Animal (2010), 4:7, pp 10571074 & The Animal Consortium 2010

doi:10.1017/S1751731110000844
animal

Carbohydrate quantitative digestion and absorption

in ruminants: from feed starch and fibre to nutrients
available for tissues
P. Nozie`re1-, I. Ortigues-Marty1, C. Loncke1 and D. Sauvant2
1
INRA, UR1213 Herbivores, F-63122 Saint-Gene`s-Champanelle, France; 2INRA-AgroParisTech, UMR791 Modelisation systemique appliquee aux Ruminants,
16 rue Claude Bernard, F-75231 Paris, France

(Received 29 September 2009; Accepted 23 March 2010; First published online 17 May 2010)

Carbohydrates are the main source of energy in ruminants. Their site, extent and kinetics of digestion highly impact the amount
and profile of nutrients delivered to peripheral tissues, and the responses of the animal, i.e. ingestion, efficiency of production,
N and methane excretion, quality of products and welfare. Development of multi-objective feed evaluation systems thus requires
a more integrated quantitative knowledge on carbohydrate digestion and yield of terminal products, as well as on their
metabolism by splanchnic tissues. The objective of this paper is to review (i) quantitative knowledge on fibre, starch and sugar
digestion, volatile fatty acids (VFA) and glucose production and splanchnic metabolism and (ii) modelling approaches which aim
at representing and/or predicting nutrient fluxes in the digestive tract, portal and hepatic drainage. It shows that the representation
of carbohydrate digestion and VFA yield is relatively homogeneous among models. Although published quantitative comparisons
of these models are scarce, they stress that prediction of fibre digestion and VFA yield and composition is still not good enough
for use in feed formulation, whereas prediction of microbial N yield and ruminal starch digestion seems to be more satisfactory.
Uncertainties on VFA stoichiometric coefficients and absorption rates may partly explain the poor predictions of VFA. Hardly any
mechanistic models have been developed on portal-drained viscera (PDV) metabolism whereas a few exist for liver metabolism.
A qualitative comparison of these models is presented. Most are focused on dairy cows and their level of aggregation in the
representation of nutrient fluxes and metabolism highly differs depending on their objectives. Quantitative comparison of these
models is still lacking. However, recent advances have been achieved with the empirical prediction of VFA and glucose production
and fluxes through PDV and liver based on the current INRA feed evaluation system. These advances are presented. They illustrate
that empirical prediction of ruminal VFA and intestinal glucose production can be evaluated by comparison with measured net
portal net fluxes. We also illustrate the potential synergy between empirical and mechanistic modelling. It is concluded that
concomitant empirical and mechanistic approach may likely help to progress towards development of multi-objective feed
evaluation systems based on nutrient fluxes.

Keywords: ruminant, carbohydrate, volatile fatty acids, glucose, meta-analysis

Implications tissues, as well as modelling approaches which aim at repre-

Evolution of feed evaluation systems towards tools allowing
prediction of multiple animal responses (efficiency, excretion,
quality of products, welfare, etc.) requires quantitative inte-
gration of knowledge on site and extent of digestion, which
highly impact the amount and profile of nutrients delivered
to peripheral tissues. We present quantitative knowledge on
fibre, starch and sugar digestion, volatile fatty acid and glu-
cose production, absorption and metabolism by splanchnic
-
E-mail: noziere@clermont.inra.fr
senting and/or predicting nutrient fluxes in digestive tract,
portal and hepatic drainage.
Introduction
Current feed evaluation systems for ruminants have
been partly developed to adjust nutrient supply to animals
requirements. Given the multiplicity of new objectives
weighing on ruminant production systems (efficiency of
production, N and C excretion, quality of products and
welfare), the evolution of feed evaluation systems needs to

1057
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 Nozie`re, Ortigues-Marty, Loncke and Sauvant
contribute to a better prediction of multiple animal respon-
ses to diets. It is now well documented that most of targeted
animal responses to diet are closely related to site, extent
and kinetics of digestion of energy supplied by dietary
carbohydrates that highly impact the amount and profile of
nutrients delivered to peripheral tissues. Whereas energy is
currently still considered as an aggregated unit, develop-
ment of multi-objective feed evaluation systems requires
the integration of quantitative knowledge on carbohydrate
digestion and yield of terminal products, as well as on their
metabolism by splanchnic tissues. It is a challenge because
of the diversity in diet composition and intake levels existing
in ruminant production systems. The objectives of this paper
are to review (i) quantitative knowledge on fibre, starch
and sugar digestion, volatile fatty acid (VFA) and glucose
production and splanchnic metabolism and (ii) modelling
approaches which aim at representing and/or predicting
nutrient fluxes in the digestive tract, portal and hepatic
drainage. Several results presented in this paper originate
from meta-analyses of literature data, using databases
developed at INRA gathering published results in vivo on
digestion (BoviDig; Sauvant et al., 2000), VFA ruminal pro-
duction (VFA-Prod; Nozie`re et al., 2007), and blood nutrient
fluxes across splanchnic tissues (Flora; Vernet and Ortigues-
Marty, 2006). Most of the meta-analyses presented in this
paper have already been published; others are presented as
unpublished synthesis of literature data.
Cell walls, starch and soluble carbohydrates: extent
and rate of ruminal digestion
Several types of carbohydrates are found in feedstuffs: cell
wall (CW) insoluble or soluble carbohydrates, starch and
water-soluble carbohydrates (WSC). The CW insoluble carbo-
hydrates are classically characterized as the fraction inso-
luble in a neutral detergent solution, called NDF. It consists
of cellulose, hemicelluloses and lignin, a small amount of
N-containing material and residual starch for cereals if no
amylase treatment is previously applied. The NDF does not
include CW soluble material such as pectins. Next to NDF,
starch and soluble sugars, a significant fraction of carbohy-
drates (generally more than 10%) remains unaccounted for
in standard feed analysis. It likely consists of xylans, glucans
and organic acids.
CW insoluble carbohydrates
NDF ranges from 40% to 80% of dry matter (DM) in forages,
depending on the botanical family, vegetation stage and
preservation. In concentrate and by-products, NDF ranges
from traces (i.e. corn gluten meal) to more than 80% of DM
(i.e. buckwheat hulls, corn cobs, extracted grape pips meal,
etc.). Depending on diet composition, NDF content accounts
for 30% to 80% of DM intake. For forages, NDF digestibility
in the total tract ranges from 40% to 85%. Undigestible NDF
highly depends on organic matter (OM) digestibility for
grass, legumes and straws (INRA, 2007). For concentrates,
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digestibility of NDF can be indirectly evaluated from digest-
ibility of OM, starch, CP and fatty acids (Sauvant et al.,
2008), and ranges from 20% to 90%. Given their NDF con-
tent and digestibility, only few forages (e.g. fresh brome
grass), and concentrates (e.g. soya bean hulls, palm kernel
meal), contain nearly 50% of digestible NDF (dNDF) in DM.
Ruminal digestion of NDF apparently starts after a lag
phase. In sacco, this lag phase is positively related to the NDF
content and can reach 10 h (Sauvant and Van Milgen, 1995).
Time required for comminution and microbial colonization
contributes to this lag phase. Physical breakdown of particles is
the outcome of mastication during ingestion and rumination,
which in turn facilitates hydration, microbial colonization,
release of enzymes and hydrolysis. Mastication time ranges
from 400 to 1000 min/day, corresponding to a chewing index
of approximately 20 to 100 min/kg DM intake in dairy cows
(Sauvant et al., 1990). This index is closely related to dietary
CW content (Dulphy et al., 1993) and granulometry (Sauvant,
2000). An extensive study by Yang (1991) demonstrated that
microbial colonization starts very early, with rates varying from
10% to 40%/h in sacco, and is proportional to NDF content
(approximately 50 mg microbial DM/g NDF after 3 h) due to the
fact that CW provides a wide surface area for microbial
attachment. Maximal colonization also depends on particle
size, varying between 10% to 15% (particles .0.1 mm) and
40% to 60% (particles ,0.1 mm). Following digestion, it
decreases towards an asymptote where microbial mass is
mainly associated with the indigestible fraction. Thus, an
important microbial population remains present in the rumen
and contributes to rumen stability.
Compared with other carbohydrates, the ruminal digestion
rate of dNDF, which depends on the extent and nature
of lignification, is low (2% to 8%/h). Therefore, the extent of
rumen digestion of NDF is highly dependant on the residence
time of particles in the rumen, and thus on the lag phase
of recently consumed large particles and on the fractional
turnover rate of small particles (2% to 8%/h). Fractional
turnover rate of particles depends on particle size and density
(Lechner-Doll et al., 1991), as well as on intake level (with an
average increase of 0.74%/h for 1 g DM intake/100 kg BW;
Sauvant, 2003). The ruminal degradation of NDF is depressed
with concentrate supplementation. This is clearly related to a
decrease in activity of fibrolytic enzymes of the microorgan-
isms adhering to plant particles (Nozie`re et al., 1996), rather
than to changes in the structure of the cellulolytic bacterial
community (Martin et al., 2001). Modifications in cellulolytic
activity may be partly explained by the shift in ruminal pH.
In sacco, this is mainly reflected by a decrease in fractional
degradation rate, but also by an increase in the undegradable
fraction (Van Milgen et al., 1992).
Since ruminants do not secrete endogenous fibrolytic
enzymes, NDF escaping ruminal digestion is not digested in
the small intestine. It is only partly (and slowly) degraded
in the hindgut, since the cellulolytic activity in the caecum
is much lower than in the rumen (Michalet-Doreau et al.,
2002), and the residence time of particles in the hindgut
is lower than in the forestomachs (Huhtanen et al., 2004).

