There is an extremely wide range of different animal species from different parts of the world and a wide range of pathogens, of which some are known and frequently found while others are rare and completely uninvestigated. Their close cohabitation with reptiles demands deep investigation regarding the influence of these species and their microflora on people and autochthonous animal species. The origin of pet reptiles in trade is often unknown; they could be bred in captivity, offspring of wild-caught parents or taken directly from the wild. The variety of different pathogens is very large. The presence of several pathogens in one host and stressful situations can have a negative influence on the health status. Investigation in this field is not satisfactory and many exotic and not familiar pathogens are rarely discovered. There is also a possibility of transmission of the pathogens to people.
A healthy reptile has a number of pathogens, all kept in check by a healthy immune system and the beneficial gut flora. When a reptile is highly stressed or under prolonged moderate to severe stress, the immune system falters. In cases of improper environmental temperatures, starvation, or prolonged dehydration, the beneficial gut flora die off and organisms benign in small numbers gain ascendancy and start causing problems.
Snakes
The most frequent parasites found in snakes (Table 4) were Strongylid nematoda (Kalicephalus sp.) in 20.4%. Among eleven snakes (6 different species), four had Strongylid eggs while others had also adults in their intestines. Kalicephalus sp. is a hookworm from the order Strongylida, family Diaphanocephalidae. Parasites have a big and deep buccal cavity with milling plates and denticles. The muscularized oesophagus is thick and has bulbous ends (Figure 1). Some morphologic characteristics of Kalicephalus sp. are well described by Telford [19].
Other frequently found parasites were pentastomes. Reptiles periodically eliminate eggs of parasites to the surrounding. Pentastomes do carry zoonotic potential, but among those parasitizing reptiles only Armillifer and, more recently, Porocephalus (Figure 2) have been unquestionably associated with accidental human infections. However, precautions should always be taken when managing any animals with pentastomiasis. Treatment is very difficult and unsuccessful [20–22]. We detected different forms (four different species) of pentastomes in six snakes (11.1%) and four of them had also eggs in their intestines. The wormlike arthropod Porocephalus crotali was found on the surface of the lung. Sexual dimorphism is pronounced, females are larger than males. The head of females is separated from the trunk by a distinct neck (Figure 3). Embryonated eggs had outer and inner shell containing an embryo with clearly visible four legs (Figure 4).
Ascarid eggs, Oxyurid eggs, Strongyloides sp., Capillaria sp., Trematoda, Acanthocephala, Trichomonadidae, Cryptosporidium sp. (Figure 5), Cyclospora sp. (Figures 6 and 7) and Nyctotherus sp. were also detected. Similar parasite invasions are described in the literature [21, 23, 24]. Ascarid eggs which we found were spherical to subspherical with brownish-yellow shell, striated and 6.5 μm thick. We assume the eggs belong to ascaridoid nematoda Ophidascaris sp., which is frequently found in pythonid and colubrid snakes. Ascarid nematoda is one of the most important pathogen for snakes and infestation can be fatal [25].
In one Spotted Desert racer pinworm eggs were found. Klingenberg [24] described the same eggs in Ball Pythons. In our case pinworm eggs originated from eaten mice. We also detected some arthropod eggs of mice mites (Myocoptes musculinus, Myobia musculi) in snake intestines. We agree with Greiner and Schumacher [26] that some not typical eggs in snake faeces can be found because snakes often feed with rodents.
In one Corn Snake a huge dilatation of stomach and diarrhoea was found. Modified Ziehl-Neelsen staining was positive for Cryptosporidium sp. This parasite can cause a serious health problem in snakes with hypertrophic gastritis, regurgitation, progressive wasting and death [27]. The latest results indicate the potential zoonotic risk of cryptosporidium isolated from reptiles and not only from mammals [28].
The common snake mite, Ophionyssus natricis (Figure 8) was found in one Boa constrictor. Schultz described this mite infestation in one pet python and transmission to human [14]. Reptiles suffer from anemia during heavy mite infestation, which can also lead to haemorrhagic septicaemia that is usually fatal. Another author described papulo-vesicular eruptions of the skin in man [19].
In one Ball Python Amblyomma sp. ticks were determined.
