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

Short communication

H elminth control practices and infections in growing pigs inFrance

*P.A. Belœil, C. Chauvin, C. Fablet, J.P. Jolly, E. Eveno, F. Madec, J.M. ReperantˆFrench Agency for Food Safety (AFSSA), Pig and Poultry Veterinary Research Laboratory, Zoopole, BP 53, 22440Ploufragan, France

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 faecalsamples were taken from pens housing 16-week-old pigs. Samples were examined by coproscopy. Farm practices werechecked for the risk factors of infestation previously described in literature. Information was obtained during a visit of thefacilities and an interview with the farm owner /manager. Anthelmintics were used in most herds (97%). Treatments wereroutinely prescribed, such as flubendazole in the diet of the piglets and ivermectin for sows. Finisher pig infestation mayoccur despite these treatments: five samples in our study contained helminth eggs, four samples contained strongylid eggs(Hyostrongylus rubidus or Oesophagostomum spp.), and one sample containedTrichuris suis eggs. We can conclude thathelminths are controlled, but that parasites can still be present in indoor intensive pig operations. Hygiene efforts must becontinued. 2002 Elsevier Science B.V. All rights reserved.

Keywords: Parasitology; Helminths; Anthelmintics; Finishing pigs

1 . Introduction Routine anthelmintic use in animal feed shouldeffectively prevent infestation. However, studies

Endoparasitic infestations in pigs, especially with from Australia, Denmark and Germany have re-helminths, are still common in Europe (Joachim et ported that helminths may be found in intensiveal., 2001). Indoor intensive rearing is considered to indoor pig farms (Mercy et al., 1989; Roepstorff andbe a protective system compared to outdoor rearing Jorsal, 1989; Joachim et al., 2001). Helminth infesta-systems (Roepstorff and Jorsal, 1989; Roepstorff and tion can cause economic losses (Stewart et al., 1985;Nansen, 1994; Nansen and Roepstorff, 1999). Stewart and Hale, 1988) or could be a risk factor for

other digestive tract diseases, such asLawsoniaintracellularis infection (Mansfield and Urban, 1996;Pearce, 1999) or intestinal carriage ofSalmonella(Steenhard et al., 2002).

*Corresponding author. Tel.:1 33-296-016-208; fax:1 33-As the most recent study on helminth infestation296-016-253.

prevalence and parasite control practices in FranceE-mail address: jm.reperant@ploufragant.afssa.fr(J.M. Reper-ant). 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

100 P.A. Belœil et al. / Livestock Production Science 81 (2003) 99–104

an exploratory survey was carried out in fattening 2 .3. Faecal sampling and examination of penpigs raised in 78 intensive indoor farrow-to-finish faecal samplesfarms. In order to determine whether managementpractices in the farms surveyed allowed pig helminth Faecal samples were collected from 16-week-oldinfestation, presence of helminths in growing pig pigs. The mean age at sampling was 116.7 daysfaeces was assessed and farm practices were checked (S.D. 5.3) i.e., 6–7 weeks after arrival of the pigletsfor previously described risk factors for infestation in the fattening house at an average age of 70 days.(Jacobs and Dunn, 1968; Mercy et al., 1989; Pearce, In fattening rooms, five fresh faecal samples were1999; Joachim et al., 2001). randomly collected from five different places on the

floor and were pooled. The pooled sample, refriger-ated until examination (at 58C), was submitted to aflotation test in saturated sodium chloride solution

2 . Materials and methods(Thienpont et al., 1979). After homogenisation,centrifugation and examination of the supernatant,

2 .1. Farmsthe positive samples were submitted to the McMastertechnique (Thienpont et al., 1979) to determine the

A total of 78 indoor farrow-to-finish pig farmsnumber of eggs per gram of faeces. Three g of each

were involved in the survey. They were affiliated topooled sample were suspended in 42 ml of saturated

17 pig production or feedstuff companies. The farmssodium chloride solution, filtered, homogenised and

were located in the French regions of Bretagne, Paysthe eggs were counted in the McMaster chambers.

´ ´de la Loire, Nord-Pas de Calais, and Midi-Pyrenees.Whenever eggs were detected, identification as

They were visited between January and June 2001.strongylid, Trichurissuis or Ascaris suum eggs was

They were selected according to the farmer’s and theconfirmed by a second operator. Measurements were

farm veterinary surgeon’s willingness to cooperate.performed using an ocular micrometer and photo-

A retrospective review of their technical profilegraphs were taken.

(number of sows, live-born piglets / litter, pigletsweaned/sow/year, average daily weight gain from25 to 105 kg, average daily intake from 25 to 105

3 . Resultskg) showed no major difference compared to thewider national reference group (Anonymous, 2001),

3 .1. Management and housing: worm controlexcept for the number of sows which was greater in

programmes and treatmentsour survey.

