Nutritional and Health Benefits of Inulin and Oligofructose

The Application of Ecological Principles and Fermentable Fibers to Manage

the Gastrointestinal Tract Ecosystem1
Randal K. Buddington2 and Evan Weiher
Department of Biological Sciences, Mississippi State University, Mississippi State, MS 39762

ABSTRACT Because diet can influence the structure and functions of the gastrointestinal tract, there are
opportunities for using diet as a ‘‘management tool’’ to affect the resident microbiota. Fermentable fibers increase
the densities of beneficial bacteria and stimulate growth and functions of the healthy intestine. Recent findings
show that after acute diarrhea, the use of an oral electrolyte solution with the fermentable fiber oligofructose
accelerates recovery of beneficial bacteria, reduces the relative abundance of detrimental bacteria, stimulates
mucosal growth and enhances digestive and immune functions. This review will focus on how the principles of
stream ecology can be applied to better understand the distribution of bacteria along the length of the gastroin-
testinal tract, the effect of diarrhea on the gastrointestinal ecosystem and how fermentable fibers can be used as
a ‘‘management tool’’ to promote gastrointestinal health in normal states and during recovery from diarrhea. J.

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Nutr. 129: 1446S–1450S, 1999.

KEY WORDS: ● gastrointestinal ● bacteria ● diet ● ecosystem ● fiber ● oligofructose ● inulin

Gastrointestinal health and the relations with diet and the
resident bacteria are of growing concern (Kelly et al. 1994).
Although diet is known to influence the healthy intestine,
much less is known about the responses to diet during disease
states. Diarrhea, particularly chronic forms with associated
enteritis, disturb intestinal structure, functions and the resi-
dent bacteria, and often lead to secondary systemic infections
and malnutrition. The effect of diarrhea is greatest for infants
and young farm animals because they suffer the highest inci-
dences of morbidity and mortality. In light of this, there is a
need to develop more effective nutritional and therapeutic
approaches that will accelerate recovery of the gastrointestinal
tract (GIT).
The GIT of mammals has several regions that can be
considered as distinct habitats with assemblages of microor-
ganisms that are adapted to local physical, chemical and biotic
characteristics. Although the GIT meets the general tenets of
an ecosystem, as proposed by Tansley (1935), the use of the
term ecosystem has been questioned (Santini and Palka 1997).
Whether or not the GIT is an ecosystem is not as important as
the application of ecological principles to understand the
complex and poorly understood interactions among dietary
inputs, functions and resident organisms of the GIT, and the
implications to health. It is appropriate to view the GIT as an
ecological system and that by applying ecological principles, a
1
Presented at the conference Nutritional and Health Benefits of Inulin and
Oligofructose held May 18 –19, 1998 in Bethesda, MD. This symposium was
supported in part by educational grants from the National Institutes of Health
Office of Dietary Supplements, the U.S. Department of Agriculture and Orafti
Technical Service. Published as a supplement to The Journal of Nutrition. Guest
editors for the symposium publication were John A. Milner, The Pennsylvania
State University, and Marcel Roberfroid, Louvain University, Brussels, Belgium.
2
To whom correspondence should be addressed.
better understanding of the distributions and interactions of
organisms can be achieved.
The principles of stream ecology are appropriate and very
relevant for determining whether dietary inputs, particularly
fermentable fibers, can be used to manage the GIT ecosystem
in health and for accelerating recovery from disease states such
as diarrhea. The following sections will describe ecosystem
concepts with an emphasis on river ecosystems and the simi-
larities shared with the GIT of mammals. We focus on the
physical and chemical features of stream systems and the GIT,
and their relations with the biological components. Subse-
quent sections characterize disturbances of the GIT caused by
diarrhea and how fermentable fibers may be useful for accel-
erating recovery. A concluding section presents our perspec-
tives. We did not set out to provide an exhaustive review of
the literature. Instead, we selected publications that will allow
readers to become familiar with the relevant principles of
ecology. It is our hope that readers will recognize that an
interdisciplinary approach will be essential for understanding
the complex relations between diet and the GIT ecosystem.
Ecosystem concepts and river systems
The ecosystem concept has been attributed to Tansley
(1935), and there have been various refinements since then.
Ecosystems were originally described as including biotic and
abiotic components, which constitute structural elements,
whereas the flow and cycling of energy and matter that main-
tain the ecosystem are considered functional elements (Aber
and Melillo 1991, Odum 1971). Studies of ecosystems usually
focus on either the movement of energy and matter among the
different components (Odum 1971 and 1968) or on the feed-
ing behaviors of the organisms (Pimm 1982). Recent studies
have revealed interesting relations among the types (i.e., di-

0022-3166/99 $3.00 © 1999 American Society for Nutritional Sciences.