Consequently, the hindgut accounts on average for only 10%
of total tract NDF digestion. Factors influencing ruminal
degradation (and consequently total tract digestibility) of
NDF are not only the intrinsic characteristics of feedstuffs,
particularly their lignification, but also factors related to diet
composition and intake level, that is, the amount and activity
of fibrolytic microorganisms, and the passage rate of particles
through the rumen.
Starch
Starch can account for a substantial proportion of DM in
ruminant diets, and can exceed 50% of DM intake in inten-
sive diets based on ensiled cereals and/or grains. The starch
content of grains varies among cereals from 40% DM (oat)
to 87% DM (rice), depending as well on varieties, location,
year, climatic conditions and agronomic practices. The starch
content of corn silages (17% to 41%) depends mainly on
plant maturity, that is, the proportion of grain in the plant
(32% to 54%), with an average increment of 0.7 g starch/g
grain. Since ruminant saliva contains no amylase, starch
degradation is primarily the result of bacterial enzymes,
following attachment and colonization of grain particles by
amylolytic bacteria. Protozoa play a key role on delaying
starch degradation since they can transitorily store starch
granules (Jouany and Thivend, 1972).
The proportion of starch digested in the rumen varies
between 25% and nearly 100% of starch intake, and can
reach up to 10 g/day per kg BW (Swingle et al., 1999).
Compared with NDF, starch is rapidly degraded in the rumen.
An extensive quantitative review of data on starch content
and in sacco degradation kinetics of grains (Offner et al.,
2003) has been largely included in the values tabulated
by INRA-AFZ (2004). It showed that ruminal starch degrad-
ability varies widely among starch sources, from 60% on
average for corn and sorghum to 95% for wheat, triticale or
rye, depending on both the extent of the soluble fraction
(20% to 80%) and the fractional degradation rate of the
insoluble starch (5% to 60%/h). Grain processing also
affects starch ruminal degradation. For example, toasting
reduces starch degradability for oat and barley (231 and
217 g/100 g, respectively), whereas steam-flaking increases
starch degradability for corn and sorghum (126 g/100 g
after 1 h). Decreasing mean particle size while improving
accessibility of digestible starch to microbial enzymes
increases in sacco starch degradability, by an average of
16 g degradable starch/100 g in corn when mean particle
size decreases by 1 mm (Offner et al., 2003). Genotype also
highly affects starch degradation, with in sacco starch
degradability ranking from 40% to 80% for corn depending
on its vitreousness (Philippeau et al., 2000), which affects
microbial colonization of grain (McAllister et al., 1990). The
in sacco degradability of starch in maize silages is less
documented due to methodological difficulties. It apparently
ranges from 75% to 95%, and decreases an average of 7%
when DM of whole plant increases of 10%. However,
grinding silages before in sacco incubation induces large
losses of starch particles through bag pores. When grains are
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Carbohydrate digestion and nutrient fluxes
sampled just before harvesting, particle losses are drastically
reduced, allowing adequate determination of in sacco
degradation, with starch degradability ranging from 40% to
90% depending on genotype and maturity, both reflected by
vitreousness. The depressing effect of vitreousness on starch
degradability is similar for both mature and immature corn
grains, averaging 28% when vitreousness increases 10%
(Philippeau et al., 2000). Together with intrinsic character-
istics of feedstuffs, intake level also negatively affects rum-
inal starch digestibility (RSD) by increasing passage rate of
particles through the rumen. This effect is less important for
starch (and particularly for highly degradable starch) than for
NDF, due to the higher ratio of degradation rate/passage
rate. The amylolytic activity of bacteria increases with starch
availability (Nozie`re and Michalet-Doreau, 1997) and may
not be a limiting factor for ruminal starch digestion in most
situations.
Water-soluble carbohydrates
WSC, including lactate in silages, normally accounts for less
than 15% of DM, but could reach more than 20% at stem
elongation or ear emergence in ryegrass. The disappearance
rate of WSC from the ruminal fluid is very high (.400%/h;
Weisbjerg et al., 1998), and it is generally admitted that WSC
are fermented in the rumen instantaneously after being
released from the plant cells. However, based on the tran-
sitory post-prandial accumulation of WSC in the rumen with
diets rich in WSC, the capacity of microbes to take up and
metabolize WSC is probably limited by thermodynamic laws
of metabolic pathways. Moreover, the uptake of carbon
chains by microbial cells could be much more rapid than their
fermentation, with a maximal level of carbohydrate accu-
mulation in microbial cells about 1 h after the meal, and a
subsequent decrease at 5% to 20%/h (Sauvant and Van
Milgen, 1995). This short-term adaptation delays the dis-
posal of energy by microbes. Consequently, whereas frac-
tional degradation rates of 150% to 300%/h are assumed for
WSC in some rumen models (Russell et al., 1992; Petruzzi
et al., 2002), a much lower fractional degradation is more
likely, but experimental evidence is lacking. Satisfactory
adjustments are obtained assuming a fractional rate of
around 40%/h (D. Sauvant, unpublished). Assuming a frac-
tional passage rate of liquid lower than 15%/h, a low pro-
portion of ingested WSC may escape ruminal degradation,
and is highly digested in the small and large intestines.
Representation of carbohydrate digestion in rumen models
In most detailed rumen models, a minimum of four fractions
of dietary carbohydrates are generally represented, including
soluble carbohydrates, degradable starch, degradable and
undegradable CW. Those fractions are generally based on
their chemical composition (ADL for undegradable CW), or
by in sacco or in vitro data (to separate soluble and unde-
gradable fractions). In the Cornell model (CNCPS), the
number of carbohydrate pools has been recently expanded
by considering separately VFA and lactic acid from silages,
other organic acids, sugars and soluble fibre (Lanzas et al., 2007).
1059
 Nozie`re, Ortigues-Marty, Loncke and Sauvant
Processes occurring during lag time are generally not expli-
citly represented, or are included without any transition
from the lag phase to the digestion process. Whereas it is
generally assumed that the lag compartments are subjected
neither to passage from the rumen nor to microbial degra-
dation (Baldwin et al., 1987b; Chilibroste et al., 2008), a
lower lag time before digestion than before transit, has been
proposed (Sauvant et al., 1996). Such inclusion of lag time
is of undeniable interest for dynamic representation of pro-
cesses, but their interest to improve predictions of the
average daily flows at duodenum remains questionable
(Bannink et al., 1997). Regulation of CW degradation rate
according to pH is generally taken into account, with fairly
comparable levels of corrections among models. For starch,
regulation of degradation rate according to microbial bio-
mass is taken into account in some models (Baldwin et al.,
1987b; Dijkstra et al., 1992). Concerning passage rate, two
or three outflow rates are generally considered. The liquid
and the solid phases are either considered globally (Dijkstra
et al., 1992), or separated between forage and concentrate
particles (Sniffen et al., 1992; Lescoat and Sauvant, 1995), or
between large and small particles (Baldwin et al., 1987b;
Petruzzi et al., 2002). Although most models represent the
effect of intake level on flow rates, equations vary widely
among models. This largely impacts predictions, as under-
lined by Dijkstra and France (1996). A more mechanistic
representation of transit has been proposed in some models
(Sauvant et al., 1996), and deserves further exploration.
Published quantitative comparisons of mechanistic rumen
models based on their ability to predict ruminal digestion of
CW and/or starch are only scarce and restricted to steady
state evaluations. Bannink et al. (1997) compared models of
Baldwin (1995), Danfaer (1990) and Dijkstra et al. (1992).
Offner and Sauvant (2004a) compared models of Molly
(Baldwin et al., 1987b), CNCPS (Sniffen et al., 1992; Pitt
et al., 1996; Fox et al., 2000) and Lescoat and Sauvant
(1995). The evaluations differed according to the estimation
of the various input parameters, the amount and diversity of
feeding situations, and the tested statistical evaluation
methods, which lead to some differences in their conclu-
sions. Both evaluations stressed that none of the current
models accurately predicted fibre digestion, whereas Offner
and Sauvant (2004a) underlined the fairly good capacity of
Lescoat and Sauvants (1995) model to predict starch ruminal
digestion from in sacco measurements.
Production and absorption of VFA
Mechanisms involved in ruminal production of VFA
The VFA, as well as NH3, gas (CO2 and CH4), and occasion-
ally lactic acids, are end products of microbial fermentation
in the rumen. They consist mainly of acetate, propionate and
butyrate, and to a lower extent of valerate, caproate, iso-
butyrate and iso-valerate. The VFA mainly derive from dietary
carbohydrates, but in diets rich in rumen degradable protein,
deaminated amino acids (AAs) significantly contribute to
VFA yield via isobutyric, isovaleric and 2-methylbutyric acids
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produced from valine, leucine and isoleucine, respectively.
Following hydrolysis of dietary polymers, monomers are
fermented in the cytoplasm into VFA via glycolysis and
pyruvate. Acetate and butyrate are both formed from acetyl
coA, whereas propionate is mainly formed via the succinate
and to a lower extent via lactate (i.e. acrylate) pathway.
Valerate and caproate are assumed to be formed following
condensation of acetyl-CoA and propionyl-CoA. The fer-
mentation processes involve transfer of molecular H and
generates metabolic energy in the form of adenosine tri-
phosphate (ATP) that is subsequently utilized by micro-
organisms for their maintenance and growth. The partition
among the fermentative pathways is regulated through
thermodynamic laws by both ATP/ADP and NADH2/NAD
cofactor ratios, which reflect energy status and redox
balance, respectively. It is likely that when available C is
in excess, fermentation pathways that provide less ATP are
favoured (Sauvant and Van Milgen, 1995). The VFA compo-
sition, and the subsequent loss of C in gasses, are mainly
determined by the composition of the microbial population,
and thus largely determined by both intake level and dietary
composition, particularly the nature of carbohydrates and
their degradation rate. Typically, the development of fibro-
lytic microorganisms induces high levels of acetate, whereas
the development of amylolytic microorganisms induces an
increase in the proportion of propionate, allowing increased
utilization of excess reducing power. Concentrate diets, and
particularly diets rich in WSC, may also promote develop-
ment of protozoa that induces an increase in butyrate rather
than propionate (Brossard et al., 2004).
Quantitative evaluation of production of VFA
Total VFA. In most rumen models that represent VFA yield,
the total amount of VFA and gas produced is calculated
from the amount of degraded OM that is not incorporated
into microbial mass. Estimations are thus highly dependent
on the accurate representation of substrate degradation and/
or microbial synthesis. Moreover, a major problem in evalu-
ating the accuracy of estimations is that the evaluation is
based on measurements of VFA concentrations rather than
on rates of VFA production. Indeed, due to methodological
constraints (see review by France and Dijkstra, 2005), the
VFA yield is only rarely measured so that the actual value is
generally not known. More direct empirical approaches can
be developed to predict the ruminal production of VFA,
based on measured VFA production rate (VFA-PR) and on
estimation of the energy available in the rumen. The most
common in vivo methods for measuring the VFA-PR are
based on the use of VFA labelled with 14C (Sutton et al.,
2003), or 13C (Markantonatos et al., 2008). Although steady
state condition is normally assumed, the interpretation of
tracer data using dynamic modelling allows their adaptation
for non-steady state conditions. The total VFA-PR can be
determined after administration of any one of the individual
VFA (or of a VFA mixture), and determination of total VFA
enrichment, assuming VFA as a homogeneous pool (single-
pool scheme). Since it is the main limiting factor for microbial
 Carbohydrate digestion and nutrient fluxes

