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Parasitic diseases of equids in Iran (1931–2020): a literature review

Abstract

Parasitic infections can cause many respiratory, digestive and other diseases and contribute to some performance conditions in equids. However, knowledge on the biodiversity of parasites of equids in Iran is still limited. The present review covers all the information about parasitic diseases of horses, donkeys, mules and wild asses in Iran published as articles in Iranian and international journals, dissertations and congress papers from 1931 to July 2020. Parasites so far described in Iranian equids include species of 9 genera of the Protozoa (Trypanosoma, Giardia, Eimeria, Klossiella, Cryptosporidium, Toxoplasma, Neospora, Theileria and Babesia), 50 helminth species from the digestive system (i.e., 2 trematodes, 3 cestodes and 37 nematodes) and from other organs (i.e., Schistosoma turkestanica, Echinococcus granulosus, Dictyocaulus arnfieldi, Parafilaria multipapillosa, Setaria equina and 3 Onchocerca spp.). Furthermore, 16 species of hard ticks, 3 mite species causing mange, 2 lice species, and larvae of 4 Gastrophilus species and Hippobosca equina have been reported from equids in Iran. Archeoparasitological findings in coprolites of equids include Fasciola hepatica, Oxyuris equi, Anoplocephala spp. and intestinal strongyles. Parasitic diseases are important issues in terms of animal welfare, economics and public health; however, parasites and parasitic diseases of equines have not received adequate attention compared with ruminants and camels in Iran. The present review highlights the knowledge gaps related to equines about the presence, species, genotypes and subtypes of Neospora hughesi, Sarcocystis spp., Trichinella spp., Cryptosporidium spp., Giardia duodenalis, Blastocystis and microsporidia. Identification of ticks vectoring pathogenic parasites, bacteria and viruses has received little attention, too. The efficacy of common horse wormers also needs to be evaluated systematically.

Background

Horses were tamed and brought to Iran by the Aryans around 3000 years ago [1, 2]. In ancient Iran, the institutions for the treatment and care of animals and humans are similar, and sometimes the same person was responsible for treating both humans and animals. Ancient Iranians considered horses the most important animals, and ruminants were less so [2]. The great impact of horses was related to their use in guarding frontiers and in conquests [3]. Several infectious diseases were known to early veterinarians in Iran [2]. In his comprehensive book on horse medicine (al-Furusiyah wa-al-Baytariyah, in English: Equestrian and Veterinary Services), Ibn Akhi Hozam (died circa 842 A.D.), one of the most authoritative figures in Iranian veterinary literature, described the characteristics, habits and diseases of horses as well as treatment methods with a focus on mange mite infestation and itching in horses and its transmission to humans. Another scientist, Ali ibn Dawud (died circa 1363), described gastrointestinal helminthiases of horses in his book Al-aqwal al-Kafiyah wa-al-Fusul al-Shafiyah fī al-Khayl (in English: Enough Words and Treatment Classes in Horses) [4].

Modern veterinary knowledge found its way into Iran during the 1850s via European veterinarians who were mainly in charge of royal stables and military services [5]. However, the first record of veterinary parasitology activities in Iran is the 1931 report by Carpentier who diagnosed Trypanosoma evansi in the blood of sick horses in southern Iran [6]. Since the 1930s, Iranian veterinarians have been trained in faculties of veterinary medicine in Iran and have conducted modern veterinary parasitology research.

There is no updated official report on the population of equines in Iran; however, according to the Equestrian Federation of Iran, about 25,000 certified horses of different breeds such as Arabian, Turkmen, Thoroughbred, Darehshori, Kurd and Caspian are distributed throughout the country (H. Katebi, personal communication). Although there are numerous donkeys, working horses and mules in Iran, no information about their populations could be obtained from the Ministry of Agriculture or from the Veterinary Organization. In this article, we review the published research on equine parasites in Iran from 1931 to July 2020. For this purpose we checked all available documents on each of the search terms which included a combination of Iran or Iranian (in Persian, English and French) with each of the generic names of the parasites of equids as mentioned in the reference book “Veterinary Parasitology” [7], the “Handbook of Equine Parasite Control” [8] and checklist of strongylid parasites [9]. The databases and search engines employed for the present literature review were those of PubMed (www.pubmed.gov), Google (www.google.com), Scientific Information Database of Iran (www.sid.ir), the collection of defended theses at all Iranian universities (https://irandoc.ac.ir/) and the collection of proceedings of Iranian scientific congresses on veterinary medicine, animal science and parasitology (https://www.civilica.com/). Valid names of the reported parasites in older literature were obtained from updated resources [9, 10]. The abstract of present literature review in Persian language is provided as an Additional file 1.

Protozoan infections

Trypanosomosis

Trypanosoma evansi is one of the most pathogenic and economically important protozoan parasites of horses. The disease called “surra” in the acute form is characterized by symptoms such as fluctuating fever, weakness, lethargy, anemia, severe weight loss, transient local or general cutaneous eruption, petechial hemorrhages on the eyelids, vulvar and vaginal mucosa, hemorrhages into the anterior chamber of the eye, abortion, alteration of locomotion and edema."Chronic manifestations include a progressive weight loss (described as “living skeletons”), loss of appetite and emaciation accompanied by jaundice and highly colored urine [11].

Infection with T. evansi has been reported in horses, donkeys and mules in different countries in Asia, Africa, South America and Europe [12]. Trypanosoma evansi is now considered as an emerging zoonotic parasite [13]. Trypanosoma was first reported in Iran in 1876 and was known to be fatal for horses [14]. After massive mortality of > 3000 horses in 1930 in the south of Iran, T. evansi was diagnosed in the blood of diseased animals [6]. In 1935, an outbreak of surra occurred in camels in the surroundings of Tehran [15]. Experimental infection of horse and donkey with T. evansi isolated from an infected camel caused disease after an incubation period of 6 days but the animals could survive after 40 days by the end of the experiment [15, 16]. Although infection rates of up to 19.47% for Trypanosoma spp. infections have been reported in camels from different regions of the country [17], there are few reports on T. evansi infection in equids. Trypanosoma evansi was diagnosed in two outbreaks of surra in mules in Dezfoul in 1961 and in horses in Kharameh in 1993 [18]. Association of T. evansi infection in a mare with abortion in Shiraz has also been documented [19]. Since Iran does not lie within the tsetse belt, trypomastigotes in animals have usually been assigned to T. evansi according to their morphological and morphometric features upon microscopic examination. Trypanosoma spp. were not detected in the only PCR-based study on 116 horses, donkeys and mules from six geographical regions in Iran [20]. Although no study has been conducted to define vectors of T. evansi in the country, reports of natural infections with T. evansi in camels [21], dogs [22] and water buffalo [23] with no history of travel show that non-cyclic transmission occurs.

Trypanosoma equiperdum is another important veterinary trypanosome infecting equids. Dourine is a disease caused by this species and is endemic in Africa and Asia; it is also found in the Middle East, southeastern Europe and South America. Trypanosoma equiperdum is the only trypanosome with transmission occurring during copulation of horses. However, experimental infections inoculating parasites via the intravenous or intraperitoneal route indicate that mechanical transmission by blood-feeding flies cannot be excluded as a possible route [24]. The infection presents with typical edema of the genital organs as well as weakness, emaciation, urethral discharge, characteristic plaques in the skin and neurological symptoms such as lack of coordination of the hind legs. Dourine in horses is generally fatal without treatment but is usually subclinical in donkeys and mules [25]. In Iran, dourine and its chemical treatment have been reported by veterinarians in southern and western areas since the 1930s. As in the 1940s in Iran, suramin (Naganol), arsphenamine (Salvarsan), Neosalvarsan and other common medications were extremely expensive, new treatment protocols with oral arsenic and orpiment accompanied by intravenous injection of tamsulosin or oral arsenic accompanied by intra-arterial injection of Suramin were developed [26]. Trypanosoma equiperdum has been isolated only once in Iran [27]. In one study on 119 equids (75 horses and 44 donkeys and mules) in Gonbad region, north of Iran, T. equiperdum was not detected in blood smears, but using mercuric chloride and formol gel tests 48% of horses and 77.27% of donkeys and mules were positive for the infection [28]. In Fars Province, 16 equids (10 stallions, 5 mares and 1 male donkey) were suspected to be infected with T. equiperdum according to their clinical characteristics such as edema in the genital organs and paraphimosis in stallions and cutaneous plaques with skin thicknesses on the neck and chest in mares, though no Trypanosoma was observed in clinical samples [29]. In a single case report, T. equiperdum was detected microscopically in a genitalia wash of a stallion from the southeast of Iran [30].

Giardiosis

There are very few data on Giardia duodenalis in horses although the parasite is commonly found in feces of asymptomatic animals. Although uncommon, giardiosis in horses has been found to be associated with diarrhea, a poor hair coat, ill thrift and weight loss. Assemblages A, B and E have been identified in horses [31]. All of these assemblages are pathogenic for humans so horses could represent a reservoir of G. duodenalis with the potential to cause disease in humans through direct contact or by contamination of food and/or water supplies.

There are only two reports on Giardia infection in horses in Iran. In one study from Ahvaz (southwestern Iran), trichrome-stained fecal smears of 100 racing horses of different ages were studied microscopically and 40% were found infected with cysts of Giardia [32]. In another study conducted in the same region, 35.7% of the fecal samples of Arabian horses (n = 42) were molecularly positive for G. duodenalis. Assemblages E and AI were the most prevalent [33].

Coccidiosis (Eimeria lueckarti and Klossiella equi)

Until recently, there was confusion concerning the etiological identity of Eimeria species in equids. A comprehensive examination of samples and literature in 2018 led to the recognition of E. leuckarti as the only valid species of Eimeria in equids, which has been consistently found in numerous surveys worldwide [34]. Eimeria leuckarti infects the horse (Equus caballus), donkey (Equus asinus), mule (Equus mulus), Asian wild ass (Equus hemionus), Mountain zebra (Equus zebra) and Grant’s zebra (Equus quagga). Infections are more common in foals than in adult animals. Foals can acquire infection on the day of birth, probably from the contaminated environment rather than from oocysts excreted by their mares. Most infections are considered coincidental or without clinical relevance, although enteritis has been reported in a few cases [34]. In Iran, there are few reports on eimeriosis in equids with infection rates of 0.5–57.14% in horses [35,36,37,38,39] and 7.7% in donkeys [36]. As many other researchers who performed coproscopy did not report Eimeria oocysts in fecal examinations, it seems that eimeriosis is not common in the country considering that equines in Iran are not treated with coccidiostatic and coccidiocidal compounds.

There is also one report of Klossiella equi, a rare coccidian parasite of the renal parenchyma of equids with no clinical signs in the kidneys associated with this parasite [40]. In 2011, different developmental stages of the parasite were observed in histopathological study of renal sections of a 10-year-old donkey (Equus asinus asinus) [41].

Cryptosporidiosis

Cryptosporidium spp., gregarines that infect a wide range of vertebrates, are the causative agents of zoonotic infections associated with food- and waterborne outbreaks [42]. Cryptosporidium spp. have a fecal-oral transmission route and induce a self-limiting disease in immunocompetent individuals, but it may cause a debilitating infection with typical aqueous diarrhea and weight loss in infants, young animals and immunocompromised individuals [43]. In equines, clinical manifestations are rare; however, generally the pathogenicity of Cryptosporidium spp. depends on both the genetic background and immune status of the animals and the virulence of the specific genotypes and subtypes involved [44]. In horses and donkeys Cryptosporidium horse genotype, C. parvum and C. hominis are responsible for > 90% of infections. Cryptosporidium andersoni and C. muris have been reported in at least five cases while C. tyzzeri, C. felis, C. erinacei, C. proliferans and C. ryanae have each been reported in fewer than five animals [45,46,47]. All of these species and genotypes except C. proliferans have been reported in humans [48]. In Iran infection rates of 2.0–26.7% in horses and mules of different regions have been reported (Table 1). There are also two reports of possible transmission of Cryptosporidium to humans related with them [49, 50]. However, all of the studies on equine cryptosporidiosis were based on microscopic examination of Ziehl-Neelsen-stained fecal smears.

Table 1. Prevalence rates of Cryptosporidium spp. in equids in Iran

Toxoplasmosis

Toxoplasma gondii is an obligate intracellular protozoan parasite that can infect an exceptionally wide range of warm- and cold-blooded animals as well as humans making it one of the most widespread parasites on earth [59]. Approximately 30% of the world’s population is infected with this cosmopolitan food- and water-borne parasite [60].

In equids worldwide, T. gondii has been detected by both indirect (serology) and direct (PCR, mouse bioassay) tests although there is no confirmed report of clinical toxoplasmosis in horses suggesting that they might be resistant to toxoplasmosis [61]. Several epizootiological studies have been conducted for the detection of anti-Toxoplasma antibodies in blood serum of horses and donkeys from Iran (Table 2). There is also one research article on detection of T. gondii in blood samples by PCR-RFLP in Urmia Province. In that work, 2 of 126 horses (1.6%) tested positive [62]. Accordingly, eating raw horse meat may expose consumers to T. gondii [63] with severe cases of human toxoplasmosis reported in France due to the consumption of imported South American and North American horsemeat contaminated with highly pathogenic strains of the parasite [64]. However, as meat of equids is not consumed in Iran because of cultural and religious beliefs, horses and donkeys might not play a significant role in the epidemiology of human infections in the country. Furthermore, it has been shown that drinking raw milk of livestock can pose a risk to humans [65]. As consumption of milk of horses and donkeys has recently become popular in the country, proper thermal treatment of milk should receive more consideration.

