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STUDY OF GASTRO-INTESTINAL STRONGYLOSISIN A SHEEP FLOCK ON PERMANENT PASTURE.

1. SHEEP PARASITISM IN 1977J. Hubert, D. Kerbœuf, L. Grüner

To cite this version:J. Hubert, D. Kerbœuf, L. Grüner. STUDY OF GASTRO-INTESTINAL STRONGYLOSIS IN ASHEEP FLOCK ON PERMANENT PASTURE. 1. SHEEP PARASITISM IN 1977. Annales deRecherches Vétérinaires, INRA Editions, 1979, 10 (4), pp.503-518. �hal-00901228�

STUDY OF GASTRO-INTESTINAL STRONGYLOSISIN A SHEEP FLOCK ON PERMANENT PASTURE

1. SHEEP PARASITISM IN 1977

J. HUBERT1 D. KERBŒUF L. GRÜNER

1. N. R. A. , Centre de Recherches de Tours,i Laboratoire de Parasitologie, 2 Laboratoire d’Eco%gie des Parasites,

Nouzilly, 37380 Monnaie, France.

Résumé

ETUDE DES STRONGYLOSES GASTRO-INTESTINALES DANS UN TROUPEAU OVIN SURPATURES PERMANENTES. 1. LE PARASITISME DES MOUTONS EN 1977. - Une enquêteépidémiologique visant à définir qualitativement et quantitativement le parasitisme gastro-intestinal ovin est mise en place dans le Limousin.Cinq agneaux sont sacrifiés régulièrement toutes les 4 semaines de mai à janvier de l’année sui-vante. Des bilans parasitaires complets sont effectués sur ces animaux ainsi que des mesures dutaux de pepsinogène sanguin. Pour préciser l’influence du parasitisme sur la croissance des ani-maux, le gain de poids d’agneaux traités régulièrement et non traités est comparé.Les résultats des autopsies montrent que le parasitisme est essentiellement lié au développementde u Strongles ». Des observations effectuées sur le troupeau indiquent que la moniéziose peutaussi jouer un rôle non négligeable.Le niveau parasitaire, déjà important un mois après la mise à l’herbe, atteint son maximum enjuillet-août. L’année 1977 est caractérisée par un très fort taux de parasitisme.Parmi les espèces rencontrées, deux jouent un rôle essentiel : Ostertagia circumcincta et Hae-moncus contortus.L’examen de la croissance des agneaux indique qu’en 6 mois, le gain de poids des animaux traitésest le double de celui des non-traités.Les effets du parasitisme sont aggravés par la faible valeur fourragère de la prairie et l’existenced’un surpâturage.Les dosages de pepsinogène sanguin confirment l’intérêt de cette mesure pour situer le tauxmoyen d’infestation d’un troupeau par les parasites de la caillette. Il semble que dans certainscas, il puisse aider à préciser la succession des pics d’infestation par les différentes espèces.

It is not possible, at the moment, to give aprecise figure but economic losses recorded insheep farming due to gastro-intestinal parasi-tism are appreciable.The main parasites responsible are widely

known but investigations dealing with the fre-quency of different species and their fluctua-tions during the year have been carried outmore or less thoroughly in different countries.The situation is relatively well defined in

Great Britain where a great deal of researchhas been carried out both in ewes and lambs(Connan, 1968 ; Gibson and Everett, 1972 ;Boag and Thomas, 1973, 1975). These wor-kers have been able to work out a pattern ofinfestation as a function of the type of rearingand the contamination of the pasture whenanimals were put out to graze (Parnell et al.,1954 ; Crofton, 1957 ; Boag and Thomas,1971, 1975, 1977 ; Thomas and Boag, 1972).These results led to the recommendation ofcontrol programmes (Michel, 1969 ; Boag andThomas, 1973 ; Gibson, 1973). In Australiaand New-Zealand, precise data are also availa-ble (Parnell, 1963 ; Anderson, 1972, 1973 ;Donald and Waller, 1973 ; Wlasoff, 1973). In

France, only 2 series of epidemiologicalresearch investigations have been caried out,using systematic parasitic evaluations. Onewas carried out by Euzeby et al. in 1964 andthe other by Nicolas et al. in 1967, and bothtook place in the Limousin region. The resultsobtained during these studies as well as somefigures obtained during more sporadic slaugh-tering were gathered and analysed by Ray-naud and Leimbacher (1977). These authorshave suggested a standardization of theexpression of results and a definition of severallevels of parasitic infestation which would faci-litate comparisons of data from different sour-ces.

