World Rabbit Sci. 2007, 15: 127 - 140
© WRSA, UPV, 2003
Correspondence: L. Falcão-e-Cunha, email@example.com
Received October 2006 - Accepted July 2007.
ABSTRACT: This review is focused on the most studied and developed substances which are commonly known
as alternatives to dietary antibiotics, particularly as far as rabbit feeds are concerned. After a reminder of the
reason to be and success of antibiotic growth promoters, and why they lately came to be banned in the
European Union, we successively deal with probiotics, prebiotics, enzymes and organic acids. Data on rabbits
are, as expected, quite scarce when compared to species such as pigs and poultry. Nevertheless, the
available performance results are discussed together with the possible mechanisms of action. Special mention
is made of the effects of these substances on digestibility and caecal activity.
Key words: Probiotics, prebiotics, enzymes, organic acids, rabbits
ALTERNATIVES TO ANTIBIOTIC GROWTH PROMOTERS IN RABBIT
FEEDING: A REVIEW.
Falcão-e-Cunha L.*, Castro-Solla L.*, Maertens L.†, Marounek M.‡, Pinheiro V.§,
Freire J.*, Mourão J.L.§
*Inst. Superior de Agronomia, Univ. Técn. de Lisboa, TAPADA DA AJUDA, Portugal
†Inst. Agricultural and Fisheries Res., Animal Sci. Unit, MELLE, Belgium
‡Inst. Animal Physiology and Genetics, Czech Academy of Sci., UHRINEVES, Czech Republic
§Dpt. Zootecnia, UTAD-Univ. Trás-os-Montes e Alto Douro, VILA REAL, Portugal
The use of antibiotic growth promoters (AGPs) in animal production began half a century ago, when
Stokstad and Jukes added residues of chlortetracycline production to chicken feed. They were
added with the objective to serve as a source of vitamin B12, but they caused a growth stimulation
that was far too large to be explained only as a vitamin effect (review by Brezoen et al., 1999). The
almost obvious cause lay in the antibiotic activity of the residues. This observation was quickly
extended to other antibiotics and to other animal species, leading to widespread adoption of AGP
inclusion in feeds.
During the last decades considerable amounts of antibiotics were used in animal production, both as
therapeutic and as growth promoting agents. Therapeutic usage of antibiotics is typically a high
dose-short term one, the substance being either injected, or administered via feed or water. Growth-
promoting usage is typically the opposite, i.e., a low dose-long term administration, usually given in
feed. A certain degree of overlapping exists of course between the two usages. Prophylactic usages,
while intentionally therapeutically, can resemble growth-promoting usages, and the latter can have a
degree of prophylactic action. On the other hand, growth promotion in short-lived species (e.g.
broilers) is necessarily short-term. In the former EU legislation, the two usages were strictly segregated.
AGPs were a small, and lately vanishing, subset of the whole antibiotic arsenal. Still, they more or
less consistently improved the production performances, with most of the economic benefits being
passed to consumers, via lower prices of meat, eggs, and other animal products. AGPs also had
secondary advantages, which are often forgotten. By decreasing feed usage per production unit,
FALCAO et al.
AGPs can reduce the amount of land needed for feedstuff production, the imports of feedstuffs of
many countries, and the manure volume (manures are a liability in many modern production systems).
Most AGPs used in cattle production can also reduce methane emissions.
Though a lot of research was done on the modes of action of AGPs, less is known about them than
about their practical effects. Dozens of mechanisms were proposed over the years, some of them
specific to ruminants, and it is likely that most, if not all of them, can contribute to the overall result.
The fact that germ-free animals usually do not respond to AGPs strongly suggests that their main
and/or immediate actions occur in the gut microbial ecosystem. It is no wonder then that there is still
no final agreement on the mechanisms of action of AGPs: they are acting in an extraordinarily complex
system, definitely more than thought only few years ago, before the widespread adoption of molecular
techniques of microbiological identification. Furthermore, interactions between the microbes and the
gut immune system, another very complex and incompletely understood one, can only add to the
difficulties of the subject.
Table 1, mostly based on the 1997 Commission on Antimicrobial Feed Additives report (1997), but
also on Barton (2000) and Gaskins et al. (2002), summarizes many of the effects of AGPs, e.g., a
degree of inhibition of pathogenic microorganisms, a reduction in microbial toxic metabolites, a
lowering of the turnover of the epithelium, a nutrient-sparing effect, and a reduction in intestinal
motility. Still another often mentioned mechanism is a reduction in the bacterial deconjugation of bile
Two of the former mechanisms are worth stressing: the lower epithelial turnover, because a significant
part of the energy and nutrients of the diet is used in the maintenance of the gut; and the inhibition
of pathogens, because it is usually assumed that AGPs are used much below the antibiotic minimum
inhibitory concentrations. It is commonly assumed that AGPs help to reduce the disease burden,
thus improving performances and animal welfare, and a disease-preventing and/or a subclinical
disease reducing effect is partly supported by the common observation that AGPs efficiency is
inversely related to the hygienic conditions of the farm (Barton, 2000).
At the farm level AGPs cause improvements in feed efficiency, in growth rate, and in egg production.
Improvements in growth rate and feed conversion rate (FCR) happen even when intake is maintained
constant, which points to a specific effect on efficiency, probably related to nitrogen metabolism
Tabl e 1 : S ome of the p hysio logical, nutr itional a nd me tab o lic effects attr ibuted to antimic rob ia l feed
additives (Commission on Antimicrobial Feed Additives, 1997)
Physiological effects Nutritional effects Metabolic effects
Gut food transit REnergy retention IAmmonia production R
Gut wall diameter RGut energy loss RToxic amine production R
Gut wall le ngth RNitrogen retention IAlfa-toxin production R
Gut wall weight RLimiting amino ac id supply IFatty acid oxidation R
Gut absorptive capacity IVitamin ab s orpt io n IFaecal fat excretion R
Faecal moisture RVitamin synthesis RLiver protein synthesis I
Mucos al cell turnover RTrace element absorption IGut alkaline phosphatase I
Stress RFatty acid absorption IGut urease R
Feed intake R = I Glucose absorption I
Calcium ab sorption I
Plasma nutrients I
R: a reduction; = : no effect; I: an increase
ALTERNATIVES TO ANTIBIOTIC GROWTH PROMOTERS
(Gaskins et al., 2002). This might help to explain the fact that young animals usually give stronger
responses to AGPs than the older ones.
DIETARY ANTIBIOTICS IN RABBITS
It was initially thought that AGPs, being antimicrobial in nature, would be necessarily
counterproductive in animal species where a very significant part of digestion is done by microbes.
