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Influence of different types of bedding material on the prevalence of pododermatitis in rabbits
Journal Pre-proof Influence of different types of bedding material on the prevalence of pododermatitis in rabbits
P. Wolf, R. Speers, M.G. Cappai PII:
S0034-5288(19)30700-3
DOI:
https://doi.org/10.1016/j.rvsc.2019.12.004
Reference:
YRVSC 3933
To appear in:
Research in Veterinary Science
Received date:
15 July 2019
Revised date:
6 October 2019
Accepted date:
1 December 2019
Please cite this article as: P. Wolf, R. Speers and M.G. Cappai, Influence of different types of bedding material on the prevalence of pododermatitis in rabbits, Research in Veterinary Science (2019), https://doi.org/10.1016/j.rvsc.2019.12.004
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Journal Pre-proof 1
Influence of different types of bedding material on the prevalence of
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pododermatitis in rabbits
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P. Wolf1, R. Speers2, M. G. Cappai3
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Running head: Wolf et al., FPD in rabbits
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*Correspondence:
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Prof. Dr. Petra Wolf, Chair of Nutrition Physiology and Animal Nutrition, University of
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Rostock, Justus-von-Liebig Weg 6b, 18059 Rostock, Germany. Tel: +49 381 498 3320
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Fax: +49 381 498 3322
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E-mail address: [email protected]
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Chair of Nutrition Physiology and Animal Nutrition, University of Rostock, Germany
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Speers Hoff, Stelle, Germany
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Chair of Animal Nutrition, Department of Veterinary Medicine, University of Sassari, Italy.
Journal Pre-proof ABSTRACT
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Pododermatitis is a disorder with a complex etiology, because potentially determined by
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various factors such as posture, nutrition and genetics. In the case of presence of pododermal
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lesions, it is often noticed that rabbits go to eat at the bowl less frequently, but an evident
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weight loss is not always perceptible. In fact, similarly to poultry, overweight animals seem to
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be prone to the onset of pododermatitis. An experiment was carried out to test the effect of
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different types of bedding material (straw vs. wood shavings vs. coarse bark mulch vs. cotton)
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on the prevalence of pododermatitis in 30 fattening Separator rabbits. Once a week, the four
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experimental runs were assessed for contamination (macroscopic contamination by
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faeces/urine/litter) as well as for lesion scoring of the footpad. In addition, the water and
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ammonia binding behaviour of bedding was tested. The most favourable values as to dry
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matter, NH3 (p<0.05) and also scoring of the litter were generally observed when cotton was
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used as bedding material. This is probably due to the high water binding capacity, the faster
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water release and the structural effects of the material itself (softness). By contrast, the
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structure of the coarse bark mulch was not suitable for binding liquids (especially urine) and
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led to increased contamination of the barrels. These results suggest that rabbits with an
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increased tendency to sore soles should be kept on bedding materials with desirable physical
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properties (e.g. cotton litter).
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Key words
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Pododermatitis, sore legs, bedding material, rabbit, housing
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Journal Pre-proof INTRODUCTION
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The occurrence of lesions in the area of the sole is a common health problem in rabbits,
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especially in those kept as pets, in which skin injuries are usually accompanied by secondary
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mixed infections, not rarely ending in the organization into purulent abscesses and ulceration
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(Wolf and Kamphues, 2009). Such clinical condition and the development of lesions are
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similar in farmed rabbits. The independent scientific opinion of the European Food Safety
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Authority issued in 2005 reported that the prevalence of footpad lesions in intensively farmed
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rabbits ranged between the 5% and the 15%, but numbers could increase when also hock
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lesions were considered, the latter being reported to be the commonest cause of culling. In
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farmed rabbits, the prevalence of sole lesions mainly involve breeding rabbits, especially
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does, due to the longer life span, higher body weight (in comparison with growing rabbits)
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and prolonged and continuous contact with the litter (Rosell and De La Fuente, 2013). In a
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report of 2013 on footpad lesion prevalence in farmed rabbits conducted in Spain, a
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significant decrease was pointed out over a decade period, thanks to the improvement of
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husbandry conditions (Rosell and De La Fuente, 2013). Pododermatitis and, in general,
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footpad lesions are associated with evident pain and suffering (Morton and Griffiths 1985)
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and represent an issue of both animal health and welfare. At present, pododermatitis in rabbits
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continues to represent an issue but the new flooring systems appear to be a good strategy to
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improve health and welfare conditions of does (Masthoff and Hoy, 2019). In addition to
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genetic factors, keeping conditions of animals may also act as predisposing factors (Masthoff
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et al. 2017). Similarly to poultry production, the development of the disease can be
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accelerated in the case of overweight animals (Wolf, 2005). These conditions have already
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been identified in productive poultry as the actual cause of foot pad lesions (Kamphues et al.
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2011, Youssef 2011) as well as in game birds like captive partridges (Cappai et al., 2018).
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In farmed rabbits partial or inadequate change of bedding material may be a predisposing
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cause to increase the prevalence of pododermatitis at farm level. Thus, animal sitting on wet
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Journal Pre-proof litter for a long time in a confined space is acknowledged to be critical. In fact, NH3 is irritant
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for skin and mucosa and may be toxic when gaseous concentrations increase. Bacterial
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fermentations occurring in the litter contribute to form gaseous NH 3 from urine and faeces,
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responsible to induce a mucociliar reflex and apnea in the rabbit (Lindeberg et al., 1987),
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often leading to conjunctivitis and respiratory disease (Hartung, 1990; Martens, 2000). High
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concentrations of NH3 in the stable air can impair the health and thus the performance of
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animals (Tiedemann 1991). As to pathophysiology, increased NH3 concentrations primarily
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damage the respiratory tract and the defense system of upper ways as well as of trachea and
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lungs. Almost all respiratory diseases are adversely affected by higher concentrations of NH3
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(Van Caenegem and Wechsler 2000), as NH3 has keratolytic properties and irritates both skin
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and mucous membranes (Tiedemann 1991). Van Caenegem and Wechsler (2000) explain this
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toxic effect of ammonia with the formation of NH4OH- on the moist mucous membranes,
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which has a liquefying effect on cell proteins and can thus lead to deep necrosis. In high doses
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NH3 can lead to an increase in blood pressure and respiratory rate as well as to burns of the
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upper respiratory tract, which in turn opens the way for infections (Tiedemann 1991).
