John Chitty BVetMed CertZooMed MRCVS
Based on a presentation to the BCG Symposium at the Open University, Milton Keynes, on 12th May 2007
Respiratory disease is common in chelonia. A large part of this is due to husbandry practices and certain anatomical features of the reptile respiratory system. In chelonia gulping movements of the throat may be seen (gular pumping). It is thought that these are not linked to inspiration/expiration but are used to move air over the olfactory membranes in the oropharynx and nasal chambers respectively, except in freshwater turtles/terrapins and soft-shelled turtles where some degree of oxygen exchange may occur in the pharynx. Additionally the cloacal bursa and the skin may also be involved in respiration in these species.
Respiratory drive is principally by means of detection of low partial pressures of oxygen, unlike in mammals where it is raised carbon dioxide levels that drive respiration rates. This has implications in anaesthesia where use of pure oxygen may inhibit spontaneous breathing and slow recovery. However, it should also be noted that reptiles can withstand very low oxygen levels for extended periods. This may be due to their ability to switch from aerobic to anaerobic respiration.
In some species the respiratory system may have other functions. Certainly in aquatic chelonia the dorsally placed lungs may act as a buoyancy aid.
As mentioned earlier, certain features of the reptilian respiratory system predispose it to disease:
- Lack of a muscular diaphragm means that discharges cannot be coughed up.
- Many authors suggest that a poorly developed muco-ciliary escalator in the airways also reduces the ability of the reptile to clear discharges.
- Their ability to withstand long periods of hypoxia means that respiratory diseases are often well-advanced before signs are seen.
Clinical examination and history
In all cases it is essential to perform a full clinical examination and take a detailed clinical history. There are certain aspects of special importance in respiratory disease:
|Table 1. History taking in chelonian respiratory disease|
|Disease history |
(both of this problem and in the past)
|Species kept (mixed species?), mixing with new animals or owner contact with other reptiles, parasitic problems, treatments used by the owner, environmental disinfection.|
|Environment ||Temperature: too high may cause chronic dehydration and drying of mucous membranes; too low may result in lowered immunity and resistance to infection.|
Humidity: too high may promote excessive load of environmental micro-organisms; too low will lead to mucous membrane drying.
Sanitation: poorly sanitised vivaria have been associated with an increased incidence of respiratory disease.
Nutrition: although malnutrition is rarely a primary cause of respiratory disease, it may be a contributory factor in stress and immunosuppression. Specifically, hypovitaminosis A has been described as an underlying cause of LRTD and URTD (Lower/Upper Respiratory Tract Disease) in reptiles, especially chelonia.
The following may be indicative of respiratory disease and may be described by the owner or noted on clinical examination:
|Table 2. Clinical signs of respiratory disease|
|Dyspnoea/tachypnoea ||Dyspnoea may take the form of an obviously exaggerated respiratory effort, increased gulping motions in the throat (although need to be careful to distinguish from gular pumping – see above) or an extended neck.|
|Cyanosis of mucous membranes|
|Altered buoyancy ||Aquatic species|
|Generalised signs |
- Weight loss, lethargy, dehydration.
- Altered behaviour – all species may seek cooler areas and become less active. This is designed to lower metabolic rate to enable the animal to cope better with hypoxia from respiratory disease.
- Stomatitis. A careful examination should be made of the mouth as stomatitis and respiratory disease often occur together. Poor environmental conditions can be a part of the cause of either condition. In chelonia upper respiratory disease and nasal discharge may be an extension of stomatitis owing to the incomplete palate.
