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Parascaris spp. eggs in horses of Italy: a large-scale epidemiological analysis of the egg excretion and conditioning factors

Parasites & Vectors volume 14, Article number: 246 (2021) Cite this article

Abstract

Background

Equine ascariosis, caused by Parascaris spp., is a worldwide endoparasitic disease affecting young horses in particular. Despite the great number of horses reared in Italy, large-scale epidemiological surveys dealing with ascariosis prevalence in the country are not reported in the current literature. For this reason, the present survey aims to describe, for the first time, the spread and infestation of Parascaris spp. in a large population of Italian horses (6896 animals) using faecal egg counts, and further to identify risk factors associated with ascarid egg shedding.

Methods

Individual rectal faecal samples collected during routine veterinary examinations were used and Parascaris spp. prevalence was tested against the animal’s age, sex, housing conditions, geographic provenance as well as the respective sampling season.

Results

Among the examined stables, 35.8% showed at least one horse to be positive for Parascaris spp. eggs and an overall prevalence of 6.3% was found. Ascariosis rates tended to decrease significantly with age and, proportionally, 80.0% of the recorded Parascaris spp. eggs were found in 0.7% of the examined animals. Statistically significant differences among prevalence rates were found between the different geographic areas of provenance and prevalence was found to be higher in horses reared outdoors compared to those raised indoors. Analysis of data based on sex and season did not show any significant differences. Despite the lower prevalence found compared to other European countries, ascariosis was concluded to represent a significant health challenge for horses reared in Italy, especially foals. Age (foals and yearlings) and outdoor rearing were identified to be significant risk factors for Parascaris spp. egg shedding. Furthermore, the relevance of the infected horses over 6 years of age should not be underestimated as these represent a significant source of contamination for younger animals.

Conclusions

The development of improved treatment protocols based on regular faecal examination combined with follow-up assessment of the efficacy of integrated action plans would prove beneficial in regard to animal health and anthelmintic resistance reduction in the field.

Graphical Abstract

Background

Equine ascariosis is a worldwide endoparasitic disease caused by Parascaris spp. that predominantly affects the health status of young horses [1, 2]. In foals, these parasites can be found in up to 100% of cases [3, 4] and, according to its severity and stage, is characterised by nasal discharge, coughing, a rough or bristly hair coat, slow growth and occasional small intestine rupture following the heavy accumulation of worms [5,6,7]. Nevertheless, the main clinical finding related to Parascaris spp. infection is small intestinal impaction [6, 7].

Typically, ascariosis is defined as an infection caused by Parascaris equorum; however, in the USA, Switzerland and Sweden, Parascaris univalens has recently been recognized as the dominant species affecting horses [8,9,10]. In any case, the two species are considered morphologically identical and can only be distinguished through karyotyping; P. univalens possesses one pair of germ line chromosomes with respect to the two of P. equorum [9, 11]. Additionally, recent mitochondrial genome analysis revealed these two to be very closely related and may represent the same species after all [12].

The life cycle of Parascaris spp. initiates with the ingestion of parasite eggs containing infective L2 larvae (larvae develop within 9–14 days after egg excretion within the faeces of infected horses) by a suitable host [7]. After hatching in the host’s intestine, larvae embark on a migration following the hepato-tracheal migratory route before finally returning to the small intestine [13, 14]. Adult development occurs in the jejunum where females will start laying eggs within about 10–15 weeks of infection [5, 15, 16].

Mature Parascaris spp. females are particularly fertile, which can lead to high faecal egg counts (FEC) and significant soil and pasture contamination (requiring adequate management), even in the case of limited parasite burden [17, 18]. Overall, a single infected horse has been reported to be able to output upwards of 50 million eggs per day [19]. Furthermore, eggs of Parascaris spp. can survive in the external environment (pastures, paddocks, boxes, etc.) in excess of 1 year [13, 18, 20].

Foal ascariosis control programs are based on year-round monthly rotational anthelmintic treatment with benzimidazole (e.g. fenbendazole—FBZ), tetrahydropyrimidine (e.g. pyrantel—PYR) and macrocyclic lactones (e.g. ivermectin—IVM and moxidectin—MOX) [21]. In Italy, the treatment of foals is predominantly carried out using IVM and PYR starting from 2 months of age and is repeated every 2 months up to 1 year of age [22].