Table 2. Seroprevalence of T. gondii antibodies in blood serum of equids in Iran

Neosporosis

Horses are known to be intermediate hosts of Neospora hughesi, which seems to represent a species different from N. caninum. Neospora hughesi causes myeloencephalitis, forming tissue cysts smaller than those of N. caninum with thinner cyst walls and smaller bradyzoites [76]. It is, however, not clear whether N. hughesi is the sole species of Neospora that infects horses. Despite the antigenic and molecular differences between the two species [77], N. caninum tachyzoites were used as antigens in all serological prevalence studies on horses and donkeys in Iran. In these studies, seroprevalences of 20.0–40.8% in horses [73, 78,79,80,81] and 52% in the only study on donkeys were reported [81].

Piroplasmosis (Theileria equi and Babesia caballi)

Equine piroplasmosis, caused by two hemoprotozoan apicomplexan parasites (Theileria equi and Babesia caballi), is a tick-borne disease of horses, mules, donkeys and zebras that has also been reported in dogs and dromedary camels, therefore raising doubts about piroplasm host specificity [82, 83]. At least 33 ixodid species within the genera Hyalomma, Dermacentor, Rhipicephalus, Ixodes, Amblyomma and Haemaphysalis have been implicated as competent vectors for B. caballi, T. equi or both [84]. In endemic areas, there are no overt clinical signs of infection but clinical disease can manifest in different forms as subacute or chronic [85]. Acute disease may also occur and is characterized by fever (temperature > 40 °C), malaise, reduced appetite, anorexia, constipation followed by diarrhea, tachycardia, tachypnea, petechiae, splenomegaly, thrombocytopenia and hemolytic anemia leading to hemoglobinuria and icterus [86].

Piroplasmosis was first reported in the Iranian literature in the 1930s when B. caballi was diagnosed in the blood smears of Hungarian mares imported to Iran [6]. It was not discovered whether the infection of these horses occurred in Iran or outside the country [87]. In the 1940s, microscopic and serological diagnosis of both B. caballi and T. equi (referred to as Piroplasma caballi and Nuttallia equi) were performed, and infected horses were treated with Gonacrine® (3,6-diamino-10-methylacridinium chloride; SPECIA, Paris, France), Trypaflavin® (acriflavine hydrochloride; Bayer, Leverkusen, Germany) and Acaprin® (quinuronium sulfate; Bayer, Leverkusen, Germany) [88, 89]. For almost 50 years there has been no report of piroplasmosis, but since 1992, and upon diagnosis of a horse with T. equi [90], research and reports have begun again. Although clinical disease with B. caballi and T. equi has been documented sporadically [91,92,93,94,95], epizootological studies (Table 3) show that both theileriosis and babesiosis are present all over the country, and infected horses, donkeys and mules are subclinically affected. Not much is known about ticks vectoring equine piroplasms but DNA of T. equi has been found in Hyalomma excavatum and Rhipicephalus bursa ticks collected from infected horses [96].

Table 3. Prevalence of Theileria equi and Babesia caballi in equids in Iran

Helminthoses

Nematodoses

Infections with strongylids (Nematoda: Strongylidae)

The nematode parasites of horses belong to 7 suborders, 12 families, 29 genera and 83 species. The majority (19 of 29 genera and 64 of 83 species) are members of the Strongylidae family, which includes the most common and pathogenic nematode parasites of horses [9]. Migratory strongylids (Strongylus vulgaris, Strongylus edentatus and Strongylus equinus commonly named “large strongyles”) occur in the large intestine. Clinically, these are the most important of the equine parasites with S. vulgaris considered a major threat to equine health. Large strongyles might cause severe pathological consequences and clinical signs, which differ depending on the species. On the other hand, non-migratory strongylids (commonly named “small strongyles”) include cyathostomins and non-migratory strongyline species such as Triodontophorus spp., Craterostomum spp. and Oesophagodontus spp., which are very common nematode parasites of equids. Non-migratory strongylids are considered much less pathogenic; however, many of these worms may damage the intestinal mucosa and result in emaciation and diarrhea, which is sometimes accompanied by colic, weight loss, fever and even death [8, 9, 114].

In Iran, infection of equids with large and small strongyles has commonly been reported in horses, donkeys and mules following coproscopic examinations or fecal culture under general terms such as “Strongylus spp. eggs,” Strongylus spp. larvae,” “cyathostomins eggs” and “cyathostomins larvae.” Infection rates between 4.4 and 69.2% in horses [35,36,37, 114,115,116,117,118,119,120,121,122,123,124,125,127], 65.4 and 96.4% in four studies on donkeys [36, 117, 128, 129] and 80% in the only study on mules [117] have been reported.

Based on necropsies, 27 species of strongylids from 10 genera have been recorded in Iran. In some instances, the species names were corrected according to the checklist of Lichtenfels et al. [9]. Based on our intensive searches, the strongylid fauna of horses and donkeys in Iran consists of members of the genera Strongylus (n = 3), Oesophagodontus (n = 1), Triodontophorus (n = 3), Cyathostomum (n = 4), Coronocyclus (n = 3), Cylicodontophorus (n = 1), Cylicocyclus (n = 5), Cylicostephanus (n = 5), Gyalocephalus (n = 1) and Poteriostomum (n = 1) (Table 4).

Table 4 Strongylinae and cyathostominae species recovered from horses and donkeys in Iran

Parascariosis (Parascaris equorum and Parascaris univalens)

Parascaris spp. reside in the small intestine of equids and are one of the largest known parasitic nematode species measuring up to 50 cm in length at the adult stage. Following ingestion of the third-stage larva (L3) within the egg, larvae are released and penetrate the small intestinal wall to begin a somatic migration via the bloodstream through the liver, heart and lungs. Then, the larvae migrate proximally in the pulmonary tree or are coughed up into the pharynx where they are swallowed and return to the stomach and small intestine, growing progressively to adult ascarids [8, 114].

The tradition in veterinary parasitology has been to refer to one equine ascarid species, Parascaris equorum. However, the published literature contains scant mention of a cryptic ascarid species infecting horses, named Parascaris univalens [141142], which is the dominating species infecting horses in Sweden, Switzerland and the USA, and possibly globally [143]. A sequence of the mitochondrial cytochrome c oxidase subunit 2 (cox2) gene (GenBank: MG676884) from Iranian isolates shows > 99% identity with sequences for both P. equorum and P. univalens available on GenBank [144]. As P. equorum and P. univalens are notoriously difficult to distinguish morphologically and their mitochondrial DNA genomes are very similar [145], cytological analysis of chromosome organization and the phenomenon of “chromatin diminution” [P. univalens (2n = 2) and P. equorum (2n = 4)] is the only established technique for differentiating these two species [146]. Since none of the reports of P. equorum in Iran were accompanied by karyotyping, we use Parascaris spp. in this article.

Infection of horses with Parascaris spp. is a common infection in equids, and prevalences of 12.2–40.0% in horses [35, 36, 115, 116, 118, 121,122,123,124,126, 133, 136, 147, 148] and 3.8–20.0% in three studies on donkeys [36, 117, 129] have been reported. Karyotyping of Parascaris spp. of equids in Iran will shed light on the distribution of P. univalens and P. equorum in the country.

Pinworm infections (Oxyuris equi and Probstmayria vivipara)

Nematodes of the Oxyuroidea, or pinworms, reside in the posterior alimentary tract. Oxyuris equi, the common pinworm of the equids, is rarely considered a major threat to equine health, but heavy infections may result in fatigue, decreased performance and loss of body condition. However, females of O. equi protrude from the anus and deposit eggs in a sticky film in the perineal area that becomes irritating to the host when the proteinaceous fluid dries. Consequently, horses rub their tail heads and rumps against fixed objects, causing local damage to the skin, haircoat and tail [8, 114]. Probstmayria vivipara, a less well-known pinworm species of equids, can complete its life cycle without leaving the host. Probstmayria vivipara is only detectable microscopically and is not known to be pathogenic to the horse even though populations may number in the hundreds of thousands [8]. In Iran, eggs and adults of O. equi have been reported (mostly in fecal egg count) in horses [35, 37, 115, 116, 118, 122, 124, 136, 148] and donkeys [36, 131, 148]. Probstmayria vivipara, however, has only been reported in necropsied donkeys with > 500,000 worms collected from a single animal [131, 149].

Stomach worm infections (Habronema spp. and Draschia spp.)

Equid habronemosis is a widespread parasitic disease caused by three species of spirurid nematodes that reside as adults in the stomach, Habronema microstoma (the most common), Habronema muscae and Draschia megastoma. Habronemosis causes mild to severe clinical symptoms, i.e., gastric, cutaneous, mucocutaneous and pulmonary diseases, depending on the parasite’s stage of development and on localization. Their life cycle requires an intermediate host, represented by dung-inhabiting secretophagous or hematophagous muscid flies [150]. As the egg stages of Habronema and Draschia are quite small and might not survive the flotation process, the diagnosis is mainly based on necropsy findings. In Iran, since the first report of H. muscae in horses in 1966 [151], all three species of stomach worms have been reported from horses as either single or multiple infections [115, 136, 152,153,154]. Examination of 45 slaughtered donkeys in a study showed very high infection rates with H. muscae and H. microstoma (80% and 66.6%) while 13.3% of donkeys were infected with D. megastoma [131]. Ocular habronemosis in one horse with conjunctivitis and lacrimation [155] and also summer sore cases [156, 157] have been reported. Gastric infection of Persian onager (Equus hemionus onager) with H. muscae has been documented, too [158].

Trichurosis

Equids are not common hosts for Trichuris species, but there are a few reports of detection of parasite eggs from Iran, specifically in fecal examinations of two horses, two donkeys and one mule [117]. Infection of horses, donkeys and mules has also been reported from Turkey [159, 160]. Almost 40 years ago adult male and female T. suis were isolated from the cecum and colon of a dead horse [161]. However, there is no other report on finding adult whipworm nematodes in equids.

Lungworm infections

Dictyocaulus arnfieldi infects the respiratory tract of equids worldwide [8]. Donkeys are more suitable hosts of D. arnfieldi than horses as donkeys can tolerate large numbers of parasites with few clinical signs of overt respiratory disease [162]. In a comparative study, the prevalence of the infection was 65% in donkeys, 22.72% in mules and 4.54% in horses, and the mean intensity was 34.3 worms in donkeys, 36.5 in mules and 2.0 in horses [163]. In Iran, eggs and larvae of D. arnfieldi have been examined in feces of horses, donkeys and mules [37, 164, 165] but few scientific data are available.

Threadworm infections

Female Strongyloides westeri nematodes parasitize the small intestine of equids. The infection is mainly observed in suckling foals, but older horses are occasionally found infected as well. Infection occurs via skin penetration by third-stage larvae, ingestion of third-stage larvae from a contaminated environment or lactogenic transmission from the mare. Equine strongyloidosis is recognized as a rare cause of disease [166]. Adult S. westeri nematodes in horses [115] and eggs or larvae in feces of horses [125, 167] and donkeys have been reported in Iran [129, 148].

Trichostrongylosis

Trichostrongylus axei is the only gastrointestinal nematode that equines share with ruminants via cross-infection. This parasite occurs in the abomasum of sheep, cattle, goats and camels in Iran [167,168,170]. Infection of human patients with T. axei has also been reported [171]. Adult nematodes have been isolated from horses [115] and donkeys [128, 131]. There are also some reports on detection of eggs of T. axei in coproscopic examinations in horses [125, 172], donkeys and mules [172]. However, eggs of T. axei are morphologically indistinguishable from those of the other intestinal strongyles, and differentiation requires fecal culture [114]. As coproculture was not performed in the latter studies, the results remain dubious.

Filarioidean infections (Parafilaria spp., Onchocerca spp. and Setaria spp.)

Adult Parafilaria multipapillosa occurs in subcutaneous and intermuscular connective tissue of equines. Nodules form in the overlying skin, and the nodules may rupture and bleed or leak tissue fluids [8]. In Iran, microfilariae of P. multipapillosa have been reported in peripheral blood samples [173,174,175] and embryonated eggs and/or microfilariae from hemorrhagic discharges of skin nodules [176] of horses and donkeys. The enzootic areas for P. multipapillosa are the Caspian littoral, steppes and forest steppes with temperate-wet climate and altitudes of up to 1500 m [176].

Regarding the Onchocerca species, infection of equids with four species of Onchocerca, i.e., O. reticulata, O. cervicalis, O. raillieti and O. boehmi (syn. Elaeophora boehmi), have been reported [177]. Adult nematodes are found deep in the connective tissues such as in the nuchal ligament area and the distal limbs [8]. In Iran, microfilariae of O. reticulata, O. cervicalis and O. boehmi have been examined in peripheral blood samples of horses and donkeys [173, 175, 178]. However, so far there is no report on Onchocerca nodules in equids in the country.

Setaria equina is a filarioid nematode that lives free in the abdominal cavity of equids. Equine setariosis is considered non-pathogenic in most cases although serious pathogenic effects could occur when they reside in unusual habitats such as the eye, brain, spinal medulla and testicles of horses [179]. In Iran, microfilariae of S. equina have been examined in peripheral blood [175, 178], and adults have been isolated from the abdominal cavity of donkeys [131], in the testicles of one horse [180], in the cecum and colon of two horses [130] and eyes of two horses [181]. There is also one report of subconjunctival setariosis due to S. equina in a 15-year-old girl in Tabriz, a city in the northwest of the country [182].

Eyeworm infections

Horses are the definitive hosts of Thelazia lacrymalis and T. rhodesi transmitted by many species of muscid face flies according to the geographical distribution [183]. Adult worms usually reside in the conjunctival cul-de-sac, beneath the nictitating membrane, in excretory ducts of the Harderian gland, in the ducts of the lacrimal glands or rarely free in the conjunctiva [184]. Pathologies range from no gross lesions to mild conjunctivitis, photophobia and lacrimation up to severe lesions such as keratitis and in some chronic cases corneal ulceration [185]. Eyeworm infections of equids have not received any attention in Iran. In an old document, the author mentioned one case of T. rhodesi infection in a horse from Babol, northern Iran [186]. However, in a study on ophthalmic diseases of 901 horses in Tehran, no eyeworms were reported [187]. In a report from 2014, eyeworms of one horse in the southeastern region of the country was diagnosed with T. lacrymalis [188]. As both species T. lacrymalis and T. rhodesi are endemic in several regions of Iran [189, 190], equine thelaziosis seem to be underdiagnosed.

