Engineering 3 (2017) 716–725

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Engineering
j o u r n a l h o m e p a g e : w w w . e l s e v i e r. c o m / l o c a t e / e n g

Research
Animal Nutrition and Feed Science—Review

Nutritional and Metabolic Consequences of Feeding High-Fiber

Diets to Swine: A Review
Atta K. Agyekum a, C. Martin Nyachoti b,*
a
Prairie Swine Center Inc., Saskatoon, SK S7H 5N9, Canada
b
Department of Animal Science, University of Manitoba, Winnipeg, MB R3T 2N2, Canada

a r t i c l e i n f o a b s t r a c t

Article history: At present, substantial amounts of low-cost, fibrous co-products are incorporated into pig diets to reduce
Received 1 March 2017 the cost of raising swine. However, diets that are rich in fiber are of low nutritive value because pigs cannot
Revised 18 April 2017 degrade dietary fiber. In addition, high-fiber diets have been associated with reduced nutrient utilization
Accepted 20 April 2017
and pig performance. However, recent reports are often contradictory and the negative effects of high-fiber
Available online 24 May 2017
diets are influenced by the fiber source, type, and inclusion level. In addition, the effects of dietary fiber
on pig growth and physiological responses are often confounded by the many analytical methods that are
Keywords: used to measure dietary fiber and its components. Several strategies have been employed to ameliorate the
Gut physiology
negative effects associated with the ingestion of high-fiber diets in pigs and to improve the nutritive value
High-fiber diets
of such diets. Exogenous fiber-degrading enzymes are widely used to improve nutrient utilization and pig per-
Nutrient utilization
Pigs formance. However, the results of research reports have not been consistent and there is a need to elucidate
Sow welfare the mode of action of exogenous enzymes on the metabolic and physiological responses in pigs that are fed
high-fiber diets. On the other hand, dietary fiber is increasingly used as a means of promoting pig gut health
and gestating sow welfare. In this review, dietary fiber and its effects on pig nutrition, gut physiology, and sow
welfare are discussed. In addition, areas that need further research are suggested to gain more insight into
dietary fiber and into the use of exogenous enzymes to improve the utilization of high-fiber diets by pigs.
© 2017 THE AUTHORS. Published by Elsevier LTD on behalf of the Chinese Academy of Engineering and
Higher Education Press Limited Company. This is an open access article under the CC BY-NC-ND
license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

1. Introduction are the major component of dietary fiber.

In general, diets that are rich in dietary fiber have a lower nutri-
Conventional swine diets contain substantial amounts of cere- tive value for monogastric animals, including pigs, because these
al grains (e.g., corn and wheat) and protein supplements such as animals’ digestive enzymes are not suited to degrading non-starch
soybean meal to provide pigs with the energy and nutrients they polysaccharides [2]. The ingestion of high-fiber diets also has the
require. However, recent trends in the demand and supply of these potential to adversely affect energy and nutrient utilization and
conventional feedstuffs require swine producers around the world consequently result in lower pig performance [3–6]. Therefore, only
to seek low-cost alternatives such as cereal co-products from the a minimal level of fiber is typically included in diets fed to swine.
bio­fuel and milling industries to feed their pigs, in order to reduce However, dietary fiber has received a considerable amount of atten-
feed costs [1]. The majority of these co-products have a high en- tion in recent years because some fiber components have beneficial
ergy and nutrient content but are fibrous in nature. When fibrous effects on pigs when fermented in the intestine [7,8], and can also
co-products are incorporated into pig diets, the carbohydrate com- affect satiety and animal behavior [9,10].
position inevitably changes from a high-starch diet toward a diet This review discusses dietary fiber, its effects in pig nutrition, and
containing less starch and more non-starch polysaccharides, which the mechanisms involved in its utilization. Furthermore, the effects

* Corresponding author.
E-mail address: [email protected]

http://dx.doi.org/10.1016/J.ENG.2017.03.010
2095-8099/© 2017 THE AUTHORS. Published by Elsevier LTD on behalf of the Chinese Academy of Engineering and Higher Education Press Limited Company.
This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
 A.K. Agyekum, C.M. Nyachoti / Engineering 3 (2017) 716–725 717

