13
Syndromes and Conditions of Commonly Kept Tortoise and Turtle Species WalterJ. Rosskopf Jr., D VM, Dip.AB VP, and Myra K. Shindo, BA, BS, MS, MA Turtle and tortoise species are commonly presented to veterinarians for diagnosis and treatment in exotic an- imal oriented practices. The conditions and syndromes are extremely variable, considering the diversity of the species encountered. The conditions and husbandry in- volved with water turtles is very different from what is encountered with land tortoises and turtles. A thor- ough knowledge of the subject is therefore imperative. This article reviews the conditions most commonly en- countered in working with aquatic and land turtles and tortoises. 2003 Elsevier Inc. All rights reserved. Key words: Turtle, tortoise, chelonian, mycoplasmosis, bacterial diseases, nutritional disorders, parasite infes- tation, vitamin A deficiency. T urtles and tortoises, or chelonians, are com- monly kept as pets worldwide. These ani- mals are frequently presented to veterinarians for diagnosis and treatment. Knowledge of com- mon syndromes and conditions is imperative to success in managing the species. Turtles and tortoises occur in a wide range of habitatst and climatic conditions. Proper diet and a clean environment are essential for health in captivity. Some water turtles require brackish water for health to be maintained. Tropical spe- cies require a heated environment, whereas in- dividuals from northern climates may do well in less climatically controlled environments. Smaller aquatic species may do well in an aquar- ium, whereas larger species may do better in a large pond. Filtration systems are imperative in the keeping of water turtles. Proper ultraviolet light with a basking area provided is important. Overcrowding or the presence of dominant an- imals may produce a stressful situation that can result in disease. Dietary and husbandry require- ments for chelonians are extremely variable, too. One should read as much as possible on all species encountered in practice. Dietary recommendations for chelonian spe- cies are especially variable. Even experienced zookeepers, hobbyists, and reptile specialists fre- quently disagree on what constitutes a proper diet for many of the species. Commercial diets for water turtles are now available and work well. The authors have used commercial koi food for water turtles of many species with excellent re- sults. The feeding of live food such as earth- worms and fish, though usually safe, can be a source of infectious organisms. Terrestrial tur- tles, such as Box Turtles, do well on a diet of vegetables, live food, and some low-fat dog or cat food (the latter foods are disparaged by many, but have a place in the diet if used judiciously!). Tortoises are best allowed to forage on natural grasses and are supplemented with vegetables and hay. Alfalfa or timothy pellets are frequently fed to immature tortoises. Careful supplementa- tion with calcium-mineral supplements helps to avoid imbalances. Overuse of supplements can be harmful, however. New tortoise diets (biscuit- like) are now available and widely used. The terminology used with turtles and tor- toises is quite variable. We shall use the term "tortoise" to refer to the large land animals with elephantine rear feet. Terrestrial turtles are land-based turtles (usually smaller than tortoises and anatomically variable). Water turtles are fresh-water turtles that spend the majority of their time in water. We won't use the term "ter- rapin" (usually refers to water turtles in certain areas of the United States) and we won't discuss sea turtles (not kept as pets). The term "tor- toise," for interest's sake, is often used in Great Britain and Australia to refer to water turtles (such as the Murray River Tortoise in Australia, which is a water turtle) (Figs 1 and 2). From Avian and Exotic Animal Hospital of Los Angeles County, Hawthorne, CA. Address correspondence to: Walter Rosskopf DVM, DABVP, 4871 West Rosecrans Avenue, Hawthorne, CA 90250. 2003 Elsevier Inc. All rights reserved. 1055-937X/03/1203-0127530.00/0 doi:l O. 1053/saep. 2003. 00022- 7 Seminars in Avian and Exotic Pet Medicine, Vol 12, No 3 (July), 2003: pp 149-161 149

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Page 1: Leopard Tortoise

Syndromes and Conditions of Commonly Kept Tortoise and Turtle Species Walter J. Rosskopf Jr., D VM, Dip.AB VP, and Myra K. Shindo, BA, BS, MS, MA

Turtle and tortoise species are commonly presented to veterinarians for diagnosis and treatment in exotic an- imal oriented practices. The conditions and syndromes are extremely variable, considering the diversity of the species encountered. The conditions and husbandry in- volved with water turtles is very different from what is encountered with land tortoises and turtles. A thor- ough knowledge of the subject is therefore imperative. This article reviews the conditions most commonly en- countered in working with aquatic and land turtles and tortoises. �9 2003 Elsevier Inc. All rights reserved.

Key words: Turtle, tortoise, chelonian, mycoplasmosis, bacterial diseases, nutritional disorders, parasite infes- tation, vitamin A deficiency.

T urtles and tortoises, or chelonians, are com- monly kept as pets worldwide. These ani-

mals are frequently presented to veterinarians for diagnosis and treatment. Knowledge of com- m o n syndromes and conditions is imperative to success in managing the species.

Turtles and tortoises occur in a wide range of habitats t and climatic conditions. Proper diet and a clean envi ronment are essential for health in captivity. Some water turtles require brackish water for health to be maintained. Tropical spe- cies require a heated environment , whereas in- dividuals f rom nor thern climates may do well in less climatically controlled environments. Smaller aquatic species may do well in an aquar- ium, whereas larger species may do bet ter in a large pond. Filtration systems are imperative in the keeping of water turtles. Proper ultraviolet light with a basking area provided is important . Overcrowding or the presence of dominan t an- imals may produce a stressful situation that can result in disease. Dietary and husbandry require- ments for chelonians are extremely variable, too. One should read as much as possible on all species encounte red in practice.

Dietary recommendat ions for chelonian spe- cies are especially variable. Even exper ienced

zookeepers, hobbyists, and reptile specialists fre- quently disagree on what constitutes a p rope r diet for many of the species. Commercia l diets for water turtles are now available and work well. The authors have used commercial koi food for water turtles of many species with excellent re- sults. The feeding of live food such as earth- worms and fish, though usually safe, can be a source of infectious organisms. Terrestrial tur- tles, such as Box Turtles, do well on a diet of vegetables, live food, and some low-fat dog or cat food (the latter foods are disparaged by many, but have a place in the diet if used judiciously!). Tortoises are best allowed to forage on natural grasses and are supplemented with vegetables and hay. Alfalfa or t imothy pellets are frequently fed to immature tortoises. Careful supplementa- tion with calcium-mineral supplements helps to avoid imbalances. Overuse of supplements can be harmful, however. New tortoise diets (biscuit- like) are now available and widely used.