1446S
 DIETARY MANAGEMENT OF THE GIT ECOSYSTEM
versity), densities and functional roles of organisms and the
functional components of ecosystems (Hooper and Vitousek
1997, Schulze and Mooney 1994, Tilman et al. 1997).
River ecosystems are continua with a series of changes in
structural and functional elements (Cummins 1974). This is
immediately obvious when headwaters of rivers are compared
with the eventual outflow into the ocean. The changes along
the continuum result in a series of broad divisions (e.g., upper,
middle and lower sections), with the changes between each
division ranging from gradual to very abrupt.
Usually the upper sections of rivers have high water veloc-
ity, are heterotrophic and are well oxygenated. Many, but not
all components of the biota are dependent on allochthonous
organic inputs (Wallace et al. 1997). The wider middle regions
tend to have slower water movement, are autotrophic and
have high species richness (diversity is usually maximum
here). The lower regions are again heterotrophic and are
characterized by large volumes of slowly moving water with
high sediment levels and low oxygen content; they have lower
species diversity than the mid-region.
The hydrologic regime is a critical determinant of the
structure and functions of a river ecosystem (Angradi 1997,
Dynesius and Nilsson 1994, Naiman and Decamps 1997, Nils-
son et al. 1991). The disturbances caused by floods create
heterogeneity by slowing competitive exclusion and by pro-
ducing microhabitats for regeneration. Corresponding with
this, the frequency and magnitude of flooding are important
factors influencing stream ecosystems and the recovery time
(Fisher et al. 1999). Seasonal, tidal and other small floods are
considered necessary for maintaining the health and diversity
of river ecosystems (Dynesius and Nilsson 1994, Nilsson et al.
1991). Larger floods are less frequent, but have major influ-
ences on ecosystem structure that effectively ‘‘reset’’ the eco-
system back to an earlier successional stage (Angradi 1997,
Auble et al. 1994, Toner and Keddy 1997).
The water column of rivers is separated from the terrestrial
ecosystem by the riparian zone. This component of rivers can
be considered as a semipermeable membrane that regulates the
exchange of materials between aquatic and terrestrial ecosys-
tems (Naiman and Decamps 1997). The riparian zone harbors
a diverse mixture of aquatic and terrestrial characteristics and
can act as a refuge for some organisms during floods. However,
the riparian zone is particularly sensitive to environmental
disturbances (Naiman and Decamps 1997).
The ability of ecosystems to resist invasion by exotic (non-
native) species is of great interest. Although invading exotic
species can reduce diversity, only rarely are native species
completely removed or replaced (Mooney and Drake 1986,
Planty-Tabacchi et al. 1996). Interestingly, the very factors
that are thought to promote high diversity (e.g., frequent,
small disturbances, moderate resource limitation) make an
ecosystem inherently more susceptible to invasion (Lodge
1993, Planty-Tabacchi et al. 1996).
It is important from ecological and management perspec-
tives to restore river ecosystems to the ‘‘natural state’’ after a
disturbance. In general, ecological restoration is based on the
maintenance and restoration of ecological processes. Return-
ing the hydrologic state (rate and variability of flow) to ‘‘nor-
mal’’ is necessary for recovery of ecosystem structure and
function. Thereafter, several strategies can be used to hasten
the process for the resident organisms. Pesticides have been
used infrequently if the recovery of a system is hindered by the
invasion of an exotic species, but this management tool is
considered as a last resort. More commonly, native species that
have been suppressed or extirpated are reintroduced in an
attempt to hasten their recovery. Another set of management
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tools includes manipulating the hydrology and adjusting
chemical characteristics.
The gastrointestinal tracts of mammals as ‘‘rivers’’
The abiotic characteristics. The various GIT regions
have different structural and functional elements that provide
a continuum of habitat types. The differences between adja-
cent regions can be dramatic (stomach vs. small intestine) or
gradual (e.g., jejunum vs. ileum). The upper reaches of the
GIT river system originate at the pyloric sphincter, much the
way many river systems originate from a lake or reservoir.
Regulating the tonicity of the pyloric sphincter allows con-
tents of the stomach to enter the intestine, much as dams
regulate the flow of water into rivers.