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Ammonia can also have a negative effect on the function of the blood by reducing the number
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of erythrocytes and the oxidation capacity of haemoglobin. A neurotoxic effect in the form of
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nervousness was also mentioned (Adam 1973; Meyer 1988). In addition, obese animals move
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less in the available space and therefore sit on a given spot, so that a long lasting pressure on
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the soles of the feet can be exerted under own body mass (Drescher and Schlender-Böbbis
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1996). In view of these reasons, footrest and small sized group of animals were proposed to
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be introduced and in farm integrated strategies were recently reviewed (Szendrő et al., 2019)
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in light of efficacious measures to decrease the prevalence of footpad lesions of does (Figure
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1). In the absence of EU Directives on rabbit protection, at present several European countries
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promulgated own guidelines aiming to improve rabbit health and welfare. In 2017, the
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European Parliament issued a resolution to change conventional caging systems with cages
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respectful of rabbit health, normal behaviour and welfare based on scientific reference in the
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field (Szendrő et al., 2019). In light of this background, also bedding material plays a crucial
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role in the interplay of surface to surface contact, which should be comfortable and safe,
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hygienic and economic. For example, inappropriate bedding materials with low absorbent
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capacity or thin bedding material in plastic cages (Drescher 1993) quickly lead animals to sit on wet litters and the soles of their feet kept damp for long periods (Masthoff et al. 2015).
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In addition, the wet bedding also causes conversion of urine and faeces, which can lead to
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NH3 pollution of the environment. In fact, NH3 is irritant for skin and mucosa and may be
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toxic when gaseous concentrations increase. Bacterial fermentations occurring in the litter
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contribute to form gaseous NH3 from urine and faeces, responsible to induce a mucociliar
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reflex and apnea in the rabbit (Lindberg et al., 1987), often leading to conjunctivitis and
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respiratory disease (Hartung, 1990; Martens, 2000). High concentrations of NH3 in the stable
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air can impair the health and thus the performance of animals (Tiedemann 1991). Increased
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NH3 concentrations primarily damage the respiratory tract and the defense system of the
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trachea and lungs. Almost all respiratory diseases are adversely affected by higher
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concentrations of NH3 (Van Caenegem and Wechsler 2000), as NH3 has keratolytic properties
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and irritates and irritates the skin and mucous membranes (Tiedemann 1991). Van Caenegem
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and Wechsler (2000) explain this toxic effect of ammonia with the formation of NH 4OH- on
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the moist mucous membranes, which has a liquefying effect on cell proteins and can thus lead
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to deep necrosis. In high doses NH3 can lead to an increase in blood pressure and respiratory
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rate as well as to burns of the upper respiratory tract, which in turn opens the way for
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infections (Tiedemann 1991). Ammonia can also have a negative effect on the function of the
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blood by reducing the number of erythrocytes and the oxidation capacity of haemoglobin. A
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neurotoxic effect in the form of nervousness was also mentioned (Adam 1973; Meyer 1988).
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The present study aimed to test the influence of different bedding materials (straw vs. wood
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shavings vs. coarse bark mulch vs. cotton) on litter quality and foot health of rabbits.
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MATERIAL AND METHODS
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Animals and diet
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This trial enrolled 30 adult (age 7.7 ±0.48 months, min. 7 months n=10, max. 8 months n=20)
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female fattening rabbits (Separator rabbits; body mass 3.36 ± 0.81 kg). Animals received hay
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and a commercial mixed feed (MF) in pelleted form, based on green meal (see Table 1).
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Separator rabbits, all previously kept on perforated plastic floors, are a relatively small-sized
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breed. The soles of all animals were checked at the beginning of the experiment to ensure that
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only rabbits without previous damage to the soles of the feet were tested, as a pre-requisite for
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enrollment in the trial. Animals were kept in the original farm until completion of the
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experiment and underwent thorough health checks throughout the period.
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Food and water were offered fresh daily. The determination of feed and water consumption of
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the animals took place daily by subtracting feed left over from feed offered as well as water
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remainders. The animals were kept in floored housing (enclosure size 200 x 100 x 100 cm - L
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x H X W) in groups of 6 animals each. The floor was completely covered (litter height: 20
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cm) with straw (S; long stalks), wood shavings (H), bark mulch (R), bark mulch with
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raspberry leaves (R+I) and cotton material (B) (see Figure 2).
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Sampling method and laboratory analysis
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In order to simulate posture errors from practice (Endlicher, 2013), the bedding material was
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spread once a week, otherwise the bedding was left in place and care was taken to ensure that
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the floor was completely covered. Litter samples were taken at fixed, defined places (in all 4
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corners of the floor, 15 cm from the edge, in the middle and 3 samples each within a radius of
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10 cm around the feed and water bowl), combined to a pooled sample and processed for the
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analyses. The dry matter content was determined in accordance with the VDLUFA
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Journal Pre-proof association regulations by drying the material in weight-constant porcelain bars at 103 °C up
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to a constant weight. To measure the ammonia content at a distance of 20 cm above the
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bedding (about eye level of the rabbits), the sample was placed in an airtight incubator. After
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6 hours, the NH3 concentration in the air cube was read with the aid of a gas detector tube
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(Dräger-Röhrchen Ammoniak 5/a, Dräger, Lübeck), the end of which was held 20 cm above
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the bedding, and the associated gas pump, a small bellows pump (Dräger gas detector pump
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accuro, Dräger, Lübeck).