This reasoning mainly applies to ruminants, but can be extended to hindgut-fermentation herbivores,
such as the rabbit. Practical experience, supported by scientific evidence, showed that this was not
necessarily the case. Some AGPs improve the performances of ruminants and rabbits. Zinc bacitracin
was the most used AGP in rabbit feed.
THE ANTIBIOTIC BAN
Although frequently unsound, increasing worries with food safety led European consumers to oppose
the usage of AGPs in animal feeds. Part of the worry with the AGPs had to do with eventual antibiotic
residues in meat, milk and eggs. As a matter of fact, the antibiotics that were cleared for use as AGPs
in the EU had practically no intestinal absorption. Insignificant absorption, together with a limited
antimicrobial spectrum, and a lack of critical therapeutic applications (either human or veterinary)
were prerequisites for the approval of AGPs in Europe. Problems with antibiotic residues sometimes
occur particularly in milk, but in this case related to local udder treatments, not to in-feed AGPs.
Other consumers, together with a significant part of the medical profession, pointed out that AGPs,
being antibiotics administered at low doses and during long time intervals, could only lead to microbial
resistances in farm animals. This is a significant criticism and one that is supported by scientific
evidence (Wegener, 2006). AGPs select for resistant strains and the fact that different species of
bacteria can interchange genetic material only makes matters worse. But controversy still exists as
far as the practical significance of these resistances is concerned, and in particular about its
contribution to the escalating, and worrying problem of antibiotic resistance in pathogenic organisms.
Its contribution is possibly minor, especially when compared to massive, but by and large
unavoidable, antibiotic usage in hospitals, and to inadequate and partly avoidable antibiotic usage
by consumers, general practitioners, and field veterinarians. Yet, the environment was ripe for AGP
Scandinavian countries, starting with Sweden in 1986, were the first to ban AGPs. Their partial
success in curbing resistances surely contributed to the general EU ban of AGPs, starting in 2006,
and the fact that such a ban is now a considered hypothesis in the USA. It cannot and should not be
forgotten, however, that the Scandinavian ban was only a part of a series of weapons of a global
strategy against bacterial resistance to antibiotics, which also included serious efforts geared towards
the medical profession, and the general public.
Scandinavia was a test bed for the ban of AGPs. After an initial period, when the withdrawal of AGPs
was partly compensated by increasing therapeutic usage of antibiotics in farms, farmers and
technicians adapted to a new reality, finally reducing, as intended, global antibiotic usage. A number
of feed additives, commonly described as antibiotic alternatives, helped to ease the transition to this
At the same time, growing criticism of AGP utilization in animal production fuelled the search for non-
antibiotic substances, which might have similar effects in food-producing animals. Because this was
the main stimulus for their study and development, they are commonly referred to as alternatives to
antibiotics, yet there is little in common between them, and they are often interesting in their own,
with or without antibiotic ban. Among the many alternatives, probiotics, prebiotics, symbiotics,
FALCAO et al.
enzymes and organic acids were perhaps the most studied and developed. The first three, which may
be considered as a group, have also been much looked upon from a human nutrition and health point
of view. But other alternative products can be mentioned, such as immune system stimulators and
plant or herbal extracts.
Interest in these alternative products grew significantly in the eighties. Understandably, performance
studies initially outnumbered mode of action studies, but a significant amount of research has already
been done on the latter % often in vitro or with laboratory animal tests, less frequently with farm
species. After initial, and then often justified, distrust of these products by animal nutritionists and
veterinarians, they became generally and rightly accepted, to the point that the EU feed additive
legislation was altered to make room for them.
In common with antibiotics, most if not all of these alternative products can act upon the gut microbiota,
and the gut immune system; and, thus being, their mode of action will probably turn out to be as
complex to unravel as the mode of action of AGPs. Another possible common point is the fact that
they can be more useful and cost-effective in certain critical periods (e.g. weaning) and/or when
environmental conditions are suboptimal.
In the monogastric camp, alternatives to antibiotics were, as expected, mostly studied in pigs and
poultry (Thomke and Elwinger, 1998; Doyle, 2001). Because of the peculiar digestive physiology of
the rabbit, it can be hazardous to simply extend the conclusions of such studies to this species. We
shall stress some differences when they are relevant.
Interest in probiotics is invariably traced back to Elie Metchnikoff’s studies about the potential
benefits of fermented milks in human nutrition, in the beginning of the twentieth century. The word
probiotic itself was introduced much later. There has been some controversy regarding the
operational definition of probiotics (e.g. kind of microorganisms, whether they have to be alive or
not), but widely accepted is the definition as a preparation of live microorganisms which, when
administered in adequate amount, have beneficial effects on the health of the person or animal
(Hamilton et al., 2003).
Several reviews (e.g. Ziemer and Gibson, 1998; Ouwehand et al., 1999; Simon et al., 2003) have
suggested a number of possible mechanisms of action of probiotics, among which a reduction of
metabolic reactions which produce toxic substances, the stimulation of host enzymes, the production
of vitamins or antimicrobial substances, the competition for adhesion to epithelial cells and an
increased resistance to colonization, and the stimulation of the immune system of the host.
A number of studies mention the production of a range of antimicrobial substances by probiotic
bacteria. Among such substances are organic acids, hydrogen peroxide and bacteriocins, which can
kill other microbes, alter their metabolism, and/or reduce their production of toxins (Rolfe, 2000). But
it should not be forgotten that some of these mechanisms were verified in vitro, and so need to be
substantiated in vivo to be more than hypothesis (Thomke and Elwinger, 1998; Guillot, 2001).
In vivo studies with farm species have mainly looked at performances and health status, but some
work has been done on the effects of probiotics on the gut microbiota, including pathogenic species,
and on the gut morphology and physiology. In some studies, animals were used as a human model
(Thomke and Elwinger, 1998).
Most microorganisms used in probiotics are strains of Gram-positive bacteria of the genera Bacillus
(B. cereus, var. toyoi, B. licheniformis, B. subtilis) Enterococcus (E. faecium), Lactobacillus (L.
ALTERNATIVES TO ANTIBIOTIC GROWTH PROMOTERS
acidophilus, L. casei, L. farciminis, L. plantarum, L. rhamnosus), Pedicoccus (P. acidilactici) and
Streptococcus (S. infantarius). Some yeast and fungi are also used, most frequently some strain of
A significant number of trials show positive effects of probiotics, especially among younger animals,
such as chicks and piglets, raised in less than ideal hygienic conditions (reviewed by Thomke and
Elwinger, 1998, and Simon et al., 2003). But a certain number without positive or even negative
effects have also been published (Doyle 2001).
