- Email: [email protected]
Gastrointestinal Parasites of Stabled and Grazing Horses in Central and Northern Greece
SHORT COMMUNICATION Gastrointestinal Parasites of Stabled and Grazing Horses in Central and Northern Greece Margarita Papazahariadou, DVM, PhD, Dipl EVPC, Elias Papadopoulos, DVM, MSc, PhD, Dipl EVPC, Anastasia Diakou, DVM, PhD, and Socrates Ptochos, DVM
ABSTRACT The aim of this investigation was to compare parasites found in feces from stabled and grazing horses in Greece. For this, a total of 223 fecal samples were collected from horses from various parts of Central and Northern Greece. One hundred fifty were stabled and 73 were grazing horses, used for riding, working, or breeding. One hundred came from seven riding clubs, 73 from one breeding farm, and 50 were work horses from five farms. Parasitologic investigation was performed by applying three fecal examination techniques (Teleman’s, zinc flotation, and stained smears) to detect ova, larvae, and oocysts of parasites. It was found that 77 the 223 horses (34.5%) in the study were infected with one or more parasite species. In the stabled horses, the most common parasites detected were eggs of strongyles, Strongyloides spp, Anoplocephala spp, Habronema spp, and Parascaris equorum and oocysts of Eimeria spp and Cryptosporidium spp; in the grazing horses, Anoplocephala spp. Strongyles were significantly more prevalent in the group of stabled horses than in the other group (P < .05). The results of the current study demonstrate that parasite infection is highly prevalent in horses in Greece. Keywords: Horses; Stabled; Grazing; Parasites; Greece
result in the maintenance of parasites in an area. Prevalence data on endoparasites from equine populations are of great importance, particularly those that reflect the impact of chemotherapy. Knowledge about the parasite genera that are more common in one area or in a certain type of equine population assists in their diagnosis and effective control. In Greece, a few studies on the prevalence of equine parasites have been carried out in the past, though none recently.3,4 Conversely, a high number of sport horses are imported into the country or travel to different areas of Greece, increasing the risk of the introduction and spread of exotic parasite infections. Additionally, in the different regions of Greece, horses are kept under a range of management systems (grazing or stabled) with short or long time at pasture, depending mostly on their use. Because of the lack of epidemiologic information on the horse parasite fauna, current helminth control practices rely on irregular and often unnecessary use of anthelmintics on many of these farms. The aim of this investigation was to compare parasites found in feces from stabled and grazing horses used for riding, working, or breeding. Also, a secondary aim was to compare the resulting data with similar past research in Greece.
MATERIALS AND METHODS
From the Laboratory of Parasitology and Parasitic Diseases, Faculty of Veterinary Medicine, Aristotle University, Thessaloniki, Greece. Reprint requests: Elias Papadopoulos, Laboratory of Parasitology and Parasitic Diseases, Faculty of Veterinary Medicine, Aristotle University, 541 24 Thessaloniki, Greece. 0737-0806/$ - see front matter Ó 2009 Elsevier Inc. All rights reserved. doi:10.1016/j.jevs.2009.03.005
A total of 223 fecal samples were collected from horses from various parts of Central and Northern Greece during 20062007. One hundred fifty were stabled and 73 were grazing horses, 88 were male and 135 female, of various breeds or crossbreds. They were used for riding, working, or breeding. One hundred were from seven riding clubs, 73 from one breeding farm, and 50 were working horses from five farms. Animals were aged 2 to 20 years; however, the exact age of some of them was not possible to ascertain. The sampled horses were divided into four age groups: (1) 2 to 5 years old (n ¼ 11 animals), (2) 6 to 10 (n ¼ 84), (3) 11 to 15 (n ¼ 92), and (4) 16 to 20 (n ¼ 36). All animals spent some time during the day, ranging from a couple of hours to the whole day, in open paddocks with or without vegetation. Riding and working animals were stabled, and the broodmares were grazed. All animals in the study had been treated previously