Table 1 Empirical equations developed from INRA feed evaluation system to assess digestive and net portal fluxes of VFA, glucose and
b-hydroxybutyrate
Equation Explained variable Prediction equation Sy.x Origin of predictors

1 Rumen total VFA yield (mmol/day per kg BW) 8.9 1 8.03 3 RfOM intake 11.8 INRA tables (2007)
Rumen VFA molar proportions (mol/100 mol)
2 Acetate 54.2 1 12.0 log (100 dNDF/dOM) 2 0.052 1.23 Measured
RStD 2 1.99 3 DM intake
3 Propionate 19.7 2 6.63 log (100 dNDF/dOM) 1 0.070 1.45 Measured
RStD 1 2.62 3 DM intake
4 Butyrate 19.0 2 3.99 log (100 dNDF/dOM) 2 0.026 RStD 0.88 Measured
5 Starch ruminal digestibility (RStD) (g/100 g starch) 43.9 1 0.68 StED 2 8.27 3 DM intake 11.9 INRA tables (2007)
6 Starch digested in small intestine (StdSI) St (1 2 RStD/100) 3 (74.05 2 1.22 St Measured
(g/day per kg BW) (1 2 RStD/100)) 3 DM intake/1000
Net portal fluxes (mmol/day per kg BW)
7 Total VFA 1.44 1 5.93 RfOM intake 5.83 INRA tables (2007)
VFA molar proportions (mol/100 mol)
8 Acetate 58.7 1 25.1 (0.9 dNDF/RfOM) 2.23 INRA tables (2007)
9 Propionate 34.0 2 18.9 (0.9 dNDF/RfOM) 2.18 INRA tables (2007)
10 Butyrate 7.9 2 7.3 (0.9 dNDF/RfOM) 1.10 INRA tables (2007)
11 Glucose 22.47 1 2.19 StdSI 0.84 Equation (6)
12 b-hydroxybutyrate 2.74 (62.11) 1 0.252 3 RfOM intake 0.86 INRA tables (2007)
VFA 5 volatile fatty acids.
RfOM 5 rumen fermentable OM intake; StdSI 5 starch digested in small intestine: g/d per kg BW.
DM intake: kg/d per 100 kg BW.
dNDF 5 digestible NDF; dOM 5 digestible OM; RfOM 5 rumen fermentable OM; St 5 starch: g/100 g DM.
RStD 5 starch ruminal digestibility; StED 5 starch in sacco degradability: g/100 g starch.
Equations 1 to 4: Nozie`re et al. (2010); equations 5 and 6: Offner and Sauvant (2004b); equations 7 to 12: Loncke et al. (2009b).

protein synthesis, the energy available in the rumen is
represented in the various N feed evaluation systems over
the world. In the French PDI system and its Dutch version
(DVE/OEB), it is estimated by the rumen fermentable OM
(RfOM) 5 digestible OM non-degradable CP (in sacco)
non-degradable starch (in sacco) fat a fermentation
product (with a 5 constant). Using a database that gathered
results of measured VFA-PR (Nozie`re et al., 2007), and
homogeneously characterizes dietary treatments according
to INRA feed tables, we showed a close relationship
between estimated RfOM intake and measured total VFA-PR
(Table 1, equation (1)). The relationship suggests an average
increment of 8.0 mol (60.6) of total VFA-PR/kg RfOM
(Nozie`re et al., 2010). This prediction presents no significant
interfering factors, and appears irrespective on whether
changes in RfOM intake are due to changes in DM intake
and/or in dietary RfOM content. Moreover, this slope, cor-
responding to approximately 540 g VFA/kg RfOM, is fully
consistent with the efficiency of microbial synthesis, which is
assumed in the PDI system to be approximately 300 g
microbial matter/kg RfOM, the rest consisting of gas.
Stoichiometry of fermentations. Several attempts have been
made to provide stoichiometric coefficients describing par-
tition of C between each VFA for each fermented substrate
(Figure 1). Using a large database, Murphy et al. (1982)
proposed, for five fermented substrates (soluble carbohy-
drates, starch, hemicellulose, cellulose and protein) separate
coefficients for roughage and concentrate diets. These
coefficients (Murphy et al., 1982; Murphy, 1984) have been
widely used in several mechanistic rumen models (Baldwin
et al., 1987b; Dijkstra et al., 1992), but their evaluation
indicated that the prediction of VFA molar proportions in
the rumen remained inaccurate (Neal et al., 1992; Bannink
et al., 1997). Using a similar approach, Bannink et al. (2006),
proposed new coefficients derived from data exclusively
on true (instead of apparent) ruminal digestion in lactating
cows. VFA predictions were however not substantially
improved. To avoid the discontinuity between roughage and
concentrate data sets, Friggens et al. (1998) developed a
minimalist design using sheep, allowing the comparison
of a wide range of diets differing in intake level, nature
and percentage of concentrate. The derived coefficients,
based on dietary chemical composition (CP, starch, sugar and
cellulose) rather than on ruminal digestion, were restricted
to grass-based diets. Sveinbjorrnsson et al. (2006) using a
large database on dairy cows restricted to Nordic diets, also
derived coefficients based on dietary chemical composition
(CP, starch, lactic acid, NDF from forage, NDF from con-
centrate and a rest fraction defined as OMNDFstarchCP
lactateVFA), and proposed corrections of coefficients,
depending on concentrate ether extract and feeding level. The
model of Lescoat and Sauvant (1995) primarily aimed at
predicting AA flows, used a more simple empirical approach
based on mean responses of VFA profiles to percentage of
concentrate, but this approach has been proved to be inac-
curate (Offner and Sauvant, 2004a). Besides digested sub-
strates, the specific effect of rumen pH on stoichiometry of
VFA from fermentation of WSC and starch, has also been
included by Argyle and Baldwin (1988), Pitt et al. (1996) and

