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PergamonInrcrnationul Journal.for Parasitology, Vol . 21. No. 7, pp. X2.5 xl I. 19970. 1997 Australian Society for Parasitology. Published by Elsevm Smnce Ltd

Printed in Great RntamPII: SOO20-7519(97)00037-4 0020 7519197 117~,t1~~000

and Larval. He sAhnasal SecretinH. V. SIMPSON,*$ D. E. B. LAWTON,* D. C. SIMCOCK,* G. W. REYNOLDS*and W. E. POMROYt

*Department of Physiology and Anatomy, Massey University, Palmerston North, New ZealandTDepartment of Veterinary Pathology and Public Health, Massey Un iversity, Palmerston North,New Zealand(Received 9 December 1996; accepted 26 February 19971

Abatract43hp-s~ H. V., Lswton D. E. B., Sirncock D. C., Reynolds G. W. i?z Polpvoy W. E. 1997. Ef&cts

Parasitology. PgbM ed by Elsevier Science Ltd.Key words: sheep; Haemonchus contortus; experimental infection; adult worm transfer; abomasal pH; serumgas∈ serum pepsinogen.

INTRODUCTION (Holmes & MacLean, 1971; McLeay et al., 1973; And-Parasitism of the sheep abomasum by Haemonchus erson et al., 1976a, 1976b, 1981, 1985; Coop et al.,contortus inhibits gastric acid secretion and increases 1977) and in cattle by Ostertagia ostertugi (Jenningsserum pepsinogen and gastrin concentrations et al., 1966; Fox et (II., 1987, 1993; Hilderson PI al.,(Christie et al., 1967; Christie, 1970; Mapes & Coop, 1991)1970, 1973; Dakkak et al., 1981, 1982; Nicholls et al., The adult stagesof the parasite appear to be largely1985, 1987, 1988; Blanchard & Wescott, 1985; Fox et responsible for the altered secretory activity of theal., 1988). These effects on gastric function are pro- abomasum, since the transfer into cattle of adult 0.duced also in sheep by Ostertagia circumcincta ostertagi (McKellar et al., 1986, 1987) and 0. cir -cumcincta into sheep (Anderson et al., 1985; Lawton

et aI., 1996) rapid ly induced these ef%cts, whereasfTo whom correspondence should be addressed. Tel: 64- after larval infection of sheep there was a delay in06-3.56-9099; Fax : 64-06-350-5674; E-mail: H.V.Sim pson@ response until the parasite had progressed beyondmassey.ac.nz. the early larval stages (Lawton et al., 1996). Parasite

825

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826 H. V. Simpson CI a lexcretory/secretory (ES) products may initiate thephysiological changes in the host abom asum, sincethe mucosa l damage associated with the progressionof larvae to adult stages is not essential (McLeay etal., 1973; McKellar et ul., 1987).

Evidence on the nature of the host-parasite inter-action remains circumstantial and relies heavily on theinter-re lationships between temporal changes in thedifferent parameters. After infection of sheep and cat-tle with Ostertagia, serum pepsinogen concentrationincreasesbefore either serum gastrin or abomasal pH(Anderson et al., 1985; McKellar et al., 1986, 1987;Lawton et al., 1996), indicating that the effects of theparasites on abomasal secretion may not be mediatedby identical mechanisms. Increased circulating pep-sinogen is generally attributed to a leak lesion(Murray, 1969; Holmes & MacLean, 1971). In morerecent studies, serum gastrin and abomasal pHinitial ly increased together (Nicho lls et al., 1988; Foxet al., 1988; Lawton et al., 1996), suggesting that thehypergastrinaemia may be secondary to loss of theinhibi tory effects of acid-feedback on the G cell ; how-ever, later in the parasitism, abomasal pH frequentlydecreases while serum gastrin remains eIevated, sothat other fa ctors may also be involved (Lawton etal., 1996).The present experiments examine the associationbetween increased se rum pepsinogen and gastrin andabomasal pH in sheep after infection with either larvalor adult H. contortus and also after drenching toremove adult worms. The aim was to compare theserelationships with previous o bservations in sheepinfected with 0. circumcincta and identify comm onfeatures which might shed light on the mech anismsinvolved.