Journal of Equine Veterinary Science Vol 29, No 4 (2009)
233
INTRODUCTION Gastrointestinal parasitism is a common health problem in horses worldwide. Parasites can produce varying degrees of damage, depending on the type and number present and the immune status of the host.1 Problems associated with parasite infection include diarrhea, colic, weight loss, poor growth, emaciation, unexpected sudden death, impaired growth, and predisposition to other infectious diseases.2 Very often subclinical infections occur and may
M Papazahariadou et al Vol 29, No 4 (2009)
234
with anthelmintics for parasites, largely receiving ivermectin or moxidectin, although detailed records for individuals were unavailable. However, none of the animals had been treated for at least 4 months before the sampling took place. A fecal sample was taken from each animal by a plastic glove, put into an isotherm box and transferred to the Laboratory of Parasitology and Parasitic Disease of the Faculty of Veterinary Medicine (Aristotle University of Thessaloniki, Greece) for examination. Parasitologic examination of feces was carried out according to Teleman’s5 sedimentation method and the zinc flotation method6 for detection of ova, larvae, cysts, and oocysts of parasites. Also, smears of the feces were prepared and stained with modified safranin-methylene blue stain7 to detect and identify protozoan parasites (Cryptosporidium spp and Cyclospora spp). All eggs, larvae, and oocysts found were identified according to morphologic characteristics under light microscopy.1 Horses expelling any parasite element (ova, larvae, or cysts) in their feces were characterized as infected. Differences in the proportion infected in various classes were compared statistically by the chi-squared test using SPSS (version 15.0).
RESULTS Of the 223 horses included in the study, 77 (34.5%) were infected with one or more parasite species. The numbers of infected horses, stabled or grazing, according to sex, are presented in Table 1. There was no significant difference in the number of infected stabled males or females (P > .05). No valid comparison was possible for grazing animals, because all of the infected animals were female. There was a strong negative relationship between age and infection; 8 of the 11 horses (73%) in the 2- to 5-year-old age group were infected, 38 of the 84 (45%) 6- to 10-yearold animals, 26 of the 92 (28%) 11- to 15-year-old animals, and five of the 36 (14%) 16- to 20-year-old animals were infected. Eggs of strongyles, Strongyloides spp, Anoplocephala spp, Habronema spp, and Parascaris equorum were found and also oocysts of Eimeria spp and Cryptosporidium spp (Table 2). The most common parasite detected in the stabled horses was strongyles, and in the grazing horses, it was Anoplocephala spp. The values observed for the prevalence of tapeworm eggs are probably minimum estimates, because the eggs do not float well and hence are likely to have been underestimated in the analysis. Strongyles were significantly more prevalent in the group of stabled horses than in the grazed horses (P < .05). Parascaris equorum eggs were found in one case of a 2-year-old horse. No difference in infection between grazed and stabled animals was observed for the other parasite genera, but low prevalences precluded statistical comparison. Strongyles were
Table 1. Number of infected male and female horses and the overall number (plus percentage infected), within stabled and grazing animal categories, from a survey carried out in various parts of Central and Northern Greece during 2006 to 2007 Number Infected Horse Group
Male
Female
Total
Stabled Grazing Total
27 0 27
21 29 50
48 (32.0%) 29 (39.7%) 77 (34.5%)
generally more common in younger animals. Cyclosporalike oocysts were detected in three samples, but they were not positively identified (sporulation failed).
