Accepted Manuscript

Effects of Ivermectin and Moxidectin on Fecal Egg Count and Egg Reappearance
Rate in Horses

C. A. Shea Porr, Ph.D., Victoria F. Hedinger, undergraduate, Lauren R. Hamm,

undergraduate, Morgan M. Ernst, undergraduate, Barbie M. Papajeski, M.S., Michelle
L. Santiago, Ph.D., Amanda J. Davis, Ph.D.
PII: S0737-0806(17)30118-1
DOI: 10.1016/j.jevs.2017.06.011
Reference: YJEVS 2345

To appear in: Journal of Equine Veterinary Science

Received Date: 15 March 2017

Revised Date: 28 June 2017
Accepted Date: 30 June 2017

Please cite this article as: Porr CAS, Hedinger VF, Hamm LR, Ernst MM, Papajeski BM, Santiago ML,
Davis AJ, Effects of Ivermectin and Moxidectin on Fecal Egg Count and Egg Reappearance Rate in
Horses, Journal of Equine Veterinary Science (2017), doi: 10.1016/j.jevs.2017.06.011.

This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to
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 ACCEPTED MANUSCRIPT

1 Effects of Ivermectin and Moxidectin on Fecal Egg Count and Egg Reappearance Rate in Horses

2 C. A. Shea Porr, Ph.D., cporr@murraystate.edu, corresponding author

3 Victoria F. Hedinger, undergraduate

4 Lauren R. Hamm, undergraduate

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5 Morgan M. Ernst, undergraduate

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6 Barbie M. Papajeski, M.S., bpapajeski@murraystate.edu

7 Michelle L. Santiago, Ph.D., msantiago1@murraystate.edu

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8 Amanda J. Davis, Ph.D., adavis53@murraystate.edu

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Murray State University, 101 Equine Instructional Facility, Murray, KY, 42071, USA
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13 Abstract

14 Parasite resistance to some commonly used anthelmintics is increasing and egg reappearance

15 period (ERP) appears to be decreasing. The objective of this project was to evaluate the efficacy

16 of ivermectin (IVE) and moxidectin (MOX) on fecal egg counts (FEC) and ERP in horses. Fecal

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17 samples (n=46) were collected and evaluated for parasite eggs using the Modified McMaster

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18 Fecal Egg Count technique. Eggs per gram of feces (EPG) were recorded. Horses were randomly

19 allocated based on pre-study FEC (low, <200 EPG; moderate, 200-500 EPG; high, >500 EPG),

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20 age (young, ≤15 yr; old, ≥16 yr), and housing (stall or pasture). Treatments included control

21 (CON, no treatment, n=10), IVE (n=10), or MOX (n=10). Fecal samples were collected and

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evaluated every 2 wk for 12 wk after treatment. Statistical analysis was performed using PROC
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23 MIXED of SAS. Fixed effects included treatment, age, and location with week as a repeated

24 measure. Fecal egg count reduction tests were 100% for IVE and MOX, indicating that both
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25 anthelmintics were effective. However, parasite eggs began to appear in IVE horses in wk 6 and
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26 MOX horses in wk 8. Currently reported ERP for IVE and MOX are 6-8 wk and 10-12 wk,
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27 respectively, suggesting decreased efficacy of MOX. In pastured horses, MOX was more

28 effective in reducing FEC than IVE (1.84 versus 6.43 EPG, respectively; P=0.01). Data suggests
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29 that anthelmintic use improved internal parasite control and that MOX may have greater efficacy

30 than IVE, however the shorter ERP for MOX may indicate that MOX efficacy may be
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31 decreasing.
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33 Keywords: Equine, Ivermectin, Moxidectin, Egg Reappearance Period

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36 1. Introduction

37 Internal parasites are a common health concern for many livestock species, including equines.

38 Common species of concern include strongylidae (strongyles), nematode (roundworms), and

39 cestodes (tapeworms). Parasite infestation can have a negative effect on horses’ health, including

