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The Contribution of Mathematical Modeling to Understanding Dynamic Aspects of Rumen Metabolism

View Article: PubMed Central - PubMed

ABSTRACT

All mechanistic rumen models cover the main drivers of variation in rumen function, which are feed intake, the differences between feedstuffs and feeds in their intrinsic rumen degradation characteristics, and fractional outflow rate of fluid and particulate matter. Dynamic modeling approaches are best suited to the prediction of more nuanced responses in rumen metabolism, and represent the dynamics of the interactions between substrates and micro-organisms and inter-microbial interactions. The concepts of dynamics are discussed for the case of rumen starch digestion as influenced by starch intake rate and frequency of feed intake, and for the case of fermentation of fiber in the large intestine. Adding representations of new functional classes of micro-organisms (i.e., with new characteristics from the perspective of whole rumen function) in rumen models only delivers new insights if complemented by the dynamics of their interactions with other functional classes. Rumen fermentation conditions have to be represented due to their profound impact on the dynamics of substrate degradation and microbial metabolism. Although the importance of rumen pH is generally acknowledged, more emphasis is needed on predicting its variation as well as variation in the processes that underlie rumen fluid dynamics. The rumen wall has an important role in adapting to rapid changes in the rumen environment, clearing of volatile fatty acids (VFA), and maintaining rumen pH within limits. Dynamics of rumen wall epithelia and their role in VFA absorption needs to be better represented in models that aim to predict rumen responses across nutritional or physiological states. For a detailed prediction of rumen N balance there is merit in a dynamic modeling approach compared to the static approaches adopted in current protein evaluation systems. Improvement is needed on previous attempts to predict rumen VFA profiles, and this should be pursued by introducing factors that relate more to microbial metabolism. For rumen model construction, data on rumen microbiomes are preferably coupled with knowledge consolidated in rumen models instead of relying on correlations with rather general aspects of treatment or animal. This helps to prevent the disregard of basic principles and underlying mechanisms of whole rumen function.

No MeSH data available.


Response in rumen VFA concentration with increment of concentrate allowance after calving (results reproduced from Bannink et al., 2012). (A) Observed development in rumen VFA concentration with two rates of daily increment in concentrate allowance after calving to a maximum of 12 kg concentrate DM/d (in 10 days, solid curve; in 20 days, dashed curve). (B) Predicted development in rumen VFA concentration when increasing concentrate allowance to a maximum of 12 kg DM/d in 5, 7.5, 10, or 20 days after calving. The model describes rumen VFA absorption, growth of epithelial mass and surface area, epithelial VFA metabolism and VFA transport to portal blood in response to rumen VFA production. The model was calibrated using the trial for which results are depicted in (A), including estimated rumen VFA production rate and observations on rumen epithelial tissue development. Bars indicate the moment maximum VFA concentration is achieved during the various strategies of increment of concentrate allowance; the black bar indicates steady-state VFA concentration achieved at 25 days after calving.
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Figure 5: Response in rumen VFA concentration with increment of concentrate allowance after calving (results reproduced from Bannink et al., 2012). (A) Observed development in rumen VFA concentration with two rates of daily increment in concentrate allowance after calving to a maximum of 12 kg concentrate DM/d (in 10 days, solid curve; in 20 days, dashed curve). (B) Predicted development in rumen VFA concentration when increasing concentrate allowance to a maximum of 12 kg DM/d in 5, 7.5, 10, or 20 days after calving. The model describes rumen VFA absorption, growth of epithelial mass and surface area, epithelial VFA metabolism and VFA transport to portal blood in response to rumen VFA production. The model was calibrated using the trial for which results are depicted in (A), including estimated rumen VFA production rate and observations on rumen epithelial tissue development. Bars indicate the moment maximum VFA concentration is achieved during the various strategies of increment of concentrate allowance; the black bar indicates steady-state VFA concentration achieved at 25 days after calving.