In Parascaris spp., anthelmintic resistance (AR) to macrocyclic lactones, probably due to intensive use of these drugs, has been widely reported since 2002 [23,24,25]. Additionally, recent reports have suggested AR to pyrantel salts and benzimidazole drugs to be present as well [1, 26, 27]. In Italy, AR to PYR and IVM in ascarids in horses has been reported since 2009 [22].

Recently, a survey on the therapeutic plan applied by Italian horse breeders for the control of ascariosis highlighted that anthelmintic treatment is administered without prior faecal examination in 85.3% of cases, and in 57.8% with a dosage based solely on a visual weight estimation of the animal. Furthermore, only 21.3% of the farmers generally removed horse faeces from pastures as part of ascariosis prophylaxis [28].

Despite the large number of horses (154,505 individuals) reared in Italy, to the best of our knowledge, no large-scale epidemiological surveys dealing with ascariosis prevalence in horses are reported in the present literature. Moreover, studies which do graze this subject are mostly related to anthelmintic efficacy trials [22, 29].

Against this background, the present survey aims to describe, for the first time, the spread and infestation of Parascaris spp. in a large population of horses throughout Italy using faecal egg counts (FEC), and further to identify risk factors associated with ascarid egg shedding.

Methods

Sampling and coprological examination

The study population for this research had been defined in a parallel study evaluating the excretion of gastrointestinal strongyle eggs [30].

A total of 6896 randomly selected horses, ranging from 6 months to 36 years old, were examined through coproscopic analysis for the presence of ascarid eggs between 2015 (n. 4164) and 2016 (n. 2732). Animals from 548 different stables located throughout all regions and islands of Italy were included.

Individual rectal faecal samples collected during routine veterinary examinations were sent, vacuum-packed, in refrigerated containers, to the parasitology laboratory of the Department of Veterinary Medicine of the University of Sassari through an express courier within 3 days after collection.

Each faecal sample was accompanied by a form filled in by the sampling veterinarian with the horse’s data including age, sex, housing conditions and stable. Coprological examination was carried out through the modified McMaster method as described by Raynaud [31], using a sodium chloride (NaCl) supersaturated solution (specific gravity = 1.2) for flotation and an egg detection limit of 15 eggs per gram (EPG) of faeces. Parascaris spp. eggs were identified by morphology [7].

Statistical analysis

Data were collected on a spreadsheet (Microsoft Excel®) and subsequently processed using Minitab® (Minitab, Inc., State College, Pennsylvania, USA) and Epi Info® 6.0 (Centers for Disease Control and Prevention [CDC]/World Health Organization [WHO], Atlanta, GA, USA) software. For elaboration, χ2 test, χ2 test for trend, Pearson correlation, Mann-Whitney test, Kruskal–Wallis test and calculation of odds ratio (OR) were performed. Results were considered statistically significant at a P-value lower than 0.05 (P < 0.05).

Statistical analyses were performed based on various attributes of the monitored horses including age groups (6–11 months, 1 year, 2 years, 3 years, 4–5 years, 6–10 years, > 10 years of age); sex; sampling season (winter, spring, summer, autumn) and housing condition (box, outdoor, indoor/outdoor). Animals were stratified into five classes according to their parasite EPG levels: (1) ≤ 50 EPG; (2) between > 50 and 200 EPG; (3) between 200 and 500 EPG; (4) between > 500 and 1000 EPG; (5) > 1000 EPG.

Data were also processed according to the animals’ geographic provenance as follows: Zone 1-Northern Italy (Piedmont, Lombardy, Trentino Alto Adige, Friuli Venezia Giulia, Veneto, Emilia Romagna and Liguria); Zone 2-Central Italy (Tuscany, Umbria, Marche, Latium, Abruzzi, Molise); Zone 3-Southern Italy (Campania, Basilicata, Apulia, Calabria and Sicily).

The mean intensity (MI) was calculated as the arithmetic mean of EPG values on the total number of infected horses in their respective category.

Results

Among the examined stables, 35.8% showed at least one horse to be positive for Parascaris spp. eggs (95% CI 31.9–39.9) and the overall prevalence for all examined horses was 6.3% (435/6896; 95% CI 5.8–6.9). An EPG mean of 40.0 ± 454.2 and a MI of 634 ± 1702.9 was obtained.

Kolmogorov–Smirnov normality test showed the EPG values attained from the examined horses not to be normally distributed (KS = 0.472; P = 0.010).

