Total prevalence of helminthoses (77.19%) detected in horses in this study is in concordance with the results of Mehfooz et al (2008) − 75% and Singh et al (2012) − 75.73%, and higher than the results obtained by Saeed et al (2010) − 65.51%, Matto et al. (2015) − 38.79%, Yadav et al. (2014) − 59.25% and Khan et al. (2020) − 43.33%.
Strongylid monoinfections were detected in 64.05% examined horses, while coinfection with P. equorum, Anoplocephala spp. and O. equi was detected in 7.12% animals. The highest prevalence of strongylidosis was detected in free-ranging horses younger than three years, during summer and autumn. Monoinfections were the most prevalent in Šumadija and West Serbia region (74.71%), while coinfection by P. equorum was dominant in South and East Serbia region (8.41%).
The prevalence of strongylidosis is in concordance with studies in other countries such as Strongylus spp. 77.10% in Turkey (Umur and Aҁici 2009), S. vulgaris 64% in Denmark - (Nielsen et al. 2012), large strongylids 62% in Island (Eydal and Gunnarasson 1994) and 61% in Sweden (Tydén et al. 2019). Lower prevalences were detected in Brazil – 40% (Teixeira et al. 2014), India – 25% (Yadav et al. 2014) and Pakistan – 17.95% (Khan et al. 2020).
During the whole period and all the seasons in this study (2017 and 2018) low intensity infections caused by strongylids were diagnosed constantly in large number of horses (38.69%). These infections were the most prevalent in male stable horses in Belgrade region, during spring season. This finding suggests that subclinical strongylidosis is continuously present in the epizootiological area of Serbia. The disease is usually asymptomatic and neglected by horse owners which cause indirect effect in infected animals (behavioral changes, lower fertility, low physical condition and reduction of working ability, reduction of resistance and higher susceptibility to infections of other etiology). Therefore, from the economic aspect and the aspect of animal welfare, timely diagnosis and proper therapy of the disease is very important in horse husbandry.
Strongylus vulgaris can cause blood clots and clogging of arteries and arterioles of the intestine, causing ischemia of intestine and septic peritonitis (Pihl et al. 2018). Small strongylids can cause larval cyathosomosis in young animals, followed by serious inflammatory reaction in colon and cecum, which may cause fatal diarrhea (Lyons et al. 2000). Very complex etiopathogenesis and problems with diagnostic, therapy and control make this parasitosis a constant challenge for parasitologists and causes serious problems for field veterinarians and horse owners.
P. equorum was diagnosed as monoinfection (2.37%) and coinfection with strongylids (6.20%) and the highest prevalence was detected in horses younger than three years (16.98%) during autumn. Monoinfections were the most prevalent in stable horses (3.48%) in Vojvodina region (3.02%), while coinfections were dominant in free-ranging horses (20.69%) in South and East Serbia regions (8.41%). Low intensity infections (in horses younger than three years in winter) and medium intensity infections (in free-ranging horses) prevailed.
Two decades ago, there were no detailed studies or available data regarding the prevalence and intensity of infection by this ascarid in horses in Europe. The prevalence of 41.3% was detected in Lithuania (Kazlauskas, 1958) and in Belgium only 5.33% (Pecheur et al. 1979). Studies in Poland have shown that 26% of horses was infected with maximum number of 142 parasite per animal (Gawor 1995), and in Germany in 56% positive horses maximum seven nematodes per animal (Cirak et al. 1996). Borgsteede and Beek (1998) detected P. equorum in 28.6% in Netherlands with maximum parasite burden of 308 per animal.
In France, Laugier et al. (2012) detected higher prevalence of parascariosis in foals 3–4 months old, compared to foals 8–9 months old. P. equorum was found with a prevalence of 22% in horses younger than three years in Spain (Francisco et al. 2009), in 225 foals and 6% of yearlings in Germany (Hinney et al. 2011), 22% of foals 10–223 days old in central Kentucky (Lyons et al. 1981), in 27.4% primitive horses younger than three years in Poland (Slivinska et al. 2016), in 90% foals in Island (Eydal and Gunnarasson, 1994). Parascariosis was also found in 2% of riding horses and 1,3% working horses in Greece and Macedonia (Sotiraki et al. 1997), 20% horses in Brazil (Teixeira et al. 2014), 14.45% in Turkey (Umur and Aҁici, 2009) and 18.75% in India (Yadav et al. 2014).