This information, which provided an inva-luable foundation, needed to be confirmedand completed. It is, indeed, essential, to esti-mate precisely the relative abundance of spe-cies which have very different pathogeniceffects and which in association can someti-mes worsen the incidence of disease.

For this purpose an experiment was set upin 1977, using a flock of sheep in the Limousinregion. This enabled the existing parasitism, tobe studied in a field flock as well as its deve-

lopment over one year using parasite counts,quantitative coproscopic examinations and theserum levels of pepsinogen.

It is usually thought that the main manifes-tations of parasitism are delays in growth evenin the absence of clinical symptoms of theinfestation. In order to define the influence ofdigestive strongyloses on the weight gain ofthe animals, in terms of the severity of inhibi-tion and the date of onset, the growth of twogroups of lambs was compared. One groupwas treated systematically every four weekswhile the other was not treated.

This study also involves examinations ofparasite populations on pasture and their epi-demiological importances. These results willbe described in another paper.

Material and Methods

A. EXPERIMENTAL STRUCTURE

1. Management of the flockThese studies were carried out in the North

Limousin area where agricultural productionconcerns mainly grazing lambs. The oldestand most prevalent sheep farming uses perma-nent or semi-permanent pastures.The consequences of the increasing pro-

duction, which squares with the present requi-rements of sheep farming are a rise in thenumber of sheep and a longer time of grazing.

This type of management is an importantcause of increased parasitism.The flock under study was situated near

Bellac (Haute-Vienne). The animals grazed in a12 ha permanent pasture divided into four

parts. During previous years these parts hadbeen grazed by sheep, and after these had left,no disinfection was carried out and no fertili-zers were added.

To assess the grazing value of this pasture,an analysis of flora according to the techniqueof De Vries and De Boer (1959) was carried out

during the spring. The fodder value was mea-sured by Poissenet and Daget’s index (1969).A flock of 120 ewes and 140 lambs of a

texel-southdown cross breed was broughtonto the land in mid-March. The managementof the flock during the year is summarized infigure 1. It comprised two periods : a summerperiod in the meadow and a winter period inenclosures near the farm buildings. During thesummer, the animals did not receive food

apart from grass. From August onward, thelambs which were not selected for the experi-ment, were gradually removed from the flockand sold.

2. Study of parasitism.All lambs selected for the trial were 2

months old at the beginning of the experimentin May. They weighed between 15 and 18 kgand remained with the whole flock. In order tomonitor the existing parasitism and its deve-

lopment, 60 lambs were allocated at randomto 12 groups of 5 sheep. The slaughtering dateof each group was chosen by the drawing oflots. The first one was sacrificied soon afterthe start of the trial and thereafter at 4 weeklyintervals until February of the following year.The animals did not receive any strongylicideduring the experiment. Treatments againstmonieziosis alone were administered (Yome-sane N.D. 200 mg/kg). Individual coproscopi-cal tests were carried out on the last two

groups every month during the trial period.Parasitism was also studied in ewes by copros-copic controls on 20 animals every four weeks.Ewes were subjected to regular polyvalentantihelmintic treatments every seven weeks.

3. The effect of parasitism on the growth oflambs

The influence of parasitism on growth wasevaluated by regular weighings every fourweeks, from the 10th of May to the 25th ofOctober. Two groups of 10 lambs were com-pared : one was treated each month with

Thiabendazole N.D. (110 mg/kg) ; the otherwas untreated.

The yield of the carcasses was recorded andcompared with those of lambs treated accor-ding to the « farmers’ prophylaxis » plan, thatis to say about every 7 weeks during the pas-ture season.

B. PARASlTOLOGlCAL TECHNIQUES

1. Coproscopical tests.The Mc Master technique modified by Ray-

naud (1970) was used. The flotation solutionused was potassium iodomercurate (d =

1.44).

2. Parasite counts

In the slaughter house, the digestive tractwas collected and divided into three parts,abomasum, small intestine and caecum-colon.The mature worms in these different por-

tions were collected by straining the washingson a 150 ! gauze cloth.The immature worms in the abomasum and

the small intestine were obtained by a furtherfiltration of the liquid on a 38 p strainer.The parasites in the mucous membrane

were isolated by peptic digestion for 4 h at atemperature of 37° C. Prior to counting,worms were suspended in 4 litres of water(adults) or 1 litre (immature). After homogeni-zation by magnetic agitation, 2 samples of 200ml removed for counting mature worms and asample of 100 ml for counting immatureworms. In the case of adults, if the first samplecontained more than 50 worms in 100 ml, onlyone of the 200 ml samples was studied. Withregard to immature worms the entire 100 mlsuspension was examined. The entire productof peptic digestion was also examined.