The terminology used with turtles and tor- toises is quite variable. We shall use the te rm "tortoise" to refer to the large land animals with e lephant ine rear feet. Terrestrial turtles are land-based turtles (usually smaller than tortoises and anatomically variable). Water turtles are fresh-water turtles that spend the majority of their t ime in water. We won ' t use the term "ter- rapin" (usually refers to water turtles in certain areas of the United States) and we won ' t discuss sea turtles (not kept as pets). The term "tor- toise," for interest 's sake, is often used in Great Britain and Australia to refer to water turtles (such as the Murray River Tortoise in Australia, which is a water turtle) (Figs 1 and 2).

From Avian and Exotic Animal Hospital of Los Angeles County, Hawthorne, CA.

Address correspondence to: Walter Rosskopf DVM, DABVP, 4871 West Rosecrans Avenue, Hawthorne, CA 90250.

�9 2003 Elsevier Inc. All rights reserved. 1055-937X/03/1203-0127530.00/0 doi: l O. 1053/saep. 2003. 00022- 7

Seminars in Avian and Exotic Pet Medicine, Vol 12, No 3 (July), 2003: pp 149-161 149

Page 2: Leopard Tortoise

150 Rosskopf Jr. and Shindo

Figure 1. Australian Snake Neck turtles. Courtesy of Ellen Nichol.

Tortoise Conditions and Syndromes Upper Respiratory Disease Syndrome

The respiratory disease condition that is com- monly encountered in desert tortoises has been known fbr decades. I would estimate that 80% of the desert tortoises that I have seen in practice are brought in because of this disease. In over 33 years of practice, I have seen well over 25,000 cases (and this is a conservative estimate)! All of us in practice in the 1970s and 1980s were per- plexed by this condition, which was commonly thought to be viral in etiology. Death rates at that time were high. In the late 1980s, the dis- ease began to be seen in wild desert tortoise populations in enormous numbers, L,2 The se- nior author was doing contract work for the Bureau of Land Management and was asked by director Dr. Kristin Berry if there was a known cause and treatment for this condition. She was told the problem was a long-standing enigma in pet tortoises, 3 and that Dr. ElliotJacobson of the University of Florida, Gainesville, would be the investigator to contact. He was invited to inves- tigate the disease and we are forever indebted to him for his findings.

Pathologic studies of 17 ill desert tortoises from the Desert Tortoise Natural Area in Cali- fornia and 1 ill desert tortoise from Utah indi- cated that major microscopic lesions were con- fined to the upper respiratory tract (URT). 3 Electron microscopic studies revealed small (350-900 nm) pleomorphic organisms resem- bling mycoplasma in close association with the surface epithelium of the URT of ill tortoises. Mycoplasma was cultured from the nasal pas-

sageways of ill tortoises and, at the time, repre- sented only the second report of isolation of a mycoplasma from a reptile. Mycoplasma tesludinis was previously isolated from the cloaca of a Spur- Thighed Tortoise; however, the pathogenicity of this organism is unknown. The mycoplasma iso- lated from the desert tortoise was named Myco- plasma agassizii, with strain PS6 the strain type. In a transmission study, that organism was demon- strated to be the cause of URT disease in the desert tortoise. M. agassizii has been isolated from the wild gopher tortoises in Florida with rhinitis, and transmission studies also have con- firmed it as the causative agent. An enzyme- linked immunosorbent assay has been devel- oped to determine exposure to this organism. 4

Direct contact between tortoises appears to be an important route of transmission. Myco- plasma can be cultured from nasal discharge fluids of affected tortoises, and because of this, transmission can be either direct or indirect through objects contaminated with infective na- sal fluids. 4

Enrofloxacin has been shown to be extremely effective in treating tortoises with mycoplasmo- sis. A combination of systemic medication, along with saline-enrofloxacin (30:1) nasal flushes, works well to control the disease. Most of these tortoises probably remain carriers for life, but can be retreated successfully if periodic flare-ups occur. The use of doxycycline, which is very effective in rat mycoplasmosis, doesn ' t seem to work as well in tortoises, but it is an alternative duug in cases of apparent resistance to Enro- floxacin. Secondary bacteria such as Pasteurella

Figure 2. Infant Australian Snake Neck turdes. Cour- tesy of Ellen Nichol.

Page 3: Leopard Tortoise

Syndromes and Conditions of Tortoise and Turtle Pet Species" 151

sp. 5 and other organisms may require the use of other antibiotics, as well.

MycoDlasma sp. uppe r respiratory infections may be seen in a wide variety of tortoise species worldwide. Jacobson states that mycoplasmal in- fections with secondary Gram-negative bacterial infection have been implicated in URT disease in Desert Tortoises (Gopherus agassizii), Gopher Tortoises (G0pher, us polyphemus), Greek and Her- mann ' s Tortoises ( Testudo graeca and Testudo her- manni), Leopard Tortoises (Ge0chel0ne pardalis), Radiated Tortoises (Gopherus radiata), and In- dian Star Tortoises (Gopherus elegans).G

Aamcdotal evidence would suggest that the same organism or related ones cause the uppe r respiratory disease syndrome in Sulcata Tor- toises (Ge0chel0ne sulcata) and many others of the world's tortoises. The respiratory disease seen in box turtles and water turtles appears to be asso- ciated with a wide variety of Gram-negative bac- teria and not the mycoplasma agent, a l though there is still some debate on the subject.

It is also interesting to note that tortoise spe- cies seem quite variable in their susceptibility to uppe r respiratory disease syndrome. Anecdot- ally, Sulcata tortoises seem to respond to treat- men t much faster than desert tortoises. Some tortoise species seem relatively resistant to the organism.

Disorders Involving the Shell

Malnutrit ion is widespread among captive tor- toises. Inadequate mineral intake with fast growth can lead to severe deformity of the shell.