Data processed by year showed prevalence rates of 6.8% (95% CI 6.1–7.6) and 5.6% (95% CI 4.8–6.5) with EPG means of 44.8 ± 512.4 and 32.64 ± 326.15 (Mann–Whitney test: U = 14,429,342, P = 0.386) and MI of 659 ± 1899 and 587 ± 1264 (U = 33,661, P = 0.794) for 2015 and 2016, respectively. A statistically significant difference in overall prevalence was found between both years (χ2 =  4.2412, P = 0.0394).

Data processed according to age groups for 5065 horses are shown in Table 1. Prevalence rates tended to decrease significantly with age (χ2 = 386.202, df= 6, P < 0.001) as well as EPG means (Kruskal–Wallis test: H = 491.09, P < 0.001), MI of EPG (H = 25.79; P < 0.001) and OR values; the correlation between age and EPG levels was in effect negative (Pearson Correlation r = − 0.079; P < 0.001).

Table 1 Prevalence rates, mean eggs per gram (EPG) value and mean intensity (MI) of EPG reported for different age groups and their statistical analysis (P-value < 0.001)
Full size table

Proportionally, 80.0% of the recorded Parascaris spp. eggs were found in 49 horses, representing 0.7% of the total examined animals and having EPG values between 750 and 19,065. Moreover, 48.5% (95% CI 0.36–0.63) of these horses were younger than 1 year of age.

Analysis of data based on sex (on a subset of 5137 animals: 2366 females and 2771 males) did not show any significant differences (χ2 = 0.1663; P = 0.683) (Table 2). Neither did Mann–Whitney comparison between EPG means (U = 6,088,128; P = 0.851) and MI EPG (U = 20,702; P = 0.074) show significantly different values in females compared to males.

Table 2 Prevalence rates, mean eggs per gram (EPG) EPG value, mean intensity (MI) of EPG and odds ratio (OR) reported for different seasons, sex, areas and housing conditions
Full size table

Seasonal prevalence rates did not differ significantly (χ2 = 0.437; df = 3; P = 0.509), nor did the mean EPG levels (H = 53.09; P = 0.272) and EPG MI values (H = 1.79; P = 0.618) show any significant differences. Results stratified by sampling seasons are reported in Table 2.

Results obtained through stratification based on the geographic provenance (Table 2) showed significant differences between the prevalence rates for the three different areas, increasing from south to north (χ2 = 14.155; df = 2; P = 0.0008). Non-parametric Kruskal–Wallis test showed no significant differences with respect to the EPG means (H = 5.27; P = 0.072) and EPG MI (H = 1.79; P = 0.617) in the three investigated areas.

Data stratification related to 5696 horses based on housing type highlighted significant differences in Parascaris spp. prevalence (χ2 = 23.119; df = 2; P < 0.001), with the highest prevalence rates found in horses raised outdoors (8.1%). Comparison between the EPG means found in horses with different lifestyles was also significant through Kruskal–Wallis test (H = 53.09; P < 0.001). The highest EPG means (55.6 EPG) were found in horses reared outdoors, while the highest MI EPG were recorded in box-raised horses (506.4 EPG). Results related to housing type are reported in detail in Table 2.

Data processed according to EPG classes are shown in Table 3. Prevalence rates as well as OR values tended to decrease significantly in the highest EPG levels (χ2 = 16,231.2; df = 5; P < 0.0001).

Table 3 Prevalence rates reported according to classes of eggs per gram (EPG) for the 435 horses shedding Parascaris spp. eggs (P-value <  0.0001)
Full size table

Discussion

The present study reports, for the first time, results of an epidemiological survey on Parascaris spp. eggs in Italian horses, including over 6000 animals from all over the country. More than one-third of the examined stables (38.5%) tested positive for Parascaris spp. eggs, which is lower than the prevalence reported in the literature for Finland (47%) [32], the UK (50%) [33] and Kentucky (86%) [34]. The overall Parascaris spp. prevalence (6.3%) found in horses screened in this survey is lower than those reported in similar studies carried out in other countries [1, 3, 32, 33, 35,36,37,38], but higher than that reported in Germany [39], as shown in Table 4. However, the prevalence of Parascaris spp. eggs found in foals (36.7%), which allows for a better comparison of the spread of infestation of these parasites, aligns with the results of a previous study carried out in the UK (38%) [33]. This being said, the prevalence rate of Parascaris spp. in yearlings reported in the present study (17.3%) is higher than the 4% reported by Relf et al. [33]. Furthermore, the prevalence of egg shedding reported in foals in our survey is higher than that reported in Germany (2.9% in horses up to 2 years of age) [39] where the parasitic pressure seems to be particularly low compared to other studies, including this one; this is probably due to the management of outdoor conditions with particular regard to the horse pasture safety and hygiene management in a broad sense [40]. Considerably higher prevalence of egg shedding was found in Normandy, France (30.5% with EPG means of 388) [3] and Finland (50% with EPG means of 360) [2]. Lastly, a study carried out on horses up to 2 years of age in Cuba reported a prevalence of Parascaris spp. of 26.7% [38], while the prevalence found in our study was reported to be 17.7% for the same age category.