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40 weight loss, intestinal ulcers, and higher incidence of colic [1]. Anthelmintics are the primary

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41 means of controlling internal parasites in horses, and their use can have beneficial effects on

42 growth and performance of horses [2]. However, overuse has resulted in development of parasite

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43 resistance to some anthelmintics [3, 4, 5]. Commonly used and currently available drug

44 classifications of dewormers used for equines include benzimidazoles, pyrimidines, praziquantel,

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and macrocyclic lactones [6]. Ivermectin (IVE) and moxidectin (MOX) are commonly used
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46 macrocyclic lactones. Macrocyclic lactones disturb nervous transmission in nematodes, resulting

47 in paralysis and death [6].

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49 There are two factors that should be considered when attempting to evaluate anthelmintic
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50 efficacy: fecal egg count reduction (FECR) and egg reappearance period (ERP). The FECR test

51 calculates the percentage reduction in fecal egg count (FEC) before treatment and 2 weeks’ post-
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52 treatment. Resistance would be concluded if reductions were less than 95% for IVE or MOX,

53 [6], but this has not been documented in the United States. The ERP measures the time interval
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54 between treatment and the resumption of eggs appearing in fecal samples. Shortened ERP is
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55 considered a precursor to resistance. When the products were released, ERP was 9-13 weeks for

56 IVE (released in the early 1980’s) and 16-22 weeks for MOX (released in the late 1990’s).

57 Current reported ERP for IVE and MOX are 6-8 weeks and 10-12 weeks, respectively [6].

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59 Several reviews of parasite management have been published [6, 7, 8]. Specific research has

60 shown that benzimidazoles and pyrimidines, much older dewormers, have repeatedly been

61 shown to be ineffective against equine parasites [4, 5]. Also, likely due to use on farms with high

62 treatment intensities (deworming every 8 wk), parasites appear to have built up resistance to IVE

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63 and MOX in various locations around the world [9, 10, 11, 12]. When horses that had been

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64 regularly dewormed with IVE were administered MOX, parasites exhibited some resistance to

65 both IVE and MOX [13], possibly due to the similar chemical makeup of IVE and MOX. Within

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66 the U.S., one study reported an ERP of 15–24 weeks in horses in Alabama dewormed with MOX

67 [14]. However, research in central Kentucky has shown a shortening ERP for horses treated with

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IVE or MOX [10, 15, 16], with eggs reappearing within 4 weeks of treatment.
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70 Horses at Murray State University are not under high treatment intensity, and no resistance was
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71 detected in a pilot study [17]. However, given the shortening ERP for horses in central Kentucky,
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72 an evaluation of the Murray State University equitation herd was conducted. Management
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73 changes could be enacted should a shortened ERP be detected. Based on a review of the

74 literature, the hypothesis was that both IVE and MOX would show a shortened ERP, with IVE
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75 having a shorter ERP than MOX.

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77 2. Materials and Methods

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78 This research was approved through Murray State University’s Institutional Animal Care and

79 Use Committee.

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81 2.1 Horse Population

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82 University-owned horses were used as subject animals. All had been owned for a minimum of

83 one year prior to the study. Nine horses were housed in stalls, 14 were housed on pasture, and

84 seven spent time in both a stall and on pasture. Horses ranged in age from 5-25 years. Animals

85 15 years and younger were grouped as “young”, while horses 16 years and older were grouped as

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86 “old”. There were four mares and 26 geldings, and all animals were predominantly stock-type or

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87 other light horse breeds.

