Natural infections of Strongyloides westeri: prevalence in horse foals on several farms in central Kentucky in 1992

Natural infections of Strongyloides westeri: prevalence in horse foals on several farms in central Kentucky in 1992

Veterinary Parasitology, 50 ( 1993 ) i 01-107 0304-4017/93/$06.00 © 1993 - Elsevier Science Publishers B.V. All rights reserved 101 Natural infectio...

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Veterinary Parasitology, 50 ( 1993 ) i 01-107 0304-4017/93/$06.00 © 1993 - Elsevier Science Publishers B.V. All rights reserved

101

Natural infections of Strongyloides westeri: prevalence in horse foals on several farms in central Kentucky in 1992 Eugene T. Lyons*, Sharon C. Tolliver, J. Harold Drudge, David E. Granstrom, Sandra S. Collins Department of Veterinary Science, Gluck Equine Research Center, University of Kentucky, Lexington, KY 40546-0099, USA (Accepted 27 December 1992 )

Abstract

During the period 28 February- 1 July 1992, fecal samples were collected and examined for eggs of

Strongyloides westeri once from each of 382 horse foals (364 Thoroughbreds, 16 Standardbreds, one Lippizaner, and one draft-type horse ) in central Kentucky. Ages of the foals at the time of sampling ranged from 7 to 63 days (mean 22 days). The nine farms in the study were considered to have overall excellent deworming programs. None of the foals had been treated with an antiparasitic compound before the study. Eggs of S. westeri were found in 6% (22 of 382) of the foals on 78% (7 of 9) of the farms. Current prevalence of this parasite in foals is discussed relative to studies before the availability and usage of effective drugs.

Introduction

Strongyloides westeri is a tiny nematode (about 9 m m long) found as an adult in the small intestine of foals. The main source of infection of foals is believed to be from parasitic stages ( L 3 ) in mares' milk acquired by foals while nursing (Lyons et al., 1969, 1973 ). Probably, to a lesser degree, infections in foals also occur from free-living third-stage larvae that are ingested in feed or penetrate the skin (Lyons et al., 1973 ). This parasite has been incriminated circumstantially as a cause of diarrheas in foals (Lyons et al., 1991 ). The purpose of the present study was to determine the current prevalence of S. westeri in foals by examining their feces for eggs of this parasite. Information obtained would be an indicator of the effectiveness of contemporary antiparasitic drugs, such as the benzimidazoles and ivermectin, on this parasite. Of particular interest was comparison of prevalence at this time with that several years ago when effective drugs were unavailable. *Corresponding author.

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Table 1 Antiparasitic treatment o f d a m s of foals from which fecal samples were collected for examination for eggs o f S t r o n g y l o i d e s westeri in 1992 Farm

No. of mares

T r e a t m e n t relative to foaling Before foaling a Drug ( n )

A

31

Ba C

13 183

D

24

After foaling b Days c

Drug ( n )

Range

Mean

IVE (9) PRT (8) FBZ (4) ND(10) N D (13) IVE (183)

1-65 2-50 43-67 0-84

36 29 58 39

PRT (16) N D (8)

0-54 -

21 -

-

-

IVE (10) PRT (16) NT (2) N D (3) 1VE (13) IVE (44) NT (139) lYE (2) PRT (5)

-

N T N D

E F

23 33

H

21 38

1

16

G

d

IVE (23) IVE (15) PRT (1) OBZ (12) ND(5)

32-131 22-102 70 2-54 -

88 48 70 24 -

( 1 2 )

(5)

PRT (23) IVE (16) PRT (3) OBZ (2) FBT(1)

-

-

-

N T

-

-

-

ND(I) c

-

-

-

N D

IVE (21) IVE (11) PRT (2) OBZ ( 2 )

5-102 47-87 3-60 26-30

N D (23) IVE ( 3 ) OBZ (8) N D (2) e

. 76-86 25-65 72-82

ND (3)

57 59 32 28 .

.

(6)

Mean

2-24 3-31 0-0 0-26 14-20 0-10

10 11 0 9 17 4

-

-

-

-

-

-

.