The lack of consistency in results can be traced to an important number of causes, some of them
related to the animal, others to the probiotic. Among the former, and apart from natural individual
differences (Simon et al., 2003), one may list all the factors that may influence the animal gut microbiota,
such as diet, stress and/or disease. Among the latter, the choice of species and strains, the
technological preparation of the probiotic, the manufacturing of the feed, the dose of administration,
and interactions between probiotic and drugs, just to name a few.
The live bacteria and/or yeasts of the probiotic must be able to withstand the manufacture and
storage of the feeds where they are included. This is particularly critical with non-spore forming
bacteria (e.g. Lactobacillus, Pedicoccus and Streptococcus). At least one commercial product sold
for ruminants is based on recognisably dead microorganisms, and as such is free from these
prerequisites. Whether it should be technically be considered a probiotic is open to question.
Also, probiotics must resist the animal digestive secretions and present no risk of toxicity for it.
According to Guillot (2001), probiotic organisms must attain concentrations in the order of 106-107
per g in the intestinal content to have any observable effect.
The formulation of the feed can be tailored so as to maximize the effect of a probiotic, and this is in a
certain way the basis for symbiotics % preparations containing a combination of a probiotic and a
prebiotic. Working with piglets, Bomba et al. (2002) showed that maltodextrins and polyunsaturated
fatty acids could potentiate probiotics in the small intestine, while fructo-oligosaccharides (FOS)
could potentiate them in the large intestine.
Probiotics for rabbits
There are naturally fewer studies with probiotics in rabbits than in other monogastric farm species.
Several studies exist nevertheless, which are limited to the assessment of the effect on growth, feed
conversion, reproduction and mortality; sometimes caecal activity and digestibility are studied too.
Table 2 synthetically describes a reasonable number of experimental trials with probiotics in growing
and fattening rabbits. The results of these trials were used to make the graphs depicted in Figure 1,
which show average daily gain (ADG), feed conversion ratio (FCR), and mortality, respectively. ADG
and FCR are expressed as a percentage of the controls; mortality as the absolute difference, in
percentage points, between a treatment and the corresponding control.
It is worthwhile noting that, while it is true that the differences were not statistically significant in
many trials, improvements in ADG were obtained in 15 out of 20 trials. It can be added that in one of
the only two negative result trials, the diet was deficient in fibre (only 10% of ADF). The same can,
by and large, be said about FCR. Mortality was also reduced in a great part of the trials where it was
measured (7 positive, 6 null, and 3 negative results).
The number of trials where reproduction results were studied is smaller. The results are summarized
in Table 3 and suggest that the main effect can be an increase in litter weight at weaning; but the
differences were not always statistically significant.
FALCAO et al.
Table 2: A summary of s ome experimenta l p rotocols us ed in pro biotic trials with growing and fattening rabb its
Reference Days on trial Probiotic No.
trial(1) Pro biotic level Unit
Rabbits/cages Dietary fibre Trial conditions
Luick et al., 1992 36 d Lacto-sacc (2) 1 0.2% 15 23.1% ADF Experimental
Luick et al., 1992 36 d Lacto-sacc(2) 2 0.2% 14 9.9% ADF Experimental/low fibre
Gippert et al., 1992 28-84 d Lacto-sacc (2) 3 0.1% 172 10.6% CF Commercial
Gippert et al., 1992 42-77 d Lacto-sacc(2) 4 0.1% 100 10.6% CF Experimental
amani et al., 1992 28-84 d Lacto-sacc(2) 5 0.1% 24 16.7% CF Commercial
De Blas et al., 1991 30 d-2 kg LW Paciflor (Bacillus CIP
5832) 6 0.01% (106 spores/g) 45 36.5% NDF Between 23-28ºC and
Maertens and De
28-70 d Biosaf S. cerevisae 7 0.15% 60 15.5% CF Optimal housing
co nd itions
9 0.15% 93 15.5% CF Le ss favourable
conditions (high density
during several months)
10 1% 95
Maertens et al., 1994 28-70 d Paciflor
(Bacillus CIP 5832)
11 0.01% (106 spores/g) 90 16% CF Optimal housing
co nd itions
12 0.01% (106 cfu/g) 142 16% CF Les s favourable
co nd itions
Jerome et al., 1996 30-79 d Saccharomyces cerevisae 13 106 spores/g 18 cages with 6
rabbits 16.5% CF Experimental
Kustos et al., 2004 35-77 d Bioplus 2B
(B. lichenif ormis, B.
14 0.04% (1.28 H 106cfu/g) 60 15.5% CF Experimental 18-23ºC
- Thermal stress
Amber et al., 2004 35-126 d Lact-A-Bac (L.acidophilus)15 0.05% (8 H 1011 cfu/g) 27 1 2.5% CF Experimental
Tro c ino et al., 2005 35-70 d Toyocerin
(B. cereus var. toyo i)
16 0.02% (2 H 105 spores/g) 63 cages 41% NDF Commercial
17 0.1% (1 H 109 spores/g) 62 cages
Esteve-García et al.,
28 d Toyocerin
(B. cereus var. toyo i)
18 0.02% 15 H 5 cages 14.9% CF Experimental
19 0.05% 15 H 5 cages
20 0.10% 15 H 5 cages
(1) Number of trial in the graphic 1, 2, and 3. (2 )Lactobacillus acidophilus + Streptococcus faecium + yeasts + enzymes (protease, cellulase, amilase) LW= live weight. . cfu= colony-
ALTERNATIVES TO ANTIBIOTIC GROWTH PROMOTERS
The effect of probiotics on digestibility was addressed by several researchers. While neither Gippert
et al. (1992) nor Luick et al. (1992) found any effect, others did. In the trial of Yamani et al (1992),
Lacto-Sacc (a complex product containing microorganisms % Lactobacillus acidophilus,
Streptococcus faecium and yeasts % but also enzyme activities % protease, cellulases, amylase)
improved crude fibre digestibility at 8 and 12 weeks. Amber et al. (2004), working with Lact-A-Bac
(Lactobacillus acidophilus), got improvements in the digestibilities of energy and of most analytical
fractions (DM, CP, EE), including crude fibre.
Since probiotics can influence gut microbiology, several authors looked at their effects upon the
caecum microbiota, either by counting bacteria (Amber et al., 2004) or their products, VFA in particular
(Maertens et al., 1994). In the study of Amber et al. (2004), the probiotic significantly increased
cellulolytic bacteria counts (cfu/ml), while at the same time decreasing the counts of ureolytic ones.
In this study, caecal pH was unaffected by the probiotic. In the study of Maertens et al. (1994), the
probiotic Paciflor did not affect either pH or VFA caecal levels.
To better understand the effects, and to design better probiotics for rabbits, it will be necessary to
apply to this species the kind of studies which are already common in humans, in laboratory animals,
and in other farm species. Research must be done on details referred by Klis and Jansman (2002) such
as lumen physico-chemical conditions and enzyme activities; morphology, absorption capacity and
barrier effect of the epithelium and also in the effect in status of the gut immune system. The same
reasoning applies to prebiotics and symbiotics, discussed in the next section.