3. Messurement of pepsinogen levelsWith the aim to study the evolution of

serum pepsinogen throughout the year, bloodsamples were taken from five sheep the day ofeach monthly slaughter and at the same timefrom animals of the flock designed to be

slaughtered at the end of the experiment. Theserum was collected and the pepsinogen mea-surements were carried out using a techniquedescribed previously (Kerbceuf, 1975).

Results

A. ANALYSlS Of FLORA (table 11

The results of this analysis show that thegrazing land has a low fodder value. A compa-

rison of these observations with those recor-ded for other permanent meadows of NorthLimousin shows that this pasture is represen-tative of the region studied (Carnis, 1969).A more or less permanent high water con-

tent was revealed by the presence of hydrophi-lic plants (carex, rushes, cardamines). It wasnoticed that there was a tendency to overgra-zing, as indicated by the existence of nume-rous « rosette » type plants.

B. PARASITIC EXAMINATIONS

1. Coproscopy (table 2, fig. 2)During the count, no distinction was made

between the eggs of Nematodirus and thoseof other species of strongles. The tests carriedout on the ewes and the animals treated everyfour weeks show a very low level of egg pro-duction throughout the trial. At the beginningof July, a slight peak was noticed in the trea-ted lambs, which corresponded to the begin-ning of infestations in the untreated animals.In the untreated animals, egg excretion was

low at the beginning of the trial (60eggs/gram) but it rose quickly from Julyonwards and reached a very high level in earlyAugust (around 8 000 eggs/gram). Then it

dropped back progressively. In December,however, the number of eggs per gram wasstill 1250. The inspection of individual resultsdid not reveal any self-cure phenomenon.

Since parasitic counts were carried out

monthly, no coprocultures were performed.

2. Parasite counts (table 3 to 6 ; fig. 3a, 3band 4).The results in these tables deal with the

counts on 54 animals out of the 60 in the trial.6 sheep died during the experiment, 2 of ente-rotoxaemia and 4 of haemonchosis. Apartfrom the results dealing with the digestivestrongyles, post-mortem examinations revea-led that most animals had lung strongylosislinked to the development of Protostrongyli-nae from June onwards. Examination of theliver revealed only one case of dicrocoeliosis inSeptember and none of fasciolasis.

a. infestation spectrumThe chronological order of infestation by

gastro-intestinal strongles was as follows.In mid-April, one month after being put out

to graze, the animals were already very infec-ted (mean = 11000 worms). In July-August,the level of parasitism reached its highestpoint (around 25000 parasites on average).From September, a slow drop in infestationwas recorded. At the end of November, therewas still an average of 6200 worms per animal.

b. enumeration of species.The main species were : Ostertagia circum-

cincta, Haemonchus contortus, Trichostron-

gylus colubriformis.Other species found regularly but in small

numbers were : Nematodirus spathiger,Nematodirus filicollis, Oesophagostomumvenulosum, Chabertia ovina.Some species were more seasonal. Tricho-

strongylus axei and Cooperia curticei were

only present at the early part of the year fromMay till August.c. patterns for individual species

Osteriagia circumcinctaThis species prevailed mainly at the begin-

ning of the grazing season. It appeared in

great numbers from June and reached itsmaximum number in July-August (16000 and15300 worms). It remained at a medium level

throughout the autumn. From Januaryonwards, most worms were at the inhibitedlarval stage IV (85 to 100 per cent).Haemonchus contortusThis parasite was present in small numbers

from June. After a progressive increase, it rea-ched a very high peak of 7000 worms on ave-rage, but stayed above 2000 worms.

Trichostrongylus colubriformisThe results showed that this inhabitant of

the small intestine was present during the gra-zing season in a significant constant quantityfrom July to November (4000 worms). A slightpeak, however, was noticed in September(7000 worms).

3. Variations in the pepsinogen level (table 7,fig. 5)

At the beginning of the experiment, beforethe infection began, the pepsinogen level ofthe lambs was very low (61 mU Tyr ± 18 *1. It

. standard error.

started to rise following the first infestations inJune. A peak was observed at the beginningof July (824 ± 186 mU Tyr) when there weremost worms in the abomasum.

A fresh increase was recorded at the end ofSeptember. At that time, the number of para-sites such as Ostertagia had markedly decrea-sed while the population of Haemonchus hasreached a maximum. The pepsinogen levelremained relatively high throughout the latterpart of the grazing season and a new peakoccurred at the end of December.