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At the beginning of the test and once a week during the 12-week test period, the health of the
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pad of the foot was assessed. The footpad was scored according to Masthoff et al. (2015), in
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which both the lesions and the degree of contact material of the soles of the feet were taken
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into account (see Table 2).
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The assessment of the footpad health was always carried out by the same person in order to
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exclude possible subjective influences.
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Analysis of data and statistics
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The statistical evaluation was carried out with SAS Version 9.4 (SAS Institute Inc., 2012).
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The Shapiro-Wilk test was used to check the normal distribution. Furthermore, the data were
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subjected to a two-factorial analysis (ANOVA). In all statistical analyses effects were judged
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to be significant at p < 0.05.
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RESULTS
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With an identical feed supply and a comparable water consumption, it was possible to
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determine significantly different dry matter contents for the various bedding materials
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deployed (see Figure 3). The significantly highest dry matter content could be determined
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with 67.6% using cotton. The bedding was slightly damper when bark mulch was used,
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whereby the addition of raspberry leaves had no effect on the dry matter content (59.6% for
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pure bark mulch, 60.2% for bark mulch with raspberry leaves). There were no significant
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differences in dry matter content between the long-stacked straw and the wood chips. Both
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Journal Pre-proof bedding materials had the significantly highest moisture content compared to bark mulch and
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cotton bedding.
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No statistically significant differences could be found between groups as to the ammonia
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concentrations (see Figure 4). However, cotton litter showed the highest binding capacity for
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ammonia, with the lowest ammonia content of 1.15 ppm measured 20 cm above the litter. The
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highest concentrations could be found in the air above the straw.
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Once a week the soles of the rabbits' feet were assessed. In addition to the degree of
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contamination, particular attention was paid to lesions (see Table 3).
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The rabbits kept on cotton litter, followed by straw and wood shavings had the significantly
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lowest degree of contamination of the legs. These are materials that per se have no colouring,
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so the legs cannot discolour. The situation was different with bark mulch. This has a certain
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inherent colour which, in combination with the humic acids, led to a discolouration of the legs
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(but also of the lower abdomen when lying down). A pollution by excrement and urine took
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place alongside, but since animals in each group received identical feeds, the effects should
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not be linked to the diet, but can be led back primarily to the bedding materials.
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DISCUSSION
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The differences observed in the DM content of the different types of bedding material are
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probably due to the different compaction of the material itself, like previously reported by
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Abd El-Wahab in poultry and turkeys (2011). The spaces between the individual particles of
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the bark mulch allow air to circulate between the individual particles, resulting in faster water
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evaporation and consequently in faster drying. With wood chips, on the other hand, the
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material is compacted. While bark mulch also has a porous structure, straw - especially long-
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stalked qualities - has a lower water retention capacity.
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Also ammonia content over bedding differed according bedding material used. Straw is one of
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the most frequently used bedding materials in pet rabbits (Berghoff 1989; Beynon and Cooper
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1997; Schall 2008), offers the animals additional employment opportunities (playing,
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Journal Pre-proof gnawing, digging), thus enabling species-typical behaviour and enriching the animals'
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environment (ARRP 2003). In this case, however, it did not contribute to a reduced ammonia
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content in the air.
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Studies by Lipman (1999) and Ras et al. (2002) showed that higher NH 3 concentrations were
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found after the use of wood shavings than, for example, in bark mulch, which is in line with
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the results. This was followed by cellulose bedding and corn cob substrate, which produced
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the lowest NH3 emissions. In the present investigations, the use of cotton had the clearest
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effects on NH3 release. Various mechanisms may be responsible for this observation. Not
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only liquid, but also urea can be absorbed by the bedding, which is therefore no longer
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available to microorganisms. It is therefore conceivable that more urea was absorbed by
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cotton than by straw. In addition, already formed NH3 can also be deposited by the bedding
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and thus prevented from entering the gas phase (ARRP, 2003; Kaliste, 2004). Thus it would
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be possible that NH3 was formed, but was absorbed by the cotton to a greater extent than by
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straw and therefore could not enter the airspace of the incubator.
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Minimizing the NH3 concentration in the vicinity of rabbits is an important prophylactic
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measure against the development of respiratory diseases, conjunctivitis and mucous
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membrane irritations (Hartung, 1990; Marten, 2000).
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Rabbits react very sensitively to increased NH3 concentrations in the air (Lange 2005) and
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avoid these areas if possible (Bessei et al. 2001). Since rabbits are mostly kept in cages in
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groups and therefore have little possibility to move to areas with lower NH 3 concentrations, it
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can be assumed that a reduction of NH3 emissions would increase the well-being and normal
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behaviour of animals.
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The influence of NH3 on the development of dermatitis of the sole surfaces is discussed in
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various animal species, e.g. turkeys, but in rabbits no investigations were available. However,
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it can be assumed that identical patho-mechanisms exist here. Overall, unsuitable soils, lack
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Journal Pre-proof of bedding, stress and obesity are regarded as direct causes of so-called "sore legs" (Schlolaut,
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1998; Wolf, 2005).
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The rabbits showed the highest degree of lesions on the straw bedding. This is probably due
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to a mechanical noxious effect of the longer straws rather than to the higher moisture content
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(see Figure 3).
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Among the most discussed factors influencing the foot pad health of commercial poultry are
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body weight, genetics, stable climate, stocking density, feeding, bedding material and bedding
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moisture (Mayne et al., 2006; Große-Liesner, 2007; Berk, 2009; Youssef et al., 2011; Bellof
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et al., 2014). In this context, the type of bedding and the associated water-binding capacity of
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the material are becoming increasingly important. Studies on turkey hens have shown that
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wood shavings and straw shavings or the combination of both types of bedding, in contrast to
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lignocellulose, performed much worse as bedding and had a negative effect on the health of
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the footpad (Berk, 2009). In this study, wood chips and straw also performed worse and are in
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agreement with comparative reference.
