Internohmd Journalfor Parasilology Vol. 23, No. 3,~. 411413, 1993 002&7519/93 $6.00 + 0.

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Printed in Great Britain Pergamon Press Lrd
0 1993 Ausrrolim Socieryfor Parasitology

RESEARCH NOTE

AN OUTBREAK OF HAEMONCHOSIS ASSOCIATED WITH

ANTHELMINTIC RESISTANCE IN SHEEP

C. L. YADAV,* R. P. UPPAL~§ and S. KALRA:

Departments of *Veterinary Parasitology, tveterinary Pharmacology and SAnimal Breeding, CCS Haryana Agricultural
University, Hisar-125004, India

(Received 16 September 1992; accepted 10 December 1992)

Abstract-YmAv C. L., UPPALR. P. and KALRAS. 1993. An outbreak of haemonchosis associated with
anthelmintic resistance in sheep. International Journal for Parasitology 23: 411413. An outbreak of
haemonchosis associated with anthelmintic resistance was recorded in a flock of 150 crossbred lambs.
Closantel and ivermectin were 100% effective against Huemonchus contortus while fenbendazole and
morantel reduced faecal egg counts by 87 and 29%, respectively. Levamisole showed an efficacy of 95%. At
double the recommended dose (10 mg kg-‘), fenbendazole had an efficacy of 99% against H. contorfus
infection. This appears to be the first report of an outbreak of haemonchosis associated with fenbendazole
and morantel resistance in a strain of H. contortus in sheep.

INDEX KEY WORDS: Huemonchus contortus; outbreak; treatments; anthelmintic resistance; mortality;
lambs.

RESISTANCEto phenothiazine in a strain of Haemon- Clinical parasitic gastroenteritis due to hae-

thus contortus was first reported by Drudge, Leland, monchosis was diagnosed in the last week of
Wyant & Elam (1954). Since then, H. contortus September 199 1 in a new crop of 150 crossbred lambs,
resistant to a number of anthelmintics have been born in March/April 1991 on the University sheep
described in grazing animals from different parts of the breeding farm. The clinical signs of haemonchosis
world (Waller, 1987; Taylor & Hunt, 1989; Prichard, shown by the animals included rapid weight loss,
1990). In India, strains of parasite resistant to fen- weakness, emaciation, submandibular oedema and
bendazole in sheep and levamisole in goats have also prostration. Five animals died even though the flock
been recorded (Yadav, 1990; Yadav & Uppal, 1992). had been treated orally with fenbendazole (5 mg kg-‘)
Haemonchosis as a clinical disease has been as- or morantel(l0 mg kg-‘) in the months of June, July
sociated with ‘hypobiosis’ (Connan, 1971; Michel, and September. The recovery of adult H. contortus
1974). The resumption of the development of the parasites from the abomasum of lambs that had died
hypobiotic larvae and their subsequent maturation confirmed the disease.
have been reported to be associated with increased When treatment failed to alleviate the deteriorating
pasture contamination (Procter & Gibbs, 1968; condition of the flock, 50 out of 150 lambs were
Ayalew & Gibbs, 1973) and outbreaks of the disease separated and their faecal samples were examined for
(Gibbs, 1964). Subclinical infection results in reduced eggs per gram (epg) by a modified McMaster tech-
growth and milk production (Thomas & Ali, 1983). nique on 30 September 1991. Based on the result of the
Heavy infestations on account of newly ingested faecal examination, the lambs were randomly divided
larvae may also cause acute disease, production losses into five treatment groups of 10 each to compare the
and death (Yadav, Uppal & Prerna, 1992). faecal egg count reduction abilities of the drugs:
The present communication describes an outbreak fenbendazole (Panacur; Heochst India Ltd, Bombay),
of the disease associated with the presence of anthel- morantel (Banminth; Pfizer Ltd, Bombay), levamisole
mintic resistance in sheep. (Lemasol; Ranbaxy Laboratories Ltd, New Delhi),
closantel (Exinot; Cadila Laboratories Pvt. Ltd,
Ahmedabad) and ivermectin (Ivomec; Merck, Sharp
5 To whom all correspondence should be addressed. and Dohme, Agvet., U.S.A.). The types of the

