Helminth control practices and infections in growing pigs in France

Livestock Production Science 81 (2003) 99–104 www.elsevier.com / locate / livprodsci

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Helminth control practices and infections in growing pigs in France P.A. Belœil, C. Chauvin, C. Fablet, J.P. Jolly, E. Eveno, F. Madec, J.M. Reperant* ˆ , BP 53, 22440 Ploufragan, France French Agency for Food Safety (AFSSA), Pig and Poultry Veterinary Research Laboratory, Zoopole Received 22 October 2001; received in revised form 29 July 2002; accepted 13 August 2002

Abstract Internal parasite control practices and helminth infestations were investigated in 78 pig farms in France. Pooled faecal samples were taken from pens housing 16-week-old pigs. Samples were examined by coproscopy. Farm practices were checked for the risk factors of infestation previously described in literature. Information was obtained during a visit of the facilities and an interview with the farm owner / manager. Anthelmintics were used in most herds (97%). Treatments were routinely prescribed, such as flubendazole in the diet of the piglets and ivermectin for sows. Finisher pig infestation may occur despite these treatments: five samples in our study contained helminth eggs, four samples contained strongylid eggs (Hyostrongylus rubidus or Oesophagostomum spp.), and one sample contained Trichuris suis eggs. We can conclude that helminths are controlled, but that parasites can still be present in indoor intensive pig operations. Hygiene efforts must be continued.  2002 Elsevier Science B.V. All rights reserved. Keywords: Parasitology; Helminths; Anthelmintics; Finishing pigs

1. Introduction Endoparasitic infestations in pigs, especially with helminths, are still common in Europe (Joachim et al., 2001). Indoor intensive rearing is considered to be a protective system compared to outdoor rearing systems (Roepstorff and Jorsal, 1989; Roepstorff and Nansen, 1994; Nansen and Roepstorff, 1999).

*Corresponding author. Tel.: 1 33-296-016-208; fax: 1 33296-016-253. E-mail address: [email protected] (J.M. Reperant).

Routine anthelmintic use in animal feed should effectively prevent infestation. However, studies from Australia, Denmark and Germany have reported that helminths may be found in intensive indoor pig farms (Mercy et al., 1989; Roepstorff and Jorsal, 1989; Joachim et al., 2001). Helminth infestation can cause economic losses (Stewart et al., 1985; Stewart and Hale, 1988) or could be a risk factor for other digestive tract diseases, such as Lawsonia intracellularis infection (Mansfield and Urban, 1996; Pearce, 1999) or intestinal carriage of Salmonella (Steenhard et al., 2002). As the most recent study on helminth infestation prevalence and parasite control practices in France was published in 1976 (Raynaud and Jolivet, 1976),

0301-6226 / 02 / $ – see front matter  2002 Elsevier Science B.V. All rights reserved. doi:10.1016/S0301-6226(02)00192-6

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an exploratory survey was carried out in fattening pigs raised in 78 intensive indoor farrow-to-finish farms. In order to determine whether management practices in the farms surveyed allowed pig helminth infestation, presence of helminths in growing pig faeces was assessed and farm practices were checked for previously described risk factors for infestation (Jacobs and Dunn, 1968; Mercy et al., 1989; Pearce, 1999; Joachim et al., 2001).

2. Materials and methods

2.1. Farms A total of 78 indoor farrow-to-finish pig farms were involved in the survey. They were affiliated to 17 pig production or feedstuff companies. The farms were located in the French regions of Bretagne, Pays ´ ´ de la Loire, Nord-Pas de Calais, and Midi-Pyrenees. They were visited between January and June 2001. They were selected according to the farmer’s and the farm veterinary surgeon’s willingness to cooperate. A retrospective review of their technical profile (number of sows, live-born piglets / litter, piglets weaned / sow / year, average daily weight gain from 25 to 105 kg, average daily intake from 25 to 105 kg) showed no major difference compared to the wider national reference group (Anonymous, 2001), except for the number of sows which was greater in our survey.

2.2. Data collection Information on anthelmintic treatments, presence of rodents and housing conditions were obtained by means of a questionnaire. The facilities were checked for rodent faeces in order to confirm the farmers’ reports. The quality of cleaning was also assessed visually (presence or absence of dung remaining from a previous batch of pigs) by inspecting fattening rooms just before restocking. Veterinary service officers at slaughterhouses provided the inspection reports concerning the liver (milk spots due to Ascaris suum) of pigs from the farms surveyed.