of dietary fiber on pig gut health and sow welfare are discussed. a better control of the fermentation process that takes place in the
Finally, areas that require further research to expand our knowledge pig’s gut and could assist nutritionists in predicting the energy con-
on fiber and some of the strategies used to improve fiber utilization tribution and prebiotic effect of a diet or feedstuff.
in pigs are outlined.
2.2. Analytical methods for characterizing dietary fiber
2. Dietary fiber
Several methods exist for characterizing the dietary fiber com-
2.1. Definition and classification ponent of feeds and feedstuffs; the choice of an analytical method
depends on the aims of the investigator [12,17,18]. Based on how the
Plant carbohydrates can be classified as sugars, disaccharides, fibrous remnants are isolated and measured, dietary fiber analyti-
oligosaccharides, or polysaccharides (i.e., starch and non-starch cal methods are classified into three groups: chemical-gravimetric,
polysaccharides). Sugars, oligosaccharides, and starch are found in enzymatic-gravimetric, and enzymatic-chemical methods. The
the interior of the plant cell, whereas non-starch polysaccharides, numerous fiber analytical methods and the variability among these
together with lignin, are the main constituents of the plant cell methods and among the obtained results make it rather difficult to
walls, and are called dietary fiber. The term “dietary fiber” has sev- compare information from different studies [19]. However, methods
eral definitions; however, all these definitions have limitations be- that categorize dietary fiber into soluble and insoluble components
cause plant cell wall components are variable and complex in their seem to provide the most accurate interpretation of study results.
chemical and physical composition and in their metabolic effects. In what follows, the analytical methods most commonly used for
The initial definition of dietary fiber as “the sum of lignin and cell measuring dietary fiber are briefly discussed.
wall polysaccharides that are resistant to enzymatic hydrolysis in
the digestive system of man” was coined by Trowell et al. [11] in re- 2.2.1. Crude fiber method
lation to human medicine. However, this definition of dietary fiber Crude fiber analysis is a chemical-gravimetric method that is part
is also applicable to other monogastric animals, such as pigs [12]. of the Weende proximate analysis used for feed ingredients [19]. It
The Codex Alimentarius Commission [13] finalized the definition was introduced to differentiate between carbohydrate that is “avail-
of dietary fiber as “carbohydrate polymers with 10 or more mono- able” and carbohydrate that is “unavailable” for digestion. The aim
meric units, which are not hydrolyzed by the endogenous enzymes of crude fiber analysis is to mimic the digestive actions of the gastric
in the small intestine of humans.” Dietary fiber also includes any and pancreatic secretions by boiling a feed with dilute acid followed
polysaccharides that reach the hindgut, such as resistant starch and by a dilute alkali solution [19]. The crude fiber analytical method is
oligosaccharides, which constitute plant cell contents and include very robust and reproducible within and among laboratories; how-
fructo-oligosaccharides. The main constituents of the plant cell wall ever, there is incomplete recovery of cellulose, hemicellulose, and
polysaccharides are cellulose, hemicellulose, and pectin. lignin. Therefore, crude fiber is not considered to be an acceptable
Cellulose is a linear polymer of glucose units with β-(1→4) link- definition for dietary fiber and is not suitable for characterizing the
ages, whereas pectin consists mainly of glucuronic acid units joined fiber component in pig feed. However, many regulatory agencies use
in chains by α-(1→4) glycosidic linkages. The most abundant organic crude fiber for quality control purposes and for regulating the mini-
substrate on earth, cellulose forms the main structural component mum fiber content allowed in a feed.
of plant cell walls. Hemicelluloses are a complex matrix of polysac-
charides that include xylose, arabinose, galactose, mannose, glucu- 2.2.2. The detergent (Van Soest) methods
ronic acid, and β-glucans. Lignin is a phenolic polymer that anchors The detergent methods, which are chemical-gravimetric proce-
the cell wall polysaccharides and is not digested or fermented by dures, were developed by Van Soest in the 1960s. These methods
porcine intestinal enzymes or bacteria, respectively [2,7,8,14]. employ detergents to progressively extract neutral detergent fiber
Non-starch polysaccharides can be classified as insoluble or sol- (NDF), acid detergent fiber (ADF), and acid detergent lignin (ADL)
uble based on their solubility in water or weak alkali [12]. Insoluble [18,19]. The NDF procedure recovers the insoluble components of di-
non-starch polysaccharides include cellulose and some hemicellulo- etary fiber (i.e., cellulose, hemicellulose, and lignin) after digesting a
ses, and soluble non-starch polysaccharides include pectins, gums, feed or ingredient in a solution at a neutral pH. Thus, the nutritional
and β-glucans. Soluble non-starch polysaccharides are more rapidly advantages of the NDF procedure are that it is able to approximate
fermented in the gastrointestinal tract of the pig than insoluble the insoluble dietary fiber fraction of a feedstuff and that its results
non-starch polysaccharides [7,12]. For insoluble non-starch polysac- are reproducible [19]. The ADF procedure recovers mainly cellulose
charides, little or no fermentation occurs in the upper gut; rather, and lignin by digesting a diet or feedstuff in a solution at an acidic
fermentation remains low in the hindgut of pigs [15]. pH [18], whereas the ADL recovers lignin using sulfuric acid. A more
Dietary fiber (or non-starch polysaccharide fractions) is currently accurate estimate of hemicellulose and cellulose is obtained when
classified based on physicochemical properties in order to provide the NDF, ADF, and ADL are determined sequentially using the same
more information on its metabolic and physiological activities. The sample [18].
physicochemical properties of dietary fiber that are relevant to pig The detergent procedures, although an improvement over the
nutrition include viscosity, hydration, and fermentability. Viscosi- crude fiber method, do not recover soluble dietary fiber (e.g., pec-
ty describes the dissociation of non-starch polysaccharides in the tins, gum, and β-glucans) [19]. Therefore, these procedures can
gastrointestinal tract to form high molecular weight viscous aggre- underestimate the total dietary fiber, especially for starchy feeds or
gates. Soluble fibers such as β-glucans, gums, or pectins increase ingredient samples, although probably not for cereal co-products,
digesta viscosity when ingested by pigs. Fermentability describes which have a high insoluble fiber concentration.
the ability of non-starch polysaccharides to be fermented by the
microflora harbored in the intestine. Soluble fiber is generally more 2.2.3. Total dietary fiber method
fermentable than insoluble fiber. The hydration properties are swell- The total dietary fiber method was introduced to overcome some
ing capacity, solubility, water-holding capacity, and water-binding of the pitfalls of the detergent procedure. The total dietary fiber
capacity [16]. The water-holding capacity of a fiber affects its fer- method is important for feedstocks intended for monogastric ani-
mentability. Thus, when physicochemical parameters are incorpo- mals, including pigs, with hindgut fermentation. This procedure em-
rated into pig feed formulation, they may provide nutritionists with ploys enzymes to simulate the processes that take place within the
718 A.K. Agyekum, C.M. Nyachoti / Engineering 3 (2017) 716–725