Figure 1. Average daily gain (ADG), feed
conversion ratio (FCR) and mortality of
growing rabbits during the trials
summarised in the Table 2. Reference
numbers corresponds to the trial number of
Table 2. Average daily gain (ADG) and feed
conversion ratio (FCR) are expressed as
percentage of the controls; mortality as the
absolute difference (%) between the
treatment and the control.
FALCAO et al.
At this moment there are only two probiotics approved for rabbits in the EU. One of them is bacterial,
i.e. Bacillus cereus var. toyoi, the other is a yeast, i.e. Saccharomyces cerevisiae NCYC Sc 47.
Prebiotics are another possible alternative to antibiotics. A very recent term, prebiotic usually refers
to oligosaccharides which are not digested by the animal enzymes, but can selectively stimulate
certain intestinal bacteria species, which have potential beneficial effects on the host health. Prebiotics
can be either directly extracted from natural sources (plants, yeasts, milk), or be produced by partial
acid or enzymatic hydrolysis of polysaccharides or by transglycosylation reactions (Oku, 1996). The
main commercial oligosaccharides are nowadays the fructo-oligosaccharides (FOS), the a-galacto-
oligosaccharides (GOS), the transgalacto-oligosaccharides (TOS), the mannan-oligosaccharides
(MOS) and the xilo-oligosaccharides (XOS)
While probiotics are meant to bring beneficial microbes to the gut, oligosaccharides are supposed to
selectively stimulate the beneficial microbes that already live there. They have two clear advantages
relative to probiotics: a technological one, because there are no critical problems with the thermal
processing of the feed and the acid conditions of the stomach, and a safety one, because they do not
introduce foreign microbial species into the gut. Beneficial microbes, if stimulated, will better be able
to compete with the undesirable ones. But prebiotics can also have other beneficial effects, irrespective
of stimulating that part of the gut microbiota (Forchielli and Walker, 2005): firstly, they can prevent
the adhesion of pathogens to the mucosa, by competing with its sugar receptors, and secondly they
can directly stimulate the gut immune system.
The mode of action of prebiotics has been mainly studied in vitro and with laboratory animals, and
most of the works published relate to human foods. Positive effects have been found in farm animals,
such as improvements in daily gain, feed conversion ratio and/or health status, but the effect tends
to vary with the oligosaccharide and the conditions of utilization (Patterson and Burkholder, 2003;
Lan et al., 2005).
Prebiotics for rabbits
Some prebiotics were already tested in rabbits. Most of the works published to date concern their
effects on the production performances, and/or the caecal microbiota; more recently, there has been
work on their effects on gut morphology.
The effects of prebiotics on rabbit performances have been at best inconsistent. As far as FOS are
concerned (Table 4), Aguilar et al. (1996) got a positive effect on growth rate, without effect on FCR;
Mourão et al. (2004) found the opposite, i.e., no effect on growth rate but a tendency for an
improvement in FCR; differently, Lebas (1996) did not get any effect at all. Results were also null for
Peeters et al. (1992), working with GOS, whereas Gidenne (1995) got a significant negative effect of
GOS on morbidity and mortality.
Table 3 : Effect of probiotics on reproductive performances (differences in % of control group) (adapted
from Maertens et al., 2006).
Reference Probiotic Parturition
Litter weight at
Litter size at
Maertens and De Groote, 1992 Biosaf +3.5 +1.3
Maertens et al., 1994 Paciflor Bacillus cip 5832 +6.4* !1.3
Nicodemus et al., 2004 Bacillus cereus var. toyoi !10.2* +7.6 +9.9
Pinheiro et al., 2006 Bacillus cereus var. toyoi +5.4 !3.3
ALTERNATIVES TO ANTIBIOTIC GROWTH PROMOTERS
In rabbits, prebiotics should create unfavourable conditions for pathogenic microrganisms in the
caecum. A few research trials were conceived with this objective in mind. The results of Morisse et
al. (1992) are supportive of a barrier effect of FOS in the caecum: the saprophyte E. coli population
increased, the VFA production increased, the ammonia levels in caecal contents decreased. But
Maertens et al. (2004), testing FOS and inulin, only got an effect on the molar proportions of VFA. As
far as other prebiotics are concerned, both GOS (Peeters et al., 1992) and MOS (Mourão et al., 2006)
were able to increase the caecal VFA levels. On the contrary Gidenne (1995) did not observed any
effect of GOS addition on cecal VFA pattern.
Fructans with a lower degree of polymerization may be hydrolyzed by microbes residing in the upper
intestine, especially when the rabbit is actively practicing caecotrophy (Carabaño et al., 2001). If not,
as can happen in very young animals, they shall primarily act in the caecum. Maertens et al. (2004)
showed that, when rabbits are not allowed to practice caecotrophy, the ileal digestibilities of FOS
and inulin are similar and not far from 50%.
MOS, which are thought to act mainly by preventing colonization more than by stimulating beneficial
microorganisms, are considered promising prebiotics (Kocher, 2006). Many pathogens have fimbriae
which specifically attach to the mannose residues of intestinal cell receptors and by connecting to
MOS instead will not attach to the mucosa. In several trials with MOS (Fonseca et al., 2004; Pinheiro
et al., 2004; Mourão et al., 2006), performances were comparable to the ones obtained with AGPs. As
to the effect on gut morphology, Mourão et al. (2006) reported that MOS increased the length of ileal
villi, possibly a result of the reduction in microbial counts, which they also detected.
Lack of consistency in the results obtained with prebiotics can be explained by differences in the
experimental protocols, e.g. number of animals, hygienic conditions, nature of prebiotic, amount of
prebiotic added to feed. This latter factor has been stressed by several researchers (e.g. Mourão et
al., 2006). If the amounts that must be added are very high, the use of prebiotics is compromised by
cost. Also, it is just possible that prebiotics which show benefits in long-living animals, humans in
particular, do not show them in short-living species, such as the rabbit.
Last but not least, it should not be forgotten that rabbit diets are naturally rich in fibrous feedstuffs,
some of them having significant amounts of oligosaccharides. A possible alternative to commercial
prebiotics would be to select the feedstuffs containing the most desirable oligosaccharides for each
phase in the rabbit life.
The idea of adding enzymes to feeds is old, but its practical implementation dates from the end of the
eighties (Choct, 2006). Before this period enzymes were not only too expensive, they were tailored
for other uses, laundry and food in particular, and as such were generally inadequate, and by
consequence useless for the feed industry. Furthermore, most of them were not thermostable and so
could not remain active after pelleting of the feed. Add to this the fact that many would not resist the
Table 4: Effect of FOS addition on performances and mortality of growing rabbits from the trials.