MATERIALS AND METHODSExperimental design. Experiment 1. Four sheep wereinfected with 10000 H. contortus larvae by ruminal intu-bation and another 4 sheep acted as uninfected controls.

Experiment 2. Four sheep were infected w ith approximately9000 adult Haemonchus worms via an abomasal cannula.After 96 h, these 4 sheep (but not control animals) weretreated orally with 0.4mg kg- ivermectin (Ivo mec ; Merc k& Co. Inc., Rahw ay, U .S.A.) and sampling was continuedfor a further 192 h. Four sheep acted as uninfected controlsfrom which the normal range for the parameters was estab-lished.Animals. All anim als were nematode-naive, 20-week-oldRom ney-cros s sheep (2 male, 2 female in each group) of bodyweight 24-37 kg. A cannula was surgically inserted undergeneral anaesthesia into the greater curvature of the abo-mas um at the junction of the body and antral regions andexteriorized through the ventral right flank (Hecke r, 1974).

Prophylactic antibiotic treatment (Streptopen; Pitman-Moore, 5 ml i.m. daily) was given for 3 days post-operatively.A recovery period of 7days wa s allowed before exper-

imentation. The sheep were housed in individual metabolismcrates and provided with w ater ad lib. and fed once daily at9.30a.m. with 200g luceme chaff plus 600g lucerne nuts.After a control sampling period of 4 and 7 days for E xperi-men ts 1 and 2, respectively. the animals were infected w ithH. contortus. On a few days, some infected sheep did n otconsum e all the feed offered. Diarrhoea did not occur, butSheep 9 and 12 produced soft faeces on Da y 3.

Transfer of adult H. contortus . Donor sheep were killedby captive bolt and exsanguination 23 days after larval infec-tion. The abomasal contents were pooled and concentratedby sedimentation at 37C to a volume of approximately 2.5 I.Worm counts w ere performed on 5 samples of 10 ml. With in4 h of collection of the worm s, the abomasa of recipientanimals were drained through the cannulae and 2~01s of300mI of concentrated contents were infused through thecannula at an interval of 1Smin. Each animal receivedapproximately 9000 23-day-old worm s. No larval stages wereseen in the infusate.Blood and abomasalfluid samples. In Experiment 1, blood

and abomasal contents were collected 30 min before, and 2-3 h after, feeding for determination of serum pepsinogen andgastrin and abomasal pH. A fter infection, sheep in Experi-ment 2 were sampled 2 hourly for 48 h, then 4 hourly untilanthelmintic treatme nt. Thereafter samples were taken 46 hourly for the f irst day and then twice da ily to 192 h. Bloodwas collected by jugular venipuncture into plain evacuatedtubes, the serum separated and stored at -20C for gastrinand pepsinogen assa y. About 1 ml of abomasal contents w asaspirated into a syringe through the cannula and the pHmeasured with a PHM 82 Standard p H Meter (Radiom eter,Copenhagen).Serum pepsinogen. Serum pepsinogen concentration wasdetermined in duplicate using the method of Pom roy &Char-leston (1989). Briefly, 0.25ml of serum was acidified with1.25ml of 0.06M HC l and incubated for 3 h at 37C . Onemillil itre of 10% TCA was added, the mixture centrifuged at3500 r.p.m . for 15 min and 1 ml of supema tant added to 2 mlof 0.5 M NaO H. The l iberated tyrosine was est imated by theaddition of 0.5 ml Folin-CiocaIteau reagent and reading theabsorbance at 700 run. Pepsinogen activity was determinedfrom the difference in free tyrosine between the incubatedsample and a non-incubated blank and expressed asmU tyrosine 1-l.Serum gastrin. Serum gastrin w as determined in triplicateby a radioimmunoas say (Simpson ef al., 1993) based on themethod of Hansky & Cain (1969). The antiserum used wasHanskys Ab74 (the generous g if t o f Dr J. Hansky). Synthetichuman nsG17 (Research Plus, Bayanne, NJ, U.S.A.) wasused to prepare radioactive label and standards.Parusifology. Infective larvae (L3) were obtained from cul-tures of faeces from sheep infected with a pure strain of H.

contortus. Larvae were confirmed to be motile. Larvae wereexsheathed with 0.2% sodium hypochlorite and rinsed withwater I h before intraruminal infection. Faecal egg countsper g (e.p.g.) were determined using a modified McM astermethod (Stafford et al., 1994) on faecal samples collectedperrectum. For all sheep, samples were collected before and2 days after su rgery. In Experiment 1, sheep were sampled atweek ly intervals and in Experiment 2 they were sampled4 days after transfer of worm s and 4 days later, after treat-ment with anthelmintic.

