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A questionnaire survey on nematode control practices on horse farms in Denmark and the existence of risk factors for the development of anthelmintic resistance
Veterinary Parasitology 78 (1998) 49±63
A questionnaire survey on nematode control practices on horse farms in Denmark and the existence of risk factors for the development of anthelmintic resistance S. Lendala, M.M. Larsena, H. Bjùrnb,c,*, J. Cravenc, M. ChrieÂla, S.N. Olsend a
Division of Ethology & Health, The Royal Veterinary and Agricultural University, BuÈlowsvej 13, DK-1870, Frederiksberg C., Denmark b Section of Parasitology, Department of Pathology and Epidemiology, Danish Veterinary Laboratory, BuÈlowsvej 27, DK-1790 Copenhagen V, Denmark c Danish Centre for Experimental Parasitology, The Royal Veterinary and Agricultural University, BuÈlowsvej 13, DK-1870, Frederiksberg C., Denmark d Department of Clinical Studies, Large Animal Medicine, The Royal Veterinary and Agricultural University, BuÈlowsvej 13, DK-1870, Frederiksberg C., Denmark Received 22 September 1997; accepted 16 January 1998
Abstract A questionnaire survey to obtain information on endoparasite control practices and management on 68 Danish horse farms was undertaken in 1995. The study revealed that foals, young horses and adults were, on average, annually treated 4.3, 4.0 and 3.7 times, respectively. The most commonly used drug from 1993±1995 was ivermectin. On average 2.4 different drugs were used annually. The most used method of weight estimation was eye measure: for foals by 78%, for youngsters by 81% and adults by 82% of the herd owners. The most commonly used weight in the dosing of anthelmintics was individual weight of the horse: 72% of the herd owners dosed their foals this way, 76% their youngsters and 75% their adults. Sixty two percent of the herd owners treated at turn out, 47% at housing, 57% treated when buying new horses, 26% treated when stabling visiting horses, 78% applied pasture change and 18% performed alternate/mixed grazing. Sixty one percent of the herds had experienced problems with diarrhoea and in 18% of the cases the suspected cause was considered to be endoparasites. 33% of the farms performed disease registration and on 25% Faecal Egg Count Reduction tests had been performed before entering this study. The herd owners
* Corresponding author. Fax: 0045 35 300181; e-mail: [email protected] 0304-4017/98/$19.00 # 1998 Elsevier Science B.V. All rights reserved PII S 0 3 0 4 - 4 0 1 7 ( 9 8 ) 0 0 1 1 7 - 4
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obtained their formation about endoparasite control from veterinarians, meetings and papers in that order of importance. # 1998 Elsevier Science B.V. Keywords: Horse; Epidemiology; Control methods-Nematoda; Resistance
1. Introduction Most endoparasite control programmes rely on prophylactic use of anthelmintics but the value of these are under threat due to development of anthelmintic resistance (AR). Therefore, it is important to obtain information on the use of anthelmintics and relevant management practices in order to recommend control measures that can prolong the life span of the existing anthelmintics on the market. Studies on the use of anthelmintics have been performed for cattle in England and Wales (Michel et al., 1981), cattle and sheep in England (Gettinby et al., 1987), sheep in New Zealand (Brunsdon et al., 1983) and USA (Tritschler et al., 1986; Reinemeyer et al., 1992) and goats in New Zealand (Pearson and McKenzie, 1986). Factors that promote the development of AR are known to be the repeated use of anthelmintics with the same mode of action for several years; frequent treatments; under dosing of the anthelmintic (Bjùrn et al., 1991). Other factors responsible for the development of AR could be permanent pastures, high stocking rates and no treatment of new horses introduced into the herd (Bjùrn et al., 1991). All the above mentioned factors makes it necessary to investigate the association between AR and the risk factors in management which potentially contribute to its development. Such studies have been made for sheep in New Zealand and Australia (Kettle et al., 1982; Edwards et al., 1986) and for pigs (Dangolla, 1994), goats (Maingi et al., 1996a) and sheep (Maingi et al., 1996b) in Denmark, but no recorded information is available on the endoparasite control programmes in horse herds. Since AR has been documented against the cyathostomes in Denmark (Bjùrn et al., 1991), it is important to evaluate the management practices that may accelerate the development of AR. Therefore, a questionnaire survey was carried out in 1995 in order to obtain information on the practical endoparasite control on horse farms and the information was validated in a repeatability study. The objective of the study was to investigate the endoparasite control practices on Danish horse farms in order to detect risk factors for the development of AR. Furthermore, a repeatability study was performed in order to validate the original questionnaire data. 2. Materials and methods In 1994, members of `The Danish Horse Practising Veterinarian Society' were asked to participate in the study. After selection, 22 veterinarians volunteered and a total of 68 herds with more than 15 horses were included. The herds were from all over the country. The inclusion criterion for the minimum herd size was made because a Faecal Egg Count
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Reduction Test (FECRT) was due to be performed later that year. The FECRT was described by Craven et al., 1998 and the results of the AR study referred to in this paper were calculated by the method described by Coles et al., 1992. At the beginning of 1995 a questionnaire was developed. It included year of establishment, size of the herd, use of anthelmintic products during the period from 1990 to 1995, factors and advisers involved in the choice of anthelmintic, treatment strategies and relevant management factors (use of pasture etc.). The questionnaire included 22 questions of which three were open-ended (year of establishment, size of the herd and total size of the farm area) and the others close-ended. Whenever possible the questions were divided into the following age categories: Horses younger than one year of age (foals), horses between one and three years of age (youngsters) and horses older than three years (adults). The veterinarians were instructed to select the herds, interview the owner and return the questionnaire before the end of April 1995. No formal procedures were possible to implement in order to secure representativeness among the participating veterinarians and herds with this design. In the repeatability study in 1997 questions on year of establishment, type and size of herd, size of area, reason for treating with anthelmintics and use of anthelmintics during the period 1993 to 1995 were included. Two additional questions on whether there had been any problems with diarrhoea in the herd and if there were any changes made in the treatment strategies were also included. A total of 66, out of the original 68 herd owners participated in the repeatability study. Furthermore, the veterinarians were interviewed in order to obtain information about the reason for selecting the horse herds to the 1995 study. The veterinarians were asked to describe their recommendations regarding endoparasite control practices and if these recommendations had altered after participating in the 1995-study. Responses were obtained from all 22 veterinarians. If the questionnaire was not correctly filled in, efforts were made to reach the herd owners by telephone in order to correct the mistakes. All responses from the repeatability study and the veterinarians were collected by telephone interviews. 3. Data analysis Bivariate analyses were performed in order to find significant differences in the data material. Chi-square analysis was used for class variables. Means and standard deviations were stated for continuous variables. Agreement between the two questionnaires was expressed as kappa-values (Fleiss, 1981). The 95% confidence intervals for the kappavalues were calculated according to Armitage and Berry (1987). When percentages of responses were calculated missing values were excluded from the denominator. 4. Results The distribution of herds, the mean number of horses and the average areas are shown in Table 1. The mean deviation in answers on the number of horses from the
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Table 1 Distribution of the 68 farms in the study with respect to herd type, the mean number of horses (mean) with the standard deviation ( SD) and the average area (in ha) with the range (min.±max.) in each herd type Herd typea
No. (%)
Mean no. of horses( SD)
Average area and range (min.±max.)
Stud-farm Pension Riding school Other typesb
36 11 14 7
27 23 39 36
12.5 10.0 10.2 8.3
(53) (16) (21) (10)
(15.0) (8.0) (15.4) (20.1)
(3.3±85.0) (4.0±16.6) (2.8±21.5) (5.0±12.0)
a
The herd types were significantly different (p0.001). The category `other types' includes three stables for trotting horses, two farms who could not be placed in just one category, one stallion station and one stable for race horses.
b
questionnaire to the repeatability study are shown in Figs. 1±3 and show that the herd owners remembered the number of foals better than the number of youngsters and adults. In Table 2 the number of annual treatments and mean number of treatments in the different age categories are listed. In 1993 and 1994 the mean number of different anthelmintic products used was 2.5 per year and in 1995 was 2.4 products.