88

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89 2.2 Sample Collection and Evaluation

90 Fresh fecal samples were collected from 46 horses that had not been dewormed in at least 6

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months. All samples were collected within a 3-day window each sampling period. Horses were
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92 confined to stalls or round pens or were tied to a rail and observed until they defecated. As soon

93 as horses defecated, several fecal balls were gathered from several places in the pile. These were
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94 placed in plastic Ziploc bags, labeled with the date and horse’s name, and stored in a refrigerator
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95 at 4 C [18]. Samples were analyzed within 1 week of collection using the Modified McMaster's
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96 Fecal Egg Counting technique. This procedure has a sensitivity of 25 eggs per gram (EPG) of

97 feces. Fecal samples were thoroughly mixed in the collection bag before 4 grams were removed
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98 for testing. The subsample was thoroughly mixed in 26 ml of floatation medium before being

99 strained into a separate test tube. Strained samples were then mixed again before being pipetted
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100 onto the McMaster slide chambers. Slides were allowed to sit for 3 minutes before being read on
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101 a microscope. Eggs within the two marked chambers were counted, and that number was

102 multiplied by 25 to get a result in EPG. At least two repetitions were conducted on each fecal

103 sample to ensure an accurate parasite egg count. Strongyle eggs were the predominant parasite

104 egg identified and were the only ones counted and included for statistical analysis.

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106 2.3 Treatment Groups

107 Pre-treatment fecal exam results revealed that 11 horses (23.4%) were high shedders (>500

108 EPG), five horses (10.9%) were moderate shedders (200 – 500 EPG), and the remaining 30

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109 horses (65.2%) were low shedders (0 – 200 EPG). Horses were randomly allocated to treatment

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110 based on pre-treatment parasite load, age, and housing location with 10 horses per treatment.

111 Control horses (CON) received no anthelmintic treatment. Treated horses were dewormed with

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112 ivermectin (IVE) (oral paste, Zimecterin Gold, Merial Limited, Duluth, GA, United States) or

113 moxidectin (MOX) (oral gel, Quest Plus, Zoetis, Kalamazoo, MI, United States) based on

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manufacturer recommendations. Horses were weighed on a portable equine scale (Jack Mann
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115 Scales, Inc., KY, United States) before being dosed. Fecal samples were collected every 2 weeks

116 until 12 weeks’ post-treatment and were handled and evaluated as described previously.
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118 2.4 Statistical Analysis

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119 Statistical analysis was performed using SAS (SAS Inst. Inc., Cary, NC). Horses were

120 considered as the experimental units with week as a repeated measure. The PROC MIXED
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121 procedure was used for determining effects of anthelmintic treatment on fecal egg counts. Fixed
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122 effects included treatment, age category, and housing location. All possible interactions were
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123 evaluated and reduced to include interactions between treatment and week of collection, and

124 treatment and location. Two preplanned orthogonal contrasts were used to determine effects and

125 included comparisons between: 1) CON vs treated (IVE and MOX) horses and 2) IVE vs MOX

126 horses. Fecal egg count data, represented as eggs/gram, was log transformed to the log10(X+1)

127 with geometric means reported.

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128

129 3. Results and Discussion

130 The FECRT was 100% for both IVE and MOX treatments. This shows that IVE and MOX were

131 effective against strongyles. While there is evidence of parasite resistance, defined as an FECRT

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132 of less than 95% for macrocyclic lactones, to anthelmintics in many countries [9, 10, 11], it has

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133 not been shown in the United States. That being said, several studies have noted decreased ERP

134 in the United States when IVE and MOX were used [10, 15, 16]. Reported ERP for IVE and

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135 MOX are 6 to 8 weeks and 10 to 12 weeks, respectively [6]. In this study, eggs began to appear

136 in IVE treated horses in week 6 and in MOX treated horses in week 8. This suggests a decreased

137 efficacy of MOX in this group of horses.

