Interactions between dietary fibre, endo-parasites and Lawsonia intracellularis bacteria in grower–finisher pigs

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Veterinary Parasitology 87 (1999) 51–61

Interactions between dietary fibre, endo-parasites and Lawsonia intracellularis bacteria in grower–finisher pigs G.P. Pearce ∗ Animal Science Research Centre, Harper Adams University College, Newport, Shropshire, TF10 8NB, UK Received 2 February 1999; accepted 28 June 1999

Abstract Samples of faeces and feed were collected from grower and finisher pigs kept on 25 commercial breeder–finisher units in the West-Midlands region of England. Faecal samples were examined for parasite eggs (Ascaris suis, Trichuris suum and strongylid species) using faecal flotation; and for Lawsonia intracellularis bacteria using the polymerase chain reaction. Feed samples were subjected to proximate analysis for energy, protein and fibre content and enzymic colorimetry for levels of non-starch polysaccharides (NSPs). Characteristics relating to housing, feeding and dung disposal systems and husbandry practices were recorded for each farm and assessed for their association with the presence of parasites and L. intracellularis at the herd level. Ascaris eggs were identified in 8% of herds, Trichuris eggs in 20% of herds and in strongylid eggs (Oesophogostomum and/or Hyostrongylus) in 44% of herds. Lawsonia intracellularis was detected in 15% of herds investigated. Herds positive for Trichuris and Ascaris had significantly lower levels of digestible energy and higher levels of neutral detergent fibre, total and insoluble NSPs in their diets than negative herds (p < 0.05). Housing weaners on slatted floors was associated with a significant decreased risk of parasite infection in grower–finishers (odds ratio = 0.09, p = 0.04) compared to housing on solid floors. The use of grower diets high in NSPs was associated with an increased risk of Trichuris infection (odds ratio = 27.6, p = 0.007). There was also an association at the herd level between infection with L. intracellularis and the presence of Trichuris eggs (odds ratio = 17.43, p = 0.069). It is concluded that control of dietary fibre intake (NSPs in particular) for growers and environmental hygiene (dung removal) for weaners appear to be the most important factors controlling parasite infection in grower–finisher pigs in the UK at present. The current move towards more straw based systems is thus likely to exacerbate the influence of these factors and is likely to result in

∗ Present address: Department of Agriculture, University of Aberdeen, MacRobert Building, 581King Street, Aberdeen, AB24 5UA, UK. Tel.: +1224-274123; fax: +1224-273731 E-mail address: [email protected] (G.P. Pearce)

0304-4017/99/$ – see front matter ©1999 Elsevier Science B.V. All rights reserved. PII: S 0 3 0 4 - 4 0 1 7 ( 9 9 ) 0 0 1 5 7 - 0

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G.P. Pearce / Veterinary Parasitology 87 (1999) 51–61

increased parasite infection in grower–finisher pigs in the UK. ©1999 Elsevier Science B.V. All rights reserved. Keywords: Pig-Nematoda; Dietary fibre; Lawsonia intracellularis; Feeding and nutrition

1. Introduction Endo-parasite infection in grower–finisher pigs can have a major economic impact on the profitability of pig production through reductions in performance (Stewart and Hale, 1988). Parasites such as Ascaris suum, Trichuris suis and Oesophogostomum are known to reduce daily liveweight gain and feed conversion efficiency at low levels of infection and can cause mortalities at higher levels (Pattison et al., 1980; Stewart et al., 1985; Stewart and Hale, 1988). It has been suggested that recent changes in pig husbandry methods towards extensification and increased use of straw bedding may lead to increased risk of endo-parasite infection in pigs kept under these conditions (White, 1994). Indeed the presence of bedding (Dangolla et al., 1996) and rearing outdoors (Roepstorff and Nansen, 1994) have been shown to be associated with higher prevalence of endo-parasite infections in pigs. While such conditions undoubtedly increase the degree of contact between pigs and infective larvae and/or eggs in faeces leading to greater infection rates, these conditions also lead to changes in dietary intake which may have important influences on the survival and pathogenicity of endo-parasites after ingestion by the pig. It has recently been demonstrated that high intakes of grass in pigs on pasture was associated with increased establishment of Ascarids and Oesophagostomum nematodes in outdoor-reared pigs (Petkevicius et al., 1996). Furthermore, experimental diets differing in their content of lignin and non-starch polysaccharides (NSPs) have been shown to influence the establishment of gut nematodes in pigs (Petkevicius et al., 1997). Grass and straw are characterised by having high levels of lignin and NSPs which are resistant to digestion by endogenous enzymes of the monogastric animal (Bach-Knudsen, 1997). The possible influence of varying levels of dietary fibre intake on the occurrence of endoparasites infection in pigs reared under commercial conditions has not been reported to date. It has recently been suggested that a synergism occurs between infection with endo-parasites and infection with enteric bacteria such as Lawsonia intracellularis in producing clinical signs of enteric disease and reduced performance in grower pigs (Mansfield and Urban, 1996). Furthermore, it has also been recently demonstrated that dietary levels of NSPs can have important influences on the pathogenicity of certain enteric bacteria in the pig (Pluske et al., 1996). Whether an interaction between endoparasites and enteric bacteria occurs under commercial conditions has not been investigated to date. The present study was designed to investigate the relationship between the occurrence of intestinal nematodes, infection with Lawsonia intracellularis bacteria and variations in the fibre (NSP) components of the diet fed to grower–finisher pigs kept under commercial conditions.