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Again in rabbits, it was shown that one of the decisive factors for the occurrence of
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pododermatitis is the moisture to which the sole of the foot is exposed.
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In commercial poultry, increased pododermatitis prevalence was observed with litter moisture
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contents of more than 35% and an exposure of the animals of more than 4 hours per day (Abd
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El-Wahab, 2011). Recommendations therefore assume that litter moisture should not exceed
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30% to ensure good foot pad health. In this study, lesions were found in rabbits in all litter
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materials except cotton, so that this limit seems justified in rabbit husbandry. However, the
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incidence of lesions was not as pronounced as in poultry. This may be due to the fact that
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rabbits spread the body mass over four legs, with the hind legs also having a larger contact
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surface. In addition, the soles of the rabbit's feet are hairy, while poultry lack this isolation.
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CONCLUSION
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increased pressure on the soles of the feet. This effect is particularly noticeable when the
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animals are also sitting on moist bedding. The footpad is usually protected by dense hair, but
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this mechanism is lost in overweight animals. If the skin in this area is permanently moist,
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lesions can easily occur. As bedding is usually not sterile, secondary bacterial infections are
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also common. The therapy should not only reduce the possible excess weight, but also keep
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the rabbits on a dry bedding such as cotton, which does not lead to further lesions. However,
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even with this material, care should be taken to ensure that the bedding is changed regularly.
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Mayner, R., Hocking, P., Else, R., 2006. Foot pad dermatitis develops at an early age in commercial turkeys. Br Poultry Sci 47, 36-42. Meyer, H., 1988. Einflüsse von Luft- und Wasserqualität auf das Mastergebnis von Puten. Dtsch. Geflügelwirtsch. und Schweineprod. 6, 159 - 162 Morton, D.B., Griffiths, P.H., 1985. Guidelines on the recognition of pain, distress and discomfort in experimental animal and an hypothesis for assessment. Vet Rec 116, 431-436. Ras, T., Van De Ven, M., Patterson-Kane, E.G., Nelson, K., 2002. Rats' preferences for corn versus wood-based bedding and nesting materials. Lab Anim 36, 420 - 425.
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Rosell, J.M., de la Fuente, L. F., 2013. Assessing Ulcerative Pododermatitis of Breeding Rabbits. Animals 3, 318-325.
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Schlolaut, W., 2002. The domestic rabbit as a farm animal. www.lohmann-information.com, 1 - 11.
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Sound H., 2008. Rabbit. In: Diseases of pets, 7th edition. Gabrisch K, Zwart P, ed. Hanover:
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Schlütersche, 1 - 47. Szendrő Z.S., Trocino A., Hoy, S.T., Xiccato, G., Villagrá, A., Maertens, L., 2019. A review of recent
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research outcomes on the housing of farmed domestic Rabbits: reproducing does. World Rabbit
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Science 27, 1-14. Tiedemann, H., 1991. Erdwärmetauscher für Schweineställe. in: Kuratorium für Technik und
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f
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Bauwesen in der Landwirschaft (Hrsg.): KTBL-Schrift 340. Landwirtschaftsverlag GmbH,
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Münster, S. 89 – 103
e-
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Van Caenegem, L., Wechsler, B., 2000. Stallklimawerte und ihre Berechnung. Eidgenössische Forschungsanstalt für Agrarwirtschaft und Landtechnik, Tänikon, S. 9 - 41
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pr
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Wolf, P., 2005. Nutrition of pets - obesity. Small animal concretely 1, 19 - 22.
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Wolf, P., Kamphues, J., 2009. Inquiries from the veterinary feeding consultation to small rodents.
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Small animal practice, 54, 317 - 321.
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Youssef, I., 2001. Experimental studies on effects of diet composition and litter quality on development and severity of foot pad dermatitis in growing turkeys. .Dissertation, Tierärztliche
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Hochschule, Hannover, Germany.
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Table 1: Chemical composition of hay and mixed feed offered to rabbits during the
352
experimental trial
353
DM
CA
CP
CL
CF
diet hay
NfE
Ca
P
Mg
Na
K
Content in g/kg Dry matter 920
45.5
101
9.16
325
519
4.25
3.57
1.71
1.51
16.2
879
77.7
160
18.7
142
602
10.3
5.04
2.23
2.20
14.1
Mixed
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diet
DM= dry matter, CA=crude ash, CP=crude protein, CL=crude fat, CF= crude fibre,
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NfE=Nitrogen-free extracts
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Table 2: Score for assessment of footpad health, based on degree of contamination and lesions
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(according to Masthoff et al., 2015)
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degree of contamination
Score
Lesions
0
neat
0
Without
1
slightly soiled
1
lightly injured
2
moderately contaminated
2
moderately injured
3
heavily soiled
3
Severe injured
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Table 3: Evaluation of the foot pad health of rabbits in relation to the bedding material.
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Values are expressed as Mean±S.D.
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Foot pad health Bedding material
contamination
lesions
0.9a ± 0.3
2.1a ± 0.5
wood shavings
1.0a ± 0.2
1.9a ± 0.4
bark mulch
2.4b ± 0.3
1.7a ± 0.5
bark mulch + raspberry leaves
2.0b ± 0.2
1.5a ± 0.2
cotton
0.1c ± 0.0
0.6b ± 0.2
a,b,c
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0.05).
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straw
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Different letter in the same row indicate that difference of means are statistically significant (p<
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Figure captions
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Fig. 1 Footpad lesions of a rabbit
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Fig. 2 Litter material for rabbit housing; a) straw, b) wood shavings, c) bark bulk with added
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raspberry leaves, d) cotton
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Fig. 3 Dry matter (DM) content in bulk samples of the several litter materials: straw (S), wood
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shaving (H), bark bulk (R), bark bulk with raspberry leaves (R+I), cotton (B). DM content
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significantly differs between bedding materials (p<0.05).