Fig. 1. The repeatability of the questionnaires regarding the number of foals. The figure shows the distribution of deviations* in the remembrance of the numbers. (* The mean deviation and the standard deviation was 1.1 (1.6) in 1995, 1.1 (1.5) in 1994 and 1.7 (1.8) in 1993.)
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Fig. 2. The repeatability of the questionnaires regarding the number of youngsters. The figure shows the distribution of the deviations* in the remembrance of the numbers. (* The mean deviation and the standard deviation was 2.6 (2.9) in 1995, 2.2 (3.0) in 1994 and 1.8 (2.6) in 1993.)
Table 2 Frequency of annual anthelmintic treatments in 68 Danish horse herds Foals
Youngsters
Adults
(0±1)
(1±3)
(>3)
11
6
Treatments per year
n (%)
n (%)
n (%)
1 2 3 4 5 6 9 10 Mean number of treatments per year
2 (4) 4 (7) 7 (12) 21 (37) 13 (22) 8 (14) 1 (2) 1 (2) 4.3
2 (3) 4 (7) 11 (18) 30 (48) 7 (11) 8 (13) 0 0 4.0
2 (3) 12 (18) 10 (15) 32 (47) 5 (7) 7 (10) 0 0 3.7 ( p0.01)
Age categories (years) Missinga
a
Questionnaires with no responses.
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Fig. 3. The repeatability of the questionnaires regarding the number of adults. The figure shows the distribution of the deviations* in the remembrance of the numbers. (* The mean deviation and the standard deviation were 3.0 (3.5) in 1995, 3.4 (4.2) in 1994 and 3.9 (4.2) in 1993.)
In 1995 ivermectin was the most commonly used anthelmintic in Danish horse herds followed by the benzimidazoles and pyrantel. The same picture was seen in the previous years (Table 3). The kappa-values and the corresponding 95% confidence intervals for the remembrance of the use of the four chemical classes of anthelmintic compounds approved to treat horses in Denmark (benzimidazoles, pyrantel, ivermectin and dichlorvos), were for the year 1995: 0.54 [0.45; 0.62], for 1994: 0.60 [0.51; 0.69], and for 1993: 0.59 [0.50; 0.69]. The kappa-values for combinations of drugs were 0.28 [0.14; 0.42], 0.46 [0.31; 0.61] and 0.45 [0.30; 0.60] for the years 1995, 1994 and 1993, respectively. The most preferred drug formulation was paste (most preferred in 57 (84%) herds) and the least preferred drug formulations were mixture (least preferred in 58 (72%) herds); pellets (least preferred by 45 (66%)) and granulate (least preferred by 38 (56%)). The reasons for treating with anthelmintics were to avoid diseases/unthriftiness in 59 (87%) herds, to be safe in 11 (16%), to prevent the horses from giving low competition performances in 7 (10%) and to save feeding costs in 5 (7%) herds. The most commonly used method for body weight estimation was eye measure. It was used for foals in 46 (78%) herds, for youngsters in 51 (81%) and for adults in 56 (82%).
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Table 3 The number (and percentages) of horse farms who uses various anthelmintics during the period 1990±1995 Class n
1995
1994
1993
1992
1991
1990
66
67
65
61
55
50
2
1
3
7
13
18
Group 1 Benzimidazoles
44 (67)
47 (70)
60 (92)
47 (77)
37 (67)
34 (68)
Group 2 Pyrantel
37 (56)
40 (60)
26 (40)
22 (36)
13 (24)
9 (18)
Group 3 Ivermectin
60 (91)
63 (94)
57 (88)
54 (89)
47 (85)
41 (82)
Group 5 Dichlorvos
7 (11)
6 (9)
5 (8)
5 (8)
5 (9)
6 (12)
Other drugs Do not remember
6 (9) 0
4 (6) 0
5 (8) 0
4 (7) 1 (2)
2 (4) 2 (4)
2 (4) 4 (8)
Missing
a
n: Number of farms. a Questionnaires with no responses.
There was no significant difference in the weight estimation method between herd types. When dosing with anthelmintics, the individual weight of the horses was the most frequently used method in all age categories; for foals in 42 (72%) herds, for youngsters in 47 (76%) and for adults in 51 (75%). The different management practices in the various herd types are shown in Table 4 and it is shown that FECR-tests had been performed in 17 (25%) herds. The reason for performing this test was diarrhoea in 5 (29%), own interest in 3 (18%), and colic in 2 (12%) cases. In 40 (61%) herds problems with diarrhoea had been observed. In 21 (53%) of these cases the veterinarian was called. The duration of the diarrhoea lasted either less than a week in 16 (40%) of the cases or more than one month in 17 (43%). In 10 (25%) of the cases the herd owner did not know the causal factor for the diarrhoea and in 12 (39%) they believed that is was because they feed silage. Endoparasites were the suspected cause in 7 (18%) of the cases and in 4 (10%) of the cases the suspected cause was the fact that the horses ate sand. The most important factors in choosing an anthelmintic (Table 5) were the possibilities of direct administration, the experience of `good effect' of the anthelmintic and the veterinarian's recommendation. In Table 6 the importance of different sources of information on endoparasite control is presented. There was no significant difference between herd types in the sources of information. In 32 (47%) herds advisers were involved in planning the anthelmintic treatment strategies. The most commonly used adviser was the veterinarian (used by 31 (97%) herd
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Table 4 The use of different management practises in the different herd types Management factor
Stud farms No. (%)
Pastures are permanent Pasture rotation is used a Horses are moved to mown pastures Alternate grazing is used Horse dung is spread on pastures Performs anthelmintic treatment at turn out Performs anthelmintic treatment at pasture rotation Performs anthelmintic treatments at housing New horses are treated at introduction Visiting horses are treated Problems with diarrhoeab FECR-tests have been performed earlier Disease registration is performedc Adviser is used in the planning of anthelmintic treatment Changes in the parasite control routines are made after participating in the study
21 (62) 30 (88) 21 (64)
Pensions No. (%)
Riding schools No. (%)
Other herd types No. (%)
Total No. (%)
n
6 (55) 8 (73) 7 (70)
13 (93) 8 (73) 7 (64)
6 (86) 3 (43) 1 (17)
46 (70) 49 (78) 36 (60)
66 63 60
9 (25) 5 (16)
2 (18) 2 (20)
1 (7) 2 (14)
0 0
12 (18) 9 (14)
68 63
22 (61)
9 (82)
9 (64)
2 (29)
42 (62)
68
7 (19)
4 (36)
2 (14)
0
13 (19)
68
17 (47)
5 (45)
8 (57)
2 (29)
32 (47)
68
21 (58)
7 (64)
8 (57)
3 (43)
39 (57)
68
8 (22) 23 (72) 9 (25)
4 (36) 10 (71) 5 (45)
6 (43) 4 (44) 1 (7)
0 3 (27) 2 (29)
18 (26) 40 (61) 17 (25)
68 66 68
17 (47)
0
3 (21)
2 (29)
22 (32)
68
19 (53)
4 (36)
5 (36)
4 (57)
32 (47)
68
8 (25)
4 (29)
0
5 (45)
17 (26)
66
a
p0.05 p0.039 c p0.013 The percentages are calculated for the number of positive respondents, n is the total number of respondents. b
owners), the second mostly used were other farmers, used by 5 (16%), and agronomists were used by 4 (13%) herd owners. There was no significant difference between herd types. In 17 (26%) herds changes have been made after participating in the study. The most common changes were the dosing of anthelmintics based on individual weights (used by 14 (82%) herd owners) and changes in the conditions regarding anthelmintic treatments (regarding choice of anthelmintics etc.) in 12 (71%) herds. In 6 (35%) herds the change was to fewer annual treatments, 6 (35%) tried to limit infection and 5 (29%) improved pasture hygiene. Three (18%) herd owners performed faecal egg counts before treatment and 2 (12%) herds owners increased the number of annual treatments. There was no significant difference between herd types in the changes made.
