Terrapin tales 5GD /DVRKDSSDQ NE SGD . HC Ö" SK@ M SHB 5T QSKD å 5NQSNHRD 4 NB HDSX Terrapin tales march 2003 Dedicated to the conservation and care of turtles and tortoises Article REPRINT* E ntamoeba invadens: The tortoises, which are highly susceptible to fatal infection6. C helonian Connection W hile the incidence of E. invadens-associated amoebiasis is relatively small, it has been documented in a number of By Sandy Barnett, MATTS President species of turtles and tortoises, including species generally Like many MATTS members, I keep a variety of reptiles considered to be relatively resistant (see table right). a t my house–snakes, lizards, and turtles. All my turtles are It appears that tortoises, as a group, are prone to more “ boxies” (Terrapene carolina carolina), although I occasion- serious illness by E. invadens infection than other chelo- a lly foster other species on a short-term basis. During a nians7. However, some species of the genera Geochelone r ecent conversation with a fellow MATTS member, I and Testudo are reported to be natural carriers that do not mentioned that I am always careful to tend my snakes and normally develop active infections.2 l izards before dealing with any chelonians in my house, 6 a nd I always take care of tortoises before turtles. W hen Box turtles (Terrapene spp.) and semi-aquatic and aquatic asked why, I said it was out of concern for possible turtles (Chelodina, Chelydra, Chrysemys, Cuora, Emydura, Po- docnemis, Pseudemys and Trionyx)2 are also reported to be transmission of Entamoeba invadens (an amoebic proto- zoan) from my turtles to more susceptible animals. (I carriers and do not normally develop active infections. Resistance may be highest in purely aquatic turtles7. don’t know that my boxies are carrying Entamoeba, but I want to play it safe.) Although there may be differences in species susceptibil- M y friend asked where he could read more about this ity, all chelonians are probably vulnerable if they are suf- organism and the illness (amoebiasis) that it causes. I ficiently immune-compromised or underdeveloped (as in the case of very young, very old, and debilitated animals) didn’t have any material on hand to loan him but said I would look into it. That was the inspiration for this arti- and if presented with a sufficiently high load of the para- site. Prime candidates for active infections would be cle. In the following paragraphs, I describe the life history of E. invadens, the symptoms and pathology of E. invadens newly imported, wild-caught animals that normally serve as carriers for E. invadens. These animals are often se- infections in chelonians, and procedures for diagnosing, verely immune suppressed (and ill) due to the atrocious treating, and preventing such infections. way in which they are handled, transported and held be- W ho is affected? fore sale. E. invadens is considered the most significant pathogenic Life History (disease-causing) amoebic protozoan of captive lizards and snakes worldwide1,2,3. Most sources suggest that E. E. invadens has a direct life cycle (there is no intermediate host). An animal is infected by ingesting cyst-laden feces, invadens is usually nonpathogenic to crocodilians4, turtles and some tortoises2,5, and lives in the gut of these animals or material contaminated by such feces (e.g. bedding, 2 without harming them (a living arrangement called food). W hen a susceptible animal ingests cysts, they de- “ commensal symbiosis”). A notable exception is the giant velop into motile trophozoites in the lumen (cavity) of the animal’s small intestine. After multiplying, the tro- *with minor modifications by the author. (Contact: www.matts-turtles.org) MARCH 2003 1 Terrapin tales phozoites pass into the colon where they mature. Many Species of chelonians in which E. invadens invade the mucosa (wall) of the gastrointestinal tract a associated amoebiasis has been reported where they may or may not initiate pathology; others are p assed in the stool, while still others are transformed into Common Name Scientific Name Gulf coast box turtle Terrapene carolina cysts before being passed in the stool. • major The excreted cysts are ready to infect yet another animal when ingested. Any trophozoites that are passed rapidly • Three-toed box turtle T. c. triungulis d esiccate once outside the body, most likely rendering • Malayan box turtle Cuora amboinensis them non-infective. • Yellow-margined box C. flavomarginata turtle Survival data on E. invadens cysts in the environment are not available. However, such information has been re- • Indochinese box turtle C. galbinifrons p orted for E. histolytica, a closely related protozoan. The • Serrate box turtle C. serrata infective cyst stage of E. histolytica can survive in the envi- Heosemys grandis ronment for more than 14 days at a temperature of 8°C • Giant Asian pond turtle (46.4°F), up to eight