Content uploaded by Peter H Brooks
Author content
All content in this area was uploaded by Peter H Brooks on Dec 20, 2013
Content may be subject to copyright.
African Journal of Biotechnology Vol. 8 (9), pp. 1758-1767, 4 May, 2009
Available online at http://www.academicjournals.org/AJB
ISSN 1684–5315 © 2009 Academic Journals
Review
Potential of bacterial fermentation as a biosafe method
of improving feeds for pigs and poultry
A. T. Niba1*, J. D. Beal2, A. C. Kudi2 and P. H. Brooks2
1Department of Animal Production, University of Dschang, P. O. Box 447, Dschang, Cameroon.
2Faculty of Science, School of Biological Sciences, University of Plymouth, Drake Circus, Plymouth, Devon PL 4 8AA,
United Kingdom.
Accepted 6 February, 2009
The use of fermented liquid feeds in monogastric animal nutrition is regarded as one of the biosafe
methods of animal production. This paper examines bacterial fermentation of feed substrates for
production of fermented liquid feeds for pigs and moist feeds for poultry. Emphasis is placed on the
interplay of factors affecting feed fermentation and their relationship to feed quality. The resistance of
fermented feeds to enteropathogenic contamination prior to feeding and their potential contribution to
African agriculture is highlighted.
Key words: Fermented liquid feed technology, pigs, poultry.
INTRODUCTION
There is considerable concern over the use of antibiotic
growth promoters (AGPs) in animal production. Their
extensive usage has resulted in the selection for survival
of resistant bacteria species or strains (Doyle, 2001;
Montagne et al., 2003; Khaksefidi and Rahimi, 2005).
This resistance can be transferred to other previously
susceptible bacteria and can be hazardous to both
animal and human health (Montagne et al., 2003).
The use of in-feed AGPs has been banned in the
European Union (Wilkie et al., 2005; Williams et al.,
2005) and there are further attempts to reduce or remove
in-feed AGPs worldwide (Jin et al., 1998; Yegani and
Korver, 2008). This would have significant implications on
gut microbial profiles (Yegani and Korver, 2008) as well
as increase competition between gut microflora and the
host for available nutrients (Dibner and Richards, 2005).
However, there is an active search for alternatives to
AGPs in animal feeding. This includes the use of
probiotics, organic acids, prebiotics, minerals, enzymes,
herbs, phenolic aromatic components and fermented
feeds (FF) (Knarreborg et al., 2002; Reid and Friendship,
2002; Verstegen and Williams, 2002; Dahiya et al., 2006;
Steiner, 2006; Missotten et al., 2007). FF is considered
*Corresponding author. Email: at_niba@hotmail.com or
atniba@yahoo.fr.
as a biosafe method for replacing AGP in pigs
(Knarreborg et al., 2002; Kobashi et al., 2008) and poultry
(e.g. Heres et al., 2003a; Heres et al., 2003b; Heres et
al., 2003d; Niba, 2008). FFs are characterised by high
numbers of lactic acid bacteria (LAB) (approximately 109
cfu/ml of feed) and high concentrations of lactic acid
(>150 mM) (Heres et al., 2003a; Niba, 2008). In chickens,
the organic acid content of fermented feeds has been
reported to improve foregut barrier function against
pathogens by increasing acidity and lowering the pH
(Heres et al., 2003d; Engberg et al., 2006). The
proportion of chlortetracycline-resistant Escherichia coli
strains was significantly reduced in the gut of weaned
piglets fed fermented liquid feed (FLF) (22.2%) compared
with dry feed (88.9%) (Kobashi et al., 2008). This review,
examines the potential of bacterial fermentation of feeds
as a means of improving feeds for pigs and poultry.
Emphasis will be placed on the interplay of factors
affecting feed fermentation and their relationship to feed
quality.
FERMENTED LIQUID FEED TECHNOLOGY
Man has known the use of microbes for preparation of
food products for thousands of years and all over the
world a wide range of fermented foods and beverages
contribute significantly to the diet of many people (Achi,
2005). The use of liquid feeds in animals has created an
opportunity for recycling of liquid co-products from the
human food industry especially in the European pig
industry (Scholten et al., 1999; Brooks et al., 2003a). This
has considerably reduced the need for alternative
methods of disposal of these products, like drying,
disposal to land fill or burning (Scholten et al., 1999).
However, liquid feeds have the potential to serve as
potent reservoirs of enteropathogens unless steps are
taken to prevent their introduction and proliferation during
storage and feeding (Beal et al., 2002). Brooks et al.
(2001) also stated that liquid-feeding systems can easily
become contaminated. They further observed that the
development of computerised liquid-feeding systems
capable of feeding pigs ad libitum has rekindled interest
in the possibility of liquid feeding for weaner pigs. This, in
addition to recent developments in the use of lactic acid
bacteria in the accelerated fermentation of feed
substrates for animal feeding as well as reducing the
possibility of contamination by enteropathogens (Beal et
al., 2002; Beal et al., 2005), has provided a good basis
for improvement in pig nutrition. It is also having much
promise in other farm animal species especially poultry
(Heres et al., 2003b; Skrede et al., 2003; Niba, 2008) and
aquaculture (Refstie et al., 2005). Fermented liquid feed
technology could make important contributions to African
agriculture especially in semi-arid and hot areas (Niba et
al., 2008b). In such areas, ambient temperatures (appro-
ximately 30°C) could support efficient lactic acid
fermentation of feeds (Beal et al., 2002; Niba, 2008).
Furthermore, wet feeding in hot climates has been shown
to improve feed intake and growth rates in poultry
(Forbes, 2003).
According to Beal et al. (2002), lactic acid bacterial
fermentation of feeds provides a feed that has a pH of 3.8
- 4.0 and contains 150 - 250 mmol/L lactic acid. A similar
range of fermented feed pH has been reported by Geary
et al. (1996) (3.8 - 4.2), Christensen et al. (2007) (3.6 -
4.2), Scholten et al. (1999) (3.5 - 4.5) and Moran et al.
(2006) (<3.8). The synergistic effect of a high lactic acid
concentration and low pH is believed to act in concert to
give fermented feeds their antimicrobial activity. This
enables them to withstand contamination by pathogens
like Salmonella spp. (Geary et al., 1996; van Winsen et
al., 2001a; Beal et al., 2002; van Winsen et al., 2002),
Campylobacter spp. (Heres et al., 2004), and coliforms
(Russell et al., 1996).
