Management and feeding strategies to improve fattening rabbit intestinal
health
L. Maertens
ILVO (Institute for Agricultural and Fisheries Research), Animal Sciences Unit, Scheldeweg 68, 9090 Melle,
Belgium
Abstract
The appearance of Epizootic Rabbit Enteropathy (ERE) at the end of the last century has
caused dramatic losses in young rabbits. However, significant progress has been made both
in on-farm management strategies and in nutritional tools to overcome losses due to ERE.
An all-in all-out batch production system with thoroughly cleaning and disinfection has
proved its efficiency to reduce mortality. Moreover, significant progress has been made
between the role of some dietary factors and rabbit gut health. An excess of dietary protein,
an imbalance between insoluble and soluble fibre and an insufficient dietary level of soluble
fibre have been linked with decreased gut health and higher mortality rates. The very
quickly increase in feed intake after weaning is another high risk factor for enteric diseases.
A feed restriction allowing a more regular feed intake and growth pattern has proved its
efficiency both in experimental conditions and in farms. These three synergistic tools
(hygiene, diet composition and feed intake regulation) constitute the key strategy to
optimize gut health and to reduce the losses in fattening rabbits without an excessive use of
antibiotics. Under such conditions the proliferation of C. perfringens and the production of
the α-toxin into the gut is broken down.
Introduction
In intensive animal producing units, large numbers of animals (e.g., piglets, broilers and
rabbits) are housed in mainly closed houses. This high density of animals leads to increased
infection pressure. Especially in sensitive young animals, a high incidence of digestive
disorders is observed. The EU-wide ban of AGPs (antimicrobial growth promoting agents),
with its last phase in 2006, has increased these problems. Zinc bacitracin was the most used
AGP in rabbit feed [1]. Moreover, even the therapeutic treatment with antibiotics of foodproducing animals has been viewed critically because of the antibiotics’ impact on the
development of resistant bacteria and/or residues that compromise human health [2].
Besides the growing concern for more animal friendly produced products, we cannot
deny the growing public concern for “healthily” produced food. In many EC countries urgent
programs are now established to reduce strongly (e.g. France, Belgium, the Netherlands …)
or even to ban the use of medicated feeds. However, farmed rabbit production is
characterized by a mortality and morbidity which seems considerably higher than in other
farmed animal species due to enteric and respiratory infections [3].
With the widespread introduction of Epizootic Rabbit Enteropathy (ERE) at the end of
the last century, losses due to enteropathies compromised rabbit production. Without the
use of in-feed antibiotics losses up to 40 % of the weaned rabbits were observed [4].
Although the etiology of ERE is still unclear, the opportunistic role of Clostridium perfringens
has been emphasized.
C. perfringens is a normal inhabitant of the rabbit caecum but changes in feeding and in
environmental conditions can trigger the proliferation and the presence of C. perfringens αtoxin [5]. However, if not treated with antibiotics, all rabbits suffering from ERE have much
higher caecal counts of C. perfringens toxinotype A than healthy rabbits [6].
Recently significant progress has been made to enhance gut health and to minimize the
losses due to ERE. Besides proper management strategies, both quantitative as qualitative
feed characteristics are the most important practical tools to reach this goal and will be
discussed in this paper.
1.
Management tools
Rabbit production systems have changed dramatically since the introduction of artificial
insemination in the late 1980s. Individual management of each female has been replaced by
group (batch) handling systems where e.g. insemination, weaning or delivery to the
slaughter house are concentrated on only a few fixed days. This not only improved on farm
management but also improved management in the total production chain (farmer, feed
company, slaughterhouse, etc.), which facilitated traceability procedures [7].
Batch handling of females has also made it possible to develop real “all-in all-out”
production systems. Such systems are recognized in all animal productions as the basis for
overcoming and controlling disease problems, leading to a reduction in antibiotic use. The
“single batch system” (in French, “la bande unique”) has been increasingly used. In 2010,
35% of the commercial farms in France (From the 914 followed) already used such a
completely “all-in all-out” management system [8]. The single batch system fits perfectly
with an “all-in all-out” system, which allows total cleaning and infection every 11-12 weeks
when using a 42-day rebreeding system.
With increasing introduction of the combination of single batch plus all-in all-out,
mortality after weaning decreased from 13-14% before 1990 to less than 10% after 2000 and
dropped on average till 7% in2010 (Fig. 1). From a scientific viewpoint, however, we may not
exclusively attribute this significant reduction in mortality to the aforementioned change in
rabbit management. Nevertheless, this positive trend goes hand in hand with the increasing
use of “all- in all- out” and is observed in spite of the enteropathy problems [3] and the ban
of antimicrobial growth promoting agents.
15
14
Mortality (%)
13
12
11
10
9
8
7
6
5
Figure 1. Average mortality rate after weaning in French rabbitries (n= 900-1100) [8]
Our experimental unit provided another example of the effect of a clean environment.
