Cryptosporidium, Tyzzer, 1907

Koehler, Anson V., Scheelings, T. Franciscus & Gasser, Robin B., 2020, Cryptosporidium cf. avium in an inland-bearded dragon (Pogona vitticeps) - A case report and review of the literature, International Journal for Parasitology: Parasites and Wildlife 13, pp. 150-159 : 154-157

4.3. Cryptosporidium of reptiles

Numerous studies have used PCR to molecularly characterise Cryptosporidium in reptiles (e.g., Xiao et al., 2004; Kuroki et al., 2008; Pedraza-Díaz et al., 2009; Richter et al., 2011; Díaz et al., 2013) and, typically, C. serpentis Type A is the dominant Cryptosporidium taxon in snakes, followed by C. varanii , and C. varanii is dominant in lizards (reviewed in Bogan et al., 2019; Latney and Wellehan, 2020). C. serpentis causes a gastric form of Cryptosporidium , and the major symptoms and pathology are gastritis, regurgitation and midbody oedema, while C. varanii causes an intestinal form of disease, with symptoms of proliferative enteritis and chronic wasting ( Bogan et al., 2019; Lateny and Wellehan, 2020).

The following cases of Cryptosporidium sp. in reptiles were reported prior to the routine diagnostic use of PCR and, therefore, some of these uncharacterised species might have belonged to the C. avium clade: Gastric cryptosporidiosis from a wild frilled lizard ( Chlamydosaurus kingi ) from Australia (Oros´et al., 1998); oocysts found in the gut epithelium of the starred lizard ( Agama stellio ) in Israel ( Ostrovska and Paperna, 1990); oocysts in the cloacas of two Madagascar giant day geckos ( Phelsuma madagascariensis grandis ) from the USA ( Upton and Barnard, 1987); proliferative enteritis in leopard geckos ( Eublepharis macularius ), USA ( Terrell, 2003); renal cryptosporidosis in both an iguana and a Parson’ s chameleon ( Calumma parsonii ), USA ( Frye et al., 1999); tympanic cavity of a green iguana, USA ( Fitzgerald et al., 1998); and aural-pharyngeal polyps in three green iguanas, USA ( Uhl et al., 2001). A survey of 150 pet lizards and snakes in Italy detected Cryptosporidium but the taxa could not be characterised due to a low quality of sequence data obtained using a PCR-based approach ( Rinaldi et al., 2012). Some recent studies did not use PCR, such as in the case of eight captive green iguanas in Poland, which were submitted for treatment for cryptosporidiosis after showing signs of diarrhoea (Gałęcki and Sok´oł, 2018). In our opinion, future studies should use PCR-coupled sequencing of SSU, actin and hsp70 gene regions to allow comparisons with available data sets.

Inland bearded dragons are very popular animals in the pet trade ( Doneley, 2006) and are also frequently kept in zoological parks. The first molecularly-characterised case of Cryptosporidium from Pogona vitticeps was C. varanii (syn. C. saurophilum ) from the St. Louis Zoo in the

154

155

USA ( Xiao et al., 2004). As bearded dragons are common pets, Grosset et al. (2011) attempted to test the effect of paromomycin – an aminoglycoside antimicrobial – on Cryptosporidium . These authors characterised experimental infections of an unknown species of Cryptosporidium (sourced from an adult P. vitticeps ) in 10 P. vitticeps individuals (4 months of age), which remained asymptomatic throughout the trial; they noted that the infection was highly contagious (infecting separated, uninfected control animals), and emphasised the point that asymptomatic carriers can quickly spread infection to other species housed nearby, as might be the case in zoos and pet stores Grosset et al. (2011). Other than these aforementioned cases, the present case from a wildlife sanctuary in Australia and a previous case from Scotland ( Lewis et al., 2020) are the only records of Cryptosporidium from inland bearded dragons.

4.4. Current state of knowledge about C. cf. avium and associated cryptosporidiosis

In order to adequately discuss our findings in relation to the current state of knowledge in the area, we elected to review the literature to provide up-to-date information on C. cf. avium . Table 2 reveals some biases in the studies of members of the C. avium clade. Two thirds of the studies related to animals associated with the pet trade and/or zoos (66%; 16/24) ( Table 2). Clearly, domestic pets are more likely to be treated and subsequently reported by clinicians as cases vis-`a-vis wildlife cases. The species diversity in Table 2 is likely limited, because the types of pets examined would typically include exotic animals, such as Psittaciformes , and commonly-kept reptiles, such as iguanas and bearded dragons. Ostriches were also well-sampled (66.6%; four of six C. ornithophilus reports) due to ostrich farming being relatively common ( Santos et al., 2005; Meireles et al., 2006; Nakamura et al., 2009;

156

Nguyen et al., 2013; Holubova´et al., 2020). There is also a bias in the countries (including Australia, Brazil, China, Czech Republic and Japan), from which studies were published, as these are countries in which there is an active research focus on Cryptosporidium . There were limited samples directly from wild-caught animals (n = 4) (Seva´et al., 2011; Nakamura et al., 2014; Holubova´et al., 2018; Batista et al., 2019). We believe that investigating such animals is critical when attempting to discover a possible endemic origin for C. avium cases, vis-`a-vis those from pet shops, zoos and agriculture.