STEPHEN DIVERS B.Sc.(Hons.), M.I.Biol., C.Biol., B.Vet.Med., M.R.C.V.S..
Presented to the British Chelonia Group Symposium, 27 April 1996
The Structure and Diseases of the Chelonian Shell
Turtles, tortoises and terrapins are unique amongst reptiles in being amongst the oldest living relics of the class Reptilia and possessing a bony shell. This shell is undoubtedly the most obvious physical characteristic of this order comprising of 244 species in 2 suborders, Pleurodira and Cryptodira.
Structure of the Shell
The shell is composed of an upper domed part called the carapace and a lower flatter plastron. The two parts are joined by bridges on either side with openings at the front and back for the head and limbs. The shell is an extension of the skin and merges with the skin that covers the limbs and head. The outer layer of shell is made up of horny shields or scutes arranged in a specific order and the colour of the shell varies widely from species to species.
The shell is developed from a standard skin structure with a dermal and epidermal components, however the lower layer or dermis has become ossified (bony) and the epidermis has been modified into a horny keratinised outer covering. The shell starts to develop within the incubating egg but this process is incomplete by the time of hatching. Continued shell growth and development is dependent upon an adequate intake of calcium and exposure to ultraviolet light for endogenous vitamin D3 production. The shell grows by producing deeper larger scutes which are visible under the smaller older scutes, such that a rim of growth is obvious. In most cases, the old scutes are retained giving rise to a number of rings, however these scutes may be shed (as in Red-eared Terrapins) making ageing from counting the rings very imprecise. The ribs and spinal column are fused to the carapace. This gives the chelonia the unique attribute of having their pectoral (shoulder) and pelvic (hip) girdles within their rib cage!
Diseases of the Shell
Considering the large nature of the shell and its primary function as an integument (skin) structure the shell can be diseased by a number of different organisms and for a number of different reasons. Bacterial, fungal, viral and parasitic infections have been documented, while of the non-infectious problems, metabolic bone disease, thermal and chemical burns, trauma and systemic disease are most often encountered. The majority of these diseases are caused or exacerbated by poor husbandry (environment and nutrition) and although potentially serious and even life-threatening, prompt veterinary attention carries a good prognosis in the majority of cases.
Primary infectious diseases are those affecting the integument with, at least initially, no internal or systemic involvement. Bacterial shell disease is quite common and frequently gram-negative bacteria are cultured and isolated. Aquatic species tend to be affected by poor filtration and unhygienic water conditions. Septicaemic cutaneous ulcerative disease (S.C.U.D.) is a severe bacterial shell infection often caused by Citrobacter spp. bacteria which is seen commonly in aquatic, soft shell turtles (Trionyx spp., Apalone spp.). The terrestrial species appear more prone to shell damage from blunt trauma or thermal injury, which can become secondarily infected.
Fungal diseases are less common and often seen where skin cases are inappropriately diagnosed and treated with broad-spectrum antibiotics by owners. In these instances the use of broad-spectrum antibiotics has killed all the bacteria present, including the normal bacterial flora of the shell, enabling a secondary fungal infection to take place. Primary fungal infections are more commonly diagnosed in the aquatic species: wound debridement (exposure and cleaning), fungal culture, and application of specific anti-fungal preparations are often successful.
Viral diseases represent a relatively rare diagnosis in reptile practice but this is probably a reflection of the difficulty in isolating and identifying viruses and the fact that viral lesions can quickly become contaminated with a secondary bacteria or fungus. Primary viral skin diseases have been identified in turtles (e.g. grey patch disease of green sea turtles) but the lesions are usually restricted to the skin and not the shell. Viral bodies are extremely small and beyond normal light microscopy.
Ectoparasitic diseases are less commonly seen in chelonia than they are in snakes and lizards, but ticks are still seen with frequency especially in wild caught specimens. However, in most cases these ectoparasites feed on the softer skin tissue adjacent to the shell.
Primary non-infectious diseases are more common in the solitary pet reptile.Thermal burns may be acute due to extreme damage such as those induced by overhead ceramic heaters. Alternatively, the tortoise may find itself in a garden bonfire, having previously sought sanctuary within a pile of garden refuge. Garage and house fires, although sporadic and thankfully rare occurrences, have resulted in serious burns to the housed or hibernating chelonians. Thermal injury can be much more insidious in nature and the use of under floor heat mats can certainly cause chronic damage to the plastron. In these cases particularly, the thermal injury does not become apparent until secondary bacterial infection becomes obvious.