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 Nozie`re, Ortigues-Marty, Loncke and Sauvant
(a) 80
70
%C2
60
50
40
5 15
%C3
(b) 70
60
%C2
50
40
10 20
%C3
Figure 1 Variations in stoichiometric coefficients (mol/100 mol volatile fatty acids) for rumen digested structural (a: 2 2 hemicellulose ; cellulose; NDF)
and non-structural (b: 2 2 soluble sugars, starch, both E) carbohydrates, according to dietary composition: high-forage (J), high-concentrate (K) or all
(E) diets. After Murphy et al. (1982); Bannink et al. (2006); Sveinbjornsson et al. (2006).
Bannink et al. (2006), but pH also depends on VFA. These
stoichiometric models, focused on the transformation of the
different specific substrates, indirectly represent the differ-
ential effects of amylolytic v. cellulolytic bacteria. In contrast,
protozoa, which use all types of substrates, but produce a
higher proportion of butyrate than bacteria are not generally
represented. Nagorcka et al. (2000) set up separate stoi-
chiometric coefficients of VFA yield for amylolytic bacteria,
fibrolytic bacteria and protozoa. Taken together, these results
stress the challenge for an accurate prediction of stoichio-
metry. Indeed, coefficients derived from dietary composition
appear to be too restrictive for generic application, given
the variability of rate and extent of fermentation. It is not
certain that the same coefficients can be used for all dietary
composition or intake levels. On the other hand, use of
coefficients derived from digested substrates requires an
accurate estimation of chosen digestible substrates. Another
major problem in evaluating the accuracy of stoichiometric
coefficients is that the evaluation is based on measurements
of VFA concentrations rather than on rates of VFA production.
Moreover, the assumptions made for derivation of the stoi-
chiometric estimates (e.g. efficiency of microbial synthesis,
absorption rates, etc.) vary widely among studies, and impact
the results of the comparative evaluation. Friggens et al.
(1998) clearly illustrated the limitations of such empirical
regressions and the lack of their general applicability. More
mechanistic approaches, based on representation of thermo-
dynamic laws have been attempted (Kohn and Boston, 2000;
Offner and Sauvant, 2006). Although first results were pro-
mising, such an approach does not appear sufficiently mature
to date for predictive purposes.
1062
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25
%C3
15
5
25 10 20 30
%C4
30
%C3
20
10
30 10 20 30
%C4
More empirical approaches have also been developed
based on interpretation of bibliographic databases with
appropriate statistical methods of meta-analysis (Nozie`re
et al., 2010). Through a wide diversity of experimental
factors (BoviDig database; Sauvant et al., 2000) changes in
the ratio between dNDF and dOM largely appear to explain
changes in VFA molar proportions in the rumen, according to
a curvilinear response. Residual variability around the pre-
diction is largely explained by RSD reflecting the effect of
site of starch digestion, DM intake and pH, which is in line
with Friggens et al. (1998), Sveinbjornsson et al. (2006) and
Bannink et al. (2006). Final models (Table 1, equations (2) to
(4)) including dNDF/dOM, RDS and DMi exhibit very low
Sy.x compared with other published models derived either
from stoichiometric models (Bannink et al., 2006) or from
more simple approaches based on a unique aggregated
covariable such as percentage of concentrate (Lescoat and
Sauvant, 1995) or NDF dietary content (Sauvant, 2003).
Moreover, the curvilinear effect of dNDF/dOM, as well as the
effect of DM intake on VFA profiles suggests that for a given
fermented substrate, stoichiometric coefficients may not be
considered as constant.
The calculation of the production rate of individual VFA
could be possible assuming proportionality between VFA
production and concentration, but this assumption is generally
considered as not always valid. The use of interchanging
compartmental models (3-pool scheme for acetate, propio-
nate and butyrate) allows to take into account interconver-
sions between VFA, and is not dependent on the assumed
proportionality between VFA production and concentration.
Using this approach, Sutton et al. (2003) concluded that the