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139 Contrast statements indicated that FEC differed in CON versus horses treated with either

140 anthelmintic (31.70 versus 2.4 EPG, respectively; P = 0.052). However, no differences were
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141 found between IVE and MOX treated horses (2.96 versus 1.84 EPG, respectively; P = 0.2705).
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142 The initial model included fixed effects of treatment, age category, and location with week as a

143 repeated measure. The model was reduced and refit to include the main effects of treatment and
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144 location and two-way interactions between treatment with week and location. A treatment by
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145 week interaction was found for FEC (Table 1). The greatest number of strongyle EPG were
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146 observed in CON horses and differed from IVE and MOX treated horses from weeks 2 to 8 (P ≤

147 0.02). However, no differences were observed between IVE and MOX treated horses during this

148 time (P = 0.16). This is not surprising as both IVE and MOX are macrocyclic lactones. It would

149 be expected for them to promote a similar response in FEC. During week 10, no differences were

150 found between any of the treatment groups (P ≥ 0.22). Curiously, FEC in CON horses were

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151 numerically lower than any other period for this group but were not substantially different for

152 IVE nor MOX treated horses (19.18, 13.48, and 6.43 EPG, respectively; P ≥ 0.22). During week

153 12, CON horses differed from MOX treated horses (29.19 versus 3.36 EPG, respectively; P =

154 0.02) but were similar to IVE treated horses (14.8 EPG; P = 0.47). Although EPG’s were

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155 numerically different between IVE and MOX treatments in weeks 10 and 12, no significant

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156 differences were found (P = 0.12). This implies a continued suppression of egg production by

157 parasites in horses in both treatment groups.

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158

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159 Table 1. Effects of anthelmintic treatment on average EPG within week.
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Week CON IVE MOX P-Value
a b
2 43.65 0.63 1.00b <0.00
4 29.61a 0.63b 1.00b <0.00
6 26.76a 1.37b 1.00b <0.00
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a b b
8 52.35 6.30 1.78 <0.02
10 19.18a 13.48a 6.43a >0.22
12 29.19a 14.8a,b 3.36b =0.02
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160 Values reported as geometric means.

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161 Different letters within the same row differ, P ≤ 0.05

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163 Housing can also impact equine exposure to parasites. Horses maintained on pasture have

164 exposure rates related to stocking density. Grazing horses will often select the same areas to
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165 graze while allowing other areas to over-grow. This can be due to the use of certain areas as
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166 places for urination and defecation, or may simply be due to the palatability of forages in the

167 field. Also, horses have been shown to graze shorter patches of forage greater than 1 meter from

168 feces, where risk of infection is lower [19]. If stocking rates are high, pastures may become

169 overgrazed and horses may be forced to eat in areas they would normally avoid, increasing their

170 exposure to parasites. Rotational grazing allows for movement of horses to more lush pasture

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171 and may decrease equine exposure to parasites. Horses housed in stalls are in close proximity to

172 manure where eggs are shed. However, these horses are often turned out daily for exercise and to

173 allow stalls to be cleaned. This may limit exposure to fecal parasites. Decisions on housing were

174 made based on individual horse and program needs. Stalled horses were turned out daily for

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175 exercise and stalls were cleaned during that time. Pastured horses were rotated regularly and

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176 stocking rates were moderate. An interaction was found between treatment and location (P =

177 0.01). For stalled horses, CON horses differed from horses treated with either IVE or MOX

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178 (9.04, 1.83, 1.37 EPG, respectively; P ≤ 0.01) but no differences were found between IVE and

179 MOX treated horses (P = 0.69). Location was considered “pasture” for any horses that either

180
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remained on pasture full or part time during the study. In pastured horses, MOX treatment was
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181 more effective in reducing strongyle EPG compared to IVE treatment (1.84 versus 6.43 EPG,

182 respectively; P = 0.01). However, both anthelmintics proved to be effective in reducing FEC
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183 compared to CON (111.07 EPG; P < 0.00). In CON and IVE horses, FEC were lower for stalled
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184 animals compared with pastured horses (P ≤ 0.03). There was no difference for MOX treated
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185 horses (P = 0.99). It may be important to note that some stalled horses had access to pasture the

186 previous summer (n=2, mid-May to mid-August), potentially increasing their exposure to
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187 parasites that may have been dormant during the winter months. The increase in FEC in CON

188 horses wk 2 primarily resulted from increases in pastured animals. Four of the five stalled horses
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189 showed 0 EPG during both the pre- and wk 2 collections, while only one of the pastured horses
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190 showed the same result. Even though stalled horses had lower FEC than pastured horses, values

191 reported here placed the majority of animals in the low shedding category, suggesting that

192 changes in management are not required.