digestive tract [19], and may separate dietary fiber into soluble and weight [4]. Increasing the inclusion rate of distillers dried grains
insoluble fiber. The carbohydrates included in the definition of total with solubles from 0 to 20% in nursery pig diets [24] and from 0 to
dietary fiber include celluloses, hemicelluloses, oligosaccharides, 30% in growing pig diets [5] linearly decreased pig body weight, al-
lignin, pectins, and gums. Thus, total dietary fiber differs from non- though the diets were formulated to contain similar net energy and
starch polysaccharides because lignin is included in the definition. standard ileal digestibility amino acids. Results from some studies
The total dietary fiber method recovers more of the fibrous compo- [25,26] suggest that the decline in pig growth rate that occurs when
nents than the NDF method, although it does not recover oligosac- high-fiber diets are fed is generally limited to the growing period
charides that are soluble in aqueous ethanol. rather than the finishing period. Conversely, in some studies [27–29],
There are two major methods to this procedure: enzymatic-gravi- high-fiber diets had no adverse effects on pig performance in the
metric and enzymatic-chemical methods. The enzymatic-gravimetric growing or finishing phases, compared with the control.
methods are used to measure both insoluble and soluble fractions The abovementioned studies reported on various types of feeds
of dietary fiber; the AOAC Official Method 985.29 is the final version that were termed “high-fiber” diets, which contained varying
of these methods [20]. This procedure includes treatment of the amounts of ingredients (i.e., purified and natural fiber sources).
sample with enzymes to remove starch and protein, precipitation This may partly explain the varying responses to high-fiber diets in
of soluble fiber with aqueous ethanol, isolation and weighing of terms of pig growth, because different inclusion rates of high-fiber
the residue and, finally, correction for protein and ash in the resi- ingredients and fiber types will elicit different responses. Further-
due [19,21]. The enzymatic-chemical methods also use enzymes to more, the specific fiber components and analytical methods used to
remove starch, followed by precipitation of the soluble non-starch measure fiber differed in those studies. Thus, crude fiber, NDF, total
polysaccharides with aqueous ethanol. Thereafter, the neutral sugars dietary fiber, and non-starch polysaccharides cannot be used inter-
are quantified by gas-liquid chromatography or high-performance changeably as equal measures of dietary fiber when assessing the
liquid chromatography, and uronic acid is quantified by colorimetry effects of high fiber ingestion on pig performance.
[19]. Diets that are bulky due to the addition of fibrous feedstuffs have
The Uppsala and Englyst methods are the two most common been reported to depress feed intake in pigs due to gut fill [4,30,31].
enzymatic-chemical methods available. The Uppsala method quan- In gestating sows, early satiety due to the intake of high-fiber diets
tifies the non-starch polysaccharides portion as the sum of amylase- prevents certain stereotypies and thus is paramount to sow welfare
resistant polysaccharides, uronic acid, and lignin, whereas the Eng- [10], whereas in growing pigs, reduced feed intake is detrimental to
lyst method does not include lignin and resistant starch in the final performance. However, in growing-finishing pigs, feed intake does
value [22]. Although the total dietary fiber methods are an improve- not always decrease when the pigs are fed high-fiber diets. For ex-
ment over the detergent procedures, they are still time-consuming, ample, feed intake did not decrease in growing-finishing pigs that
laborious, and relatively expensive. were offered diets containing up to 30% cereal grain co-products
from the ethanol industry in several experiments [5,6,32–34]. In
3. Dietary fiber in pig nutrition pigs raised in a thermo-neutral environment, feed intake is typically
influenced by the diets’ energy content rather than by the bulki-
Starch and non-starch polysaccharides differ not only in chem- ness of the diet [35]. The addition of fibrous feedstuffs to pig diets
ical structure but also in the type of nutrients they supply. Starch dilutes the dietary energy content. Therefore, a decrease in dietary
digestion in the upper gut results in glucose, whereas non-starch energy content is typically associated with increased feed intake
polysaccharide degradation in the lower gut results in volatile fatty to compensate for the energy required to support the maintenance
acids [16,23]. In addition, pigs do not secrete the digestive enzymes and growth of pigs. Nonetheless, a period of adaptation to a fibrous
required to break down non-starch polysaccharides, whereas they diet is required before growing pigs are able to consume enough of a
do secrete the enzymes required to hydrolyze starch. Furthermore, high-fiber diet to compensate for the dietary energy dilution [35].
starch and non-starch polysaccharides differ in terms of their effects
on other nutrients in the digestion process and on the performance 3.2. Effects of fiber on nutrient digestibility
of pigs [16,23]. Several authors have reviewed aspects of high-fiber
diets in pig nutrition. Taken together, the available information sug- Pre-cecal and total tract nutrient digestibilities in pigs have been
gests that dietary fiber has both positive and negative effects on the reported to be negatively affected by high-fiber diets. Several mech-
pig. anisms have been put forward to explain the negative impact of
Most of the information on dietary fiber in pig nutrition has been high-fiber diets on nutrient digestion. In this context, soluble fiber
generated using purified fiber sources such as pectin, cellulose, and has been reported to increase digesta viscosity and thereby slow
guar gum, along with partially identified fiber from sources such as down the diffusion of the substrate and enzymes in the porcine
wheat bran [12], as opposed to information generated using natural small intestine, which hampers nutrient digestion and absorption
fibrous feedstuffs such as distillers dried grain with solubles. Natu- [3]. Indeed, it has been reported that soluble fiber from diets based
ral fibrous feedstuffs are usually composed of more than one fiber on purified guar gum, sugar beet pulp, oats, wheat, and barley in-
type; that is, they are composed of both soluble and insoluble fiber. creased digesta viscosity, leading to a reduction in nutrient digestion
Therefore, the effect of natural fibrous feedstuffs on the digestive [4,12,36]. On the other hand, insoluble fiber reduces digesta passage
physiology of pigs may not necessarily be similar to that of purified rate, thereby allowing less mixing time for digestive enzymes and
fiber. In the following sections, fiber effects on growing pigs are dis- dietary components [3]. For example, insoluble fiber from wheat
cussed in the context of fiber that has been obtained from purified bran, corn bran, and cellulose reduced digesta transit time in several
and natural sources. studies, leading to decreased nutrient digestibility [4,10,37,38]. How-
ever, the fiber in distillers dried grains with solubles (predominately
3.1. Effects of fiber on pig growth performance insoluble) had no effect on digesta transit time in the experiment
by Urriola and Stein [39]. This suggests that the effect of insoluble
The effect of high-fiber ingestion has generally been to reduce fiber on digesta transit time may vary among studies, and probably
pig growth rate. However, the reports obtained have often been con- depends on the presence of interfering factors that are likely to exist
tradictory. For example, feeding growing pigs diets containing either in fiber from natural feedstuffs. Nonetheless, insoluble non-starch
7% guar gum or 7% cellulose reduced growth rate and final body polysaccharides have been reported to decrease digesta transit time
 A.K. Agyekum, C.M. Nyachoti / Engineering 3 (2017) 716–725 719