The mechanism of action of fermented feeds and
fermented co-products in controlling enteropathogens
both in vitro and in vivo has been reviewed extensively
(Brooks et al., 1996; Scholten et al., 1999; Hansen et al.,
2000; van Winsen et al., 2001a; Beal et al., 2002;
Demeckova et al., 2002; Hojberg et al., 2003; Boesen et
al., 2004; van Immerseel et al., 2004; Beal et al., 2005;
Moran et al., 2006). The antimicrobial effects of lactic acid
are believed to be exerted by the ability of the undissociated
acid to gain entry into the cell, disrupt pH homeostasis and
consequently cause nucleic acid and protein damage
(Beal et al., 2002). According to Moran (2001), the low
Niba et al. 1759
pH, dissociation constant (pKa value),and the molar
concentration are factors that determine the inhibitory
activity of lactic and acetic acid in fermented feed. While
inside the cell, the acid dissociates and causes a drop in
pH. This stops enzymatic processes and causes the
proton motive force to collapse. The anion may also
destroy the cell wall resulting in cell death (van Winsen et
al., 2001a; van Winsen et al., 2001b). However, Alakomi
et al. (2000) earlier stated that disruption of the outer
membrane by acids could involve both dissociated and
undissociated forms. As indicated, the likely action on the
outer membrane of Salmonella could be protonation of
anionic components such as carboxyl and phosphate
groups. This consequently weakens the molecular
interactions between outer membrane components thus
increasing its permeability.
In a recent review by Brooks (2008) on fermented
liquid feeds for pigs, increasing feed cost, withdrawal or
reduction of antimicrobial growth promoters (AGP) in
feeds and quality assurance programmes related to
Salmonella in pig meat were given as reasons why
producers should adopt liquid feeding. However, he
indicated that the success of liquid feeding depended on;
i.) Microbial fermentations and selection of LAB capable
of generating lactic acid levels above 100 mmol/L that
can significantly reduce numbers of enteropathogens and
the incidence of Salmonella.
ii.) Batch fermentation of the cereal portion of feeds with
inoculants capable of generating high lactic acid concen-
trations to give more consistent results of fermentation.
iii.) Fermentations that could preserve the feed, improve
the availability of nutrients, reduce the level of anti-
nutrients and have LAB with probiotic properties.
Meanwhile, the three principal components involved in
the fermentation process are the fermenting micro-
organisms, the feed substrate and the enabling
environment for fermentation (Figure 1).
INFLUENCE OF MICRO-ORGANISM AND FEED
SUBSTRATE ON FERMENTATION
The selection of LAB for feed fermentation to meet
desired feed and production objectives has been
highlighted in previous reviews (Brooks et al., 2003b;
Brooks, 2008). The choice of feed substrates to obtain
high numbers of LAB (109 cfu/g feed) and levels organic
acids (>150 mmol/L) or a consistent fermentation product
has also been researched (Canibe et al., 2007a; Niba et
al., 2007; Lyberg et al., 2008; Niba, 2008; Niba et al.,
2008b; Olstorpe et al., 2008) or reviewed (Brooks, 2008).
Fermentation objectives that have influenced the use of
LAB have centred on;
i.) Selection for rapid production of organic acids (mainly
lactic acid) to ensure biosafety (e.g. Missotten et al.,
1760 Afr. J. Biotechnol.
Environment
-Time (hours)
-Temperature
-Moisture content
-Air Composition
Substrate
-Carbohydrates
-Proteins
-Fibres
-Feathers
Micro
-
organism
-LAB
-Yeasts and fungi
Figure 1. Interactions in the fermentation medium. Fermentation conditions influence rate
of fermentation, type of microbe and substrate quantity and quality affects the medium.
2007; Missotten et al., 2008).
ii.) Selection for homolactic fermentation to improve feed
palatability.
iii.) Breakdown of anti-nutrients and increased bioavai-
lability of nutrients (e.g. Bertsch et al., 2003; Brooks et
al., 2003a; Oboh, 2006; Skrede et al., 2007; Lyberg et al.,
2008; Okpako et al., 2008).
A summary of how some of these objectives relate is
shown in Table 1.
The advantages of fermenting feeds can be summarised
from the table as follows;
i.) Reduction in the level of anti-nutrients within the feed.
ii.) Improved bioavailability of minerals (e.g. P, Ca, Mg
and Cu).
iii.) Increase in protein contents (lysine, histidine and
methionine).
iv.) Breakdown of indigestible carbohydrates.
INFLUENCE OF FERMENTATION LENGTH AND
CONDITIONS
The length of steeping feed ingredients, the type of feed
substrates and fermentation conditions influence the
quality of the fermentation product. Steeping time has
been related to its effects on the activity of endogenous
enzymes and the breakdown of anti-nutrients within the
grain. According to Choct et al. (2004a) the effects on
growth and feed intake for weaner pigs resulting from
steeping of feed for 15 h might be related to the release
and activation of endogenous enzymes in the grain. The
activation of these enzyme systems within the grain can
act on cell wall structures in a similar way to exogenous
feed enzymes (Choct et al., 2004b). In reviewing the
effect of steeping in liquid feeding systems, Brooks et al.
(1996) indicated that phytases that were naturally present
in the pericarp of some grains (like cereals) could be
activated by soaking. They also stated that soaking feed
for 8 - 16 h before feeding increased the bioavailability of
phosphorus, calcium, magnesium and copper. In another
study (Lyberg et al., 2008), the phytase activity for a
cereal grain mix of wheat, barley and triticale was 1382
FTU /kg DM and inositol hexaphosphate bound-
phosphorus and total phosphorus were 2.2 and 3.7 g/kg
DM. After fermentation, dietary inositol hexaphosphate
was completely degraded to release phosphorus.