Digesta move at a higher velocity in the proximal small
intestine, just as the headwaters of rivers do, and the digesta
have a higher oxygen content than those in more distal
segments. Initially, composition of the digesta is determined
largely by dietary inputs and secretions from the stomach,
intestine, pancreas and gall bladder. As digesta proceed dis-
tally, flow rates and oxygen content decline, and the compo-
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sition changes as a result of digestive processes (hydrolysis and
absorption) and microbial metabolism. The ileocolonic junc-
tion regulates the flow of digesta into the colon (Faussone-
Pellegrinni et al. 1993), and when it is removed, such as in
ileostomy patients, digesta move faster. The contents of the
colon move even more slowly, have a higher dry matter
content (i.e., suspended solids) and are virtually anaerobic.
The mucosa of the GIT is much like the riparian zone of
rivers in that it effectively ‘‘traps’’ nutrients and transfers them
to the organism. It is effectively a semipermeable membrane
that acts as an interface that effectively regulates the exchange
of materials between the organism and the lumenal contents.
The mucosa is metabolically very active (Cant et al. 1996) and
influences the composition of the digesta by its secretory and
digestive functions. Furthermore, the secretions and the pro-
teins of the brush border membrane influence the adherence
and metabolic activities of bacteria (Kelly et al. 1994). There
is also regional variation in mucosal architecture. The villi
shorten from the proximal to distal small intestine and are
barely present in the colon. This influences the amount of
surface area available for digestion and bacterial attachment,
as well as the depth of the unstirred layer.
The biotic components. The .400 different species of
bacteria from numerous genera that can be recovered from the
GIT of most mammals include both resident species and those
that are transient (Simon and Gorbach 1986). On the basis of
their interactions with the host and their metabolic activities,
the different bacteria can be further categorized into those that
are perceived as being beneficial and those that have the
potential of detrimentally influencing the host (Gibson and
Roberfroid 1995). Although the importance of the bacteria
resident in the GIT in health and disease is well recognized
(Simon and Gorbach 1987), little is understood about the
complex interactions between the host and the bacteria, and
the implications for health and disease (Bry et al. 1996).
Just as biotic components vary in the different segments of
rivers (horizontal zonation), the assemblages of bacteria differ
among regions of the GIT. Bacterial densities increase from
the stomach to the colon. As with any ecosystem, the distri-
bution and abundance of organisms in the GIT are not static.
This is evident from the different densities and metabolic
activities of bacteria in subjects fed different diets (Moore et
al. 1987) and in patients with short-bowel syndrome (Kaneko
et al. 1997).
1448S SUPPLEMENT
The qualitative and quantitative differences in bacteria
resident in the different GIT regions probably reflect adapta-
tion of bacteria to specific environmental conditions. This is
evident from the increasing proximal to distal abundance of
obligate anaerobes, corresponding with declining oxygen ten-
sions and increasing redox potentials. The restriction of Hel-
icobacter pylori to the gastric regions provides another example.
Additionally, if the GIT is truly similar to a river, then the
lower small intestine should have the highest species diversity,
but not necessarily the highest density, and may be more
susceptible to invasion by exotic (pathogenic) species. This
interesting possibility has not been adequately explored.
In addition to the horizontal zonation of bacteria and other
organisms along the GIT, there are vertical gradients of species
distribution. The mucosa, like the riparian zone of rivers,
provides an environment that differs physically and chemically
from the digesta in the lumen. It is not surprising that bacterial
populations associated with the mucosa differ from those of the
digesta. It is also recognized that the bacteria associated with
the mucosa are likely to have a greater potential to influence
the host than those present in the lumen (Poxton et al. 1997).
Moreover, the adherent bacteria influence mucosal and en-
terocyte architecture, the expression of genes and processing of
gene products (Bry et al. 1996, Hill and Cowley 1989). Despite
these interactions, much less is known about the assemblages
of mucosal bacteria that are attached to the mucosa than those
of the lumenal contents.
Dietary management of the GIT ecosystem
There is increasing interest in using dietary inputs to man-
age the GIT microecology (Collins and Gibson 1999). How-
ever, the influences of diet are complex; they involve several
possible mechanisms of action, all of which are not yet well
understood. Dietary inputs can serve as substrates for the
bacteria. Some components of the diet can alter the assem-
blages of bacteria, just as adding certain fertilizers to aquatic
systems can change the composition and interactions of the
resident organisms. For example, some products of the hydro-
lysis of casein stimulate the proliferation of bifidobacteria
(Poch and Bezkorovainy 1991). Moreover, the fermentation of
dietary inputs by lactic acid bacteria results in short-chain fatty
acids and other metabolites that reduce pH and inhibit the
growth of many species of bacteria (Russell and Diez-Gonzalez
1998). Other dietary components can reduce the ability of
some bacteria to adhere to enterocytes (Oyofo et al. 1988).