411
412 C. L. YADAV, R. P. UPPAL and S. KALRA

TABLE I-SUMMARY OF THE ANTHELMINTICSUSED ON THE Fenbendazole and morantel treatments reduced epg
UNIVERSITY
SHEEP
FARMBETWEEN1986 AND 1991 by 87 and 29% respectively (Table 2). Levamisole
treatment produced 95% reduction in epg while
Year Month (anthelmintic)
closantel and ivermectin showed 100% efficacy. The
pooled coproculture of each group for positive epg
1986 Feb Mar Apr May Aug Ott
showed 100% H. contortus larvae. In the fenbendazole
(B) (B) (T) (B&L) (A) (A&F)
1987 Jan Mar Jul Ott Dee
group, three lambs died within 10 days of treatment.
Apr
(L) (L) (L) (B&F) (F) (F&L)
Submandibular oedema was observed in two lambs in
1988 Apr May Jun Sep Ott the fenbendazole-treated group and in three lambs of
(A) (A) (A) (A) (B) the group given morantel. The lambs receiving leva-
1989 Apr Jun Jul Nov misole, closantel or ivermectin did not show sub-
(B&F) (F&M) (F&M) (M) mandibular oedema and their health also showed signs
1990 Apr May Jul Aug Ott
of improvement. As the condition of the lambs
(B) (B) (B) (B) (B) continued to deteriorate, six lambs died between 11
1991 Feb Apr Jun Jul Sep Ott
and 19 October. Therefore, 10 lambs from this flock
(M) (M) (B) (B) (B&F) (F)
were again selected randomly and were faecally sam-
B, Banminth; T, thiabendazole; L, levamisole; A, albendazole; pled for epg; the flock was dosed with fenbendazole at
M, mebendazole; F, fenbendazole. double the recommended dose. At this dose, a com-
parison of pre- and post-treatment epg and worm
of the anthelmintics used over the last 6 years are counts showed a reduction of more than 99% 10 days
summarized in Table 1. On the same day, the remain- following treatment (Table 3). From the flock, seven
ing 100 lambs of the flock were treated with the lambs died during the first 6 days of treatment though
recommended dose (5 mg kg-’ of fenbendazole. the mortality was completely checked thereafter.
Because of the severity of the condition the lambs of The FECR test is widely used to indicate the
the two flocks were maintained indoors, separately, on presence of resistant strains of nematodes (Vizzard &
dry bhoosa, green fodder and concentrates. Wallace, 1987). In this test, resistance to anthelmintics
Ten days later, faecal samples of animals of each is presumed when the FECR value is lower than 90%.
experimental group were examined again for epg and On the basis of this criterion, H. contortus had
clinical signs. The larvae of pooled post-treatment developed resistance to fenbendazole and morantel
samples, as well as those of pretreatment samples, but not to closantel and ivermectin. Lower reductions
were cultured and identified. in egg counts in fenbendazole- and morantel-treated
The data on epg and worm counts were transformed groups could be due to newly ingested larvae or
to logarithms (count + 1) to calculate the geometric emergence of arrested larvae and their subsequent egg
means. The faecal egg count reduction (FECR) per- output on maturation following treatment. However,
centage of each treated group was then determined such a possibility seems unlikely in the present case
(Presidente, 1985). because lambs were not sent for grazing until the last

TABLE 2-DATA ON FAECALEGGCOUNT AND WORMCOUNT (GEOMETRIC

MEAN).MORTALITY
AND
GENERAL
HEALTH
OFCROSSBRED
LAMBS
FOLLOWING
TREATMENT
WITHDIFFERENT
ANTHELMINTICS

Treatment (mg kg-‘) Faecal egg count FECR(%) worm Mortality

count
Pretreatment Post-treatment

Fenbendazole, 5 14,965 1987 86.8 1498 3

(3) (2)
Levamisole, 7.5 14,328 764 94.1 - 0
(4) (0)
Closantel, 10 13,510 (0”) 100 _ 0
(4)
Ivermectin, 0.2* 7894 100 - 0
(3) (i)
Morantel, 10 10,134 7164 29.7 - 0
(2) (3)

Figures in parentheses indicate submandibular oedema.

* Drug given subcutaneously; all other drugs given orally.
 Research Note 413

(10 mg kg-‘) ON EPGAND

TABLE 3-EFFECT. OF FENBENDAZOLE GIBBS H. C. 1964. Observations on an outbreak of clinical
WORMCOUNT parasitism in ewes during the winter months. Canadian
Veterinary Journal 5: 8-l 1.
Parameter Pretreatment Post-treatment Reduction GUFTA R. P., RUPRAH N. S. & YADAV C. L. 1986. Some
(%) observations on the spring rise phenomenon in sheep of
Haryana (India). Indian Veferinary Journal 63: 449453.
em 1431 10 99.30 HERD R.P., STREITELR. H., MCCLURE K. E. & PARKER C. F.
Worm count 1627(6) 15(7) 99.07 1984. Control of hypobiotic and benzimidazole-resistant
nematodes of sheep. Journal of the American Veterinary
Figures in parenthesis indicate the number of animals that Medical Association 184: 726-730.
died. HOTSON I. K., CAMPBELL N. J. & SMEAL M. G. 1970.
Anthelmintic resistance in Trichostrongylus colubrtformis.
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development in H. contortus has not been observed in MARTIN P. J. 1985. Nematode control schemes and anthel-
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died due to haemonchosis also confirmed that the 2940. CSIRO Division of Animal Health, Melbourne,
parasite had developed resistance. Australia.
MICHEL J. E. 1974. Arrested development of nematodes and
A reduction of 95% in epg in levamisole-treated
some related phenomena. Advances in Parasitology 12:
lambs did not suggest resistance of the parasite to this
219-366.
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PRESIDENTEP. J. A. 1985. Methods for detection of resistance
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