Fermentation of the carbohydrate-rich cereal compo-
nents of the diet separately and combining them with the
protein-rich components just before feeding has some
practical and nutritional advantages (Beal et al., 2002;
Brooks et al., 2003b; Beal et al., 2005; Moran et al.,
2006; Canibe et al., 2007a; Brooks, 2008). Fermenting
the protein rich components produces undesirable end-
products, such as biogenic amines, which could affect the
palatability of fermented liquid feed (Canibe et al.,
2007a). Furthermore, some studies have reported the
degradation of free amino acids added to diets during
fermentation (Handoyo and Morita, 2006; Canibe et al.,
2007b). However, Niven et al. (2006) demonstrated that
the loss of lysine from fermented liquid pig feed was due
to metabolism of lysine by E. coli present in the feed
rather than its utilisation as an energy source by LAB. It
was observed that inoculation of feed with LAB and 50
mmol/L lactic acid at the beginning of fermentation
resulted in lysine levels remaining unaltered after 72 h
fermentation. The addition of acid reduced or eliminated
the E. coli and allowed the lysine to remain intact during
Niba et al. 1761
Table 1. Effect of micro-organisms and feed substrates on feed fermentation.
Fermentation type Substrate pH Lactic acid
or effects
on diet
Acetic acid
or effects
on diet
Ethanol or
effects on
diet
Source
L. plantarum, P.
pentosaceus, Yeasts
Wheat and wheat by-
products
<3.8
4.53
<60†
22.21*
<10†
22.42*
<10†
9.12*
(Moran et al.,
2006)
(Beal et al.,
2005)
Spontaneous
fermentation.
(LAB and Yeasts)
Barley 4.30 34.43* 27.34* 10.74* (Beal et al.,
2005)
Lactobacillus brevis Soybean white flakes 4.8 Elimination of indigestible carbohydrates
and lowered trypsin inhibitor activity (Refstie et al.,
2005)
Lactobacillus sp. (strain
AD2), L. plantarum
(AM4).
Barley and wheat and
barley whole meal flours - Significant reduction in phytic acid, dietary
fibre and -glucans (33.5-18.4 g/kg in
barley), alpha-amylase activity in barley
(Skrede et al.,
2001; Skrede et
al., 2002; Skrede
et al., 2003;
Skrede et al.,
2007)
Lactobacillus acidophilus Sesame seed meal - Phytic acid reduced to below detectable
limits and tannin contents reduced from 20
to 10 g/Kg
(Mukhodhyay
and Ray, 1999)
Lactobacillus plantarum Complete diets of
cereals and soybean
meal
3.6 Reduction in feed dry matter and insoluble
non-starch polysaccharides, increased
viscosity of feed
(Christensen et
al., 2007)
Unspecified in vitro
fermentation
(LAB and yeasts)
Pig grower diet 4.9-5.3 Reduced contents of total and free lysine
(g/kg crude protein, threonine and
methionine
(Canibe et al.,
2007c)
Phytic acid in cereals - Increase in apparent bioavailability of
Phosphorus, Calcium, Magnesium and
Copper
(Brooks et al.,
2001; Brooks,
2008)
LAB fermentation
Fermented fish silage
supplementation in quail
diet
Increase in egg production and quality
(Haugh unit) (Zynudheen et
al., 2008)
Kocuria rosea Poultry feathers
(fermented feather
meal)
- Improved content and availability of amino
acids, lysine 3.46%, histidine 0.94%,
methionine 0.69%.
(Bertsch et al.,
2003; Bertsch
and Coello,
2005)
Aspergillus nigeir and L.
rhamnosus Cassava peel meal - Increase in proteins (24.4%), ash (7.52%),
crude fibre (10.62%) and decrease in
cyanide (7.35 mg/kg)
(Okpako et al.,
2008)
Saccharomyces
cerevisae and
Lactobacillus spp.
Cassava peel meal - Increase in protein content (21.5%) and
decrease in cyanide (6.2 mg/kg), and
phytate (789.7 mg/100 g).
(Oboh, 2006)
† g/kg dry matter, *mmol/L, WDG-wet wheat distiller’s grain.
the fermentation process.
The main goal of fermentation is a high lactic acid
concentration (>150 mmol/L) and a low pH (<4.5). Tem-
perature affects fermentation rate and low temperatures
may yield insufficient quantities of fermentation end-
products. According to Carlson and Poulsen (2003) an
increase in fermentation temperature from 10 to 20°C
improved the proportion of total barley phytate that was
degraded during an 8 h fermentation from 48 to 55%.
Corresponding values for total wheat phytate degraded
were 52 and 62%. At 38°C it required 2 h for 72% of the
total phytate to be degraded. Fermentation of a cereal
grain mix at 10°C produced 8.6 gl-1 of lactic acid
compared with 13.6 gl-1 at 20°C (Lyberg et al., 2008). At
low temperatures yeast predominates and produces
ethanol (Brooks, 2008). Insufficient lactic acid concentra-
1762 Afr. J. Biotechnol.
tion with 24 h fermentation cycles which are more
practical on farms may be the case at low temperatures.
Furthermore, spontaneous fermentation of a cereal grain
mix at 10°C required 7 days for the pH to drop to 4.0
compared with 5 days for 15 and 20°C. Prolonged
fermentation also results in considerable variation in
species composition of fermented pig feed (Olstorpe et
al., 2008). Fermentation at 30°C seems ideal as at 35
and 40°C there was no significant effect on lactic
utilisation of feed nutrients like added synthetic lysine by
and acetic acid concentrations (Table 2) while butyric
acid and ethanol concentrations were significantly
increased (Beal et al., 2005). Lactic acid fermentation of
sorghum and maize at 30°C produces high levels of lactic
acid (>150 mmol/L) as fermented cereal-base for moist
chicken feed (Niba, 2008; Niba et al., 2008a; Niba et al.,
2008b).
LIQUID TO FEED RATIOS
An important aspect of a successful liquid feeding regime
is the liquid to feed ratio of the diet. This affects the dry
matter content of diet and may also have implications for
the intake and organic acid concentration of the feed.
Research to confirm the ideal dry matter content of liquid
diets is limited (Choct et al., 2004a). In pigs, a wide range
of liquid to feed ratios (3:1, 4:1) (Choct et al., 2004a),
(2:1) (Demeckova et al., 2002; Choct et al., 2004a; Xuan
Dung et al., 2005), (2.5:1)(Russell et al., 1996; Boesen et
al., 2004), (3.5:1) (Geary et al., 1996) have been used. In
chickens, these ratios have been reduced to 1.3:1 (Yasar
and Forbes, 1999) and 1.4:1 (Heres et al., 2003a; Heres
et al., 2003b; Heres et al., 2003c; Heres et al., 2003d;
Heres et al., 2004). With lower liquid to feed ratios,
fermented chicken feeds could be considered as
fermented moist feeds rather than liquid feeds (Niba,
2008). However, the DM concentration of feed has been
shown to have little overall effect on the pattern of
microbial activity (Geary et al., 1996). Meanwhile,
increasing water to feed ratios improved both DM and
energy digestibility of diets for pigs. However, since in
commercial practice with pigs liquid to feed ratios can
vary from 2:1 to 7:1 (Choct et al., 2004a), performance is
likely to be affected by DM intake (Table 3).
