Strongylids in domestic horses: Influence of horse age, breed and deworming programs on the strongyle parasite community

doi:10.1016/j.vetpar.2016.07.024

Veterinary Parasitology

Volume 227, 30 August 2016, Pages 56-63

https://doi.org/10.1016/j.vetpar.2016.07.024 Get rights and content

Highlights

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Analysis of the relationships in horse infection with strongylids and horse age, breeds and different management strategies was performed.
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The effect of horse age on strongyle egg shedding (EPG) in horses was near the limit of significance.
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33 strongylid species were collected; a correlation between the prevalence and proportion of species in the strongylid community was observed.
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The highest number of species (32) was found in young horses (1.5–4 years old); the lowest (17) – in old horses (>16 years).
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Frequency of treatments was found to affect infections on the community structure much more than age and breed.

Abstract

An extensive analysis of the relationships between strongylid egg shedding in domestic horses and the strongylid community structure in regard to the age of the horses, their breeds and different strategies of horse management, particularly with anthelmintic treatment programs was performed. Domestic horses (n = 197) of different ages (5 months to 22 years) and of various breeds from 15 farms with different types of deworming programs were included in this study. Strongylids (totally, 82,767 specimens) were collected in vivo after deworming of the horses with the macrocyclic lactone anthelmintic (“Univerm”, 0.2% aversectin C), and identified to the species level. Models of multiple regressions with dummy variables were used to estimate the effects of age, breed, type of farm and deworming programs on number of eggs shed per gram of feces (EPG value) and the strongylid community.

Totally, 33 strongylid species were collected (8 species of Strongylinae and 25 – of Cyathostominae); a significant correlation (r = 0.67; p < 0.001) between the prevalence and proportion of species in the strongylid community was observed. The highest number of species (32) was found in young horses (1.5–4 years old); the lowest (17) – in old horses (>16 years). Foals (<1 year old) had significantly higher EPG value than older horses. The linear regression models of the strongyle egg counts (EPG) with three predictors: horse age (AGE), number of strongylids (SN), and type of farm (FARM) revealed significant effects of SN and FARM, but an effect of AGE was near the limit of significance. Horses from farms with rare or no anthelmintic treatments (type A) shed significantly more strongyle eggs than horses from farms with regular treatments; frequency of dewormings – 1–2 (type B) or 3–4 and more times per year (type C) did not have a significant impact on the EPG value. Thoroughbreds, Ukrainian Saddlers and Russian Racers had much higher EPG values comparing to non-breed horses.

Analysis of the relation of age of the horses and structure of the strongylid communities revealed that foals (<1 year old) and old horses (>16 years old) were significantly less infected by large strongyles as compared to other horses. Species from the genus Triodontophorus and Strongylus vulgaris infected foals and young horses; whereas S. edentatus and S. equinus were registered in horses >1.5 years old. Differences in proportions of separate strongylid species in the community related to age were insignificant (p > 0.05). Frequency of anthelmintic treatments was found to affect horses infections with strongylids and strongylid community structure much more than intrinsic factors such as age and breed.

Introduction

Nematodes from the order Strongylida, especially small strongyles or cyathostomins, are considered as the predominate and most pathogenic group of horse parasites worldwide (Herd, 1990, Love et al., 1999, Lyons et al., 1999, Lyons et al., 2001, Kaplan, 2002, Matthews et al., 2004, Matthews, 2008, Corning, 2009). These nematodes parasitize wild and domestic equids and cause severe health problems, decreasing productivity and breeding qualities of horses (Owen and Slocombe, 1985, Dvojnos and Kharchenko, 1994, Gawor, 1995, Love et al., 1999). Rapid development of anthelmintic resistance in nematodes of horses and other farm animals requires new approaches to traditional methods of parasite control (Kaplan, 2002, Osterman Lind et al., 2005, Matthews, 2008, Kaplan and Nielsen, 2010, Nielsen et al., 2014).