Gullet worm infections

Gongylonema spp., also known as gullet worms, are globally distributed parasitic nematodes that reside in the upper digestive tract of a wide range of domestic and wild mammals [191]. Although human infections with this nematode are rare, over 60 cases have been reported worldwide [192]. In Iran, Gongylonema spp. have been diagnosed in cattle, sheep, buffalo, goats, camels, wild boars and a human patient [170, 193, 194] and are reported as G. pulchrum by tradition. In the only report from equines of Iran, Gongylonema spp. was diagnosed in the esophagus and stomach of a donkey [195]. Gongylonemosis has long been known to occur in horses and donkeys [196]. However, recent separation of G. nepalensis from G. pulchrum (which is almost identical in morphology except for distinctly shorter left spicules) in addition to reports of infection in buffaloes, cattle, sheep, goats, wild European mouflons and a red fox [191] would suggest that equids can also be hosts for G. nepalensis.

Cestodosis

Tapeworm infections (Anoplocephala perfoliata and Anoplocephala magna)

Anoplocephalid cestodes occur worldwide and are potential causes of various forms of colic. These tapeworms utilize intermediate hosts, comprising numerous species of oribatid mites ingested accidentally by horses during grazing. Three species of cestodes, i.e., Anoplocephala perfoliata, A. magna and Anoplocephaloides mamillana, are known to infect equids; A. perfoliata is by far the most prevalent [197]. In Iran, the two Anoplocephala species have been reported in horses [115, 130, 198] and donkeys [131, 199]. Eggs of Anoplocephala spp. have also been detected in feces of horses [35, 37, 125] though identification was not performed except for one study reporting the eggs as A. perfoliata [200].

Hydatidosis (Echinococcus spp.)

In equines cystic echinococcosis (CE) is generally a rare finding, mostly incidentally diagnosed at slaughter or postmortem examination. The hydatid cysts commonly develop in the liver and lungs. The cysts have a reported longevity of several years and rarely cause severe clinical symptoms [201]. Cases of equine cystic hydatidosis have been reported from Europe, the Middle East, South and East Africa, North America and Southeast Asia [202]. In many of these cases, the identity of the causative Echinococcus taxon was not confirmed [203]. It is assumed that E. equinus (horse strain/G4) is the only species that produces fertile cysts in equines whereas the recovery of small sterile cysts of E. granulosus in horses confirms that the horse is not an efficient host for this species [204]. Echinococcus equinus is probably not infective to humans [205]. Cystic echinococcosis is hyperendemic in Iran, and occurrence of E. granulosus (G1–G3), E. ortleppi (G5) and E. intermedius (G6/7) in dogs, humans and livestock, i.e., sheep, goats, cattle and camels, is extensively reported [206]. Regarding infection of equids, however, hydatidosis has not received adequate attention, and only three articles are available. In serodiagnosis of hydatidosis in horses, only 6 sera of 193 samples (3.11%) tested positive [207]. In donkeys, it can be concluded that both E. granulosus and E. equinus are present. In a study in 1987, the authors stated that hydatid cysts in the lungs of two donkeys did not have protoscolices [199] but in 2014 hydatid cysts in the liver of one infected animal harbored protoscolices with morphological characteristics consistent with previous descriptions in Switzerland and Jordan [208]. In the latter study, nucleotide sequences of a partial sequence of cox1 from donkey were similar to the corresponding sequence of E. equinus in GenBank [208]. Dogs, black-backed jackals (Canis mesomelas) and interestingly lions (Panthera leo) have been identified as definitive hosts of E. equinus [209]. So far, E. equinus has not been recorded in the canine in Iran [206].

Trematodosis

Liver fluke infections (Fasciola spp. and Dicrocoelium spp.)

Horses and donkeys can acquire infection with both Fasciola hepatica and F. gigantica in their liver [210, 211]. Infected horses with liver flukes show clinical signs including poor performance, fatigue, diarrhea, inappetence and jaundice [212]. Very recently failure to establish infection of horses after oral challenge with metacercariae raised fundamental questions on the pathophysiology and epidemiology of equine fasciolosis [213]. In Iran, eggs of Fasciola spp. have been found in feces of horses with a prevalence of 3–50% [35, 136, 214, 215], and adult F. hepatica flukes have been isolated from bile ducts of donkeys [131, 199].

Dicrocoeliosis is caused by several Dicrocoelium spp. that live in the bile ducts and gall bladder of domestic and wild ruminants but occasionally affect other animals including horses and humans [216]. In Iran, eggs of Dicrocoelium spp. have been reported from 1 to 33.3% of horses [122, 125, 136]. Adult flukes have also been isolated from livers of 6.7% of donkeys in two studies [131, 199]. Equine hepatic Dicrocoelium dendriticum infection has also been reported from Azerbaijan, Turkey, Denmark, Nigeria, Switzerland and Canada [217, 218]. However, there is no information regarding the clinical effect of the lancet fluke in equids due to lack of experimental infections. Furthermore, although D. dendriticum is the most widespread liver fluke worldwide, special care must be taken for reporting Dicrocoelium spp. eggs in feces as eggs of D. dendriticum, D. suppereri and D. hospes are similar morphologically [219, 220].

Schistosomosis

Horses, donkeys and mules are susceptible to a wide range of schistosomes, e.g., S. bovis, S. japonicum, S. indicum, S. nasale, S. spindale and Heterobilharzia americana [220,221,222,224]. In Iran, where S. turkestanica is endemic, the infection has been reported from cattle, sheep, goats, buffaloes and camels in addition to causing cercarial dermatitis in humans [225, 226]. An article dated 1973 mentioned that one donkey in southwestern Khuzestan was found infected with a few S. turkestanica worms and concluded that donkeys were not important hosts for this parasite [227]. After almost 35 years of no report, eggs of S. turkestanica were detected in feces of two horses in northwestern Iran [125].

Arthropod infections

Tick infestation

Ticks play a vital role in the stable maintenance and natural transmission of several equine-infective tick-borne pathogens, including protozoa (e.g., T. equi, B. caballi) [84], bacteria (e.g., Anaplasma phagocytophilum, Borrelia burgdorferi, Coxiella burnetii, Rickettsia spp.) [228,229,230,231,232] and viruses (e.g., Crimean-Congo hemorrhagic fever virus) [233]. In Iran so far 16 species of the Ixodidae (hard ticks) from five genera (Ixodes, Haemaphysalis, Rhipicephalus, Dermacentor and Hyalomma) have been collected from horses, donkeys and mules (Table 5) [92, 96, 97, 233,234,235,236,237,238,239,240,241,242,244]. No species of the Argasidae (soft ticks) have been reported. As in older literature Hyalomma excavatum and Hyalomma turanicum were mentioned as subspecies of Hyalomma anatolicum and Hyalomma marginatum, we use the currently accepted name according to the most recent list of valid species names [245] although it is difficult to know exactly which species has been tested. The most commonly collected ticks from horses, donkeys and mules in different geographical regions of Iran are H. anatolicum, Rhipicephalus bursa and Rhipicephalus annulatus (Table 5).

Table 5. Tick species collected from horses, donkeys and mules in Iran

At least 33 ixodid species in the genera Hyalomma, Dermacentor, Rhipicephalus, Ixodes, Amblyomma and Haemaphysalis have been implicated as competent vectors for B. caballi, T. equi or both [84]. In the only study on molecular detection of piroplasms in ticks infesting horses in Iran, the salivary glands of H. excavatum and R. bursa scored positive for T. equi in PCR, but no tick contained B. caballi DNA [96]. There is no other published research on examination of pathogens in ticks from equines in the country, although, for instance, H. anatolicum, H. marginatum, R. bursa, R. sanguineus, H. asiaticum and H. dromedarii are the most frequent species of tick vectors for Crimean-Congo hemorrhagic fever (CCHF) virus in Iran [246]. Horses and donkeys are known to be susceptible to CCHF virus although there is no evidence that they develop any symptomatic disease [233]. More studies are needed to define the role of equines in the epidemiology of tick-borne diseases.

Mange mite infection

A variety of mites may infest equids. Sarcoptes scabiei var. equi (scabies and head mange), Chorioptes bovis (pastern mange), Psoroptes equi (body mange), Pyemotes tritici (straw itch mite) and Trombicula and Eutrombicula species (chiggers) are associated with pruritic equine skin diseases [247]. The prevalence of sarcoptic and psoroptic mange is very low among equines in Iran [248]. To date, Psoroptes equi [reported as Psoroptes communis var. equi (Hering)], Sarcoptes scabiei var. equi (Gerlach) and Chorioptes bovis have been isolated from horses in the country [249, 250].

Lice infestation

Two types of lice feed on equines. Chewing lice (Werneckiella equi and Bovicola (Werneckiella) ocellatus) feed on the epidermal debris and prefer the dorsolateral trunk while sucking lice (Haematopinus asini) feed on blood and tissue fluid and most commonly infest the mane, tail and fetlock region [247, 251]. In Iran, infestations with Haematopinus asini and Werneckiella equi (reported as Bovicola equi) among horses and donkeys are rarely seen in the southeast and northeast areas [249, 252].

Bot flies (Gasterophilus spp.)

The genus Gasterophilus (Oestridae, Gasterophilinae), known commonly as bot flies, include nine valid species [253]. Female flies attach eggs on the hair coat of equid hosts and larvae migrate to the oral cavity via different routes depending on the species. First-instar larvae reside in the mouth, but second- and third-instar larvae are found attached to the mucosa of different regions of the equid gastrointestinal tract, i.e., stomach, duodenum, colon or rectum. Generically, gasterophilosis is characterized by difficulties in swallowing (throat localization of the immature stages), gastric and intestinal ulcerations, gut obstructions or volvulus, rectal prolapse, anemia, diarrhea and digestive disorders [254]. In Iran four species of Gasterophilus (G. intestinalis, G. nasalis, G. pecorum and G. inermis) have been isolated from horses, donkeys, mules and Persian onagers [131, 158, 255,256,257,258]. Endoscopic examinations have shown that bot flies are causes of gastric ulcers in horses in northwestern Iran [259].

Equine ked infestation

Hippobosca equina, also known as “forest fly,” usually parasitizes horses but also bites cattle, dogs, red deer, camelids, rabbits and humans. Adult winged flies lay larvae in the environment, where they immediately pupate, and new winged adults hatch from pupae, starting host-seeking behavior [260]. Humans bitten by this ked species often require emergency treatment because of allergic reactions [261]. These keds are regarded as both mechanical and biological vectors of Corynebacterium pseudotuberculosis [262]. Although H. equina is known to occur in Iran [263], so far infestation of horses and mules has been reported from the south of the country [264].

Archeoparasitological findings

Since 2010 an international team has been studying the Iranian salt mine of Chehrabad, in the province of Zanjan, which was in operation under the Achaemenids (sixth to fourth century BC) and Sassanids (fourth to sixth century AD). Archeologists discovered the mummified remains of five miners who had been killed in a mining accident, and since then an extensive excavation has been initiated. Other than parasites of the mummies, Oxyuris equi eggs have been found in coprolites of equines in the site [265]. Furthermore, eggs of F. hepatica in coprolites of equids dating back to 224–651 AD [266], Anoplocephala spp. and strongyles eggs in equine coprolites [267] show that these parasites have been present in equids in Iran from ancient times.

Conclusions

The present review reflects the current state of knowledge on the parasitic fauna of equids in Iran. Parasites and parasitic diseases of equines have not received adequate attention compared with those of ruminants and camels. Regarding helminths, as horse meat is not consumed in Iran because of cultural and religious beliefs there are no slaughterhouse data. Furthermore, although donkeys were slaughtered and fed to zoo carnivores in the last decades and their parasite fauna could be evaluated, this practice stopped almost 10 years ago upon the Glanders outbreak in tigers and lions in Tehran Zoo [268]. Hence, there is a need for country-wide planning of careful examination of a limited number of horses and donkeys that are killed for educational purposes or die for various reasons. A collaboration among parasitologists, pathologists and field veterinarians will make this goal achievable. Infection of equids with eyeworms also has not received adequate attention although the two species T. lacrymalis and T. rhodesi are endemic in some parts of the country [189, 190]. Moreover, several outbreaks of trichinellosis were associated with consumption of horse meat [269] but there is no information on equines in Iran. Detection of protozoan infections has been focused mainly on serological studies of T. gondii and N. caninum. Further research is needed based on multilocus PCR-RFLP genotyping [270] to improve current understanding of the transmission dynamics of infected equines to people consuming their milk. Identification and genotyping of Cryptosporidium spp. and Giardia duodenalis as zoonotic hazards have been neglected. A possible presence of N. hughesi, Sarcocystis (S. neurona, S. bertrami and S. fayeri) [271] and potentially zoonotic Blastocytis [272] and microsporidia [273] in the country requires further investigations. Regarding ticks, our information about the presence of pathogens in ixodids is also limited to a single study while T. equi and B. caballi have been reported from almost all regions of the country. In the absence of anthelmintics for horses in the market in Iran, there is a lack of products labeled for use in horses with known pharmacokinetics and pharmacodynamics as well as safety levels. Extra-labeled products, e.g., fenbendazole suspensions and ivermectin solutions formulated for ruminants and mebendazole formulated for humans, are commonly administered to horses. Hence, examination of the efficacy of formulations specific for horses with benzimidazoles, tetrahydropyrimidines, macrocyclic lactones, piperazine and praziquantel is essential [274]. The gap in the production of horse wormers should be filled by domestic pharmaceutical companies.

Availability of data and materials

All data generated or analysed during this study are included in this published article.

Abbreviations

PCR:

Polymerase chain reaction

DNA:

Deoxyribonucleic acid

CCHF:

Crimean-Congo hemorrhagic fever

DT:

Dye test

MAT:

Modified agglutination test

IFAT:

Immunofluorescent antibody test

LAT:

Latex agglutination test

References

  1. 1.