Pyramidal shell growth is a c o m m o n p rob lem in raising tortoises in captivity. It is such a com- m o n occurrence that it is rare to have a captive- raised tortoise that grows in a normal way. When I see a normal- looking captive tortoise, I usually quiz the client on the diet supplied. I am often shocked at some serendipitous combinat ion that has luckily worked in this particular pet. The etiology of pyramidal shell growth is unknown. Suggested etiologies include excess dietary pro- tein, too rapid growth, vitamin or mineral excess or deficiency, metabolic bone disease, and spe- cies predisposition, v

Traumat ic injuries to the shell caused by lawn mowers and automobiles are commonly encoun- tered, especially in the spring, when tortoises come out of hibernation. Canine attack with

severe t rauma is all too frequently seen in tor- toises.

Shell rot (1 or more erosive lesions involving either the uppe r or lower shell, or both) usually occurs as a result of traumatic injury to the shell or exposure to filthy environmental conditions, a l though infectious diseases can be associated with the disorder. 8

Shell-repair techniques have been developed to a fine art in reptile medicine. A n u m b e r of acrylics and patching materials work well on che- lonian shell problems, sq~

Oral Herpesvirus Infection of Tortoises

A herpesvirus has been isolated f rom necro- tizing oral or beak lesions in several species of tortoise. 1~ Species commonly kept in captivity that are affected by this virus include the Argen- tine Chaco Tortoise (Geochelone chilensis), the Desert Tortoise of the southwestern Uni ted States (G. agassizii), and the Greek Spur- Thighed Tortoise (T. graeca). This virus causes necrotizing lesions in the oral cavity and beak commissures of the tortoise, resulting in nasal and ocular discharge, regurgitation, and an- orexia. A fecal-oral transmission route is sug- gested. ,2-14

T r e a t m e n t of lesions that appea r to be caused by the herpesvirus is suggested, even if definitive diagnostic evidence is lacking. I f possible, however, a section of the necro t iz ing tissue should be submi t t ed for histologic inter- pre ta t ion , because positive ident if icat ion of the viral part icles in the ep i the l ium can be achieved with e lec t ron microscopy. T r e a t m e n t of the oral lesions with a p repa ra t ion of 5% acyclovir o i n t m e n t appl ied topically to the le- sion is somet imes effective. Some severe, non- responsive cases r e spond to oral acyclovir at a dosage of 80 m g / k g orally q24 h o u r until the signs clear. Antibiotics can be used to t rea t the secondary bacter ial infect ions that typically oc- cur because of i rr i tat ion of the ep i the l ium s u r r o u n d i n g the beak and oral cavity. Quaran- tine of newly acqui red animals is essential to de te r the spread of this disease in tortoise colonies. ~

In Southern California, we have seen numer- ous herpes cases in desert tortoises and Russian (Horsefield's) Tortoises. Most have responded well to t reatment , bu t some have died.

Page 4: Leopard Tortoise

152 Rosskopf Jr. and Shindo

acid in the blood, and gout) are routinely seen. Infections of the hear t are also common.

Figure 3. Adult Chinese soft-shell turtle. Courtesy of Waiter Rosskopf, DVM.

Hypervitaminosis A--Skin Sloughing or Peeling Syndrome of Tortoises

A specific p rob lem in tortoises became evi- dent in the early 1980s when vitamin A injec- tions were frequently given to parrots with vita- min A deficiency dietary problems. Practitioners began to give injections of vitamin A regularly to desert tortoises with URT infections. At the time, we suspected the tortoises were reacting to cer- tain antibiotics.

Hypervitaminosis A iatrogenic dermatosis, which presents as patches of dry skin that progresses to a generalized sloughing of the ep- ithelium, can follow a single vitamin A injection at a dosage higher than 10,000 I U / k g intramus- cularly. 15 Secondary bacterial or fungal infec- tions frequently follow this condition, and re- quire t rea tment with systemic and topical antibi- otics. Additional vitamin A injections are not advisable. I f the animal is generally deficient in vitamin A, then dietary changes can be imple- men ted in lieu of the injections, because oral supplementa t ion of vitamin A in conjunct ion with normal feeding practices is not known to cause this problem, lz

Internal Infections

A wide variety of bacterial infections occur in captive tortoises (Fig 3). Often, multiple organs are involved. Liver a n d / o r kidney disease is com- m o n because of" the septic nature of tortoise diseases and the filtering action of these 2 or- gans. Chronic hepatitis and chronic kidney dis- ease (the latter resulting in elevated levels of uric

Mouth Rot (Infectious stomatitis)

This condition results ei ther as the direct re- sult of traumatic injury to the oral cavity and its lining, or secondary to systemic disease. This condit ion should be treated locally (topically) as well as systemically to prevent the possibility of internal abscessation. Beak and jaw deformat ion may occur, necessitating periodic corrective tr imming. If mou th rot does not respond in the way the clinician would expect, herpesvirus in- fection should be suspected. 11k14

Abscesses

Bacterial abscesses are common, result ing f rom puncture wounds and o ther t raumatic in- juries. Because tortoises readily develop internal abscesses, systemic antibiotics must be used to treat all abscesses (external or otherwise).

Organ Failure

The ravages of a lifetime of low-grade infec- tions and water deprivation may result in cirrho- sis a n d / o r o ther pathology of the liver, or chronic kidney disease and failure in aged tor- toises. Blood-chemistry analysis is necessary to make the diagnosis.

Impactions and Foreign-Body Ingestion

Sand impact ion occurs commonly in hatch- lings. Therefore , they should not be kept on sand, but ra ther on hard dirt or indoor-outdoor carpeting. Surgery to relieve a sand impact ion or retrieve foreign bodies f rom the intestinal tract is a complicated procedure with a poor outlook.

Sulcata tortoises are particularly p rone to rock and substrate ingestion. Long-term laxative use and fecal softeners along with the judicious use of metoc lopramide may be necessary in treat- m e n t of these cases.

Reproductive Problems

Metritis, retained eggs, and egg-yolk peritoni- tis are c o m m o n among female tortoises. Some of

Page 5: Leopard Tortoise

Syndromes and Conditions of Tortoise and Turtle Pet Species 153

these problems can be managed medically. Oth- ers require surgical intervention.

Prolapses

Prolapses of the penis, uterus, intestine, or urinary bladder are not u n c o m m o n . General anesthesia is necessary to correct these condi- tions. The prolapsed organ must be carefully replaced inside the body. Simply pushing it back into the cloaca where it is out of sight may result in a slow death. A thorough diagnostic workup (x-rays, laboratory testing, etc.) must be per- fo rmed to help diagnose their causes.