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Table 5 The importance of various factors involved in the choice of anthelmintics on horse farms (n68) Factor
Most important n (%)
Important n (%)
Not Important n (%)
Price of the drug Can be administered in feed Directly administration Experience of `good effect' Feed mill recommended Veterinarian recommended Pharmacist recommended Commercial advertisements
8 11 52 50 0 43 0 0
23 12 12 11 5 19 5 9
37 45 4 7 63 6 63 59
(12) (16) (76) (74) (63)
(34) (18) (18) (16) (7) (28) (7) (13)
(54) (66) (6) (10) (93) (9) (93) (87)
Thirty nine (53%) herds were included in the study because the veterinarian suspected them to be problem herds or have AR in the herds. Twenty four (33%) herds were selected due to the herd size and eight (11%) herds were sampled by convenience. The last 2 (3%) herds were selected because the herd owner applied after having heard about the study. The number of farms that each veterinarian entered the study varied from one to nine. The factors that influenced the veterinarian's recommendations to the herd owners on endoparasite control were conditions of the pastures (whether there was grazing or not, whether there was pasture rotation, stocking rates etc.) for 16 (73%) veterinarians. Factors regarding the herd (grouping of horses by age, herd size, replacement of horses etc.) for 15 (67%). Nine (41%) veterinarians stated that factors regarding the health of the horses (problems with colic/diarrhoea, suspected endoparasitic problems, level of parasite infection in the herd etc.) influenced their recommendations to the herd owners. AR influenced only 3 (14%) of the veterinarians in their recommendations to the herd owners. Changes in the recommendations given to herd owners after the participation in the FECR-study were made by 13 (59%) veterinarians: all stated that they have made changes in the choice of anthelmintics and 3 stated that they paid more attention to the AR problem.
Table 6 The importance of different sources to give information about endoparasite control (n68) Source
Most important n (%)
Important n (%)
Not important n (%)
Meetings/courses Papers Agronomist Veterinarian Feed mill Pharmacist Other farmers
24 32 11 52 0 1 14
25 21 16 13 11 3 37
19 15 41 3 57 64 17
(35) (47) (16) (77) (2) (21)
(37) (31) (24) (19) (16) (4) (54)
(28) (22) (60) (4) (84) (94) (25)
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5. Discussion The fact that some herd owners did not remember the number of horses in their herd indicates that there is a frequent exchange of horses between farms which can cause the spread of AR. When the exchange rate of horses is high it becomes difficult to estimate the total number of horses in one year. It was impossible to calculate the stocking rate, because we have no information of the area that was used for pastures. Riding schools and the category `other herd types' are often big herds with a small area and therefore have a high stocking rate. The results of the questions on use of anthelmintics revealed a lack of knowledge. Sixty seven percent of the farmers used benzimidazole anthelmintics in 1995 in spite of the fact that the prevalence of AR to benzimidazoles was 78% (Craven et al., 1998). In 1996, after the AR study was finished and the farmers had received the results, 55% of the farms still used benzimidazoles. The use of ivermectin has increased to a critical level: 91% stated that they used ivermectin at least once a year in 1995. Ivermectin is, at present, the only drug with 100% effectivity against the adult cyathostomes but resistance to this drug has developed within a very short period of time in other livestock species. Ivermectin was first marketed in 1981 (Shoop et al., 1995) and resistance was detected in Haemonchus contortus in sheep in South Africa by Carmichael et al. (1987). This means that there is a potential danger of AR developing against this drug in horse parasites due to uncritical use. The fact that ivermectin is the most commonly used anthelmintic in Danish horse herds is consistent with the question on the importance of the price of the drug in which only 12% stated that the price was important to the choice of anthelmintic. If ivermectin is used in a sensible manner it is highly effective against benzimidazole resistant parasites (Herd, 1992) but if used indiscriminately without considering the possibility of development of AR, it is not likely that it will maintain its effectiveness. Eighty seven percent of the herd owners treated because they wanted to avoid unthriftiness/diseases. This means that endoparasite control is aimed as prophylaxis and not as a `treatment', after determination of EPG, as it ought to. Anthelmintics should be used strategically and the number of annual treatments should be minimized in order to extend the life span of the available anthelmintics. This means that the times of treatment should be determined according to the epidemiology of the parasite. Strategic treatment times are prior to turn out and pasture rotation (Herd, 1992) so that heavy contamination of pastures can be avoided. It is seen that foals, youngsters and adults are treated in different ways. Under estimation of body weight leads to under dosing of anthelmintics which is demonstrated to be a risk factor for the development of AR (Wescott, 1986; Waller, 1987). Therefore, it is critical that the majority of herd owners estimates the body weight by eye measure. Another factor that might lead to under dosing is the fact that the most preferred drug formulation (paste) are marketed in tubes in which the maximum treatment dose is for a horse with a weight of 500 or 600 kg and a normal riding horse does easily exceed this weight.
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Measures to prevent development of parasitism and subsequently AR are widely used: pasture rotation (78%), moving the horses to mown pastures (60%) and alternate/mixed grazing with other species (18%). Pasture rotation is an effective control strategy if it is used properly: The same pasture should only be used once in each grazing season since it is of no value to move horses back to a pasture that has already been contaminated. It should be stressed that no information whether the rotation was to a clean pasture was available. The use of measures that could reduce the infection level of the pastures revealed a lack of knowledge. The herd owners treated horses they bought more frequently than horses that were just visiting for a period (57% versus 26%). From a parasitological point of view there is no difference between introducing a horse whether it is bought or just visiting, but the herd owners seemed to regard the two things differently. This is critical because AR can be introduced in a herd with a horse harbouring anthelmintic resistant parasites. The use of treatment at turn out varied between 29% in `other herd types' to 82% in pensions and treatment at pasture rotation varied from none in `other herd types' to 36% in pensions. Treatment of new horses prior to introduction into a herd also minimises the risk of infection and the risk of spreading AR (Herd, 1992). The spread of horse manure on the pastures varied between none in the `other herd types' to 20% at the pensions. This practice constitutes a major risk of infection. The existence ± and spread ± of AR also means that more attention should be paid to other control measures than the use of anthelmintics. These are often aimed at reducing the pasture infectivity level which could have risen to a dangerous level by the end of summer or in autumn (Eysker et al., 1986). This means that much can be achieved by avoiding heavily infected pastures in the second half of the grazing season. One method to avoid the risk of massive infection in late summer/autumn is pasture rotation to safe pastures (Bjùrn et al., 1991). Another method is to reduce the relative stocking density by alternate or mixed grazing with cattle or sheep (Eysker et al., 1986). Removal of horse manure from the pastures (Herd, 1986) is yet another method of reducing the pasture infectivity level. It is of great importance that the herd is checked for AR (FECR-tests) so that only effective anthelmintics are used and unnecessary anthelmintic treatments are avoided (Herd, 1992). It is advisable to have the parasite status of the herd determined prior to anthelmintic treatment. FECR-tests were only performed in 25% of the herds. Possible reasons for performing faecal examinations could be assumed to be due to cyathostomes since unthriftiness and diarrhoea were the major reasons. Cyathostomatosis, is characterized by diarrhoea, colic, weight loss, delayed shedding of the winter coat, edema and unthriftiness (DiPietro et al., 1990; Kelly and Fogarty, 1993; Reid et al., 1995) and is thought to be associated with the synchronous emergence of L4 larvae from tissue cysts, often during the winter and spring (Uhlinger, 1991: Reid et al., 1995). This study revealed that 61% of the herds have experienced problems with diarrhoea. In a study of reasons for diarrhoea in horses Love et al. (1992) found cyathostomatosis in 27% of the cases and another 27% remained undiagnosed. In this study, herd owners suspected parasites in 18% of the cases and the reason was unknown in 25%. The most common duration of diarrhoea were less than a week (40%) or longer than one month (43%). This is consistent with the reports on