7 4 10 8 4 -

1

( 4 )

. IVE (16) .

Range

7-7 1-9 1-24 2-14 4

N T (21) IVE (32) N T (5) N D (1)

82 49 77 .

Days c

1 -

0-21 -

4 -

2-3 -

3 -

.

.

1VE, ivermectin; PRT, pyrantel pamoate; FBZ, fenbendazole; OBZ, oxibendazole; FBT, febantel. NT, no treatment (definitely no drug given ). ND, not determined (data unavailable as to w h e t h e r / w h a t drug was given). aLast therapeutic treatment before foaling. bThis is the only therapeutic treatment between foaling and collection of foal feces. CDay 0 is day of foaling. dOn continuous daily pyrantel tartrate. e M a r e ( s ) dewormed, but n a m e of d r u g ( s ) not determined.

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Materials and methods Feces were collected from foals for examination for S. westeri eggs from 28 February to 1 July 1992. Most of the fecal samples were taken from the rectum of the foals, with a few being recovered from freshly passed piles in wellbedded stalls. A total of 382 horse foals from nine farms in central Kentucky were sampled once. The breeds included 364 Thoroughbreds, 16 Standardbreds, one Lippizaner, and one draft-type horse. None of the foals was treated with an antiparasitic compound before collection of fecal samples. Older horses on the farms were on routine deworming programs. Antiparasitic treatments (therapeutic) of mares (last one before foaling and the only one between foaling and sampling of foals) were given at 0-131 days before foaling and 0-31 days after foaling (Table 1 ). They included use of ivermectin before and/or after foaling for all mares for which data were available. Other compounds given to the mares were pyrantel pamoate, oxibendazole, febantel, and fenbendazole. In a few instances, the drug given to some mares was unknown or it was not determined whether any treatment was administered. On some farms, ivermectin was given to the mares on the day of foaling (Farm B ) or at about 3 days after foaling (Farm I). Also, mares on Farm E received pyrantel pamoate 1 week after foaling. On other farms, ivermectin or other drugs were not administered in relationTable 2 Data on foals whose feces were examined for eggs o f S t r o n g y l o i d e s westeri in 1992 Farm a

No. sampled

M

A Bb C Dc E F G H I Total

18 7 87 8 11 20 9 20 9 189

F

13 6 96 16 12 13 12 18 7 193

Bi~h date range Total

31 13 183 24 23 33 21 38 16 382

2/14-6/09 2/17-5/02 1/26-6/05 2/12-4/16 2/11-5/20 1/15-5/28 1/22-4/28 1/19-4/26 3/18-5/29 1/15-6/09

Age when sampled (days)

Fecalsamples positive

Range

No.

16-48 10-36 13-37 13-23 12-36 9-63 7-62 13-60 14-31 7-63

M, male; F, female. aAll foals were Thoroughbred except as noted. bStandardbreds (all). cStandardbred ( n = 3 ) ; Lippizaner ( n = 1 ); draft ( n = 1 ).

Mean

27 23 19 18 20 25 27 30 22 22

1 0 2 2 11 4 1 0 1 22

%

3 0 1 8 48 12 4 0 6 6

Age o f f o a l ( d a y s ) Range

Mean

20

20 17 20 22 33 52

15-19 19-20 14-27 14-63 52 25 14-63

25 24

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Table 3 Data on antiparasitic treatment of mares whose foals had fecal samples positive for eggs o f S t r o n g y loides westeri in 1992

Farm

Foals-positive

Before foaling

No.

Age ( d a y s )

Drug

Days

20 17 15 20 19 14 24 17 19 26 26 21 20 27 19 16 63 23 31 14 52 25

ND IVE IVE PRT PRT IVE IVE IVE IVE IVE IVE |VE IVE IVE IVE IVE ND IVE IVE IVE IVE ND a

46 12 0 1 48 67 74 100 107 107 112 113 120 128 131 39 60 29 96 72

A C

1 2

D

2

E

11

F

4

Gb I

1 1

Foaling date

2/27 3/22 5/12 2/22 2/23 2/27 3/17 3/24 4/19 4/26 4/26 5/01 5/02 5/09 5/17 5/20 1 / 15 2/24 3/29 5/28 3/22 4/27