Of 65 known species of strongylid nematodes (family Strongylidae), more than 40 have been registered in domestic horses (Dvojnos and Kharchenko, 1994, Lichtenfels et al., 2008, Kuzmina et al., 2011). Simultaneous parasitizing of multiple strongylid species in each horse complicates the diagnostics of the infection levels as well as conducting of the tests on anthelmintic resistance such as the egg hatch test (EHT), larval development assay (LDA) or larval migration inhibition assay (LMIA) (McArthur et al., 2015). From 10 to 12 of the most abundant cyathostomins (subfamily Cyathostominae) species were reported to form the core of the strongylid communities in domestic horses all over the world (Ogbourne, 1976, Reinemeyer et al., 1984, Mfitilodze and Hutchinson, 1985, Dvojnos and Kharchenko, 1994, Gawor, 1995, Bucknell et al., 1996, Silva et al., 1999, Collobert-Laugier et al., 2002, Kuzmina et al., 2005, Tolliver et al., 2015). These species were also found to be resistant to benzimidazole anthelmintics (Eysker et al., 1988, Osterman Lind et al., 2007, Kuzmina and Kharchenko, 2008). Rarer species with low prevalence and intensity are rapidly eliminated from the strongylid community after regular deworming, that significantly decreases the species diversity in domestic horses as compared to wild ones (Dvojnos and Kharchenko, 1994, Kuzmina and Kharchenko, 2008, Kuzmina et al., 2011), and, probably, increases the pathogenic effect of the parasites on the host (Petney and Andrews, 1998).

Effective strategies of horse strongylid control have to consider many factors such as types of farms and horse management, as well as the peculiarities of strongylid communities in horses of different ages and breeds. Formation of the strongylid communities in horses of different ages has been studied in different countries in a small number of animals (Russell, 1948, Todd et al., 1950, Round, 1969, Lyons et al., 2011). Sparse data on the presence or absence of infections with intestinal parasites in regard to the breeds and ages of horses were also reported by various authors (Francisco et al., 2009, Kornaś et al., 2010, Saeed et al., 2010, Slivinska et al., 2016). However, since the traditional parasitological method of necropsy do not allow collecting helminths from a sufficient number of horses of different age groups, especially of valuable brood horses, the age-related alterations in the species diversity in the strongylid community remain unexplored. Application of the in vivo method of intestinal helminth collection after deworming (Kuzmina et al., 2005, Kuzmina et al., 2007) allowed us to collect more than 80,000 strongylids from almost two hundred domestic horses of different age, including brood horses, for an extensive parasitological analysis. The main goal of this analysis was to explore the relations in strongyle egg shedding in domestic horses and species diversity in the strongylid community associated with age and type of horse management, particularly with anthelmintic treatment programs. An analysis of the relationship between horse breeds and the strongylid communities was also performed.

Section snippets

Materials and methods

The study was carried out between 2004 and 2012, on 197 domestic horses (Equus caballus L.) of different ages (5 months to 22 years) from 15 horse farms throughout different regions of Ukraine (Table 1). All horses included in this study were kept under stable–pasture or stable–paddock conditions. They were kept in individual stables at night and had access to grazing on permanent pastures or paddocks for 6–14 h per day depends on season. To investigate the influence of horse management (type of

Results

All horses included in the study were infected with strongylids; from 25 to 3275 EPG was registered in horses from different farms (Table 1). The foals up to 1 year old shed significantly higher number of strongylid eggs than older horses (Kruskal–Wallis test, p <0.05) (Table 2). Strongylid eggs were not found in samples collected from the horses on the 14th day after treatment; thus we concluded that all lumenal stages of strongylids were expulsed from the intestines.

Totally, 82,767 specimens of

Discussion

This study highlights the role of internal and external factors that contribute to the biodiversity and structure of the strongylid community in domestic horses. Studies conducted in various countries have shown that up to 20 or more strongylid species can simultaneously parasitize an individual horse (Reinemeyer et al., 1984, Ogbourne, 1976; Mfitilodze and Hutchinson, 1990, Dvojnos and Kharchenko, 1994, Gawor, 1995, Bucknell et al., 1995, Bucknell et al., 1996, Silva et al., 1999, Lyons et

Conflict of interest

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Acknowledgments

The authors thank Dr. Yuriy Kuzmin from the I. I. Schmalhausen Institute of Zoology of the NAS of Ukraine and Prof. Terry R. Spraker from the Colorado State University, USA, for their comments and corrections to the manuscript.

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Research paperStrongylids in domestic horses: Influence of horse age, breed and deworming programs on the strongyle parasite community

Highlights

Abstract

Introduction

Section snippets

Materials and methods

Results

Discussion

Conflict of interest

Acknowledgments

Vet. Parasitol.

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Aust. Int. J. Parasitol.

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Int. J. Parasitol.

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J. Comp. Pathol.

Vet. Parasitol.

Vet. Parasitol.

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Research paper
Strongylids in domestic horses: Influence of horse age, breed and deworming programs on the strongyle parasite community