DISCUSSION The results of the current study demonstrate that parasite infection is highly prevalent in horses in Greece. However, compared with previous reports, our results clearly show an overall reduction in prevalence rate. Himonas3 reported that 100% of horses examined in Greece were parasitized with at least one Strongylus species. Later, Sotiraki et al4 reported that the prevalence of parasites in working horses was 62.4%, whereas in our study a mean prevalence of 34.5% was found. From the current study, it is apparent that a long-term benefit from the usage of macrocyclic lactones or other anthelmintics in equines and an increasing animal welfare concept among horse owners exist. In our study, grazing horses were infected with more parasite genera than the stabled horses. In a similar study8 of intestinal parasite infection of horses from riding clubs in the Krakow area in Poland, mean prevalence and eggs per gram (EPG) counts were higher in horses under the pasture system (73.9%) than in horses on paddocks with grass (42.1%) or without grass (19.2%). The fact that, in our case, the stabled horses were more infected with strongyles than those grazed (30.7% and 15.1%, respectively) may perhaps be attributed to the development and maintenance of better immunity against parasite infection in grazed animals, because they are more often challenged.9 Horses from stud farms in Sweden shed significantly higher numbers of strongyle eggs compared with those from other type of farms, such as riding schools and boarding stables.10 Our findings, together with the results of these studies, further support the principle that the management system is of major importance as a predisposing factor to parasite infection. In general, strongyle infection was the most prevalent (25.6%) parasite detected in the study. In previous investigations, strongyles were also detected in high percentages, up to 45.6%.4
M Papazahariadou et al Vol 29, No 4 (2009)
235
Table 2. Number (%) of stabled and grazing horses found to be infected with a range of genera of nematode parasites, in a survey carried out in various parts of Central and Northern Greece during 2006 to 2007 Number (and Percentage) Infected Horse Group Strongyles Strongyloides Anoplocephala Habronema Parascaris Eimeria Cryptosporidium Stabled Grazing Total
46 (30.7) 11 (15.1) 57 (25.6)
0 4 (5.5) 4 (1.8)
0 19 (26.0) 19 ( 8.5)
Anoplocephala perfoliata eggs were found in grazing animals at a prevalence of only 26%. This can be attributed to the much longer presence of grazing animals on pasture, resulting in consumption of fresh grass and therefore an increased chance of ingesting the cysticercoids in the intermediate hosts compared with stabled animals. Additionally, the common use of macrocyclic lactones in horses, which have no activity against tapeworms, may further contribute to the presence of tapeworms in grazing horses. Sotiraki et al4 found A. perfoliata in only 0.4% of the examined horses. The increased prevalence in our study may be explained mainly through the long-term use of macrocyclic lactones that have no effect against this parasite. In studies in which Cryptosporidium spp have been identified, the prevalence of infection varies and may reach high percentages. Our finding is that 7.2% of the examined horses were infected with Cryptosporidium spp. This prevalence is similar to that reported by Himonas et al (8.2%).11 It seems that, worldwide, this parasite is common in horses, particularly in foals. However, to compare findings, it is important to interpret them on the basis of the diagnostic test used and to consider its sensitivity.12 Infection with Eimeria species occurs worldwide in horses.13 Eimeria leuckarti is the only species that has been reported in Greece previously at a prevalence of 2.6%.4 Our finding (4%) is similar, but this parasite has been detected only in the stabled horses and not in the grazing animals. Horse helminthes are commonly studied post mortem using autopsy methods, an approach that allows species identification.14 However, necropsy studies have limitations, such as high cost, and horse examination at abattoirs often deal with old animals with low parasitic burdens and diverse or unknown grazing histories.15 Furthermore, the investigation of intestinal parasite communities of valuable brood horses, in a representative sample, by autopsy methods is almost impossible.16 For this reason, examination of intestinal helminthes of horses has been conducted after deworming, using highly effective modern anthelmintic drugs. This method enables the collection and identification of all luminal stages of the intestinal nematodes.15,16 Finally, more sensitive molecular methods, such as polymerase chain reaction, may be used in combination with others described
0 2 (2.7) 2 (0.9)
0 1 (1.4) 1 (0.4)
9 (6) 0 9 (4.0)
7 (4.7) 9 (12.3) 16 (7.2)