Alternatively, diet can indirectly influence the bacteria by
modulating GIT structure and associated functions. The re-
sulting changes in the physical and chemical characteristics of
the environments in the different GIT regions can be expected
to alter the densities, relative proportions and metabolic char-
acteristics of the resident bacteria.
Fermentable fibers, such as oligofructose and inulin, selec-
tively increase the abundance of lactic acid bacteria while
decreasing the percentages of potential pathogens and putre-
factive bacteria in several species (Gibson and Wang 1994,
Wang and Gibson 1993, Williams et al. 1994). They also
influence the metabolic activities of the bacteria (Buddington
et al. 1996).
There is less known about the responses of GIT structure
and associated functions to fermentable fiber. Adding oligo-
fructose and beet pulp, which include fermentable compo-
nents, to the diet of dogs resulted in longer intestines with
more surface area and greater mucosal mass compared with the
intestines of dogs fed a diet with cellulose, which is poorly
fermented (Buddington et al. 1999). Moreover, inclusion of
fermentable fiber into a diet for dogs caused an increase in
rates of active glucose transport by the apical membrane
(McBurney et al. 1998), and the responses were more profound
in the proximal small intestine (Buddington et al. 1999).
Similar responses occurred in mice fed diets with oligofructose
and inulin compared with those fed a diet with cellulose (our
unpublished data).
Because mammals are unable to digest fermentable fibers,
the increases in intestinal dimensions and functional capaci-
ties provide evidence for interactions among the diet, the
resident bacteria and GIT characteristics. Recent findings in-
dicate that bacterial fermentation of fiber triggers the release of
glucagon-like peptides 1 and 2, gastric inhibitory peptide and
possibly other enteric hormones. These then stimulate muco-
sal growth and upregulation of transport processes in the
proximal intestine (McBurney et al. 1998). Therefore, the
GIT bacteria, much like many organisms in other ecosystems,
are able to modify their environment (Hill and Cowley 1990).
By doing so, they can act like the feedback agents described for
other ecosystems (Jones et al. 1994, Pahl-Wostl 1995). The
GIT ecosystem is unique in that the bacteria are able to trigger
changes ‘‘upstream’’ via neuroendocrine responses, which are
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particularly evident in diarrhea.
The impact of diarrhea on the GIT
Periodic small increases in the volume and flow rates of
digesta, such as those associated with meals, are normal and
appear to be essential for maintaining GIT structure and
functions. This is similar to river systems. It is the larger-scale
disturbances caused by diarrhea that can detrimentally influ-
ence the GIT and the host. Disruption of mucosal barrier
functions during severe diarrhea increases the risk of bacterial
translocation, subsequent sepsis and overstimulation of im-
mune system functions (Fink 1994).
Species with the shortest generation times recover faster
after floods. However, such species are often considered as
‘‘weeds’’ and are less desirable. The same appears to be true for
the GIT after diarrhea (Oli et al. 1998). Antibiotics also
disturb the GIT bacterial assemblages (Jackson et al. 1989),
and this can affect the structure and functions of the mucosa.
The changes in the microenvironment can lead to the prolif-
eration of some pathogens, such as Clostridium difficile (Wilson
1993).
Dietary management of the GIT during recovery from
diarrhea
The depletion of fluids and electrolytes caused by diarrhea
is of particular importance during infancy. Although oral
rehydration therapy has proven successful for replenishing
fluids and electrolytes, commercially available oral electrolyte
solutions do not address the disturbances to the structure and
functions of the GIT, and the resident microbiota.
There are two therapeutic strategies that do not involve
antibiotics that can be applied to accelerate the recovery of
the GIT ecosystem and restore the ‘‘normal’’ bacterial assem-
blages. The first uses probiotics to ‘‘seed’’ the GIT with bac-
teria perceived as beneficial and by doing so, competitively
exclude pathogens (Stavric et al. 1991). The probiotic ap-
proach alters the composition and metabolism of the GIT
bacterial assemblages (Djouzi et al. 1997, Jiang and Saviano
1997) and can alter the transfer of nutrients from the intestine
to the blood (Rychen and Nunes 1995). However, the benefits
are transient, lasting only for as long as the time the bacteria
are administered. Usually, the probiotic bacteria are not able
 DIETARY MANAGEMENT OF THE GIT ECOSYSTEM
to establish and maintain significant populations in the GIT.
As a result, they rapidly diminish after the probiotic is stopped,
probably due to competitive exclusion by species already
present in the GIT and adapted for existing conditions.
The prebiotic approach uses diet components to selectively
encourage the growth of beneficial species, and although it is
not as frequently used, this approach is gaining in popularity.