    Schmitt R. 1987. ARYANS. Encyclopædia Iranica, II/7. https://www.iranicaonline.org/articles/aryans. Accessed 28 Aug 2020.

  2. 2.

    Tadjbakhsh H. Traditional methods used for controlling animal diseases in Iran. Rev Sci Tech. 1994;13:599–614.

    CAS  PubMed  Google Scholar 

  3. 3.

    Otranto D, Stevens JR, Brianti E, Dorchies P. Human and livestock migrations: a history of bot fly biodiversity in the Mediterranean region. Trends Parasitol. 2006;22:209–13.

    PubMed  Google Scholar 

  4. 4.

    Tadjbakhsh H. Ancient knowledge of parasitic diseases. J Vet Lab Res. 2012;4:5.

    Google Scholar 

  5. 5.

    Shaki M, Tājbaḵš Ḥ, Sajjādī Ṣ. 1993. DĀM PEZEŠKĪ (veterinary medicine). Encyclopaedia Iranica, VI/6. https://iranicaonline.org/articles/dam-pezeski-veterinary-medicine. Accessed 28 Aug 2020.

  6. 6.

    Carpentier G-A-L-E. Les services vétérinaires en Perse. Paris: Librairie Le François; 1931.

  7. 7.

    Taylor MA, Coop RL, Wall RL. Veterinary parasitology. 4th ed. Oxford: Wiley Blackwell; 2016.

    Google Scholar 

  8. 8.

    Nielsen MK, Reinemeyer CR. Handbook of equine parasite control. 2nd ed. Hoboken: Wiley Online Library; 2018.

    Google Scholar 

  9. 9.

    Lichtenfels JR, Kharchenko VA, Dvojnos GM. Illustrated identification keys to strongylid parasites (Strongylidae: Nematoda) of horses, zebras and asses (Equidae). Vet Parasitol. 2008;156:4–161.

    PubMed  Google Scholar 

  10. 10.

    GBIF.org. Global biodiversity information facility home page. 2020. https://www.gbif.org. Accessed 28 Aug 2020.

  11. 11.

    Desquesnes M, Holzmuller P, Lai DH, Dargantes A, Lun ZR, Jittaplapong S. Trypanosoma evansi and surra: a review and perspectives on origin, history, distribution, taxonomy, morphology, hosts, and pathogenic effects. BioMed Res Int. 2013;2013:194176.

    PubMed  PubMed Central  Google Scholar 

  12. 12.

    Aregawi WG, Agga GE, Abdi RD, Büscher P. Systematic review and meta-analysis on the global distribution, host range, and prevalence of Trypanosoma evansi. Parasit Vectors. 2019;12:67.

    PubMed  PubMed Central  Google Scholar 

  13. 13.

    Fong IW. New and emerging parasitic zoonoses. Cham: Springer International Publishing; 2017. p. 211–39.

    Google Scholar 

  14. 14.

    Lingard A. Report on horse surra. Bombay: Government Central Press; 1893.

    Google Scholar 

  15. 15.

    Delpy L, Rafyi A. La trypanosomiase du dromadaire en Iran, etude experimentale de Trypanosoma evansi (Steel, 1885). Arch Razi Inst. 1947;5:33–50.

    Google Scholar 

  16. 16.

    Shimi A. Study of Surra disease in Iran. DVM Thesis, University of Tehran, Iran; 1940.

  17. 17.

    Sazmand A, Joachim A. Parasitic diseases of camels in Iran (1931–2017)—a literature review. Parasite. 2017;24:21.

    PubMed  PubMed Central  Google Scholar 

  18. 18.

    Hashemi-Fesharaki R, Esmaeil-Nia K, Habibi GR, Sarkarzadeh P. Investigations on trypanosomosis in equine. In: Proceedings of the 1st national congress of equine health and diseases, 12th–14th November, 1996, Tehran, Iran; 1996. p. 60–1.

  19. 19.

    Badiei K, Ahmadi MR, Nazifi S. Equine trypanosomiasis (T. evansi): a case report associated with abortion. Iran Vet J. 1998;1:69–75.

    Google Scholar 

  20. 20.

    Mahzounieh M, Tahmasby H, Amiri-Dehcheshmeh J, Monji H. Molecular epidemiology of Trypanosoma in equids in Iran. Vet Res Biol Prod. 2012;99:20–4.

    Google Scholar 

  21. 21.

    Sazmand A, Eigner B, Mirzaei M, Hekmatimoghaddam S, Harl J, Duscher GG, et al. Molecular identification of hemoprotozoan parasites in camels (Camelus dromedarius) of Iran. Iran J Parasitol. 2016;11:568–73.

    PubMed  PubMed Central  Google Scholar 

  22. 22.

    Hosseininejad M, Shirani D, Nabian S, Nassiri SM, Mazaheri R. Trypanosoma evansi in three dogs in Iran. Comp Clin Pathol. 2006;16:69–71.

    Google Scholar 

  23. 23.

    Rocky A, Razi Jalali MH, Hajikolaei MRH, Hamidinejat H, Shirazi M. First report of infection of water buffalo with Trypanosoma evansi in Ahvaz city. In: Proceedings of the 2nd Iranian congress of veterinary pathobiology, 22nd–23th November, 2010, Garmsar, Iran; 2010.

  24. 24.

    Claes F, Büscher P, Touratier L, Goddeeris BM. Trypanosoma equiperdum: master of disguise or historical mistake? Trends Parasitol. 2005;21:316–21.

    CAS  Google Scholar 

  25. 25.

    Giordani F, Morrison LJ, Rowan TG, De Koning HP, Barrett MP. The animal trypanosomiases and their chemotherapy: a review. Parasitology. 2016;143:1862–89.

    PubMed  PubMed Central  Google Scholar 

  26. 26.

    Safvat-Safaei AH. Dourine. DVM Thesis, University of Tehran, Iran; 1937.

  27. 27.

    Khalili K. An investigation of dourine and isolation of Trypanosoma equiperdum in Iran. Arch Razi Inst. 1973;25:69–72.

    Google Scholar 

  28. 28.

    Mostafalo Y. Seroepidemiological study of dourine in equids. DVM Thesis, University of Tehran, Iran; 1990.

  29. 29.

    Dehghani S. Swollen testicles in horses (Dourine). In: 3rd convention of Iranian veterinary clinicians, 29th–31st October, 2002, Mashhad, Iran; 2002.

  30. 30.

    Anvari D, Firooz-Jahantighi F, Pishadast S, Hashemi SH. First report of Trypanosoma equiperdum infection of horse from Sarbaz city. In: Proceedings of the 3rd national congress of equine health and diseases, 29th April–1st May, 2015, Shiraz, Iran; 2015. p. 41.

  31. 31.

    Ryan U, Cacciò SM. Zoonotic potential of Giardia. Int J Parasitol. 2013;43:943–56.

    CAS  PubMed  Google Scholar 

  32. 32.

    Alizadehnia P. A survey on Giardia and Cryptosporidium in horses in Ahvaz. DVM Thesis, Shahid Chamran University of Ahvaz, Iran; 2010

  33. 33.

    Jafari H, Razi-Jalali M, Seyfiabad-Shapouri M, Haji-Hajikolaii M. Prevalence and genotyping of Giardia duodenalis among Arabian horses in Ahvaz, southwest of Iran. Arch Razi Inst. 2016;71:177–81.

    Google Scholar 

  34. 34.

    Dubey JP, Bauer C. A review of Eimeria infections in horses and other equids. Vet Parasitol. 2018;256:58–70.

    PubMed  Google Scholar 

  35. 35.

    Tavassoli M, Dalir-Naghadeh B, Esmaeili-Sani S. Prevalence of gastrointestinal parasites in working horses. Polish J Vet Sci. 2010;13:319–24.

    CAS  Google Scholar 

  36. 36.

    Karimi-Ghahfarrokhi E, Ahmadi A, Gholipour-Shahraki S, Azizi H. Eimeria leuckarti (Flesch, 1883; Reichenow, 1940) from worker horses and donkeys of Shahrekord, Iran. Int J Adv Biol Biomed Res. 2014;2:1980–4.

    Google Scholar 

  37. 37.

    Seif P. Prevalence of gastrointestinal parasitic helminthes in horses in Kermanshah city by stool examination. DVM Thesis, Razi University, Iran; 2016.

  38. 38.

    Sadeghi-Dehkordi Z, Sazmand A, Shahbazi R, Kiannejad M. Identification of gastrointestinal parasites in rural horses in Hamedan province. In: Proceedings of the 4th international congress and the 11th national congress of parasitology and parasitic diseases of Iran, 9th–11th October, 2019, Urmia, Iran; 2019. p. 228.

  39. 39.

    Chalechale A, Javedani M, Olfati S, Nikoosefat Z, Ferdowsian MM. Investigation of parasitic infection of the gastrointestinal tract of Darreh-Shouri breed horses in Shahreza county. In: Proceedings of the 3rd national congress of equine health and diseases, 29th April–1st May, Shiraz, Iran; 2015. p. 50.

  40. 40.

    Léveillé AN, Bland SK, Carlton K, Larouche CB, Kenney DG, Brouwer ER, et al. Klossiella equi infecting kidneys of Ontario horses: life cycle features and multilocus sequence-based genotyping confirm the genus Klossiella belongs in the Adeleorina (Apicomplexa: Coccidia). J Parasitol. 2019;105:29–40.

    PubMed  Google Scholar 

  41. 41.

    Rezaie A, Bahrami S, Ansari M. Klossiella equi in a donkey—a first case report from Iran. Trop Biomed. 2013;30:543–6.

    CAS  PubMed  Google Scholar 

  42. 42.

    Zahedi A, Paparini A, Jian F, Robertson I, Ryan U. Public health significance of zoonotic Cryptosporidium species in wildlife: critical insights into better drinking water management. Int J Parasitol Parasites Wildl. 2016;5:88–109.

    PubMed  Google Scholar 

  43. 43.

    Sazmand A, Rasooli A, Nouri M, Hamidinejat H, Hekmatimoghaddam S. Prevalence of Cryptosporidium spp. in camels and involved people in Yazd Province, Iran. Iran J Parasitol. 2012;7:80–4.

    CAS  PubMed  PubMed Central  Google Scholar 

  44. 44.

    Burton A, Nydam D, Dearen T, Mitchell K, Bowman D, Xiao L. The prevalence of Cryptosporidium, and identification of the Cryptosporidium horse genotype in foals in New York State. Vet Parasitol. 2010;174:139–44.

    CAS  PubMed  Google Scholar 

  45. 45.

    Laatamna AE, Wagnerová P, Sak B, Květoňová D, Aissi M, Rost M, et al. Equine cryptosporidial infection associated with Cryptosporidium hedgehog genotype in Algeria. Vet Parasitol. 2013;197:350–3.

    PubMed  Google Scholar 

  46. 46.

    Feng Y, Ryan UM, Xiao L. Genetic diversity and population structure of Cryptosporidium. Trends Parasitol. 2018;34:997–1011.

    CAS  PubMed  Google Scholar 

  47. 47.

    Hatam-Nahavandi K, Ahmadpour E, Carmena D, Spotin A, Bangoura B, Xiao L. Cryptosporidium infections in terrestrial ungulates with focus on livestock: a systematic review and meta-analysis. Parasit Vectors. 2019;12:453.

    PubMed  PubMed Central  Google Scholar 

  48. 48.

    Ryan U, Hijjawi N, Xiao L. Foodborne cryptosporidiosis. Int J Parasitol. 2018;48:1–12.

    PubMed  Google Scholar 

  49. 49.

    Nouri M, Rasooli A, Sardari H, Zolfi-Lighvan M. Role of horse in transmission of cryptosporidiosis to human. In: Proceedings of the 3rd national congress on zoonoses, 23th–25th April, 1996, Mashhad, Iran; 1996.

  50. 50.

    Naghibi A, Vahedi H. Prevalence of cryptosporidial infection in horse and man in Mashhad, Iran. Arch Razi Inst. 2002;54:101–6.

    Google Scholar 

  51. 51.

    Sardari H. Investigation of cryptosporidiosis in horses and humans exposed to horses (Turkmen Sahra Region). DVM Thesis, Shahid Chamran University of Ahvaz, Iran; 1993.

  52. 52.

    Tavassoli M, Sodagar-Skandarabadi M, Soltanalinejad F. A survey on cryptosporidial infection in horse in Urmia area, northwestern Iran. Iran J Vet Res. 2007;8:86–90.

    Google Scholar 

  53. 53.

    Vajdi R, Dianat V. Prevalence of Cryptsosporidium infection in dairy cattle, horses and children of Tabriz. In: Proceedings of the 15th Iranian veterinary congress, 26th–28th April, 2008, Tehran, Iran; 2008. p. THVC15_546.

  54. 54.

    Mirian S, Asadi M, Ferdowsi H, Rezakhani A. Survey on horse cryptosporidial infection in Tehran Province. Arch Razi Inst. 2010;65:45–7.

    Google Scholar 

  55. 55.

    Zehtab H, Makhdoomi M. Study of Salmonella and Cryptosporidium infection of horses under 6 months of age in Golestan province. In: Proceedings of the 17th Iranian veterinary congress, 28th–30th April, 2012, Tehran, Iran; 2012. p. VC-804.

  56. 56.

    Rasuli S, Khodadadi A, Sadagiyani M, Moradpoor A, Salman-Zadeh R. Equine Cryptosporidium prevalence in border line villages of Urmia Province. J Vet Clin Res. 2012;3:41–9.

    Google Scholar 

  57. 57.

    Heidari H, Gharakhani J. Study of Cryptosporidium infection in the livestock (cattle, sheep, dogs, fowls) and humans, in Hamadan city and its suburbs during 2006–2011. Avicenna J Clin Med. 2012;19:67–74.