for the identification of some species of encysted larval cyathostomes . ACKNOWLEDGMENT The authors thank Professor Richard Wall (Bristol, UK) for comments on the manuscript. REFERENCES 1. Soulsby EJL. Helminths, arthropods and protozoa of domesticated animals. Philadelphia: Lea and Febiger; 1982. 2. Taylor MA, Coop RL, Wall RL. Veterinary parasitology. Oxford, UK: Blackwell Publishing; 2007. 3. Himonas CA. Fecal survey on the helminthiasis of equines. Hellenic Vet 1968;4:239–248. 4. Sotiraki S, Badouvas A, Himonas C. A survey on the prevalence of internal parasites of equines in Macedonia and Thessalia-Greece. J Equine Vet Sci 1997;17:550–552. 5. Piekarski G. Medizinische parasitologie in Tafeln. Berlin: Springer Verlag; 1973. 6. Truant AL, Elliott SH, Kelly MT, Smith JH. Comparison of formalinethylether sedimentation, formalin-ethyl acetate sedimentation, and zinc sulfate flotation techniques for detection of intestinal parasites. J Clin Microbiol 1981;13:882–884. 7. Visvesvara GS, Moura H, Kovasc-Nace E, Wallace S, Eberhard ML. Uniform staining of Cyclospora oocysts in fecal smears by a modified safranin technique with microwave heating. J Clin Microbiol 1997; 35:730–733. 8. Kornas S, Nowosad B, Skalska M, Boloz T. Intestinal parasites infection of horses from riding clubs in Krakow area. Wiad Parazytol 2004; 50:323–327. 9. Klei TR. Equine immunity to parasites. Vet Clin North Am Equine Pract 2000;16:69–78. 10. Osterman Lind E, Hoglund J, Ljungstrom BL, Nilsson O, Uggla A. A field survey on the distribution of strongyle infections of horses in Sweden and factors affecting faecal egg counts. Equine Vet J 1999; 31:68–72. 11. Himonas C, Antoniadou-Sotiriadou K, Sotiraki S, Papazahariadou M. Intestinal protozoa of animals in Macedonia. Bull Hell Vet Med Soc 1998;49:300–306. 12. Majewska AC, Solarczyk P, Tamang L, Graczyk TK. Equine Cryptosporidium parvum infections in western Poland. Parasitol Res 2004; 93:274–278.
236
M Papazahariadou et al Vol 29, No 4 (2009)
13. Epe C, Coati N, Schnieder T. Results of parasitological examinations
15. Osterman Lind E, Eysker M, Nilsson O, Uggla A, Hoglund J. Expulsion
of faecal samples from horses, ruminats, dogs, cats, hedgehogs and
of small strongyle nematodes (cyathostomin spp) following deworming
rabbits between 1998 and 2002. Dtsch Tierarztl Wochenschr 2004;111:243–247.
of horses on a stud farm Sweden. Vet Parasitol 2003;115:289–299. 16. Kuzmina TA, Kharchenko VA, Starovir AI, Dvojnos GM. Analysis of
14. Bucknell DG, Gasser RB, Beveridge I. The prevalence and epidemi-
the strongylid nematodes (Nematoda: Strongylidae) community af-
ology of gastrointestinal parasites of horses in Victoria. Austr Int J
ter deworming of brood horses in Ukraine. Vet Parasitol 2005;
Parasitol 1995;25:711–724.
131:283–290.
ABSTRACT The aim of this investigation was to compare parasites found in feces from stabled and grazing horses in Greece. For this, a total of 223 fecal samples were collected from horses from various parts of Central and Northern Greece. One hundred fifty were stabled and 73 were grazing horses, used for riding, working, or breeding. One hundred came from seven riding clubs, 73 from one breeding farm, and 50 were work horses from five farms. Parasitologic investigation was performed by applying three fecal examination techniques (Teleman’s, zinc flotation, and stained smears) to detect ova, larvae, and oocysts of parasites. It was found that 77 the 223 horses (34.5%) in the study were infected with one or more parasite species. In the stabled horses, the most common parasites detected were eggs of strongyles, Strongyloides spp, Anoplocephala spp, Habronema spp, and Parascaris equorum and oocysts of Eimeria spp and Cryptosporidium spp; in the grazing horses, Anoplocephala spp. Strongyles were significantly more prevalent in the group of stabled horses than in the other group (P < .05). The results of the current study demonstrate that parasite infection is highly prevalent in horses in Greece. Keywords: Horses; Stabled; Grazing; Parasites; Greece
result in the maintenance of parasites in an area. Prevalence data on endoparasites from equine populations are of great importance, particularly those that reflect the impact of chemotherapy. Knowledge about the parasite genera that are more common in one area or in a certain type of equine population assists in their diagnosis and effective control. In Greece, a few studies on the prevalence of equine parasites have been carried out in the past, though none recently.3,4 Conversely, a high number of sport horses are imported into the country or travel to different areas of Greece, increasing the risk of the introduction and spread of exotic parasite infections. Additionally, in the different regions of Greece, horses are kept under a range of management systems (grazing or stabled) with short or long time at pasture, depending mostly on their use. Because of the lack of epidemiologic information on the horse parasite fauna, current helminth control practices rely on irregular and often unnecessary use of anthelmintics on many of these farms. The aim of this investigation was to compare parasites found in feces from stabled and grazing horses used for riding, working, or breeding. Also, a secondary aim was to compare the resulting data with similar past research in Greece.