Lizards
The most frequent parasites found in lizards (Table 5) were Oxyurid nematoda in 57.1%. We confirmed these parasites in 15 different species of lizards, most frequently in Chinese Water Dragons (80.0%), Spiny-tailed Lizards (75.2%), Green Iguanas 73.1%, (Figure 9) and Leopard Geckos (55.2%) (Figure 10). Two different shapes of pinworm eggs were seen. One of them was Pharyngodon sp. while we could not identify other Oxyurid eggs.
Pinworms are common in the distal part of the intestine, especially in lizards and turtles. Adults that we found were up to one cm long, white, with characteristic oesophagus with bulbous end (Figure 11). They have a direct life cycle [23]. Lizards living in captivity in small enclosures can re-infect themselves over and over again, which causes the worms to multiply much faster than in the wild.
Klingenberg [23] mentioned that mouse pinworms are also often seen in reptile excrements, but these parasites do not cause diseases in reptiles.
It is important to distinguish between pinworm eggs and eggs of mice mites. In our research the eggs of mice mites were seen more often than pinworm eggs in reptiles eating rodents.
Strongylid nematoda were confirmed in eight different species of lizard (in 11.8%), most frequently in Black Agamas in 40.0% (2/5) and Spiny-tailed Lizards in 21.4% (27/126).
Nyctotherus sp. was determined only in Uromastyx species. Spiny-tailed Lizards (Uromastyx hardwickii and Uromastyx dispar) were infestated with these ciliated protozoans in 21.7%. Both forms, a bean shaped body with cilia and smaller ovoid cyst with thick membrane and operculum were found. The size of found cysts was 41 × 29 μm (Figure 12). Balantidium sp. was determined in lizards (Green Iguana and Spiny-tailed Lizards) in small percentage. Other authors [26, 29] described Nyctotherus sp. and Balantidium sp. as commonly found in herbivorous lizards and also in turtles and snakes with transmission by ingestion of infective cysts. They are not considered as pathogens.
Trematoda eggs (Figure 13) were found in 9.4% in six different species, mostly in Tokay Geckos in 83.3%. Digenea trematoda infections occur commonly, particularly in the mouth and oesophagus. Greiner and Schumacher [26] described pulmonary and biliary trematoda. In our case we did not distinguish between these different species. Trematoda can be also found in chameleons but were not established in our research [29].
In Figures 14 and 15 invasion with ascarid adults is seen in Monitors at necropsy. Ascarid eggs were found in geckos (Leopard Gecko (Figure 16) and Tokay Gecko) in 46.8% and in one agama (Bearded Dragon). Klingenberg [30] also reported finding roundworms in chameleons imported from Africa.
Pentastomid eggs were found in Monitors (Yellow Monitor (100%), Bengal Monitor (12.5%)) and in Tokay Geckos (83.3%). In Tokay Geckos eggs and adults in lungs were confirmed (Figure 17). Klingenberg [31] described Pentastomes also in Bearded Dragons. Parasites found in our research belong to the genus Porocephalus, which can pose a potential zoonotic risk. Transmissions of other species of Pentastomes from many different reptiles to people are mentioned and confirmed [12, 21, 32].
Physaloptera sp. adults and eggs (Figures 18, 19 and 20) were found in six different species of lizards (Spiny-tailed Lizards, Green Iguanas, Geckos and Monitors) in 6.3%. Telford [19] described massive invasions, particularly in Horned Lizards (Phrynosoma sp.).
Filarioid parasites were found in 5.4% of lizards (different species of Monitors, Spiny-tailed Lizards, and in one Leopard Gecko) (Figures 21, 22, 23, 24, 25, 26 and 27). The majority of adult males and females with lot of eggs Onchocercidae, Dirofilariinae, Oswaldofilaria sp. were found in the abdominal cavity and nodules on pleura, peritonea and lungs in Monitors.
Nodules were also seen in connective tissue muscles and under the skin of Spiny-Tailed Lizards and in one Leopard Gecko. In those nodules larvae were found. Adult parasites were confirmed in abdominal cavity. Females with specific morphology on the caudal end were seen. Characteristic papillae and tale with papillar comb indicate they belong to family Onchocercidae, Dirofilariinae, Setaria digitata.
In our previous research microfilaria were not confirmed in blood smears, but some filarioid worms have been found in the abdominal cavities and subcutaneous granulomas of Monitors [1].
According to literature data these parasites have an indirect life cycle and are usually transmitted by arthropods. Filarioid worms can migrate and cause blisters and ulcers on the skin [25, 33].