C. THE EFFECT OF PARASlTlSM ONGROWTH (table 8 and 9, fig. 6)

From June a continuous drop in the growthrate of the control animals was noticed, com-pared to that of the treated animals. A studyof the results shows that in 168 days theweight gain of the treated lambs was doublethat of the controls despite a slowing-down ofthe growth of the treated animals in July-August when Monieza expansa widely infec-ted the flock.

These results were confirmed at slaughte-ring time when the carcass yield of the untrea-ted animals never exceeded 48 per cent of thelive weight during the whole of the grazingseason (table 91.

Conclusion

1. Parasitological results

The epidemiological study showed that 1977was very propitious for the development of ahigh level of parasitism in the flock studied.The comparison of these results with thoseobtained by Euzeby et al. (1964) and with theparasitic levels defined by Raynaud and Leim-bacher (1977) shows that the infestation levelswere very high compared to those usuallyrecorded. These authors did not mention morethan 6 000 worms in the digestive tract at the

peak of contamination, while an average of26 000 were counted at certain periods of timein the present paper.The time course of infestation was similar to

the description of Euzeby et al. (1964) at leastat the beginning of the year, with a peak,mainly due to Ostertagia spp. which started inspring and reached its highest point in July.The studies carried out by these authors bet-ween 1961 and 1963, have clearly demonstra-ted the occurrence of a second wave of infes-tation during the autumn or even at the begin-ning of winter. This infestation was more mar-ked than the summer one.

In this study, this second increase was notfound. The results show a persistent highparasite level until November, then a gradualand an average of 2 000 worms was reached in

January. The main difference between theseresults and those obtained by Euzeby et al.(1964) for this time of the year concerns

Nematodirus spp. The latter authors counteda large number of these parasites largely res-ponsible for the autumn maximum.

During the present experiment only a smallnumber of Nematodirus was collected. Thisseems to confirm that autumn infestations aremainly due to this parasite. The great numberof Haemonchus contortus which becomes thepredominant species in September remainsthe most important aspect of our results.These results are very different from those

published previously. Since this species wasconsidered as rare or not very numerous when

present (Euzeby et al., 1964) ; Raynaud andLeimbacher, 1977).The figures in this study reveal an average of

around 7 000 H. contortus in September, lea-ding to death in some cases. Such a seriousinfestation by this parasite does not seen tohave been reported previously.Another difference from the patterns descri-

bed in other countries is that data show a verylimited amount of inhibition of developmentoccurring in Ostertagia circumcincta and nonein Haemonchus contortus : trials carried out in

Britain showed that in sheep, as in cattle, it ispossible to record very high percentages ofinhibition of development at the fourth stagelarvae for these species.

In O. circumcincta, the inhibition beganonly in the autumn and reached a maximum ofmore than 90 per cent during December andJanuary (Connan, 1971 ; Reid and Armour,1972). In our experiment the ratio of the fourthstage larvae slowly rose in the autumn andtheir number never exceeded 1 000 worms. Itis difficult to estimate the extent of the inhibi-tion rate with such results.

The lack of inhibition of development ismore obvious in H. contortus during this time.In mid-autumn and winter, this might be rela-ted to the very important decrease in the num-ber of H. contortus during this time.

Nevertheless, Waller and Thomas (1975)and Connan (1971) established that for thisworm the inhibited larvae appeared very earlyin the year and reached 100 per cent fromOctober.

Waller and Thomas (1975) recorded 57 percent of inhibition as early as July and 75 percent during August. These authors deductedfrom these results that inhibition of develop-ment of H. contortus may be considered to bean adaptation to overcome the unfavourableconditions of the external environment in Bri-tain.

Similar results were recorded in New Zea-land where Brundson (1973) stated that inhibi-tion percentages in H. contortus reached 100per cent from April. We never recorded suchinhibition percentages. If the findings obtainedin France in the Limousin region are confir-med, they might mean that different climaticeffects do not induce the same features of sur-vival adaptation as the climatic conditions ofEngland do. The results also suggest that thisparticular development is linked to the unusualhigh temperatures in summer 1976. Haemon-chus contortus is able to withstand droughtand develops rapidly when the temperature ishigh. Gruner et aL (1977) recorded the samephenomenon during the summer of 1976 in anearby animal breeding farm. The rather mildwintery conditions certainly allowed the free-living stages to survive in large numbers and toinfect the lambs soon after they were turnedto pasture at the beginning of May.