MATERIALS AND METHODS
From the Laboratory of Parasitology and Parasitic Diseases, Faculty of Veterinary Medicine, Aristotle University, Thessaloniki, Greece. Reprint requests: Elias Papadopoulos, Laboratory of Parasitology and Parasitic Diseases, Faculty of Veterinary Medicine, Aristotle University, 541 24 Thessaloniki, Greece. 0737-0806/$ - see front matter Ó 2009 Elsevier Inc. All rights reserved. doi:10.1016/j.jevs.2009.03.005
A total of 223 fecal samples were collected from horses from various parts of Central and Northern Greece during 20062007. One hundred fifty were stabled and 73 were grazing horses, 88 were male and 135 female, of various breeds or crossbreds. They were used for riding, working, or breeding. One hundred were from seven riding clubs, 73 from one breeding farm, and 50 were working horses from five farms. Animals were aged 2 to 20 years; however, the exact age of some of them was not possible to ascertain. The sampled horses were divided into four age groups: (1) 2 to 5 years old (n ¼ 11 animals), (2) 6 to 10 (n ¼ 84), (3) 11 to 15 (n ¼ 92), and (4) 16 to 20 (n ¼ 36). All animals spent some time during the day, ranging from a couple of hours to the whole day, in open paddocks with or without vegetation. Riding and working animals were stabled, and the broodmares were grazed. All animals in the study had been treated previously
Journal of Equine Veterinary Science Vol 29, No 4 (2009)
233
INTRODUCTION Gastrointestinal parasitism is a common health problem in horses worldwide. Parasites can produce varying degrees of damage, depending on the type and number present and the immune status of the host.1 Problems associated with parasite infection include diarrhea, colic, weight loss, poor growth, emaciation, unexpected sudden death, impaired growth, and predisposition to other infectious diseases.2 Very often subclinical infections occur and may
M Papazahariadou et al Vol 29, No 4 (2009)
234
with anthelmintics for parasites, largely receiving ivermectin or moxidectin, although detailed records for individuals were unavailable. However, none of the animals had been treated for at least 4 months before the sampling took place. A fecal sample was taken from each animal by a plastic glove, put into an isotherm box and transferred to the Laboratory of Parasitology and Parasitic Disease of the Faculty of Veterinary Medicine (Aristotle University of Thessaloniki, Greece) for examination. Parasitologic examination of feces was carried out according to Teleman’s5 sedimentation method and the zinc flotation method6 for detection of ova, larvae, cysts, and oocysts of parasites. Also, smears of the feces were prepared and stained with modified safranin-methylene blue stain7 to detect and identify protozoan parasites (Cryptosporidium spp and Cyclospora spp). All eggs, larvae, and oocysts found were identified according to morphologic characteristics under light microscopy.1 Horses expelling any parasite element (ova, larvae, or cysts) in their feces were characterized as infected. Differences in the proportion infected in various classes were compared statistically by the chi-squared test using SPSS (version 15.0).
RESULTS Of the 223 horses included in the study, 77 (34.5%) were infected with one or more parasite species. The numbers of infected horses, stabled or grazing, according to sex, are presented in Table 1. There was no significant difference in the number of infected stabled males or females (P > .05). No valid comparison was possible for grazing animals, because all of the infected animals were female. There was a strong negative relationship between age and infection; 8 of the 11 horses (73%) in the 2- to 5-year-old age group were infected, 38 of the 84 (45%) 6- to 10-yearold animals, 26 of the 92 (28%) 11- to 15-year-old animals, and five of the 36 (14%) 16- to 20-year-old animals were infected. Eggs of strongyles, Strongyloides spp, Anoplocephala spp, Habronema spp, and Parascaris equorum were found and also oocysts of Eimeria spp and Cryptosporidium spp (Table 2). The most common parasite detected in the stabled horses was strongyles, and in the grazing horses, it was Anoplocephala spp. The values observed for the prevalence of tapeworm eggs are probably minimum estimates, because the eggs do not float well and hence are likely to have been underestimated in the analysis. Strongyles were significantly more prevalent in the group of stabled horses than in the grazed horses (P < .05). Parascaris equorum eggs were found in one case of a 2-year-old horse. No difference in infection between grazed and stabled animals was observed for the other parasite genera, but low prevalences precluded statistical comparison. Strongyles were
Table 1. Number of infected male and female horses and the overall number (plus percentage infected), within stabled and grazing animal categories, from a survey carried out in various parts of Central and Northern Greece during 2006 to 2007 Number Infected Horse Group
Male
Female
Total
Stabled Grazing Total
27 0 27
21 29 50
48 (32.0%) 29 (39.7%) 77 (34.5%)
generally more common in younger animals. Cyclosporalike oocysts were detected in three samples, but they were not positively identified (sporulation failed).
