe8AXQt4wuBCs3364d-WCA2Od5GJ8RjZMcdUJNm6fkw0A5x0I4CfktJT7tmUc1EtywnnP-ChgQ5ZLuksOA00zzcvORxPoQwqm-oB0NrU-UWO9o2YqKe-rT5H-9BGrt4Wa6NYejBT3vv7A4FvzFFJydA7pkfpIg7G1zYp39DqFUrGVbHosr8iL2YSCr4_rGbn99PH71XV38_Xzl6vLm85KIWtn0GzNpMCNrEdwZgArnMRJcezHYYBZwFoDIziDQSop3bjt7dD34wzjqMQZOT_M3ef0a8FS9c4XiyGYiGkpmgFTshcSWKPdgdqcSsk46332O5OfGtJr0rolrdek9Zp082-Po5dph-6v_hNtA--PwBRrwpxNtL78c2oEBlI09-7gZpO0ucvN3H5r5yho_zW09zQxHAS2qB48Zl2sx2jR-Yy2apf8fy75G8sMor0</recordid><startdate>20120601</startdate><enddate>20120601</enddate><creator>Storm, A.C.</creator><creator>Kristensen, N.B.</creator><creator>Hanigan, M.D.</creator><general>Elsevier Inc</general><general>Elsevier</general><scope>FBQ</scope><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>7X8</scope></search><sort><creationdate>20120601</creationdate><title>A model of ruminal volatile fatty acid absorption kinetics and rumen epithelial blood flow in lactating Holstein cows</title><author>Storm, A.C. ; Kristensen, N.B. ; Hanigan, M.D.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c434t-aea8ab50d916e0da70c3d4eb52e69770f30a70c0a321074544d986c7669f09953</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2012</creationdate><topic>Absorption</topic><topic>acetates</topic><topic>Acetates - analysis</topic><topic>Animal productions</topic><topic>Animals</topic><topic>Apraxia, Ideomotor</topic><topic>Biological and medical sciences</topic><topic>blood</topic><topic>blood flow</topic><topic>body weight</topic><topic>butyrates</topic><topic>Butyrates - analysis</topic><topic>Cattle</topic><topic>cows</topic><topic>crude protein</topic><topic>dairy cow</topic><topic>Epithelium - metabolism</topic><topic>Epithelium - physiology</topic><topic>epithelium blood flow</topic><topic>equations</topic><topic>Fatty Acids, Volatile - metabolism</topic><topic>Female</topic><topic>Food industries</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Holstein</topic><topic>Isobutyrates - analysis</topic><topic>lactation</topic><topic>Lactation - physiology</topic><topic>Milk and cheese industries. Ice creams</topic><topic>Models, Biological</topic><topic>permeability</topic><topic>prediction</topic><topic>Propionates - analysis</topic><topic>propionic acid</topic><topic>protein intake</topic><topic>Rumen - blood supply</topic><topic>Rumen - metabolism</topic><topic>Rumen - physiology</topic><topic>rumen epithelium</topic><topic>ruminal volatile fatty acid kinetics</topic><topic>surface area</topic><topic>Terrestrial animal productions</topic><topic>Vertebrates</topic><topic>volatile fatty acid model</topic><topic>volatile fatty acids</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Storm, A.C.</creatorcontrib><creatorcontrib>Kristensen, N.B.</creatorcontrib><creatorcontrib>Hanigan, M.D.</creatorcontrib><collection>AGRIS</collection><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>MEDLINE - Academic</collection><jtitle>Journal of dairy science</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Storm, A.C.</au><au>Kristensen, N.B.</au><au>Hanigan, M.D.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A model of ruminal volatile fatty acid absorption kinetics and rumen epithelial blood flow in lactating Holstein cows</atitle><jtitle>Journal of dairy science</jtitle><addtitle>J Dairy Sci</addtitle><date>2012-06-01</date><risdate>2012</risdate><volume>95</volume><issue>6</issue><spage>2919</spage><epage>2934</epage><pages>2919-2934</pages><issn>0022-0302</issn><eissn>1525-3198</eissn><coden>JDSCAE</coden><abstract>Ruminal absorption of volatile fatty acids (VFA) is quantitatively the most important nutrient flux in cattle. Historically, VFA absorption models have been derived primarily from ruminal variables such as chemical composition of the fluid, volume, and pH. Recently, a mechanistic model incorporated the