It is important to distinguish upper respiratory tract infection from lower. The following provides a guide – it is always important to remember that no such list can be definitive and even more important to consider that some will have both URTD and LRTD!
|Table 3. Distinguishing upper and lower respiratory disease signs|
|Lung noises on auscultation||Rarely referred noise||Sometimes|
|Unwell/systemic signs||Often not||Usually|
|Behavioural changes||Rarely, unless secondary to systemic disease||Often|
The clinical examination should include certain aspects. It is very important that, before handling (thereby increasing stress levels), the breathing should be observed for several minutes as to character and rate.
|Table 4. Clinical examination|
|Cloacal temperature||This will give an indication of the reptile’s environmental temperature and allows interpretation of the respiratory rate (as this will generally rise with increasing temperature).|
|Auscultation||This can be very difficult as it is hard to hear sounds through the shell (especially as these may be very quiet). Placing the stethoscope on the skin may result in excessive scraping noises of skin on stethoscope as the animal breathes or moves.|
Electronic stethoscopes may help as they are more sensitive and also have filters for certain frequency sounds.
Alternatively conventional stethoscopes can be used if a damp cloth is placed between diaphragm and shell. However, this will muffle the already quiet sounds.
8MHz Doppler devices can be used to auscultate the heart.
|Mouth ||Look for cyanosis, inflammation and the presence of discharges from the internal choanae and the glottis.|
|Nares and eyes||Look for discharges.|
The nares should be checked for occlusion by pieces of retained skin or dried discharges.
|Discharges||These should be examined grossly for colour and viscosity.|
Some should always be retained for cytology and culture/sensitivity.
Ancillary diagnostics are necessary to reach a definitive diagnosis:
This is one of the most useful diagnostic tools in lower respiratory tract disease. It is recommended that dorso-ventral, lateral and cranio-caudal views are obtained. The latter two views must be performed using horizontal beam radiography so the coelomic organs do not fall into the lung space thus allowing a clear view of the lung fields and a true indication of the organ positions in the animal. Organomegaly, including distension of hollow viscera, and ascites may be causes of dyspnoea in the absence of respiratory disease by compressing lung space. Sedation/anaesthesia are rarely needed for radiography of the lung fields.
In upper respiratory tract disease radiography is less useful owing to the many fine structures in this region and the lack of a well-developed sinus system.
Use of rigid endoscopy is extremely useful:
- Upper Respiratory Tract: endoscopes can be inserted via the nares (a 1.2mm semi-rigid needle scope is extremely useful in chelonia) or the internal choanae (using a 30º rigid endoscope allows a wide field of view). This allows detection of foreign bodies as well as directed sample-taking, including biopsy.
- Intra-pulmonic endoscopy: sedation or general anaesthesia is required. However, this technique allows for direct visualisation of the lung tissue and directed biopsy/sample collection. Radiography is required to direct to either the worst affected lung (in diffuse disease) or, where there are focal changes, towards the lesion. Two approaches are possible:
- Prefemoral. After aseptic preparation an incision is made in the cranio-dorsal portion of the pre-femoral area. This must be close to the septum horizontale. This is grasped and stay sutures inserted before the septum is incised and the scope inserted. The septum can be repaired at the end of the procedure. It appears necessary to take care when opening the septum as, in the author’s experience, inadvertent breaching of the septum at coelioscopy may be accompanied by considerable intra-pulmonic haemorrhage which appears at the glottis.
- Transcarapacial. This is the author’s method of choice and is particularly appropriate when investigating/treating focal masses. The carapace is prepared aseptically and a site selected. For focal lesions, radiography is used to locate the focus and a site directly above this is prepared. In diffuse disease the worst-affected lung is selected and a site selected lateral to the spine midway along the carapace. An orthopaedic drill is used to breach the carapace. Haemostats or a trocar are then used to enter the lung and an endoscope may then be inserted. Again lesions may be visualised and samples taken for histopathology, culture/sensitivity, etc. The great advantage of this approach is that the resulting hole may be left open (or a catheter inserted to allow treatment to be applied directly to the diseased tissue - see later).
Although unlikely to provide additional information about the respiratory disease, blood should be taken in all these cases. There is much information to be obtained about the presence of underlying disease, degrees of immunosuppression and the scale of the systemic white cell response to infection. The latter is very important in upper respiratory tract disease as in many of these cases the infection appears localised without a systemic response and so systemic therapies are not always necessary.