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Fig. 4 Ammonia content of several litter materials: straw (S), wood shaving (H), bark bulk
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(R), bark bulk with raspberry leaves (R+I), cotton (B). NH3 (ppm) content significantly differs
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between bedding materials (p<0.05).
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Highlights
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Footpad lesions are an issue for health and welfare of both farmed and pet rabbits
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The quality of litter acts as a co-factor on the onset of lesions.
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Body weight and physical characteristic the bedding material show an interplay in the development of
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In descending order cotton, wood shavings, coarse bark bulk and straw displayed best to least
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favourable characteristics
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bedding material
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High DM content and low NH3 are desired physico-chemical parameters to evaluate the fitness of
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pododermatitis
Figure 1
Figure 2
Figure 3
Figure 4
P. Wolf, R. Speers, M.G. Cappai PII:
S0034-5288(19)30700-3
DOI:
https://doi.org/10.1016/j.rvsc.2019.12.004
Reference:
YRVSC 3933
To appear in:
Research in Veterinary Science
Received date:
15 July 2019
Revised date:
6 October 2019
Accepted date:
1 December 2019
Please cite this article as: P. Wolf, R. Speers and M.G. Cappai, Influence of different types of bedding material on the prevalence of pododermatitis in rabbits, Research in Veterinary Science (2019), https://doi.org/10.1016/j.rvsc.2019.12.004
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Journal Pre-proof 1
Influence of different types of bedding material on the prevalence of
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pododermatitis in rabbits
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P. Wolf1, R. Speers2, M. G. Cappai3
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Running head: Wolf et al., FPD in rabbits
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*Correspondence:
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Prof. Dr. Petra Wolf, Chair of Nutrition Physiology and Animal Nutrition, University of
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Rostock, Justus-von-Liebig Weg 6b, 18059 Rostock, Germany. Tel: +49 381 498 3320
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Fax: +49 381 498 3322
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E-mail address: [email protected]
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1
Chair of Nutrition Physiology and Animal Nutrition, University of Rostock, Germany
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Speers Hoff, Stelle, Germany
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Chair of Animal Nutrition, Department of Veterinary Medicine, University of Sassari, Italy.
Journal Pre-proof ABSTRACT
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Pododermatitis is a disorder with a complex etiology, because potentially determined by
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various factors such as posture, nutrition and genetics. In the case of presence of pododermal
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lesions, it is often noticed that rabbits go to eat at the bowl less frequently, but an evident
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weight loss is not always perceptible. In fact, similarly to poultry, overweight animals seem to
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be prone to the onset of pododermatitis. An experiment was carried out to test the effect of
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different types of bedding material (straw vs. wood shavings vs. coarse bark mulch vs. cotton)
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on the prevalence of pododermatitis in 30 fattening Separator rabbits. Once a week, the four
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experimental runs were assessed for contamination (macroscopic contamination by
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faeces/urine/litter) as well as for lesion scoring of the footpad. In addition, the water and
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ammonia binding behaviour of bedding was tested. The most favourable values as to dry
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matter, NH3 (p<0.05) and also scoring of the litter were generally observed when cotton was
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used as bedding material. This is probably due to the high water binding capacity, the faster
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water release and the structural effects of the material itself (softness). By contrast, the
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structure of the coarse bark mulch was not suitable for binding liquids (especially urine) and
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led to increased contamination of the barrels. These results suggest that rabbits with an
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increased tendency to sore soles should be kept on bedding materials with desirable physical
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properties (e.g. cotton litter).
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Key words
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Pododermatitis, sore legs, bedding material, rabbit, housing
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Journal Pre-proof INTRODUCTION
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The occurrence of lesions in the area of the sole is a common health problem in rabbits,
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especially in those kept as pets, in which skin injuries are usually accompanied by secondary
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mixed infections, not rarely ending in the organization into purulent abscesses and ulceration
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(Wolf and Kamphues, 2009). Such clinical condition and the development of lesions are
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similar in farmed rabbits. The independent scientific opinion of the European Food Safety
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Authority issued in 2005 reported that the prevalence of footpad lesions in intensively farmed
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rabbits ranged between the 5% and the 15%, but numbers could increase when also hock
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lesions were considered, the latter being reported to be the commonest cause of culling. In
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farmed rabbits, the prevalence of sole lesions mainly involve breeding rabbits, especially
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does, due to the longer life span, higher body weight (in comparison with growing rabbits)
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and prolonged and continuous contact with the litter (Rosell and De La Fuente, 2013). In a
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report of 2013 on footpad lesion prevalence in farmed rabbits conducted in Spain, a
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significant decrease was pointed out over a decade period, thanks to the improvement of
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husbandry conditions (Rosell and De La Fuente, 2013). Pododermatitis and, in general,
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footpad lesions are associated with evident pain and suffering (Morton and Griffiths 1985)
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and represent an issue of both animal health and welfare. At present, pododermatitis in rabbits
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continues to represent an issue but the new flooring systems appear to be a good strategy to
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improve health and welfare conditions of does (Masthoff and Hoy, 2019). In addition to
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genetic factors, keeping conditions of animals may also act as predisposing factors (Masthoff
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et al. 2017). Similarly to poultry production, the development of the disease can be
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accelerated in the case of overweight animals (Wolf, 2005). These conditions have already
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been identified in productive poultry as the actual cause of foot pad lesions (Kamphues et al.
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2011, Youssef 2011) as well as in game birds like captive partridges (Cappai et al., 2018).