Table 4 Overall Parascaris spp. prevalence reported in different countries
Full size table

Unfortunately, further direct comparison between the present and other studies was not possible due to a lack of data uniformity.

Considering the Parascaris spp. mean FEC value of 209 EPG reported in the UK for foals younger than 1 year [33], a much higher value was found in Italy in the present study (EPG mean 546). In accordance with the results reported by Relf et al. [33], the present EPG mean does decrease with increasing age. Regardless, despite this decreasing trend, the recorded MI in older horses should not be underestimated as this could represent a significant source of environmental contamination and may pose a risk to younger animals. Especially foals within the youngest age group could be at risk as they are likely to ingest ascarid eggs while suckling the mare and exploring their immediate environs [13]. Besides, ascaridiosis is occasionally diagnosed in immunocompetent adult horses as well, even if such infections are typically observed on properties where foals also reside and do show overall low FEC values (< 50 EPG) [41].

In any case, prevalence rates and EPG values reported in this survey agree with previous studies in which ascarids are reported to be more common in horses younger than 2 years [42, 43]. Indeed, Parascaris spp. are widely recognized as the most common and pathogenic parasite in foals and yearlings [15, 25]. Most likely, this is due to the significant age-dependent and active immunity of foals, which seems to develop at around 6 months of age [19]. In fact, a bimodal pattern of Parascaris spp. egg shedding has been reported with a primary peak at 3–4 months followed by a secondary more contained peak at 8–10 months of age [44].

Despite the statistically significant differences between the overall prevalence rates of Parascaris spp. eggs recorded in 2015 and 2016 (6.8% in 2015 vs 5.6% in 2016; χ2 = 4.2412; P = 0.0394), environmental contamination levels seem to be uniform during these two periods as no significant differences in mean EPG and MI values (P < 0.05) could be pointed out. The lower prevalence recorded in 2016 (5.6% vs. 6.8% in 2015) could be explained through differences in climatic conditions in Italy observed between the two years. In 2016, a severe drought was recorded [45, 46], possibly leading to lower pasture and paddock ascarid egg loads [43].

It is important to note that the proportion of the animals found to be shedding 80.0% of the total eggs in this research (0.7%) is lower than those reported in other countries [33]. Regardless, such Parascaris spp. “high shedders” do not have the same epidemiological importance as those shedding strongyle eggs [47]. In fact, while faecal examination is adequate for the detection of ascarid eggs shedding in general, the magnitude of quantitative egg counts is not correlated to the size of the worm burden [47, 48].

Unfortunately, selective treatment strategies widely recommended for strongyle control in adult horses, with treatments based on FEC, cannot be applied in juvenile horses. In these animals (foals), which are all considered susceptible and more prone to ascarid infections, an age-defined approach is recommended [13]. At that stage, egg counts merely reflect the foal’s age rather than the actual infection status. Furthermore, leaving a proportion of foals on a given farm untreated is risky and ill-advised as cases of ascarid-associated colic most often occur in previously untreated foals between 4 and 7 months of age [7].

Regarding the seasonal data, in line with previous studies carried out in Europe [32, 39] and the USA [15], no statistically significant differences between the prevalence rates as well as the EPG means were found. Absence of seasonality of the ascarid burden in horses from Italy could be related to the high resistance of the infective eggs in the environment [18, 20] and the Mediterranean climate characterizing Italy. Indeed, significant variations in seasonal trends of ascariosis have been reported in horses raised in more arid climates such as Saudi Arabia [49].