    Google Scholar 

  58. 58.

    Ghadrdan-Mashhadi AR, Hamidinejat H, Alizadehnia P. A survey on frequency of equine cryptosporidiosis in Ahvaz. J Vet Clin Pathol. 2013;6:1723–7.

    Google Scholar 

  59. 59.

    Djurković-Djurković O, Dupouy-Camet J, van der Giessen J, Dubey JP. Toxoplasmosis: overview from a one health perspective. Food Waterborne Parasitol. 2019;12:e00054.

    Google Scholar 

  60. 60.

    Bahia-Oliveira L, Gomez-Marin J, Shapiro K. Toxoplasma gondii. In: Rose JB, Jiménez-Cisneros B. Global water pathogen project. 2017. https://www.waterpathogensorg/book/toxoplasma-gondii. Accessed 28 Aug 2020.

  61. 61.

    Dubey J, Murata F, Cerqueira-Cézar C, Kwok O. Toxoplasma gondii infections in horses, donkeys, and other equids: the last decade. Res Vet Sci. 2020;132:492–9.

    CAS  PubMed  Google Scholar 

  62. 62.

    Tavassoli M, Tabatabaei M, Javadi S, Esmaeilnejad B, Kazemnia A, Mardani K. Investigation on Toxoplasma gondii infection in domestic animals in Urmia by PCR and RFLP. Vet Res Biol Prod. 2010;85:64–70.

    Google Scholar 

  63. 63.

    Klun I, Uzelac A, Villena I, Mercier A, Bobić B, Nikolić A, et al. The first isolation and molecular characterization of Toxoplasma gondii from horses in Serbia. Parasit Vectors. 2017;10:167.

    PubMed  PubMed Central  Google Scholar 

  64. 64.

    Pomares C, Ajzenberg D, Bornard L, Bernardin G, Hasseine L, Dardé ML, et al. Toxoplasmosis and horse meat, France. Emerg Infect Dis. 2011;17:1327–8.

    PubMed  PubMed Central  Google Scholar 

  65. 65.

    Boughattas S. Toxoplasma infection and milk consumption: meta-analysis of assumptions and evidences. Crit Rev Food Sci Nutr. 2017;57:2924–33.

    CAS  PubMed  Google Scholar 

  66. 66.

    Nabavi-Monfared S. Serological study of toxoplasmosis in horses. DVM Thesis, Shiraz University, Iran; 1991.

  67. 67.

    Hajialilo E, Ziaali N, Harandi MF, Saraei M, Hajialilo M. Prevalence of anti-Toxoplasma gondii antibodies in sport horses from Qazvin, Iran. Trop Anim Health Prod. 2010;42:1321–2.

    PubMed  Google Scholar 

  68. 68.

    Raeghi S, Akaberi A, Sedeghi S. Seroprevalence of Toxoplasma gondii in sheep, cattle and horses in Urmia north-west of Iran. Iran J Parasitol. 2011;6:90–4.

    CAS  PubMed  PubMed Central  Google Scholar 

  69. 69.

    Sadeghi-Sarvestani A. Toxoplasma infection in farm animals: a seroepidemiological survey in Fars Province, South of Iran. MD Thesis, Shiraz University of Medical Sciences, Iran; 2012.

  70. 70.

    Asgari Q, Sarkari B, Amerinia M, Panahi S, Mohammad-pour I, Sadeghi-Sarvestani A. Toxoplasma infection in farm animals: a seroepidemiological survey in Fars Province, south of Iran. Jundishapur J Microbiol. 2013;6:269–72.

    Google Scholar 

  71. 71.

    Razmi GR, Abedi V, Yaghfoori S. Seroprevalence of Toxoplasma gondii infection in Turkoman breed horses in the North Khorasan Province. J Vet Lab Res. 2013;5:105–12.

    Google Scholar 

  72. 72.

    Gharekhani J. Toxoplasma gondii infection in domestic animals in Hamedan, Iran: a sero-epidemiological study. Bull Univ Agric Sci Vet Med Cluj Napoca. 2014;71:68–72.

    Google Scholar 

  73. 73.

    Tavalla M, Sabaghan M, Abdizadeh R, Khademvatan S, Rafiei A, Razavi-Piranshahi A. Seroprevalence of Toxoplasma gondii and Neospora spp. infections in Arab horses, southwest of Iran. Jundishapur J Microbiol. 2015;8:e14939.

    PubMed  PubMed Central  Google Scholar 

  74. 74.

    Amanollahi S, Sakhaee E, Golchin M. Serological study of equine toxoplasmosis in southeast of Iran. Vet J Equine Sci. 2017;1:12–6.

    Google Scholar 

  75. 75.

    Gharekhani J, Gerami-Sadeghian A, Tavoosidana G, Sohrabei A. Seroepidemiology of Toxoplasma gondii infection in dogs and domestic equine from western Iran. Comp Clin Pathol. 2015;24:255–8.

    Google Scholar 

  76. 76.

    Dubey J, Hemphill A, Calero-Bernal R, Schares G. N. hughesi and neosporosis in horses and other equids. In: Neosporosis in animals. Boca Raton: CRC Press; 2017. p. 397–410.

    Google Scholar 

  77. 77.

    Khan A, Shaik JS, Sikorski P, Dubey JP, Grigg ME. Neosporosis: an overview of its molecular epidemiology and pathogenesis. Engineering. 2019;6:10–9.

    Google Scholar 

  78. 78.

    Hosseini M, Moraveji M, Tahamtan Y, Rahimian A, Mohammadi G, Namavari M. Seroprevalence of Neospora spp. in horses in north east of Iran. Iran J Parasitol. 2011;6:64–8.

    PubMed  PubMed Central  Google Scholar 

  79. 79.

    Moraveji M, Hosseini M, Amrabadi O, Rahimian A, Namazi F, Namavari M. Seroprevalence of Neospora spp. in horses in South of Iran. Trop Biomed. 2011;28:514–7.

    CAS  PubMed  Google Scholar 

  80. 80.

    Garedaghi Y. Seroepidemiology of Neospora sp. in horses in East-Azerbaijan Province of Iran. Res J Biol Sci. 2011;6:224–6.

    Google Scholar 

  81. 81.

    Gharekhani J, Tavoosidana GR, Naderisefat GR. Seroprevalence of Neospora infection in horses and donkeys in Hamedan Province, western Iran. Vet World. 2013;6:620–2.

    Google Scholar 

  82. 82.

    Qablan MA, Sloboda M, Jirků M, Oborník M, Dwairi S, Amr ZS, et al. Quest for the piroplasms in camels: identification of Theileria equi and Babesia caballi in Jordanian dromedaries by PCR. Vet Parasitol. 2012;186:456–60.

    CAS  PubMed  Google Scholar 

  83. 83.

    Bahrami S, Alborzi AR, Mosallanejad B, Javanshiri-Ghasem-Abadi H. Molecular detection of Theileria equi in dogs from rural areas around Ahvaz. Iran Vet J. 2018;13:5–8.

    Google Scholar 

  84. 84.

    Scoles GA, Ueti MW. Vector ecology of equine piroplasmosis. Ann Rev Entomol. 2015;60:561–80.

    CAS  Google Scholar 

  85. 85.

    Onyiche TE, Suganuma K, Igarashi I, Yokoyama N, Xuan X, Thekisoe O. A review on equine piroplasmosis: epidemiology, vector ecology, risk factors, host immunity, diagnosis and control. Int J Environ Res Public Health. 2019;16:1736.

    CAS  PubMed Central  Google Scholar 

  86. 86.

    Wise L, Kappmeyer L, Mealey R, Knowles D. Review of equine piroplasmosis. J Vet Int Med. 2013;27:1334–46.

    CAS  Google Scholar 

  87. 87.

    Delpy LP. Agents pathogènes observés en Iran dans le sang des animaux domestiques. Arch Razi Inst. 1939;1:72–7.

    Google Scholar 

  88. 88.

    Darjezi A. Horse malaria and finding a new way to identify it. DVM Thesis, University of Tehran, Iran; 1937.

  89. 89.

    Jalil H. Trypaflavin and Gonacrine in the treatment of horse piroplasmosis. DVM Thesis, University of Tehran, Iran; 1940.

  90. 90.

    Nouri M, Lotfollahzadeh S. Report of a case of horse babesiosis in Ahvaz. J Fac Vet Med Univ Tehran. 1994;48:49–54.

    Google Scholar 

  91. 91.

    Oryan A, Aslani M, Rezakhani A, Maleki M, Shad-del FA. Babesia caballi and associated pathologic lesions in a horse. Equine Pract. 1994;16:33–7.

    Google Scholar 

  92. 92.

    Aslani MR. A case report of Babesia caballi infection in a foal. J Appl Anim Res. 2000;17:253–6.

    Google Scholar 

  93. 93.

    Seifi HA, Mohri M, Sardari K. A mixed infection of Babesia equi and Babesia caballi in a racing colt: a report from Iran. J Equine Vet Sci. 2000;20:858–60.

    Google Scholar 

  94. 94.

    Sakha M. Successful treatment of babesiosis in a horse. J Fac Vet Med Univ Tehran. 2007;62:155–7.

    Google Scholar 

  95. 95.

    Arfaei-Akhouleh A, Rasooli A, Razi-Jalali M, Hamidinejad H, Rouhizadeh A, Rocky A. Equine theileriosis in two Arab mares in Ahvaz. Iran Vet J. 2013;9:1030108.

    Google Scholar 

  96. 96.

    Abedi V, Razmi G, Seifi H, Naghibi A. Molecular and serological detection of Theileria equi and Babesia caballi infection in horses and ixodid ticks in Iran. Ticks Tick Borne Dis. 2014;5:239–44.

    PubMed  Google Scholar 

  97. 97.

    Davoudi J, Rasooli S, Jafari K. Investigation of Babesia spp. infection and its vector ticks in equids of Mianeh city. J Vet Pathobiol. 2010;1:49–58.

    Google Scholar 

  98. 98.

    Malekifard F, Tavassoli M, Yakhchali M, Darvishzadeh R. Detection of Theileria equi and Babesia caballi using microscopic and molecular methods in horses in suburb of Urmia, Iran. Vet Res Forum. 2014;5:129–33.

    PubMed  PubMed Central  Google Scholar 

  99. 99.

    Bahrami S, Ghadrdan A, Mirabdollahi S, Fayed M. Diagnosis of subclinical equine theileriosis in center of Iran using parasitological and molecular methods. Trop Biomed. 2014;31:110–7.

    CAS  PubMed  Google Scholar 

  100. 100.

    Bahrami S, Ghadrdan A, Pourmahdi-Borujeni M, Vafayi SM. Epidemiology of Theileria equi in Persian Arab horses from Iran. Vet Med (Praha). 2014;59:409–14.

    CAS  Google Scholar 

  101. 101.

    Purmehdi-Chelickdani R. Detection of Theileria equi and Babesia caballi using PCR method in horses in suburbs of Tabriz. DVM Thesis, Tabriz University, Iran; 2014.

  102. 102.

    Razi-Jalali M, Rocky A, Shahriari A, Ghadrdan-Mashadi A, Hamidinejat H, Jolodar A, et al. Hematological parameters and clinical signs associated with equine piroplasmosis in purebred Arabian horses of Ahvaz. Iran Vet J. 2015;11:65–75.

    Google Scholar 

  103. 103.

    Abedi V, Razmi G, Seifi H, Naghibi A. Molecular detection of equine piroplasms in donkeys (Equus asinus) in North Khorasan Province, Iran. Iran J Vet Res. 2015;16:202–4.

    CAS  PubMed  PubMed Central  Google Scholar 

  104. 104.

    Habibi G, Esmaeilnia K, Hablolvarid MH, Afshari A, Zamen M, Bozorgi S. Microscopic and molecular detection of Theileria (Babesia) equi infection in equids of Kurdistan Province, Iran. Iran J Parasitol. 2016;11:86–90.

    PubMed  PubMed Central  Google Scholar 

  105. 105.

    Farsijani F. Identification and diagnosis of Babesia infection in horses using real time-PCR. DVM Thesis, Tabriz University, Iran; 2016.

  106. 106.

    Namjoofard H. Study of prevalence of blood parasitic infections in Kerman horses. MSc. Thesis, Shahid Bahonar University of Kerman, Iran; 2017.

  107. 107.

    Kakekhani S, Rahbari S, Madani R, Bokaei S. Molecular and microscopic detection of Theileria equi and Babesia caballi in horses in Kurdestan Province, Iran. Arch Razi Inst. 2017;72:51–5.

    Google Scholar 

  108. 108.

    Hosseini SR, Taktaz-Hafeshejani T, Khamesipour F. Molecular detection of Theileria equi and Babesia caballi infections in horses by PCR method in Iran. Kafkas Univ Vet Fak Derg. 2017;23:161–4.

    Google Scholar 

  109. 109.

    Kakekhani S, Rahbari S, Madani R, Bokaei S. A survey on the infestation of Theileria equi and Babesia caballi in Donkeys in Kurdestan Province, Iran. Vet Res Biol Prod. 2018;31:93–8.

    Google Scholar 

  110. 110.

    Ebrahimi M, Adinehbeigi K, Hamidinejat H, Tabandeh MR. Molecular characterization of Theileria equi infection in horse populations belonging to West Azerbaijan, Iran: insights into the importance of equine merozoite antigen (EMA)-1 in its diagnosis. Ann Parasitol. 2018;64:21–7.

    PubMed  Google Scholar 

  111. 111.

    Mohammad-Naseri A. Detection of Babesia and Theileria infection in horses of Lorestan province using microscopic and molecular methods. DVM Thesis, Lorestan University, Iran; 2018.

  112. 112.

    Kalantari M, Sharifiyazdi H, Ghane M, Nazifi S. The occurrence of hemotropic Mycoplasma ovis-like species in horses. Prev Vet Med. 2020;175:104877.

    Google Scholar 

  113. 113.