Definition of normal values. All values for serum pepsin-ogen, serum gastrin and abom asal pH in samples collected

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Adult and larval H. contorrus infection $27Table I-Pre-infection abomasal pH, serum gastrin and serum pepsinogen values for each infected sheep (n = 7 for Sheep14; n = 14 for Sheep 9-12). Also shown are values from a population of parasite-naive sheep (n = 1000) used to define theupper lim it of the normal range as mean + 2 SD .

SheepI2349

IO1112Population

Abomasal pH Serum gastrin (PM) Serum pepsinogeu (mU tyrosiue I )Mean Mean+2S.D. Mean Meanf2S.D. Mean Meani2S.D2.61 3.33 53 15 113 xi52.88 3.20 56 71 62 lb23.04 3.41 68 92 301 5312.97 3.30 74 95 105 4512.68 3.22 66 84 123 2552.74 3.34 46 62 209 3172.65 3.31 73 125 206 3182.71 3.29 48 74 42 IO62.80 3.26 38 64 223 4%

from parasite-naive sheep (controls and pre-infection) werecompared with normal population reference ranges derivedfrom over 1000values or eachparameter n parasite-naivesheep (Lawton et al., 1996). The upper lim its of the normalpopulation reference ranges (mean + 2 S.D .) were abomasalpH, 3.26; serum pepsinogen, 54mU I- and serum gastrin,64pM (Table 1). For each sheen, he pre-infection rangeswere alculated for eachparameterand also used o definenormal values. A parameter was considered to be elevatedwhen 2 successive values were above the designated upperlimit.

RESULTS

ControlsThere were small fluctuations in abomasal pH and

serum gastrin and pepsinogen concentration in con-trol sheep, with the only consistent trend being anincrease in serum gas&in after feeding in someanimals. In the pre-infection period, a few sheep (par-ticu larly Sheep 3 and 11) had elevated serum gastrinlevels in anticipation of feeding which raised theirindividual calculated upper limits for normal values.Individual pre-infection values (Table 1) were gen-eral ly similar to estimated population values (Lawtonet al.. 1996), although serum pepsinogen was lower.Individual ranges were used for comparison afterinfection, except for serum gastrin in Sheep 3 and 11in which the individual range was unusually high sincethe sheep sometimes became excited around feedingtime. In these animals, the population range was usedfor evaluation of serum gastrin.

Injbction with larval H. contortusIn general, al l 3 parameters were raised by the para-sitism althongh the magnitude of the changes varied

between the 4 individual sheep (Fig. 1). Changes inabomasal pH were small . The timing of changes inabomasal pH and serum gastrin and pqtinogen wasmore easily discerned when the efkts were huger, butno consistent differences between sheep were appar-ent. There were no increases before Day 2 and ail 3parameters had begun to increase by Day 4 or 5. Ingeneral, peak values were reached between Days 8 and10, after which all decreased steadi ly. Abomasat pWwas usually within the normal range again by Day15, whereas serum gas&in and pepsinogen, althoughdeclining, generally remained elevated on Da ys 20.~25, except when there had only been a small initial rise.Sheep 2 and 4 had barely detectable serum pepsinogenlevels before and after infection and were classed asnon-responders.