Reference Average daily gain Feed conversion Mort ality
(% control -% experim.)
Ag uilar et al., 1996 P<0.001 (32.3 vs 35.9 g/d) NS (3.16 vs 3.10) NS (6.3 vs 5.9)
Lebas, 1996 NS (35.5 vs 35.6 g/d) NS (3.30 vs 3.30) -1
Mourão et al., 2004 NS (40.1 vs 40.6 g/d) P<0,01 (3.6 vs 3.3) NS (19.4 vs 16.7)
1 Very low mortality (1%), not related to the FOS content.
FALCAO et al.
acid of the stomach, and/or the digestive proteases, and it is not hard to understand why they
tended to fail in the beginning.
The first successful enzymes to be added to feeds were beta-glucanases and xylanases, which are
able to partially hydrolyze non-starch polysaccharides (NSP) of wheat, rye, triticale, oats and barley.
The benefits of these enzymes are firmly established in poultry feeding, and their commercial use is
already widespread. They reduce the intestinal viscosity caused by beta-glucans and arabinoxylans,
respectively, and this in turn improves the absorption of nutrients, the quality of the litter, and the
cleanliness of the eggs. Also, they can reduce the available substrates for microbial proliferation in
the ileum and caecum, while stimulating the more beneficial organisms, as a result of the
oligosaccharides and/or sugars they are able to release (Bedford, 2000). Moreover, these enzymes
allow for greater flexibility and thus lower costs in feed formulation, especially when maize is scarce
and/or very expensive compared to other cereals. While complete hydrolysis can be desirable in the
case of glucans, because it leads to glucose, partial hydrolysis of arabinoxylans can probably suffice,
as long as viscosity is satisfactorily reduced.
The second successful enzymes, although on a smaller scale, were the phytases. Phytases not only
liberate an otherwise unavailable part of the feed phosphorus, thus reducing the need for phosphates
and the excretion of this mineral element, they can also improve the availability of other nutrients.
Phytases can be economically interesting when phosphates are scarce and expensive and/or
phosphorus levels in manures are taxed.
Other enzyme activities have already been studied, examples being a-1,6 galactosidases and b-1,4-
mananases, used to hydrolyze flatus-causing oligosaccharides of soybeans and other legume grains.
In a recent review of 14 trials of soybean-based diets for pigs, supplemented with a-1,6 galactosidases,
b-1,4-mananases, or enzyme complexes, Kim and Baker (2003) concluded that the enzymes had positive
effects on growth performances and digestibility in 70% of the cases.
Glucose-liberating cellulases are perhaps the Holy Grail of feed enzymes, but up till now they have
only met partial successful. The large complexity and interlinkages of the cell wall structure of plants
are partly responsible for the weak response. Cellulases have been often tested, and are sometimes
used, in silages, which also are animal feeds. But enzymes for silages are a special topic, which shall
not be discussed here.
Enzymes used in feeds are thus all hydrolases. They should be tailored to the composition of the
feed, be heat-tolerant, so as to resist pelleting, be acid-resistant, so as to resist gastric transit, and be
resistant to the own proteases of the animal. When interpreting effects, it should not be forgotten
that most commercial enzymes are in reality crude extracts which contain a whole series of enzyme
activities besides the main and declared one.
Enzymes for rabbits
Most of the trials that were performed during the last decade (Remóis et al., 1996; Fernandez et al.,
1996; Pinheiro and Almeida, 2000; Falcão-e-Cunha et al., 2004; Garcia et al., 2005) could not detect
any significant effect of enzymes on rabbits performances. The only exception was the decrease in
mortality which García et al. (2005) found with proteases and proteases + xylanases (probably reducing
protein flow to the caecum). Some positive results were also obtained by other researchers: Eiben et
al. (2004), testing cellulases, got improvements in FCR and mortality of rabbits weaned at 23 days of
age, whereas ADG was unaffected.
It is interesting to note that in some trials enzymes improved fibre digestibility. Such was the case in
the studies of Fernandez et al. (1996) and Bolis et al. (1996). The latter authors got significant
ALTERNATIVES TO ANTIBIOTIC GROWTH PROMOTERS
improvements when cellulase and enzyme pool (xylanase, b-glucanase, b-gluccosidase, pentosanase,
myloglucosidase, acid and neutral protease) was added on NDF (+5%) and ADF (+13%) digestibilities,
yet at the same time getting reductions of digestible and metabolizable energies, and nitrogen balance,
in comparison with the control diets.
The effects of enzymes on the different parts of the rabbit gut were addressed by several researchers.
Sequeira et al. (2000) could only detect a lowering of gastric pH but the enzyme complex composed
of amylase, xylanase, b-glucanase and pectinase did not have any effect on the digestive parameters
measured. Exogenous enzymes frequently fail to significantly affect enzyme activities in the gastric,
intestinal and caecal contents (Sequeira et al., 2000), even in the period succeeding an early weaning
(Falcão-e-Cunha et al., 2004).
Although rabbits are better able to digest phytic phosphorus than poultry and swine, they are not
the equal of ruminants in this regard. In a trial of Gutiérrez et al. (2000), exogenous phytases improved
not only the utilization of phosphorus (+24%), but also increased nitrogen digestibility (+7%).
According to these authors, phytases can be useful in rabbit diets.
It is not unlikely that, due to its peculiar digestive physiology, and in particular the fact that caecotrophy
casts microbial enzymes along the whole length of the gut (Marouneck et al., 1995), rabbits be less
responsive than other animals to supplementation with exogenous enzymes. This does not entirely
rule out the interest of supplementation, but probably restricts it to particular phases in the life of the
Organic acids and salts have a long-history in the food and the feed industries, which commonly use
them as preservatives. Some authors also consider them to be a viable alternative to antibiotics, in
pig feeds namely, where they already have had considerable success. According to Partanen and
Mroz (1999), formic, acetic, propionic, butyric, lactic, sorbic, fumaric, tartaric and citric are the most
promising of organic acids in this regard.
The so called acidification started with piglet diets and was thought as a means to compensate the
relatively low gastric production of acid of the young animals, particularly when subject to early
weaning. It was later verified that it could also been advantageous in the later phases of growth,
when they could both improve the apparent digestibility of energy and protein, and the absorption
and retention of some minerals (Partanen and Mroz, 1999; Diebold and Eidelsburger, 2006). Several
hypotheses have been proposed to explain the positive effects of acidification. The classical ones
see the acid as replacing gastric HCl: the activation of proteolytic enzymes, the denaturation and
unfolding of feed proteins, the barrier effect against microorganisms brought with the feed. But other
non-alternative hypothesis can be mentioned: a residual antimicrobial effect in the lower gut, a
specific trophic effect on the intestinal mucosa, an action as nutrients.