Trauma is often seen in garden tortoises following an attack by a dog or fox, while hibernating species may succumb to the effects of rats if the hibernating quarters are not rodent-proof. Accidental damage caused by the careless use of mallets, sledgehammers, and lawnmowers can often lead to severe damage to the carapace with shell fractures and displacement of the fragments into the chelonian body. Damage to the rim of the shell can often be treated conservatively by adopting a standard veterinary approach to wound management. Deep, central wounds to the carapace and plastron can be primarily repaired with the use of fibreglass patches and epoxy resin, although it must be stressed that such repairs should only be carried out on fresh, uninfected wounds. The shell is living tissue, and such damage may cause profuse bleeding, resulting in life-threatening anaemia and the need to perform blood transfusions in extreme cases. The sensitive nature of the bony shell also makes anaesthesia and analgesia essential before any surgical shell repair is undertaken. Infected wounds must be thoroughly debrided and cleaned under anaesthesia and the use of wet dressings is usually employed. Primary repair is unlikely to be recommended but may be possible if all infection is removed and the infectious disease controlled.
Chemical burns are a rarity but the author has seen a case of a chemical shell burn due to contact with industrial hydrochloric acid. Obviously, such materials have no place in proximity to any animal.
Systemic diseases can affect many organs including the shell. Metabolic bone disease is a term used to describe a group of diseases affecting the bones of the skeleton and shell dermis. An absolute lack of calcium, a diet with a calcium:phosphorus ratio of less than 1:1, a lack of vitamin D3 (usually by deprivation of ultraviolet light) or a high protein diet can produce this problem. The initial sign is often a softening or pyramiding of the shell but as the disease progresses so the pull of the thoracic and pelvic muscles cause the carapace to sink giving the shell a saddle-like appearance. Radiographs and blood calcium and phosphorus evaluations provide the diagnosis and although treatment will arrest the condition and improve the strength of the bones the distortion to the shell is permanent.
Any disease which affects the metabolism of the chelonian will affect the shell. Stunting of growth due to undernutrition is demonstrated by a lack of growth lines, although more frequently extensive growth lines indicate the commoner problem of overfeeding. Septicaemia is life threatening and may cause haemorrhages under the scutes giving a diffuse speckled red pattern to the shell. Young growing animals are particularly affected by nutritional imbalance.
Many owners prefer to clean their tortoise's shell and apply oil to add a decorative shine to the carapace. Keeping the shell clean is important and will help prevent shell infections. However, the use of topical oils, although not detrimental, have no real beneficial effect on the health of the shell. Good husbandry and sound nutrition are what are important for a healthy shell.
Measuring the length of the horizontal carapace can give an indication of the health status of a chelonian when compared to the animal's weight. This technique is known as the Jackson Ratio and was first described by Jackson in 1980. These weight-length graphs have been produced for a variety of species, in particular the Mediterranean tortoises (Testudo graeca and Testudo hermanni) and the red-eared terrapin (Trachemys scripta elegans). In summary the shell is an indicator of the well-being of any chelonian and so should be inspected with regularity.
THE TORTOISE CAESAREAN
Reproductive problems in tortoises represent a challenge to the veterinary surgeon, not least because in order to gain access to the reproductive tract (ovaries, oviducts and shell glands) one must first negotiate the shell. Its surgical uniqueness is somewhat more problematical and of immense interest to the reptile surgeon. In most cases, reptile (particularly lizard and snake) outer surfaces can be incised with a sharp scalpel blade providing access to the deeper tissues and organs. However, with a tortoise some form of high powered surgical saw is needed!
Surgical access to the coelomic cavity of the tortoise (similar to the abdominal cavity of mammals) is often employed to remove abnormal eggs from the oviducts/shell glands. Affected animals often present in a state of hyperactivity (nest searching) or if left unaided, become lethargic and anorexic. A radiograph or X-ray will confirm the presence of eggs. If the eggs appear to be normal in both size, shell thickness and calcification, then all that may be required is the provision of a suitable nest site such as loose soil/sand mixture in a sunny position within the garden enclosure. If this fails to work then 1-2 injections of the hormone oxytocin are usually effective in stimulating egg laying as long as the blood calcium levels are adequate. If the eggs are abnormal on the radiograph, that is to say they are too large or of an abnormal shape to fit through the pelvic opening, or if an egg is broken then induction of egg laying may actually make matters worse. In these, quite rare cases, it is necessary to perform surgery.