in the hindgut, whereas digesta transit time in the small intestine is their production and a decrease in their reabsorption before the end
unaffected or reduced [3,37]. of the ileum, the result is decreased ileal nitrogen and amino acid
Diets that are rich in non-starch polysaccharides encapsulate nu- digestibility. Dietary fiber can also adsorb amino acid and peptides,
trients and thereby hamper their accessibility to digestive enzymes thereby withholding them from digestion in the small intestine [17]
for hydrolysis [3]. Ingestion of fibrous diets has been reported to and leading to decreased ileal nitrogen and amino acid digestibility.
reduce nutrient digestibility in pigs through increased endogenous
intestinal nutrient losses [3,7,17,40,41]. In addition, ingestion of fi- 3.2.3. Fiber effect on lipid digestion
brous diets leads to increased thickness of the unstirred water layer The effect of fiber on lipid digestibility has been investigated
adjacent to the intestinal mucosa, which can impair nutrient diges- extensively in pigs. Shi and Noblet [54] reported that ingestion of
tion and absorption [42]. high-fiber diets decreased lipid digestibility in pigs. Similarly, feed-
ing growing pigs cereal-based diets containing 20% or 40% wheat
3.2.1. Fiber effect on starch digestion bran decreased lipid digestibility [37]. Dietary fiber depresses lipid
Although endogenous carbohydrate-degrading enzyme activities digestibility through several mechanisms. For example, dietary
may be reduced by fiber ingestion [43], several studies [36,44,45] fiber can increase digesta passage rate and thereby limit the time
have reported that starch digestibility in pigs is not affected by required by digestive enzymes to digest dietary lipids [55,56]. Alter-
dietary fiber content, and that dietary starch is almost completely natively, dietary fiber can bind with bile salts in the duodenum and
digested at the end of the small intestine. The lack of a fiber effect render bile salts unavailable for the emulsification of dietary lipids.
on starch digestibility is suggested to be due to the relatively long This in turn requires the synthesis of additional bile salts from blood
length of the small intestine, which ensures that starch is digest- cholesterol and thereby lowers blood cholesterol [55,56].
ed efficiently before the end of the ileum [36]. However, Wenk [3] Reduction in lipid digestibility has been reported to be depend-
suggested that a fiber-rich diet may reduce digesta transit time and ent on the type of fiber. Soluble fiber increases digesta viscosity and
allow a greater amount of undigested starch to pass through the ile- thereby prevents substrate-enzyme interaction and decreases lipid
um. Indeed, Gao et al. [46] and Agyekum et al. [47] recently observed digestion, whereas insoluble fiber reduces digesta transit time in the
that the addition of 5% inulin or 30% distillers dried grains with digestive tract and thus increases lipid excretion in the feces [57].
solubles to a corn-soybean meal-based diet fed to growing-finishing However, not all studies have reported a negative effect of fiber-rich
pigs reduced ileal starch digestibility, probably due to increased ileal diets on lipid digestion. For example, the addition of wheat bran,
starch flow. Nonetheless, although overall starch digestibility may corn bran, soybean hulls, and sugar beet pulp to increase the fiber
not be affected by dietary fiber, the rate of starch digestion and ab- content of diets fed to pigs did not affect lipid digestibility relative
sorption decreases due to fiber ingestion [48,49]. to the control diet [38]. Kil et al. [58] also observed that the dietary
The decrease in the rate of starch digestion has been attributed inclusion of purified NDF (from Solka-Floc) did not affect lipid di-
to the luminal viscosity and nutrient-encapsulating effect of intact gestibility relative to the control. Conversely, Högberg and Lindberg
cell wall polysaccharides [48]. Soluble fiber appears to have a great- [45] reported that feeding growing pigs diets that contained the
er impact on starch digestion and absorption than insoluble fiber brans from oats, wheat, and rye increased lipid digestibility. Simi-
[49,50]. The reduction in starch absorption that occurs when pigs larly, Gao et al. [46] reported that the addition of 5% inulin or 5% so-
are fed fiber-rich diets may also be due to the decreased dietary dium carboxymethylcellulose (CMC) increased lipid digestibility in
starch load, in comparison with low-fiber diets, which are typically growing pigs. Agyekum et al. [47] also reported that adding 30% dis-
rich in starch. tillers dried grains with solubles to a growing pig diet had no effect
on ileal lipid digestibility, whereas fecal lipid digestibility tended to
3.2.2. Fiber effect on protein digestion increase. Fat or oil is typically added to fibrous diets to compensate
The literature contains a plethora of information on the effect for the energy-dilution effect of fiber. However, it has been shown
of fiber on protein digestion in pigs. In general terms, ingestion of that lipid digestibility increases when dietary lipid content increases
a fibrous diet reduces both ileal and total tract protein digestibility. [58]. Therefore, the above-mentioned studies showing that lipid di-
The reduction in ileal protein and amino acid digestibility due to gestibility increased irrespective of fiber content may be due to the
fiber ingestion has been reported to be associated with increased increased dietary lipid content that was intended to compensate for
endogenous and exogenous nitrogen and amino acid losses, where- the low energy content. Nonetheless, increasing dietary lipid con-
as increased microflora (bacterial protein) excretion in the feces is tent has also been reported to depress fiber digestibility [57]. Addi-
primarily responsible for the reduction in total tract protein digesti- tional studies are warranted to establish the role of fiber (i.e., form
bility observed in pigs [3,17,51]. and type) in lipid digestibility.
Endogenous ileal nitrogen and amino acid losses refer to the ni- Depression in lipid digestibility has been reported to be more
trogen or amino acids that are present in endogenously synthesized pronounced at the fecal level than at the end of the ileum [57].
proteins and that have not been digested and reabsorbed before Therefore, the values for hindgut lipid fermentation (calculated
reaching the end of the ileum [17,51]. These losses can be classified as total tract digestibility – ileal digestibility) are usually negative,
into basal loss, which is the minimum quantity of nitrogen and ami- indicating that dietary fiber intake may increase endogenous lipid
no acids that is inevitably lost in all diets, and specific losses, which synthesis by microflora in the hindgut of pigs. However, not all of
are influenced by dietary ingredient composition [51]. the studies mentioned above reported a net lipid synthesis in the
Concerning diet-specific ileal endogenous nitrogen and amino hindgut of pigs due to fiber ingestion. Thus, fiber ingestion did not
acid losses, several studies have reported that ingestion of fibrous result in net lipid synthesis in the studies by Kil et al. [58] and Gao et
diets increases the secretion of digestive enzymes and juices to ac- al. [46], whereas increased fiber intake did result in net lipid synthe-
commodate dietary fiber in the digestive tract. For example, Langlois sis in the studies by Shi and Noblet [54], Högberg and Lindberg [45],
et al. [52] reported that a diet containing 40% wheat bran increased and Agyekum et al. [47]. Kil et al. [58] and Gao et al. [46] used puri-
pancreatic juice and enzyme secretion in growing pigs. Increases fied dietary fiber sources (i.e., CMC, inulin, and Solka-Floc), whereas
in bile juice, mucin, and sloughed epithelial cells have also been Shi and Noblet [54], Högberg and Lindberg [45], and Agyekum et al.
reported to be due to fiber ingestion in pigs [17,41,53]. Digestive [47] used fiber from natural sources (i.e., cereal co-products) in their
juices, mucin, and sloughed epithelial cells are rich in nitrogen and studies. Therefore, a possible reason for the discrepancy may be the
amino acids. Therefore, when fiber ingestion causes an increase in fiber source used in the various studies.
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3.3. Effects of fiber on viscera organs organs that are drained by the portal vein and liver (collectively
termed the splanchnic tissues) are metabolically active tissues; thus,
Ingestion of high-fiber diets leads to an increased secretion of they require a substantial proportion of the whole-body energy (and
digestive juices and enzymes, as mentioned previously. This implies nutrient) supply for their maintenance, although they represent less
an increase in the workload of the secretory organs, leading to hy- than 15% of the total body mass [67]. Indeed, Yen et al. [68] showed
pertrophy. In addition, in order to compensate for the low energy that the portal vein alone accounts for nearly 25% of the whole-body
value of high-fiber diets, the increase in feed intake results in adap- energy demand (measured in terms of the amount of oxygen, O2,
tive changes in the gastrointestinal tract [59]. For example, Jin et consumed) in pigs. Furthermore, the splanchnic tissues account for
al. [59] observed a 33% unit increase in the rate of cell proliferation nearly 45% of the whole-body energy demand in pigs [67].
in the jejunum and colon of pigs that were fed a 10% wheat straw- Sodium-potassium adenosine triphosphatase (Na+/K+-ATPase)
containing diet, compared with the control. These changes led to activities and protein turnover have been reported to be responsible
an enlargement of some or all of the organs comprising the gastro- for the high energetic demands of the splanchnic tissues [69,70]. A
intestinal tract [60]. For example, pigs that were fed corn-soybean study by Kelly et al. [71] provides evidence to implicate these two
meal diets containing 40% alfalfa meal had heavier stomach, small processes in the energy demanded by these organs. In that study,
intestine, large intestine, and liver weights than pigs that were fed a Na+/K+-ATPase and protein synthesis activities were estimated to
corn-soybean meal control diet [61,62]. account for 15%–41.5% and 27%–31% of oxygen consumption by the
Pigs that were fed diets containing barley, canola meal, and alfal- visceral organs, respectively. Thus, it follows that changes in the
fa meal showed increased per-kilogram empty body weight of the portal vein mass due to high fiber ingestion would exert an addi-
liver, cecum, and colon (on a dry matter basis) compared with pigs tional energy demand for maintenance. For example, Yen et al. [72]
that were fed a casein-cornstarch-based diet [63]. In addition, pigs reported that growing pigs that were fed a (high-fiber) diet based
that were fed a diet containing 30% distillers dried grains with sol- on barley-canola meal had an increased portal vein mass and an
ubles showed increased visceral organ mass relative to the control- increased maintenance energy requirement (measured as fasting O2
fed pigs [33]. However, Jin et al. [59] found that feeding growing consumed by the portal vein and by the whole-body animal) com-
pigs a diet containing 10% wheat straw had no effect on changes in pared with pigs that were fed a (low-fiber) diet based on casein and
visceral organ mass compared with the control. In the study by Jin cornstarch. However, Agyekum et al. [33] did not observe increased
et al. [59], pigs were fed a fibrous diet for 14 d. However, the dietary whole-body fasting O2 consumption in growing pigs that were fed a
fiber level in the study by Jin et al. was lower than the fiber level in corn-soybean meal diet containing 30% distillers dried grains with
the studies mentioned above [33,61,62], which showed increases solubles, in spite of an increased portal vein mass relative to pigs
in visceral mass due to fiber ingestion in pigs. Therefore, the lack of that were fed the control diet. The smaller sample size (four pigs per
effect of fiber ingestion on visceral mass in the study by Jin et al. [59] treatment) in the study by Agyekum et al. [33] may partly explain
could be due to the inclusion level of dietary fiber and to the dura- the lack of effect shown by the high-fiber diet on the maintenance
tion of the adaptation period employed in their study. requirement in the pigs. Nonetheless, the increased energetic and
Studies on pigs suggest that high fiber ingestion alters intestinal nutrient demand of the portal vein in pigs due to high fiber in-
epithelial morphology. For example, ingestion of a diet containing take reduces the amount of energy and nutrients available for the
10% wheat straw enlarged the villi and deepened the crypts in the growth of tissues of economic importance, such as muscle. Indeed,
jejunum and ileum of growing pigs compared with the control [59]. the ingestion of a fiber-rich diet was shown to reduce pig carcass
Crypt cell proliferation and depth also increased in the colon of weight in several studies, albeit with similar slaughter body weights
pigs and sows that were fed diets high in fiber compared with the [33,73,74].
control [59,64,65]. Furthermore, the villus height-to-crypt depth The third mechanism by which the intake of a high-fiber diet
decreased in the small intestine of pigs that were fed high-fiber negatively affects energy metabolism relates to the increased en-
diets [33,59] compared with the control, suggesting an increased dogenous nitrogen and amino acid production that occurs via in-
crypt cell proliferation and an increased number of cells exhibiting creased secretions of digestive juices and enzymes, which are due
DNA fragmentation. The effects of fiber on alteration in intestinal to fiber ingestion. This result is because the increased production of
morphology and development depend on fiber solubility and water- endogenous nitrogen and amino acids is associated with increased
holding capacity. Thus, soluble fibers are fermented to produce fer- gut protein turnover, that is, increased transport of the products of
mentation products—and butyrate in particular—which serve as an digestion and blood flow through the digestive tissues [75]. Howev-
energy substrate for colon cell proliferation [65]. On the other hand, er, these processes demand a substantial amount of energy, which
insoluble fibers have an abrasive effect on the intestinal wall, as they leads to an increase in the maintenance energy requirement [3], and
scrape the mucosa [66]. This abrasiveness may cause an increase in thereby reduces the amount of energy retained for edible pork pro-
mucin production and in the rate of intestinal mucosal cell turnover. duction. In addition, increased endogenous nitrogen and amino acid
production, coupled with reduced reabsorption and pre-cecal amino
3.4. Effects of fiber on energy metabolism acid digestibility (as discussed previously), leads to an increased
amino acid maintenance requirement [41,51] and thereby decreases
The effects of fiber on the energy metabolism of pigs have been amino acid availability for growth and production.
studied extensively. Results from such studies show a negative effect However, fiber can contribute to the energy supply of the pigs
of fiber ingestion on the energy metabolism of pigs. Several mecha- upon fermentation in the hindgut. In this case, the amount of en-
nisms have been adduced to explain the negative effects of fiber on ergy that is contributed varies depending on feed ingredients, fiber
the energy metabolism of pigs. Firstly, and as mentioned previously type, and interactions with other dietary factors [10]. Upon fermen-
in this review, dietary fiber may decrease the digestibility of starch, tation, the volatile fatty acids produced are metabolized through a
lipid, and protein, which are energy-yielding substrates, resulting in series of anaerobic energy-yielding reactions to produce adenosine
decreased energy digestibility; thus, fiber may reduce the amount of triphosphate (ATP), which is used to produce energy [10]. Indeed,
energy retained for edible pork production. reports [67] suggest that the absorbed volatile fatty acids can supply
The second mechanism to explain the negative effects of fiber up to 28% of the maintenance energy requirement of pigs. Acetate,
relates to the increased visceral organ mass that is caused by the propionate, and butyrate produce the largest quantities of energy.
ingestion of high-fiber diets, as mentioned previously. The visceral The numbers of moles of ATP produced by acetate, propionate,
 A.K. Agyekum, C.M. Nyachoti / Engineering 3 (2017) 716–725 721