DISCUSSION The results of the current study demonstrate that parasite infection is highly prevalent in horses in Greece. However, compared with previous reports, our results clearly show an overall reduction in prevalence rate. Himonas3 reported that 100% of horses examined in Greece were parasitized with at least one Strongylus species. Later, Sotiraki et al4 reported that the prevalence of parasites in working horses was 62.4%, whereas in our study a mean prevalence of 34.5% was found. From the current study, it is apparent that a long-term benefit from the usage of macrocyclic lactones or other anthelmintics in equines and an increasing animal welfare concept among horse owners exist. In our study, grazing horses were infected with more parasite genera than the stabled horses. In a similar study8 of intestinal parasite infection of horses from riding clubs in the Krakow area in Poland, mean prevalence and eggs per gram (EPG) counts were higher in horses under the pasture system (73.9%) than in horses on paddocks with grass (42.1%) or without grass (19.2%). The fact that, in our case, the stabled horses were more infected with strongyles than those grazed (30.7% and 15.1%, respectively) may perhaps be attributed to the development and maintenance of better immunity against parasite infection in grazed animals, because they are more often challenged.9 Horses from stud farms in Sweden shed significantly higher numbers of strongyle eggs compared with those from other type of farms, such as riding schools and boarding stables.10 Our findings, together with the results of these studies, further support the principle that the management system is of major importance as a predisposing factor to parasite infection. In general, strongyle infection was the most prevalent (25.6%) parasite detected in the study. In previous investigations, strongyles were also detected in high percentages, up to 45.6%.4
M Papazahariadou et al Vol 29, No 4 (2009)
235
Table 2. Number (%) of stabled and grazing horses found to be infected with a range of genera of nematode parasites, in a survey carried out in various parts of Central and Northern Greece during 2006 to 2007 Number (and Percentage) Infected Horse Group Strongyles Strongyloides Anoplocephala Habronema Parascaris Eimeria Cryptosporidium Stabled Grazing Total
46 (30.7) 11 (15.1) 57 (25.6)
0 4 (5.5) 4 (1.8)
0 19 (26.0) 19 ( 8.5)
Anoplocephala perfoliata eggs were found in grazing animals at a prevalence of only 26%. This can be attributed to the much longer presence of grazing animals on pasture, resulting in consumption of fresh grass and therefore an increased chance of ingesting the cysticercoids in the intermediate hosts compared with stabled animals. Additionally, the common use of macrocyclic lactones in horses, which have no activity against tapeworms, may further contribute to the presence of tapeworms in grazing horses. Sotiraki et al4 found A. perfoliata in only 0.4% of the examined horses. The increased prevalence in our study may be explained mainly through the long-term use of macrocyclic lactones that have no effect against this parasite. In studies in which Cryptosporidium spp have been identified, the prevalence of infection varies and may reach high percentages. Our finding is that 7.2% of the examined horses were infected with Cryptosporidium spp. This prevalence is similar to that reported by Himonas et al (8.2%).11 It seems that, worldwide, this parasite is common in horses, particularly in foals. However, to compare findings, it is important to interpret them on the basis of the diagnostic test used and to consider its sensitivity.12 Infection with Eimeria species occurs worldwide in horses.13 Eimeria leuckarti is the only species that has been reported in Greece previously at a prevalence of 2.6%.4 Our finding (4%) is