In line with previous studies, no significant differences were found between the prevalence rates, EPG means and MI between sexes [37, 50,51,52]. The vast majority of positive animals in this study consisted of young horses managed in a uniform manner, independently of their respective sex (fillies or colts). Therefore, any significant correlation between gender and prevalence and intensity of infection reported by Imani-Baran et al. [36] is, as stated by Relf et al. [33], probably due to variations in management strategies rather than differences in susceptibility or receptivity between fillies and colts.

Results regarding the animals’ housing suggest keeping animals outdoors (compared to horses being kept in stables) to be an important risk factor for the occurrence of ascariosis, as previously reported [2, 33, 38]. In this regard, hygienic management of manure, which is applied on a daily basis for stabled horses, may explain the reduced ascarid burden reported in the literature [2]. However, our results point to stabled horses having higher MI and mean EPG values (506.4 EPG) and thus requiring appropriate manure management protocols to reduce environmental contamination of confined spaces such as boxes.

Although very little is known regarding effective procedures for the reduction of Parascaris spp. pressure at present, management of pastures, paddocks and stalls can play a critical role in ascariosis epidemiology. Furthermore, conditions required to reduce ascarid contamination may be substantially different from those known to be effective against strongyles [7]. Next, daily management of the manure in boxes where foals and mares are kept year-round could prove an effective control strategy considering the resistant nature of ascarid eggs. Lastly, little is known regarding which molecules (and their relative dosage) may be appropriate for the safe removal or inactivation of equine ascarid eggs from the environment [7, 13].

Conclusions

In conclusion, results of the present survey show, despite the lower Parascaris spp. prevalence found compared to other European countries, ascariosis to represent a health challenge for horses reared in Italy, especially young animals. Furthermore, the relevance of the MI attained from horses over 6 years of age should not be underestimated as these animals represent a possible source of continuous re-infestation responsible for significant environmental contamination and horizontal transmission. Thus, these horses can be considered “egg shedders”, posing a severe health challenge for young animals. Finally, housing type (specifically outdoor rearing) and geographical location should be implemented as risk factors within Parascaris spp. monitoring and control programs for Italian horses, with a specific focus on reduction of risk exposure.

Availability of data and materials

The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.

References

  1. Armstrong SK, Woodgate RG, Gough S, Heller J, Sangster NC, Hughes KJ. The efficacy of ivermectin, pyrantel and fenbendazole against Parascaris equorum infection in foals on farms in Australia. Vet Parasitol. 2014;205:575–80.

    Article  CAS  PubMed  Google Scholar 

  2. Hautala K, Näreaho A, Kauppinen O, Nielsen MK, Sukura A, Rajala-Schultz PJ. Risk factors for equine intestinal parasite infections and reduced efficacy of pyrantel embonate against Parascaris sp. Vet Parasitol. 2019;273:52–9.

    Article  CAS  PubMed  Google Scholar 

  3. Laugier C, Sevin C, Menard S, Maillard K. Prevalence of Parascaris equorum infection in foals on French stud farms and first report of ivermectin-resistant P. equorum populations in France. Vet Parasitol. 2012;188:185–9.

    Article  PubMed  Google Scholar 

  4. Lyons ET, Tolliver SC. Strongyloides westeri and Parascaris equorum: observations in field studies in thoroughbred foals on some farms in Central Kentucky, USA. Helminthologia. 2014;51:7–12.

    Article  Google Scholar 

  5. Clayton HM, Duncan JL. Clinical signs associated with Parascaris equorum infection in worm-free pony foals and yearlings. Vet Parasitol. 1978;4:69–78.

    Article  Google Scholar 

  6. Cribb NC, Cote NM, Boure LP, Peregrine AS. Acute small intestinal obstruction associated with Parascaris equorum infection in young horses: 25 cases (1985–2004). N Z Vet J. 2006;54:338–43.

    Article  CAS  PubMed  Google Scholar 

  7. Nielsen MK. Evidence-based considerations for control of Parascaris spp. infections in horses. Equine Vet Educ. 2016;28:224–31.

    Article  Google Scholar 

  8. Jabbar A, Littlewood DTJ, Mohandas N, Briscoe AG, Foster PG, Muller F, et al. The mitochondrial genome of Parascaris univalens - implications for a “forgotten” parasite. Parasit Vectors. 2014;7:428.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Nielsen MK, Wang J, Davis R, Bellaw JL, Lyons ET, Lear TL, et al. Parascaris univalens - a victim of large-scale misidentification? Parasitol Res. 2014;113:4485–90.