Bladder Stones

Bladder stones, composed of uric acid, re- quire many years to form and may reach unbe- lievably large sizes (baseball size is not uncom- mon) . Desert tortoises are p rone to this disease condit ion because of the urinary bladder ' s func- tion of storage and resorpt ion of water. These functions often result in the deposit ion of small particles of uric acid within the b ladder and the gradual accumulat ion of more uric acid residues a round this nucleus over the years. When these stones become large enough to irritate the blad- der lining or to mechanically impair urination, interfere with walking, or otherwise result in pain, most desert tortoise owners will become suspicious that something is wrong. The diagno- sis is conf i rmed with radiographs. Correct ion involves surgical removal of the s toneJ 5,~6

Iron Storage Disease

Some desert tortoises suffer f rom excessive accumulat ion of elemental iron within the liver. This results in chronic hepatitis and, eventually, cirrhosis. The cause is unknown but blood breakdown in disease and enzyme deficiency are both possible etiologies. Owners should not of- fer iron tablets to their desert tortoises. Foods and water supplies high in iron should also be avoided.

Intestinal Parasites

Small pinworm-like parasites, large strongyle- type worms, and large roundworms can infect captive tortoises. Fur thermore , several proto-

zoan parasites (Giardia, Trichomonas, etc.) can cause disease. Some c o m m o n worms are consid- ered normal by some investigators27

Entamoeba Invadens Infection in Tortoises

Amoebiasis periodically causes severe disease in tortoises. Epidemics are not u n c o m m o n and special ment ion of the problem is warranted. Dysenteric diarrhea may be seen. Investigators have described severely ill animals as icteric, ane- mic, and in varying stages of circulatory col- lapse, as

Diagnosis is made by wet mounts or Tr ichrome stains, tS-2~ Trea tmen t involves metro- nidazole and iodoquinal. 21

Myiasis (Maggot Infestation)

Fly strike and maggot infestation are ex- tremely common, especially with wounded and traumatized tortoises. These animals are virtu- ally defenseless and flies can easily take advan- tage of their weakened condition. Any tortoise that is known to be ill or suffering f rom a wound anywhere should be housed indoors or other- wise pro tec ted f rom flies within a screened en- closure. Long-term soakings in betadine solu- tion and removal of the maggots by hand are procedures used in the m a n a g e m e n t of such cases.

Ticks

Wild or newly acquired desert tortoises may be infested with ticks. They should be carefully removed. In April 2000, a ban was placed on the importa t ion of certain species of African tor- toises into the Uni ted States. It was found that some of these tortoises harbored ticks that car- ried virulent viruses with the potential to deci- mate hoofed stock. Practitioners should make owners of such tortoises aware of the potential problem, especially if the tortoises are to be kept near hoofed stock. 12

Before the ban, most impor ted leopard and Sulcata tortoises seen by the authors were in- fested with hard ticks!

Diabetes Mellitus

Desert tortoises may develop diabetes melli- tus, which requires closely moni to red medical

Page 6: Leopard Tortoise

154 RosshopJJy. and Shindo

care. We have encounte red several cases of dia- betes in desert tortoises over the years. Insulin has a long-lasting physiologic effect in these rep- tiles, in my experience. High glucose levels may also occur in severe kidney disease in tortoises, as in avian species.

Ocular Disorders

A wide variety of disorders involving the eyes and related structures afflict tortoises. Some of these include cataracts, corneal ulcers, ocular infections, punc ture wounds and o ther trau- matic injuries, conjunctivitis, keratoconjunctivi- tis, keratitis sicca (dry eye), and hatchling eye syndrome (vascular scarring). Bacterial infec- tion may cause some of these conditions or oth- erwise cause secondary complications. Eye in- volvement may accompany symptoms of the re- spiratory complex. Cataracts may result fi'onl traumatic injury or infection. Some are, no doubt, hereditary. Unusual eye color variations are also noted f rom time to time.

Normal Ocular Discharge in Some Tortoises

Some tortoises have no functional nasolacri- real system and tears are lost f rom spillage or evaporation. 22 Red-Footed (Geochelone carbona- r~a) and Yellow-Footed Tortoises (Geochelone den- ticulata) normally have a clear ocular discharge. 7

Gular Overgrowth

Older tortoises may develop large, overgrown gular projections (forward project ion of the lower shell, unde r the neck). This condit ion can result in a severe mechanical interference with eating and swallowing. Correction involves trim- ming of this project ion with a Stryker saw.

Submandibular Sex-Gland Inflammation

During breeding season, the large chin or sex glands of the male desert tortoise may increase in size and drain. The en la rgement noted may be normal , but infections of these glands may occur. Cytology can help to differentiate be- tween normal and infected submandibular glands.

Figure 4. Box turtles eating. Courtesy of Ellen Nichol.

Ivermectin Reaction

This commonly used vermifuge canno t be used by injection in any of the chelonian species. The use of this medicat ion will result in flaccid paresis or paralysis of the limbs. 7,2~

Goiter in Giant Tortoises

Goiter has been frequently repor ted in giant tortoises such as the Galapagos Tortoise and the Aldabran Tortoise. Little is known about its eti- ology, and clinicians are caut ioned abou t the potential ha rm of dietary supplementa t ion of iodine, e3

Box Turtles and Other Terrestrial Turtles

Disease Resulting from Malnourishment and Vitamin Deficiencies

Many diseases afflicting captive terrestrial tur- tles are, at least in part, the result of malnutri- tion (Fig 4). Turtles that do not receive all o f the nutrients vital to sustain op t imum health do not remain healthy, and become ill f rom a variety of causes. Hatchlings are the most p rone to disease resulting f rom dietary deficiencies, because their nutrit ional requirements exceed those of adult turtle, and because their rate of growth is so rapid. Hatchl ing turtles often exhibit soft shells associated with protein and mineral deficiencies, and deformed shells associated with abnormal ly fast growth f rom high protein diets. Adult tur- tles, by contrast, are unlikely to exhibit soft-shell problems, but may show signs of anemia, weight

Page 7: Leopard Tortoise

Syndromes and Conditions of Tortoise and Turtle Pet Species 155

ease. Dietary deficiency of vitamin A is consid- ered by many to be the major predisposing cause. Squamous metaplasia, as is seen in avian species, predisposes the turtle to colonization and subsequent infection by a variety of bacterial pathogensY 5

Trea tmen t of the condit ion involves lancing the abscesses, appropr ia te antibiotic and vitamin therapy, and careful consideration to correct ing possible predisposing factors such as inadequate diet, cleanliness, or stress.