When we compared the results of the same batch of weanlings housed in an “all-in all-out”
unit with the littermates housed in a continuously occupied unit, not only the mortality was
much lower (1.8% vs 12.1%) but also daily weight gain of the surviving rabbits was 2.3%
higher (43.4 vs 42.4 g) [9].
Recently the positive effects of cleaning and infection between batches was clearly
demonstrated by Spanish colleagues [10]. Under farm conditions, a trial was first executed
in a cleaned and disinfected house and repeated without cleaning in the same rabbit house.
The mortality due to ERE increased dramatically (Table 1) in the second trial. The enhanced
mortality was associated with significant increased counts of C. perfringens spores 14 days
after weaning both in the caecum but also in the environment.
Table 1. Effect of cleaning and disinfection on mortality and C. perfringens spores [10].
Trial 1:
Cleaned and
disinfected
Trial 2
Not
disinfected
P-value
1.04
16.0
P=0.001
1.68 x 104
2.26 x 105
P=0.001
Batch B : mortality, %
6.0
20.4
C. perfringens spores at air extracter (cfu/g dust)
700
832 000
P<0.001
P<0.001
Batch A : mortality ( %)
C. perfringens spores d14 (cfu/g caecum)
Based on different experiments in farms the following regression was obtained
between mortality and environmental counts of C. perfringens spores [10] :
Mortality (%) = 5.67 x C. perfringens spores on the air extractors (log CFU/g) -12,4
(RSD = 2.64; R2 = 0.863; P<0.001; n=9)
This highlights undoubtedly the large impact of farm environmental hygiene on the
onset of digestive diseases.
2.
Nutritional Tools
2.1. Diet composition
Protein requirements are high in young animals. Protein is not only necessary for body
growth, but also to develop and renew intestinal mucosa. However, replacing fiber by
protein results in an excess of protein, which increases the risk of diarrhea [11,12]. One
hypothesis to explain this could be that animals fed high protein diets create a higher
availability of substrates for microbial growth, with prevalence of pathogenic species [13].
Accordingly, a lower ileal flux of protein (-20%) was observed with a low protein diet (16.2%
vs. 18.9%), together with a lower mortality (1.3% vs 7.7%) and decreased detection
frequency of Clostridium perfringens in the ileum [14]. This event would be more important
in young rabbits due to the unachieved digestive maturation. This was illustrated by the
dietary addition (1%) of glutamine in 25-day-old rabbits, resulting in a highly reduced
mortality and frequency of detection of Clostridium spp. and Heliobacter spp. at the ileum
and caecum level [15].
In practical diets, the crude protein level has therefore to be limited till 15.5 in view of
favoring gut health. Moreover, this reduces also the losses of N through the environment
due to a higher N-retention (16). However, to optimize the production performances
attention has to be drawn to fulfill the amino acids requirements.
The dietary fiber supply plays a major role in the prevention of digestive troubles [17].
Due to improved analytical methods to estimate fiber fractions and intensive research, the
role of the different fractions has become much better defined [18].
Lignins and, to a lesser extent, cellulose remain largely undigested because their
polyphenolic structure is not hydrolyzed by the bacteria in the rabbit caecum. Lignins play a
dominant role in the transit time in the gut, and increasing levels are associated with a
HRi, %
60.0
ADL = Acid detergent lignin (Van-Soest
sequential procedure).
50.0
40.0
HRI = Health risk from digestive trouble =
Mortality + morbidity rate by diarrhea,
measured from 28 to 70d of age, on at least
40 rabbits/diet (Data for 10 diets ranging
from 14 to 20% ADF level [19].
30.0
y = 139x-1.17
R2 = 0.71
20.0
10.0
% ADL
0.0
1.0
2.0
3.0
4.0
5.0
6.0
Figure 2. Reduction of digestive troubles incidence according to dietary lignin [19].
significant reduction of the digesta retention time. Several experiments have revealed a
relationship between the dietary Acid Detergent Lignin (ADL) level and the mortality due to
enteritis [20]. This relationship was even more pronounced when the health risk index (HRi)
was confronted with the dietary ADL level (Fig. 2).
Based on these data, the recommended ADL level in the diet is 5.5% ADL after weaning
and at least 5.0% during the following growing period to prevent digestive troubles (Table 2).
Hemicellulose and pectins are considered as digestible fiber because their digestibility is
around 30% and 70%, respectively. The retention time in the caeco-colic segment is
relatively short (8-12h), therefore these rapidly fermentable cell-wall polysaccharides play a
key role in the rabbit digestive processes. They are important to obtain a correct
fermentative activity both in the small intestine and the caecum. It has been shown that the
uronic acids (a main part of the pectins) modulate the fermentative activity in the caecum
and the caecal pH. By consequence, a sufficient dietary content of these digestible fibers is
necessary, in addition to the indigestible fraction, to optimize digestive health [19].