    Afshar NA, Malekifard F, Rezaei SA, Tavassoli M. Hematological and biochemical changes in naturally occurring equine piroplasmosis in donkeys (Equus asinus) of Northwest of Iran. Acta Parasitol. 2020. https://doi.org/10.2478/s11686-020-00223-0.

    Article  Google Scholar 

  114. 114.

    European Scientific Counsel for Companion Animal Parasites. A guide to the treatment and control of equine gastrointestinal parasite infections. Worcestershire: ESCCAP; 2019. https://www.esccap.org/uploads/docs/70ep8j2z_0796_ESCCAP_Guideline_GL8_v8_1p.pdf.

  115. 115.

    Mirzayans A, Anwar M, Maghsoudloo H. Gastrointestinal helminths of horses in Iran. Trop Anim Health Prod. 1974;6:106.

    CAS  PubMed  Google Scholar 

  116. 116.

    Eslami A, Bokai S, Tabatabai V. Equine parasites in Iran. J Equine Vet Sci. 2005;25:143–4.

    Google Scholar 

  117. 117.

    Eslami A, Gharehdaghi Y, Hashemzadeh-Kargari A. Fecal examination of the equids of Tabriz from the viewpoint of gastrointestinal helminthes infestation. J Vet Clin Pathol. 2008;1:245–50.

    Google Scholar 

  118. 118.

    Hosseini S, Bokaei S, Roodgari R. Study of helminth infection in riding horses around Tehran. Iran Vet J. 2008;4:32–9.

    Google Scholar 

  119. 119.

    Moazeni M, Ebrahimi H. The study of infection rate with strongyles in the horses of Shiraz and its suburbs regarding to age, sex and method of feeding. Iran J Vet Clin Sci. 2009;2:23–8.

    Google Scholar 

  120. 120.

    Tajik J, Mirshahi A, Razmi GR, Mohammadi GR. A survey of helminth infection of Turkmen horses in Jargalan region, north Khorasan. Vet Res Biol Prod. 2010;2:53–6.

    Google Scholar 

  121. 121.

    Ferdowsi H, Rezaei F, Asadi M, Rezakhani A. A study of infection rate with strongyles in horses of Tehran Province regarding to age, sex and season. In: Proceedings of the XVth international congress of the international society for animal hygiene, 3rd–7th July, 2011, Vienna, Austria; 2011. vol. 2. p. 921–4.

  122. 122.

    Khosravi M, Kavosh F, Taghavi-Moghadam A, Ghaem-Maghami S, Pirali-Kheirabadi K, Rahimi-Feyli P, et al. Comparison of helminth and hard tick infestation between riding and work horses in Ahwaz, Iran. Comp Clin Pathol. 2012;21:333–6.

    Google Scholar 

  123. 123.

    Gholamian M. Assessment of helminthic infection of digestive system in horses of Khuzestan province. MSc. Thesis, Shahid Chamran University of Ahvaz, Iran; 2014.

  124. 124.

    Karimian-Ghotbabadi S. The prevalence study of horse gastrointestinal helminthes in Jahrom district, Fars province. DVM Thesis, Zabol University, Iran; 2016.

  125. 125.

    Shahbazi P, Tooloei Kaleibar M, Zamanzad Ghavidel E, Hasanzade A. Survey on gastrointestinal parasitic helminthes in club and rural horses of Ardabil city, Iran. J Vet Clin Pathol. 2018;12:113–22.

    Google Scholar 

  126. 126.

    Mirian SJ, Mohammadi A, Asadi M, Ferdowsi H. A survey on horse gastrointestinal worms in Tehran province. J Anim Environ. 2019;11:63–8.

    Google Scholar 

  127. 127.

    Heidari H. Prevalence of gastrointestinal parasites in horses in the suburbs of Hamedan. In: Proceedings of the 17th Iranian veterinary congress, 28th–30th April, 2012, Tehran, Iran; 2012. p. VC-676.

  128. 128.

    Tavassoli M, Arjmand Yamchi J, Hajipour N. A survey on the prevalence of strongyles species in working donkeys in North-West of Iran. J Parasit Dis. 2016;40:1210–2.

    PubMed  Google Scholar 

  129. 129.

    Imani-Baran A, Abdollahi J, Akbari H, Jafarirad S, Moharramnejad S. Anthelmintic activity of crude powder and crude aqueous extract of Trachyspermum ammi on gastrointestinal nematodes in donkey (Equus asinus): an in vivo study. J Ethnopharmacol. 2020;248:112249.

    CAS  PubMed  Google Scholar 

  130. 130.

    Sadr AM. An investigation on intestinal helminths of horses in Tehran. DVM Thesis, University of Tehran, Iran; 1958.

  131. 131.

    Hosseini S, Meshgi B, Eslami A, Bokai S, Sobhani M, Ebrahimi SR. Prevalence and biodiversity of helminth parasites in donkeys (Equus asinus) in Iran. Iran J Vet Med. 2009;3:95–9.

    Google Scholar 

  132. 132.

    Alidadi N, Tavasoli M, Farshid A, Mortaz E, Hashemiasl M. A case of recurrent thromboembolic colic in a horse of Urmia. Iran J Vet Res. 2001;2:77–85.

    Google Scholar 

  133. 133.

    Yaghuobi-Amanluo HA. Strongylus vulgaris infection in Hemedan horses. MSc. Thesis, Bu-Ali Sina University, Iran; 2018.

  134. 134.

    Borji H, Moosavi Z, Ahmadi F. Cranial mesenteric arterial obstruction due to Strongylus vulgaris larvae in a donkey (Equus asinus). Iran J Parasitol. 2014;9:441–4.

    PubMed  PubMed Central  Google Scholar 

  135. 135.

    Eslami A, Kiai B. Identification of cyathostomes in equines in Iran. Iran J Vet Res. 2007;8:45–57.

    Google Scholar 

  136. 136.

    Eslami A, Poorsepasi F, Imanitabar F, Hosseini S. A survey on worm infestation in Isfahan race horses. Vet Res Biol Prod. 1998;38:130–1.

    Google Scholar 

  137. 137.

    Nematollahi A, Ashrafi-Helan J, Haghi-Noshahr A. Severe infection of two donkeys with Thriodontophorus serratus. In: Proceedings of the 16th Iranian veterinary congress, 27th–29th April, 2010, Tehran, Iran; 2010. p. THVC16_1047.

  138. 138.

    Ghorbanzadeh B. An investigation on small strongyles species of equine in Urmia. MSc. Thesis, Urmia University, Iran; 2013.

  139. 139.

    Eslami A. Veterinary helminthology, vol. 3. In: Nematoda & acanthocephala. 2nd ed. Tehran: University of Tehran Press; 2006.

    Google Scholar 

  140. 140.

    Oryan A, Farjani-Kish G, Rajabloo M. Larval cyathostominosis in a working donkey. J Parasit Dis. 2015;39:324–7.

    CAS  PubMed  Google Scholar 

  141. 141.

    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.

    PubMed  Google Scholar 

  142. 142.

    Martin F, Höglund J, Bergström 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.

    CAS  PubMed  Google Scholar 

  143. 143.

    Malekpour SH, Rakhshandehroo E, Yektaseresht A. Molecular characterization of β-tubulin gene associated with benzimidazole resistance in larvae of field isolates of Parascaris (Nematoda: Ascarididae). J Parasit Dis. 2019;43:672–8.

    PubMed  Google Scholar 

  144. 144.

    Gao J, Zhang X, Wang X, Li Q, Li Y, Xu W, et al. According to mitochondrial DNA evidence, Parascaris equorum and Parascaris univalens may represent the same species. J Helminthol. 2019;93:383–8.

    CAS  PubMed  Google Scholar 

  145. 145.

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

    Google Scholar 

  146. 146.

    Soozani M, Moazeni M. Ascariasis in horses of Shiraz and suburburs. Vet Res Biol Prod. 2004;17:96–7.

    Google Scholar 

  147. 147.

    Rashki M. Prevalence of parasitic infections of equids in different regions of Sistan. MSc. Thesis, Zabol University, Iran; 2016.

  148. 148.

    Eslami A, Meshgi B, Naem S. First report on the presence of Probstmayria vivipara and its redescription. J Fac Vet Med Univ Tehran. 2007;62:137–8.

    Google Scholar 

  149. 149.

    Barlaam A, Traversa D, Papini R, Giangaspero A. Habronematidosis in equids: current status, advances, future challenges. Front Vet Sci. 2020;7:358.

    PubMed  PubMed Central  Google Scholar 

  150. 150.

    Mirabzadeh Ardekani M. An investigation on Habronema and its pathogenicity. DVM Thesis, University of Tehran, Iran; 1966.

  151. 151.

    Nadalian MG, Hosseini S, Tavassoli A, Raoufi A. Gastritis and gastric perforation due to Habronema spp. in the horse. J Equine Vet Sci. 1997;17:385–6.

    Google Scholar 

  152. 152.

    Naem S. The comparative morphology of three equine habronematid nematodes: SEM observations. Parasitol Res. 2007a;101:1303–10.

    PubMed  Google Scholar 

  153. 153.

    Rakhshandehroo E, Sharifiyazdi H, Shayegh H, Ahmadi A. Molecular and morphological comparison of two different types of Habronema muscae (Nematoda: Habronematidae) in horse. Parasitol Res. 2014;113:4439–45.

    PubMed  Google Scholar 

  154. 154.

    Mostafavi M, Seifi H, Borji H. Report of ocular habronemiasis in a Turkmen stallion. In: Proceedings of the 16th Iranian veterinary congress, 27th–29th April, 2010, Tehran, Iran; 2010. p. THVC16_0566.

  155. 155.

    Nazem Y, Abrishamchian ST. Comparison of the effect of intramuscular injection of ivermectin compared with oral route in the treatment of cutaneous habronomiasis in horses. In: Proceedings of the 3rd national congress of equine health and diseases, 29th April–1st May, 2015, Shiraz, Iran; 2015. p. 154.

  156. 156.

    Ghadrdan-Mashadi A, Esmaeilzadeh S, Zakian A, Faramarzian K, Haddad P. Report of habronmiasis in a 3-year-old Arabian stallion. In: Proceedings of the 3rd national congress of equine health and diseases, 29th April–1st May, 2015, Shiraz, Iran; 2015. p. 156.

  157. 157.

    Zaheri BA, Ronaghi H, Youssefi MR, Hoseini SM, Omidzahir S, Dozouri R, et al. Gasterophilus pecorum and Habronema muscae in Persian onager (Equus hemionus onager), histopathology and parasitology survey. Comp Clin Pathol. 2015;24:1009–13.

    Google Scholar 

  158. 158.

    Demir S, Tınar R, Aydın L, Çırak VY, Ergül R. Prevalence of helminth species according to faecal examination in equids in Bursa. Turk J Parasitol. 1995;19:124–31.

    Google Scholar 

  159. 159.

    Uslu U, Güçlü F. Prevalence of endoparasites in horses and donkeys in Turkey. Bull Vet Inst Pulawy. 2007;51:237–40.

    Google Scholar 

  160. 160.

    Polishchuk MG, Zverzhanovsky MI. Horse-the new host of the nematode Trichocephalus suis. Proc Kuban Agric Inst. 1980;184:71–2.

    Google Scholar 

  161. 161.

    Nicholls J, Clayton H, Duncan J, Buntain B. Lungworm (Dictyocaulus arnfieldi) infection in donkeys. Vet Rec. 1979;104:567–70.

    CAS  PubMed  Google Scholar 

  162. 162.

    Silva MdGQe, Silva AVM, Costa HMdA, Dictyocaulus arnfieldi (Cobbold, 1884): comparative analysis of the occurrence in horses, mules and donkeys. Braz J Vet Res Anim Sci. 1884;1996(33):223–5.

    Google Scholar 

  163. 163.

    Saadi A, Tavassoli M, Dalir-Naghadeh B, Samiei A. A survey of Dictyocaulus arnfieldi (Nematoda) infections in equids in Urmia region, Iran. Ann Parasitol. 2018;64:235–40.

    PubMed  Google Scholar 

  164. 164.

    Sharifi K, Borji H, Milani P. First report of Dictyocaulus arnfieldi infestation in a horse in Mashhad, Iran. Iran J Vet Sci Technol. 2010;2:45–50.

    Google Scholar 

  165. 165.

    Miller F, Bellaw J, Lyons E, Nielsen M. Strongyloides westeri worm and egg counts in naturally infected young horses. Vet Parasitol. 2017;248:1–3.

    CAS  PubMed  Google Scholar 

  166. 166.

    Pakzad-Shahabi M, Borji H, Adib-Neushabouri M. Investigation of gastrointestinal parasitic infection in equestrians around Mashhad. In: Proceedings of the 15th Iranian veterinary congress, 26th–28th April, 2008, Tehran, Iran; 2008. p. THVC15_533.

  167. 167.

    Ghadirian E, Mofidi C, Bijan H. Premiers travaux sur l’identification de différentes espèces de Trichostrongylus en Iran. Ann Parasitol Hum Comp. 1968;43:467–76.

    CAS  PubMed  Google Scholar 

  168. 168.

    Eslami A, Fakhrzadegan F. Les Nématodes parasites du tube digestif des bovins en Iran. Rev Elev Med Vet Pays Trop. 1972;25:527–9.

    Google Scholar 

  169. 169.

    Mirzayans A, Halim R. Parasitic infection of Camelus dromedarius from Iran. Bull Soc Pathol Exot Filiales. 1980;73:442–5.

    CAS  PubMed  Google Scholar 

  170. 170.

    Sharifdini M, Derakhshani S, Alizadeh SA, Ghanbarzadeh L, Mirjalali H, Mobedi I, et al. Molecular identification and phylogenetic analysis of human Trichostrongylus species from an endemic area of Iran. Acta Trop. 2017;176:293–9.

    PubMed  Google Scholar 

  171. 171.