2.3. Faecal sampling and examination of pen faecal samples Faecal samples were collected from 16-week-old pigs. The mean age at sampling was 116.7 days (S.D. 5.3) i.e., 6–7 weeks after arrival of the piglets in the fattening house at an average age of 70 days. In fattening rooms, five fresh faecal samples were randomly collected from five different places on the floor and were pooled. The pooled sample, refrigerated until examination (at 5 8C), was submitted to a flotation test in saturated sodium chloride solution (Thienpont et al., 1979). After homogenisation, centrifugation and examination of the supernatant, the positive samples were submitted to the McMaster technique (Thienpont et al., 1979) to determine the number of eggs per gram of faeces. Three g of each pooled sample were suspended in 42 ml of saturated sodium chloride solution, filtered, homogenised and the eggs were counted in the McMaster chambers. Whenever eggs were detected, identification as strongylid, Trichurissuis or Ascaris suum eggs was confirmed by a second operator. Measurements were performed using an ocular micrometer and photographs were taken.

3. Results

3.1. Management and housing: worm control programmes and treatments Housing and flooring systems, hygiene practices, observations recorded and anthelmintic treatments are shown in Table 1. Anthelmintic drugs were used in 97% of the 78 farms investigated (76 / 78). One farmer reported that he never treated breeding sows or gilts. Sows were treated either in pregnancy facilities (64%) or in the farrowing rooms (33%). Fifty-five percent of administrations were made by injection, 45% per os via feed or water. Twenty-six percent of farmers never treated growing and finishing pigs. Grower pigs were mainly treated by infeed drug administration. Sixtyseven percent of first-phase post-weaning feed contained an anthelmintic drug. Ten percent of farmers applied an anthelmintic treatment at the fattening

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Table 1 Anthelmintic treatments, hygiene practices, observations recorded and housing and flooring systems in the 78 farms surveyed Definition of variable

Level

n

%

Infested farms a a b c d e

Anthelmintic treatment of: Gilts during acclimatisation period Boar Sows Growers Fattening pigs Hygiene practices: Sows washed before entering the farrowing room Frequency of dung removal during the lactation period

Rodent control

Observations: Presence of rodents observed by farmers Residual dung in the fattening rooms when restocking Housing and flooring systems: Gilts during acclimatisation period

Sows in service period

Pregnant sows

Post-weaning unit

Fattening unit

a

Yes No Yes No Yes No Yes No Yes No

40 38 65 13 76 2 56 22 10 68

51 49 83 17 97 3 72 28 13 87

– a a – – a – a – a

– b b – b – b – – b

c – – c – c c – – c

– d d – d – d – – d

– e – e – e – e – e

Yes No Never Once a day Twice a day More frequently Contract with a specialized firm Use of baits No measure taken

30 48 9 33 35 1 50 26 2

39 61 12 42 45 1 64 33 3

a – – a – – a – –

– b – b – – b – –

– c – c – – c – –

– d – d – – d – –

e – – e – – e – –

Observed Not observed Presence Absence

51 65 27 35 24 31 54 69

a – – a

b – b –

c – – c

d – d –

– e e –

Confined in stalls on slatted floor Confined in stalls on partially slatted floor Confined in stalls 1 straw Group housing on slatted floor Group housing on partially slatted floor Group housing 1 straw Outdoor 1 straw Confined in stalls on slatted floor Confined in stalls on partially slatted floor Group housing on slatted floor Group housing on partially slatted floor Group housing 1 straw Confined in stalls on slatted floor Confined in stalls on partially slatted floor Group housing on slatted floor Group housing on partially slatted floor Group housing 1 straw Slatted floor Partially slatted floor Straw or bedding Slatted floor Partially slatted floor Straw or bedding

12 6 28 2 6 21 3 47 17 4 4 4 43 17 9 3 6 67 5 6 72 2 4

– – – – – a – – a – – – a – – – – a – – a – –

– – – b – – – b – – – – b – – – – b – – b – –

c – – – – – – c – – – – c – – – – c – – c – –

– – d – – – – – d – – – d – – – – d – – d – –

– – – – – e – – – e – – e – – – – – – e e – –

Farm a had Trichurus suis eggs, b–e had strongylid eggs (Hyostrongylus rubidus or Oesophagostomum spp.).

15 8 36 3 8 27 4 60 22 5 5 5 55 22 11 4 8 86 6 8 92 3 5

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Table 2 Deworming treatment: nature of anthelmintics depending on the type of pigs treated (n 5 78 farrow-to-finish herds, France) Class of pig

n

Anthelmintics used (%) Doramectin Ivermectin Flubendazole Fenbendazole Oxibendazole Levamisole

Gilts during acclimatisation period Boar Sows Growers Fattening pigs

40

12.5

50

15

–

17.5

5

65 76 56 10

7 8 – –

57 45 – –

9 17 71.5 30

10 7 – –

12 18 27 20

5 5 1.5 50

stage in addition to an infeed post-weaning drug administration. The distribution of anthelmintic use according to the type of pigs treated is shown in Table 2.