Transjiz r ofadult H. contortusAlthough variable in magnitude between sheep,there were increases in all parameters in all sheepexcept serum pepsinogen in Sheep 12 which was anon-responder (Fig. 2). Abomasal pH and serum

gas&in increased at about the same time (at about38 h in Sheep 11, but at 22 h in Sheep 9 and 10 andprobably in Sheep 12 in which a small increase, butsti ll within the pm-infection range, occurred with theincrease n serum gastrin at 22 h). These ncreaseswerebefore, or at the same time as, increases in serumpepsinogen (serum pepsinogen was raised at 2hh inSheep 10 and 36-38 h. n Sheep 9 and 11).The magnitude of the increases in abomasal pW.serum pepsinogen and serum gas&in was independentof one another in individual animals. Serum gastrincontinued to increaseuntil drenching, reaching valuesaround 6OOpM in all 4 sheep whereas abomasai pHreached a peak value at around 48 h. In the 3responder sheep, the max imum value for serum pep-

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828 H. V. Simpson et a l.SHEEP 1 1 1 SHEEP2 SHEEP 3 1 SHEEP 4

Fig. 1 . Abomasal pH and serum gastrin and pepsinogen co ncentrations before (m) and 3 h after (A) feeding in 4 parasite-naive sheep infected intraruminally with 10 000 H. contortus larvae. The horizontal dotted lines represent 2 S.D .s above themean values determined for each animal before infection and the solid line the corresponding population value.1 1 SHEEP10 SHEEP 11 SHEEP 12

Fig. 2. Abomasal pH and serum gas&in and pepsinogen c oncentrations in 4 parasite-naive sheep into which approximately9000 adult H. contortus were transferred through abomasal cannulae. The horizontal dotted lines represent 2 S.D .s abovethe mean values determined for each animal before infection and the solid line the corresponding population value.

sinogen just before drenching represented a 4-fold within 2days and particularly rapid in Sheep i0increase. (within 8 h). Serum gastrin and pepsinogen took in

After drenching, the time for the 3 parameters to exce ss of 4 days in 2 sheep. In Sheep 10, serum gastrinreturn to pre-infection levels varied. Abomasal pH was elevated for 34days after abomasal pH was inshowed the steepes t fall, being in the normal range the normal range.

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Adult and larvalH. contortus infection xJ.9Parasitology

No eggs were seen n the faecesof uninfected sheepduring the experimental period. Sheep 1-4 (infectedwith larvae) had no eggs n the faeces on Day 18, buton Day 25 the faecaf egg counts (FEC) were 3050,50, 15 850 and 17 500 e.p.g., respectively. Sheep whichreceived adult worms all had evidence of estab-lishment: on Day 4 the faecal egg counts were 2100,4100, 4150 and 2150e.p.g. for Sheep 9-12, respec-tive ly. No eggs were detected after treatment withanthelmintic. .

DISCUSSIONThis study has shown for the first time that thedirect transfer of adult Haemonchus contortus worms

into recipient sheep rapidly alters abomasal secretoryactivity in a similar manner to that demonstrated inprevious studies with Ostertagia spp. in sheep andcattle, and that the pathophysiological effects of all 3speciesare linked to the presence of adult worms andnot to larval development in the mucosa. The rapidityof recovery after worm removal by drenching high-lights the reversibility of acid suppression in the pres-ence of adult worms.Adult H. contortus, but not early larval stages,inhibited gastric acid production and raised serumgastrin and pepsinogen concentrations, as alsoaccompanies the parasitism of sheep by 0. cir-cumcincta (Anderson et al., 1985; Lawton et al., 1996)and cattle by 0. ostertagi (McKellar et al., 1986,1987).The initial disturbance to abomasal secretion by all ofthese speciesof worms is unlikely to be caused by thetissue damage associated with the histotrophic stagesof these parasites and chemical mediation wouldappear more likely.The magnitude of the responses to the differentparasites and in individual animals can be very vari-able and was not related to the faecal egg count. InExperiment 1, Sheep 2 and 4 were non-respondersfor serum pepsinogen but had low and high FEC,respectively, while Sheep 4 had overall the smallestresponse for all 3 parameters but the highest FEC.Infection with H. contortus larvae inhibited abomasalsecretion about 2days earlier than with 0. c ircum-cincta in sheep of the same age and breed (Lawton etul., 1996), as might be expected from a more rapidprogression through the larva l stages; effects of theparasites on abomasal function were apparent by 4-5 days when the 3rd moult would occur (Stol l, 1943;Sommerville, 1954, 1963; Christie et al., 1967).Although the responses to larval Haemonchus weresmall (Fig. l), the transfer of 9000 adult worms pro-duced very marked effects on abomasal secretion (Fig.

