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Entamoeba Invadens R O UNDTAB LI Entamoeba invadens Entamoeba invadens is a very significant protozoan pathogen affecting several reptile taxons. Amoebiasis is often associated with disease in squamates, but can also cause significant morbidity and mortality in chelonians as well. This panel has extensive experience in chelonian medicine and will provide up-to-date information on diagnosing and treating chelonian species with amoebiasis. Barbara Bonner, DVM, MS The Turtle Hospital of New England 1 Grafton Road, Upton, MA 01568-1569, USA Tufts University School of Veterinary Medicine, North Grafton, MA 01536, USA Downloaded from http://meridian.allenpress.com/jhms/article-pdf/11/3/17/2203726/1529-9651_11_3_17.pdf by guest on 29 September 2021 Mary Denver, DVM Baltimore Zoo Druid Hill Park, Baltimore, MD 21217, USA Michael Gamer, DVM, DACVP Northwest Zoo Path 18210 Waverly, Snohomish, WA 98296, USA Charles Innis, VMD VC A Westboro Animal Hospital 155 Turnpike Road, Route 9, Westboro, MA 01581, USA Moderator: Robert Nathan, DVM 1). Which species of chelonians do you see with Entamoeba Geochelone elegans. We have seen clinical disease in mata invadens? matas, Chelus fimbriatus, and African mud turtles, Pelusios Bonner: I have seen Entamoeba and clinical signs of ill subniger. health that improved upon treatment in Gulf coast box turtle, Garner: Northwest ZooPath has cases of amoebiasis in all Terrapene Carolina major, three-toed box turtle, T. Carolina groups of reptiles, including snakes, lizards, chelonians, and triungulis, leopard tortoise, Geochelone pardalis, Travancore crocodilians. Since inception in 1994, we have accumulated tortoise, Indotestudo forsteni, Geoemyda yuwonoi, spiny tur­ 13 cases of amoebiasis in tortoises, and one case in a turtle. tle, also known as the “cog-wheel turtle,” Heosemys spinosa, These cases include the following: hinged back tortoise, H. grandis, Chinese box turtle (yellow-margined box turtle or Kinixys spp. (5), Travancore/Forsten’s tortoise, Indotestudo yellow-rimmed box turtle), Cuora flavomarginata, Malayan forsteni (3), impressed tortoise, Manouria impressa (2), yel­ box turtle, Cuora amboinensis, Indochinese box turtle(flower- low foot tortoise, Geochelone denticulata (1), Indian star back), hundred-flower box turtle, white-fronted box turtle, tortoise, Geochelone elegans (1), elongated tortoise, three-hill box turtle, Cuora galbinifrons, C. serrata, flat shell Indotestudo elongata (1), and black bellied notched turtle, turtle, Notochelys platynota, Geoemyda spengleri, Borneo Graptemys nigrinoda (1). The disease may be more common black leaf turtle, Siebenrockiella crassicollis, serrated hinge- in tortoises than turtles. back tortoise, Kinixys erosa, Bell’s hinge-back, Kinixys Innis: I have found amoeba cysts and trophozoites in the belliana, Home’s hinge-back, Kinixys homeana, and others. feces of numerous species of chelonians. My clinical impres­ Denver: We have seen many species of chelonians that test sion is that terrestrial and semiaquatic species seem more positive for the presence of entamoeba by culture but which often infected than very aquatic species, but this may repre­ have no clinical signs. These include eastern box turtles, sent a caseload bias. I have reviewed 34 chelonian necropsies Terrapene c. Carolina, bog turtles, Clemmys muhlenbergi, from the past two years for which I have detailed histopathol- musk turtles, Sternotherus odorata, Indian flapshell turtles, ogy. Amoebiasis was identified in three cases: black-breasted Lissemys punctata, red-footed tortoises, Geochelone car- leaf turtle, Geomyda spengleri, redfoot tortoise, Geochelone bonaria, spotted turtles, Clemmys guttata, gopher tortoises, carbonaria, and Indian star tortoise, Geochelone elegans. Gopherus polyphemus, map turtles, Graptemys geographica, Although this represents a relatively small series of cases, the common mud turtles, Kinosternon subrubrum, Batagur tur­ incidence of amoebiasis is notable. There are a number of tles, Hardella thurjii, diamondback terrapins, Malaclemmys additional case reports in the literature documenting amoebia­ terrapin, Murray river turtles, Emydura macquarrii, sis in a variety of chelonian species (e.g. J Herp Med Surg Siebenrock’s snakeneck turtles, Chelodina siebenrockii, 10.1). I think that any species should be considered suscepti­ Egyptian tortoises, Testudo kleinmanni, and star tortoises, ble. Finally, it is important to note that amoebae, although Volume 11, No. 3,2001 Journal of Herpetological Medicine and Surgery 17 most often identified in wild-caught animals, can affect cap­ nation of sloughed colonic pseudomembrane, and that animal tive bom animals, particularly young or debilitated specimens; survived with treatment. and may affect saurians more easily