Occurrence of health-compromising protozoan and helminth infections in tortoises kept as pet animals in Germany

Abstract

BackgroundExotic reptiles such as tortoises, have become increasingly common domestic pets worldwide and are known to host different gastrointestinal parasites. Some of these parasites bear zoonotic potential. In the present survey, we parasitologically examined tortoise faecal samples (n = 1005) from 19 different species held as pets in private German households and German zoological gardens.MethodsSaline faecal smears were used to generate prevalence data for potentially health-compromising gastrointestinal parasites. In addition, we performed complete parasitological dissections of dead tortoises (n = 49) to estimate endoparasite burdens precisely.ResultsAnalysed tortoise faecal samples contained a broad spectrum of endoparasites. We detected ten taxa of endoparasites; oxyurid nematodes (e.g. Tachygonetria spp.) were the most prevalent parasites in faecal samples (43.18%), followed by ascarids (Angusticaecum spp.) (0.01%), Hexamita spp. (0.007%), Balantidium spp. (0.007%), trichomonads (0.004%), Strongyloides spp. (0.003%), Entamoeba spp. (0.005%), Hartmanella spp. (0.001%), Blastocystis spp. (0.002%), heterakids (0.001%) and Trimitus spp. (0.001%). Additionally, we investigated dead tortoise individuals (n = 49; of 10 different species) for aetiological diagnosis and estimation of endoparasite burden. Of these individuals, 38 (77.6%) were infected with parasites and 14 (28.6%) of them died most probably due to severe parasitic infection. Oxyurid infections correlated positively with calcium deficiency and metabolic bone disease (MBD) as well as nephrosis/nephritis, mainly occurring in juvenile tortoises (< 5 years of age).ConclusionsThe saline faecal smear technique proved to be efficient in detecting different metazoan and protozoan parasite stages in tortoise faeces. The prevalence of oxyurid infections was particularly high. In combination with pathological findings in clinical oxyuridosis obtained from necropsied animals, our findings call for further, detailed investigations on pathogenesis and immunology of oxyurids in pet reptiles. Coprological analyses for parasite detection should be mandatory before tortoises are transferred to a new owner, animal group, or public and private enclosures such as zoos. We advocate for regular health screenings in pet tortoises and, if parasitic infections are diagnosed, adequate medication or alternative hygiene management should be considered to improve and maintain individual and population health.Electronic supplementary materialThe online version of this article (10.1186/s13071-018-2936-z) contains supplementary material, which is available to authorized users.

Prevalence and intensity of gastrointestinal parasites in the vulnerable spur-thighed tortoise (<em>Testudo graeca</em>) from the central-western of Morocco

“…Nevertheless, Balantidium sp. is suspected as a potential pathogen and has been reported to cause colitis (Hallinger et al, 2018). It has been also described in the liver of heavily infected tortoises, associated with hepatic abscesses (Satbige et al, 2017;Hallinger et al, 2018).…”

“…is suspected as a potential pathogen and has been reported to cause colitis (Hallinger et al, 2018). It has been also described in the liver of heavily infected tortoises, associated with hepatic abscesses (Satbige et al, 2017;Hallinger et al, 2018). They are also responsible for causing Balantidiasis with a range of mild to severe clinical appearances (Schuster & Ramirez-Avila, 2008;Cervone et al, 2016).…”

“…In tortoises, some nematodes can cause malabsorption or intestinal problems (Martinez-Silvestre, 2011), and inflammatory lesions due to parasite migration (Hidalgo-Vila et al, 2011). These health problems have prompted several researchers to carry out works on gastrointestinal parasite incidents (Chávarri et al, 2012;Hedley et al, 2013;Hallinger et al, 2018;Huffman et al, 2018). In this context, many studies have been conducted on infections (Bouamer et al, 2003;Gagno, 2005;Traversa et al, 2005;Al-Barwari & Saeed, 2007;Fournié et al, 2015;), but most of them on captive populations (De Castet -Flamant, 2002;Cutler, 2004;Pasmans et al, 2008;Pelichone et al, 2010;Chávarri et al, 2012;Hallinger et al, 2018).…”

Endoparasites infecting exotic captive amphibian pet and zoo animals (Anura, Caudata) in Germany

“…As such, further pathogen isolation on sheep blood agars (5%), MacConkey agars, alongside Sabourand dextrose agars (SDA) (BioMerieux, Charbonnier les Bains, France) was performed. Bacterial isolates were diagnosed by Gram straining, oxidase and catalase tests, as well as a commercially available API 20E/NE® kit (BioMerieux, Charbonnier les Bains, France) as described for poikilothermal vertebrates, such as amphibians and reptiles (Marenzoni et al 2015 ; Hallinger et al 2018 ).…”

“…In addition, specific intrinsic associated risk factors (e.g., age, sex, species, host immune status) and extrinsic risk factors (e.g., poor hygiene housing conditions, temperature, humidity, animal density, nutrition) might lead to relevant parasitic burdens (Mutschmann 2010 ; Beck and Pantchev 2013 ; Hallinger et al 2019 ; 2020 ). Reinfection with resistant reproductive stages of certain endoparasites (e.g., oxyurid eggs) can lead to heavy parasitism and/or even death of pet reptiles/amphibians (Frank 1981 ; Pasmans 2008 ; Beck and Pantchev 2013 ; Wolf et al 2014 ; Hallinger et al 2018 ).…”