and butyrate are 10, 18, and 28, respectively, and the hydrolysis of gases [3], which, upon absorption, contribute to the dietary energy
1 mol of ATP into adenosine diphosphate (ADP) releases 7.3 kcal supply [78] as previously discussed. It has also been suggested that
(1 kcal = 4.184 kJ) of energy. Therefore, the potential energy that is the volatile fatty acids are beneficial to intestinal development and
absorbed upon fiber fermentation (in the case of cellulose) can be gut health in pigs [10,76]. For example, butyrate is used as an energy
approximately 70% of the energy that is produced when glucose is source for colonic cell proliferation. In addition, propionate and a
oxidized. However, the amount of energy that is available to the pig certain amount of butyrate are used for gluconeogenesis, and nearly
for productive functions from fiber fermentation is low as a result of two-thirds of acetate is metabolized in the muscle cells [79].
the energy losses due to methane and hydrogen (H2) production, as As previously discussed, when fiber is fermented, the microbial
well as to the heat of fermentation [10]. fermentation products can promote the proliferation of the mucosal
epithelium by increasing gut length, mass, and villus height. This in
3.5. Effects of fiber on fermentation and intestinal health turn increases the intestinal surface area to increase the absorptive
capacity. In addition, the products of fiber fermentation are used
Because pigs do not secrete the enzymes that are required to hy- to promote bacterial growth [3,78,79]. Therefore, dietary fiber in-
drolyze dietary fiber, the disappearance of dietary fiber in the diges- gestion not only influences nutrient utilization, but also influences
tive tract of pigs is ascribed to microbial fermentation. Fermentation other physiological functions in the pig gut. In this context, some
occurs mainly in the hindgut, that is, the cecum and colon, due to components of dietary fiber have been reported to confer benefits
the dense microbial populations in this region of the gut, although to pig gut health via the promotion of beneficial intestinal bacterial
considerable fermentation can happen before the end of the ileum proliferation and the prevention of colonization of opportunist path-
[3,15,76]. Furthermore, different fiber types have different suscep- ogens. Different fiber sources influence bacterial proliferation differ-
tibility to microbial fermentation; thus, soluble fiber generally has ently. For example, the fermentation of resistant starch influences
a faster fermentation rate than insoluble fiber. Indeed, it has been the proliferation of bifidobacteria [80], whereas pectin fermentation
shown that the fermentation of soluble fiber occurs in the proximal stimulates lactobacilli proliferation [81]. The fermentation of cere-
colon, whereas the fermentation of insoluble fiber is gradual and al grains with high levels of insoluble non-starch polysaccharides
can be sustained until the end of the colon [77]. It has also been stimulates the growth of cellulolytic Ruminococcus-like bacteria and
reported that the addition of insoluble fiber to pig diets may lead to xylanolytic Clostridium-like bacteria [82,83].
low or insignificant microbial fermentation in the small intestine, However, the results of studies on the effects of dietary fiber on
although fermentation remains low in the hindgut [15]. Therefore, the intestinal health of pigs have been contradictory. For example,
it follows that diets containing a high amount of insoluble fiber may some studies link soluble fiber to an increased risk of post-weaning
hamper fiber fermentation in pigs. For example, Urriola and Stein colibacillosis and swine dysentery [84–87]. The main issue is that
[39] and Gutierrez et al. [34] reported that the addition of up to 30% the soluble fiber increases digesta viscosity and undigested nutri-
distillers dried grains with solubles and 40% corn bran with solu- ents and delays digesta passage rate; thus, it provides nutrients
bles, respectively, to diets based on corn-soybean meal reduced the and a milieu that are conducive to pathogen proliferation and col-
total tract and hindgut disappearance of total dietary fiber and of onization, which hampers animal health. Conversely, other studies
NDF in growing pigs compared with pigs that were fed diets based [88] reported beneficial effects of soluble fiber in protecting against
on corn-soybean meal. Nonetheless, fiber fermentation in sows is enteric diseases in pigs. Insoluble fiber, on the other hand, has been
greater than in growing pigs owing to the longer digesta retention linked with reduced colonization of the gut by pathogenic bacteria
time in the hindgut and to the well-developed gut capacity in sows and reduced severity of enteric infections [89–92] because insolu-
[37,54]. ble fiber decreases digesta transit time and thereby decreases the
Dietary fiber fermentation by the gut microflora results in the time available for pathogens to proliferate. However, not all studies
production of volatile fatty acids—mainly acetic, propionic, and support the ability of insoluble fiber to promote intestinal health
butyric acids—along with carbon dioxide (CO2), H2, and methane (Table 1) [84,85,88,89,91,93–97]. Nonetheless, it is recognized that