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2. Materials and methods 2.1. Farm selection Twenty-five commercial breeder–finisher units were selected from the data base of a previous study (Pearce, 1999) to participate in the present study. All units were situated in the West-Midlands region of England and were selected on the criteria of having grower–finisher pigs present on the farm and were chosen to represent the variety of husbandry systems existing in the UK at the present time as detailed elsewhere (Pearce, 1999). Data on farm characteristics such as herd size, housing, feeding and dung disposal systems was obtained utilising a postal questionnaire sent to each farm in advance of the farm visit. Each unit was visited once between November 1996 and July 1997 and samples of faeces and feed were collected at that time. Bulk faecal samples were collected from five pens housing grower pigs (30–45 kg liveweight) and five pens housing finisher pigs (45–90 kg liveweight). The number of eggs of Ascaris suum, Trichuris suis and strongylid species (Oesophagostomum and/or Hyostrongylus) in each bulked pen faecal sample were determined using the McMaster technique (with a minimum detection rate of 20 eggs per gram). Individual samples of freshly voided faeces were also collected from 10 grower pigs and 10 finisher pigs on each farm and examined for the presence of Lawsonia intracellularis bacteria using the polymerase chain reaction as reported by Jones et al. (1993). Separate samples of grower and finisher feed were also collected from each farm and their chemical composition was analysed using standard techniques. Levels of NSPs in each feed sample were analysed by enzyme-chemical colorimetry using the technique reported by Englyst (1989). 2.2. Statistical analysis Differences in the dietary components between parasite positive and negative herds were assessed using analysis of variance (Genstat 5, Rothamstead, UK). Correlations between dietary components and numbers of parasite eggs and/or L. intracellularis positive pigs were assessed using Spearman rank tests (Genstat 5, Rothamstead, UK). Data relating to farm characteristics were entered into the statistical data package ‘Epi-Info’Version 6.02 (CDC, Atlanta, Georgia, USA) (Dean et al., 1994) and associations with the occurrence of parasites and/or L. intracellularis were detected using Yates’ corrected chi-squared test. 3. Results Mean herd size of farms taking part in this study was 213.8 sows ± 21.3 (range 60–600 sows) with 70% of herds farrowing sows indoors and 30% farrowing outdoors. Tables 1 and 2 illustrate the farm characteristics and husbandry procedures employed on the farms utilised in this study. These variables were entered into the univariate analysis to identify factors associated with presence of endo-parasites and L. intracellularis at the herd level.

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G.P. Pearce / Veterinary Parasitology 87 (1999) 51–61

Table 1 Presence of parasite infection in herds with different facilities

Flooring Solid Straw/shavings Slatted

Weaners

Growers

Finishers

Parasite Parasite (n) +ve (%) −ve (%)

Parasite Parasite (n) +ve (%) −ve(%)

Parasite Parasite (n) +ve(%) −ve(%)

77a 66 39b

23 33 61

(13) (15) (18)

66 46 61

33 54 39

(15) (18) (13)

77a 69 36b

23 31 64

(13) (16) (14)

Dung removal system Manual Slurry

64 55

36 45

(11) (18)

45 60

55 40

(11) (15)

67 40

33 60

(12) (15)

Ventilation system Natural Controlled

57 43

43 57

(21) (7)

54 75

46 25

(24) (4)

54 60

46 40

(22) (5)

Feeding system Trough or hopper Floor Meal Wet Home mixed

58 50 0 0 62

42 50 0 0 38

(26) (2) (0) (0) (8)

58 0 61 0 54

42 100 39 0 46

(26) (1) (13) (0) (13)

58 0 54 50 57

42 100 46 50 43

(26) (1) (13) (8) (14)

Pen preparation between batches None/remove solids 44 56 Cleaning with water 61 39 Cleaning and disinfect 50 50 Rest after cleaning 54 46

(9) (18) (12) (11)

55 55 33 66

45 45 66 33

(18) (9) (6) (3)

53 62 40 66

47 48 60 33

(19) (8) (5) (3)

a b

Significant effect of factor on parasite status (OR > 1.0; p < 0.05). Significant protective effect of factor on parasite status (OR < 1.0; p < 0.01).

Strongylid species eggs were identified in 44% (11/25) of the herds, Trichuris suis in 20% (5/25) and Ascaris suum in 8% (2/25) (Table 3). Lawsonia intracellularis was detected in 15% (3/25) of herds examined (Table 3). As shown in Table 4, the grower diet used in herds which were positive for Ascaris suum had significantly lower levels of digestible energy (DE) (p < 0.001), and significantly higher levels of neutral detergent fibre (NDF) (p < 0.001), total NSPs (p < 0.01) and insoluble NSPs (p < 0.01) than Ascarid negative herds. Herds which were positive for Trichuris suis also had significantly higher levels of NDF (p < 0.05) and total NSPs (p < 0.05) in the grower diet and tended to have higher insoluble NSPs (p = 0.07) in the grower diet and lower DE in the finisher diet (p = 0.082) than Trichuris negative herds. Between herds, there was a significant correlation between the levels of NSPs in the grower diet and the number of Trichuris suis eggs found in the faeces samples (total NSP r = 0.65, p = 0.001; soluble NSPs, r = 0.60, p = 0.02; insoluble NSPs r = 0.64, p = 0.01). There was also a significant correlation at the herd level between the number of pigs positive for Lawsonia intracellularis and the number of Trichuris suis eggs found in the grower faeces (r = 0.83, p = 0.01) and finisher faeces (r = 0.90, p = 0.001) and the number of Ascaris suum eggs found in the finisher faeces (r = 0.94, p = 0.001).

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Table 2 Prevalence of parasite infection in herds utilising different husbandry procedures Parasite Positive

Negative (number of herds)

Herd size >200 sows 100–200 sows
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