Heavy invasions with Cyclophyllidea cestoda, Anoplocephalidae, Oochoristica sp. (Figures 28, 29, 30, 31, 32, 33, 34, 35, 36 and 37) were determined in Green Iguanas and Spiny-tailed Lizards. Two different species of Oochoristica sp. were found. One was small, 1.0 to 2.7 cm in length (in Spiny-tailed Lizards) and the other was longer - 28 to 30 cm (Green Iguana). In eggs of both species hexacanth embryos with six hooks with oncospheres in uterine capsule were seen. The specific morphology is described by several authors. McAllister et al. described more than 40 species in genus Oochoristica in lizards throughout the word [23, 31, 33, 34].
Acanthocephala larvae (Figures 38, 39, 40 and 41), were about 1 cm long and seen only in the coelomic cavity mostly on intestine serosa. Monitors, Spiny-tailed Lizards and one Black Agama were invaded. We can conclude that these reptiles are paratenic hosts in which larvae are frequently encysted in tissue. We could not find any clinical signs of disease. Similar findings are described by Beck and Pantchev [25].
Cryptosporidiosis in companion and captive exotic animals has received particular attention in recent years due to the public health concerns. Among the exotic animals cryptosporidiosis in snakes and lizards is a chronic life threatening disease [28, 35]. Traversa et al. [28] described the zoonotic genotype in the faeces of captive European tortoises. In our research we found oocysts in the faeces of clinically healthy Monitors. The source of infection was infected mice, in which oocysts were confirmed and clinical signs were present. That indicates a potential risk for humans.
Among Apicomplexa Isospora (Figure 42) and Eimeria (Figure 43) were determined in low percentage (0.9 and 0.6%). Other authors [1, 33] describe these parasites in much higher percentages. Motile protozoans Trichomonadidae were found in two lizards. Capillaria sp. eggs, Strongyloides eggs and Heterakidae were detected only in one case.
Two geckos had Trombiculid mites (Geckobia sp.) around the eyes (Figure 44).
Turtles
The most frequent parasites found in turtles (Table 6) were Oxyurid nematoda in 81.8% (Figure 45). We confirmed these parasites in 10 different species of turtles, most frequently in Hermann's tortoises (92.5%). In tortoises we found Oxyurid nematoda (Pharyngodonidae, Tachygonetria sp.) in 33.3% to 92.5% and in turtles (European Pond Turtle and red-Eared Sliders) only in 10.0% to 16.7%. This parasite is common in herbivore reptiles. Oxyurid nematoda have developed a commensal relationship with their host [21, 36, 37].
Strongylid nematoda (43.7%) and Balantidium sp. (26.2%) were found mostly in Chelonians. Among Strongylid nematoda, Camallanus sp. (Figure 46) were most frequently present. Ciliated protozoan Balantidium sp. is an important commensal organism but may reach high levels in the presence of gastrointestinal diseases [33].
Ascarid nematoda (20.3%) (Figures 47, 48 and 49) were established in Spur-thighed Tortoises in 56.9% and in Hermann's Tortoises in 11.5% . These parasites migrate through various organ systems and can lead to inflammatory lesions in the lung and other organs, which was also confirmed in our investigation. Similar findings are described by other authors. They describe secondary diarrhoea, anorexia, vomiting and loss of condition [26, 37, 38].
Trematoda eggs, in surprising contrast to the literature data - where this parasite is rarely mentioned in turtles - were found in high percentage in Marginated Tortoises in 60.0% and Spur-thighed Tortoises in 26.4% in our investigation. Clinical signs were not observed. Klingenberg [23] described that flukes are often seen in aquatic turtles eating fish and frogs.
In our investigation Strongyloides sp., Cestoda and Nyctotherus sp. were also detected in less than 5%. Prevalence of Nyctotherus sp. was lower than described by other authors [23, 33].
Ectoparasites in two Indian Star Tortoises, two Radiated Tortoises and one Hermann's Tortoise were Amblyomma sp.
Hyalomma sp. ticks were found only in four Spur-thighed Tortoises. Hyalomma aegyptium in Spur-thighed Tortoises were also described by Tavassoli et al. [39]. The authors mention that only adults are specific for tortoises.
One turtle had migration of fly larvae Calliphoridae (Lucilia sp.) because of the damage on the skin caused by Hooded Crows' bites. We could not find any literature data about Crows being harmful for turtles.