days at 28-34ºC (82.4-93.2ºF) and 1- • Spiny turtle H. spinosa 11 2 days at 37°C (98.6°F) . It is possible that E. invadens is • Malayan flat-shelled turtle Notochelys platynota equally sensitive. It has been found that E. invadens sur- Geoemyda spengleri v ives but will not multiply at a temperatures of 12.5°C • Black-breasted leaf turtle (54.5°F)12. • Sulawesi forest turtle Heosemys (Geoemyda) yuwonoi Symptoms • Black marsh turtle Siebenrockiella C linical signs can vary widely and often are the same crassicollis vague signs seen with many other chelonian illnesses. In • Mata mata Chelus fimbriatus some cases, symptoms, if present at all, may be limited to • African mud turtle Pelusios subniger mild weight loss (or failure to grow at a normal rate) and Loggerhead musk turtle Sternotherus minor. p oor appetite right up to the time of death9.. • minor b The most common signs are diarrhea (possibly accompa- • Loggerhead turtle Caretta caretta nied by blood and excessive mucus) and irregular appe- Chelonia mydas b tite. Other clinical signs include vomiting, listlessness, • Green sea turtle w eakness, low weight and signs of dehydration (e.g. • Gopher tortoise Gopherus polymerus sunken eyes, thick oral mucus). If the lungs are infected (a • Travancore tortoise Indotestudo forsteni condition generally associated with more chronic infec- Bell‘s hinge-back tortoise Kinixys belliana t ions), labored breathing, mouth/nasal discharge and • wheezing may be noted. • Serrated hinge-back K. erosa tortoise Mild symptoms may continue with little change for • Home‘s hinge-back K. homeana months, or progress rapidly towards death. Unfortu- tortoise nately, in some cases no clinical signs are obvious until a • Impressed tortoise Manouria impressa • Red-footed tortoise Geochelone carbonaria Table Notes • Yellow-footed tortoise G. denticulata a This table is compiled from cases brought to a small number of vet- • Indian star tortoise G. elegans erinarians2,7,8,9,10, and should not be interpreted as an all-inclusive list • Leopard tortoise G. pardalis of species in which amoebiasis has occurred. • West African spurred G. sulcatta b This infection was only possible because the animal was maintained tortoise in freshwater. E. invadens cannot survive in saltwater where the species • Elongated tortoise Graptemys nigrinoda naturally occurs2 2 MARCH 2003 Terrapin tales evaluation, to check for internal parasites. d ay or so before death, eliminating any opportunity for t reatment7,9. Unfortunately, a standard fecal exam may not give reli- able results with regard to E. invadens. Such screening T here have been no studies published on the duration of rarely detects E. invadens unless there is a very large num- i llness in chelonians experimentally inoculated with E. ber of trophozoites present and the sample is very fresh invadens. However, deaths have been reported to occur in (trophozoites breakdown rapidly once excreted from the experimental infections in snakes as early as 13 days and body, thereby evading detection, and identification based 2 up to 77 days after inoculation . The length of the illness solely upon the cyst stage is difficult)7. a nd time to death is undoubtedly dependent upon a n umber of factors, including the size and possibly the It may be possible to obtain a stool fixative (e.g., polyvi- s train of the infectious dose, the health status of the ani- nyl alcohol) from your vet that prevents the breakdown of the trophozoites. However, even if a stool sample is mal at the time of inoculation, the level of maturity of the animal’s immune system, and probably the species of very fresh or properly preserved, it is often a case of luck a nimal involved. that an animal is shedding the organism at the time that the stool sample is collected since shedding is often in- termittent. Even animals with severe cases of amoebiasis “Unfortunately, in some cases no may have repeated negative fecal screenings9. clinical signs are obvious until a day A more accurate means of diagnosing an active E. in- or so before death, eliminating any vadens infection involves a cloacal flush in which fluid is opportunity for treatment.” gently flushed into the cloaca via a catheter-tipped sy- 13 ringe, and then suctioned back out . The sample is then centrifuged to separate the solids from the liquid, and the P athology retrieved material is examined under a microscope or cul- tured for identification. E. invadens most commonly affects the host’s gastrointes- t inal tract, especially the colon, invading the intestinal If you follow this route, you should insist that the flush m ucosa and destroying cells. The extent of damage is sample be cultured. In an extensive study13, it was deter- v ariable, but may result in intestinal inflammation, ero- mined that microscopic examination of in vitro cultures is E. invadens sion and often ulceration and perforation.