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Abstract

Cryptosporidium parasites infecting horses are distributed worldwide. The reported prevalence of equine cryptosporidiosis is quite variable, ranging from 0% to 37.8%. According to the literature, horses can become infected with various Cryptosporidium species, including Cryptosporidium parvum, Cryptosporidium hominis, Cryptosporidium muris, Cryptosporidium horse genotype, Cryptosporidium tyzzeri, and Cryptosporidium andersoni. Here we review the literature on equine cryptosporidiosis dating back to 1978. Because of the possibility of the human parasite Cryptosporidium hominis infecting horses, we examined the phylogeny of the Cryptosporidium small subunit ribosomal RNA and GP60 genes isolated from horses and found evidence of equine cryptosporidiosis caused by this species which is commonly assumed to be restricted to humans.

Key words

coccidia, cryptosporidium spp., foal, horse

Introduction

Cryptosporidiosis is a globally distributed infection causing sporadic gastroenteritis, abdominal pain, vomiting and fever. Several zoonotic species have been identified in humans, but most cases of human cryptosporidiosis are caused by C. parvum and C. hominis [1]. Cryptosporidiosis has long been recognized as a serious veterinary problem in neonatal ruminants [2]. C. parvum is the main species found in goats [3], lambs, calves[4] and foals [5].

The observation that equines may be infected with Cryptosporidium species similar to those infecting humans [6-11], prompted to focus this review on the global occurrence of Cryptosporidium spp. in equines and review the literature describing Cryptosporidium species found in horses.

Taxonomy

The genus Cryptosporidium is classified in the phylum Apicomplexa, class Sporozoae, subclass Coccidia, order Eucoccidiida, suborder Eimeriina and family Cryptosporididae [12]. The taxonomic classification of the genus is still being debated, as recent phylogenetic studies have shown proximity to the subclass Cryptogregaria, which is part of the Gregarines in the phylum Apicomplexa, class Gregarinomorphea. This proposed classification is based on reports that oocysts can multiply outside the host, on the presence of a specialized feeding organelle and the absence of the apicoplast [13-19]. Recent studies using DNA sequencing have led to the currently proposed taxonomy of the genus Cryptosporidium comprising 31 species and more than 70 genotypes [20], including the newly described species Cryptosporidium proliferans [21] and Cryptosporidium avium [22]. The taxonomic classification of Cryptosporidium isolated from equines based exclusively on genetic data is uncertain, particularly in the absence of characteristic morphological traits of the oocysts and a lack of data on host range.

Epidemiology of equine cryptosporidiosis

Cryptosporidium in equines is distributed worldwide an on all continents. Most studies reviewed here are from American and European countries 38.4%, and 35.9% respectively, while studies from Asia, Oceania and Africa are 12.8%, 7.7% and 5.1%, respectively. Most studies reporting on Cryptosoporidium in equines are from North America, only three reports described equine infections from South Americans, whereas literature on Cryptosporidium in equines from Central America no was identified in our search (Table 1).

Table 1. Global occurrence of Cryptosporidium, species and GP60 genotype in equines according to diagnostic methodology

Subtitle: Tissues  Stained with Hematoxylin and Eosin (HE), Wolbach-Giemsa (W-G), Electronic Microscopy (EM), Sucrose Centrifugation (SC), Sucrose Flotation (SF), Fecal Flotation (FF), Immunoflorescence (IF), Direct Fluorescent Antibody (DFA), Levitation Centrifugation Tests (LC), Sheather Fotation (SF), Immunofluorescent Microscopy (IM), Acid-Fast (AF), Immunofluorescence Test (IFA), Flow Cytometry (FC), Polymerase Chain Reaction (PCR), Epifluorescence Microscopy (EPM), Ziehl-Neelsen (ZN), Periodic Acid-Schiff (PAS), Giemsa (G), Direct Immunofluorescence (DI), Flotation (F), Sedimentation (S), Centrifugation and Flotation (CF), Safranine–Methylene-Blue (SMB), Modified Acid-Fast (MAF), Lugol Staining (LS), Imunogenetic Separation (IS), Enzyme-Linked Immunosorbent Assay (ELISA), Modified Kinyoun Technique (MKT), Real-time-PCR – RT-PCR, Aniline-Carbol-Methyl Violet Staining Method (ACMVSM), Sheather's Sugar Floatation Technique (SSFT

Between 2003 and today, many researchers have used PCR to identify Cryptosporidium species in equine samples, advancing our understanding of the occurrence of this parasite and the role of horses and foals in the epidemiology of cryptosporidiosis. Table 1 shows that horses can become infected with C. parvum, C. hominis, C. muris, C. tyzzeri, C. andersoni, C. erinacei and what has been named Cryptosporidium horse genotype [23]. The first two species are infectious to humans, and are responsible for approximately 90% of human cryptosporidiosis cases [1,24]. The susceptibility of horses to the same species infecting humans indicates that horses may play a role in the zoonotic transmission of these parasites.