CONTROLLED FERMENTATION USING STARTER
CULTURES
Successful fermentation results have also been found to
be dependent on the type of fermentation adopted. A
brief definition of the methods of fermentation is given in
Table 4. Spontaneous (Beal et al., 2005), backslopping
(Moran et al., 2006), inoculated or controlled fermenta-
tions (e. g. Christensen et al., 2007; Canibe et al., 2008)
have been investigated as methods that could be used
for production of fermented liquid feeds. Spontaneous
fermentation has been discouraged (Brooks et al., 2003b;
Brooks, 2008) because in this system yeast, which can
tolerate low pH and a low temperature, can predominate.
Yeast fermentation of starch will result in alcohol and
carbon dioxide production. The production of CO2
represents a loss of feed dry matter and energy value.
Such feeds could be unpalatable due to ‘off’ flavours
resulting in reduced feed intake. Secondly, spontaneous
fermentation may not guarantee a rapid build-up of lactic
acid in the feed, which is necessary for biosafety of the
feed and to limit the pathogens (Niven et al., 2006).
Lastly, since feed ingredients differ in their load of natural
microflora, spontaneous fermentation of the same raw
material at different times results in inconsistent end-
products.
Backslopping has been practiced on many farms (Beal
et al., 2002). The limitations of this method have recently
been highlighted in the review by Brooks (2008). In
addition to these limitations, additions of fresh feed to a
dynamic fermenting medium could have adverse impli-
cations on microbial balance and the ability of the feed to
resist enteropathogens. Temperature shifts during
addition that are outside the optimal range of particular
pathogens could provoke the secretion of cold-shock
proteins (Beal et al., 2002). Such cold shock proteins
could increase pathogen tolerance to lactic acid in feed
fermented at 20°C compared with 30°C.
Controlled fermentation or inoculated fermented liquid
feed would appear preferable for production of fermented
liquid feeds for pigs or fermented moist feeds for chick-
ens because more predictable results could be obtained.
Selection for LAB that produce lactic acid rapidly, with
high 24 h lactic acid (>150 mmol/L) contents (Brooks,
2008), should be the primary objective. The selection of
LAB for other factors, such as probiotic properties is
beyond the scope of this review.
EFFECTS OF FERMENTED FEED ON PERFORMANCE
OF PIGS
In growing pigs, the daily weight gains (kg/day) of FLF
fed groups (0.572) and acidified feed (AF) fed groups
(0.567) were significantly higher (P < 0.05) than pigs on a
dry diet (DF) (0.515) and non-fermented liquid feed
(NFLF) (0.498) (Xuan Dung et al., 2005). Plasma urea
nitrogen was also significantly lower (P < 0.05) in FLF fed
pigs than the dry diet, non-FLF and AF. As observed by
Demeckova (2003), piglets from gilts fed FLF were 300
and 450 g heavier than piglets from the gilts fed NFLF (P
< 0.01) and DF fed gilts (P < 0.001).
Demeckova et al. (2002) reported that faeces from
sows fed FLF feed had significantly (P < 0.001) lower
numbers of coliforms than sows fed NFLF or DF. They
also reported that piglets from sows fed FLF excreted
faeces that were higher in LAB (7.7 vs 7.3 log10 cfu/g, P <
0.01) and lower coliforms (7.5 vs 8.1 log10 cfu/g, P <
0.001) than faeces from piglets of DF-fed dams. Further-
Niba et al. 1763
Table 2. Effect of incubation time and fermentation temperature on feed fermentation.
Incubation
time (h) Temperature
(°C)
pH Lactic acid or
effects on diet Acetic acid or
effects on diet Ethanol or effects
on diet Source
24 - 3.75 54.5† Yeast population
increases 10- fold Yeast population
increases 10- fold
48 - 3.65 Yeasts population
stabilizes and
coliforms
eliminated mainly
by backslopping
Yeasts population
stabilizes and
coliforms eliminated
mainly by
backslopping
Yeasts population
stabilizes and
coliforms eliminated
mainly by
backslopping
(Moran et al.,
2006)
24 - 4.69 11.68* 17.22* 6.81*
48 - 4.34 31.92* 27.55* 10.62*
72 - 4.21 46.14* 30.75* 12.79*
- 30 4.47 30.16* 16.42* 11.69*
- 35 4.41 25.29* 26.57* 9.78*
- 40 4.36 28.64* 32.89* 8.42*
(Beal et al.,
2005)
48 20 4.2 115* Dvalue (min)-250
72 20 3.9 164* Dvalue (min)-164
96 20 3.8 167* Dvalue (min)-137
48 30 3.8 161* Dvalue (min)-45
72 30 3.8 196* Dvalue (min)-38
96 30 3.8 203* Dvalue (min)-34
(Beal et al.,
2002)
0a 10 - NDb 5.5c
0a 15 - NDb 5.5c
0a 20 - NDb 5.5c
3a 10 - NDb NDc
3a 15 - NDb 5.3c
3a 20 - 2.1b 5.6c
5a 10 - NDb 3.8c
5a 15 - 2.1b 4.6c
5a 20 - 3.1b 4.9c
7a 10 - 2.0b 4.5c
7a 15 - 2.1b 6.2c
7a 20 - 2.1b 5.7c
(Olstorpe et
al., 2008)
0 20 - <3.0±0.00c 5.0±1.27d 3.9±0.00b
6 20 - <3.0±0.00c 6.0±0.12d <3.2±0.21b
24 20 - 8.1±0.75c 7.1±0.56d 3.6±0.16b
48 20 - 9.5±0.34c 6.7±0.87d 3.7±0.95b
0 20 - ND 4.7±0.03 ND
6 20 - ND 4.9±0.16 1.9±0.11
24 20 - ND 5.9±0.42 6.8±0.14
48 20 - 91.2±27.66 20.9±6.21 15.5±1.31
(Canibe et al.,
2007c)
17-19a 10 1.8 10.4 1.2
17-19a 15 1.9 10.4 1.2
17-19a 20 2.2 10.5 1.1
17-19a 10 3.3b 7.2c 2.4d
17-19a 15 3.2b 5.9c 2.3d
17-19a 20 4.8b 7.4c 2.0d
(Lyberg et al.,
2008)
†g/kg dry matter, *mmol/L, Dvalue (min)-decimal reduction time (minutes) of Salmonella in fermented feed, adays, byeasts counts (cfu/g feed), cLAB counts
(cfu/g feed), dEnterobacteriaceae counts (cfu/g feed), dmoulds, ND-not detected.