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In farmed rabbits partial or inadequate change of bedding material may be a predisposing
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cause to increase the prevalence of pododermatitis at farm level. Thus, animal sitting on wet
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Journal Pre-proof litter for a long time in a confined space is acknowledged to be critical. In fact, NH3 is irritant
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for skin and mucosa and may be toxic when gaseous concentrations increase. Bacterial
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fermentations occurring in the litter contribute to form gaseous NH 3 from urine and faeces,
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responsible to induce a mucociliar reflex and apnea in the rabbit (Lindeberg et al., 1987),
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often leading to conjunctivitis and respiratory disease (Hartung, 1990; Martens, 2000). High
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concentrations of NH3 in the stable air can impair the health and thus the performance of
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animals (Tiedemann 1991). As to pathophysiology, increased NH3 concentrations primarily
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damage the respiratory tract and the defense system of upper ways as well as of trachea and
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lungs. Almost all respiratory diseases are adversely affected by higher concentrations of NH3
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(Van Caenegem and Wechsler 2000), as NH3 has keratolytic properties and irritates both skin
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and mucous membranes (Tiedemann 1991). Van Caenegem and Wechsler (2000) explain this
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toxic effect of ammonia with the formation of NH4OH- on the moist mucous membranes,
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which has a liquefying effect on cell proteins and can thus lead to deep necrosis. In high doses
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NH3 can lead to an increase in blood pressure and respiratory rate as well as to burns of the
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upper respiratory tract, which in turn opens the way for infections (Tiedemann 1991).
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Ammonia can also have a negative effect on the function of the blood by reducing the number
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of erythrocytes and the oxidation capacity of haemoglobin. A neurotoxic effect in the form of
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nervousness was also mentioned (Adam 1973; Meyer 1988). In addition, obese animals move
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less in the available space and therefore sit on a given spot, so that a long lasting pressure on
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the soles of the feet can be exerted under own body mass (Drescher and Schlender-Böbbis
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1996). In view of these reasons, footrest and small sized group of animals were proposed to
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be introduced and in farm integrated strategies were recently reviewed (Szendrő et al., 2019)
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in light of efficacious measures to decrease the prevalence of footpad lesions of does (Figure
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1). In the absence of EU Directives on rabbit protection, at present several European countries
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promulgated own guidelines aiming to improve rabbit health and welfare. In 2017, the
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European Parliament issued a resolution to change conventional caging systems with cages
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respectful of rabbit health, normal behaviour and welfare based on scientific reference in the
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field (Szendrő et al., 2019). In light of this background, also bedding material plays a crucial
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role in the interplay of surface to surface contact, which should be comfortable and safe,
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hygienic and economic. For example, inappropriate bedding materials with low absorbent
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capacity or thin bedding material in plastic cages (Drescher 1993) quickly lead animals to sit on wet litters and the soles of their feet kept damp for long periods (Masthoff et al. 2015).
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In addition, the wet bedding also causes conversion of urine and faeces, which can lead to
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NH3 pollution of the environment. In fact, NH3 is irritant for skin and mucosa and may be
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toxic when gaseous concentrations increase. Bacterial fermentations occurring in the litter
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contribute to form gaseous NH3 from urine and faeces, responsible to induce a mucociliar
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reflex and apnea in the rabbit (Lindberg et al., 1987), often leading to conjunctivitis and
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respiratory disease (Hartung, 1990; Martens, 2000). High concentrations of NH3 in the stable
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air can impair the health and thus the performance of animals (Tiedemann 1991). Increased
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NH3 concentrations primarily damage the respiratory tract and the defense system of the
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trachea and lungs. Almost all respiratory diseases are adversely affected by higher
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concentrations of NH3 (Van Caenegem and Wechsler 2000), as NH3 has keratolytic properties
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and irritates and irritates the skin and mucous membranes (Tiedemann 1991). Van Caenegem
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and Wechsler (2000) explain this toxic effect of ammonia with the formation of NH 4OH- on
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the moist mucous membranes, which has a liquefying effect on cell proteins and can thus lead
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to deep necrosis. In high doses NH3 can lead to an increase in blood pressure and respiratory
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rate as well as to burns of the upper respiratory tract, which in turn opens the way for
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infections (Tiedemann 1991). Ammonia can also have a negative effect on the function of the
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blood by reducing the number of erythrocytes and the oxidation capacity of haemoglobin. A
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neurotoxic effect in the form of nervousness was also mentioned (Adam 1973; Meyer 1988).
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The present study aimed to test the influence of different bedding materials (straw vs. wood
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shavings vs. coarse bark mulch vs. cotton) on litter quality and foot health of rabbits.
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MATERIAL AND METHODS
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Animals and diet
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This trial enrolled 30 adult (age 7.7 ±0.48 months, min. 7 months n=10, max. 8 months n=20)
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female fattening rabbits (Separator rabbits; body mass 3.36 ± 0.81 kg). Animals received hay
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and a commercial mixed feed (MF) in pelleted form, based on green meal (see Table 1).
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Separator rabbits, all previously kept on perforated plastic floors, are a relatively small-sized
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breed. The soles of all animals were checked at the beginning of the experiment to ensure that
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only rabbits without previous damage to the soles of the feet were tested, as a pre-requisite for
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enrollment in the trial. Animals were kept in the original farm until completion of the
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experiment and underwent thorough health checks throughout the period.
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Food and water were offered fresh daily. The determination of feed and water consumption of
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the animals took place daily by subtracting feed left over from feed offered as well as water
135
remainders. The animals were kept in floored housing (enclosure size 200 x 100 x 100 cm - L
136
x H X W) in groups of 6 animals each. The floor was completely covered (litter height: 20
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cm) with straw (S; long stalks), wood shavings (H), bark mulch (R), bark mulch with
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raspberry leaves (R+I) and cotton material (B) (see Figure 2).
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Sampling method and laboratory analysis
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In order to simulate posture errors from practice (Endlicher, 2013), the bedding material was
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spread once a week, otherwise the bedding was left in place and care was taken to ensure that
142
the floor was completely covered. Litter samples were taken at fixed, defined places (in all 4
143
corners of the floor, 15 cm from the edge, in the middle and 3 samples each within a radius of
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10 cm around the feed and water bowl), combined to a pooled sample and processed for the
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analyses. The dry matter content was determined in accordance with the VDLUFA
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Journal Pre-proof association regulations by drying the material in weight-constant porcelain bars at 103 °C up
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to a constant weight. To measure the ammonia content at a distance of 20 cm above the
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bedding (about eye level of the rabbits), the sample was placed in an airtight incubator. After
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6 hours, the NH3 concentration in the air cube was read with the aid of a gas detector tube
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(Dräger-Röhrchen Ammoniak 5/a, Dräger, Lübeck), the end of which was held 20 cm above
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the bedding, and the associated gas pump, a small bellows pump (Dräger gas detector pump
152
accuro, Dräger, Lübeck).