The antimicrobial activity of organic acids is basically the same, irrespective of acting in food, feed,
or gut lumen (Diebold and Eidelsburger, 2006). Indissociated organic acids easily cross the cellular
membrane and tend to dissociate when inside the neutral pH of the microbial cytoplasm. The protons
thus liberated can upset the microbial metabolism, namely by inhibition of enzymes and/or transport
systems. The efficiency of a given acid depends on its pKa, the pH value at which it will be half
dissociated. Higher pKa acids tend to be more effective. On the other hand, the antimicrobial
effectiveness of organic acids tends to increase both with their chain length and their degree of
unsaturation (as reviewed by Partanen and Mroz, 1999).
FALCAO et al.
The minimum inhibitory concentrations of organic acids for pathogenic microorganisms has been
measured in vitro (Strauss and Hayler, 2001 cited by Diebold and Eidelsburger, 2006; Mroz, 2005).
The results show that the degree of inhibition depends both on the acid and the bacterial species
Responses to organic acids are, however, variable. Part of the differences may have to see with the
intrinsic acid activity and buffering capacity of the diets.
Some researchers have also tested medium-chain fatty acids, which also have antimicrobial activity
(Decuypere and Dierick, 2003). They were tested either free, or esterified in triglycerides. When
esterified, they can be liberated by endogenous or exogenous lipases. This will possibly happen in
the intestine, and in this case the gastric mechanisms might be ruled out.
Organic acid for rabbits
Studies of organic acids are few, and their results far from consistent, in the case of rabbits (Maertens
et al., 2006). Recently, Brazilian researchers (Scapinello et al., 2001; Michelan et al., 2002) found that
the inclusion of 1,5% of fumaric acid in the feeds of growing rabbits tended to improve both the daily
gain and the feed efficiency, but the differences were not statistically significant. Similar results were
reported by Hollister et al. (1990) (Table 5).
A group of Czech researchers have been studied intensively the effects of medium-chain fatty acids.
In a study of Skøivanová and Marounek (2002), the inclusion of 0,5% of caprylic acid reduced post-
weaning mortality, without affecting any other performance trait. In a later trial, Skøivanová and
Marounek (2006), testing the medium-chain fatty acids esterified in triglycerides, reached the same
results, i.e. a significant reduction in post-weaning mortality, no effect on feed intake, daily gain, or
Combining organic acids with prebiotics (Scapinello et al., 2001) or with probiotics (Michelan et al.,
2002) did not significantly improve performances, though mortality was significantly reduced in one
trial (Hollister et al., 1990) where fumaric acid was combined with Lacto-Sacc.
The amount of research on alternatives to AGPs is limited in rabbits, compared to other farm species.
Probably, many studies remain unpublished because of confidentiality, either because of favourable
(protection for use with license …) or unfavourable results. Most of the published works have dealt
with growth performances, much less with reproduction and mechanisms of action. Although results
have often been inconsistent, a number of studies suggest that it will be possible to develop
alternatives for this species as well. Because of the complexity of its digestive system, part of the
work to be done shall necessarily be by trial and error, but advances in the fundamental modes of
action has to lead to species designed alternatives. Also, combinations of two or more of these types
of products, as in symbiotics, are still an opportunity to fully explore.
Tabl e 5 : Effect of organic acid addition in performances (differences in % of control group) and mortality
(% contr ol - %expe rimenta l) of growing r abbits on the trials.
Refere nc e Avera ge d aily gain F eed c onve rsio n Mortality
Ho lliste r et al., 1990 !4.0% (40.1 vs 38.5 g/d) +3.77% (3.77 vs 3.91) !7.2% (17.9 vs 10.7)
S ca pinello et al., 2001 +10.7% (28 vs 31 g/d) !3.9% (3.34 vs 3.21) -1
Michelan et al., 2002 +22.0% (27.5 vs 33.6 g/d) !14% (4.13 vs 3.55) -1
1 values not reported
ALTERNATIVES TO ANTIBIOTIC GROWTH PROMOTERS
performance in growing rabbits. In Proc.: 6th World Rabbit
Congress, Toulouse, France, 163-166.
Fonseca A.P., Falcão-e-Cunha L., Kocher A., Spring P. 2004. Effects
of dietary mannan oligosaccharide in comparison to
oxytetracyclin on performance of growing rabbits. In Proc.: 8th
World Rabbit Congress, Puebla, México, 829-833.
Forchielli M.L., Walker W.A. 2005. The role of gut-associated
lymphoid tissues and mucosal defence. Brit. J. Nutr., 93, s41-
García A.I., García J., Corrent E., Chamorro, S., García-Rebollar P.,
De Blas C., Carabaño R. 2005. Effet de l’âge du lapin, de la
source de protéine et de l´utilisation d´enzymes sur les
digestibilités apparentes de la matière sèche et de la protéine
brute sur un aliment lapin. In Proc.: 11èmes Journées de la
Recherche Cunicole, Paris, France, 197-200.
Gaskins H.R., Collier C.T., Anderson D.B. 2002. Antibiotics as
growth promotants: mode of action. Anim. Biotechnol., 13, 29-
Gidenne T. 1995. Effect of fibre level reduction and gluco-
oligosaccharide addition on the growth performance and caecal
fermentation in the growing rabbit. Anim. Feed Sci. Techn., 56,
Gippert T., Virag, G., Nagy, I. 1992. Lacto-Sacc in rabbit nutrition.
J. Appl. Rabbit Res., 15, 1101-1104.
Guillot J.F. 2001. Consequences of probiotics release in the
intestine of animal. In J. Brufeau (Ed.) Feed Manufacturing in
the Mediterranean Region Improving Safety: from feed to
food. Zaragoza CIHEAM-IAMZ, 17-21.
Gutiérrez I., Espinosa A., García J., Carabaño R., De Blas J C. 2002.
Effects of exogenous phytase on phosphorous and nitrogen
digestibility in growing-finishing rabbits. In Proc.: 7th World
Rabbit Congress, Valencia, Spain, 277-281.
Hamilton-Miller J.M.T., Gibson G.R., Bruck W. 2003. Some insights
into the derivation and early uses of the word “probiotic”. Brit.
J. Nutr., 90, 845.
Hollister A.G., Cheeke P.R., Robinson K.L., Patton N.M. 1990.
Effects of dietary probiotics and acidifers on performance of
weanling rabbits. J. Appl. Rabbit Res., 13, 6-9.
Jerome N., Mousset J.L., Lebas F., Robart P. 1996. Effect of diet
supplementation with oxytetracycline combined or not with
different feed-additives on fattening performance in the rabbit.