1764 Afr. J. Biotechnol.
Table 3. Effect of liquid to feed ratios of diets on performance.
Liquid to feed ratio Type of operation Remarks Source
2:1, 3:1,4:1 Experimental trial No significant effect on growth and
performance parameters but FCR* of liquid
diets higher (P<0.05) than dry weaner pig diets.
(Choct et al., 2004b)
1.63: 1 to 3.25:1 Experimental trial Digestibility coefficient increase from 0.791 to
0.829 with increase in liquid to feed ratio in
pigs.
(Barber et al., 1991)
1.5:1 to 2.25:1 Experimental trial Feed intake, weight gain and carcass weights
of chickens not significantly affected. (Yalda and Forbes, 1995)
2.1:1 to 5:1 Commercial farms Good results with pigs. (Choct et al., 2004b)
1.5:1 to 3:1 Experimental trial No significant effect on pig performance (Hurst, 2002)
†DM 149 to DM 255 Experimental trial Little effect on microbial activity, DM intake,
weight gain or DM FCR of pigs (Geary et al., 1996)
*FCR- feed conversion ratios; †Diet dry matter concentrations (g/kg diet).
Table 4. Definitions of types of fermentation.
Type of
fermentation Definition Source
Spontaneous Fermentation through the action of indigenous microflora present in the
feed (Brooks, 2008)
A proportion of a previous fermentation is retained as an inoculum for
fresh feed (Moran et al., 2006).
Backslopping
Consecutive microbial re-inoculation with micro-organisms from the
previous batch (Häggman and Salovaara, 2008)
Inoculated Fermentation resulting from inoculation of feed with selected lactic acid
bacteria (Brooks, 2008)
Controlled Fermentation resulting from inoculation of feed with selected lactic acid
bacteria under controlled environmental conditions (e.g. temperature) (e.g. Beal et al., 2002)
Table 5. Economic analysis of fermented liquid feed for pigs (Nguyen Nhut Xuan Dung et al. 2005).
Parameter DF NFLF AF FLF
Feed cost, VND/kg 3528 3528 5202 3528
Total feed intake, kg 220 213 216 195
Live weight gain, kg 50.9 49.6 55.4 55.0
Feed cost/gain, VND* 15.222 15.182 20.239 12.477
*Vietnamese dong (currency), DF- dry feed, NFLF-non-fermented liquid feed, AF-acidified feed, FLF-
fermented liquid feed.
more, Xuan Dung et al. (2005) (Table 5) has indicated
that feeding FLF to growing pigs is associated with the
lowest feed cost/gain ratios compared with DF, NFLF and
AF for growing-finishing pigs in Vietnam.
EFFECTS OF FERMENTED FEED ON PERFORMANCE
POULTRY
Research on the use of fermented moist feeds on the
performance of chickens is limited. However, some stu-
dies have shown that wet feeding increases the feed
intake and growth rate of chickens (Yalda and Forbes,
1995; Yasar and Forbes, 1999; Mai, 2007). Pre-soaking
of broiler feeds for 12 and 24 h significantly increased dry
matter digestibility and body weight gain in male broilers
(25 - 40 days of age) compared with dry feed (Yalda and
Forbes, 1996). Bacterial fermentation of barley and wheat
whole meal flours with -glucan-degrading LAB has
improved growth and early feed:gain ratio in broiler
chickens (Skrede et al., 2003). A 10% inclusion of
fermented fish waste silage in poultry feed increased egg
quality and production in Japanese quails (Zynudheen et
al., 2008).
Early access to semi-moist diets for day-old chicks
stimulates gastrointestinal (GI) development and pre-
vents dehydration during transport from the hatchery (van
den Brink and van Rhee, 2007). Rapid GI tract
development after hatch is essential for optimisation of
digestive function and underpins efficient growth and
development as well as a full expression of the genetic
potential for production traits (Mitchell and Moreto, 2006;
Mai, 2007). Furthermore, the moistening capacity of the
crop of chicks during the first weeks of life is also
believed to be a limiting factor for the optimal functioning
of the gut when standard solid diets are fed (Mai, 2007).
Yasar and Forbes (1999) attributed the beneficial effects
of wet feeding to decreased viscosity of gut contents,
greater development of the layer of villi in the digestive
segments and reduced crypt cell proliferation in the
crypts of the epithelium. However, more research is
required to provide a better understanding of the
contribution of fermented moist feeds in poultry nutrition.
CONCLUSION
A successful application of fermented liquid feeds in pig
or moist feeds in chicken feeding systems depends on
the ability to select the right balance of LAB, feed
substrates and fermentation conditions capable of pro-
ducing repeatable fermentation results. Meanwhile, the
resistance of such feeds to enteropathogen contamina-
tion during short storage, and their capability to reduce
pathogen colonisation in the gut of pigs and poultry, could
have far-reaching implications for improved food and
environmental safety in warm wet regions of the African
continent.
REFERENCES
Achi OK (2005). The potential for upgrading traditional fermented foods
through biotechnology.Afri. J. Biotechnol. 4: 375-380.
Alakomi HL, Skytta E, Saarela M, Mattila-Sandholm T, Latva-Kala K,
Helander IM (2000).Lactic Acid Permeabilizes Gram-Negative
Bacteria by Disrupting the Outer Membrane. Appl. Environ.
Microbiol. 66: 2001-2005.
Barber J, Brooks PH, Carpenter JL (1991). The effects of water to food
ratio on the digestibility, digestible energy and nitrogen retention of a
grower ration. Anim. Prod. 52: 601 (Abstr.).
Beal JD, Niven SJ, Brooks PH, Gill BP (2005). Variation in short chain
fatty acid and ethanol concentration resulting from the natural
fermentation of wheat and barley for inclusion in liquid diets for pigs.
J. Sci. Food Agric. 85: 433-440.
Beal JD, Niven SJ, Campbell A, Brooks PH (2002). The effect of
temperature on the growth and persistence of Salmonella in
fermented liquid pig feed. Int.J. Food Microbiol. 79: 99-104.