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cyathostomatosis in which the durations are approximately a week (Kelly and Fogarty, 1993; Reilly et al., 1993; Mair, 1994) or more than a month (Church et al., 1986; Kelly and Fogarty, 1993). In this study the frequency of diarrhoea ± and of AR ± might be overestimated due to a selection bias as a result of the fact that 53% of the farms actually were selected due to suspected problems with parasites or AR. The cases of diarrhoea were more frequent in stud-farms and pensions than in the other herd types. In stud-farms a positive information bias might be part to the explanation due to more frequent disease registration (47% performed disease registration) or a higher number of young horses. The lack of remembrance is probably due to the fact that only 32% of the herd owners perform disease and treatment registration. The lack of registration is a risk factor for the development of AR, because specific control strategies are essential in order to recall the used products and time of administration. It will be almost impossible to make control strategies to prevent the development of AR and be certain that they will be followed by the herd owners which is important if the control programmes should be effective (DiPietro, 1992). In 97% of the herds using advisers, the veterinarians were involved in the planning of endoparasite control strategies. Seventy seven percent of herd owners stated that the veterinarian was the most important source of information on endoparasite control and 63% followed the veterinarians' recommendation of the choice of anthelmintics. Therefore it must be assumed that the veterinarian is the most important source of information on endoparasite control, but this might be overestimated due to the selection procedure. The recommendations to herd owners varied greatly and only 14% of the veterinarians stated that the AR problem had influenced their advice. Fifty nine percent of the veterinarians have changed their recommendations after participating in the AR-study. The most frequent change is that they no longer recommend benzimidazole in favour of ivermectin, a recommendation that includes a rising risk of AR to ivermectin. One of the major reasons for choosing an anthelmintic is the experience of `good effect' of the anthelmintic. The only possible method of determining whether the effect of an anthelmintic is satisfactory is by performing FECR-tests. This was only done in 25% of the herds. It is difficult to say whether there is a difference in the risk of AR between herd types because of the small sample size of both this questionnaire study and the AR study (Craven et al., 1998), but the categories `other herd types' and riding schools revealed greater number of AR than stud-farms and pensions, probably because of the relatively high stocking rate. AR towards benzimidazoles was present in all the examined herds from the category `other herd types' and resistance against both pyrantel and the benzimidazoles was found in riding schools. It should be stressed that the study is too small to detect statistical differences. The repeatability in this study was relatively low compared to other studies (Slater et al., 1992; Dangolla, 1994; Scholl et al., 1994 and Maingi et al., 1996b). The kappa-values on the remembrance of drug classes were fair but lower than in the studies mentioned above. The fact that the kappa-value is lower for the year 1995 than for the two previous years reflects that the herd owners did not plan the anthelmintic treatments and were only stating ideas for 1995 when the interview took place. It is expected that the kappa-value is
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lower in 1993 than in 1994. The kappa-values for drug combinations were low in all three years. The conclusion to this is that the herd owners remember some of the drugs they have used but not the combinations. This is probably due to the fact that the herd owners used an average of 2.4 different anthelmintic products annually which makes it difficult to remember. Twenty six percent of the herd owners had made changes after participating in the ARstudy. The changes were without strategy which is not good when trying to avoid increasing AR. Most of the changes were to not use benzimidazoles any more, only few have made alternative prophylactic arrangements, like more pasture rotation etc. The main conclusion of this study is that there is a massive lack of exact knowledge among herd owners about how to control endoparasites and avoid development of AR. This is consistent with the findings from other studies among owners of sheep and goat farms in Denmark (Maingi et al., 1996a). A concerted effort has to be made to inform the farmers about the importance of carefully planned control strategies against endoparasites so the increasing development of AR can be stopped. The sources of knowledge about the control of endoparasites were evaluated by the herd owners and it became clear that the veterinarian, meetings and articles were the most important ones. This means that these sources would be appropriate channels for future communication. It is of particular importance to make the veterinarians aware of the AR problem and to inform them about the appropriate endoparasite control strategies since they are the most important source of information to the herd owners and since their present guidelines to herd owners are not at all clear. Information directly to farmers in magazines is feasible but in-service training of veterinarians must have a top priority. Acknowledgements This study was supported by Merial (formerly MSD-AgVet.), Copenhagen, Denmark. We would also like to thank the veterinarians for providing the link between us and the herd owners. Thanks also to the herd owners for taking the time to answer the questionnaire. References Armitage, B., Berry, G., 1987. Statistical Methods in Medical Research, 2nd ed. Blackwell Scientific Publication, pp. 100±104. Bjùrn, H., Sommer, C., Schougaard, H., Henriksen, Sv.Aa., Nansen, P., 1991. Resistance to benzimidazole anthelmintics in small strongyles (Cyathostominae) of horses in Denmark. Acta. Vet. Scand. 32, 253±260. Brunsdon, R.V., Kissling, R., Hosking, B.C., 1983. A survey of anthelmintic usage for sheep: a time for change? N.Z. Vet. J. 31, 24±29. Carmichael, T., Visser, R., Schneider, D., Soll, M., 1987. Haemonchus contortus resistance to ivermectin. J. S. Afr. Vet. Ass. 58, 93. Church, S., Kelly, D.F., Obwolo, M.J., 1986. Diagnosis and successful treatment of diarrhoea in horses caused by immature small strongyles apparently insusceptible to anthelmintics. Equine Vet. J. 18(4), 401±403.
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Coles, C.G., Bauer, C., Borgsteede, F.H.M., Geerts, S., Klei, T.R., Taylor, M.A., Waller, P.J., 1992. World Association for the Advancement of Veterinary Parasitology (W.A.A.V.P) methods for detection of anthelmintic resistance in nematodes of veterinary importance. Vet. Parasitol. 44, 35±44. Craven, J., Bjùrn, H., Henriksen, Sv.Aa., Nansen, P., Larsen, M., Lendal, S., 1998. A survey of anthelmintic resistance on Danish horse farms, using 5 different methods of calculating faecal egg count reduction. Equine Vet. J. (In press). Dangolla, A., 1994. Epidemiological analysis of helminthological data from Danish sow herds with emphasis on occurrence of anthelmintic resistance. Ph.D. Thesis. The Royal veterinary and Agricultural University, Copenhagen. DiPietro, J.A., 1992. Daily anthelmintic therapy in horses. Comp. Cont. Educ. Pract. Vet. 14(5), 651±654. DiPietro, J.A., Klei, T.R., French, D.D., 1990. Contemporary topics on Equine parasitology. Comp. Cont. Educ. Pract. Vet. 12(5), 713±721. Edwards, J.R., Wroth, L., de Chaneet, C.G., Brasie, R.B., Karlson, J., Mercombes, P.W., Parton Morgan, G., Roberts, D., 1986. Survey for anthelmintic resistance in Australian sheep flocks. 2. Relationship with sheep management and parasite control practices. Aust. Vet. J. 63, 139±143. Eysker, M., Jansen, J., Mirck, M.H., 1986. Control of strongylosis in horses by alternate grazing of horses and sheep and some other aspects of the epidemiology of strongylidae infections. Vet. Parasitol. 19(1±2), 103±115. Fleiss, J.L., 1981. Statistical Methods for Rates and Proportions, 2nd ed. Wiley, Chichester, pp. 212±236. Gettinby, E., Armour, J., Bairden, K., Plenderleith, R.W.J., 1987. A survey by questionnaire of parasitic worm control in cattle and sheep at the Glasgow University Lanark practice. Vet. Record 121, 487±490. Herd, R.P., 1986. Parasite control in horses: Pasture sweeping. Mod. Vet. Pract. 67, 893±898. Herd, R.P., 1992. Choosing the optimal equine anthelmintic. Veterinary Medicine 87(3), 231±239. Kelly, J.C., Fogarty, U.M.G., 1993. Outbreak of larval cyathostomiasis on a thoroughbred stud-farm. Irish Vet. J. 46, 133±136. Kettle, P.R., Vlassoff, A., Ayling, J.M., McMurty, L.W., Smith, S.J., Watson, A.J., 1982. A survey of nematode control measures used by sheep farmers and anthelmintic resistance on these farms. Part 2. South Island excluding the Nelson region. N.Z. Vet. J. 30, 79±81. Love, S., Mair, T.S., Hillyer, M.H., 1992. Chronic diarrhoea in adult horses: a review of 51 referred cases. Vet. Record 130(11), 217±219. Maingi, N., Bjùrn, H., Thamsborg, S.M., Dangolla, A., Kyvsgaard, N.C., 1996a. A questionnaire survey of nematode parasite control practices on goat farms in Denmark. Vet. Parasitol. 66, 25±37. Maingi, N., Bjùrn, H., Thamsborg, S.M., Dangolla, A., Kyvsgaard, N.C., 1996b. Worm control practices on sheep farms in Denmark and implications for the development of anthelmintic resistance. Vet. Parasitol. 66, 39±52. Mair, T.S., 1994. Outbreak of larval cyathostomiasis among a group of yearling and two-year-old horses. Vet. Record 135, 598±600. Michel, J.F., Lotham, J.O., Leech, P.K., 1981. Use of anthelmintics for cattle in England and Wales during 1978. Vet. Record 108, 252±258. Pearson, A.B., McKenzie, R., 1986. Parasite control in fibre goats ± results of a postal questionnaire. N.Z. Vet. J. 34, 198±199. Reid, S.W.J., Mair, T.S., Hillyer, M.H., Love, S., 1995. Epidemiological risk factors associated with a diagnosis of clinical cyathostomiasis in the horse. Equine Vet. J. 27(2), 127±130. Reilly, G.A.C., Cassidy, J.P., Taylor, S.M., 1993. Two fatal cases of diarrhoea in horses associated with larvae of the small strongyles. Vet. Record 132, 267±268. Reinemeyer, C.R., Rohrbach, B.W., Grant, V.M., Radde, G.L., 1992. A survey of ovine parasite control practices in Tennessee. Vet. Parasitol. 42, 111±122. Scholl, D.T., Farver, T.B., Dobbelaar, P., Brand, A., Brouwer, F., Mass, N., 1994. Repeatability evaluation of a dairy farm management questionnaire. Prevent. Vet. Med. 18, 129±143. Shoop, W.L., Mrozik, H., Fisher, M.H., 1995. Structure and activity of avermectins and milbemycins in animal health. Vet. Parasitol. 59, 139±156. Slater, M.R., Scarlett, J.M., Donoghue, S., Erb, H.N., 1992. The repeatability and validity of a telephone questionnaire on diet and exercise in dogs. Prevent. Vet. Med. 13, 77±91.