Table 2. Some recommended dietary levels in a complete feed to optimize digestive
health*
As % of a diet with
90% DM
Crude protein
NDF
ADF
ADL
Soluble fibre
Digestible fibre
Starch
Young rabbits (4 - 7 weeks)
Growing (7 - 10 weeks)
15.0-15.5
32.0-34.0
≥ 19.0
≥ 5.5
≥ 12.0
≥22.0
<15.0
15.5-16.0
30.0-32.0
≥ 18.0
≥ 5.0
≥ 12.0
≥20.0
free
* Adapted from Gidenne et al., 2010 [19]) and Trocino et al., 2012 [25]).
However, the dietary digestible fiber content has to be in balance with the other fiber
fractions; if the content is too high, health risks increase. It is therefore recommended to
remain below a dietary ratio of dig. fiber/ADF under 1.3 [19].
Very recently, the dietary soluble fiber level has been linked with an optimal caecal
fermentative activity and gut health in rabbits [22,23,24,25]. A dietary level of at least 10%
seems to be necessary to favor the gut morphology and the immune response and to reduce
the presence of C. perfringens colonies in the caecum.
Based on a meta-analysis [25], with all trials in which soluble fibre and health status
were evaluated (n=18), soluble fibre was the dietary characteristic with the highest
relationship:
Mortality rate of growing rabbits = 35.98 – 2,594 soluble fibre (% as fed) ± 3.139
In this meta-analysis [25], soluble fibre was a more accurate dietary factor than
digestible fibre to predict gut health. According to Trocino et al. [25] this is because
digestible fibre is not likely to measure the fibre really digested by the rabbit with all type of
diets.
However, the methodology to determine the soluble fibres in raw materials and diets is
complex and different methods are used. This complicates hardly its practical use in
formulating balanced rabbit diets for optimal gut health. Soluble fibre is assumed as the
difference between total dietary fibre (TDF) and neutral detergent fibre (NDF). Therefore
instead of soluble fibre, neutral detergent soluble fibre (NDSF) is sometimes used for this
dietary fraction.
Table 3. Effect of dietary NDSF level on digestive parameters at 35d, and mortality in 25d
weaned rabbits[22].
Dietary NDSF1 level, % (as fed)
Jejunum morphology and functionality (35d)
Villi length, µm
Crypt depth, µm
Saccharidase activity (U/mg tissue)
Immune response in lamina propria (35d)
CD4+, %
CD8+, %
C. perfringens, %2
Mortality 25-60 d, %
1
NDSF according to Hall et al.[20]
2
12
9
7
P level
721a
89b
8500a
567b
115a
7100b
492c
113a
5400c
0.05
0.05
0.05
35
21b
8b
5.3b
33
27b
6b
8.5ab
26
31a
19a
14.4a
NS
0.05
0.05
0.05
Frequency of detection in the ileum or caecum
The main source of soluble fibre used in rabbit diets is sugar beet pulp, that contain
nearly 25% [26]. Another possible source of soluble fibre is chicory pulp with a level of 27%
of pectins and 7% of inulins [27]. Good performances were recently obtained with an
inclusion till 20% of chicory pulp in fattening diets. However, due to the low mortality in that
trial, conclusions related to gut health could not be drawn [27].
Apart from its role as nutrient, also the physical structure of the diet (mainly fibre rich
particles) has an impact on passage of digesta, and especially large particles (>0.3 mm)
reduce the retention time in the gut. A slower rate of digesta passage has already longtime
been related with an impairment of rabbit health [19]. Recently it has been shown that fine
grinding (screen 1.5 mm) of the cereals and coarse (screen 4.5 mm) tended to improve the
ileal digestibility, reduced the ileal flux and does not increase caecal weight [28].
2.2. Restricted feeding
Besides qualitative aspects, quantitative aspects of feeding have proven to be helpful to
overcome losses due to diarrhea. Based on mainly French studies and the success under
practical conditions, the majority of the French commercial rabbit farms no longer feed
weanlings ad libitum. Reducing feed intake by at least 25% has proven to be very helpful to
overcome enteritis problems between the ages of 5-8 weeks due to enhanced gut health
[29]. The mortality rate of restricted fed rabbits was only half of those fed free pellets [30].
Recently, also in Spanish studies the positive effects of an early feed restriction on the
health status were confirmed in a context with high incidence of digestive troubles [31].
Feeders were withdrawn from 17:30 to 09:30 between the age of 35 (weaning) and 49 days.
Each litter of 8 kits was divided and 4 kits were fed ad libitum and 4 were time restricted fed.
Results are summarized in Table 3.
Table 3. Effect of a time limited access to the feeder (8 h) on the health status and
production performance [31].