In Proc.: 6th World Rabbit Congress. Toulouse, France, 205-
Kim S.W., Baker D.H. 2003. Use of enzyme supplements in pigs
diets based on soyabean meal. Pig News and Information, 24,
Klis J.D. van der, Jansman A.J.M. 2002. Optimising nutrient
digestion, absorption and gut barrier function in monogastrics:
reality or illusion. In M.C. Blok, H.A. Vahl, L. de Lange, A.E.
van de Braak, G. Hemke, M. Hessing (Eds.) Nutrition and
Health of the Gastrointestinal Tract. Wageningen Academia
Publishers, The Netherlands, 15-36.
Kocher A. 2006. Interfacing gut health and nutrition: the use of
dietary pre- and probiotics to maximise growth performance in
pigs and poultry. In D. Barug, J. de Jong, A.K. Kies, M. W.A.
Verstegen (Eds.) Antimicrobial Growth Promoters.
Wageningen Academic Publishers, The Netherlands, 289-310.
Kustos K., Kovács D., Gódor-Surmann K., Eiben, C.S. 2004. Effect
of probiotic Bioplus 2b® on performance of growing rabbit. In
Proc.: 8th World Rabbit Congress, Puebla, México, 874-879.
Lan Y., Verstegen S., Tamminga S., Williams B.A. 2005. The role of
the commensal gut microbial community in broiler chickens.
World´s Poultry Sci. J. 61, 3, 95-104.
Lebas F. 1996. Effects of fruct-oligo-saccharides origin on rabbit’s
Aguilar J.C., Roca T., Sanz E. 1996. Fructo-oligo-saccharides in
rabbit diet. Study of efficiency in suckling and fattening periods.
In Proc.: 6th World Rabbit Congress, Toulouse, France, 73-
Amber K.H., Yakout H.M., Hamed Rawya S. 2004. Effect of feeding
diets containing yucca extract or probiotic on growth,
digestibility, nitrogen balance and caecal microbial activity of
growing new zealand white rabbits. In Proc.: 8th World Rabbit
Congress, Puebla, México, 737-741.
Barton M.D. 2000. Antibiotic use in animal feed and its impact on
human health. Nutr. Res. Rev., 13, 279-299.
Bedford M.R. 2000. Exogenous enzymes in monogastric nutrition
– their current value and future benefits. Anim. Feed Sci. Techn.,
Bolis S., Castrovilli C., Rigoni M., Tedesco D., Luzi F. 1996. Effect
of enzymes addition in diet on protein and energy utilization
in rabbit. In Proc.: 6th World Rabbit Congress, Toulouse,
Bomba A., Nemcová R., Gancareikova S., Herich R., Guba P.,
Mudronová D. 2002. Improvement of the probiotic effect of
micro-organisms by their combination with maltodextrins,
fructo-oligosacharides and polyunsaturated fatty acids. British.
J. Nutr., 88, s95-s99.
Brezoen A., Van Haren W., Hanekamp J.C. 1999. Emergence of a
debate. AGPs and Public Health. Human Health and Antibiotic
Growth Promoters (AGPs): Reassessing the risk. Heidelberg
Appeal Nederland Foundation, 131 pp.
Carabaño R., García J., De Blas J.C. 2001. Effect of fibre source on
ileal apparent digestibility of non-starch polysaccharides in
rabbits. Anim. Sci., 72, 343-350.
Choct M. 2006. Enzymes for the feed industry: past, present and
future. World’s Poultry Sci. J., 62, 3, 5-15.
Commission on Antimicrobial Feed Additives.1997. Antimicrobial
Feed Additives. Government Official Reports 1997: 132,
Ministry of Agriculture Stockholm.
De Blas C., García, J. Alday S. 1991. Effects of dietary inclusion of
a probiotic (PACIFLOR*) on performance of growing rabbits.
J. Appl. Rabbit Res., 14, 148-150.
Decuypere J.A., Dierick N.A. 2003. The combined use of
triacylglycerols containing medium-chain fatty acids and
exogenous lipolytic enzymes as an alternative to in-feed
antibiotics in piglets: concept, possibilities and limitation.
An overview. Nutr. Res. Rev., 16, 193-209.
Diebold G., Eidelsburger U. 2006. Acidification of diets as an
alternative to antibiotic growth promoters. In D. Barug, J. de
Jong, A.K. Kies, M.W.A. Verstegen (Eds.) Antimicrobial
Growth Promoters. Wageningen Academic Publishers, The
Doyle M.E. 2001. Alternatives to antibiotic use for growth
promotion in animal husbandry. FRI Briefings, April 2001,
Eiben C.S., Mézes M., Zijártó N., Kustos K., Gódor-Surmann K.,
Erdélyi M. 2004. Dose-dependent effect of cellulase
supplementation on performance of early-weaned rabbit. In
Proc.: 8th World Rabbit Congress, Puebla, México, 799-804.
Esteve-Garcia E., Rafel O., Jiménez G. 2005. Eficacia de Toyocerin®
en conejos de engorde. In Proc.: XXX Symposium de
Cunicultura de Asescu, Villadolid, 85-89.
Falcão-e-Cunha L., Reis J., Freire J.B., Castro-Solla L. 2004. Effects
of enzyme addition and source of fiber on growth and fibrolytic
activities of growing-finishing rabbits. In Proc.: 8th World
Rabbit Congress, Puebla, México, 1532-1537.
Fernández C., Merino J.M., Carabaño R. 1996. Effect of enzyme
complex supplementation on diet digestibility and growth
FALCAO et al.
growth performance in 2 seasons. In Proc.: 6th World Rabbit
Congress. Toulouse, France, 211-215.
Luick B.R., El-Sayaad A.E., Cheeke P.R. 1992. Effect of
fructooligosaccharides and yeast culture on growth performance
of rabbits. J. Appl. Rabbit Res, 15, 1121-1128.
Maertens L., De Groote G. 1992. Effect of a dietary supplementation
of live yeast on the zootechnical performances of does and
weanling rabbits. J. Appl. Rabbit Res., 15, 1079-1086.
Maertens L., Van Renterghem R., De Groote G. 1994. Effects of
dietary inclusion of Paciflor® (Bacillus CIP 5832) on the milk
composition and performances of does and on caecal and growth
parameters of their weanlings. World Rabbit Sci., 2, 67-73.
Maertens L., Aerts J., De Boever J. 2004. Degradation of dietary
oligofructose and inulin in the gastro intestinal tract and the
effects on pH and volatile fatty acids. World Rabbit Sci., 12,
Maertens L., Falcão-e-Cunha L, Marounek M. 2006. Feed additives
to reduce the use of antibiotics. In: L. Maertens and P. Coudert
(Eds.) Recent Advances in Rabbit Science. ILVO, Melle,
Marounek M., Vovk S., Skrivanová V. 1995. Distribution of activity
of hydrolytic enzymes in the digestive tract of rabbits. Br. J.