similar, but this parasite has been detected only in the stabled horses and not in the grazing animals. Horse helminthes are commonly studied post mortem using autopsy methods, an approach that allows species identification.14 However, necropsy studies have limitations, such as high cost, and horse examination at abattoirs often deal with old animals with low parasitic burdens and diverse or unknown grazing histories.15 Furthermore, the investigation of intestinal parasite communities of valuable brood horses, in a representative sample, by autopsy methods is almost impossible.16 For this reason, examination of intestinal helminthes of horses has been conducted after deworming, using highly effective modern anthelmintic drugs. This method enables the collection and identification of all luminal stages of the intestinal nematodes.15,16 Finally, more sensitive molecular methods, such as polymerase chain reaction, may be used in combination with others described
0 2 (2.7) 2 (0.9)
0 1 (1.4) 1 (0.4)
9 (6) 0 9 (4.0)
7 (4.7) 9 (12.3) 16 (7.2)
for the identification of some species of encysted larval cyathostomes . ACKNOWLEDGMENT The authors thank Professor Richard Wall (Bristol, UK) for comments on the manuscript. REFERENCES 1. Soulsby EJL. Helminths, arthropods and protozoa of domesticated animals. Philadelphia: Lea and Febiger; 1982. 2. Taylor MA, Coop RL, Wall RL. Veterinary parasitology. Oxford, UK: Blackwell Publishing; 2007. 3. Himonas CA. Fecal survey on the helminthiasis of equines. Hellenic Vet 1968;4:239–248. 4. Sotiraki S, Badouvas A, Himonas C. A survey on the prevalence of internal parasites of equines in Macedonia and Thessalia-Greece. J Equine Vet Sci 1997;17:550–552. 5. Piekarski G. Medizinische parasitologie in Tafeln. Berlin: Springer Verlag; 1973. 6. Truant AL, Elliott SH, Kelly MT, Smith JH. Comparison of formalinethylether sedimentation, formalin-ethyl acetate sedimentation, and zinc sulfate flotation techniques for detection of intestinal parasites. J Clin Microbiol 1981;13:882–884. 7. Visvesvara GS, Moura H, Kovasc-Nace E, Wallace S, Eberhard ML. Uniform staining of Cyclospora oocysts in fecal smears by a modified safranin technique with microwave heating. J Clin Microbiol 1997; 35:730–733. 8. Kornas S, Nowosad B, Skalska M, Boloz T. Intestinal parasites infection of horses from riding clubs in Krakow area. Wiad Parazytol 2004; 50:323–327. 9. Klei TR. Equine immunity to parasites. Vet Clin North Am Equine Pract 2000;16:69–78. 10. Osterman Lind E, Hoglund J, Ljungstrom BL, Nilsson O, Uggla A. A field survey on the distribution of strongyle infections of horses in Sweden and factors affecting faecal egg counts. Equine Vet J 1999; 31:68–72. 11. Himonas C, Antoniadou-Sotiriadou K, Sotiraki S, Papazahariadou M. Intestinal protozoa of animals in Macedonia. Bull Hell Vet Med Soc 1998;49:300–306. 12. Majewska AC, Solarczyk P, Tamang L, Graczyk TK. Equine Cryptosporidium parvum infections in western Poland. Parasitol Res 2004; 93:274–278.
236
M Papazahariadou et al Vol 29, No 4 (2009)
13. Epe C, Coati N, Schnieder T. Results of parasitological examinations
15. Osterman Lind E, Eysker M, Nilsson O, Uggla A, Hoglund J. Expulsion
of faecal samples from horses, ruminats, dogs, cats, hedgehogs and
of small strongyle nematodes (cyathostomin spp) following deworming
rabbits between 1998 and 2002. Dtsch Tierarztl Wochenschr 2004;111:243–247.
of horses on a stud farm Sweden. Vet Parasitol 2003;115:289–299. 16. Kuzmina TA, Kharchenko VA, Starovir AI, Dvojnos GM. Analysis of
14. Bucknell DG, Gasser RB, Beveridge I. The prevalence and epidemi-
the strongylid nematodes (Nematoda: Strongylidae) community af-
ology of gastrointestinal parasites of horses in Victoria. Austr Int J
ter deworming of brood horses in Ukraine. Vet Parasitol 2005;
Parasitol 1995;25:711–724.
131:283–290.