In certain areas, no association was found between age of horses and the prevalence of P. equorum, such as 21.6% in older horses in Lesotho (South Africa) (Upjohn et al. 2010), 16.3% in horses older than eight years in Ethiopia (Getachew et al. 2008), and in Pakistan − 22% in horses older than two years (Khan et al. 2010) and 33.33% stable horses (Khan et al. 2020).
The usual pattern of acquisition of immunity against P. equorum may differ in some developing countries, which may be influenced by management strategies. Although younger horses are true hosts for adult ascarids, patent infections may also be present in older horses (Upjohn et al. 2010). In the current study in Serbia, low prevalences of P. equorum were found in horses 3–10 of age (8.16%) and horses older than ten years (3.38%).
Parascariosis is usually asymptomatic and it is found in yunger horses, while it is rarely diagnosed in older animals due to acquired immunity (Suderman et al. 1979). The most common negative effect is perforation of the intestine by the large number of parasites (Clayton and Duncan 1980).
Female ascarids are very fertile and their eggs have tick wall, which makes them very resistant in the environment (Perry 2002) – for at least 18 months up to three years (Ihler 1995).
Ascarid eggs embryonate in the environment in the period of ten days, at the temperature of 25–27ºC. This provides the preconditions for parasite transmission through several generations of foals (Claiton 1986). Infectious L3 larvae from strongylid eggs are released into the environment where they can migrate shorter distances (Langrova et al. 2003). Unlike strongylids, infectious L2 larvae from ascarid eggs are released only in the host (Claiton 1986).
High prevalence of helminthoses in winter (79.71%) and summer (72.11%) can be explained by the fact that the winter of 2017/18 was one of the warmer winters in Serbia, with an average temperature of 14.5ºC; while the summer of 2018 was humid and rainy, with the temperatures above 30ºC (data obtained by Republic Hydrometorological Service of Serbia, 2017, 2018)
Anoplocephalid eggs were detected in 0.18% horses as monoinfection in winter, while 0.73% horses were coinfected with strongylids during all the seasons. The highest prevalence of Anoplocephala spp. was diagnosed in horses 3–10 years old (1.02%), exclusively in stable horses and semi-free ranging horses, mainly as high intensity infections during spring and summer. Spring of 2018 was extremely warm spring for Serbia climate, with the average temperature of 18.2ºC. Together with the rainfall, bioecological preconditions were made for the development of transient hosts (nonparasitic mites from Oribatidae family) and infection of horses during summer. Individual cases of Anoplocephala spp. infections were detected in all examined regions.
Epidemiological studies of equine anoplocephalidosis conducted in Central Spain shown significant humidity-dependent sesonality (Meana et al. 1998). The highest prevalence has been detected in autumn (37.5%) and winter (32.3%), while the prevalences were significantly lower in spring (9.2%) and summer (10.8%). During the section of horses in Belgium, Agneessens et al. (1998) detected the prevalence of tapeworms of 28.9% and no significant differences during seasons were noticed.
High intensity infection of horses with A. perfoliata can cause spastic colic of various degrees (Nielsen 2016). Localisation of parasites in ileocaecal junction can cause ulcers at the place of fixation of parasites, intestinal invagination, acute catarrhal enteritis, phisical opstruction and/or change of intestinal motility (Pavone et al. 2011; Back et al. 2013).
Low prevalence of Anoplocephala (0.91%), can be explained by the data that the examined horses were mainly kept in stables, under controlled conditions. In that manner, the contact with the transient hosts is disabled. It is assumed that the occasional use of individual horses on pastures for work or maintaining physical conditions, as well as consumption of grass or hay, were a potential risk factors for their contact with oribatid transient hosts.