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194 Research has shown that younger horses are more prone to parasite infestation in relation to

195 mature horses. Horses between 2 and 5 years of age had higher FEC than adults, and there was a

196 trend for geriatric horses to have higher FEC than mature horses [20]. In this study, horses

197 ranged from 5 to 25 years of age. Horses were grouped into two age categories for statistical

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198 evaluation; however, there was no effect of age so it was dropped from the model.

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199

200 Another factor that may have had an impact on FEC is time of year. Small strongyles tend to

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201 emerge in the spring to mature and lay eggs [21], and previous research has reported FEC to be

202 lowest in February, increase until May, and then remain high until September before declining

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[20]. While ERP is typically about 8 wk, it can occur more quickly in warmer weather,
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204 particularly when concurrent with high humidity [22]. In addition, higher FEC have been

205 reported during warm, wet climate conditions [20]. Egg development may slow or stop once
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206 temperatures are below 7° C or above 32° C. It takes only days for eggs to develop under optimal
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207 conditions but may take weeks or months under suboptimal ones. Weekly environmental
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208 temperatures during the study period (March to May) ranged from 11° C to 22° C. This is in the

209 optimal temperature range for egg development.

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211 Horses at Murray State University have typically been dewormed twice annually, once each in
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212 the spring and fall. Drug classifications are rotated between macrocyclic lactones and other drug
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213 categories. While FEC are calculated by students in several courses throughout the year, they are

214 not calculated for every horse and the values are not consistently used to determine which horses

215 are in need of deworming. This is partly due to the educational component of the program.

216 Students in pre-veterinary, veterinary technician, and equine programs gain hands-on experience

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217 by assisting with the health care needs of the University herd. These courses do not always occur

218 at the same time of year and are not always organized relative to past fecal collections or

219 dewormings. It is possible that rotation of anthelmintics, even in non-intensive program such as

220 the one used at Murray State University, may contribute to the decreased ERP seen for MOX. It

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221 may be appropriate to revise the teaching protocols to allow students to gain experience dosing

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222 horses by using water as a placebo rather than having them actually administer an anthelmintic to

223 the animals unless that animal is truly in need of deworming. This could include horses with

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224 higher FEC [23], allowing for targeted deworming in the application of anthelmintics and still

225 giving students hands-on experience. That being said, strategic or targeted deworming alone may

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not be effective in managing parasites. Targeted deworming is the process of administering
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227 anthelmintics to horses based on FEC results. Typically, animals are dewormed if FEC are above

228 200 to 300 EPG [23]. Recent research has shown that grazing horses that have been dewormed
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229 with those that have not may increase the risk of reinfection of the treated horses [24] and that
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230 horses that were selectively dewormed based on FEC had a higher incidence of parasitism than
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231 those dewormed without performing FEC [25]. This suggests that targeted deworming may be

232 appropriate for most horses, but it may still be appropriate to deworm even horses with lower
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233 FEC.

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235 4. Conclusions
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236 Data suggests that increased internal parasite control can be achieved through the use of

237 anthelmintics in horses participating in non-intensive programs and that MOX may provide

238 increased efficacy in equine compared to IVE treatment. That being said, decreased ERP for

239 MOX treated horses suggests that the efficacy of MOX may be decreasing. Modifying current

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240 practices to include more frequent and comprehensive FEC on all horses and then selectively

241 deworming those who require it while using water to simulate deworming for student practice in

242 those animals that do not may enhance the efficacy of the anthelmintics being used. Combining

243 FEC results and pasture management strategies may also improve parasite management in this

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244 herd of horses.

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245

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246 Acknowledgements: Thanks go to MWI Animal Health for their support on this project.

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248 Funding: This work was supported by Murray State University’s Office of Undergraduate
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249 Research and Scholarly Activity.

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