Where funds allow and where there is access to these facilities, these may be useful imaging techniques.
May be useful in the overall assessment of underlying disease and assessing gut parasite loads.
A sterile catheter may be inserted via the glottis. A small volume of saline is syringed into the trachea and then re-collected. This can be submitted for bacteriology/mycology, cytology/parasitology and virology. However, it should be noted that where there are focal lung lesions this technique is unlikely to isolate significant organisms. In chelonia an alternative approach is to perform a lung wash by inserting a needle via the pre-femoral fossa. This is particularly appropriate in cases of unilateral pneumonia.
In addition to the methods described above, bacteriological swabs may be inserted into the nares or internal choanae (URTD) or through the glottis (LRTD). The latter technique is, like tracheal washing, comparatively insensitive in isolating lung pathogens. Similarly, in URTD it should be remembered that many of the organisms isolated in these non-sterile sites will be of secondary importance. Samples can be submitted for aerobic, anaerobic and fungal cultures.
Cytology is a very useful tool in these cases. Tracheal washes, swabs from any region as well as endoscopically-obtained lung biopsies may be submitted for cytology. This may give an idea of the type of organism present (e.g. yeast vs bacteria) and so give an idea of appropriate therapy while waiting for culture/sensitivity results. Cytology may also reveal the presence of parasitic ova/larvae. In chelonian URTD scrapings of tongue mucosa are extremely useful and may reveal intra-nuclear inclusion bodies typical of herpesvirus infections.
Tissue biopsies and tracheal washes/swabs may be submitted for virological examination/culture. PCR tests are now available for detection of chelonid herpesviruses and Mycoplasmas. It is important that viral/mycoplasmal samples are taken and stored properly so the testing laboratory should always be asked how this should be done in order to reduce false negative results.
CAUSES, THERAPY AND PREVENTION
Upper Respiratory Tract Disease (URTD)
In some cases foreign bodies may be involved (e.g. pieces of hay or grass entering the nares. NB: this will result in a unilateral, rather than a bilateral discharge). However, typically it is an infectious disease often referred to as Runny Nose Syndrome (RNS).
Generally this involves inflammatory lesions of the nares, nasal cavity and, especially, the mouth and pharynx.
Symptoms vary from a simple discharge (clear to yellow-green) to an extremely unwell animal with swelling of the head and neck. In some cases there is extensive abscessation of the nasal cavity and destruction of surrounding bone. In very severe cases there may also be an associated pneumonia. The discharge from the nose is derived both from the nasal area and from the mouth (saliva).
Underlying (primary) factors include:
- Husbandry. Typically URTD is seen in the UK in the spring (post-hibernation) or in the autumn when temperatures drop. There will also be a rise in cases during periods of prolonged cool weather in the summer. Mechanical irritation by dust etc. may mimic, exacerbate or be an underlying cause of URTD in chelonia.
- Mixing of species. This is partly due to the different micro-organisms carried/tolerated by each species (see below) and partly due to the stress induced by mixing; hence the problems seen after individuals of the same species are mixed.
Anorexia is common though this may be an effect of the infection or a result of the underlying husbandry problems leading to the URTD.