Bertsch A, Alvarez R, Coello N (2003). Nutritional evaluation of Kocuria
rosea fermented feather meal as an alternative protein source in
poultry feed. Rev. Cient.-Fac. Cienc. Vet. 13: 139-145.
Bertsch A, Coello N (2005). A biotechnological process for treatment
and recycling poultry feathers as a feed ingredient. Bioresour.
Technol. 96: 1703-1708.
Boesen HT, Jensen TK, Schmidt AS, Jensen BB, Jensen SM, Moller K
(2004). The influence of diet on Lawsonia intracellularis colonization
Niba et al. 1765
in pigs upon experimental challenge. Vet. Microbiol. 103: 35-45.
Brooks PH (2008). Fermented Liquid Feed for Pigs, CAB Reviews:
Perspectives in Agriculture, Veterinary Science, Nutrition and
Natural Resources, http://www.cababstractsplus.org/cabreviews/,
pp. 1-18.
Brooks PH, Beal JD, Niven SJ (2003a). Liquid feeding of pigs: I
Potential for reducing environmental impact and improving
productivity, Review paper presented at the conference on Effect of
genetic and non-genetic factors on carcass and meat quality of pigs,
Siedlce, Poland, pp. 7-22.
Brooks PH, Beal JD, Niven SJ, Demeckova V (2003b). Liquid feeding of
pigs: II Potential for improving pig health and food safety, Review
paper presented at the conference on Effect of genetic and non-
genetic factors on carcass and meat quality of pigs., Siedlce,
Poland, p.23-40.
Brooks PH, Geary TM, Morgan DT, Campbell A (1996). New
developments in liquid feeding. Pig Vet. J. 36: 43-64.
Brooks PH, Moran CA, Beal JD, Demeckova V, Campbell A (2001).
Liquid feeding for young piglet, In: Varley MA, Wiseman, J. (Eds.),
The Weaner Pig, Nutrition and Management, CABI Publishing,
Oxon, UK, pp. 153-178.
Canibe N, Hojberg O, Badsberg JH, Jensen BB (2007a). Effect of
feeding fermented liquid feed and fermented grain on
gastrointestinal ecology and growth performance in piglets. J. Anim.
Sci. 85: 2959-2971.
Canibe N, Miettinen H, Jensen BB (2008). Effect of adding Lactobacillus
plantarum or a formic acid containing-product to fermented liquid
feed on gastrointestinal ecology and growth performance of piglets.
Livestock Sci. 114: 251-262.
Canibe N, Virtanen E, Jensen BB (2007b). Effect of acid addition to pig
liquid feed on its microbial and nutritional characteristics. Livestock
Sci. 108: 202-205.
Canibe N, Virtanen E, Jensen BB (2007c). Microbialogy and nutritional
characteristics of pig liquid feed during fermentation. Anim. Feed
Sci. Technol. 134: 108-123.
Carlson D, Poulsen HD (2003). Phytate degradation in soaked and
fermented liquid feed--effect of diet, time of soaking, heat treatment,
phytase activity, pH and temperature. Anim. Feed. Sci. Technol.
103: 141-154.
Choct M, Selby EAD, Cadogan DJ, Campbell RG (2004a) .Effect of
liquid to feed ratio, steeping time, and enzyme supplementation on
the performance of weaner pigs. Austr. J. Agric. Res. 55: 247-252.
Choct M, Selby EAD, Cadogan DJ, Campbell RG (2004b). Effects of
particle size, processing, and dry or liquid feeding on performance of
piglets. Austr. J. Agric. Res. 55: 237-245.
Christensen P, Glitso V, Pettersson D, Wischmann B (2007). Fibre
degrading enzymes and Lactobacillus plantarum influence liquid
feed characteristics and the solubility of fibre components and dry
matter in vitro. Livestock Sci.109: 100-103.
Dahiya JP, Wilkie DC, Van Kessel AG, Drew MD (2006). Potential
strategies for controlling necrotic enteritis in broiler chickens in post-
antibiotic era. Anim. Feed Sci. Technol. pp. 60-88.
Demeckova V (2003). Benefits of fermented liquid diets for sows, and
their piglets [PhD Thesis], Department of Agriculture and Food,
Faculty of Land, Food and Leisure University of Plymouth, Plymouth,
p. 287.
Demeckova V Kelly D, Coutts AGP, Brooks PH, Campbell A (2002).
The effect of fermented liquid feeding on the faecal microbiology and
colostrum quality of farrowing sows. Int. J. Food Microbiol. 79: 85-
97.
Dibner JJ, Richards JD (2005). Antibiotic Growth Promoters in
Agriculture: History and Mode of Action. Poult. Sci. 84: 634-643.
Doyle EM (2001). Alternatives to antibiotic use for growth promotion in
animal husbandry, Food Research Institue Report funded by
National Pork Producers Council, University of Wisconsin-Madison,
Wisconsin-Madison, USA, p. 15.
Engberg RM, Johansen NF, Jensen BB (2006). Fermented feed for
laying hens.Reproduction, Nutr. Dev. 46: S93 (Abstract).
Forbes JM (2003). Wet foods for poultry. Avian Poult. Biol. Rev. 14:
175-193.
Geary TM, Brooks PH, Morgan DT, Campbell A, Russell PJ (1996).
Performance of weaner pigs fed ad libitum with liquid feed at diffe-
1766 Afr. J. Biotechnol.
rent dry matter concentrations. J. Sci. Food Agric. 72: 17-24.
Häggman M, Salovaara H (2008). Microbial re-inoculation reveals
differences in the leavening power of sourdough yeast strains. LWT
- Food Sci. Technol. 41: 148-154.
Handoyo T, Morita N (2006). Structural and Functional Properties of
Fermented Soybean (Tempeh) by Using Rhizopus oligosporus. Int.
J. Food Prop. 9: 347-355.
Hansen LL, Mikkelsen LL, Agerhem H, Laue A, Jensen MT, Jensen BB
(2000). Effect of fermented liquid food and zinc bacitracin on
microbial metabolism in the gut and sensoric profile of m.
longissimus dorsi from entire male and female pigs. Anim. Sci. 71:
65-80.
Heres L, Engel B, Urlings HAP, Wagenaar JA, Van Knapen F (2004).