The ability to selectively encourage the proliferation of ben-
eficial bacteria is well established for oligofructose and inulin
(Gibson et al. 1995) as well as other fermentable fibers (e.g.,
lactosucrose; Kumemura et al. 1994). Recently, there has been
interest in using fermentable fiber as a management tool that
will accelerate recovery of the GIT during and after diarrhea.
One of the desired consequences of adding fermentable fiber to
oral electrolyte solutions is the decline in the relative abun-
dance of potential pathogens, even though they tend to re-
cover faster after diarrhea (Oli et al. 1998). Other potential
benefits include production of metabolites that are beneficial
to the host (e.g., short-chain fatty acids and vitamins) or
reduce the growth of pathogens (Wang and Gibson 1993), and
faster recovery of mucosal mass and digestive capacities, pos-
sibly including immune functions. The influence of ferment-
able fiber on the densities of nutrient transporters may have
profound clinical relevance. The apical sodium-dependent
glucose transporter, SGLT-1, appears to have a dual function
as water carrier (Loo et al. 1996), and this may be shared by
transporters for other nutrients. Therefore, any therapeutic
approach that increases densities of nutrient transporters may
enhance rehydration.
CONCLUSIONS AND PERSPECTIVES
The diversity of mammalian feeding habits are matched by
the variation in structural and functional features of the GIT
(Stevens 1988). GIT characteristics are set by genetic deter-
minants that match digestive abilities with the natural diet.
The bacterial assemblages found in the mammalian GIT are
also highly variable and species specific. For example, bi-
fidobacteria are not present at significant densities in all mam-
mals (Buddington and Sunvold 1998). Furthermore, the abil-
ity of different species of bifidobacteria to bind to enterocytes
varies among species of mammals. This may influence the
competitive interactions between beneficial and pathogenic
bacteria (Bernet et al. 1993).
Even the bacteria present in GIT ecosystems of closely
related individuals can differ (Hinton and Linton 1987), just
as rivers differ in abiotic and biotic characteristics, even when
they are located in the same geographical area. As a conse-
quence, a successful management tool for one species, or even
individual, may not provide the same benefits for another.
Therefore, it can be predicted that adding fermentable fiber to
the diet will cause varying responses among individuals, spe-
cies, life history stages and states of health.
In clinical settings, it is difficult to obtain samples from the
various regions of the GIT, and diagnoses are generally limited
to bacteriologic analyses of stool samples. However, bacterial
populations and metabolism vary spatially along the GIT, and
the interactions that occur in proximal regions of the GIT
(e.g., small intestine) among the bacteria, the host and dietary
inputs may have a greater effect on health than what is evident
from stool samples. For example, bacterial responses to fer-
mentable fiber appear to be greater in the proximal bowel than
in the colon (McBain and MacFarlane 1997). Corresponding
with this, we have found that the influences of oligofructose
on bacterial populations are more pronounced in the small
intestine and proximal colon of suckling pigs compared with
1449S
fecal samples (unpublished data). As a consequence, stool
samples, like the water draining into the ocean, can provide
only limited insights about events and processes occurring
‘‘upstream’’ in more proximal regions of the GIT. Therefore,
just as ecologists use key indicators to monitor ecosystems,
there is a need to identify species of bacteria or other factors
that can be examined in stool samples and that will provide
insights about events and processes throughout the GIT.
The ‘‘age’’ of an ecosystem also influences responses to
floods and management strategies. It is uncertain if the age of
the GIT is similarly an important determinant of the responses
to dietary inputs. During the first weeks and months after
birth, digestive functions mature (e.g., onset of gastric secre-
tion, changes in rates of absorption for various nutrients),
which alters GIT microenvironments and coincides with shifts
in the composition of the bacterial assemblages (Swords et al.
1993). Although infants are at greater risk from complications
caused by diarrhea than adults, it is unknown if this applies to
the developing GIT.
If more effective management tools and protocols (e.g.,
prebiotics, probiotics, synbiotics or antibiotics) are to be de-
veloped, future research must be directed at answering several
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questions. These include, but are not restricted to, identifying
the key environmental factors that control the composition of
the GIT microbiotic community, determining species diversity
along the GIT and the relations with stability and resistance to
invasion, and understanding which bacterial species should be
managed to promote optimal health and where in the GIT
such management strategies should be targeted. Although the
lactic acid bacteria are considered as beneficial, it is of impor-
tance to decide which species or strains provide the most
benefits for various hosts and what the benefits are. It is our
contention that applying relevant ecological theory for river
systems to the GIT will facilitate understanding about how
fermentable fibers and other dietary components can be used
to manage the GIT in health and disease, as well as to define
potential limitations.
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