Anaesthetic and Surgical Procedure
Before surgery, it is important to ensure that the animal is stabilised. The tortoise may be dehydrated, have a severe egg peritonitis if a broken egg is present or be suffering from another debilitating disease. Blood samples for haematology and limited biochemistry enable the vet to assess the animal's ability to undergo surgery. The use of an intravenous or intraosseous drip which in addition to the use of modern anaesthetics such as propofol and isoflurane makes modern reptile anaesthesia a safe procedure in the vast majority of cases.
Once stable, the tortoise is anaesthetised with an intravenous injection of propofol, which causes a rapid loss of consciousness. Then, a small tube is inserted into the wind pipe so that oxygen and the anaesthetic gas, isoflurane, can be administered during the operation. The tortoise is then turned upside down and the plastron is thoroughly scrubbed and disinfected. There are various instruments to cut through bone, but I use an oscillating sector plastor/bone cutter. The serrated edge oscillates, it does not rotate, so it will cut through rigid bone but merely wobbles soft tissue causing less damage. Using this saw, a bone flap is cut in the plastron (underside of shell) being careful not to go too deep and risk damaging the two paired veins that lie just under the plastron. The bone flap is cut in the preoperative room as this generates dust, but once the flap has been cut, the tortoise is moved into a sterile theatre before the square of shell is removed to reveal the body cavity.
When in theatre, the tortoise is placed on a heat mat and connected to an ECG and respiratory monitor. A sterile, transparent drape covers the tortoise and the shell flap is removed and placed in sterile saline to keep this bone tissue alive and healthy as it will have to be replaced at the end of the operation. The coelomic membrane is cut between the two ventral veins to reveal the body cavity. It is usually possible to see the heart beating during the operation. Once in, it is a relatively simple task to locate the eggs within the oviducts and remove them via single or multiple salpingotomy (oviduct/shell gland) incisions. If there are only 1 or 2 retained eggs then they can be removed. However, if there is a peritonitis infection due to a broken egg, a large number of retained eggs or the tortoise has a history of reproductive problems, then a complete ovariohysterectomy removing both ovaries, oviducts and shell glands is performed - essentially neutering the female and preventing any future reproductive problems.
Once the reproductive surgery has been completed the coelomic membrane is sutured back or stitched in place and the bone flap is replaced in its original orientation. The shell is cleaned and dried before 4-6 fibreglass mesh patches and fibreglass resin are used to effect a rigid and permanent repair to the shell. Post-operatively, the tortoise is maintained on a drip at 28oC and may be given antibiotics if required. In uncomplicated cases the tortoise usually starts eating by the next day and is then able to go home.
Gastro-Intestinal Nematode Parasites Of Mediterranean Tortoises (Testudo spp.)
Mediterranean tortoises consume large quantities of food during the warm summer months. However, these conditions of plenty also provide a tortoise's intestinal worms with an ideal environment in which to thrive and reproduce. During the summer months tortoises may not exhibit any obvious signs of parasitism. However, during post hibernation period of late spring or the cooler months of autumn, parasitic disease and even death can occur because of the effects of intestinal worms. These problems can be prevented or at least minimised by appropriate veterinary care.
Keymer (1978) reported the two main groups of intestinal worms to infect Testudo tortoises to be Anisakoidea (Angusticaecum spp.) and Oxyuroidea (Tachygonetria and Atractis spp.). This study, based on the postmortem examination of 144 tortoises, reported that nematode infestations were found in 43.8% of all the tortoises examined. Holt, Cooper and Needham (1979) examined 70 live tortoises and diagnosed gastrointestinal worms in 30%. Therefore, scientific evidence suggests that your tortoises have a 30-40% chance of being currently infected with worms!