Figure 5. Eastern male box turtle. Note the bright red eyes of the male box turtle. Courtesy of Ellen Nichol.

loss, mou th rot, internal infection, or abscessa- tion with chronic malnour ishment .

Abscesses (Other Than Ear)

Bacterial abscesses are c o m m o n from punc- ture wounds, bite wounds, and other injttries. Injectable antibiotics must be used under these circumstances to prevent format ion of internal abscesses or septicemia.

Respiratory Disease

Respiratory disease is c o m m o n in box turtles. Epidemics may occur in populat ions of wild box turtles, characterized by runny noses and pneu- monia. The Ornate Box Turtle (Terrapene ornata ornata) seems to be especially sensitive to respi- ratory disease in captivity, and the respiratory signs seem to be particularly devastating in this species. Enrofloxacin and cefotaxime are com- monly used antibiotics.

In Illinois, chronic bacterial p n e u m o n i a was diagnosed in 2 wild Eastern Box Turtles (T. carolina carolina) (Fig 5). Both turtles were found half buried in a dry creek bed and were severely emaciated and depressed. Histologi- cally, chronic inf lammation was identified in the nasal sinuses and lungs. A mixture of Gram- negative bacteria, including Morg'anella morgani, Acinetobacter calcoaceticus, Serratia marcescens, and Pseudomonas sp. were isolated f rom both turtles. No other pathogens were identified. The bacte- ria were considered the causative agents of the pneumonia . 24

Aural Abscesses

Aural abscesses or abcessation of the middle ear is a c o m m o n prob lem in chelonians, partic- ularly in box turtles. The exact cause of aural abscesses cannot be definitely stated, but a his- tory may include previous uppe r respiratory dis-

Internal Infections

A wide variety of bacterial infections can oc- cur. Often, multiple organ systems are involved. Liver a n d / o r kidney disease is c o m m o n because of the septic nature of turtle diseases and the filtering action of these 2 organs. Chronic hep- atitis and chronic kidney disease (the latter re- sulting in gout f rom elevations of uric acid in the blood) are routinely seen. Infections of the heart are also common. Blood tests are useful for the diagnosis of these and other prob- lems.26-29

Organ Failure

Older box turtles are subject to organ failure, most often resulting f rom chronic infection or other longstanding disease involving 1 or more organs. Diseases that usually accompany advanc- ing age in o ther animals also affect elderly box turtles (eg, ar ter iosclerosis) . .Blood chemistry analysis is necessary to diagnose these cases. 26-29

Bot Fly Infestation (Myiasis)

Box turtles are commonly subject to the rav- ages of migrat ing bot fly larvae. These large parasites are different f rom the much smaller maggots (larvae of other flies). The adult flies deposit their eggs on the skin a n d / o r mucous membranes , and the newly hatched larvae pen-

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156 Rosskopf Jr. and Shindo

etrate into the body and form large, visible lumps where they come to rest, resembling ab- scesses. These grubs may cause substantial tissue damage and mechanical interference for the turtle, and some turtles die as a result of this infestation.

Maggot Infestation

Fly strike and maggot infestations are com- mon, especially among wounded or sick box turtles. These turtles are virtually defenseless, and flies can easily take advantage of their weak- ened condition. Traumatized or diseased box turtles should be kept indoors or within a screened enclosure during their convalescence.

Shell Disorders

Shell rot occurs when either the upper shell (carapace), lower shell (plastron) or both de- velop erosions. This condition usually results from injury or chronic exposure to filthy envi- ronmental conditions. Malnutrition and infec- tion are frequent predisposing factors. Meta- bolic bone disease may result in grotesque shell development in terrestrial turtles. ~~

Dogs, fires, lawn mowers, and automobiles often inflict serious injuries to the shell.

Overgrown Upper Jaw

The upper jaw of some captive terrestrial tur- tles may occasionally overgrow. Abnormal wear patterns resulting from prior injury or a steady diet of soft food may be involved. Periodic trim- ming of the upper mandible is necessary in these cases. Metabolic bone disease may be involved in jaw overgrowthY, S~

Foreign-Body Ingestion

The intestinal impactions occasionally seen in tortoises are rarely a problem in terrestrial tur- tles. However, eating snail shells occasionally causes intestinal tract damage in box turtles. Certain individuals seem to be plagued by this problem, and should not be fed whole snails. Most box turtles can eat snails and snail shells safely.

Figure 6. Box turtle laying eggs. Courtesy of Phil Angermeyer.

Intestinal Parasites

A variety of roundworm and strongyle-type worms can parasitize captive terrestrial turtles. Reinfection results when pet turtles are permit- ted to feed in an environment in which feces are allowed to accumulate and contaminate food. Numerous deaths of terrestrial turtles occur ev- ery year from intestinal rupture and peritonitis resulting from heavy intestinal parasitism.

Few terrestrial turtles are parasite-free; there- fore, yearly fecal exams a n d / o r routine deworm- ings are recommended. Strict attention to hy- giene, frequent soil changes, and periodic rota- tions of habitats to reduce exposure to these parasites are also recommended.

Intestinal Protozoa

These parasites can cause disease and are oc- casionally found in captive box turtles. Diagnosis of Giardia, Trichomonas, and other oganisms re- quires direct microscopic examina t ion of the feces or the use of special tests, such as the Trichrome stain, available through exotic ani- mal laboratories.

Reproductive Problems

Egg-binding is a fairly common problem among female turtles. This condition results when a gravid female cannot pass an egg by herself. She typically strains excessively against the obstruction (Fig 6). The egg may be over- sized or there may be metabolic or other reasons

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for her inability to pass the egg without assis- tance. Radiographs are usually taken to confirm that the female is, in fact, fertile with eggs. Then, calcium and ho rmone injections and sometimes aspiration of the egg's contents are necessary to expel the egg.

Several other conditions are seen in repro- ductively active female turtles. Metritis and egg- yolk peritonitis are the most common.