2. The effect of parasitism on growthThe extent of the parasitism recorded led to

pathological effects and an obvious influenceon the growth.The comparison between the control ani-

mals and the treated animals brings out theefficiency of the treatments. They are, howe-ver, a few remarks which can be made aboutthe growth of the treated animals. It is likelythat the fodder value of the field did not leadto very good zootechnical performance. Adrop in weight gain compared to the previousmonth was recorded among the treated ani-mals around October which can certainly beattributed to the scarcity of grass at that timeto the unfavourable weather conditions.Nonetheless, the carcass yield for this groupwas around 50-51 per cent, which agrees withthe figures usually recorded in flocks using thesame farming method, that is a simple treat-

ment of the pasture with manure without addi-tives. These yields could perhaps be improvedby avoiding the development of seriousmonieziosis which is at the origin of a drop inweight gain found among the treated animalsin July-August and despite the administrationof a cestodicide in June (Yomesane N.D. 200

mg/kg).3. Variations in plasma level of pepsinogen.

During the preliminary trial carried out in1975 in the Limousin region, it was shown thatthere was a good correlation between themean level of pepsinogen and the averagenumber of worms in the abomasum in groupsof animals (Kerboeuf and Leimbacher, 1977).These preliminary results agreed with those

obtained by Anderson (1972) in sheep in Aus-tralia and Thomas and Waller (1975) in GreatBritain. In this initial experiment, measure-

ments were only performed until the 6th ofAugust and the parasites responsible for theinfestation were mainly worms of the Osterta-gia species. There were no data relating to thechanges of plasma level of pepsinogen asso-ciated with infection by several species duringthe same grazing season. This was the samefor Anderson (1972) and Thomas and Waller(1975) who had found mainly Ostertagia in theabomasum. The correlation between pepsino-gen and the number of worms in the aboma-sum was confirmed again in this trial at leastup to slaughtering carried out in late August.Throughout this period the infestation curveand the pepsinogen curve were parallel.

In September, the results of the pepsinogenmeasurements showed a new peak while thenumber of Ostertagia had largely decreased.

This second rise coincided in time with the

peak of Haemonchus and could certainly beattributed to the development of the latter.

Indeed, it is known that these parasites arelikely to induce rises in the pepsinogen plasmalevel, in the same way as Ostertagia (Kerboeuf,1977). A third tendency towards an increaseappeared from the end of November but thisrise is more difficult to explain, since at thistime the number of mature worms in the abo-masum was rather low. Two hypotheses canbe put forward. The first one implies that themucous layer has not regained its integrityafter the summer infestations and that the

pepsinogen levels stays high with few fluctua-tions during a rather long period. The secondresults from the observations on the numberof stage IV larvae. It was found that, betweenthe 23rd of November and the 18th of

January, the quantity of stage IV larvae pre-sent multiplied by more than 4 times. Theincrease in pepsinogen precedes the rise in thenumber of these stage IV larvae, and is parallelto it. It could perhaps be a consequence ofinfestations although it is considered that the

pepsinogen variations are mainly the results oflarvae leaving the mucous layer.

This last point needs to be confirmed by fur-ther experimentation. One comment can bemade regarding the values of pepsinogenlevels recorded in this trial. The levels foundwere never high and seem low compared tovalues reported by other authors. In particular,very low values (60 mU, mean), much lowerthan normal levels (300-600 mU), were foundat the beginning of the experiment when thelambs were parasite-free.

Ths leads one to think that there might berace or environmental factors intervering. Inthis event, it would seem wise to take note ofinitial levels when interpreting results. Theresults of this trial seem once to confirm the

usefulness of pepsinogen levels in followingthe variations of infestations in animals put outto graze.

Accepted for publication January 9th 1979.

Summary

An epidemiological study aimed at defining gastro-in:estinal parasitism in sheep qualitatively andquantitatively was carried out in the Limousin area in France.Five lambs were sacrificed regularly every 4 weeks from May till January of the following year.Complete parasite counts were performed on these animals as well as measurements of theplasma level of pepsinogen. In order to define the influence of parasitism on the growth of theanimals, the weight gains of lambs treated regularly and untreated lambs were compared.The results of post-mortem examination show that parasitism is mainly linked to the incidence ofstrongyles. Other observations in the flock have shown that Moniezosis may also play a non-negligeable part.The parasitic level, already high after one month at pasture, reached its maximum in July-August1977 and was marked by a very high level of parasitism.Among these species found, two played an essential part : Ostertagia circumcincta and Hae-monchus contortus. A study of the growth of the lambs showed that within 6 months, theweight gain of the treated animals was twice that of the untreated animals.The effects of parasitism were worsened by the low fodder value of the pasture and the occur-rence of overgrazing. The blood pepsinogen measurements confirmed the usefulness of thistechnique in establishing the mean level of infestation of a flock by parasites of the abomasum. Itseems that in some cases it could help to define the succession of peaks o! infestation by diffe-rent species.

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