Table 1
Results of studies evaluating the effects of the type of non-starch polysaccharides on performance and gut health of pigs.
Animal type Challenge model Basal diet Type of NSPa Response
Reference
Performance Intestinal health
Weanling pigs E. coli Rice Soluble ↓ Daily gain ↑ Infection, PWD incidence, proliferation, pH [85]
Weanling pigs E. coli Rice Soluble No effect ↑ Infection, PWD incidence, proliferation; ↕ pH [84]
Growing pigs Lawsonia Corn-SBM Insoluble No effect ↕ Lesion length, diarrhea prevalence, proliferation [94,95]
intracellularis
Growing pigs Swine dysentery Triticale, barley Soluble No effect ↓ Infection, PWD incidence; ↕ gut pH, SCFA [88]
Weanling pigs Non Rice, animal protein Insoluble No effect ↓ PWD incidence; firmer stool [91]
Weanling pigs E. coli Porridge oats, wheat, Soluble No effect ↓ Infection, PWD incidence, pH; ↑ Lactobacillus: [93]
animal protein coliform
Weanling pigs Non Corn, barley, soy pro- Insoluble No effect ↕ PWD incidence, lactobacilli; ↑ SCFA; ↓ E. coli, [89]
tein concentrate coliforms
Weanling pigs E. coli Corn, wheat, barley, Insoluble No effect ↕ SCFA; ↓ PWD incidence, E. coli; ↑ microbial di- [96]
SBM versity
Growing pigs Non Wheat, SBM Soluble No effect ↕ Immune response, bifidobacteria, lactobacilli, [97]
VFA; ↓ Enterobacteriaceae
E. coli: Escherichia coli; PWD: post-weaning diarrhea; SBM: soybean meal; SCFA: short-chain fatty acids; VFA: volatile fatty acids. The symbol ↑ indicates an increase in response
criteria, ↓ indicates a decrease in response criteria, and ↕ indicates no effect on response criteria.
a
NSP: non-starch polysaccharides; NSP-containing diets are compared with non-antibiotic control diets for the entire experimental period; significance is defined as P < 0.05.
722 A.K. Agyekum, C.M. Nyachoti / Engineering 3 (2017) 716–725