molar proportions of acetate and propionate only slightly
underestimated the proportions of their net production rates,
whereas the molar proportion of butyrate overestimated its
net production rate, particularly at low concentrations. Using
the VFA-Prod database, Nozie`re et al. (2010) confirmed these
conclusions over a wider range of VFA molar proportions,
and also stressed that the differences in molar proportion
of butyrate between concentration and net production were
mainly explained by methodological inter-study effects. This is
a promising result with respect to the estimation of individual
VFA ruminal fluxes based on their ruminal concentrations.
Mechanisms involved in the absorption of VFA
This aspect has been recently extensively reviewed (Gabel
and Aschenbach, 2006). Absorption of VFA through the
reticulo-rumen wall accounts for 65% to 85% of the ruminal
production, depending on the balance between the absorp-
tion rate and turnover rate of the liquid phase in the rumen.
The VFA escaping absorption in the reticulo-rumen are
absorbed in the omasum and abomasum. According to their
pKa (,4.9), over 95% of the VFA should be in ionized form
(VFA2) at the ruminal pH around 6 to 7, whereas their non-
ionized form (VFAH) may diffuse more easily than VFA2
through the double lipid layer of cell membranes. The simple
diffusion of VFAH surely occurs through the ruminal epithe-
lium, with H1 deriving from Na1/H1 exchange at the apical
side of the epithelial cells. This is favoured by the neutral
intracellular pH, which favours the intracellular VFA2 form,
thus increases the gradient of VFAH from the lumen to the
epithelial cell. The absorption of VFA2 by facilitated diffu-
sion, involving anion-exchange proteins (AE, DRA, PAT) that
promote the transfer of bicarbonate from the epithelial cell to
the rumen content cannot be ruled out. Extrusion through the
basal side partly takes place by passive diffusion of VFAH, but
anion exchange (or other transport) proteins may also be
involved, although experimental evidence is still lacking.
Most studies conducted in vivo on temporarily isolated
rumen showed that the fractional absorption rate of the
main VFA (acetate, propionate, butyrate) increases with
chain length. Data on minor VFA are only scarce but confirm
this trend, and suggest that branched-chain VFA have
lower fractional absorption rate than their non-ramified
isomers (Oshio and Tahata, 1984). The decrease in ruminal
pH increases the absorption rate of VFA (Oshio and Tahata,
1984; Dijkstra et al., 1993). The reported effects of rumen
concentrations of VFA on their fractional absorption rate
differ among studies, and may depend on associated chan-
ges in pH and/or extent of VFA metabolism in the rumen
epithelium that affects the concentration gradient between
lumen and blood. The VFA absorption rate is also positively
affected by the surface area (Perrier et al., 1994) and thus by
liquid volume (Dijkstra et al., 1993), as represented in some
rumen models (Dijkstra et al., 1993; Pitt et al., 1996).
The specific effect of osmolality on VFA absorption rates
vary among studies. Whereas some indicate that both water
and VFA absorption rates decrease on average of 23%/h
and 26%/h, respectively, when osmolality increases of
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Carbohydrate digestion and nutrient fluxes
80
70
60
50
k abs (%/h)
40
30
20
10
0
4.0 5.0 6.0 7.0
pH
Figure 2 Representation of pH effect on fractional absorption rates (kabs)
of volatile fatty acids (VFA), according to MichaelisMenten function (
and
: kabs 5 kA/1 1 (MVFA/[VFA]), with kA 5 maximum absorption
rate, MVFA 5 MichaelisMenten affinity constant, and pH linearly related
to [VFA]), or to HendersonHasselbach dissociation law (- - - : kabs 5 ki 1
(kni-ki)/(1 1 10 pH-pka), with Ki and Kni 5 fractional absorption rates of
ionized and non-ionized form, respectively). After Lescoat and Sauvant
(1995); Nozie`re and Hoch (2006); Chilibroste et al. (2008).
100 mOsm/l (Oshio and Tahata, 1984), others report that
VFA absorption rates are maximal when osmolality is close
to 350 mOsm/l (Bueno, 1972; Lopez et al., 1994), that is,
when the net transfer of H2O through the rumen wall is near 0.
The fact that VFA largely determines ruminal osmolality may
explain the discrepancy among studies.
Quantitative evaluation of absorption rates of VFA
Representation of VFA absorption widely differs among
models, with respect to single v. differentiated values for
individual VFA and saturated v. unsaturated absorption
processes. Moreover, whereas most rumen models include
the effect of pH on VFA fractional absorption rate, repre-
sentation highly differs among models (Figure 2). For
example, a MichaelisMenten function of the ruminal con-
centration of total VFA (therefore of pH) was retained by
Lescoat and Sauvant (1995) or Chilibroste et al. (2008),
whereas in Dijkstra et al. (1993) or Pitt et al. (1996), each
VFA was considered individually and the response to pH was
based on the HendersonHasselbach dissociation law
(VFA2/VFAH ratio). This latter representation appears to be
more consistent with experimental measurements using
temporarily isolated rumen. Based on the assumption that
absorption rate depends on VFA2/VFAH ratio, thus on pKa,
Nozie`re and Hoch (2006) proposed an empirical equation
relying on variation of fractional absorption rates with pH.
Based on these results, the effect of pH on VFA fractional
absorption rate may be simply represented through the
VFA2/VFAH ratio, with fixed values of 16%, 18% and 22%/h
1063
 Nozie`re, Ortigues-Marty, Loncke and Sauvant
for VFA2 v. 76%, 102% and 135%/h for VFAH, for acetate,
propionate and butyrate, respectively. Recently, based on the
assumption that the lower the rumen pH, the more transport
results from passive diffusion of VFAH rather than facilitated
and saturable transport of VFA2 (both driven by rumen con-
centrations), Bannink et al. (2008) proposed a separate repre-
sentation of these two routes of VFA absorption, and assumed
that transport from epithelium to blood is facilitated and is
faster than the facilitated transport from lumen to epithelium.
Interestingly, fractional absorption rates of individual VFA pre-
dicted by steady-state simulations with the mechanistic model
of Bannink et al. (2008) were similar to those obtained by the
empirical model of Nozie`re and Hoch (2006).
Starch intestinal digestion and glucose absorption
High amounts of cereals incorporated in the diet of produ-
cing ruminants can induce digestive disorders related to an
excessive digestion of starch in the rumen. An increase in the
dietary content of rumen digestible starch of 10 g/kg DM
drastically affects pH (20.1 unit), NDF digestion (23 g/
100 g) and the acetate/propionate ratio (20.4 mol/mol) in
the rumen (D. Sauvant, unpublished synthesis of literature
data). A shift in the site of starch digestion from rumen to
intestines can prevent these disorders, but the energy effi-
ciency of such a strategy remains questionable. Based on a
simulation model of starch intestinal digestion in steers,
Huntington et al. (2006) concluded that advantages of
digestive efficiency through increasing intestinal starch
digestion could only be obtained at low intake or with highly
processed feeds. More generally, with conventionally fed
animals, there is evidence that a non-negligible proportion
(on average 25%) of starch escaping ruminal fermentation
is recovered in faeces (Offner and Sauvant, 2004b), inducing
a decrease in OM digestibility and consequently dietary
metabolizable energy (ME). Still, perfusion experiments
indicated that at similar energy supply, duodenal glucose is
more efficient than ruminal propionate for whole body glu-
cose appearance rate (Rigout et al., 2003; Lemosquet et al.,
2009). However, the impact on milk yield and composition
remains moderate, as confirmed by a meta-analytical
approach (Rulquin et al., 2007). In addition, based on a large
database, the response of milk yield to an increase in
absorbable C appears to be similar between ruminal pro-
pionate (estimated from Table 1, equations (1) and (3)) and
intestinal glucose (estimated from Table 1, equation (6))
(D. Sauvant, unpublished synthesis of literature data).
Intestinal starch digestion
Starch escaping ruminal degradation can reach 8 g/day per
kg BW (Overton et al., 1995), that is, 70% of starch intake.
Starch entering the duodenum is submitted to the activity of
pancreatic a-amylase, that hydrolyses both amylose and
amylopectin into branched-chain products (limit dextrins,
mainly from amylopectin) and oligomers of two or three
glucose units. Oligosaccharides are submitted to hydrolysis
by brush border oligosaccharidases, that is, maltase and
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isomaltase. Most of post-ruminal starch digestion (on aver-
age 70%) occurs in small intestine, but starch digestibility in
the intestine is extremely variable from 10% to 95%. Several
studies have assessed factors that limit starch digestion
in the small intestine (see reviews by Huntington, 1997;
Harmon et al., 2004; Huntington et al., 2006). Briefly, rumi-
nant pancreas seems more responsive to energy intake than
to duodenal starch, and the brush border oligosaccharidase
activities seem to be poorly responsive to diet. Amylase is
likely more limiting than intestinal oligosaccharidase activity
in the starch digestion process (Huntington, 1997). Amylase
secretion may be enhanced by increasing duodenal entry of
protein (Taniguchi et al., 1995), but it has not been clearly
demonstrated in conventionally fed animals. The extent of
starch digestion in the small intestine can also be limited by
surface exposure of starch to enzymes in this compartment.
Based on in vivo measurements on dairy cows, several works
(Oba and Allen, 2003a and 2003b; Taylor and Allen, 2005)
suggested that the physicochemical characteristics of corn
particles limit intestinal starch digestion. Based on in sacco
degradation of corn grain, there is evidence that intrinsic
factors affecting starch ruminal degradability (particle size,
vitreousness) also affect their ability of being digested in the
intestines (Ramos et al., 2009).
Based on an extensive review of literature data, an
empirical model to predict site and extent of starch digestion
from in sacco data has been proposed by Offner and Sauvant
(2004b). Compared to previous similar attempts (Nocek and
Tamminga, 1991), this model includes the effect of intake
level, with an average effect on RSD of 20.083 g/g starch
intake, when intake level increases by 1 kg DM/100 kg
BW. This effect may likely reflect the influence of intake
on turnover rate of particles, which competes with starch
degradation. Prediction of starch digestion in the small
intestine is based on the negative relationship between
starch intestinal digestibility (g/g) and the dietary content of
starch escaping ruminal digestion (g/g), with an average
slope of 21.22. Prediction of starch digestion in the hindgut
is based on an average digestibility of 50% of starch
reaching ileum. The first evaluation of this relatively simple
model of starch digestion was based on the prediction of
faecal starch in cattle and dairy cows, which was itself
satisfactorily predicted with a Sy.x of 0.12 kg/day over a
target of 0 to 1 kg/day. More mechanistic approaches are still
scarce, but some preliminary results have been recently
presented by Bannink et al. (2009).
Glucose absorption
Starch hydrolysed into glucose can reach 5 g/day per kg BW
(Stock et al., 1987), but most of the reported values rarely
exceed 3 g/day per kg BW. Whereas the possibility of fer-
mentation of glucose in the small intestine exists (Nicoletti
et al., 1984), it is likely that most of the glucose released in
the lumen of the small intestine is subjected to absorption
and transit processes. The two main routes for transfer
of glucose from the lumen to the bloodstream are active
transport and paracellular diffusion with absorption of water