    Article  PubMed  Google Scholar 

  10. Martin F, Hoglund J, Bergstrom TF, Lindsjö OK, Tydén E. Resistance to pyrantel embonate and efficacy of fenbendazole in Parascaris univalens on Swedish stud farms. Vet Parasitol. 2018;264:69–73.

    Article  CAS  PubMed  Google Scholar 

  11. Goday C, Pimpinelli S. Cytological analysis of chromosomes in the two species Parascaris univalens and P. equorum. Chromosoma. 1986;94:1–10.

    Article  Google Scholar 

  12. Gao JF, Zhang XX, Wang XX, Li Q, Li Y, Xu WW, Gao Y, Wang CR. According to mitochondrial DNA evidence, Parascaris equorum and Parascaris univalens may represent the same species. J Helminthol. 2019;93(3):383–8.

    Article  CAS  PubMed  Google Scholar 

  13. Reinemeyer CR, Nielsen MK. Control of helminth parasites in juvenile horses. Equine Vet Educ. 2017;29(4):225–32.

    Article  Google Scholar 

  14. Lyons ET, Drudge JH, Tolliver SC. Studies on the development and chemotherapy of larvae of Parascaris equorum (Nematoda: Ascaridoidea) in experimentally and naturally infected foals. J Parasitol. 1976;62(3):453–9.

    Article  CAS  PubMed  Google Scholar 

  15. Fabiani JV, Lyons ET, Nielsen MK. Dynamics of Parascaris and Strongylus spp. parasites in untreated juvenile horses. Vet Parasitol. 2016;230:62–6.

    Article  CAS  PubMed  Google Scholar 

  16. Anderson RC. Nematode parasites of vertebrates: their development and transmission. Wallingford, Oxon, UK: CABI Publish; 2000.

    Book  Google Scholar 

  17. Di Pietro JA, Todd KS. Chemotherapeutic treatment of larvae and migratory stages of Parascaris equorum. In: Proc. 34th Ann. Conv. Am. Assoc. Equine Prac., San Diego, CA. 1988:611–618.

  18. Austin SM, Foreman JH, Todd KS, Di Pietro JA, Baker GJ. Parascaris equorum infections in horses. Compendium Equine. 1990;12:1110–9.

    Google Scholar 

  19. Clayton HM. Ascarids. Recent advances. Vet Clin North Am Equine Pract. 1986;2(2):313–28.

    Article  CAS  PubMed  Google Scholar 

  20. Ihler CF. The distribution of Parascaris equorum eggs in the soil profile of bare paddocks in some Norwegian studs. Vet Res Commun. 1995;19:495–501.

    Article  CAS  PubMed  Google Scholar 

  21. Robert M, Hu W, Nielsen MK, Stowe CJ. Attitude towards implementation of surveillance-based parasite control on Kentucky Thoroughbred farms–current strategies, awareness, and willingness-to-pay. Equine Vet J. 2015;47:694–700.

    Article  CAS  PubMed  Google Scholar 

  22. Veronesi F, Moretta I, Moretti A, Fioretti DP, Genchi C. Field effectiveness of pyrantel and failure of Parascaris equorum egg count reduction following ivermectin treatment in Italian horse farms. Vet Parasitol. 2009;161:138–41.

    Article  CAS  PubMed  Google Scholar 

  23. Boersema JH, Eysker M, Nas JW. Apparent resistance of Parascaris equorum to macrocyclic lactones. Vet Rec. 2002;150:279–81.

    Article  CAS  PubMed  Google Scholar 

  24. Reinemeyer CR. Diagnosis and control of anthelmintic-resistant Parascaris equorum. Parasit Vectors. 2009;2(Suppl. 2):S8.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Cooper LG, Caffe G, Cerutti J, Nielsen MK, Anziani OS. Reduced efficacy of ivermectin and moxidectin against Parascaris spp. in foals from Argentina. Vet Parasitol Reg Stud Reports. 2020;20:100388.

    PubMed  Google Scholar 

  26. Lyons ET, Tolliver SC, Kuzmina TA, Collins SS. Further evaluation in field tests of the activity of three anthelmintics (fenbendazole, oxibendazole and pyrantel pamoate) against the ascarid Parascaris equorum in horse foals on eight farms in Central Kentucky (2009–2010). Parasitol Res. 2011;109:1193–7.