the detrimental effect of soluble fiber on intestinal health is due to 4. Improving the feeding value of high-fiber diets
its viscosity and not to fermentability, and that combining soluble
and insoluble fiber in diets produces a superior response on indices Feed-processing techniques such as mechanical and hydrother-
of gut health [4,93,98,99]. However, it is difficult to establish the mal processing can be used to alter the physical properties of the
recommended level of dietary fiber to confer health benefits on diet in order to improve the solubility of feed ingredients that are
pigs, since it ultimately depends on the feed ingredients to be used rich in insoluble fiber [104,105]. These technologies can be em-
for diet formulation and on the fact that a high fiber inclusion rate ployed along with a diet that is rich in insoluble fiber in order to
can hamper nutrient utilization and pig performance. examine their effects on gestating sow welfare and behavior.
Several strategies have been employed to improve the nutritive
3.6. Effects of fiber on gestating sow behavior value of high-fiber diets fed to pigs, such as formulating diets based
on net energy or available nutrient basis, particle size reduction,
Restricted feeding is a common practice in gestating sows to pre- pelleting, and the use of exogenous enzymes. Such strategies have
vent excessive body weight gain and ramifications on locomotion been the object of several excellent reviews. Exogenous enzyme ap-
and reproductive functions. Although this feeding practice ensures plication has been the most widely used approach to ameliorate the
that sufficient nutrients are provided to meet the maintenance adverse effects of high-fiber diets on nutrient utilization in pigs. The
and reproductive needs of sows, it does not provide enough feed to use of this application is based on the premise that pigs do not se-
achieve satiety for the sow. A lack of satiety due to restricted feeding crete the enzymes that are required to degrade fibrous components;
has been reported to result in aggression and stereotypies [100], thus, supplementing diets that are rich in fiber with appropriate
which are of great welfare and production concern in individual enzymes can aid in this regard. Several enzyme preparations to
or group-housed gestating sows. Therefore, fibrous ingredients are degrade the fiber in pig feeds have been made commercially avail-
often incorporated into pregnant sow diets to reduce the sensation able. Among the exogenous fiber-degrading enzymes, xylanase and
of hunger and to overcome the aggression and behavioral prob- β-glucanases are the most widely used in high-fiber pig diets be-
lems associated with restricted feeding [9]. The beneficial effects of cause arabinoxylans, cellulose, and β-glucans are the most predom-
high-fiber diets have been ascribed to their ability to delay gastric inate non-starch polysaccharides in high-fiber pig diets [2,106]. Xy-
emptying [101] and increase swelling of the stomach content and lanase and β-glucanases are often used together or in combination
fermentation products [49,102]. with other commercially available carbohydrases (e.g., β-mannanase,
Fiber type or inclusion level does not influence the immediate α-galactosidase, and pectinase) as well as exogenous protease and
post-feeding behavior of sows, as the feeding duration and physical phytase in order to effectively hydrolyze high-fiber diets and there-
activities remain the same [9]. However, the long-term effective- by increase nutrient utilization by pigs [106].
ness of high-fiber diets on satiety and sow behavior depends on The application of exogenous enzymes has been studied exten-
the physicochemical properties of the dietary fiber. Soluble fiber sively in swine nutrition. However, inconsistent results have been
sources are able to reduce physical activity for several hours after obtained regarding the effects of exogenous enzymes on nutrient
feeding because they can delay and sustain nutrient absorption for utilization and growth performance in pigs that are fed high-fiber
longer periods [9,49,102]. Soluble fiber can also increase volatile diets (Table 2) [107–113]. Factors such as variation in dietary in-
fatty acid production, which can serve as a source of energy when gredient composition, variation in experimental conditions, and
the glucose supply to the gut decreases. In addition, volatile fatty ac- enzyme characteristics (i.e., source, dose, and matrix) have been put
ids can influence the production of certain gut-secreted hormones, forward to explain inconsistent study results regarding the effects of
such as ghrelin, glucagon-like peptide 1, and peptide YY, which are enzymes in pig trials [2,114].
associated with energy and lipid metabolism and which prolong the The mechanism by which supplemental enzymes influence the
feeling of satiety [103]. Therefore, soluble fiber has a greater effect metabolic response and thus the digestive physiology of pigs that
on satiety in gestating sows than insoluble fiber, owing to its greater are fed high-fiber diets is still not clearly understood. For example,
ability to modify the production of gut hormones that are involved growth is commonly used to assess the efficacy of enzymes in pigs
in satiety, lipid metabolism, and energy metabolism. that are fed high-fiber diets; however, growth relies on the interplay