(Huntington, 1997). Glucose transporters have been char-
acterized in the small intestine of ruminants (Shirazi-Beechey
et al., 1995; Zhao et al., 1998; Guimaraes et al., 2007).
SGLT1 consists of Na1-dependent glucose transporter loca-
ted in the brush border membrane of enterocytes, and driven
by an electrochemical gradient maintained by Na1/K1
ATPase located on the basolateral membrane. This high-
affinity transporter presents a great deal of homology
(.80%) between vertebrate species. The SGTL1 transports
1 mol of glucose against 2 mol of Na1 in each of its
cycle, with a Km ranging between 0.1 and 0.5 mmol/l, and
an estimated capacity of 50 to 200 cycles/s (Ferraris et al.,
1989; Hediger and Rhoads, 1994). GLUT2 functions as a
low-affinity transporter localized to both the apical and
basolateral membranes of the enterocytes (Kellett et al.,
2008). In steers, the absorption capacity for glucose (Kreh-
biel et al., 1996; Harmon and McLeod, 2001), the uptake
activity of glucose transporters (Bauer et al., 2001), as well
as the basal expression of both SGLT1 and GLUT2 mRNA
(Liao et al., 2009), highly vary along the intestinal axis,
being the highest in the jejunum and the lowest in the ileum.
There is experimental evidence in ruminant that abomasal
perfusion of partially hydrolyzed starch or glucose induces a
rapid (within a few days) increase in glucose transport
capacity (Shirazi-Beechey et al., 1995; Bauer et al., 1995 and
2001). This involves increasing mRNA content of glucose
transporters, as observed in sheep for SGTL1 (Lescale-Matys
et al., 1993; Shirazi-Beechey et al., 1995) and in ileum of
steers for both SGLT1 and GLUT2 (Liao et al., 2009).
A simulation model of starch digestion and glucose uptake
from the small intestine was developed by Huntington
(1997). Pancreatic secretions, as well as possibly fermenta-
tion of glucose, were not considered. This model considered
an active transport, with a quadratic decrease in activity
from the proximal to the distal small intestine, and a para-
cellular diffusion of glucose dependent on luminal glucose
concentration. Based on data by Kreikemeier et al. (1991),
simulations suggested that diffusion represents a small
proportion of total absorption (,15% to 20%) at physiolo-
gical luminal glucose concentrations (,3.5 mM). Simula-
tions also suggested that in adapted animals, the capacity
for active transport of glucose across the gut wall does not
seem to limit the glucose absorption, whereas starch
digestion capacity is the primary limitation.
Metabolism of VFA and glucose by
portal-drained viscera
Volatile fatty acids
Mechanisms. This aspect has been extensively reviewed
(Remond et al., 1995; Kristensen and Harmon, 2006). Briefly,
activation of VFA is the first and limiting step in their
metabolism in the portal-drained viscera (PDV). In vitro, the
acyl-(acetyl-, propionyl- and butyryl-) CoA synthetase activ-
ities in the ruminal epithelium increase with VFA chain
length and intake level, and are also regulated by the
availability of the different VFA. These regulations favour
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Carbohydrate digestion and nutrient fluxes
butyrate activation. Acetate and butyrate metabolism can
result in a complete oxidation to CO2 entering the Krebs
cycle via acetyl-CoA, and/or in the production of ketones via
acetoacetyl-CoA. A low interconversion between acetyl-CoA
and acetoacetyl-CoA (produced from the oxidation of buty-
rate) explains why acetate is preferably oxidized to CO2
while the metabolism of butyrate mainly leads to ketones.
Propionate can enter the Krebs cycle via succinyl-CoA for
complete oxidation to CO2, or via malate before being
metabolized in the extra-mitochondrial space into pyruvate,
lactate or alanine, as observed in vitro. However, in vivo
experiments based on simultaneous ruminal infusions of
propionate (up to 1.6 mmol/h per kg BW) and measurements
of net portal appearance of nutrients suggest that its con-
version to lactate or other products is quantitatively low
(Nozie`re et al., 2000; Majdoub et al., 2003; Kristensen and
Harmon, 2004). Valerate is metabolized to acetyl-coA and
propionyl CoA by b-oxidation and can thus produce both
b-hydroxybutyrate and lactate in vitro. Isobutyrate can be
metabolized in methyl-malonic or succinic acid.
Quantitative evaluation. The extent of VFA metabolism by
PDV has long been approached in vivo through measure-
ments of net portal recovery of ruminally produced (or
infused) VFA (review by Remond et al., 1995). It is now well
established that this approach overestimates PDV metabo-
lism, due to the confounding effect between microbial and
tissular metabolism. Kristensen (2001) showed in vivo that
up to 28% of the amount of 13C infused in the rumen as
[2-13C]-acetate was recovered in non-acetate VFA (20%) or
in the duodenal microbial matter as fatty acids or aminoacids
(8%). Nozie`re et al. (2003) showed in vitro that 14C supplied
as [2-14C]-propionate was incorporated within bacteria and
protozoa. This incorporation was estimated to account for
10% of net propionate production, and may be attributed
to odd-chain fatty acid synthesis. Recent results obtained
with the temporarily isolated washed rumen method in both
sheep and steers (Kristensen and Harmon, 2006) support the
hypothesis that absorbed at first pass, acetate, propionate
and isobutyrate are almost fully recovered in the portal vein
(portal recovery of 105% to 109%, 91% to 95%, 101% to
102%, respectively), whereas ruminal epithelium extensively
metabolizes butyrate and valerate (portal recovery of 18% to
52%, 16% to 54%, respectively). These results also support
a low production of acetate by the rumen epithelium, as
noted in vitro (Sehested et al., 1999). At second pass, the
PDV take up a large amount (20% to 40%) of the arterial
acetate supply. This uptake appears to be non-linearly related to
arterial supply (Nozie`re and Hoch, 2006), and probably con-
cerns tissues other than the ruminal epithelium. Assuming that
80% of the amount of acetate used by PDV is oxidized (Pethick
et al., 1981), this uptake could account for 50% of the ATP
used by PDV. Based on results of Kristensen et al. (2000b) on
sheep, the low net portal recovery of butyrate (20%) can be
attributed to ketogenesis in the rumen wall with production of
b-hydroxybutyrate (45%) and acetocetate (15%), and to oxi-
dation (20%). The PDV (likely tissues other than the ruminal
1065
 Nozie`re, Ortigues-Marty, Loncke and Sauvant
epithelium) also take up a substantial amount of arterial
b-hydroxybutyrate (Kristensen et al., 2000b), quantified at 13%
of the arterial supply to PDV in sheep.
Data on in vivo interactions between VFA within the PDV
are scarce. Unlike observations in vitro, Kristensen et al.
(2000a) reported no significant effect in vivo of short-term
infusions (12 h) of butyrate on the net portal recovery of
acetate and isobutyrate, while recovery of propionate tended
to increase as also noted with long-term infusions (1 week)
(Nozie`re et al., 2000). In both studies, a positive effect
of ruminal butyrate infusion on the net portal recovery of
butyrate and valerate was shown. Taken together, in vivo
observations on PDV, when compared to in vitro observa-
tions on ruminal epithelium, suggest the existence of an
acyl-CoA synthetase with a preferential affinity for butyrate
and valerate, which may activate acetate, propionate and
isobutyrate when preferential substrates are lacking.
Although propionate metabolism by the ruminal epithelium
appears limited in vivo, in vitro data support the fact that
propionate counteracts the depressing effect of acetate on
the formation of b-hydroxybutyrate from butyrate in the
ruminal epithelium (Baldwin and Jesse, 1996). This probably
results from a shift in the mitochondrial NADH/NAD status.
In vitro, the affinity for and the capacity of isolated rumen
epithelial cells to oxidize substrates are largely unaffected by
ME intake or the dietary forage : concentrate ratio, suggest-
ing that the ruminal environment may not affect the cellular
capacity of the ruminal epithelium to oxidize substrates
(Baldwin and McLeod, 2000).
The main efforts on mechanistic representations of epithelial
metabolism of VFA were made by Bannink et al. (2008). The
activation of VFA by CoA-synthetase was assumed to be irre-
versible, and the rate limiting step of the intraepithelial meta-
bolism. The competitive inhibition among VFA was represented.
The epithelial metabolism of VFA was assumed to provide all
energy required by the epithelium, which itself is affected by
VFA load. These functional adaptations of rumen epithelia are
represented by a feedback control mechanism, and include
representation of both papillae shape and epithelial mass.
Simulations, including this adaptative response, have large
impacts on the predicted VFA absorption rates and extent of
intra-epithelial metabolism of acetate and propionate, whereas
it is recognized that more appropriate parameterization of CoA-
synthetase activities is required. In addition, it is noticeable that
possible interconversions between VFA in the epithelium and
metabolism of arterial VFA (acetate) are not represented.
Recently developed molecular approaches appear promising
to assess the regulation of expression of genes encoding
for enzymes involved in VFA metabolism (ACAS2L, BUCS1,
BCKDHA, etc.) (Baldwin et al., 2007).
Empirical approaches based on meta-analysis have been
developed at INRA to account for prediction of net portal
appearance of VFA from dietary characteristics. The Flora
database (Vernet and Ortigues-Marty, 2006), gathering
results of portal nutrient fluxes and presenting a homo-
geneous characterization of dietary treatments according
to INRA feed tables was used (Loncke et al., 2009b).
1066
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150
Total VFAs (mmol/d per kg BW)
100
50
0
0 2 4 6 8 10 12 14 16 18
RfOM intake (g/d per kg BW)
Figure 3 Effect of rumen fermentable organic matter (RfOM) intake
on ruminal production (K) and net portal appearance (J) of total
volatile fatty acids (VFA): adjusted within-experiment models (cf Table 1,
equations (1) and (7), respectively). After Nozie`re et al. (2010); Loncke
et al. (2009b).
We showed that, net portal appearance of total VFA was
linearly and closely related to estimated RfOM intake across
a wide diversity of experimental factors (Table 1, equation
(7)). The slope suggests a net portal appearance of 5.9 mol
(60.5) of VFA/kg RfOM. The comparison with the slope
obtained on ruminal VFA production using the same princi-
ples (8.0 mol/kg RfOM, equation (1)), suggests a net portal
recovery of 75% of VFA produced in the rumen (Figure 3).
Moreover, changes in VFA molar proportions in the portal
flow appear largely explained by changes in the dNDF/RfOM
ratio (equations (8) to (10)) that was fully consistent with
observations in the rumen (equations (2) to (4)). In addition,
net portal appearance of b-hydroxybutyrate that results
from both ruminal ketogenesis and uptake of arterial
b-hydroxybutyrate by PDV, appears closely related to RfOM
intake (equation (12)).
As discussed above, although there are some differences
in VFA profiles between concentration and net production
in the rumen, the estimation of the production rate of
individual VFA using combinations of total VFA-PR and VFA
profiles models (Table 1, equations (1) to (4)) appear closely
related to their net portal appearance (Figure 4). The rela-
tionships appear quantitatively consistent with knowledge
on the extent of PDV metabolism of VFA, that is, a pre-
ferential uptake of butyrate and a negligible uptake of
acetate during first pass. Indeed, when portal appearance
is corrected for PDV uptake of arterial acetate (according to
the exponential relationship between arterial supply and
uptake proposed by Nozie`re and Hoch, 2006), the relation-
ship between the estimated ruminal production of acetate
and the first pass portal appearance of acetate does not
significantly differ from the first bisector. In addition, pro-
pionate appears largely recovered, whereas 25% of butyrate
is recovered as butyrate and 46% as b-hydroxybutyrate. This
result also suggests that whereas high levels of butyrate
infused in the rumen may induce saturation of ketogenesis in