control of VFA absorption from epithelial surface area of the reticulorumen. In the present study, we hypothesized that ruminal absorption of VFA was controlled through epithelial permeability to VFA and rumen epithelial capillary blood flow. The objective of the study was to construct a model of VFA exchange across the rumen wall that incorporates epithelial blood flow as a driving force for ruminal VFA removal. The bidirectional fluxes between the ruminal and epithelial pool of VFA were assumed mass action driven, given that passive diffusion of nonionized VFA is the dominant transmembrane VFA flux. Parameter estimates were derived by fitting the model to observed data. The model provided reliable unbiased estimates of ruminal VFA absorption and rumen epithelial blood flow. Blood flow was modeled using an equation that considered the effect of butyrate and dietary crude protein intake per kilogram of body weight. The rate constants related to the flux from ruminal fluid to epithelium were in the order isobutyrate &lt; acetate &lt; propionate &lt; butyrate (0.32±0.02, 0.72±0.2, 0.91±0.06, and 0.97±0.02 /h, respectively). The rate constants for fluxes of isobutyrate, acetate, propionate, and butyrate from the rumen epithelium to the ruminal fluid, relative to the pool size of the epithelium, were 4.78, 10.6, 13.4, and 14.3 /h, respectively. Ruminal concentrations of acetate, propionate, butyrate, and isobutyrate were predicted with root mean square prediction errors as percentage of the observed means (RMSPE) of 5.86, 5.75, 11.3, and 4.12, respectively. The epithelial blood flow was predicted with 26.3% RMSPE. Sensitivity analyses indicated that when ruminal butyrate concentration increased from 4.0 to 37.4mmol/L, blood flow of the epithelium increased 47% and the ruminal disappearance rate of propionate increased 11%. The concentration gradient of propionate between ruminal fluid and epithelium was no more than 3:1 and increased with increasing blood flow. In conclusion, a dynamic model based on rumen epithelial blood flow and bidirectional fluxes of VFA between ruminal fluid and epithelium gave unbiased predictions with low residual error of ruminal VFA absorption under washed rumen conditions. The model indicates that the effect of varying epithelial blood flow on the control of ruminal VFA absorption is related to the concentration gradient of individual VFA between ruminal fluid and epithelial blood. Epithelial blood flow may be an important determinant of ruminal absorption of VFA, a result that has not been evaluated on independent data.</abstract><cop>New York, NY</cop><pub>Elsevier Inc</pub><pmid>22612930</pmid><doi>10.3168/jds.2011-4239</doi><tpages>16</tpages><oa>free_for_read</oa></addata></record>
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subjects Absorption
acetates
Acetates - analysis
Animal productions
Animals
Apraxia, Ideomotor
Biological and medical sciences
blood
blood flow
body weight
butyrates
Butyrates - analysis
Cattle
cows
crude protein
dairy cow
Epithelium - metabolism
Epithelium - physiology
epithelium blood flow
equations
Fatty Acids, Volatile - metabolism
Female
Food industries
Fundamental and applied biological sciences. Psychology
Holstein
Isobutyrates - analysis
lactation
Lactation - physiology
Milk and cheese industries. Ice creams
Models, Biological
permeability
prediction
Propionates - analysis
propionic acid
protein intake
Rumen - blood supply
Rumen - metabolism
Rumen - physiology
rumen epithelium
ruminal volatile fatty acid kinetics
surface area
Terrestrial animal productions
Vertebrates
volatile fatty acid model
volatile fatty acids
title A model of ruminal volatile fatty acid absorption kinetics and rumen epithelial blood flow in lactating Holstein cows
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