Erections in Males

During the mating season, male terrestrial turtles periodically prot rude and rhythmically fan their penises. This copulatory organ is flower- shaped and purple, and may appear unusual or abnormal to those unfamiliar with turtles. It is most often mistaken for a prolapsed organ and may be treated as such by those unfamiliar with turtle anatomy and mating habits.

Prolapses

Prolapses of the uterus, intestine, urinary bladder, or penis (paraphimosis) may occur. The last condit ion occurs if the engorged penis cannot be re turned inside the body cavity, due to small vent size or previous trauma to the enlarged organ. Administration of an anesthetic and skillful manipulation of the organ is usually necessary to correct the prolapse. Clumsy at- tempts by owners may permanent ly damage the involved organs.

Ocular Disorders

Various disorders involving the eyes of turtles are noted from time to time. These include cat- aracts, corneal ulcers, puncture wounds and other traumatic injuries, infections, maggot in- festation, conjunctivitis, and dry eye (keratitis sicca).

Ivermectin Toxicity

As with other chelonians, a flaccid paralysis that is irreversible will occur with the use of Ivermectin.7, 21

Aquatic Turtles Nutritional Disorders

Vitamin A Deficiency--Swollen Eye Syndrome

Hypovitaminosis A is most prevalent in young aquatic and semiaquatic turtles fed diets of un- supplemented greens (iceberg lettuce), meat, and poorly formulated commercial diets. The turtles may be anorectic and growing poorly. Signs include edema, inflammation, and infec- tion of the eyes, resulting from squamous meta- plasia of Harderian glands and respiratory dis- ease. a2

Soft Shell

Water turtles must receive adequate levels and proport ions of many essential minerals (es- pecially calcium), vitamin D> and unfi l tered sunlight. An abnormally soft shell will result if any of these 3 necessities is missing, present at an inadequate level, or totally unavailable.

An adequately balanced diet and sufficient periods of exposure to unfiltered sunlight or to an artificial substitute (Vita-Lite TM) should be provided to both prevent and treat this condi- tion. Trea tment also involves dietary supplemen- tation and periodic injections of a calcium sup- p lement and vitamin D> Many hobbyists im- merse turtle blocks (solid blocks of chalk or plaster of Paris) in the water provided for their water turtles in the hope of preventing soft-shell problems. Unfortunately, these water turtles cannot benefit from the calcium carbonate pro- vided by these products unless it is ingested.

Shell Deformity (Metabolic Bone Disease)

General malnutri t ion (especially protein de- ficiency and mineral imbalances or deficiencies) in young, growing water turtles will result in 1 or more of the following consequences: deformity, pyramidal mounding of the carapace (top shell), premature cessation of shell growth, and scoliosis of the spine. Captive water turtles rarely possess normal-appearing shells because of the universality of these problems among them.

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158 Rosskopf fi. and Shindo

Egg Binding

Another disorder resulting, in part, f rom min- eral imbalance or outright mineral deplet ion is egg binding. This condition results when a fe- male water turtle is physically unable to pass 1 or more eggs without intervention or assistance. Clinical signs include obvious straining and rest- lessness, or p ro found lethargy.

Calcium is necessary for the p rope r contrac- tion of muscles, including those of the uterus. When this particular mineral is deficient in a gravid female, egg binding is likely. Malnutri- tion, lack of exposure to unfil tered sunlight, and pre-existing disease are the usual predisposing factors that contr ibute to this serious, often life- threatening condition.

Calcium and h o r m o n e injections, as well as digital manipula t ion of the egg, are usually em- ployed to relieve this condition. Sometimes, a needle can be inserted into the egg to aspirate its contents and collapse it, thereby making it easier to pass.

Bacterial Infections

Captive water turtles are prone to bacterial infections because malnutr i t ion and poo r hy- giene practices are commonplace . Fur thermore , injuries received by water turtles in the course of their day-to-day living tend to become readily infected because of the frequently high bacterial counts in their aquatic environments.

Respiratory Infections

URT disease and pneumon ia are very com- m o n among water turtles. Clinical signs may include nasal discharge, swollen eyes, sneezing, coughing, gasping, open-mouthed breathing, lethargy, weakness, and listing to one side. Ag- gressive antibiotic therapy and supportive care are required to bring these serious cases to res- olution.

Aural Abscesses

Infect ion of one or both middle ear canals is a relatively f requent occurrence. Surgery is nec- essary to open up the infected canal and manu- ally remove the pus that accumulates within its interior. Injectable antibiotics and vitamin A

therapy, plus dietary change, is used in treat- ment, as in terrestrial turtles. 25

Septicemia

There are a host of bacteria that are capable of causing severe body-wide infections in water turtles. Often, minor infections, such as those caused by wounds, increase in severity because the bacteria that were in t roduced into the initial wound are capable of traveling th roughou t the body by way of the bloodstream. Malnourish- men t ensures a weak defense against this inva- sion on the par t of the host, and the infect ion spreads. As vital organs become involved, addi- tional symptoms and a general deter iorat ion are noted. Often, ext reme redness of the skin and bleeding into it will be noted when a water turtle suffers f rom septicemia. Aggressive antibiotic therapy and supportive care are required to br ing these serious cases to resolution. Enro- floxacin, cefotaxime, and amikacin are fre- quently used antibiotics.

Shell Rot

Lesions of the shell may result f rom direct injury to its surface and substance, or as a con- sequence of malnutri t ion, generalized deteriora- tion, and infection. Bacteria a n d / o r fungi may be responsible for infections of the shell. Pri- mary forms of shell rot may also occur f rom the ingestion of shellfish laden with disease-causing bacteria ( Beneckea chitonovora) 33,34

Algae may colonize shell-rot lesions or be a pr imary cause of shell rot, a l though it is not u n c o m m o n for this agent to take up residence on the carapaces (top shells) of perfectly normal and healthy water turtles. This is usually an in- dication that the water quality of the tur t le 's enclosure needs improvement .