Corrected portal appearance of acetate
(mmol/d per kg BW)
100 40
90
80 30
70
60 20
50
40 10
30
20 0 0
20 30 40 50 60 70 80 90 100
Estimated ruminal production of
acetate (mmol/d per kg BW)
Figure 4 Relationships between estimated volatile fatty acids production in the rumen (cf Table 1, equations (1) to (4)), and their measured net portal
appearance. Portal fluxes of acetate are corrected for uptake of arterial acetate by portal drained viscera (Nozie`re and Hoch, 2006): adjusted within-
experiment models (Nozie`re et al., 2010).
the rumen wall (Krehbiel et al., 1992; Nozie`re et al., 2000),
this upper limit is likely not achieved in conventionally fed
animals. Interestingly, in steady-state simulations, the portal
recovery of individual VFA predicted with the mechanistic
model of Bannink et al. (2008) was similar to that of the
present empirical approach.
Glucose
A net portal uptake of glucose is observed when no or only a
little amount of starch escapes ruminal fermentation. When
a substantial amount of starch, dextrin or glucose is infused
in the abomasum, the portal flux of glucose shifts from net
uptake to net appearance, but the net portal recovery is not
complete ranking from 57% to 73% of glucose infused and
from 25% to 51% of starch infused, depending on experi-
mental conditions (Lindsay and Reynolds, 2005). This is
partly due to increased use of arterial glucose by PDV (Janes
et al., 1985). However, with conventionally fed animals,
this appears not associated with an increase in oxygen
consumption by PDV (Reynolds et al., 1998; Nozie`re et al.,
2005), suggesting that other substrates are conserved
(Huntington et al., 2006). Within the PDV, the mesenteric-
drained viscera (MDV) are the main users of arterial glucose,
contributing to 70% of glucose uptake, as observed with
non-starchy diet (Reynolds and Huntington, 1988). With
diets rich in maize that induce a large amount of starch
entering duodenum, the increased use of arterial glucose
occurs in both stomach and MDV tissues (Reynolds and
Huntington, 1988). Given the high increased use of arterial
glucose by PDV, the apparent portal (or mesenteric) recovery
of glucose is thus underestimated when expressed as a net
basis; it is substantially increased when changes in arterial
uptake by PDV are taken into account but remains incom-
plete (from 51% to 71%; Harmon et al., 2001). Based on
calculation of the area under the curve of net portal (or
mesenteric) fluxes of glucose against time following a star-
chy meal in sheep (Remond et al., 2009) or an abomasal
pulse of glucose in dairy cow (Larsen and Kristensen, 2007),
first pass recovery of glucose may be almost complete. The
lost glucose may be attributed to metabolism of glucose
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Carbohydrate digestion and nutrient fluxes
Net portal appearance of propionate Net portal appearance of butyrate () and -
(mmol/d per kg BW) hydroxybutyrate (o) (mmol/d per kg BW)
20
10
0 10 20 30 40 0 10 20
Estimated ruminal production of Estimated ruminal production of
propionate (mmol/d per kg BW) butyrate (mmol/d per kg BW)
within the small intestine to supply glycerol for the absorp-
tion of long-chain fatty acids, as suggested by Reynolds et al.
(1988). It may also be partly due to residual microbial
fermentation of glucose after hydrolysis of starch in the small
intestine, as suggested by Larsen and Kristensen (2007). The
contribution of arterial glucose to lactate net portal release
remains unclear. There is in vitro experimental evidence
that ruminant enterocytes possess metabolic flexibility for
oxidative metabolism of glucose, glutamine and glutamate
depending on the type and concentration of available addi-
tional substrates (Oba et al., 2004).
An empirical approach was developed for a quantitative
prediction of the net portal appearance of glucose based on
knowledge of starch digestion (Offner and Sauvant, 2004b;
Loncke et al., 2009b). A close and linear relationship was
observed between the predicted amount of starch appar-
ently digested in the small intestine (Table 1, equation (7))
and the actual net portal appearance of glucose (equation
(12)). This relationship presented no interfering factors, and
the Sy.x was rather low (0.035 mmol/h per kg BW). The
intercept of this relationship suggested a basal use of arterial
glucose by PDV averaging 0.103 mmol/h per kg BW, which is
consistent with the basal net uptake of glucose observed
with non-starch diets. The slope suggested a net portal
recovery of averaging 44%, which is consistent with the
average increment of net portal flux of glucose observed in
abomasal infusions experiments, as discussed above.
Liver metabolism of VFA and glucose
Mechanisms
Hepatic VFA metabolism in ruminants has been extensively
reviewed (Brockman, 2005; Hanigan, 2005; Lindsay and
Reynolds, 2005; Kristensen and Harmon, 2006) and only a few
points will be highlighted here. The non-ionized forms present
in very low proportions in the portal blood are absorbed
passively through hepatocyte membranes (Bergman, 1990).
The influx of the most frequent ionic forms is carrier mediated,
via monocarboxylate transporters recently shown in the liver
of ruminants (Koho et al., 2005; Kirat et al., 2007). Cytosolic
1067
 Nozie`re, Ortigues-Marty, Loncke and Sauvant
short chain fatty acids then enter mitochondria via mono-
carboxylate carrier or mitochondrial carnitine transporter
(Zammit, 1990), where they are esterified as CoA esters by
specific synthetases. Even-chain fatty acids (acetate, butyrate)
are differently taken up by the liver. Hepatic metabolism of
acetate is limited, being simultaneously oxidized and pro-
duced (Reynolds, 2002) while butyrate is largely taken up by
the liver. Both fatty acids are rather oriented towards keto-
genesis and lead to the same metabolite acetyl-CoA, which
can enter the Krebs cycle to be oxidized. Their metabolism
interacts with that of all nutrients, which can also be con-
verted to acetyl CoA. Free acetate can also be formed from
acetyl-CoA and from both peroxisomal and mitochondrial
fatty acid oxidation (Drackley, 1999 in dairy cows). Among
nutrients potentially oxidized in the liver for ATP production,
the contribution of acetate and butyrate has been questioned.
Net hepatic uptake of acetate is much lower than that of
butyrate (Reynolds, 2002), but acetate is more efficient to
produce ATP than butyrate (Gallis et al., 2007) and estimation
of ATP production from hepatic acetate utilization may lead to
underestimation. Ketogenesis is the major metabolic fate for
butyrate (Heitmann et al., 1987). Butyrate has recently been
shown to exert specific properties on human hepatocyte
growth and differentiation (Yoon et al., 1999), but evidence in
ruminants is still lacking. Odd-chain fatty acids, in particular
propionate, take a different enzymatic pathway leading to
succinyl-CoA. Two of the propionate metabolites (propionyl-
CoA and 2-methylcitrate) having inhibitory effects on the
Krebs cycle (Nguyen et al., 2007), propionate is largely used as
a precursor of gluconeogenesis. Considering the limited
absorption of glucose, and the similar whole body glucose
requirements in ruminants and monogastrics (Lindsay, 1981),
ruminants rely on hepatic gluconeogenesis for 85% of their
whole body glucose turnover (Ortigues-Marty et al., 2003a).
Glucose is synthesized from three carbon precursors, propio-
nate (for up to 50% to 70%; Veenhuizen et al., 1988; Berg-
man, 1990), AAs (mainly Ala, Gln and Gly) from 11% to 40%
(Kraft, 2009), L-lactate (7% to 44%; Krehbiel et al., 1992) and
glycerol (5%; Brockman, 2005) and may be stored temporarily
in the liver as glycogen. Contributions of individual precursor
may vary widely with the nutritional status of the animal.
Major key limiting gluconeogenic enzymes are phosphoe-
nolpyruvate carboxykinase and pyruvate kinase. Relative
expression and activity of these enzymes are indicators of
gluconeogenic activity and of precursor contributions (Velez
and Donkin, 2005).
Strong interactions exist between ketogenic and glucogenic
metabolism in the liver. Ketogenesis is down regulated by
glucogenic metabolism (Berthelot et al., 2002). In rat hepato-
cytes this down regulation is partly counteracted by carnitine
(Brass and Bayerinck, 1988), but evidence in ruminants is
lacking. Conversely, medium chain fatty acids inhibit ovine
hepatic gluconeogenesis and propionate metabolism in vitro
(Chow and Jesse, 1992). Butyrate has similar effects in vitro in
bovine hepatocytes (Aiello et al., 1989). Acute supply of buty-
rate has also a sparing effect on both hepatic glucose oxidation
and glycogen storage as shown in rats (Beauvieux et al., 2008).
1068
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Finally, VFA have long been considered mostly as provi-
ders of carbon or energy, and apart from their regulatory role
on intake, no other regulatory role has been investigated at
cellular level. Recently, a cellular signalling role has been
demonstrated for the C2 to C6 short-chain fatty acids as
activators of G protein-coupled receptors in mice adipocytes
and stimulators of leptin production. This mechanism is
suspected in mice to be involved in the regulation of intake
by chronic propionate (Brown et al., 2003; Xiong et al.,
2004). The relevance for ruminants is not yet known.
Quantitative evaluation
Quantitative measurements of hepatic metabolism are
mainly based on the arterio-venous method. Considering the
small arterio-venous differences, the risk of inaccuracy in the
results may be greater than for measurements of net portal
appearance depending on the metabolite. This black box
approach has more recently been coupled with the infusion
of labelled molecules in order to better evaluate the meta-
bolic fate of nutrients. Besides, a number of mechanistic
models of liver metabolism have been elaborated to recon-
cile quantitative information with biochemical knowledge
on the different metabolic pathways and their regulation in
the liver. All existing models apply to lactating cows, and
deal mostly with nitrogen metabolism. Nevertheless, a few
models represent VFA or glucose metabolism as subcom-
ponents of whole animal models (Waghorn, 1982; Baldwin
et al., 1987a; Danfaer, 1990; Martin and Sauvant, 2007) or
with isotope tracer components (Freetly et al., 1993) and
more recently a model of ketosis has been developed (Guo
et al., 2008). In addition, although promising for development
of further models, the hormonal effects on carbohydrate
metabolism have been rarely included in liver models (Danfaer,
1990). Limited quantitative evaluation and comparison of these
models has been published. More generic quantitative infor-
mation was derived recently from the Flora database (Vernet
and Ortigues-Marty, 2006) using data obtained in different
physiological statuses (growing, gestating, lactating, non-
producing) in both sheep and cattle.
No simple mass action law exists between hepatic input
and output of ketogenic nutrients. On a net hepatic flux basis,
metabolism of acetate seems limited in the liver because it
may be simultaneously oxidized and produced (Reynolds,
1995). Mechanistic models in lactating cows predict a net
hepatic acetate release (Freetly et al., 1993). An empirical
modelling approach recently showed that net hepatic release
may reach 0.32 to 0.56 mmol/h per kg BW, representing 20%
of acetate net portal appearance in lactating cows and 10%
in growing ruminants (Loncke, 2009) with different con-
tributions from dietary and endogenous fatty acids. However,
our results do not confirm the prediction that net hepatic
acetate release increases with the long chain fatty acid supply
(Hanigan et al., 2004, cited by Drackley and Anderson, 2006).
By contrast, butyrate is largely taken up by the liver (from
0.05 to 0.19 mmol/h per kg BW), with an average net uptake
rate of 76% of net portal appearance. Net hepatic uptake
is however lower in growing-fattening ruminants probably