Housing and flooring systems, hygiene practices,2 .2. Data collection observations recorded and anthelmintic treatments

are shown in Table 1.Information on anthelmintic treatments, presence Anthelmintic drugs were used in 97% of the 78

of rodents and housing conditions were obtained by farms investigated (76/78). One farmer reported thatmeans of a questionnaire. The facilities were he never treated breeding sows or gilts. Sows werechecked for rodent faeces in order to confirm the treated either in pregnancy facilities (64%) or in thefarmers’ reports. The quality of cleaning was also farrowing rooms (33%). Fifty-five percent of ad-assessed visually (presence or absence of dung ministrations were made by injection, 45% per os viaremaining from a previous batch of pigs) by inspect- feed or water. Twenty-six percent of farmers nevering fattening rooms just before restocking. Veterinary treated growing and finishing pigs. Grower pigs wereservice officers at slaughterhouses provided the mainly treated by infeed drug administration. Sixty-inspection reports concerning the liver (milk spots seven percent of first-phase post-weaning feed con-due to Ascaris suum) of pigs from the farms tained an anthelmintic drug. Ten percent of farmerssurveyed. applied an anthelmintic treatment at the fattening

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

aDefinition of variable Level n % Infested farms

a b c d e

Anthelmintic treatment of:Gilts during acclimatisation period Yes 40 51 – – c – –

No 38 49 a b – d eBoar Yes 65 83 a b – d –

No 13 17 – – c – eSows Yes 76 97 – b – d –

No 2 3 a – c – eGrowers Yes 56 72 – b c d –

No 22 28 a – – – eFattening pigs Yes 10 13 – – – – –

No 68 87 a b c d e

Hygiene practices:Sows washed before entering the Yes 30 39 a – – – e

farrowing room No 48 61 – b c d –Frequency of dung removal during Never 9 12 – – – – –

the lactation period Once a day 33 42 a b c d eTwice a day 35 45 – – – – –More frequently 1 1 – – – – –

Rodent control Contract with a specialized firm 50 64 a b c d eUse of baits 26 33 – – – – –No measure taken 2 3 – – – – –

Observations:Presence of rodents observed by Observed 51 65 a b c d –

farmers Not observed 27 35 – – – – eResidual dung in the fattening rooms Presence 24 31 – b – d e

when restocking Absence 54 69 a – c – –

Housing and flooring systems:Gilts during acclimatisation period Confined in stalls on slatted floor 12 15 – – c – –

Confined in stalls on partially slatted floor 6 8 – – – – –Confined in stalls1 straw 28 36 – – – d –Group housing on slatted floor 2 3 – b – – –Group housing on partially slatted floor 6 8 – – – – –Group housing1 straw 21 27 a – – – eOutdoor1 straw 3 4 – – – – –

Sows in service period Confined in stalls on slatted floor 47 60 – b c – –Confined in stalls on partially slatted floor 17 22 a – – d –Group housing on slatted floor 4 5 – – – – eGroup housing on partially slatted floor 4 5 – – – – –Group housing1 straw 4 5 – – – – –

Pregnant sows Confined in stalls on slatted floor 43 55 a b c d eConfined in stalls on partially slatted floor 17 22 – – – – –Group housing on slatted floor 9 11 – – – – –Group housing on partially slatted floor 3 4 – – – – –Group housing1 straw 6 8 – – – – –

Post-weaning unit Slatted floor 67 86 a b c d –Partially slatted floor 5 6 – – – – –Straw or bedding 6 8 – – – – e

Fattening unit Slatted floor 72 92 a b c d ePartially slatted floor 2 3 – – – – –Straw or bedding 4 5 – – – – –

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

102 P.A. Belœil et al. / Livestock Production Science 81 (2003) 99–104

Table 2Deworming 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 40 12.5 50 15 – 17.5 5period

Boar 65 7 57 9 10 12 5Sows 76 8 45 17 7 18 5Growers 56 – – 71.5 – 27 1.5Fattening pigs 10 – – 30 – 20 50

stage in addition to an infeed post-weaning drug Rearing conditions and parasite control practicesadministration. The distribution of anthelmintic use have certainly changed considerably since 1976.according to the type of pigs treated is shown in The results of the present study show that, al-Table 2. though routine anthelmintic treatments are common-

ly used, they are not systematic. The rate of anthel-3 .2. Parasite infestation mintic use varied according to animal category: sows

were the most frequently treated, fatteners were thePositive samples were found on five farms. One least frequently treated. The choice of anthelmintic

sample containedTrichuris suis eggs and four also depended on the animals concerned with varioussamples contained Hyostrongylus rubidus or anthelmintics used for the same type of animal andOesophagostomum spp. with all egg counts per gram several anthelmintics used in the same farm. Noteof faeces less than 400 eggs per gram. No liver that this study was conducted before approval oflesion was reported for the 20 farms for which the ivermectin premix, and the rate of use of ivermectinrequired information was obtained at slaughterhouse. may now be different.Due to the small number of positive samples, no The small number of samples found to be positivestatistical analysis was performed to determine risk in this study could be related to the parasite controlfactors of infestation. The status of the positive herds practices described in our study. Moreover, as re-regarding certain hygiene, treatment and housing gards the characteristics of the farms surveyed,practices is presented in Table 1. housing and flooring systems corresponded to inten-

sive farms with a low exposure to internal parasites.Infestation should not have occurred in view of the