Effect of acidified feed on susceptibility of broiler chickens to
intestinal infection by Campylobacter and Salmonella. Vet. Microbiol.
99: 259-267.
Heres L, Engel B, Van Knapen F, De Jong F, Wagenaar JA, Urlings
HAP (2003a). Fermented liquid feed reduces susceptibility of
broilers for Salmonalla enteritidis. Poult. Sci. 82: 603-611.
Heres L, Engel B, Van Knapen F, Wagenaar JA, Urlings BAP (2003b).
Effect of fermented feed on the susceptibility for Campylobacter
jejuni colonisation in broiler chickens with and without concurrent
inoculation of Salmonella enteritidis. Int. J. Food Microbiol. 87: 75-
86.
Heres L, Urlings HAP, Wagenaar JA, De Jong MCM (2003c). Trans-
mission of Salmonella between broiler chickens fed with fermented
liquid feed. Epidemiol. Infect. 132: 107-116.
Heres L, Wagenaar JA, Van Knapen F, Urlings BAP (2003d). Passage
of Salmonella through the crop and gizzard of broiler chickens fed
with fermented liquid feed. Avian Pathol. 32: 173-181.
Hojberg O, Canibe N, Knudsen B, Jensen BB (2003). Potential Rates of
Fermentation in Digesta from the Gastrointestinal Tract of Pigs:
Effect of Feeding Fermented Liquid Feed. Appl. Environ. Microbiol.
69: 408-418.
Hurst D (2002). The influence of liquid feeding on gastrointestinal
adaptation, growth and performance in the growing pig, Imperial
College at Wye, University of London,U. K., p. 295.
Jin LZ, Ho YW, Abdullah N, Jalaludin S (1998). Growth performance,
intestinal microbial populations, and serum cholesterol of broilers fed
diets containing Lactobacillus cultures. Poult Sci. 77: 1259-1265.
Khaksefidi A, Rahimi S (2005). Effect of probiotic inclusion in the diet of
broiler chickens on performance, feed efficiency and carcass quality.
Asian-Austr. J. Anim. Sci. 18: 1153-1156.
Knarreborg A, Miquel N, Granli T, Jensen BB (2002). Establishment and
application of an in vitro methodology to study the effects of organic
acids on coliform and lactic acid bacteria in the proximal part of the
gastrointestinal tract of piglets. Anim. Feed Sci. Technol. 99: 131-
140.
Kobashi Y, Ohmori H, Tajima K, Kawashima T, Uchiyama H (2008).
Reduction of chlortetracycline-resistant Escherichia coli in weaned
piglets fed fermented liquid feed. Anaerobe 14: 201-204.
Lyberg K, Olstorpe M, Passoth V, Schnürer J, Lindberg JE (2008).
Biochemical and microbiological properties of a cereal mix
fermented with whey, wet wheat distillers' grain or water at different
temperatures. Anim. Feed Sci. Technol. 144: 137-148.
Mai AK (2007). Wet and Coarse diets in broiler nutrition: Development
of the GI tract and performance, Wageningen Institute of Animal
Sciences (WIAS), Wageningen University and Research Centre,
Wageningen, The Netherlands, p. 141.
Missotten JAM, Goris J, Michiels J, Van Coillie E, Herman L, De Smet
S, Dierick NA, Heyndrickx M (2008). Screening of isolated lactic acid
bacteria as potential beneficial strains for fermented liquid pig feed
production. Anim. Feed Sci. Technol. Corrected Proof, 17 pp.
Missotten JAM, Michiels J, Goris J, Herman L, Heyndrickx M, De Smet
S, Dierick NA (2007). Screening of two probiotic products for use in
fermented liquid feed. Livestock Sci. 108: 232-235.
Mitchell MA, Moreto M (2006). Absorptive function of the small intestine:
adaptations meeting demand In: Perry GC (Ed.), Avian Gut Function
in Health and Disease. CAB International, Wallingford, U.K., p. 43-
64.
Montagne L, Pluske JR, Hampson DJ (2003). A review of interactions
between dietary fibre and the intestinal mucosa, and their conse-
quences on digestive health in young non-ruminant animals. Anim.
Feed Sci. Technol. 108: 95-117.
Moran CA (2001).Development and benefits of liquid feeding through
fermentation for the post-weaned pig. Department of Agriculture and
Food, Seale-Hyane Faculty, University of Plymouth, UK, p. 389.
Moran CA, Scholten RHJ, Tricarico JM, Brooks PH, Verstegen MWA
(2006). Fermentation of wheat: Effects of backslopping different
proportions of pre-fermented wheat on the microbialand chemical
composition. Arch. Anim. Nutr. 60: 158-169.
Mukhodhyay N, Ray AK (1999). Effect of fermentation on the nutritive
value of sesame seed meal in the diets for rohu, Labeo rohita
(Hamilton), fingerlings. Aquac. Nutr. 5: 229-236.
Niba AT (2008).Factors affecting the production of fermented moist feed
for chickens and effects on the gastrointestinal environment [PhD
Thesis], University of Plymouth, U. K., p.188.
Niba AT, Beal JD, Kudi AC, Brooks PH (2007). Effect of water quality on
in vitro fermentation of sorghum and barley for poultry diets,
Proceedings of the British Society of Animal Science Annual
Conference, British Society of Animal Science, Southport, England,
p. 243.
Niba AT, Kouchika H, Kudi AC, Beal JD, Brooks PH (2008a). Effect of
particle size and micro-organism on lactic acid fermentation of
sorghum, In: BSAS (Ed.), Proceedings of the British Society of
Animal Science, Cambridge University Press, Scarborough, U. K., p.
43.
Niba AT, Yajima K, Kudi AC, Beal JD, Brooks PH (2008b). Effect of
concentration of phenolic compounds of two sorghum varieties on
fermentation of sorghum with lactic acid bacteria for inclusion in
poultry diets, In: BSAS (Ed.), Proceedings of the British Society of
Animal Science, Cambridge University Press, Scarborough, U. K. p.
80.
Niven SJ, Beal JD, Brooks PH (2006). The effect of controlled
fermentation on the fate of synthetic lysine in liquid diets for pigs.
Anim. Feed Sci. Technol. 129: 304-315.
Oboh G (2006). Nutrient enrichment of cassava peels using a mixed
culture of Saccharomyces cerevisae and Lactobacillus spp solid
media fermentation techniques. Electron. J. Biotechnol. 9: 46-49.