than chelonians. Innis: Many animals that are shedding trophozoites and cysts are clinically affected. However, there also seem to be a 2). Are these chelonians clinically ill from Entamoeba significant number of animals that shed small numbers of invade nst cysts and are asymptomatic carriers. It is unclear exactly what Bonner: Clinically ill depends upon how one defines clini­ conditions cause some animals to become ill from Entamoeba, cally normal. It has been my experience that virtually all but a poor immune response is likely to contribute significant­ turtles who have Entamoeba invadens or other pathogenic ly. In the work that Dr. Bonner and I have done in amoeba improve clinically if it is treated. Clinical improve­ rehabilitating a number of species of Southeast Asian cheloni­ ments may be seen as increased strength, increased activity, ans, many of them are severely debilitated due to a lengthy interest in breeding, increased time out of water/resistance to collection and importation process, and seem generally dehydration (for semi-aquatics), increased, improved or more immunosuppressed. Many of those animals suffer from bacter­ consistent appetite (with resultant weight gain or increased ial sepsis, fungal infection, and metazoan parasitism; and rate of weight gain), formed stool, or just increased tolerance many of them are shedding large numbers of amoeba cysts. Downloaded from http://meridian.allenpress.com/jhms/article-pdf/11/3/17/2203726/1529-9651_11_3_17.pdf by guest on 29 September 2021 of stress. It is also important to consider the time line involved. One 3). What clinical signs are present? could see a single amoeba or a few cysts on one fecal over a Bonner: Clinical signs can vary widely. Aquatics from series of five fecals. At the time of examination, the turtle endemic parts of the world kept with good husbandry can appears to be more or less clinically without symptoms. It has have significant loads with virtually no clinical signs, except been my experience that often four to eight months later that loose stool and slower rates of weight gain/growth compared animal will be back with clinical signs of diarrhea, inap- to like animals without detectable amoeba load. The most petance, and general lethargy. This time the load will be much common universal signs, seen in aquatics, semi-aquatics, ter­ higher, with multiple amoeba and cysts seen on every fecal. restrial species, and tortoises, are diarrhea and irregular In animals that I manage and thus can assure long-term fol­ appetite. Affected chelonians can present withdrawn, dehy­ low-up, the amoeba-positive animals consistently became the drated, weak, emaciated, and anorexic. In my experience, sudden deaths, the poor-doers, or the holding-steady but fail- these signs are more likely to be seen in non-aquatics and ing-to-thrive category of turtle that in certain species, I do not seen most severely in tortoises. I have seen dysenteric diar­ wait for the onset of clinical illness before treating. rhea (loose stool every 15 min) on occasion. Severely ill Denver: As previously stated, only the mata mata and animals may be icteric, anemic, and in varying stages of cir­ African mud turtles seem to be affected clinically. culatory collapse. In my experience with this category of Garner: With one exception, all animals submitted to patient, multiple health issues often need to be addressed Northwest ZooPath had died; and the amoebic infection had simultaneously. It is difficult to be certain that all the clinical contributed significantly to the animals’ demise. One of the signs are solely related to the amoebiasis. impressed tortoises was diagnosed based on histologic exami­ Denver: The mata mata developed lethargy and inap- petance. The African mud turtles presented with sudden death. The presence of blood or mucus in the stool may also be noted. Garner: A history that includes clinical signs was available on 12 of the cases submitted to Northwest ZooPath. Acute clinical signs were seen in four tortoises. The star tortoise was passing gelatinous material in the stool. One impressed tor­ toise was asymptomatic prior to passing a colonic pseudomembrane containing the organisms. The yellow foot tortoise and one hinge back tortoise had a two day history of depression and inappetence. Eight cases had a history of chronic illness. Seven of these had histories of chronic emaci­ ation and/or anorexia; one had a history of chronic necrotizing rhinitis. Innis: Clinical signs in affected animals are often the same vague signs seen with most chelonian illnesses. As discussed below, amoebae can infect a number of organs, and the signs may differ with the location of pathology. In general, affected animals are anorexic and less active than a healthy specimen Figure.
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