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Tritschler, J.P., Giordano, D.L., Coles, C.G., 1986. Use of anthelmintics by New England sheep producers. J. Am. Vet. Med. Assoc. 189, 1309±1313. Uhlinger, C.A., 1991. Equine small strongyles: Epidemiology, pathology and prevention. Comp. Cont. Educ. Pract. Vet. 13(5), 863±869. Waller, P.J., 1987. Anthelmintic resistance and the future for roundworm control. Vet. Parasitol. 25, 177±191. Wescott, R.B., 1986. Anthelmintics and drug resistance. Vet. Clin. North Am. [Equine practice] 2(2), 367±380.
A questionnaire survey on nematode control practices on horse farms in Denmark and the existence of risk factors for the development of anthelmintic resistance S. Lendala, M.M. Larsena, H. Bjùrnb,c,*, J. Cravenc, M. ChrieÂla, S.N. Olsend a
Division of Ethology & Health, The Royal Veterinary and Agricultural University, BuÈlowsvej 13, DK-1870, Frederiksberg C., Denmark b Section of Parasitology, Department of Pathology and Epidemiology, Danish Veterinary Laboratory, BuÈlowsvej 27, DK-1790 Copenhagen V, Denmark c Danish Centre for Experimental Parasitology, The Royal Veterinary and Agricultural University, BuÈlowsvej 13, DK-1870, Frederiksberg C., Denmark d Department of Clinical Studies, Large Animal Medicine, The Royal Veterinary and Agricultural University, BuÈlowsvej 13, DK-1870, Frederiksberg C., Denmark Received 22 September 1997; accepted 16 January 1998
Abstract A questionnaire survey to obtain information on endoparasite control practices and management on 68 Danish horse farms was undertaken in 1995. The study revealed that foals, young horses and adults were, on average, annually treated 4.3, 4.0 and 3.7 times, respectively. The most commonly used drug from 1993±1995 was ivermectin. On average 2.4 different drugs were used annually. The most used method of weight estimation was eye measure: for foals by 78%, for youngsters by 81% and adults by 82% of the herd owners. The most commonly used weight in the dosing of anthelmintics was individual weight of the horse: 72% of the herd owners dosed their foals this way, 76% their youngsters and 75% their adults. Sixty two percent of the herd owners treated at turn out, 47% at housing, 57% treated when buying new horses, 26% treated when stabling visiting horses, 78% applied pasture change and 18% performed alternate/mixed grazing. Sixty one percent of the herds had experienced problems with diarrhoea and in 18% of the cases the suspected cause was considered to be endoparasites. 33% of the farms performed disease registration and on 25% Faecal Egg Count Reduction tests had been performed before entering this study. The herd owners
* Corresponding author. Fax: 0045 35 300181; e-mail: [email protected] 0304-4017/98/$19.00 # 1998 Elsevier Science B.V. All rights reserved PII S 0 3 0 4 - 4 0 1 7 ( 9 8 ) 0 0 1 1 7 - 4
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obtained their formation about endoparasite control from veterinarians, meetings and papers in that order of importance. # 1998 Elsevier Science B.V. Keywords: Horse; Epidemiology; Control methods-Nematoda; Resistance
1. Introduction Most endoparasite control programmes rely on prophylactic use of anthelmintics but the value of these are under threat due to development of anthelmintic resistance (AR). Therefore, it is important to obtain information on the use of anthelmintics and relevant management practices in order to recommend control measures that can prolong the life span of the existing anthelmintics on the market. Studies on the use of anthelmintics have been performed for cattle in England and Wales (Michel et al., 1981), cattle and sheep in England (Gettinby et al., 1987), sheep in New Zealand (Brunsdon et al., 1983) and USA (Tritschler et al., 1986; Reinemeyer et al., 1992) and goats in New Zealand (Pearson and McKenzie, 1986). Factors that promote the development of AR are known to be the repeated use of anthelmintics with the same mode of action for several years; frequent treatments; under dosing of the anthelmintic (Bjùrn et al., 1991). Other factors responsible for the development of AR could be permanent pastures, high stocking rates and no treatment of new horses introduced into the herd (Bjùrn et al., 1991). All the above mentioned factors makes it necessary to investigate the association between AR and the risk factors in management which potentially contribute to its development. Such studies have been made for sheep in New Zealand and Australia (Kettle et al., 1982; Edwards et al., 1986) and for pigs (Dangolla, 1994), goats (Maingi et al., 1996a) and sheep (Maingi et al., 1996b) in Denmark, but no recorded information is available on the endoparasite control programmes in horse herds. Since AR has been documented against the cyathostomes in Denmark (Bjùrn et al., 1991), it is important to evaluate the management practices that may accelerate the development of AR. Therefore, a questionnaire survey was carried out in 1995 in order to obtain information on the practical endoparasite control on horse farms and the information was validated in a repeatability study. The objective of the study was to investigate the endoparasite control practices on Danish horse farms in order to detect risk factors for the development of AR. Furthermore, a repeatability study was performed in order to validate the original questionnaire data. 2. Materials and methods In 1994, members of `The Danish Horse Practising Veterinarian Society' were asked to participate in the study. After selection, 22 veterinarians volunteered and a total of 68 herds with more than 15 horses were included. The herds were from all over the country. The inclusion criterion for the minimum herd size was made because a Faecal Egg Count
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51
Reduction Test (FECRT) was due to be performed later that year. The FECRT was described by Craven et al., 1998 and the results of the AR study referred to in this paper were calculated by the method described by Coles et al., 1992. At the beginning of 1995 a questionnaire was developed. It included year of establishment, size of the herd, use of anthelmintic products during the period from 1990 to 1995, factors and advisers involved in the choice of anthelmintic, treatment strategies and relevant management factors (use of pasture etc.). The questionnaire included 22 questions of which three were open-ended (year of establishment, size of the herd and total size of the farm area) and the others close-ended. Whenever possible the questions were divided into the following age categories: Horses younger than one year of age (foals), horses between one and three years of age (youngsters) and horses older than three years (adults). The veterinarians were instructed to select the herds, interview the owner and return the questionnaire before the end of April 1995. No formal procedures were possible to implement in order to secure representativeness among the participating veterinarians and herds with this design. In the repeatability study in 1997 questions on year of establishment, type and size of herd, size of area, reason for treating with anthelmintics and use of anthelmintics during the period 1993 to 1995 were included. Two additional questions on whether there had been any problems with diarrhoea in the herd and if there were any changes made in the treatment strategies were also included. A total of 66, out of the original 68 herd owners participated in the repeatability study. Furthermore, the veterinarians were interviewed in order to obtain information about the reason for selecting the horse herds to the 1995 study. The veterinarians were asked to describe their recommendations regarding endoparasite control practices and if these recommendations had altered after participating in the 1995-study. Responses were obtained from all 22 veterinarians. If the questionnaire was not correctly filled in, efforts were made to reach the herd owners by telephone in order to correct the mistakes. All responses from the repeatability study and the veterinarians were collected by telephone interviews. 3. Data analysis Bivariate analyses were performed in order to find significant differences in the data material. Chi-square analysis was used for class variables. Means and standard deviations were stated for continuous variables. Agreement between the two questionnaires was expressed as kappa-values (Fleiss, 1981). The 95% confidence intervals for the kappavalues were calculated according to Armitage and Berry (1987). When percentages of responses were calculated missing values were excluded from the denominator. 4. Results The distribution of herds, the mean number of horses and the average areas are shown in Table 1. The mean deviation in answers on the number of horses from the
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Table 1 Distribution of the 68 farms in the study with respect to herd type, the mean number of horses (mean) with the standard deviation ( SD) and the average area (in ha) with the range (min.±max.) in each herd type Herd typea
No. (%)
Mean no. of horses( SD)
Average area and range (min.±max.)