Ad libitum
Restricted feeding (8/24h)
P
Mortality
Morbidity
25.6
41.4
6.3
12.7
0.017
0.004
Live weight at 70d (g)
2,285
2,101
0.001
Scientific FCR (35-70 d)
2.96
2.81
NS
Economic FCR (35-70 d)
3.77
3.48
-
A dramatically drop in mortality was obtained through the restricted feed intake.
Although a compensatory growth occurred after the restriction period (from d 49 off), their
weight was still 8% lower at 70 days. Due to the lower losses, the economic feed conversion
ratio was nearly 8% more favorable in the restricted fed rabbits.
The feed restriction can thus be achieved by providing a limited daily quantity of feed,
but also by a time-limited access (8-9 h/day) to the feeder. In young rabbits it has already
been longtime shown that a limited access to the feeder of 8 hours daily reduces feed intake
with around 20% [32]. However, when the eating time exceeds 10 hours, only a minimal
feed restriction was induced.
Both methods, restriction in quantity or in aces to the feeder, have proved their
efficiency in reducing the losses due to enteric problems. In intensive farms, automatic
feeding systems that allow distributing a restricted quantity of feed in relation to the age of
the growing rabbit are increasingly used. They allow even to combine both methods.
In table 4, data of the quantities consumed by quickly growing strains, obtained at our
Research Institute, are presented. Taking into account that a feed restriction of minimum
20% is necessary, between the age of 5-8 weeks, corresponding quantities are calculated.
However, if the weight of the rabbits is different at weaning or e.g. a more concentrated diet
is used, quantities have to be adapted to the farm situation.
Table 4. Feed intake* and restriction scheme of fattening rabbits (per rabbit)
Age (days)
Indicative
weight (g)
Average feed
intake (g/d)
Restriction
(%)
Quantity to be
fed/day
30 – 32
800
67
20
55
33 – 35
900
75
20
60
36 – 38
1010
90
25
67
39 – 41
1 130
100
25
75
42 – 44
1 250
110
25
82
45 – 47
1 385
120
23
93
48 – 50
1 510
130
20
104
51 – 53
1 660
140
10
126
54 – 56
1 810
148
10
133
57 – 59
1 960
160
5
152
60+
2 000
free
free
* Diet with 9.7 MJ DE
An indirect method to restrict the feed intake level is to restrict the water intake [29].
Rabbits have only a quite small stomach which limits a high water and feed intake during a
short time. Therefore, when the water distribution is limited till 2.5-3 (continuous) hours per
day, feed intake is only 70% of the ad libitum intake and a reduced mortality rate due to ERE
is obtained [33]. However, this management system negatively affects the rabbits’ welfare
and thus cannot be defended.
2.3. In-feed additives
Due to the ban for in-feed used AGP’s, increasing interest has been putted to alternative
products as pro- and prebiotics, organic acids, herb extracts, enzymes, … [34]. For a review
of these alternatives and e.g. working mechanism and efficacy, reference is made to the
presentation of dr. Krieg [35].
However, in order to optimize rabbit gut health, the control and prevention of
coccidiosis in growing rabbits is still a key point [36]. Coccidiosis has been drawing more
attention as its pathological role grew following the appearance of ERE and the development
of resistance against the drugs used to normally control its diffusion [3]. This has recently
been demonstrated both under experimental and field conditions in rabbits [37]. A switch
between anticoccidials which are chemically unrelated has proven to slow down the
development of anticoccidial resistance in poultry. Unfortunately there are at present only 2
anticoccidial drugs allowed for rabbits in the EU for prophylactic in-feed use.
Hygienic measures and a prophylactic shuttle program between the two authorized
molecules are the basis to overcome coccidiosis in young rabbits and to favor their gut
health.
Conclusions
Enteropathies cause large losses mainly shortly after weaning. Management and feeding
strategies are available to optimize rabbit gut health and to reduce the losses due to
enteritis. All-in all-out management with a thoroughly cleaning and disinfection between the
batches is a necessary strategy to control the losses. The environmental count of C.
perfringens spores indirectly reflects the risk of the onset of digestive disorders at farm level
[10].
The importance of dietary factors and especially the dietary fibre level and quality on
rabbits’ health status has been strongly evidenced. A good balance between low digestible
fibre (insoluble fibre) and fermentable fibre (soluble fibre) optimizes gut health. In a context
with high incidence of digestive troubles, a feed restriction of 20-25% in the first weeks after
weaning, showed both in experimental facilities and in farms to be very helpful to overcome
large losses due to enteropathy.
All these synergistic tools have shown to reduce the risk for a proliferation of C.
perfringens in the gut and to avoid the production of the α-toxin. Such a global strategy is
the key to optimize gut health and to reduce the losses in fattening rabbits without an
excessive use of antibiotics [38].
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