    Abdollahi J. Determining frequency and diversity of gastrointestinal helminths in equines from Arasbaran, East Azerbaijan province, and evaluating the efficacy of oral ivermectin and Ajowa n (Trachyspermum ammi L.) powder on infected animal. MSc. Thesis, University of Tabriz, Iran; 2018.

  172. 172.

    Mirzayans A, Maghsoodloo H. Filarial infection of Equidae in the Tehran area of Iran. Trop Anim Health Prod. 1977;9:19–20.

    CAS  PubMed  Google Scholar 

  173. 173.

    Hedjazi M, Mirzayans A. Equine parafilariosis in Teheran area (Iran). Clinical aspects and treatment. Rev Med Vet. 1978;129:1685–95.

    Google Scholar 

  174. 174.

    Enami H. Epidemiological survey on equine filariasis in the Urmia area of Iran. J Anim Vet Adv. 2009;8:295–6.

    Google Scholar 

  175. 175.

    Maloufi F. Equine parafilariosis in Iran. Vet Parasitol. 1995;56:189–97.

    CAS  PubMed  Google Scholar 

  176. 176.

    Lia RP, Mutafchiev Y, Veneziano V, Giannelli A, Abramo F, Santoro M, et al. Filarial infection caused by Onchocerca boehmi (Supperer, 1953) in a horse from Italy. Parasitol Res. 2017;116:191–8.

    PubMed  Google Scholar 

  177. 177.

    Naghibi A. Investigation of microfilaremia in blood of horses in Mashhad equestrian clubs. In: Proceedings of the 1st national congress of equine health and diseases, 12th–14th November, 1996, Tehran, Iran; 1996. p. 124.

  178. 178.

    Marzok MA, Desouky ARY. Ocular infection of donkeys (Equus asinus) with Setaria equina. Trop Anim Health Prod. 2009;41:859–63.

    PubMed  Google Scholar 

  179. 179.

    Gharedagi Y, Jodeiri H, Rohani S. The first report of equine testicular infestation by Setaria equina in Tabriz. J Vet Clin Pathol. 2008;2:9–12.

    Google Scholar 

  180. 180.

    Asgarian O, Asgarian I. Report of two cases of infection with Setaria equina parasite in the anterior chamber of the eye and a new method of non-surgical treatment. In: Proceedings of the 16th Iranian veterinary congress, 27th–29th April, 2010, Tehran, Iran; 2010. p. THVC16_0568.

  181. 181.

    Nabie R, Spotin A, Rouhani S. Subconjunctival setariasis due to Setaria equina infection; a case report and a literature review. Parasitol Int. 2017;66:930–2.

    PubMed  Google Scholar 

  182. 182.

    Otranto D, Traversa D. Thelazia eyeworm: an original endo- and ecto-parasitic nematode. Trends Parasitol. 2005;21:1–4.

    Google Scholar 

  183. 183.

    Giangaspero A, Tieri E, Otranto D, Battistini M. Occurrence of Thelazia lacrymalis (Nematoda, Spirurida, Thelaziidae) in native horses in Abruzzo region (central eastern Italy). Parasite. 2000;7:51–3.

    CAS  PubMed  Google Scholar 

  184. 184.

    Giangaspero A, Lia R, Vovlas N, Otranto D. Occurrence of Thelazia lacrymalis (Nematoda, Spirurida, Thelaziidae) in native horses in Italy. Parassitologia. 1999;41:545–8.

    CAS  PubMed  Google Scholar 

  185. 185.

    Ebadi A. Study of Thelazia species in eyes of cattle in Tehran slaughterhouse. DVM Thesis, University of Tehran, Iran; 1961.

  186. 186.

    Bazargani T, Moadab SH, Raufi A, Masudi Fard M, Bahonar A. Study of the prevalence and type of ophthalmic diseases among different breeds of horses in Tehran riding clubs. Iran J Vet Med. 2011;5:13–6.

    Google Scholar 

  187. 187.

    Anvari D, Sharifi N, Hashemi SH. First report of isolation and identification of Thelazia lacrymalis nematodes in horse from Iranshahr city. In: Proceedings of the 3rd national congress of equine health and diseases, 29th April–1st May, 2015, Shiraz, Iran; 2015. p. 42.

  188. 188.

    Naem S. Morphological differentiation among three Thelazia species (Nematoda: Thelaziidae) by scanning electron microscopy. Parasitol Res. 2007b;101:145–51.

    Google Scholar 

  189. 189.

    Khedri J, Radfar MH, Borji H, Azizzadeh M. Epidemiological survey of bovine thelaziosis in southeastern of Iran. Iran J Parasitol. 2016;11:221–5.

    PubMed  PubMed Central  Google Scholar 

  190. 190.

    Setsuda A, Varcasia A, Scala A, Ozawa S, Yokoyama M, Torii H, et al. Gongylonema infection of wild mammals in Japan and Sardinia (Italy). J Helminthol. 2020;94:e13.

    Google Scholar 

  191. 191.

    Liu X, Wang Z, Han Y, Liu H, Jin J, Zhou P, et al. Gongylonema pulchrum infection in the human oral cavity—a case report and literature review. Oral Surg Oral Med Oral Pathol Oral Radiol. 2017;125:e49–53.

    Google Scholar 

  192. 192.

    Molavi G, Massoud J, Gutierrez Y. Human Gongylonema infection in Iran. J Helminthol. 2006;80:425–8.

    CAS  PubMed  Google Scholar 

  193. 193.

    Halajian A, Eslami A, Salehi N, Ashrafi-Helan J, Sato H. Incidence and genetic characterization of Gongylonema pulchrum in cattle slaughtered in Mazandaran Province, northern Iran. Iran J Parasitol. 2010;5:10–8.

    CAS  PubMed  PubMed Central  Google Scholar 

  194. 194.

    Sazmand A, Ehsani-Barahman S, Moradi H, Abedi M, Bahirae Z, Nourian A. Esophageal gongylonemosis in ruminants slaughtered in Hamedan and Babol, Iran. J Zoonot Dis. 2020;4:56–63.

    Google Scholar 

  195. 195.

    Movassaghi A, Razmi G. Oesophageal and gastric gongylonemiasis in a donkey. Iran J Vet Res. 2008;9:84–6.

    Google Scholar 

  196. 196.

    Baylis H. On the species of Gongylonema (Nematoda) parasitic in ruminants. J Comp Pathol Therap. 1925;38:46–55.

    Google Scholar 

  197. 197.

    Nielsen M. Equine tapeworm infections: disease, diagnosis and control. Equine Vet Educ. 2016;28:388–95.

    Google Scholar 

  198. 198.

    Niak A, Rak H. A report on occurrence of Anoplocephala perfoliata (George, 1782) in horse in Iran. J Fac Vet Med Univ Tehran. 1969;25:94–100.

    Google Scholar 

  199. 199.

    Eslami A, Nadealian M. Cestode and trematode infections of equines in Iran. J Fac Vet Med Univ Tehran. 1987;42:33–8.

    Google Scholar 

  200. 200.

    Ahmadi A, Abedi V, Ebrahimi M, Yaghfoori S. Investigation of helminthosis in Turkmen horses in North Khorasan province. In: Proceedings of the 3rd national congress of equine health and diseases, 29th April–1st May, 2015, Shiraz, Iran; 2015. p. 49.

  201. 201.

    Thompson R, Smyth J. Equine hydatidosis: a review of the current status in Great Britain and the results of an epidemiological survey. Vet Parasitol. 1975;1:107–27.

    Google Scholar 

  202. 202.

    Romig T, Deplazes P, Jenkins D, Giraudoux P, Massolo A, Craig PS, et al. Ecology and life cycle patterns of Echinococcus species. Adv Parasitol. 2017;95:213–314.

    CAS  PubMed  Google Scholar 

  203. 203.

    Blutke A, Hamel D, Hüttner M, Gehlen H, Romig T, Pfister K, et al. Cystic echinococcosis due to Echinococcus equinus in a horse from southern Germany. J Vet Diag Invest. 2010;22:458–62.

    Google Scholar 

  204. 204.

    Varcasia A, Garippa G, Pipia AP, Scala A, Brianti E, Giannetto S, et al. Cystic echinococcosis in equids in Italy. Parasitol Res. 2008;102:815–8.

    CAS  PubMed  Google Scholar 

  205. 205.

    Thompson R. Biology and systematics of Echinococcus. Adv Parasitol. 2017;95:65–109.

    CAS  PubMed  PubMed Central  Google Scholar 

  206. 206.

    Khademvatan S, Majidiani H, Foroutan M, Tappeh KH, Aryamand S, Khalkhali H. Echinococcus granulosus genotypes in Iran: a systematic review. J Helminthol. 2019;93:131–8.

    CAS  PubMed  Google Scholar 

  207. 207.

    Sakhaee E, Golchin M, Amiri H, Fayed MR, Eydi J. First serological study of equine hydatidosis in Iran. J Parasit Dis. 2016;40:1567–70.

    PubMed  PubMed Central  Google Scholar 

  208. 208.

    Eslami A, Shayan P, Bokaei S. Morphological and genetic characteristics of the liver hydatid cyst of a donkey with Iran origin. Iran J Parasitol. 2014;9:302–10.

    PubMed  PubMed Central  Google Scholar 

  209. 209.

    Wassermann M, Aschenborn O, Aschenborn J, Mackenstedt U, Romig T. A sylvatic lifecycle of Echinococcus equinus in the Etosha National Park, Namibia . Int J Parasitol Parasites Wildl. 2015;4:97–103.

    PubMed  Google Scholar 

  210. 210.

    Nansen P, Andersen S, Hesselholt M. Experimental infection of the horse with Fasciola hepatica. Exp Parasitol. 1975;37:15–9.

    CAS  PubMed  Google Scholar 

  211. 211.

    Awad W, Ibrahim A, Salib F. Using indirect ELISA to assess different antigens for the serodiagnosis of Fasciola gigantica infection in cattle, sheep and donkeys. Res Vet Sci. 2009;86:466–71.

    CAS  PubMed  Google Scholar 

  212. 212.

    Howell A, Malalana F, Beesley N, Hodgkinson J, Rhodes H, Sekiya M, et al. Fasciola hepatica in UK horses. Equine Vet J. 2020;52:194–9.

    CAS  PubMed  Google Scholar 

  213. 213.

    Quigley A, Sekiya M, Garcia-Campos A, Paz-Silva A, Howell A, Williams D, et al. Horses are susceptible to natural, but resistant to experimental, infection with the liver fluke Fasciola hepatica. Vet Parasitol. 2020;281:109094.

    CAS  PubMed  Google Scholar 

  214. 214.

    Eslami A, Hosseini S, Meshgi B. Animal fasciolosis in north of Iran. Iran J Public Health. 2009;38:132–5.

    Google Scholar 

  215. 215.

    Hosseini S, Meshgi B, Abbassi A, Eslami A. Animal fascioliasis in coastal regions of the Caspian Sea, Iran (2006–2007). Iran J Vet Res. 2012;13:64–7.

    Google Scholar 

  216. 216.

    Ashrafi K. Human dicrocoeliasis in northern Iran: two case reports from Gilan province. Ann Trop Med Parasitol. 2010;104:351–3.

    CAS  PubMed  Google Scholar 

  217. 217.

    Gaibov AD. Parasitic worms of the horses of Azerbaidjan. Papers on helminthology published in commemoration of the 30 year Jubileum of KJ Skrjabin and of the 15th anniversary of the All Union Institute of Helminthology. Moscow: All-Union Lenin Academy of Agricultural Science; 1937. p. 178–9.

  218. 218.

    Hazlett M, Stalker M, Lake M, Peregrine A. Hepatic Dicrocoelium dendriticum infection in a miniature horse. Can Vet J. 2018;59:863–5.

    PubMed  PubMed Central  Google Scholar 

  219. 219.

    Bourgat R, Seguin D, Bayssade-Dufour C. Données nouvelles sur Dicrocoelium hospes Looss, 1907: anatomie de l’adulte et cycle évolutif-Note préliminaire. Ann Parasitol Hum Comp. 1975;50:701–13.

    CAS  PubMed  Google Scholar 

  220. 220.

    Hinaidy H. Dicrocoelium suppereri nomen novum (syn. D. orientalis Sudarikov et Ryjikov, 1951) ein neuer Trematode für die Parasitenfauna Österreichs. Zentralbl Veterinarmed B. 1983;1983(30):576–89.

    Google Scholar 

  221. 221.

    MacHattie C, Chadwick C. Schistosoma bovis and S. mattheei in Irak with notes on the development of eggs of the S. hæmatobium pattern. Trans R Soc Trop Med Hyg. 1932;26:147–56.

    Google Scholar 

  222. 222.

    Farhati K, Eldin de Pecoulas P, Rajguru-Kazemi M, Bayssade-Dufour C. Les schistosomes d’animaux d’Asie. Med Mal Infect. 1995;25:107–10.

    Google Scholar 

  223. 223.

    Ross AG, Sleigh AC, Li Y, Davis GM, Williams GM, Jiang Z, et al. Schistosomiasis in the People’s Republic of China: prospects and challenges for the 21st century. Clin Microbiol Rev. 2001;14:270–95.

    CAS  PubMed  PubMed Central  Google Scholar 

  224. 224.

    Corapi W, Snowden K, Rodrigues A, Porter B, Buote M, Birch S, et al. Natural Heterobilharzia americana infection in horses in Texas. Vet Pathol. 2012;49:552–6.

    CAS  PubMed  Google Scholar 

  225. 225.

    Arfaa F, Sabaghian H, Ale-Dawood H. Studies on Ornithobilharzia turkestanicum (Skrjabin, 1913), Price, 1929 in Iran. Ann Parasitol Hum Comp. 1965;40:45–50.

    CAS  PubMed  Google Scholar 

  226. 226.

    Sahba GH, Malek EA. Dermatitis caused by cercariae of Orientobilharzia turkestanicum in the Caspian Sea area of Iran. Am J Trop Med Hyg. 1979;28:912–3.