0.8
NHR -OHB (mmol / h per kg BW)
0.7
0.6
0.5
0.4
0.3
0.2
0.1
-40 -30 -20 -10 0 10
EB (kcal / d per kg BW)
Figure 5 Relationships between energy balance (EB) and net hepatic
release of b-hydroxybutyrate (NHR b-OHB) in lactating (m), growing-
fattening (K) and non-producting (J) ruminants: adjusted within-
experiment models. After Loncke (2009).
due to a higher insulinemia (Loncke, 2009). Plasma ketone
bodies (b-hydroxybutyrate 1 acetoacetate 1 acetone) accu-
mulation has also been predicted in periparturient cows from
body fat mobilization (itself a function of BW and condition
score plus an estimation of glucose deficiency) and utilization
(Guo et al., 2008). More precisely, net hepatic release of
b-hydroxybutyrate was clearly shown by empirical models to
be driven both by digestive (acetate, butyrate, long chain
fatty acids) and endogenous precursor (non-esterified fatty
acids) supply, depending on the energy balance of the animal
(Figure 5; Loncke, 2009). In most models estimation of body
fat mobilization and hepatic utilization is a common difficulty
(Freetly et al., 1993; Danfaer, 1994; Guo et al., 2008). Inac-
curate estimation is probably responsible for a general carbon
deficit identified in mechanistic models of liver metabolism
(Hanigan et al., 2004). Recently, metabolic pathways related
to non-esterified fatty acids have been included in the model
by Martin and Sauvant (2007).
As for net hepatic glucose release (ranging from 0.67 to
1.74 mmol/h per kg BW), conditions in which, in ruminants,
hepatic gluconeogenesis is regulated by precursor avail-
ability or by other signals (e.g. portal signal, Moore et al.,
1999) is not totally clear cut. In non-lactating ruminants,
glucose turnover increases linearly with ME intake, although
the increase was higher for growing as compared with
non-productive ruminants (Ortigues-Marty et al., 2003b).
In lactating cows, milk yield increased with the supply of
gluconeogenic precursors from digestive origin (ruminal
propionate 1 intestinal glucose) up to a plateau (Rigout et al.,
2003), but the energy secreted in milk lactose linearly
responds to ME intake (Sauvant et al., 2009). Assuming that
milk yield is highly dependent on glucose availability, this
suggests that glucose turnover follows the same pattern.
Unfortunately, a very limited number of studies measured
simultaneously all the different glucose precursors in differ-
ent nutritional and physiological conditions. Relationships
between net hepatic precursor uptake and glucose release
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Carbohydrate digestion and nutrient fluxes
9
NSR glucose (mmol C / h per kg BW)
8
7
6
5
4
3
2
1
0
20
0 1 2 3 4 5 6 7 8 9
NPA precursors (mmol C / h per kg BW)
Figure 6 Relationships between estimated net portal appearance (NPA)
of glucogenic precursors and observed net splanchnic release of glucose:
raw data. After Loncke (2009).
are usually studied separately for each precursor. Propionate
is largely metabolized in the liver (from 0.08 to 1.79 mmol/h
per kg BW depending on the feeding level and nature
of diet), with 85% to 100% of net portal appearance being
taken up (Majdoub, 2002), 91% on average based on
empirical relationships (Loncke, 2009). The liver highly con-
tributes to prevent the systemic toxicity of propionate. A
fixed conversion rate of propionate into glucose is used in
Molly (Baldwin et al., 1987a) and in the model of Martin and
Sauvant (2007). However, increased availability of propio-
nate does not ensure increased hepatic glucose synthesis
(Majdoub et al., 2003; Ortigues-Marty et al., 2003b). A
subsequent dynamic model of liver metabolism clearly sug-
gested that in vitro glucose production approaches satura-
tion as propionate supply increases (Baldwin and Freetly,
1995). The quantitative contribution of AAs to hepatic glu-
coneogenesis has been difficult to evaluate. A majority of
results is based on net a-amino-nitrogen fluxes, whereas
only gluconeogenic AAs are involved (Hanigan et al., 2004)
and their hepatic supply and metabolism does not strictly
depend on intestinal absorption but also from metabolism
in the different tissues. Their contribution varies with the
balance between availability in gluconeogenic precursors,
whole body glucose demand and utilization as well as
whole body AA demand (Kraft, 2009). During body store
mobilization as in feed restriction or lactation, contribution
of endogenous precursors (in particular AAs from muscle
proteolysis) increases (Lomax et al., 1986). It is also the case
when glucose demand increases, such as after phlorizin
treatment of lactating cows (Overton et al., 1999). Con-
versely when protein anabolism increases after growth
hormone infusion (Knapp et al., 1992), AAs are spared for
protein synthesis. Recently, dietary deficits in PDI or ME (by
20% to 23%) reduced net hepatic glucose release in growing
lambs by 41% and 33%, respectively. Sparing of AAs or
adjustment of their hepatic metabolism to modifications
in whole body protein anabolism were probably involved
1069
 Nozie`re, Ortigues-Marty, Loncke and Sauvant
(Kraft, 2009; Loncke et al., 2009a). Finally, L-lactate, another
potentially important precursor of hepatic gluconeogenesis
can be either largely taken up (up to 1.94 mmol/h per kg BW)
or released (up to 0.11 mmol/h per kg BW) by the liver
(Loncke, 2009). Its potential contribution appears extremely
variable (from 7% to 44%; Krehbiel et al., 1992). Little can
be further gained by the study of individual precursors.
Consequently, an attempt has been made to elaborate
empirical relationships between the net hepatic uptake of
the summed precursors (after prediction of missing values,
Loncke et al., 2009b) and net hepatic glucose release
(Loncke, 2009). Preliminary results suggest that net hepatic
glucose release increases with precursor availability, and
that this relationship is subject to several influent factors
which remain to be quantitatively established (Figure 6 and
Loncke, 2009).
Conclusion
Mechanisms and factors involved in site, extent and rate
of carbohydrate digestion have been extensively studied
through the last decades, providing a considerable amount
of published data. The PDV and liver metabolism have
been less studied, but the amount of published results is now
substantial. Hence, despite the improved mathematical
representation of physiological mechanisms enlightened by
these experimental efforts, it should be recognized that the
ability of published mechanistic models to predict nutrient
fluxes seems to remain poor. The development of appropriate
statistical methods of meta-analyses applied to the large
corpus of published data gathered in bibliographic databases
and carefully treated by adequate statistic tools, yielded
promising results. Beyond the quantitative integration of
knowledge in terms of response laws, important biological
properties of system may emerge from this approach. For
example, whereas it appears that representation of fluxes
from lumen to portal blood may be largely restricted to
action-mass laws, fluxes through the liver appear to involve
both push and pull driving forces, that empirical modelling
helped to dissociate. The potential synergy between empirical
and mechanistic modelling should be largely useful to progress
towards more accurate mechanistic models, and develop-
ment of multi-objectives feed evaluation systems based on
nutrient fluxes.
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