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At the beginning of the test and once a week during the 12-week test period, the health of the
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pad of the foot was assessed. The footpad was scored according to Masthoff et al. (2015), in
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which both the lesions and the degree of contact material of the soles of the feet were taken
156
into account (see Table 2).
157
The assessment of the footpad health was always carried out by the same person in order to
158
exclude possible subjective influences.
159
Analysis of data and statistics
160
The statistical evaluation was carried out with SAS Version 9.4 (SAS Institute Inc., 2012).
161
The Shapiro-Wilk test was used to check the normal distribution. Furthermore, the data were
162
subjected to a two-factorial analysis (ANOVA). In all statistical analyses effects were judged
163
to be significant at p < 0.05.
164
RESULTS
165
With an identical feed supply and a comparable water consumption, it was possible to
166
determine significantly different dry matter contents for the various bedding materials
167
deployed (see Figure 3). The significantly highest dry matter content could be determined
168
with 67.6% using cotton. The bedding was slightly damper when bark mulch was used,
169
whereby the addition of raspberry leaves had no effect on the dry matter content (59.6% for
170
pure bark mulch, 60.2% for bark mulch with raspberry leaves). There were no significant
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differences in dry matter content between the long-stacked straw and the wood chips. Both
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Journal Pre-proof bedding materials had the significantly highest moisture content compared to bark mulch and
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cotton bedding.
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No statistically significant differences could be found between groups as to the ammonia
175
concentrations (see Figure 4). However, cotton litter showed the highest binding capacity for
176
ammonia, with the lowest ammonia content of 1.15 ppm measured 20 cm above the litter. The
177
highest concentrations could be found in the air above the straw.
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Once a week the soles of the rabbits' feet were assessed. In addition to the degree of
179
contamination, particular attention was paid to lesions (see Table 3).
180
The rabbits kept on cotton litter, followed by straw and wood shavings had the significantly
181
lowest degree of contamination of the legs. These are materials that per se have no colouring,
182
so the legs cannot discolour. The situation was different with bark mulch. This has a certain
183
inherent colour which, in combination with the humic acids, led to a discolouration of the legs
184
(but also of the lower abdomen when lying down). A pollution by excrement and urine took
185
place alongside, but since animals in each group received identical feeds, the effects should
186
not be linked to the diet, but can be led back primarily to the bedding materials.
187
DISCUSSION
188
The differences observed in the DM content of the different types of bedding material are
189
probably due to the different compaction of the material itself, like previously reported by
190
Abd El-Wahab in poultry and turkeys (2011). The spaces between the individual particles of
191
the bark mulch allow air to circulate between the individual particles, resulting in faster water
192
evaporation and consequently in faster drying. With wood chips, on the other hand, the
193
material is compacted. While bark mulch also has a porous structure, straw - especially long-
194
stalked qualities - has a lower water retention capacity.
195
Also ammonia content over bedding differed according bedding material used. Straw is one of
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the most frequently used bedding materials in pet rabbits (Berghoff 1989; Beynon and Cooper
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1997; Schall 2008), offers the animals additional employment opportunities (playing,
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Journal Pre-proof gnawing, digging), thus enabling species-typical behaviour and enriching the animals'
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environment (ARRP 2003). In this case, however, it did not contribute to a reduced ammonia
200
content in the air.
201
Studies by Lipman (1999) and Ras et al. (2002) showed that higher NH 3 concentrations were
202
found after the use of wood shavings than, for example, in bark mulch, which is in line with
203
the results. This was followed by cellulose bedding and corn cob substrate, which produced
204
the lowest NH3 emissions. In the present investigations, the use of cotton had the clearest
205
effects on NH3 release. Various mechanisms may be responsible for this observation. Not
206
only liquid, but also urea can be absorbed by the bedding, which is therefore no longer
207
available to microorganisms. It is therefore conceivable that more urea was absorbed by
208
cotton than by straw. In addition, already formed NH3 can also be deposited by the bedding
209
and thus prevented from entering the gas phase (ARRP, 2003; Kaliste, 2004). Thus it would
210
be possible that NH3 was formed, but was absorbed by the cotton to a greater extent than by
211
straw and therefore could not enter the airspace of the incubator.
212
Minimizing the NH3 concentration in the vicinity of rabbits is an important prophylactic
213
measure against the development of respiratory diseases, conjunctivitis and mucous
214
membrane irritations (Hartung, 1990; Marten, 2000).
215
Rabbits react very sensitively to increased NH3 concentrations in the air (Lange 2005) and
216
avoid these areas if possible (Bessei et al. 2001). Since rabbits are mostly kept in cages in
217
groups and therefore have little possibility to move to areas with lower NH 3 concentrations, it
218
can be assumed that a reduction of NH3 emissions would increase the well-being and normal
219
behaviour of animals.
220
The influence of NH3 on the development of dermatitis of the sole surfaces is discussed in
221
various animal species, e.g. turkeys, but in rabbits no investigations were available. However,
222
it can be assumed that identical patho-mechanisms exist here. Overall, unsuitable soils, lack
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Journal Pre-proof of bedding, stress and obesity are regarded as direct causes of so-called "sore legs" (Schlolaut,
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1998; Wolf, 2005).
225
The rabbits showed the highest degree of lesions on the straw bedding. This is probably due
226
to a mechanical noxious effect of the longer straws rather than to the higher moisture content
227
(see Figure 3).