2), suggesting that the 2 nematode species share thesame mode of action on obomasal secretion.The transfer of adult Haemonchus caused rapid andmore uniform effects than after larval administrationand their timing was similar to those previously seenafter adult 0. c&wncincta transfer (Lawton et al.,1996). The principal difference was the later rise inserum pepsinogen with H. contortus compared withthe early increase (by 2 h in some sheep) with 0. rir-cumcincta into sheep (Anderson et al., 1985; Lawtonet al, 1996) and 0. cwtertagi into ca lves (McKehar etal., 1986, 1987). No reason for this is immediatelyapparent, particularly sinceH. contortus preferentiallyestablish in the fundic region, where most pe inogenis produced, and not in the pyloric area (Sommerville,1963; Charleston, 1965; Dash, 1985; Rahman &Collins, 1990). The hyperpepsinogenaemia is likely tobe caused by a different mechanism from those whichincrease abomasal pH and serum gastrin. This is indi-cated by the independence of the rise in serum pep-sinogen from those in the other 2 parameters, as wel las the occurrence of non-responders which madeup 15-25% of the total number of sheen nfected withH. contortus in this study or with 0. circumcincra byLawton et al. (1996). The feature these sheep had incommon was a very low pre-infection serum pep-sinogen concentration, which may indicate aninherently lower leakage of pepsinogen into the cir-culation.Although serum gastrin initia lly increased at thesame time as abomasal pH and may be the result ofthe withdrawal of acid feedback, the 2 parameterswere largely independent and therefore other factorssuch as inflammatory mediators may be involved, atleast after the early post-infection period. The acid-secreting parietal cel l may be the princ ipal target ofthe worms, since both Ostertagia (H. V. Simpson.unpublished data) and Haemonchus (E. Haag, 1995.The effect of Haemonchus contortus excretory/secretory products on abomasal secretion. Dr Med.Vet. Thesis, Hannover) have a reduced life span invitro at low pH compared with their viability abovepH4.5. The ability to inhibit parietal cells may bcessential for survival, particularly since Haemonchuspreferentially establish in the fundic region.The mechanism of acid inhibition by abomasalparasites, which clearly followed infection with eitheradult Haemonchus or Ostertagia, is as yet unknown.The rapidity of the onset of raised abomasal pH afterworm transfer and the rapid return to pre-infectionlevels after drenching (Fig. 2) strongly support areversible chemical inhibition rather than the loss ofparietal cel ls through physical damage. The recoveryof parietal cel l function began within 2 h of drenching,too fast to be dependent on the production of new

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830 H. V. Sincells, and was complete after about 4days. Previousreports were similar: abomasal pH was normal within54-172 h after drenching to remove 0. circumcincta(Anderson et al., 1976a) or 24 h for H. contortus infec-tion (Dakkak et al., 1985). The pH of the abomasalcontents may not accurately reflect the acid-inhibitingactivity of the worms, as a low worm burden may beable to alter the activity of nearby cel lsand thus reducetheir exposure to loca l acid conditions without affect-ing the overal l pH of the contents. Raising the abom-asal pH to 5 or 6 represents a signif icant feat on thepart of the worms.In summary, this study has shown the similaritybetween Haemonchus and Ostertagia in modifyingabomasal secretory function which is like ly to beevoked through the same mechanisms. The rapidi tyof the responses o the transfer of adult worms and totheir removal by treating with anthelmintic supportsa role for worm ES products which do not appear tobe produced by the early larval stages. The simila rityof responses o H. contortus and 0. circumcinta infec-tion suggests the involvement of the same or verysimilar ES products. Identification of any chemicalmediators will probably depend on in vitro studiesusing simpler systems rather than whole animalstudies.

Acknowledgements-The technical assistanc e of B . Adling-ton, D. Anthony, S. Calder, B. Guthrie and B. Parlane isacknowledged. The gas&in antibody Ab74 w as the kind giftof Dr J. Ha nsky . W e are grateful for the generous financialsupport for this work by the C. Alma Baker Trus t and theE. & C . Thorns Bequest.

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Stoll N . R. 1943. The wandering of Haemonchus contorr~.~in the sheep. Journal of Parasitologv 29: 407-416.