Table 2
Effects of supplementing fiber-rich diets with carbohydrase complex on nutrient digestibility and performance in pigs.
Diet composition NSP enzyme Pig Nutrient digestibility Performance Reference
Wheat, SBM, wheat Cellulase, galactanase, mannan- Nursery Improved DM, starch, energy, NSP, CP, and Improved growth rate and [107]
screening, millrun ase, and pectinase phytate digestibility feed efficiency
Corn, SBM, DDGS (corn or Xylanase, α-amylase, β-glucanase, Nursery DM digestibility improved, but not CP and Improved feed efficiency, but [108]
sorghum) and protease energy not growth rate
Corn, SBM, DDGS (corn or Xylanase, α-amylase, β-glucanase, Grower- CP digestibility improved, but not DM and No significant improvement [108]
sorghum) and protease finisher energy
Corn, barley, SBM, wheat Xylanase, β-glucanase, and cellu- Grower- Improved DM, CP, ether extract, and energy Improved growth rate and [109]
DDGS lase finisher digestibility feed efficiency
Corn, SBM, corn DDGS Xylanase, β-glucanase, and man- Nursery Not determined No significant improvement [110]
nanase
Corn, SBM, corn DDGS Xylanase, β-glucanase, protease, Grower- Not determined No significant improvement [111]
and mannanase finisher in all four studies
Wheat, barley, corn, SBM, Xylanase and β-glucanase Grower- Improved DM, CP, and energy digestibility Improved gilt growth perfor- [112]
CM, corn DDSG, wheat finisher mance, but not barrows
middlings, rye
Corn-SBM, wheat mid- Xylanase, α-amylase, and protease Nursery Improved DM, CP, and energy digestibility Improved growth rate and [113]
dling, fish meal feed efficiency
CM: canola meal; DDGS: distillers dried grains with solubles; CP: crude protein; DM: dry matter.
 A.K. Agyekum, C.M. Nyachoti / Engineering 3 (2017) 716–725 723

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