It is important to note that the reported prevalence of Cryptosporidium in equines samples is quite variable, ranging from 0% [25,26] to 37.8% [27]. In our literature survey, equines of different age groups, genders and breeds were included, which may account for the wide range in reported prevalence. Thus, in Table 1, the actual prevalence may differ, in part due to the use of different diagnostic techniques, which makes it difficult to compare results from different surveys.

In New Zealand, a first-ever study was conducted on an outbreak of cryptosporidiosis in nine purebreed foals. Epidemiological, clinical, pathological and genetic data were compiled, and C. parvum isolates identified based on restriction fragment polymorphism and on the sequence of the 18S rRNA gene as belonging to what was then named “cattle” genotype of C. parvum [28] and later renamed C. parvum.

The first description of the infection of equines by Cryptosporidium hedgehog genotype (renamed C. erinacei [29], is from Algeria [30]. Cryptosporidium DNA belonging to this species was identified using PCR targeting the 18S rRNA gene and the gp60 gene. This observation indicates that the horses may participate as hosts or mechanical carriers in C. erinacei life cycle [30]. C. hominis DNA was amplified from an equine fecal sample from Algeria using PCR targeting the Heat shock Protein 70 (HSP70), the Cryptosporidium Oocyst Wall Protein (COWP) and TSP-related adhesive protein of Cryptosporidium-1(TRAP-C1) genes. C. muris was described for the first time in equine samples from Algeria by sequencing the 18S rRNA and GP60 genes [6]. These findings reinforces the hypothesis of a new species of Cryptosporidium infecting equines because until recently, few species of Cryptosporidium were found in horses, however, with the reports of C. muris and C. tyzzeri increase susceptibility to infection in horses [8]. As there are a few reports of equine infected with C. hominis [6,10,11], Laatamna’s report of a horse in Algeria infected with this species is intriguing, due to the fact C. hominis is usually described infecting humans. Similar observations were reported from China [9] and from Brazil [11]. Interestingly, these studies found similar GP60 genotypes, designated IkA15G1, IkA16G1 and IkA20G1, respectively. Although the GP60 genotypes identified in these studies are not identical, the genotypes of additional genetic markers, such as the 18S rRNA, actin and HSP70, are consistent with horses being susceptible to C. hominis or a genotypically similar species (Figure 1). Although a human case of cryptosporidiosis caused by an isolate with GP60 genotype Ik was apparently identified (NCBI nucleotide accession number KU727290), Ik alleles are not frequently observed in humans. On the other hand, similar GP60 alleles were found in C. cuniculus [31], a species infecting rabbits and humans which is closely related to C. hominis. The significance of equine infections with C. hominis, or C. hominis-like parasites, for zoonotic transmission of this species is unknown.

Figure 1. Phylogenetic trees based on the partial sequence of the 18S rRNA and GP60 genes show the phylogenetic context of Cryptosporidium sequences isolated from horses. A) Trees were generated using a 583-nt fragment of the 18S gene from equine Cryptosporidium isolates and C. hominis, C. parvum and C. meleagridis reference sequences. B) Phylogenetic tree based on approximately 100-nt fragment of the GP60 gene. Scale bars indicate 0.0010 and 0.050, respectively. BV, bovine, HM, human; DY donkey; HR/FL/WildHR, equine (horse, foal, wild horse, respectively

The occurrence of Cryptosporidium spp. is often associated with urban areas and particularly with the contamination of water supplies with human fecal material [32,33]. In Brazil, C. hominis GP60 genotype IkA20G1 and C. parvum genotypes IIaA18G3R1 and IIaA15G2R1 were collected from foals that drank water from a river that receives untreated urban wastewater [11]. The putative presence of C. hominis in horses raises public health concerns [10], since is distributed in all continents of the world. The identification in recent studies of C. hominis, or C. hominis-like parasites, in horses [6,10,11] suggests that contact between humans and horses may favor the transmission of this species, which is not commonly associated with zoonotic transmission.