Stud-farm Pension Riding school Other typesb
36 11 14 7
27 23 39 36
12.5 10.0 10.2 8.3
(53) (16) (21) (10)
(15.0) (8.0) (15.4) (20.1)
(3.3±85.0) (4.0±16.6) (2.8±21.5) (5.0±12.0)
a
The herd types were significantly different (p0.001). The category `other types' includes three stables for trotting horses, two farms who could not be placed in just one category, one stallion station and one stable for race horses.
b
questionnaire to the repeatability study are shown in Figs. 1±3 and show that the herd owners remembered the number of foals better than the number of youngsters and adults. In Table 2 the number of annual treatments and mean number of treatments in the different age categories are listed. In 1993 and 1994 the mean number of different anthelmintic products used was 2.5 per year and in 1995 was 2.4 products.
Fig. 1. The repeatability of the questionnaires regarding the number of foals. The figure shows the distribution of deviations* in the remembrance of the numbers. (* The mean deviation and the standard deviation was 1.1 (1.6) in 1995, 1.1 (1.5) in 1994 and 1.7 (1.8) in 1993.)
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53
Fig. 2. The repeatability of the questionnaires regarding the number of youngsters. The figure shows the distribution of the deviations* in the remembrance of the numbers. (* The mean deviation and the standard deviation was 2.6 (2.9) in 1995, 2.2 (3.0) in 1994 and 1.8 (2.6) in 1993.)
Table 2 Frequency of annual anthelmintic treatments in 68 Danish horse herds Foals
Youngsters
Adults
(0±1)
(1±3)
(>3)
11
6
Treatments per year
n (%)
n (%)
n (%)
1 2 3 4 5 6 9 10 Mean number of treatments per year
2 (4) 4 (7) 7 (12) 21 (37) 13 (22) 8 (14) 1 (2) 1 (2) 4.3
2 (3) 4 (7) 11 (18) 30 (48) 7 (11) 8 (13) 0 0 4.0
2 (3) 12 (18) 10 (15) 32 (47) 5 (7) 7 (10) 0 0 3.7 ( p0.01)
Age categories (years) Missinga
a
Questionnaires with no responses.
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Fig. 3. The repeatability of the questionnaires regarding the number of adults. The figure shows the distribution of the deviations* in the remembrance of the numbers. (* The mean deviation and the standard deviation were 3.0 (3.5) in 1995, 3.4 (4.2) in 1994 and 3.9 (4.2) in 1993.)
In 1995 ivermectin was the most commonly used anthelmintic in Danish horse herds followed by the benzimidazoles and pyrantel. The same picture was seen in the previous years (Table 3). The kappa-values and the corresponding 95% confidence intervals for the remembrance of the use of the four chemical classes of anthelmintic compounds approved to treat horses in Denmark (benzimidazoles, pyrantel, ivermectin and dichlorvos), were for the year 1995: 0.54 [0.45; 0.62], for 1994: 0.60 [0.51; 0.69], and for 1993: 0.59 [0.50; 0.69]. The kappa-values for combinations of drugs were 0.28 [0.14; 0.42], 0.46 [0.31; 0.61] and 0.45 [0.30; 0.60] for the years 1995, 1994 and 1993, respectively. The most preferred drug formulation was paste (most preferred in 57 (84%) herds) and the least preferred drug formulations were mixture (least preferred in 58 (72%) herds); pellets (least preferred by 45 (66%)) and granulate (least preferred by 38 (56%)). The reasons for treating with anthelmintics were to avoid diseases/unthriftiness in 59 (87%) herds, to be safe in 11 (16%), to prevent the horses from giving low competition performances in 7 (10%) and to save feeding costs in 5 (7%) herds. The most commonly used method for body weight estimation was eye measure. It was used for foals in 46 (78%) herds, for youngsters in 51 (81%) and for adults in 56 (82%).
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Table 3 The number (and percentages) of horse farms who uses various anthelmintics during the period 1990±1995 Class n
1995
1994
1993
1992
1991
1990
66
67
65
61
55
50
2
1
3
7
13
18
Group 1 Benzimidazoles
44 (67)
47 (70)
60 (92)
47 (77)
37 (67)
34 (68)
Group 2 Pyrantel
37 (56)
40 (60)
26 (40)
22 (36)
13 (24)
9 (18)
Group 3 Ivermectin
60 (91)
63 (94)
57 (88)
54 (89)
47 (85)
41 (82)
Group 5 Dichlorvos
7 (11)
6 (9)
5 (8)
5 (8)
5 (9)
6 (12)
Other drugs Do not remember
6 (9) 0
4 (6) 0
5 (8) 0
4 (7) 1 (2)
2 (4) 2 (4)
2 (4) 4 (8)
Missing
a
n: Number of farms. a Questionnaires with no responses.