The life-cycles of many reptile parasites have not yet been conclusively described. The life cycle of the oxyurid roundworms is direct without intermediate hosts, while the life cycle of most members of the Anisakoidea roundworms is indirect. However as far as I am aware no intermediate host for the tortoise Angusticaecum has been identified and therefore this parasite probably has a direct life cycle as well. The direct life cycle of these two important worms results in the adult worms within the intestines producing thousands of eggs which are deposited in the garden (or vivarium). These eggs hatch into larvae which, after a short period of time, become infective and are ingested with food as the tortoise feeds. During the autumn the eggs may remain dormant on the ground and only develop into infective stages during the following spring. The practical outcome of these biological features in the captive situation of confined space is a high density of infective material leading to a high worm burden in the tortoise.
Intestinal Worms and Disease
It is probably true to say that most tortoises with worms do not show obvious clinical signs. However, these parasites compete with the tortoise for the food material within the intestines, and food that an intestinal worm uses is at the expense of the efficiency of the host (tortoise). Therefore they are detrimental being responsible for reduced growth and breeding performance. If a female tortoise has a moderate worm burden and lays 5 eggs a year, it may be possible to improve her breeding output to 6 eggs a year if the worm burden was eliminated or reduced. Similar improvements in growth rate may also be attained in juvenile specimens that have their worm burden reduced. These subtle improvements may not seem important, but one extra hatchling would probably cover the costs of health checks and worming for both the adults in the year to come!
Worm burdens become more of a problem during periods of reproduction and stress, especially during early spring and autumn. Clinical signs of worms include diarrhoea, regurgitation, anorexia, poor weight gain/weight loss, breeding failure, adult worms passed in faeces, and even death can occur.
There is also a potential problem of abnormal host-parasite relationships. Testudo tortoises and the roundworm Angusticaecum have evolved together over thousands of years, and consequently in the wild, worm and tortoise live in a steady state. An efficient parasite does not kill its host. In the confinement of the vivarium or small garden parasite numbers can increase to abnormally high levels, capable of causing disease in the natural host. However, if an unnatural host such as a box tortoise or leopard tortoise becomes infected it is possible that, because the host has never been exposed to a particular parasite before and therefore has no inherent defence against it, small numbers of parasites could cause severe disease and even death. This is the reason why Entamoeba invadens, a normal gut protozoon of aquatic chelonia (natural host) can cause a fatal amoebic dysentery in snakes (unnatural host). It is obvious that different species of reptiles/ amphibians should not be mixed in captivity. Sometimes parasites cause disease when they take the wrong route in the host and arrive in a different organ.
Diagnosis and treatment
The chances are that existing tortoise populations will be infected with worms. A veterinary surgeon will often make a diagnosis of parasitism based upon the examination of a fresh faecal sample. Depending upon the type of parasite your veterinary surgeon will choose the most appropriate drug. I have found oxfendazole to be most effective against nematodes but other benzimidazole anthelmintics can be used, albeit repeatedly. Never attempt DIY diagnosis and treatment as effective treatment necessitates proper egg identification, and certain, commonly used, antheimintics (ivomeclin) can have fatal consequences if used in chelonia. In general worming is recommended during the spring (March/April/May) and again in late summer (August, September).
Surely our reptilian pets deserve the same level of care as our domestic dogs and cats. A routine health examination, faecal check and worming protocol will go a long way to improve tortoise health and should therefore form the basis of your chelonian health programme. Many owners are now having all new tortoises blood screened so that their, normal' blood results can be filed and used to assess a 'sick' blood result when the tortoise falls ill.
Finally, reptile health insurance is currently available through Exotic Direct on 0171 6806009/6806016.
References and further reading
Beynon P.H, Lawton M.P.C. and Cooper J.E. (1992). Manual of Reptiles. BSAVA, Cheltenham.
Frye, F.L. (1991). Biomedical and Surgical Aspects of Captive Reptile Husbandry. Second edition. Krieger, Malabar.
Holt, P.E., Cooper, J.E. and Needham, J.R. (1979). Disease of tortoises: a review of seventy cases. Journal of Small Animal Practice 20: 269286.
Jackson, O.F. (1980). Weight and measurement data on tortoises (Testudo graeca and T hermanni) and their relationship to health. Journal of Small Animal Practice 21, 409.
Keymer, I.F. (1978). Disease of chelonians: (1) Necropsy survey of tortoises. Veterinary Record 103: 548-552.
Mader, D. (1 996). Reptile Medicine and Surgery. WB Saunders, Philadelphia.
Testudo Volume Four Number Three 1996