In water turtles, bacterial infections of the shell can often become systemic, resulting in septicemic cutaneous ulcerative dermatitis, ini- tially, shell lesions are the only external indica- tion of this condition. Infected turtles with sys- temic involvement may develop additional symp- toms, however, ranging f rom anorexia and ext reme lethargy to paralysis of limbs and mus- cles (primarily in the neck). Causative agents can be Aeromonas hydrophila, Citrobacter freundii, and Serratia sp. If begun early enough, systemic

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and topical treatment often resolves this condi- tion. 12

The Eastern Diamondback terrapin (Mala- clemys terrapin littoralis) is reputed to be suscepti- ble to shell rot if the water conditions are not brackish, as in nature. We used to see this in practice when diamondback terrapins were seen in the pet trade. 8

Mouth Rot

Bacterial infection of the oral lining (mouth rot or infectious stomatitis) is usually a conse- quence of malnutr i t ion a n d / o r body-wide ill- ness. Excessive salivation and redness of the oral lining are typical early symptoms of mouth rot. Later, as the disease progresses, accumulations of cheese-like pus can usually be noted within the mouth. An objectionable odor from the mouth may be detected as well. Injectable anti- biotics, vitamins, and appropriate supportive care, including periodic cleaning of the mouth, are necessary in the treatment of this serious condition.

SalmoneUosis

In the not too distant past, water turtles, be- fore their introduction into the pet trade, were frequently housed in ponds and septic tanks contaminated with human sewage and other types of waste. Because of this environmental circumstance, these turtles were continually ex- posed to and became asymptomatic carriers of a myriad of potentially harmful intestinal bacteria.

A strong resistance to many of these bacteria (notably Salmonella spp. and Arizona spp.) en- sured that these turtles would not become ill and succumb to the diseases caused by them. The human handlers (frequently children) of these turtles, however, did not share this same degree of bacterial resistance when the latter reached the pet market. Transmission of Salmonella spp. and other harmful intestinal bacteria occurred as a consequence of turtle handling, resulting in numerous cases of human Salmonellosis.

Public health laws now require that no water turtle with a carapace (upper shell) diameter less than 4 inches can be shipped into or sold in the United States, with certain exceptions. Cur- rently, in practice, we are seeing numerous tiny water turtles being sold on the streets of Los

Angeles. These are obviously illegal, and little or nothing is being done to enforce the law.

Parasite Problems

Intestinal Parasites

A wide variety of intestinal parasites are found in water turtles, including roundworm-type worms, tapeworms, and flukes. Stool analysis and white-blood-cell counts are useful in diag- nosing parasite problems2 ~

External Parasites

Recently captured water turtles are often par- asitized with leeches. These should be carefully removed, and the victimized turtle should be protected with a relatively short course of inject- able antibiotics.

Traumatic Injuries

Most traumatic injuries to water turtles result from aggressive encounters between turtles and between household pets and turtles. Many water turtles are territorial (ie, Red-Eared Sliders and Soft-Shelled Turtles) or pugnacious (ie, Snap- ping Turtles), and fighting between water turtles (especially between individuals of the same spe- cies) often results in serious wounds to the shell a n d / o r soft tissues. Water turtles of widely vary- ing sizes should not be housed together. Adher- ence to this recommendat ion will help to reduce the number of traumatic injuries incurred.

Injuries between individuals during the mat- ing process are common. Males may become overly aggressive during copulation and inflict bite wounds on the female. The male's rapid and sometimes premature withdrawal of an en- gorged penis may traumatize the female's repro- ductive tract.

It is not at all u n c o m m o n for household pets (especially dogs) to inflict serious, often life- threatening wounds to the shells a n d / o r soft tissues of water turtles during unprovoked en- counters.

Epoxy resins and acrylic glues are often used in the repair of shell injuries in water turtles. 8-m

Foreign-Body Ingestion

Water turtles may ingest any number of a variety of foreign objects (fish hooks, gravel,

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160 Rosskopf Jr. and Shindo

aquarium parts, etc). Rarely, if ever, is the actual act of swallowing the foreign body witnessed. Usually a water turtle is presented to a veterinar- ian because of poor appetite, weight loss, a n d / o r emaciation. Radiography is usually nec- essary to confirm the diagnosis. Sometimes the ingested foreign body does not show up on the x-ray, and a barium study is necessary to make the diagnosis. Surgery must be employed in most cases to remove the foreign body.

Drowning

Hobbyists frequently house small or juvenile water turtles within enclosures that possess water levels that are too deep, or within enclosures that are hazardous in some other way. All water turtles should be provided with a resting/bask- ing area. Failure to do so may result in exhaus- tion and drowning. Juvenile water turtles often become trapped under plants and rocks or be- hind filters and drown. All such environmental hazards must be removed or corrected.

Emergency measures may save some drown- ing victims because a turtle's heart will continue to beat for many hours after apparent death has occurred. Treatment for drowning involves turn- ing the turtle upside down and moving its legs to force water from its lungs. The ambitious care- giver may also want to perform mouth-to-nose artificial respiration. If the turtle is successfully revived, then antibiotics and appropriate sup- portive care are necessary until the victim has fully recovered.

Beak Overgrowth

Like birds, turtles and tortoises have beaks (the horny coverings of both the upper and lower jaws), which tend to grow continuously for life. In the wild, the pursuit of day-to-day living seems to keep the rates of wear and growth in equilibrium. In captivity, however, these cover- ings tend to overgrow, and require periodic trimming.

Metabolic bone disease frequently results in malformed beaks in all the chelonian spe- cies.3L:~2

Problems Involving Reproductive Organs (Other Than Egg-Binding)

Erections in Males

Erections of the penis, which occur most of- ten during the mating season, may be discon- certing or bewildering to the novice observer. This condition is perfectly normal, but is most often confused with a prolapse (see prolapses).

Paraphimosis

Occasionally, the fully engorged penis re- mains so and cannot be retracted. This condi- tion is called paraphimosis. Veterinary intmwen- tion is necessary in these cases to prevent per- manent damage to the penis. Ketamine usually works well to relax the organ.

Penile Paralysis

A water turtle's penis sometimes becomes par- alyzed. The cause of this condition is unknown. Besides the obvious liability to the turtle, muti- lation of the exposed and vulnerable penis by other turtles is very likely. The penis can some- times be replaced into the turtle's cloaca. In most cases, however, the penis must be ampu- tated, which creates no problems for the turtle other than the inability to copulate, because this organ is not used for urination.

Prolapses

A prolapse occurs when a particular organ is allowed to invert itself and protrude through the ordinary external opening of that organ. In con- trast to this situation with tortoises, prolapses of the uterus or intestine are rarely seen in water turtles. If the turtle owner suspects a prolapse, then the involved organ should be kept moist and protected from trauma, and veterinary at- tention should be sought immediately.