There was no significant difference in the weight estimation method between herd types. When dosing with anthelmintics, the individual weight of the horses was the most frequently used method in all age categories; for foals in 42 (72%) herds, for youngsters in 47 (76%) and for adults in 51 (75%). The different management practices in the various herd types are shown in Table 4 and it is shown that FECR-tests had been performed in 17 (25%) herds. The reason for performing this test was diarrhoea in 5 (29%), own interest in 3 (18%), and colic in 2 (12%) cases. In 40 (61%) herds problems with diarrhoea had been observed. In 21 (53%) of these cases the veterinarian was called. The duration of the diarrhoea lasted either less than a week in 16 (40%) of the cases or more than one month in 17 (43%). In 10 (25%) of the cases the herd owner did not know the causal factor for the diarrhoea and in 12 (39%) they believed that is was because they feed silage. Endoparasites were the suspected cause in 7 (18%) of the cases and in 4 (10%) of the cases the suspected cause was the fact that the horses ate sand. The most important factors in choosing an anthelmintic (Table 5) were the possibilities of direct administration, the experience of `good effect' of the anthelmintic and the veterinarian's recommendation. In Table 6 the importance of different sources of information on endoparasite control is presented. There was no significant difference between herd types in the sources of information. In 32 (47%) herds advisers were involved in planning the anthelmintic treatment strategies. The most commonly used adviser was the veterinarian (used by 31 (97%) herd
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Table 4 The use of different management practises in the different herd types Management factor
Stud farms No. (%)
Pastures are permanent Pasture rotation is used a Horses are moved to mown pastures Alternate grazing is used Horse dung is spread on pastures Performs anthelmintic treatment at turn out Performs anthelmintic treatment at pasture rotation Performs anthelmintic treatments at housing New horses are treated at introduction Visiting horses are treated Problems with diarrhoeab FECR-tests have been performed earlier Disease registration is performedc Adviser is used in the planning of anthelmintic treatment Changes in the parasite control routines are made after participating in the study
21 (62) 30 (88) 21 (64)
Pensions No. (%)
Riding schools No. (%)
Other herd types No. (%)
Total No. (%)
n
6 (55) 8 (73) 7 (70)
13 (93) 8 (73) 7 (64)
6 (86) 3 (43) 1 (17)
46 (70) 49 (78) 36 (60)
66 63 60
9 (25) 5 (16)
2 (18) 2 (20)
1 (7) 2 (14)
0 0
12 (18) 9 (14)
68 63
22 (61)
9 (82)
9 (64)
2 (29)
42 (62)
68
7 (19)
4 (36)
2 (14)
0
13 (19)
68
17 (47)
5 (45)
8 (57)
2 (29)
32 (47)
68
21 (58)
7 (64)
8 (57)
3 (43)
39 (57)
68
8 (22) 23 (72) 9 (25)
4 (36) 10 (71) 5 (45)
6 (43) 4 (44) 1 (7)
0 3 (27) 2 (29)
18 (26) 40 (61) 17 (25)
68 66 68
17 (47)
0
3 (21)
2 (29)
22 (32)
68
19 (53)
4 (36)
5 (36)
4 (57)
32 (47)
68
8 (25)
4 (29)
0
5 (45)
17 (26)
66
a
p0.05 p0.039 c p0.013 The percentages are calculated for the number of positive respondents, n is the total number of respondents. b
owners), the second mostly used were other farmers, used by 5 (16%), and agronomists were used by 4 (13%) herd owners. There was no significant difference between herd types. In 17 (26%) herds changes have been made after participating in the study. The most common changes were the dosing of anthelmintics based on individual weights (used by 14 (82%) herd owners) and changes in the conditions regarding anthelmintic treatments (regarding choice of anthelmintics etc.) in 12 (71%) herds. In 6 (35%) herds the change was to fewer annual treatments, 6 (35%) tried to limit infection and 5 (29%) improved pasture hygiene. Three (18%) herd owners performed faecal egg counts before treatment and 2 (12%) herds owners increased the number of annual treatments. There was no significant difference between herd types in the changes made.
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Table 5 The importance of various factors involved in the choice of anthelmintics on horse farms (n68) Factor
Most important n (%)
Important n (%)
Not Important n (%)
Price of the drug Can be administered in feed Directly administration Experience of `good effect' Feed mill recommended Veterinarian recommended Pharmacist recommended Commercial advertisements
8 11 52 50 0 43 0 0
23 12 12 11 5 19 5 9
37 45 4 7 63 6 63 59
(12) (16) (76) (74) (63)
(34) (18) (18) (16) (7) (28) (7) (13)
(54) (66) (6) (10) (93) (9) (93) (87)
Thirty nine (53%) herds were included in the study because the veterinarian suspected them to be problem herds or have AR in the herds. Twenty four (33%) herds were selected due to the herd size and eight (11%) herds were sampled by convenience. The last 2 (3%) herds were selected because the herd owner applied after having heard about the study. The number of farms that each veterinarian entered the study varied from one to nine. The factors that influenced the veterinarian's recommendations to the herd owners on endoparasite control were conditions of the pastures (whether there was grazing or not, whether there was pasture rotation, stocking rates etc.) for 16 (73%) veterinarians. Factors regarding the herd (grouping of horses by age, herd size, replacement of horses etc.) for 15 (67%). Nine (41%) veterinarians stated that factors regarding the health of the horses (problems with colic/diarrhoea, suspected endoparasitic problems, level of parasite infection in the herd etc.) influenced their recommendations to the herd owners. AR influenced only 3 (14%) of the veterinarians in their recommendations to the herd owners. Changes in the recommendations given to herd owners after the participation in the FECR-study were made by 13 (59%) veterinarians: all stated that they have made changes in the choice of anthelmintics and 3 stated that they paid more attention to the AR problem.
Table 6 The importance of different sources to give information about endoparasite control (n68) Source
Most important n (%)
Important n (%)
Not important n (%)
Meetings/courses Papers Agronomist Veterinarian Feed mill Pharmacist Other farmers
24 32 11 52 0 1 14
25 21 16 13 11 3 37
19 15 41 3 57 64 17
(35) (47) (16) (77) (2) (21)
(37) (31) (24) (19) (16) (4) (54)
(28) (22) (60) (4) (84) (94) (25)
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5. Discussion The fact that some herd owners did not remember the number of horses in their herd indicates that there is a frequent exchange of horses between farms which can cause the spread of AR. When the exchange rate of horses is high it becomes difficult to estimate the total number of horses in one year. It was impossible to calculate the stocking rate, because we have no information of the area that was used for pastures. Riding schools and the category `other herd types' are often big herds with a small area and therefore have a high stocking rate. The results of the questions on use of anthelmintics revealed a lack of knowledge. Sixty seven percent of the farmers used benzimidazole anthelmintics in 1995 in spite of the fact that the prevalence of AR to benzimidazoles was 78% (Craven et al., 1998). In 1996, after the AR study was finished and the farmers had received the results, 55% of the farms still used benzimidazoles. The use of ivermectin has increased to a critical level: 91% stated that they used ivermectin at least once a year in 1995. Ivermectin is, at present, the only drug with 100% effectivity against the adult cyathostomes but resistance to this drug has developed within a very short period of time in other livestock species. Ivermectin was first marketed in 1981 (Shoop et al., 1995) and resistance was detected in Haemonchus contortus in sheep in South Africa by Carmichael et al. (1987). This means that there is a potential danger of AR developing against this drug in horse parasites due to uncritical use. The fact that ivermectin is the most commonly used anthelmintic in Danish horse herds is consistent with the question on the importance of the price of the drug in which only 12% stated that the price was important to the choice of anthelmintic. If ivermectin is used in a sensible manner it is highly effective against benzimidazole resistant parasites (Herd, 1992) but if used indiscriminately without considering the possibility of development of AR, it is not likely that it will maintain its effectiveness. Eighty seven percent of the herd owners treated because they wanted to avoid unthriftiness/diseases. This means that endoparasite control is aimed as prophylaxis and not as a `treatment', after determination of EPG, as it ought to. Anthelmintics should be used strategically and the number of annual treatments should be minimized in order to extend the life span of the available anthelmintics. This means that the times of treatment should be determined according to the epidemiology of the parasite. Strategic treatment times are prior to turn out and pasture rotation (Herd, 1992) so that heavy contamination of pastures can be avoided. It is seen that foals, youngsters and adults are treated in different ways. Under estimation of body weight leads to under dosing of anthelmintics which is demonstrated to be a risk factor for the development of AR (Wescott, 1986; Waller, 1987). Therefore, it is critical that the majority of herd owners estimates the body weight by eye measure. Another factor that might lead to under dosing is the fact that the most preferred drug formulation (paste) are marketed in tubes in which the maximum treatment dose is for a horse with a weight of 500 or 600 kg and a normal riding horse does easily exceed this weight.