    CAS  PubMed  Google Scholar 

  227. 227.

    Massoud J. Studies on the schistosomes of domestic animals in Iran: I. Observations on Ornithobilharzia turkestanicum (Skrjabin, 1913) in Khuzestan. J Helminthol. 1973;47:165–80.

    CAS  PubMed  Google Scholar 

  228. 228.

    Barlough JE, Madigan JE, DeRock E, Bigornia L. Nested polymerase chain reaction for detection of Ehrlichia equi genomic DNA in horses and ticks (Ixodes pacificus). Vet Parasitol. 1996;63:319–29.

    CAS  PubMed  Google Scholar 

  229. 229.

    Toledo R, Tamekuni K, Filho MS, Haydu V, Barbieri A, Hiltel A, et al. Infection by spotted fever rickettsiae in people, dogs, horses and ticks in Londrina, Parana State, Brazil. Zoonoses Public Health. 2011;58:416–23.

    CAS  PubMed  Google Scholar 

  230. 230.

    Laus F, Veronesi F, Passamonti F, Paggi E, Cerquetella M, Hyatt D, et al. Prevalence of tick borne pathogens in horses from Italy. J Vet Med Sci. 2013;75:715–20.

    PubMed  Google Scholar 

  231. 231.

    Veronesi F, Morganti G, Ravagnan S, Laus F, Spaterna A, Diaferia M, et al. Molecular and serological detection of tick-borne pathogens in donkeys (Equus asinus) in Italy. Vet Microbiol. 2014;173:348–54.

    PubMed  Google Scholar 

  232. 232.

    Seo MG, Lee SH, VanBik D, Ouh IO, Yun SH, Choi E, et al. Detection and genotyping of Coxiella burnetii and Coxiella-like bacteria in horses in South Korea. PLoS ONE. 2016;11:e0156710.

    PubMed  PubMed Central  Google Scholar 

  233. 233.

    Nalca A, Whitehouse CA. Crimean-Congo hemorrhagic fever virus infection among animals. In: Crimean-Congo hemorrhagic fever—a global perspective. Dordrecht: Springer; 2007. p. 155–65.

    Google Scholar 

  234. 234.

    Delpy L. Les espèces Iraniennes du genre Haemaphysalis, Koch 1844. Identité d’Haemaphysalis cholodkofskyi Olenev 192 et d’H. cinnabarina var. cretica Senevet et Caminopetros 1936. Arch Razi Inst. 1940;2:79–88.

    Google Scholar 

  235. 235.

    Abbassian-Lintzen R. A preliminary list of ticks (Acarina: Ixodidae) occurring in Iran and their distributional data. Acarologia. 1960;2:43–61.

    Google Scholar 

  236. 236.

    Abbassian-Lintzen R. Records of ticks (Acarina: Ixodidae) from southest Iran (Iranian Baluchistan and the Jiroft area). Acarologia. 1961;3:546–59.

    Google Scholar 

  237. 237.

    Mazlum Z. Ticks of domestic animals in Iran: geographic distribution, host relation, and seasonal activity. J Fac Vet Med Univ Tehran. 1971;27:1–32.

    Google Scholar 

  238. 238.

    Gholami-Parizad E. Distribution of Ixodidae and Argasidae ticks in Ilam province. MSc. Thesis, Tehran University of Medical Sciences, Iran; 1996.

  239. 239.

    Telmadarraiy Z, Bahrami A, Vatandoost H. A survey on fauna of ticks in West Azerbaijan Province, Iran. Iran J Public Health. 2004;33:65–9.

    Google Scholar 

  240. 240.

    Fiouzi-Yousefi A, Yahyaei M. Prevalence of Ixodidae ticks in horses in Golestan Province. In: Proceedings of the 15th Iranian veterinary congress, 26th–28th April, Tehran, Iran; 2008. p. THVC15_553.

  241. 241.

    Sofizadeh A, Telmadarraiy Z, Rahnama A, Gorganli-Davaji A, Hosseini-Chegeni A. Hard tick species of livestock and their bioecology in Golestan Province, north of Iran. J Arthropod-Borne Dis. 2014;8:108–16.

    PubMed  Google Scholar 

  242. 242.

    Malekifard F, Tavassoli M, Yakhchali M. A survey of hard ticks (Acari: Ixodidae) infesting donkeys in West Azerbaijan Province, Iran. Persian J Acarol. 2015;4:399–407.

    Google Scholar 

  243. 243.

    Rasouli S, Sadaghiyan M, Mazaheri Chors F, Rezaei H. Survey on hard tick species diversity and seasonal variations of equines in Maragheh. J Vet Clin Res. 2016;7:1–10.

    Google Scholar 

  244. 244.

    Hosseini-Chegeni A, Tavakoli M, Telmadarraiy Z. The updated list of ticks (Acari: Ixodidae & Argasidae) occurring in Iran with a key to the identification of species. Syst Appl Acarol. 2019;24:2133–66.

    Google Scholar 

  245. 245.

    Guglielmone AA, Robbins RG, Apanaskevich DA, Petney TN, Estrada-Peña A, Horak IG. The hard ticks of the world. New York: Springer; 2014.

    Google Scholar 

  246. 246.

    Telmadarraiy Z, Chinikar S, Vatandoost H, Faghihi F, Hosseini-Chegeni A. Vectors of Crimean Congo hemorrhagic fever virus in Iran. J Arthropod-Borne Dis. 2015;9:137–47.

    PubMed  PubMed Central  Google Scholar 

  247. 247.

    Rashmir-Raven AM. Disorders of the skin. In: Reed SM, Bayly WW, Sellon DC, editors. Equine internal medicine. St. Louis: Elsevier; 2018. p. 1159–216.

    Google Scholar 

  248. 248.

    Maghami G. External parasites of livestocks in Iran. Arch Razi Inst. 1968;20:81–3.

    Google Scholar 

  249. 249.

    Rafyi A, Alavi A, Rak H. Les espèces de mites rencontrés en Iran. J Fac Vet Med Univ Tehran. 1967;23:38–45.

    Google Scholar 

  250. 250.

    Jafari-Dehkordi A, Mohammadi-Huyyeh H. A case report of chorioptic mange dermatitis in a horse. In: Proceedings of the international congress of equine health and horse industry, 20th–21st November, 2018, Mahidasht, Iran; 2018. p. IHHIC01_014.

  251. 251.

    Dik B, Erdem I, Zerek A, Karagöz M, Mehmet Y. The first case of Bovicola (Werneckiella) ocellatus (Piaget, 1880) (Phthiraptera: Ischnocera: Trichodectidae) on a donkey (Equus asinus Linnaeus, 1758) in Turkey. Ankara Univ Vet Fak Derg. 2020;67:205–8.

    Google Scholar 

  252. 252.

    Razmi G, Aslani MR. The first report of horse infection to Bovicola equi (Linnaeus, 1758) (lnsecta, Mallophga) from Iran. Vet Res Biol Prod. 2001;14:84–5.

    Google Scholar 

  253. 253.

    Li XY, Pape T, Zhang D. Taxonomic review of Gasterophilus (Oestridae, Gasterophilinae) of the world, with updated nomenclature, keys, biological notes, and distributions. ZooKeys. 2019;891:119–56.

    PubMed  PubMed Central  Google Scholar 

  254. 254.

    Otranto D, Milillo P, Capelli G, Colwell DD. Species composition of Gasterophilus spp. (Diptera, Oestridae) causing equine gastric myiasis in southern Italy: parasite biodiversity and risks for extinction. Vet Parasitol. 2005;133:111–8.

    PubMed  Google Scholar 

  255. 255.

    Tavassoli M, Bakht M. Gastrophilus spp. myiasis in Iranian equine. Sci Parasitol. 2012;13:83–6.

    Google Scholar 

  256. 256.

    Mashayekhi M, Ashtari B. Study of Gasterophilus role in equine gastric ulcer syndrome in Tabriz area. Bull Environ Pharmacol Life Sci. 2013;2:169–72.

    Google Scholar 

  257. 257.

    Moshaverinia A, Baratpour A, Abedi V, Mohammadi-Yekta M. Gasterophilosis in Turkmen horses caused by Gasterophilus pecorum (Diptera, Oestridae). Sci Parasitol. 2016;17:49–52.

    Google Scholar 

  258. 258.

    Hoseini SM, Zaheri BA, Adibi MA, Ronaghi H, Moshrefi AH. Histopathological study of esophageal infection with Gasterophilus pecorum (Diptera: Oestridae) in Persian Onager (Equus hemionus onager). J Arthropod-Borne Dis. 2017;11:441–5.

    PubMed  PubMed Central  Google Scholar 

  259. 259.

    Rezazadeh F, Gharehaghajlou Y. Endoscopic finding of gastric ulcer in rural horse and relation with Gasterophilus spp. Iran J Vet Med. 2020;14:45–52.

    Google Scholar 

  260. 260.

    Bezerra-Santos MA, Otranto D. Keds, the enigmatic flies and their role as vectors of pathogens. Acta Trop. 2020;209:105521.

    CAS  PubMed  Google Scholar 

  261. 261.

    Vidal C, Armisén M, Bartolomé B, Rodriguez V, Luna I. Anaphylaxis to Hippobosca equina (louse fly). Ann Allergy Asthma Immunol. 2007;99:284–6.

    PubMed  Google Scholar 

  262. 262.

    Selim S. Oedematous skin disease of buffalo in Egypt. J Vet Med B. 2001;48:241–58.

    CAS  Google Scholar 

  263. 263.

    Nartshuk EP, Oboňa J. The distribution of genus Hippobosca in Transcaucasia. Acta Musei Sil Sci Nat. 2019;68:257–61.

    Google Scholar 

  264. 264.

    Ghane M, Esfandiari A, Razavi-Dinani SM. (Hippobosca infestation in a number of equines referred to the clinic of Faculty of Veterinary Medicine, Shiraz University. In: Proceedings of the 3rd national congress of equine health and diseases, 29th April–1st May, 2015, Shiraz, Iran; 2015. p. 55.

  265. 265.

    Nezamabadi M, Aali A, Stöllner T, Mashkour M, Le Bailly M. Paleoparasitological analysis of samples from the Chehrabad salt mine (northwestern Iran). Int J Paleopathol. 2013;3:229–33.

    CAS  PubMed  Google Scholar 

  266. 266.

    Askari Z, Mas-Coma S, Bouwman AS, Boenke N, Stöllner T, Aali A, et al. Fasciola hepatica eggs in paleofaeces of the Persian onager Equus hemionus onager, a donkey from Chehrabad archaeological site, dating back to the Sassanid Empire (224–651 AD), in ancient Iran. Infect Genet Evol. 2018;62:233–43.

    PubMed  Google Scholar 

  267. 267.

    Meigouni M, Makki M, Haniloo A, Askari Z, Mobedi I, Naddaf SR, et al. Herbivores coprolites from Chehrabad salt mine of Zanjan, Iran (Sassanid Era, 224–651 AD) reveals eggs of Strongylidae and Anoplocephalidae helminths. Iran J Parasitol. 2020;15:109–14.

    PubMed  PubMed Central  Google Scholar 

  268. 268.

    Mardani M, Kamali M. A review on glanders: re-emerging threat. Res Med. 2011;35:174–81.

    Google Scholar 

  269. 269.

    Rostami A, Gamble HR, Dupouy-Camet J, Khazan H, Bruschi F. Meat sources of infection for outbreaks of human trichinellosis. Food Microbiol. 2017;64:65–71.

    PubMed  Google Scholar 

  270. 270.

    Shwab EK, Zhu XQ, Majumdar D, Pena HF, Gennari SM, Dubey JP, et al. Geographical patterns of Toxoplasma gondii genetic diversity revealed by multilocus PCR-RFLP genotyping. Parasitology. 2014;141:453–61.

    PubMed  Google Scholar 

  271. 271.

    Dubey J, Calero-Bernal R, Rosenthal B, Speer C, Fayer R. Sarcocystosis in horses, mules, and donkeys (Equus spp.). In: Dubey J, Calero-Bernal R, Rosenthal B, Speer C, Fayer R, editors. Sarcocystosis of animals and humans. Boca Raton: CRC Press; 2016. p. 249–56.

    Google Scholar 

  272. 272.

    Thathaisong U, Worapong J, Mungthin M, Tan-Ariya P, Viputtigul K, Sudatis A, et al. Blastocystis isolates from a pig and a horse are closely related to Blastocystis hominis. J Clin Microbiol. 2003;41:967–75.

    PubMed  PubMed Central  Google Scholar 

  273. 273.

    Li W, Feng Y, Santin M. Host specificity of Enterocytozoon bieneusi and public health implications. Trends Parasitol. 2019;35:436–51.

    CAS  PubMed  Google Scholar 

  274. 274.

    Cain JL, Foulk D, Jedrzejewski E, Stofanak H, Nielsen MK. The importance of anthelmintic efficacy monitoring: results of an outreach effort. Parasitol Res. 2019;118:2877–83.

    PubMed  Google Scholar 

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Acknowledgements

The authors thank Prof. Moosa Tavassoli (Urmia University, Iran) for his valuable comments and Prof. Seyedhossein Hekmatimoghaddam for proofreading of the manuscript. This article was planned under the academic agreement between the Bu-Ali Sina University (Iran) and the University of Bari (Italy).

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AS performed the conceptualization of the study. AS, AB and SP defined the methodology. AS wrote and prepared the original draft of the manuscript. DO wrote, reviewed and edited the manuscript. All authors read and approved the final manuscript.

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Correspondence to Alireza Sazmand.

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Additional file 1: Text S1.

Persian translation of the abstract.

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Sazmand, A., Bahari, A., Papi, S. et al. Parasitic diseases of equids in Iran (1931–2020): a literature review. Parasites Vectors 13, 586 (2020). https://doi.org/10.1186/s13071-020-04472-w

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Keywords

  • Donkey
  • Equus
  • Horse
  • Iran
  • Mule
  • Parasite
  • Review