3.2. Parasite infestation Positive samples were found on five farms. One sample contained Trichuris suis eggs and four samples contained Hyostrongylus rubidus or Oesophagostomum spp. with all egg counts per gram of faeces less than 400 eggs per gram. No liver lesion was reported for the 20 farms for which the required information was obtained at slaughterhouse. Due to the small number of positive samples, no statistical analysis was performed to determine risk factors of infestation. The status of the positive herds regarding certain hygiene, treatment and housing practices is presented in Table 1.

4. Discussion Few data are available about helminth infestations and deworming practices in indoor intensive all-in / all-out systems. Prevalences of helminth infestations have been published for heterogeneous management systems, but not all indoor intensive all-in / all-out systems, in Denmark (Roepstorff and Jorsal, 1989) and UK (Pattison et al., 1980) in the 1980s and recently in Germany (Joachim et al., 2001). In the last survey carried out in France in the 1970s (Raynaud and Jolivet, 1976), 25 to 50% of farms with control measures were found to be positive with strongylid eggs in faecal samples from growing pigs.

Rearing conditions and parasite control practices have certainly changed considerably since 1976. The results of the present study show that, although routine anthelmintic treatments are commonly used, they are not systematic. The rate of anthelmintic use varied according to animal category: sows were the most frequently treated, fatteners were the least frequently treated. The choice of anthelmintic also depended on the animals concerned with various anthelmintics used for the same type of animal and several anthelmintics used in the same farm. Note that this study was conducted before approval of ivermectin premix, and the rate of use of ivermectin may now be different. The small number of samples found to be positive in this study could be related to the parasite control practices described in our study. Moreover, as regards the characteristics of the farms surveyed, housing and flooring systems corresponded to intensive farms with a low exposure to internal parasites. Infestation should not have occurred in view of the anthelmintic treatments given in farms that tested positive (B–E), but this infestation could be explained by a severe lack of hygiene. It has been previously demonstrated that re-infestation could not be prevented during the fattening weeks following treatment with flubendazole, probably due to infectious stages left over from previous fattening periods, despite cleaning and disinfection (Joachim et al., 2001). The role of breeding stock is also certainly important, as sows may constitute reservoirs of infestation in the herd (Joachim et al., 2001). Internal parasite infestation is therefore possible in intensive farms as shown here, especially when the worm control programme does not focus on providing a

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‘clean’ sow at farrowing. This study showed that hygiene practices were not fully applied: gilts in the acclimatisation phase were not systematically dewormed, gilts and sows were frequently not washed before farrowing. In addition, the efficacy of rodent control was incomplete and some housing systems, such as straw and semi-slatted floor, allow infestations. Rodents, such as mice, are possible paratenic hosts of parasites and rats can carry encysted larvae of Oesophagostomum spp. (Jacobs and Dunn, 1968). Housing weaners on slatted floors seems to be a protective factor against parasite infestation of grower-finishers compared to solid or partially slatted floors (Pearce, 1999; Joachim et al., 2001). However, the small number of samples tested positive may also have been underestimated. The purpose of our investigation was not to determine the prevalence of helminth infestation in the national herd, but to determine whether or not parasites could be found in faeces from young fatteners reared in modern intensive systems in which hygiene routines are supposed to be applied. Collection of pooled faeces from the floor of pens, less demanding for the operators involved, was therefore considered to be sufficient for the purposes of this study. A good assessment of helminth infestation in swine herds would have required sampling of breeding sows as well as offspring of different ages. An improved sampling scheme should also include individual rectal samples collected on a predefined proportion of animals in addition to pooled environmental faeces samples. The limited number of parasite species found in our faecal samples is in accordance with other studies (Mercy et al., 1989; Roepstorff and Jorsal, 1989; Nansen and Roepstorff, 1999; Joachim et al., 2001). No Ascaris suum eggs were found in our study, whereas several surveys have reported the presence of these eggs in pig herds and it has been considered to be commonplace (Corwin and Stewart, 1999; Joachim et al., 2001). Samples were taken 6 weeks after loading animals into fattening units, where infestation could have occurred. However, this time period of 6 weeks also corresponds to the prepatency period of Ascaris suum. Egg shedding despite early infestation would have been reduced. A small number of Ascaris suum positive samples to were also recorded in UK (Pattison et al., 1980) and

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positive pigs do not necessarily shed eggs (Roepstorff, 1998).

5. Conclusion When hygiene is good and management practices are appropriate in confined intensive swine facilities, the level of parasite infestation is low. By screening for nematodes in pig faeces and screening management practices, this study confirms that modern management and housing systems control the levels of infection to such low levels that production losses are unlikely. However, nematodes were found in growing pigs. Farmers and veterinarians should always be aware that parasites are present and should remain permanently attentive to management system and control practices in order to limit the risk of an increasing number of parasites, which would result in production losses.

Acknowledgements The authors gratefully acknowledge the farmers, veterinarians and technical staff of the companies for their cooperation.

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