After foaling Drug

Days

PRT NT NT PRT NT PRT PRT PRT PRT PRT PRT PRT PRT PRT PRT PRT ND a FBT OBZ IVE NT IVE

18 0 7 7 7 7 7 7 7 7 7 7 7 1 4 2 I 3

N D , not determined (data unavailable as to whether/what drug was given ). NT, no treatment (definitely no drug given ). IVE, ivermectin; PRT, pyrantel pamoate; FBT, febantel; OBZ, oxibendazole.

aMare(s) dewormed, but name of drug(s) not determined. bOn continuous daily pyrantel tartrate.

ship to foaling, but according to a routine deworming schedule. On Farm C, two foals were put on nurse mares (draft-type) immediately after birth because of lactation problems with their dams. Deworming data on the nurse mares are unknown except they were probably given ivermectin just before the foals were placed with them. Mares on two farms (B and G) were given pyrantel tartrate continuously. A qualitative procedure was used to recover S. westeri eggs from fecal sampies. This was the same technique as described by Lyons et al. (1988) for recovering Eimeria leuckarti oocysts from feces, except for changing the flotation solution to saturated sodium chloride (SG 1.18 ). Results Prevalence of S. westeri eggs in feces o f foals and other data on them are delineated in Table 2. The foals were born between 15 January and 9 June

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and were 7-63 days old (mean 22 days) when sampled. Of the 382 foals examined, S. westeri eggs were found in feces of 22 (6%). The age of the positive foals ranged from 14 to 63 days (mean 24 days). Foals on seven of the nine farms (78%) were infected. Prevalences for foals on the positive farms varied from 1% to 48%. Individual data are given on drug treatment of dams whose foals were positive (Table 3 ). Ivermectin was given to the dams of 17 foals at 12-131 days before foaling and O~'two at 1 or 3 days after foaling. Four mares were not treated after foaling. Data on treatment were not available after foaling for one mare and before foaling for three mares whose foals were positive. Drugs other than ivermectin, given to other mares before and/or after foaling, were pyrantel pamoate, pyrantel tartrate (continuous), oxibendazole, and febantel. The only two positive foals out of 183 sampled on Farm C had been on nurse mares, whose parasite control was uncertain, although they probably received ivermectin when brought to the farm.

Discussion

The low prevalence ofS. westeri in foals, as determined from eggs in feces, was in marked contrast to that found in former surveys. There have been previous reports that prevalence of this parasite was over 90% in foals in this area (Todd et al., 1949; Lyons et al., 1973; E.T. Lyons, unpublished data, 1969). Most of these prevalences were completed before the advent of effective drugs on S. westeri. Three compounds have label claims for removal of enteric stages ofS. westeri in foals in this country. They are thiabendazole (Drudge et al., 1982, 1983 ), oxibendazole (Drudge et al., 1981, 1985 ), and ivermectin (Ryan and Best, 1985 ). Cambendazole, which is no longer on the market, also is highly effective on this parasite in foals (Drudge et al., 1983 ). Also, cambendazole, when given to mares, was shown to have at least some activity in blocking transmission of milk stages (Lyons et al., 1977 ). Effectiveness of these drugs in removing strongyloides from foals, no doubt, contributed to reduction in transmission of this parasite. This means that, in particular, there are reduced infections because of fewer infective stages available to migrate to tissues of mares and pass through the mammary system to infect foals. Experimental data indicate that another drug, fenbendazole (currently on the market), has activity on intestinal stages of S. westeri at higher (50 mg kg- 1) than therapeutic doses (Drudge et al., 1981 ). Ivermectin, in addition to being effective on S. westeri in foals, when given to mares causes reduction of larvae passing through the mammary system (Ludwig et al., 1983 ). Thus, it has a two-fold