There are many organisms associated with this syndrome:
|Table 5. Organisms associated with URTD in chelonia|
|Bacteria and Yeast ||A variety of micro-organisms may be found in the mouth and pharynx. These are almost certainly secondary (or even tertiary) factors in URTD, but may exacerbate the condition so it is important to use an appropriate anti-microbial either topically or systemically. Choice of drug should be based on cytology initially prior to culture and sensitivity results.|
|Mycoplasma spp ||Mycoplasmosis has been extensively described as a cause of URTD in North American tortoises, especially gopher tortoises (Gopherus agassizii). Recently M. agassizii has been cultured from UK tortoises. Diagnosis is based on culture from oral cavity swabs (submitted in specialised transport medium to Mycoplasma Experience Ltd). Therapy is with fluoroquinolones or tetracyclines.|
|Viral ||Chelonid Herpesviruses (ChHV) have been described in tortoise URTD. From the author’s experiences with URTD it is likely that there are several viral strains associated with different tortoise species as mixing of species is frequently associated with development of URTD. Also, different viral strains may be associated with varying degrees of disease severity. Diagnosis of ChHV is by suggestive clinical signs (stomatitis with hyperaemic mucous membranes, especially ventro-lateral to the tongue; diphtheritic membranes may also form in the mouth and pharynx), identification of intra-nuclear inclusion bodies in cells obtained from the affected areas, or by electron microscopy/virus isolation/PCR from purulent material. Biopsies of mucous membranes may also be taken for histopathology to identify inclusion bodies. Therapy is unlikely to clear infection but regression of symptoms may be achieved using acyclovir. Mild infections appear to clear well by improving husbandry and application of F10 (Health and Hygiene Pty, SA) by nasal flush. However, all infected animals should be considered lifetime carriers and never mixed with naïve groups.|
To date, all the organisms described above may be found in both clinically healthy and diseased tortoises. This therefore represents a carrier status and not only explains the frequent recrudescence in affected tortoises, but also suggests lack of causality between organism and disease. Although there are cases where infectious organisms appear to be primary causes (especially ChHV and Mycoplasma spp, and especially when there has been entry of organism into naïve colonies, or mixing of species), in most cases husbandry problems are the primary factors. In general this syndrome is seen in the traditional garden-kept tortoise where the British climate is simply not suitable for much of the year. Given the complexity of this syndrome a full investigation of clinical cases is vital.
Initial therapy should include the following:
|Table 6. Initial therapy of URTD|
|Biological support ||The tortoise should be warmed to the species-specific preferred optimum temperature zone, and rehydrated (oral in mild cases; systemic in severe cases). Oral nutrition may also be used. It is important to note that when stomach tubing tortoises with stomatitis the mouth should be cleaned and the tube coated with iodine prior to passing through the mouth.|
|Antibiosis ||In unwell tortoises antibiotics may be used as ‘cover’ and to treat any secondary bacterial or mycoplasmal disease. Therefore fluoroquinolones or tetracyclines are the initial drugs of choice. These may be given systemically or orally (where there is often the advantage of getting some local effects). Anti-fungals may be used where large numbers of yeast are found on cytology along with a cellular inflammatory response.|
|'Topical' antimicrobials ||F10 (Health and Hygiene Pty, SA) is a broad-spectrum disinfectant and has shown a lot of promise in URTD when used as a nasal flush. 0.1ml of a 1:250 dilution is given into each nostril once daily.|
|Antivirals ||Where herpesvirus is suspected and the tortoise is unwell, acyclovir may be used.|
|Immunostimulants ||Both Propolis and Echinacea drops have been used in tortoises at the rate of one drop a day by mouth. In the author’s experience there have been some apparent benefits.|
As ever, it is vital to attempt to prevent disease occurring, especially when there is such a complex range of underlying causes:
- Do not mix different species of tortoise.
- Quarantine new individuals before entering a new colony. This should be for at least six months and preferably for twelve.
- Screening tests for Mycoplasma and ChHV may also be used. However, as false negatives are certainly positive they should not be used to replace quarantine.
- Regard all recovered tortoises as being persistently infected and needing to be permanently isolated from non-affected tortoises.