    Article  PubMed  Google Scholar 

  27. Peregrine AS, Molento MB, Kaplan RM, Nielsen MK. Anthelmintic resistance in important parasites of horses: does it really matter? Vet Parasitol. 2014;201:1–8.

    Article  CAS  PubMed  Google Scholar 

  28. Papini RA, Micol De Bernart F, Sgorbini M. A Questionnaire Survey on Intestinal Worm Control Practices in Horses in Italy. J Equine Vet Sci. 2015;35:70–5.

    Article  Google Scholar 

  29. Veronesi F, Fioretti DP, Genchi C. Are macrocyclic lactones useful drugs for the treatment of Parascaris equorum infections in foals? Vet Parasitol. 2010;172(1–2):164–7.

    Article  CAS  PubMed  Google Scholar 

  30. Scala A, Tamponi C, Sanna G, Predieri G, Dessì G, Sedda G, et al. Gastrointestinal strongyles egg excretion in relation to age, gender, and management of horses in Italy. Animals. 2020;10(12):2283.

    Article  PubMed Central  Google Scholar 

  31. Raynaud JP. Etude de l’efficacité d’une technique de coproscopie quantitative our le diagnostic de routine et le controle des infestations parasitaires des bovins, ovins, equines et porcins. Ann Parasitol. 1970;45:321–42.

    Article  CAS  Google Scholar 

  32. Aromaa M, Hautala K, Oksanen A, Sukura A, Näreaho A. Parasite infections and the risk factors in foals and young horses in Finland. Vet Parasitol Reg Stud Reports. 2018;12:35–8.

    PubMed  Google Scholar 

  33. Relf VE, Morgan ER, Hodgkinson JE, Matthews JB. Helminth egg excretion with regard to age, gender and management practices on UK Thoroughbred studs. Parasitology. 2013;140:641–52.

    Article  CAS  PubMed  Google Scholar 

  34. Lyons ET, Tolliver SC. Prevalence of parasite eggs (Strongyloides westeri, Parascaris equorum, and strongyles) and oocysts (Emeria leuckarti) in the feces of Thoroughbred foals on 14 farms in central Kentucky in 2003. Parasitol Res. 2004;92:400–4.

    Article  CAS  PubMed  Google Scholar 

  35. Mezgebu T, Tafess K, Tamiru F. Prevalence of gastrointestinal parasites of horses and donkeys in and around Gondar Town, Ethiopia. Open J Vet Med. 2013;3(06):267.

    Article  Google Scholar 

  36. Imani-Baran A, Abdollahi J, Akbari H, Raafat A. Coprological prevalence and the intensity of gastrointestinal nematodes infection in working equines, east Azerbaijan of Iran. J Anim Plant Sci. 2019;29(5):1269–78.

    Google Scholar 

  37. Othman R, Alzuheir I. Prevalence of Parascaris equorum in native horses in West Bank Palestine. Iraqi J Vet Sci. 2019;33(2):433–6.

    Article  Google Scholar 

  38. Salas-Romero J, Gómez-Cabrera KA, Aguilera-Valle LA, Bertot JA, Salas JE, Arenal A, et al. Helminth egg excretion in horses kept under tropical conditions—Prevalence, distribution and risk factors. Vet Parasitol. 2017;243:256–9.

    Article  CAS  PubMed  Google Scholar 

  39. Rehbein S, Visser M, Winter R. Prevalence, intensity and seasonality of gastrointestinal parasites in abattoir horses in Germany. Parasitol Res. 2013;112:407–13.

    Article  PubMed  Google Scholar 

  40. Aboling S, Drotleff AM, Cappai MG, Kamphues J. Contamination with ergot bodies (Claviceps purpurea sensu lato) of two horse pastures in Northern Germany. Mycotoxin Res. 2016;32:207–19.

    Article  CAS  PubMed  Google Scholar 

  41. Nielsen MK, Mittel L, Grice A, Erskine M, Graves E, Vaala W, et al. AAEP Parasite Control Guidelines. Online at American Association of Equine Practitioners. 2019. https://aaep.org/sites/default/files/Documents/InternalParasiteGuidelinesFinal5.23.19.pdf?fbclid=IwAR1VXsGa19jmLjM5Vwn-3w3tBX-2Ndz-xGdxty0SV-Qv-jUGtMqOgh6Bvrs. Accessed 14 Dec 2020.