In the Czech Republic, equines infected with C. parvum and with the horse genotype were identified using PCR targeting the 18S rDNA and HSP-70 genetic markers. This work showed that the horse genotype is more closely related to Cryptosporidium wrairi, there being a 98.7% similarity for 18S and 99% similarity for HSP-70 [23] between these taxa. C. parvum and the Cryptosporidium horse genotype have been reported in several other studies from different countries, such as the Czech Republic [8], the USA [34], Italy [27,35], China [36], and Belgium [37]. Based on these observations, we conclude that horses worldwide may be infected with Cryptosporidium parasites. Published evidence suggests that C. parvum/Cryptosporidium horse genotype and C. hominis, are the most common agent of equine infections followed by C. andersoni and C. muris, C. hedgehog (erinacei) and C. tyzzeri.

PCR allowed Cryptosporidium species detection in equine population, including zoonotic ones. These findings are important and have generated worries for public health.

Pathogenesis and clinical manifestations

The incidence of clinical C. parvum infections in newborn foals may be underestimated, perhaps accounting for cases empirically diagnosed as foal heat diarrhea [38]. In one of the earliest reports on equine cryptosporidiosis, the susceptibility of immunodeficient foals to this infection was described [39]. Immunocompetent foals where also found to develop diarrhea while eliminating Cryptosporidium oocysts [25], potentially causing economic loss to owners. Thus, it is often unclear whether the primary cause of symptoms is cryptosporidiosis or a viral agent. In most cases, other infectious agents that can also causes diarrhea were not considered or not diagnosed. In Kentucky, Cryptosporidium infections are most commonly observed in foals affected by other infections, caused by bacteria and viruses [25,40]. Symptoms are poorly described in equines [41]. More researches need to be performed to elucidate equine cryptosporidiosis symptomatology and pathogenicity of Cryptosporidium species.

In New Zealand, in post-mortem examinations of three foals, it was found that their intestines were full of fluid, were dilated, swollen and thin-walled, with no inflammation in the abdominal cavity. Microscopic examination of hematoxylin eosin stained sections of intestinal tissue revealed the presence in epithelial cells of numerous round organisms approximately two to five microns in size in much of the duodenum. These lesions were found to be consistent with cryptosporidiosis [28]. In Switzerland, a 9-day-old foal with diarrhea, fever and feces with fetid odor was also found to be infected with C. parvum [42].

Cryptosporidium caused inflammation and atrophy of the intestinal microvillous region with loss of absorptive surface, imbalance in the transport of nutrients and impairment in animal productivity [43].

Zoonotic potential

Currently, there is only one description of zoonotic transmission in equines. A study conducted in Italy it was shown that six veterinary students and hospitalized foals had symptoms consistent with cryptosporidiosis. C. parvum with GP60 genotype IIdA23G1 [44] was found in humans and animals. Students could have been infected by being in contact with foals infected with Cryptosporidium and because oocysts are highly resistant to environmental conditions and disinfectants, remaining viable for a long period of time [45].

An observation consitent with transmission between horses and other livestock species is a report of a horse infected with C. andersoni, a species commonly found in the abomasum of adult ruminants. The possible transmission between cattle and horses has also been reported from China [7]. Further evidence of horses being susceptible to C. parvum was reported from the UK, confirming that equines can potentially be a source of zoonotic infection of humans [46,47]. The extent of genetic diversity of Cryptosporidium isolated from equines was studied by sequencing polymorphic regions of the GP60 glycoprotein and heat shock protein HSP70 gene. These analyses revealed species and genotypes of Cryptosporidium genetically closely resembling those found in humans and bovines [5].

Cryptosporidium horse genotype was initially described in Przewalski’s wild horse foal [23], being considered as specific genotype of horses, as found in New York, in foals and their mares has been reported [34]. However, the Cryptosporidium horse genotype was also found in an immuno-compromised woman in England [48], suggesting a risk to human health.

Many Cryptosporidium species were found in farm animals samples [41,49]. Generally, these animals drink untreated water from rivers passing through the farm and wells. This water may be contaminated with oocysts of zoonotic and zooantroponotic species of Cryptosporidium. Once they ingest oocysts, animals can be infected or act as mechanical carriers, shedding Cryptosporidium oocysts and contaminating pasture. Most of farm animals are herbivors, so there are two ways they can be infected: drinking contaminated water or eating contaminated grass. Oocysts in the environment can be also carried by rain to watercourses allowing another susceptible living being infection.

C. parvum has been found in faecal samples of livestock [32,50]. C. parvum was also found in faecal samples of wild mustangs and Chincoteague ponies. These animals have minimal contact with humans; however, they ingest water and graze in the same places as cattle and wildlife such as deer and elk [51].

Conclusion

We verified that the genus Cryptosporidium with its species is distributed worldwide in the equine population. We also observed that most pathogenic species for humans detected in equines are C. parvum and C. hominis, evidencing a public health problem.

Competing interest

The authors declare that they have no competing interests.

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