Okpako CE, Ntui VO, Osuagwu AN, Obasi FI (2008). Proximate
composition and caynide content of cassava peels fermented with
Aspergillus nigeir and Lactobacillus rhamnosus. J. Food Agric.
Environ. 6: 251-255.
Olstorpe M, Lyberg K, Lindberg JE, Schnurer J, Passoth V (2008).
Population diversity of Yeasts and lactic acid bacteria in pig feed
fermented with whey, wet wheat distillers' grains, or water at
different temperatures. Appl. Environ. Microbiol. 74: 1696-1703.
Refstie S, Sahlstrom S, Brathen E, Baeverfjord G, Krogedal P (2005).
Lactic acid fermentation eliminates indigestible carbohydrates and
antinutritional factors in soybean meal for Atlantic salmon (Salmo
salar). Aquaculture 246: 331-345.
Reid G, Friendship R (2002). Alternatives to antibiotic use: probiotics for
the gut. Anim. Biotechnol. 13: 97-112.
Russell PJ, Geary TM, Brooks PH, Campbell A (1996). Performance,
water use and effluent output of weaner pigs fed ad libitum with
either dry pellets or liquid feed and the role of microbial activity in the
liquid feed. J. Sci. Food Agric. 72: 8-16.
Scholten RHJ, van der Peet-Schwering CMC, Verstegen MWA, Den
Hartog LA, Schrama JW, Vesseur PC (1999). Fermented co-
products and fermented compound diets for pigs: a review. Anim.
Feed Sci. Technol. 82: 1-19.
Skrede A, Sahlstrom S, Ahlstrom O, Connor KH, Skrede G (2007).
Effects of lactic acid fermentation and gamma irradiation of barley on
antinutrient contents and nutrient digestibility in mink (Mustela vison)
with and without dietary enzyme supplement. Arch. Anim. Nutr. 61:
211-221.
Skrede G, Herstad O, Sahlstrom S, Holck A, Slinde E, Skrede A (2003).
Effects of lactic acid fermentation on wheat and barley carbohydrate
composition and production performance in the chicken. Anim. Feed
Sci. Technol. 105: 135-148.
Skrede G, Sahlstrom S, Skrede A, Holck A, Slinde E (2001). Effect of
lactic acid fermentation of wheat and barley whole meal flour on
carbohydrate composition and digestibility in mink (Mustela vison).
Anim. Feed Sci. Technol. 90: 199-212.
Skrede G, Storebakken T, Skrede A, Sahlstrøm S, Sørensen M,
Shearer KD, Slinde E (2002). Lactic acid fermentation of wheat and
barley whole meal flours improves digestibility of nutrients and
energy in Atlantic salmon (Salmo salar L.) diets. Aquaculture 210:
305-321.
Steiner T (2006). Managing Gut Health: Natural Growth Promoters as a
Key to Animal Performances. Nottingham University Press,
Nottingham.
Van den Brink M, van Rhee W (2007). Early access to semi-moist diets
for day old chicks stimulates gastrointestinal tract development and
prevents dehydration during transport, World Poultry, World Poultry,
http://www.twilmij.nl/UK/pages/documents/Semi-moistdiets.pdf,
Twilmij BV, Stroe, The Netherlands, p.17-19.
Van Immerseel F, Fievez V, De Buck J, Pasmans F, Martel
A,Haesebrouck F, Ducatelle R (2004). Microencapsulated short-
chain fatty acids in feed modify colonisation and invasion early after
infection with Salmonella enteritidis in young chickens. Poult. Sci.
83: 69-74.
Van Winsen RL, Keuzenkamp D, Urlings BAP, Lipman LJA, Snijders
JAM, Verheijden JHM, Van Knapen F (2002). Effect of fermented
feed on shedding of Enterobacteriaceae by fattening pigs. Vet.
Microbiol. 87: 267-276.
Van Winsen RL, Lipman LJA, Biesterveld S, Urlings BA, Snijders JAM,
Van Knapen F (2001a). Mechanism of Salmonella reduction in
fermented pig feed. J. Sci. Food Agric. 81: 342-346.
van Winsen RL, Urlings BAP, Lipman LJA, Snijders JMA, Keuzenkamp
D, Verheijden JHM, van Knapen F (2001b). Effect of Fermented
Feed on the Microbial.Population of the Gastrointestinal Tracts of
Pigs. Appl. Environ. Microbiol. 67: 3071-3076.
Verstegen MWA, Williams BA (2002). Alternatives to the use of
antibiotics as growth promoters for monogastric animals. Anim.
Biotechnol. 13: 113-127.
Wilkie DC, Van Kessel AG, White LJ, Laarveld B, Drew MD (2005).
Dietary Amino acids affect intestinal Clostridium perfrigens
populations in broiler chickens. Can. J. Anim. Sci. 85: 185-193.
Niba et al. 1767
Williams BA, Bosch MW, Boer H, Verstegen MWA, Tamminga S (2005).
An in vitro batch culture method to assess potential fermentability of
feed ingredients for monogastric diets. Anim. Feed Sci. Technol.
p.123-124, p.445-462.
Xuan Dung NN, Manh HL, Ogle B (2005). Effects of fermented liquid
feeds on the performance, digestibility, nitrogen and plasma urea
nitrogen (PUN) of growing-finishing pigs.Livestock Research for
Rural Development 17: 1-8,
http://www.cipav.org.co/lrrd/lrd17/19/xdun17102.htm.
Yalda AY, Forbes JM (1995). Food intake and growth in chickens given
food in the wet form with and without access to drinking water. Br.
Poult. Sci. 36: 357-369.
Yalda AY, Forbes JM (1996). Effects of food intake, soaking time,
enzyme and cornflour addition on the digestibility of the diet and
performance of broilers given wet food. Br. Poult. Sci. 37: 197-807.
Yasar S, Forbes JM (1999). Performance and gastro-intestinal
response of broiler chickens fed on cereal grain-based foods soaked
in water. Br. Poult. Sci. 40: 65-76.
Yegani M,Korver DR (2008).Factors Affecting Intestinal Health in
Poultry. Poult. Sci. 87: 2052-2063.
Zynudheen AA, Anandan R, Ramachandran Nair KG (2008). Effect of
dietary supplementation of fermented fish silage on egg production
in Japanese quail (Coturnix coromandelica). Afr. J. Agric. Res. 3:
379-383.