Mentions: Maintaining rumen pH between narrow bounds is important for optimal fibrolytic activity. Regulatory mechanisms involve the buffering of rumen contents and removal of VFA (saliva secretion, VFA transport, VFA outflow). To our knowledge none of the published whole rumen models takes account of the changes in these buffering mechanisms with dietary and physiological transitions. In vivo studies with repeated measurements in transition cows reveal that the rumen wall adapts extremely quickly to changes in dietary regime through changes in morphology and histological characteristics (Bannink et al., 2012; Dieho et al., 2016). The faster of the two regimes for incrementing concentrate allowance after calving more than doubled the rate of VFA production as measured using the stable isotope technique, but the rumen wall epithelia appeared to adapt within 2–3 weeks. This adaptive response moderated the effect of the rapid increase in VFA load after calving to only modest changes in rumen VFA concentration and rumen pH (Figure 5A). Based on observed dynamics of rumen papillae size and changes in epithelial tissue, Bannink et al. (2008) proposed a model containing lumen, epithelial tissue and arterial blood compartments and described the rate of increase in rumen epithelial mass and surface area in response to the increased VFA load epithelia are exposed to after calving. Predicted VFA absorption followed observed phenomena (e.g., López et al., 2003) when assuming a far higher VFA transport rate at the serosal side (reflecting extensive epithelia protrusions and higher VFA exchange capacity) compared to the mucosal side of the epithelia. In support of this, Storm et al. (2012) demonstrated a profound effect of epithelial blood flow on rumen VFA absorption rate by modeling observations of rumen VFA absorption and epithelial blood flow. They also concluded that properties of rumen epithelial membranes, epithelial metabolism and epithelial blood flow should be represented in future models of ruminal VFA kinetics. Furthermore, assuming epithelial adaptation as modeled by Bannink et al. (2012), prevention of an accumulation of VFA during the increment of concentrate allowance after calving was predicted for a wide range of strategies (Figure 5B). This result seems to contrast with the risk of development of (subclinical) rumen acidosis during early lactation due to a rumen wall that was not yet fully adapted. It invites further in vivo testing of hypotheses on the implications of rumen adaptive capacity on rumen function.


The Contribution of Mathematical Modeling to Understanding Dynamic Aspects of Rumen Metabolism
Response in rumen VFA concentration with increment of concentrate allowance after calving (results reproduced from Bannink et al., 2012). (A) Observed development in rumen VFA concentration with two rates of daily increment in concentrate allowance after calving to a maximum of 12 kg concentrate DM/d (in 10 days, solid curve; in 20 days, dashed curve). (B) Predicted development in rumen VFA concentration when increasing concentrate allowance to a maximum of 12 kg DM/d in 5, 7.5, 10, or 20 days after calving. The model describes rumen VFA absorption, growth of epithelial mass and surface area, epithelial VFA metabolism and VFA transport to portal blood in response to rumen VFA production. The model was calibrated using the trial for which results are depicted in (A), including estimated rumen VFA production rate and observations on rumen epithelial tissue development. Bars indicate the moment maximum VFA concentration is achieved during the various strategies of increment of concentrate allowance; the black bar indicates steady-state VFA concentration achieved at 25 days after calving.
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Related In: Results  -  Collection