- Good husbandry. Ideally hibernation should be carried out in controlled units and all tortoises should have access to a heat source throughout the summer
Lower Respiratory Tract Disease (LRTD)
There can be a variety of underlying causes:
|Table 7. Causes of LRTD|
|Trauma ||Damage to the carapace may involve penetration of the pleural membranes and lungs. Chelonia can often maintain respiratory function in spite of extensive damage.|
|Shell deformity ||Deformed shells may compress the lung space.|
|Water inhalation ||It is not uncommon to see tortoises after they have fallen into garden ponds or swimming pools. In spite of being submerged for long periods of time it is rare for one to drown. However a secondary bacterial pneumonia is not uncommon. Presented cases should therefore receive supportive care (fluids, warmth, etc.) and antibiotics (e.g. ceftazidime).|
|Neoplasia ||Lung tumours have been reported in Testudo horsfieldi and a European pond turtle (Emys orbicularis) but are not a common finding. Multicentric fibropapillomas have been reported in marine turtles, believed to be caused by a herpesvirus.|
|Pneumonia ||This is common in chelonia and there are many aetiologies. In wild freshwater and marine turtles intra-cardiac/intra-arterial Spirorchid trematodes produce eggs that may induce a severe inflammatory response in the lungs if they become lodged there. In the UK this is likely to be very rare but may be seen in wild-caught specimens. Metazoan parasites and intra-nuclear coccidia have also been described as causes of pneumonia. Fungal pneumonias are seen occasionally. Aetiologies are likely to be the same as for bacterial pneumonia and these will be discussed below. Many species have been isolated including Aspergillus spp and Candida spp. Viral pneumonia is common especially in association with chelonid herpesviruses (ChHV). Also, iridovirus-associated pneumonia has been associated with fatalities in gopher tortoises (Gopherus polyphemus) and Hermann’s tortoises (Testudo hermanni).|
Bacterial pneumonia is common. Like fungal pneumonia it is often a secondary disease (involving opportunistic infection by commensal species), however mycobacteria and Chlamydophila spp have been associated with primary disease. Primary causes are similar to those described for URTD though water inhalation and septicaemic spread of bacteria can also be causes.
Initial therapy should include the following:
|Table 8. Initial therapy of LRTD|
|Biological support ||See above. NB. Aquatic chelonia should be kept out of water other than for a brief daily bath in shallow warm water.|
|Treatment of underlying disease|
|Antimicrobials ||Given the increased likelihood of fungal disease in chelonia compared with other reptiles it is vital that an attempt is made to confirm whether the disease is caused by fungi or bacteria before starting therapy as wrong therapy may worsen the situation. This is where cytology comes into its own.|
|Topical therapy ||Where transcarapacial endoscopy has been used the resultant hole can be utilised to apply therapy to any focal lesions. Similarly where endoscopy is not available the site of a focal lesion can be determined radiographically and a hole drilled over this site under sedation/anaesthesia. A catheter may be inserted as described earlier or the hole left intact but covered by moist chlorhexidine-soaked swabs. Therapy can then be applied daily to the affected lung. When recovered the stoma may be sealed using epoxy resin or fibre glass.|
|Nebulisation ||This may be used to provide ‘topical’ antimicrobials, as an expectorant, and to hydrate mucous membranes.|
Respiratory disease is common and complex in chelonia. Failure to investigate cases fully or to restrict investigation solely to the respiratory system will reduce chances of success. Most cases are secondary to poor husbandry resulting in overgrowth of commensal or ‘carried’ organisms. Therefore, maintaining good husbandry is the single most important factor in the prevention of these diseases.
Chitty, J.R. (2004). Respiratory System. In: BSAVA Manual of Reptiles, 2nd Edition. Eds: Girling & Raiti, pp 230–242. BSAVA, Gloucester, UK.
Mader, D.R. (2006). Reptile Medicine and Surgery, 2nd edition. Saunders, St Louis, Missouri.
McArthur, S.D.J., Wilkinson, R. & Meyer, J. (2004). Medicine and Surgery of Tortoises and Turtles. Blackwell publishing, Oxford, UK.
Wyneken, J. (2001). Respiratory Anatomy – Form and Function in Reptiles. Exotic DVM 3(2): 17–22.
Testudo Volume Six Number Five 2008