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advantage in controlling this parasite. Ivermectin is probably the only compound given to mares during the present study that may have directly reduced, blocked, a n d / o r eliminated milk stages. Attempts were made to collect fecal samples from foals at a young enough age that infections could be probably attributed to being derived from transm a m m a r y transmission. The prepatent period is about 10-12 days. Parasitic third stages can pass in the milk of mares for several days (at least 47 ) (Lyons et al., 1973 ). Foals in this study were sampled at an average of 22 days of age. It is possible that some infections, e.g. on Farm E, where the prevalence was highest, were from free-living stages in the environment from eggs passed by earlier infected foals. However, it is of interest that none of the mares on Farm E, with positive foals, received ivermectin within 48 days of foaling, or at all after foaling. The prevalence (1%) on Farm C is especially interesting. More foals ( 183 ) were sampled on this farm than any other. Parasite control on Farm C has included exclusive use of ivermectin about every 8 weeks for 9 years, with occasional treatment with pyrantel pamoate between ivermectin treatments (E.T. Lyons, unpublished data, 1992 ). The only two positive foals apparently were infected from nurse mares that they suckled. Finding no positive foals which were nursing their own dams provides strong indication of the effectiveness of ivermectin. It should be stated that this farm has had an excellent parasite control program for several decades (E.T. Lyons, unpublished data, 1992). Extensive use of thiabendazole and ivermectin probably contributed to reduced prevalence ofS. westeri in foals. From this study, the data show that prevalence of S. westeri has obviously decreased dramatically over time. The reduction is probably the result of the use of highly effective drugs, first the benzimidazoles and more recently ivermectin.

Acknowledgments This investigation (Paper 92-4-186 ) was made in connection with a project of the Kentucky Agricultural Experiment Station and is published with the approval of the director. Appreciation is expressed to the horse farm owners, farm managers, other farm personnel, and veterinarians who made this research possible.

References Drudge, J.H., Lyons,E.T., Tolliver, S.C. and Kubis, J.E., 1981. Clinicaltrials with fenbendazole

and oxibendazolefor Strongyloides westeriinfectionin foals. Am. J. Vet. Res., 42: 526-527. Drudge, J.H., Lyons,E.T. and Tolliver, S.C., 1982. Controlledtests of pastes of dichlorvosand

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thiabendazole against induced Strongyloides westeri infections in pony foals in 1973-1974. Am. J. Vet. Res., 43: 1675-1677. Drudge, J.H., Lyons, E.T., Tolliver, S.C. and Kubis, J.E., 1983. Clinical trials of 3 benzimidazoles for Strongyloides westeri infection in foals. Mod. Vet. Pract., 64: 414-417. Ludwig, K.G., Craig, T.M., Bowen, J.M., Ansari, M.M. and Ley, W.B., 1983. Efficacy of ivermectin in controlling Strongyloides westeri infection in foals. Am. J. Vet. Res., 44:314-316. Lyons, E.T., Drudge, J.H. and Tolliver, S.C., 1969. Parasites from mare's milk. Bloodhorse, 95: 2270-2271. Lyons, E.T., Drudge, J.H. and Tolliver, S.C., 1973. On the life cycle ofStrongyloides westeri in the equine. J. Parasitol., 59: 780-787. Lyons, E.T., Drudge, J.H. and Tolliver, S.C., 1977. Observations on development of Strongyloides westeri in foals nursing dams treated with cambendazole or thiabendazole. Am. J. Vet. Res., 38: 889-892. Lyons, E.T., Drudge, J.H. and Tolliver, S.C., 1988. Natural infection with Eimeria leuckarti: prevalence of oocysts in feces of horse foals on several farms in Kentucky during 1986. Am. J. Vet. Res., 49: 96-98. Lyons, E.T., Drudge, J.H., Tolliver, S.C. and Granstrom, D.E., 1991. The role of intestinal nematodes in foal diarrhea. Vet. Med., 86: 320-328. Ryan, W.G. and Best, P.J., 1985. Efficacy of ivermectin paste against Strongyloides westeri in foals. Vet. Rec., 117: 169-170. Todd, A.C., Kelley, G.W., Wyant, Z.N., Hansen, M.F. and Hull, F.E., 1949. Worm parasites in Thoroughbred sucklings and weanlings. A survey of incidence, development and control. Ky. Agric. Exp. Sta. Bull., 541, 24 pp.