Nutr., 73, 463-469.
Michelan A.C., Scapinello C., Natali M.R.M., Furlan A.C., Sakaguti
E.S., Faria H.G., Santolin M.L.R., Hernandes A.B. 2002.
Utilização de probiotico, ácido orgânico e antibiótico em dietas
para coelhos em crescimento: ensaio de digestibilidade,
avaliação da morfometria intestinal e desempenho. Rev. Bras.
Zootec., 31, 2227-2237.
Morisse J.P., Maurice R., Boilletot E., Cotte J. P. 1992. Assessment
of the activity of a fructo-oligossaccharides on different caecal
parameters in rabbit experimentally infected with E. coli 0.103.
Ann. Zootech., 42, 81-87.
Mourão J.L., Alves A., Pinheiro V. 2004. Effects of fructo-
oligosaccharides on performances of growing rabbits. In Proc.:
8th World Rabbit Congress, Puebla, México, 915-921.
Mourão J.L., Pinheiro V., Alves A., Guedes C.M., Pinto L., Saavedra
M.J., Spring P., Kocher A. 2006. Effect of mannan
oligosaccharides on the performance, intestinal morphology
and cecal fermentation of fattening rabbits. Anim. Feed Sci.
Technol., 126, 107-120.
Mroz Z. 2005. Organic acids as potential alternatives to antibiotic
growth promoters for pigs. Advances in Pork Production, 16,
Nicodemus N., Carabano R., Garcia J., De Blas J.C. 2004. Performance
response of does rabbit to Toyocerin® (Bacillus cereus var. toyoi)
supplementation. World Rabbit Sci., 12 109-118.
Oku T. 1996. Oligosaccharides with beneficial health effects: a
Japanese perspective. Nutr. Rev., 54 (11): s59-s66.
Ouwehand A.C., Kirjavainen P.V., Shortt C., Salminen S. 1999.
Probiotics: mechanisms and established effects. Intern. Dairy
J., 9, 43-53.
Partanen K.H., Mroz Z. 1999. Organic aids for performance
enhancement in pig diets. Nutr. Res. Rev., 12, 117-145.
Patterson J.A., Burkholder K.M. 2003. Prebiotic feed additives:
rationale and use in pigs. In Proc.: 9th Intern. Symp. on Digestive
Physiology in Pigs, Banff, AB, Canada, 319-331.
Peeters J.E., Maertens L., Geeroms R. 1992. Influence of galacto-
oligosaccharides in zootechnical performance, cecal
biochemistry and experimental colibacillosis O103/8+ in
weanling rabbits. J. Appl. Rabbit Res., 15, 1129-1136.
Pinheiro V., Almeida A. 2000. Efeito da adição de pentosanases em
dietas para coelhos em crescimento sobre as performances
zootécnicas, saúde dos animais, parâmetros fermentativos cecais
e composição química do digesta ileal. In Proc.: I Jornadas
Internacionais de Cunicultura, Vila Real, Portugal, 209.
Pinheiro V., Alves A., Mourão J.L., Guedes C.M, Pinto L., Spring
P., Kocher A. 2004. Effect of mannan oligosaccharides on the
ileal morphometry and cecal fermentation of growing rabbits.
In Proc.: 8th World Rabbit Congress, Puebla, México, 936-941.
Pinheiro V., Mourão J.L.; Silva C.; Jimenez G. 2006. Efecto de
Toyocerin® sobre los rendimientos productivos de conejas
primíparas durante el primer ciclo. In Proc.: XXXI Symposium
de Cunicultura de Asescu, Lorca, España, 125-132.
Remois G., Lafargue-Hauret P., Rouillere H. 1996. Effect of amylases
supplementation in rabbit feed on growth performance. In Proc.:
6th World Rabbit Congress, Toulouse, France, Vol. 1, 289-292.
Rolfe R.D. 2000. The role of probiotic cultures in the control of
gastrointestinal health. J. Nutr., 130, 396S-402S.
Scapinello C., Garcia de Faria H., Furlan A.C., Michelan A.C. 2001.
Efeito da utilização de oligossacarídeo manose e acidificantes
sobre o desempenho de coelhos em crescimento. Rev. Bras.
Zootec., 30, 1272-1277.
Sequeira J., Nicodemus N., Carabaño R., Villamide M.J. 2000. Effect
of type of wheat and addition of enzymes on some digestive
parameters at different sampling time. In Proc.: 7th World Rabbit
Congress. Valencia, Spain, 437-444.
Simon O., Vilfried V., Scharek L. 2003. Micro-organisms as feed
additives – probiotics. In Proc.: 9th Intern. Symp. on Digestive
Physiology in Pigs, Banff, AB, Canada, 295-318.
Skøivanová V., Marounek M. 2002. Effect of caprylic acid on
performance and mortality of growing rabbits. Acta Vet. Brno,
Skøivanová V., Marounek M. 2006. A note on the effect of
triacylglycerols of caprylic and capric acid on performance,
mortality, and digestibility of nutrients in young rabbits. Anim.
Feed Sci. Technol., 127, 161-168.
Strauss G., Hayler R. 2001. Effects of organic acids on
microorganisms. Kraftfutter, 4, 147-151 (cited by Diebold G.,
Eidelsburger U., 2006).
Thomke S., Elwinger, K. 1998. Growth promotants in feeding pigs
and poultry. III. Alternatives to antibiotic growth promotants.
Ann. Zootech., 47, 245-271.
Trocino A., Xiccato G., Carraro L., Jimenez G. 2005. Effect of diet
supplementation with Toyocerin® (Bacillus cereus var. toyoi)
on performance and health of growing rabbits. World Rabbit
Sci., 13, 17-28.
Wegener H.C. 2006. Use of antimicrobial growth promoters in food
animals: the risk outweigh the benefits. .In D .Barug, J. de Jong,
A.K. Kies, M. W.A. Verstegen (Eds.) Antimicrobial Growth
Promoters. Wageningen Academic Publishers, The
Yamani K.A., Ibrahim H., Rashwan A.A., El-Gendy K.M. 1992.
Effects of a pelleted diet supplemented with probiotic (Lacto-
Sacc) and water supplemented with a combination of probiotic
and acidifier (Acid-Pak 4Way) on digestibility, growth carcass
and physiological aspects of weanling New Zealand White
rabbits. J. Appl. Rabbit Res., 15, 1087-1100.
Ziermer C.J., Gibson G. 1998. An overview of probiotics, prebiotics
and symbiotics in the functional food concept: perspectives
and futures strategies. Dairy J., 8, 473-479.