Ivermectin Toxicity

A severe paralytic reaction occurs if Ivermec- tin is used in water turtles, as in other cheloni- arts.7, 21

References l. Jacobson E, Gaskin JM, Brown MB, et at: Chronic upper

respiratory tract disease of free ranging desert tortoises, Xerobates agassizii. J Wildl Dis 27:296, 1991

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2. Knowles C: A Survey for Diseased Desert Tortoises in and Near the Desert Tortoise Natural Area, Spring, 1989. Report prepared for The Bureau of Land Management, Riverside, CA, June 1989, Contract No. CA950-[T9-23]

3. RosskopfJr WJ: The upper respiratory syndrome in cap- tive desert tortoises: diagnosis, treatment, and manage- ment. Proceedings of the First International Symposium on Turtles and Tortoises, Conservation and Captive Hus- bandry, Chapman College, Orange, CA, 1990, pp 108- 112

4. Origgi F, Jacobson E: Diseases of the respiratory tract of chelonians. Vet Clin North Am Exotic Anim Pract 3:537- 549, 2000

5. Snipes KP, Biberstein EL: Pasteurella testudinis: a parasite of desert tortoises. IntJ Sys Bact 32:201, 1984

6. Jacobson E: The desert tortoise and upper respiratory tract disease. Bull Assoc Reptile Amphib Vets 4:6, 1994

7. Boyer TH: Turtles, tortoises, and terrapins, in Mader D (ed): Reptile Medicine and Surgery. Philadelphia, Saun- ders, 1996, pp 332-336

8. RosskopfJr WJ: Shell disease in turtles and tortoises, in Kirk RW (ed): Current Veterinary Therapy, Small Ani- mal Practice, IX. Philadelphia, Saunders, 1986, pp 751- 759

9. Kishimori J, Lowbart T, et al: Chelonian shell fracture repair techniques. Exotic DVM 3.5:35-41, 2001

10. Barten S: Shell damage, in Mader D (ed): Reptile Med- icine and Surgery. Philadelphia, Saunders, 1996, pp 413- 417

11. CooperJE, Geschmeissner S, Bone RD: Herpes-like virus particles in necrotic stomatitis of tortoises. Vet Rec 123: 554, 1988

12. Havkewicz K: Dermatology of reptiles: a clinical ap- proach to diagnosis and treatment. Vet Clin North Am Exotic Anim Pract 4:441-461, 2001

13. Jacobson, E: Diagnosis of reptilian viral disease. Proceed- ings of the AAZV, Columbus, OH, October 1999, pp 1-5

14. Posthaus H, Marschang R, et al: Study on herpesvirus infections in land tortoises in Switzerland. Proceedings of the AAZV, 1997, pp 17-18

15. Frye F: Biomedical and Surgical Aspects of Captive Rep- tile Husbandry, 2 nd Ed, Vols. I and II. Melbourne, FL, ga-eiger Publishing, 1991

16. RosskopfJr WJ, Woerpel RW, et al: Abdominal surgery in turtles and tortoises. Compend Contin Educ Pract Vet 4:326-329, 1983

17. Johnson J, Averill-Murray R, Jarchow J: Captive care of the desert tortoise Gopherus agassizii. J Herpetolog Med Surg II:8-16, 2001

18. Bouner B, Denver M, Garner M, et ah Entamoeba inva-

dens roundtable discussion, j Herpetolog Med Surg II: 17-22, 2001

19. Cranfield MR, Graczyk TK, Denver MC, et al. New ap- proaches for the diagnosis of entamoeba infections in captive reptiles. Proceedings of the ARAV, 1999, pp 17-18

20. Fudge AM (ed): Laboratory Medicine: Avian and Exotic Pets. Philadelphia, Saunders, 2000

21. Carpenter J, Mashima T, Rupiper D: Exotic Animal For- mulary. Manhattan, KS, Greystone, 1996

22. Lawton MPC: Neurological diseases. Opthalmology, in Beynon PH, Lawton MPC, Cooper JE (eds): Manual of Reptiles. Gloucestershire, UK, British Small Animal Vet- erinaty Association, 1992, pp 128-134

23. Donoghue S, LangenbergJ: Nutrition, in Mader D (ed): Reptile Medicine and Surgery. Philadelphia, Saunders, 1996, pp 148-174

24. Evans RH: Chronic bacterial pneumonia in free-ranging Eastern box turtles (Terrapene carolina carolina). ) Wild/ Dis 19:349, 1983

25. Murray M: Aural abscesses, in Mader D (ed): Reptile Medicine and Surgery. Philadelphia, Saunders, 1996, pp 349-352

26. Hawkey CM, et al: The diagnostic value of hematology in reptiles. Proceedings of the Third International Collo- quium on the Pathology of Reptiles and Amphibians, Orlando, FL, 1989, pp 56-57

27. Montali RJ, et al: Leukocytes and inflammation in rep- tiles. Proceedings of the Third International Collo- quium on the Pathology of Reptiles and Amphibians, Orlando, FL, 1989, pp 64-65

28. Rosskopf WJ, Woerpel RW: Hematology and the use of serum chemistry profiles in reptile diagnostics. Proceed- ings of the Third International Colloquium on the Pa- thology of Reptiles and Amphibians, Orlando, FL, 1989, pp 58-61

29. RosskopfWJ: Disorders of reptilian lenkocytes and eryth- rocyte, in Fudge AM (ed): Laboratory Medicine: Avian and Exotic Pets. Philadelphia, Saunders, 1999, pp 198- 204

30. Boyer TH: Metabolic bone disease, in Mader D (ed): Reptile Medicine and Surgery. Philadelphia, Saunders, 1996, pp 385-392

31. Mader D: Metabolic bone disease in caplive reptiles. Vivarium 2:12, 1990

32. Donoghue S, McKeown S: Nutrition of captive reptiles. Vet Clin North Am Exotic Anita Pract 2:69-91, 1999

33. WallachJD: The pathogenesis and etiology of ulcerative shell disease in turtles. Aquatic Mammals 4:1, 1976

34. Wallach, JD: Ulcerative shell disease in turtles. Identifi- cat Prophylaxis Treat Inti Zoo Yearbook 17:170, 1977