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Measures to prevent development of parasitism and subsequently AR are widely used: pasture rotation (78%), moving the horses to mown pastures (60%) and alternate/mixed grazing with other species (18%). Pasture rotation is an effective control strategy if it is used properly: The same pasture should only be used once in each grazing season since it is of no value to move horses back to a pasture that has already been contaminated. It should be stressed that no information whether the rotation was to a clean pasture was available. The use of measures that could reduce the infection level of the pastures revealed a lack of knowledge. The herd owners treated horses they bought more frequently than horses that were just visiting for a period (57% versus 26%). From a parasitological point of view there is no difference between introducing a horse whether it is bought or just visiting, but the herd owners seemed to regard the two things differently. This is critical because AR can be introduced in a herd with a horse harbouring anthelmintic resistant parasites. The use of treatment at turn out varied between 29% in `other herd types' to 82% in pensions and treatment at pasture rotation varied from none in `other herd types' to 36% in pensions. Treatment of new horses prior to introduction into a herd also minimises the risk of infection and the risk of spreading AR (Herd, 1992). The spread of horse manure on the pastures varied between none in the `other herd types' to 20% at the pensions. This practice constitutes a major risk of infection. The existence ± and spread ± of AR also means that more attention should be paid to other control measures than the use of anthelmintics. These are often aimed at reducing the pasture infectivity level which could have risen to a dangerous level by the end of summer or in autumn (Eysker et al., 1986). This means that much can be achieved by avoiding heavily infected pastures in the second half of the grazing season. One method to avoid the risk of massive infection in late summer/autumn is pasture rotation to safe pastures (Bjùrn et al., 1991). Another method is to reduce the relative stocking density by alternate or mixed grazing with cattle or sheep (Eysker et al., 1986). Removal of horse manure from the pastures (Herd, 1986) is yet another method of reducing the pasture infectivity level. It is of great importance that the herd is checked for AR (FECR-tests) so that only effective anthelmintics are used and unnecessary anthelmintic treatments are avoided (Herd, 1992). It is advisable to have the parasite status of the herd determined prior to anthelmintic treatment. FECR-tests were only performed in 25% of the herds. Possible reasons for performing faecal examinations could be assumed to be due to cyathostomes since unthriftiness and diarrhoea were the major reasons. Cyathostomatosis, is characterized by diarrhoea, colic, weight loss, delayed shedding of the winter coat, edema and unthriftiness (DiPietro et al., 1990; Kelly and Fogarty, 1993; Reid et al., 1995) and is thought to be associated with the synchronous emergence of L4 larvae from tissue cysts, often during the winter and spring (Uhlinger, 1991: Reid et al., 1995). This study revealed that 61% of the herds have experienced problems with diarrhoea. In a study of reasons for diarrhoea in horses Love et al. (1992) found cyathostomatosis in 27% of the cases and another 27% remained undiagnosed. In this study, herd owners suspected parasites in 18% of the cases and the reason was unknown in 25%. The most common duration of diarrhoea were less than a week (40%) or longer than one month (43%). This is consistent with the reports on
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cyathostomatosis in which the durations are approximately a week (Kelly and Fogarty, 1993; Reilly et al., 1993; Mair, 1994) or more than a month (Church et al., 1986; Kelly and Fogarty, 1993). In this study the frequency of diarrhoea ± and of AR ± might be overestimated due to a selection bias as a result of the fact that 53% of the farms actually were selected due to suspected problems with parasites or AR. The cases of diarrhoea were more frequent in stud-farms and pensions than in the other herd types. In stud-farms a positive information bias might be part to the explanation due to more frequent disease registration (47% performed disease registration) or a higher number of young horses. The lack of remembrance is probably due to the fact that only 32% of the herd owners perform disease and treatment registration. The lack of registration is a risk factor for the development of AR, because specific control strategies are essential in order to recall the used products and time of administration. It will be almost impossible to make control strategies to prevent the development of AR and be certain that they will be followed by the herd owners which is important if the control programmes should be effective (DiPietro, 1992). In 97% of the herds using advisers, the veterinarians were involved in the planning of endoparasite control strategies. Seventy seven percent of herd owners stated that the veterinarian was the most important source of information on endoparasite control and 63% followed the veterinarians' recommendation of the choice of anthelmintics. Therefore it must be assumed that the veterinarian is the most important source of information on endoparasite control, but this might be overestimated due to the selection procedure. The recommendations to herd owners varied greatly and only 14% of the veterinarians stated that the AR problem had influenced their advice. Fifty nine percent of the veterinarians have changed their recommendations after participating in the AR-study. The most frequent change is that they no longer recommend benzimidazole in favour of ivermectin, a recommendation that includes a rising risk of AR to ivermectin. One of the major reasons for choosing an anthelmintic is the experience of `good effect' of the anthelmintic. The only possible method of determining whether the effect of an anthelmintic is satisfactory is by performing FECR-tests. This was only done in 25% of the herds. It is difficult to say whether there is a difference in the risk of AR between herd types because of the small sample size of both this questionnaire study and the AR study (Craven et al., 1998), but the categories `other herd types' and riding schools revealed greater number of AR than stud-farms and pensions, probably because of the relatively high stocking rate. AR towards benzimidazoles was present in all the examined herds from the category `other herd types' and resistance against both pyrantel and the benzimidazoles was found in riding schools. It should be stressed that the study is too small to detect statistical differences. The repeatability in this study was relatively low compared to other studies (Slater et al., 1992; Dangolla, 1994; Scholl et al., 1994 and Maingi et al., 1996b). The kappa-values on the remembrance of drug classes were fair but lower than in the studies mentioned above. The fact that the kappa-value is lower for the year 1995 than for the two previous years reflects that the herd owners did not plan the anthelmintic treatments and were only stating ideas for 1995 when the interview took place. It is expected that the kappa-value is
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lower in 1993 than in 1994. The kappa-values for drug combinations were low in all three years. The conclusion to this is that the herd owners remember some of the drugs they have used but not the combinations. This is probably due to the fact that the herd owners used an average of 2.4 different anthelmintic products annually which makes it difficult to remember. Twenty six percent of the herd owners had made changes after participating in the ARstudy. The changes were without strategy which is not good when trying to avoid increasing AR. Most of the changes were to not use benzimidazoles any more, only few have made alternative prophylactic arrangements, like more pasture rotation etc. The main conclusion of this study is that there is a massive lack of exact knowledge among herd owners about how to control endoparasites and avoid development of AR. This is consistent with the findings from other studies among owners of sheep and goat farms in Denmark (Maingi et al., 1996a). A concerted effort has to be made to inform the farmers about the importance of carefully planned control strategies against endoparasites so the increasing development of AR can be stopped. The sources of knowledge about the control of endoparasites were evaluated by the herd owners and it became clear that the veterinarian, meetings and articles were the most important ones. This means that these sources would be appropriate channels for future communication. It is of particular importance to make the veterinarians aware of the AR problem and to inform them about the appropriate endoparasite control strategies since they are the most important source of information to the herd owners and since their present guidelines to herd owners are not at all clear. Information directly to farmers in magazines is feasible but in-service training of veterinarians must have a top priority. Acknowledgements This study was supported by Merial (formerly MSD-AgVet.), Copenhagen, Denmark. We would also like to thank the veterinarians for providing the link between us and the herd owners. Thanks also to the herd owners for taking the time to answer the questionnaire. References Armitage, B., Berry, G., 1987. Statistical Methods in Medical Research, 2nd ed. Blackwell Scientific Publication, pp. 100±104. Bjùrn, H., Sommer, C., Schougaard, H., Henriksen, Sv.Aa., Nansen, P., 1991. Resistance to benzimidazole anthelmintics in small strongyles (Cyathostominae) of horses in Denmark. Acta. Vet. Scand. 32, 253±260. Brunsdon, R.V., Kissling, R., Hosking, B.C., 1983. A survey of anthelmintic usage for sheep: a time for change? N.Z. Vet. J. 31, 24±29. Carmichael, T., Visser, R., Schneider, D., Soll, M., 1987. Haemonchus contortus resistance to ivermectin. J. S. Afr. Vet. Ass. 58, 93. Church, S., Kelly, D.F., Obwolo, M.J., 1986. Diagnosis and successful treatment of diarrhoea in horses caused by immature small strongyles apparently insusceptible to anthelmintics. Equine Vet. J. 18(4), 401±403.
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