228
Among the most discussed factors influencing the foot pad health of commercial poultry are
229
body weight, genetics, stable climate, stocking density, feeding, bedding material and bedding
230
moisture (Mayne et al., 2006; Große-Liesner, 2007; Berk, 2009; Youssef et al., 2011; Bellof
231
et al., 2014). In this context, the type of bedding and the associated water-binding capacity of
232
the material are becoming increasingly important. Studies on turkey hens have shown that
233
wood shavings and straw shavings or the combination of both types of bedding, in contrast to
234
lignocellulose, performed much worse as bedding and had a negative effect on the health of
235
the footpad (Berk, 2009). In this study, wood chips and straw also performed worse and are in
236
agreement with comparative reference.
237
Again in rabbits, it was shown that one of the decisive factors for the occurrence of
238
pododermatitis is the moisture to which the sole of the foot is exposed.
239
In commercial poultry, increased pododermatitis prevalence was observed with litter moisture
240
contents of more than 35% and an exposure of the animals of more than 4 hours per day (Abd
241
El-Wahab, 2011). Recommendations therefore assume that litter moisture should not exceed
242
30% to ensure good foot pad health. In this study, lesions were found in rabbits in all litter
243
materials except cotton, so that this limit seems justified in rabbit husbandry. However, the
244
incidence of lesions was not as pronounced as in poultry. This may be due to the fact that
245
rabbits spread the body mass over four legs, with the hind legs also having a larger contact
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surface. In addition, the soles of the rabbit's feet are hairy, while poultry lack this isolation.
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CONCLUSION
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increased pressure on the soles of the feet. This effect is particularly noticeable when the
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animals are also sitting on moist bedding. The footpad is usually protected by dense hair, but
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this mechanism is lost in overweight animals. If the skin in this area is permanently moist,
253
lesions can easily occur. As bedding is usually not sterile, secondary bacterial infections are
254
also common. The therapy should not only reduce the possible excess weight, but also keep
255
the rabbits on a dry bedding such as cotton, which does not lead to further lesions. However,
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even with this material, care should be taken to ensure that the bedding is changed regularly.
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REFERENCE
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Abd El-Wahab, A., 2011. Experimental studies on effects of diet composition (electrolyte contents),
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litter quality (type, moisture) and infection (coccidian) on the development and severity of foot
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pad dermatitis in young turkeys housed with or without floor heating, Diss. Med. Vet,
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Hannover, Germany.
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Berghoff, P.C., 1989.Veterinary pet practice. Volume 1: Small pets and their diseases, 1st edition. Berlin, Hamburg: Parey, 1 - 132. Berk, J., 2009. Effects of the litter species on animal health and animal performance in turkey hens. In:
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litter at different temperatures. In: Conference Proceedings 12th Workshop on the keeping and
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Münster, S. 89 – 103
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Van Caenegem, L., Wechsler, B., 2000. Stallklimawerte und ihre Berechnung. Eidgenössische Forschungsanstalt für Agrarwirtschaft und Landtechnik, Tänikon, S. 9 - 41
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Youssef, I., 2001. Experimental studies on effects of diet composition and litter quality on development and severity of foot pad dermatitis in growing turkeys. .Dissertation, Tierärztliche
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Hochschule, Hannover, Germany.
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Table 1: Chemical composition of hay and mixed feed offered to rabbits during the
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experimental trial
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DM
CA
CP
CL
CF
diet hay
NfE
Ca
P
Mg
Na
K
Content in g/kg Dry matter 920
45.5
101
9.16
325
519
4.25
3.57
1.71
1.51
16.2
879
77.7
160
18.7
142
602
10.3
5.04
2.23
2.20
14.1
Mixed
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diet
DM= dry matter, CA=crude ash, CP=crude protein, CL=crude fat, CF= crude fibre,
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NfE=Nitrogen-free extracts
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Table 2: Score for assessment of footpad health, based on degree of contamination and lesions
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(according to Masthoff et al., 2015)
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degree of contamination
Score
Lesions
0
neat
0
Without
1
slightly soiled
1
lightly injured
2
moderately contaminated
2
moderately injured
3
heavily soiled
3
Severe injured
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Score
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Table 3: Evaluation of the foot pad health of rabbits in relation to the bedding material.
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Values are expressed as Mean±S.D.
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Foot pad health Bedding material
contamination
lesions
0.9a ± 0.3
2.1a ± 0.5
wood shavings
1.0a ± 0.2
1.9a ± 0.4
bark mulch
2.4b ± 0.3
1.7a ± 0.5
bark mulch + raspberry leaves
2.0b ± 0.2
1.5a ± 0.2
cotton
0.1c ± 0.0
0.6b ± 0.2
a,b,c
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0.05).
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straw
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Different letter in the same row indicate that difference of means are statistically significant (p<
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Figure captions
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Fig. 1 Footpad lesions of a rabbit
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Fig. 2 Litter material for rabbit housing; a) straw, b) wood shavings, c) bark bulk with added
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raspberry leaves, d) cotton
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Fig. 3 Dry matter (DM) content in bulk samples of the several litter materials: straw (S), wood
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shaving (H), bark bulk (R), bark bulk with raspberry leaves (R+I), cotton (B). DM content
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significantly differs between bedding materials (p<0.05).
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Fig. 4 Ammonia content of several litter materials: straw (S), wood shaving (H), bark bulk
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(R), bark bulk with raspberry leaves (R+I), cotton (B). NH3 (ppm) content significantly differs
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between bedding materials (p<0.05).
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Highlights
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Footpad lesions are an issue for health and welfare of both farmed and pet rabbits
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The quality of litter acts as a co-factor on the onset of lesions.
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Body weight and physical characteristic the bedding material show an interplay in the development of
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In descending order cotton, wood shavings, coarse bark bulk and straw displayed best to least
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favourable characteristics
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bedding material
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High DM content and low NH3 are desired physico-chemical parameters to evaluate the fitness of
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pododermatitis
Figure 1
Figure 2
Figure 3
Figure 4