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Figure 5: Response in rumen VFA concentration with increment of concentrate allowance after calving (results reproduced from Bannink et al., 2012). (A) Observed development in rumen VFA concentration with two rates of daily increment in concentrate allowance after calving to a maximum of 12 kg concentrate DM/d (in 10 days, solid curve; in 20 days, dashed curve). (B) Predicted development in rumen VFA concentration when increasing concentrate allowance to a maximum of 12 kg DM/d in 5, 7.5, 10, or 20 days after calving. The model describes rumen VFA absorption, growth of epithelial mass and surface area, epithelial VFA metabolism and VFA transport to portal blood in response to rumen VFA production. The model was calibrated using the trial for which results are depicted in (A), including estimated rumen VFA production rate and observations on rumen epithelial tissue development. Bars indicate the moment maximum VFA concentration is achieved during the various strategies of increment of concentrate allowance; the black bar indicates steady-state VFA concentration achieved at 25 days after calving.
Mentions: Maintaining rumen pH between narrow bounds is important for optimal fibrolytic activity. Regulatory mechanisms involve the buffering of rumen contents and removal of VFA (saliva secretion, VFA transport, VFA outflow). To our knowledge none of the published whole rumen models takes account of the changes in these buffering mechanisms with dietary and physiological transitions. In vivo studies with repeated measurements in transition cows reveal that the rumen wall adapts extremely quickly to changes in dietary regime through changes in morphology and histological characteristics (Bannink et al., 2012; Dieho et al., 2016). The faster of the two regimes for incrementing concentrate allowance after calving more than doubled the rate of VFA production as measured using the stable isotope technique, but the rumen wall epithelia appeared to adapt within 2–3 weeks. This adaptive response moderated the effect of the rapid increase in VFA load after calving to only modest changes in rumen VFA concentration and rumen pH (Figure 5A). Based on observed dynamics of rumen papillae size and changes in epithelial tissue, Bannink et al. (2008) proposed a model containing lumen, epithelial tissue and arterial blood compartments and described the rate of increase in rumen epithelial mass and surface area in response to the increased VFA load epithelia are exposed to after calving. Predicted VFA absorption followed observed phenomena (e.g., López et al., 2003) when assuming a far higher VFA transport rate at the serosal side (reflecting extensive epithelia protrusions and higher VFA exchange capacity) compared to the mucosal side of the epithelia. In support of this, Storm et al. (2012) demonstrated a profound effect of epithelial blood flow on rumen VFA absorption rate by modeling observations of rumen VFA absorption and epithelial blood flow. They also concluded that properties of rumen epithelial membranes, epithelial metabolism and epithelial blood flow should be represented in future models of ruminal VFA kinetics. Furthermore, assuming epithelial adaptation as modeled by Bannink et al. (2012), prevention of an accumulation of VFA during the increment of concentrate allowance after calving was predicted for a wide range of strategies (Figure 5B). This result seems to contrast with the risk of development of (subclinical) rumen acidosis during early lactation due to a rumen wall that was not yet fully adapted. It invites further in vivo testing of hypotheses on the implications of rumen adaptive capacity on rumen function.

View Article: PubMed Central - PubMed

ABSTRACT

All mechanistic rumen models cover the main drivers of variation in rumen function, which are feed intake, the differences between feedstuffs and feeds in their intrinsic rumen degradation characteristics, and fractional outflow rate of fluid and particulate matter. Dynamic modeling approaches are best suited to the prediction of more nuanced responses in rumen metabolism, and represent the dynamics of the interactions between substrates and micro-organisms and inter-microbial interactions. The concepts of dynamics are discussed for the case of rumen starch digestion as influenced by starch intake rate and frequency of feed intake, and for the case of fermentation of fiber in the large intestine. Adding representations of new functional classes of micro-organisms (i.e., with new characteristics from the perspective of whole rumen function) in rumen models only delivers new insights if complemented by the dynamics of their interactions with other functional classes. Rumen fermentation conditions have to be represented due to their profound impact on the dynamics of substrate degradation and microbial metabolism. Although the importance of rumen pH is generally acknowledged, more emphasis is needed on predicting its variation as well as variation in the processes that underlie rumen fluid dynamics. The rumen wall has an important role in adapting to rapid changes in the rumen environment, clearing of volatile fatty acids (VFA), and maintaining rumen pH within limits. Dynamics of rumen wall epithelia and their role in VFA absorption needs to be better represented in models that aim to predict rumen responses across nutritional or physiological states. For a detailed prediction of rumen N balance there is merit in a dynamic modeling approach compared to the static approaches adopted in current protein evaluation systems. Improvement is needed on previous attempts to predict rumen VFA profiles, and this should be pursued by introducing factors that relate more to microbial metabolism. For rumen model construction, data on rumen microbiomes are preferably coupled with knowledge consolidated in rumen models instead of relying on correlations with rather general aspects of treatment or animal. This helps to prevent the disregard of basic principles and underlying mechanisms of whole rumen function.

No MeSH data available.