4 . Discussion anthelmintic treatments given in farms that testedpositive (B–E), but this infestation could be ex-

Few data are available about helminth infestations plained by a severe lack of hygiene. It has beenand deworming practices in indoor intensive all-in / previously demonstrated that re-infestation could notall-out systems. Prevalences of helminth infestations be prevented during the fattening weeks followinghave been published for heterogeneous management treatment with flubendazole, probably due to infecti-systems, but not all indoor intensive all-in /all-out ous stages left over from previous fattening periods,systems, in Denmark (Roepstorff and Jorsal, 1989) despite cleaning and disinfection (Joachim et al.,and UK (Pattison et al., 1980) in the 1980s and 2001). The role of breeding stock is also certainlyrecently in Germany (Joachim et al., 2001). In the important, as sows may constitute reservoirs oflast survey carried out in France in the 1970s infestation in the herd (Joachim et al., 2001). Internal(Raynaud and Jolivet, 1976), 25 to 50% of farms parasite infestation is therefore possible in intensivewith control measures were found to be positive with farms as shown here, especially when the wormstrongylid eggs in faecal samples from growing pigs. control programme does not focus on providing a

P.A. Belœil et al. / Livestock Production Science 81 (2003) 99–104 103

‘clean’ sow at farrowing. This study showed that positive pigs do not necessarily shed eggs (Roep-hygiene practices were not fully applied: gilts in the storff, 1998).acclimatisation phase were not systematically de-wormed, gilts and sows were frequently not washedbefore farrowing. In addition, the efficacy of rodent 5 . Conclusioncontrol was incomplete and some housing systems,such as straw and semi-slatted floor, allow infesta- When hygiene is good and management practicestions. Rodents, such as mice, are possible paratenicare appropriate in confined intensive swine facilities,hosts of parasites and rats can carry encysted larvaethe level of parasite infestation is low. By screeningof Oesophagostomum spp. (Jacobs and Dunn, 1968). for nematodes in pig faeces and screening manage-Housing weaners on slatted floors seems to be a ment practices, this study confirms that modernprotective factor against parasite infestation of management and housing systems control the levelsgrower-finishers compared to solid or partially slat- of infection to such low levels that production lossested floors (Pearce, 1999; Joachim et al., 2001). are unlikely. However, nematodes were found in

However, the small number of samples tested growing pigs. Farmers and veterinarians shouldpositive may also have been underestimated. The always be aware that parasites are present and shouldpurpose of our investigation was not to determine the remain permanently attentive to management systemprevalence of helminth infestation in the national and control practices in order to limit the risk of anherd, but to determine whether or not parasites could increasing number of parasites, which would resultbe found in faeces from young fatteners reared in in production losses.modern intensive systems in which hygiene routinesare supposed to be applied. Collection of pooledfaeces from the floor of pens, less demanding for the A cknowledgementsoperators involved, was therefore considered to besufficient for the purposes of this study. A good The authors gratefully acknowledge the farmers,assessment of helminth infestation in swine herds veterinarians and technical staff of the companies forwould have required sampling of breeding sows as their cooperation.well as offspring of different ages. An improvedsampling scheme should also include individualrectal samples collected on a predefined proportion R eferencesof animals in addition to pooled environmentalfaeces samples. Anonymous, 2001. Le porc par les chiffres 2000. Institut Tech-

The limited number of parasite species found in nique du Porc, Paris.Corwin, R.M., Stewart, T.B., 1999. Internal parasites. In: Straw,our faecal samples is in accordance with other

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1999; Joachim et al., 2001). Samples were taken 6 135–146.weeks after loading animals into fattening units, Mansfield, L.S., Urban, J.F., 1996. The pathogenesis of necroticwhere infestation could have occurred. However, this proliferative colitis in swine is linked to whipworm induced

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Mercy, A.R., de Chaneet, G., Emms, Y., 1989. Survey of internaldespite early infestation would have been reduced. A parasites in Western Australian pig herds. 2. Relationship tosmall number ofAscaris suum positive samples to anthelmintic usage and parasite control practices. Aust. Vet. J.were also recorded in UK (Pattison et al., 1980) and 66, 6–9.

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