Proglottids of these tapeworms are not excreted daily and continuously, which is why it is necessary to sample faceces from suspicious animals for several consecutive days. In this research faecal samples were collected only once, due to tehnical reasons, which may be one of the causes of such low prevalence of anoplocephalidosis.
Similar results were obtained in the studies in Poland (7.2%) (Tomczuk et al. 2015) and Turkey (2.40%) (Umur and Aҁici 2009). Also, sporadic cases of equine anoplocephalidosis were detected in Island (Eydal and Gunnarasson, 1994). Higher prevalences were detected in horses in Netherlands − 21% (Borgsteede and Beek 1996), Brazil − 16% (Teixeira et al. 2014), Sweden 15.7% (Hedberg-Alm et al. 2020), Germany − 14.3% (Hinney et al. 2011) and in primitive horses in Poland − 42.7% (Slivinska et al. 2016).
Out of the total prevalence of oxyuriosis, 3.47% were monoinfections diagnosed in December using perianal tape method. The eggs of O. equi were detected in faeces of only one horse (0.18%) as coinfection with strongylids in November.
This diagnose can be explained by the fact that that horse had high intensity infection and egg-rich deposites, probably due gravity, fell on excreted faeces. Since faeces are collected from the ground, immediately after defecation, it is possible that the contamination with O. equi eggs occurred from these deposits. Infection with O. equi was detected mainly in horses younger than three years (10.38%), as high intensity infection, and at lower prevalence in horses 3–10 years old (3.06%), as medium intensity infection. The infections were dominant in the region of Šumadija and West Serbia (21.84%) in winter, while sporadic cases were detected in the regions of Vojvodina and Belgrade. Beside stable horses (4.35%), the infections were detected in semi-free ranging horses (2.87%). Higher prevalences were detected in female horses compared to males, and no statistical significance was detected between sexes.
It is known that the development of O. equi is favored by heavy rainfall, which is confirmed by obtained results of higher prevalence of adult parasites in horses from the regions with uniformely high rainfall (Region of Šumadija and West Serbia) and the highest precipitation in the period of October-December.
Oxyuriosis has been detected with various prevalences in different studies, such as 64% in Brazil (Teixeira et al. 2014), 38.7% in primitive horses in Poland (Slivinska et al. 2016), 25.64% in stable horses in Pakistan (Khan et al. 2020), 8.7% in farm horses in Germany (Hinney et al. 2011), 1.20% in Turkey (Umur and Aҁici 2009) and sporadically in Island (Eydal and Gunnarasson 1994).
By monitoring the current pathology of autochtonous breeds of equids (domestic mountain horse and Balkan donkey) in the region of Braničevo district in the period from 2012–2018, high intensity infections with nematodes were detected (Božić et al. 2016; Tarić et al. 2016; Trailović 2019a, 2019b). Strongylids and Dictyocaulus arnfieldi were the most prevalent parasites. D. arnfieldi was dominant in all examined donkeys, but also in horses which weren’t in close contact with the donkeys. High prevalence of Strongyloides westeri was detected in donkeys and in one herd it was associated with the occurrence of diarrhea in several cubs (Trailović et al. 2019).
Ilić and Dimitrijević (2005) detected high prevalences of nematodoses in horses in districts of Braničevo (88.24%), Zlatibor (66.66%) and Nišava (85.72%). By comparing the results obtained in the current study (from the same localities), a constant maintenance of high prevalences of nematodoses, or increase in prevalences, is observed (Šumadija and West Serbia region). These findings obtained 12 years later indicate that these results are due to non-deworming or unplanned deworming of horses. Since there are no veterinary data regarding the treatment of examined horses, there is a presumption that random and occasional deworming of horses and inadequate drug selection and dosing could cause resistance to used antihelmintics. Consequently, according to the gudelines of ESCCAP(2019), deworming treatments of horses should be determined according to the age and usage of horses, while respecting the principles of good hygiene in stable and on pasture. It is recommended that the first treatment during the grazing season be performed before grazing, or 1–2 months after grazing. This is considered strategically important from the aspect of strongylid life cycle and pasture contamination by parasite eggs.