  42. Bucknell D, Gasser R, Beveridge I. The prevalence and epidemiology of gastrointestinal parasites of horses in Victoria. Australia Int J Parasitol. 1995;25:711–24.

    Article  CAS  PubMed  Google Scholar 

  43. Mfitilodze MW, Hutchinson GW. Prevalence and intensity of non-strongyle intestinal parasites of horses in northern Queensland. Aust Vet J. 1989;66:23–6.

    Article  CAS  PubMed  Google Scholar 

  44. Donoghue EM, Lyons ET, Bellaw JL, Nielsen MK. Biphasic appearance of corticated and decorticated ascarid egg shedding in untreated horse foals. Vet Parasitol. 2015;214:114–7.

    Article  CAS  PubMed  Google Scholar 

  45. ISPRA, Istituto Superiore per la Protezione e la Ricerca Ambientale. Gli indicatori del Clima in Italia nel. 2015. 2016;5:49.

  46. ISPRA, Istituto Superiore per la Protezione e la Ricerca Ambientale. Gli indicatori del Clima in Italia nel 2016. 2017;3:26.

  47. Nielsen MK, Baptiste KE, Tolliver SC, Collins SS, Lyons ET. Analysis of multiyear studies in horses in Kentucky to ascertain whether counts of eggs and larvae per gram of feces are reliable indicators of numbers of strongyles and ascarids present. Vet Parasitol. 2010;174:77–84.

    Article  CAS  PubMed  Google Scholar 

  48. Matthews J, Lester H. Control of equine nematodes: making the most of faecal egg counts. Practice. 2015;37(10):540–4.

    Article  Google Scholar 

  49. Anazi ADA, Alyousif MS. Prevalence of non-strongyle gastrointestinal parasites of horses in Riyadh region of Saudi Arabia. Saudi J Biol Sci. 2011;18:299–303.

    Article  PubMed  Google Scholar 

  50. Yadav KS, Shukla PC, Gupta DK, Mishra A. Prevalence of gastrointestinal nematodes in horses of Jabalpur region. Res J Vet Pract. 2014;2:44–8.

    Article  Google Scholar 

  51. Singh G, Soodan J, Singla L, Khajuria J. Epidemiological studies on gastrointestinal helminths in horses and mules. Vet Pract. 2012;13:23–7.

    Google Scholar 

  52. Kornaś S, Skalska M, Nowosad B, Gawor J, Labaziewicz I, Babiuch A. Occurrence of tapeworm, roundworm and botfly larvae in horses from southern Poland. Med Wet. 2007;63:1373–6.

    Google Scholar 

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Acknowledgements

Authors thank Prof. Nicolò Pietro Paolo Macciotta for supporting the statistical analysis, Mr. Francesco Salis for the technical assistance in laboratory and Mrs. Veronica Pisu of Asinara4x4 for the graphical abstract picture.

Funding

This research was partially funded by “Fondo di Ateneo per la ricerca 2019” of Prof. Antonio Scala of the University of Sassari, Italy.

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Author notes

  1. Antonio Scala and Claudia Tamponi contributed equally to this work

Authors and Affiliations

  1. Dipartimento di Medicina Veterinaria, Università di Sassari, Sassari, Italy

    Antonio Scala, Claudia Tamponi, Giuliana Sanna, Luisa Meloni, Stephane Knoll, Giampietro Sedda, Giorgia Dessì, Maria Grazia Cappai & Antonio Varcasia

  2. ACME s.r.l., Reggio Emilia, Italy

    Giulio Predieri

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  1. Antonio Scala
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Contributions

Conceptualization, AV and AS; investigation, GD, GS, PG, CT, GS, LM.; data curation, MGC; writing—original draft preparation, AV; writing—review and editing, CT, PG, SK; All authors have read and agreed to the published version of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Antonio Varcasia.

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Ethics approval and consent to participate

All the operations carried out on live animals were performed by the vet as part of the routine clinical visit and the study was carried out following the recommendations of European Council Directive (86/609/EEC) on the protection of animals.

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The authors declare that they have no competing interests.

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Scala, A., Tamponi, C., Sanna, G. et al. Parascaris spp. eggs in horses of Italy: a large-scale epidemiological analysis of the egg excretion and conditioning factors. Parasites Vectors 14, 246 (2021). https://doi.org/10.1186/s13071-021-04747-w

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Keywords

Parasites & Vectors

ISSN: 1756-3305

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