Reptilian cardiovascular anatomy and physiology: evaluation and monitoring (Proceedings)

Reptilian hearts differ significantly from those of mammals. Most reptiles possess three chambered hearts, with the exception of crocodilians. The anatomy of the great vessels is quite different from that of mammals and can be confusing to uninitiated. Adequate knowledge of normal anatomy and function is paramount in assessing health and performing certain clinical procedures. Reptile cardiovascular physiology is also significantly different from that of mammals. Reptiles are much less susceptible to the adverse effects of hypoxia and changes in blood pH, and therefore capable of enduring much wider fluctuations in heart rate, blood pressure, and oxygenation.

Anatomy and function

The location of the heart within the body cavity varies according to species. In most chelonians the heart lies on midline just caudal to the thoracic girdle, ventral to the lungs. The heart of some chelonians such as soft-shelled turtles is pushed to the side of the body cavity in order to accommodate the retracted neck. The heart of most lizards lies within the thoracic girdle, with the exception of some species such as monitors and tegus (as well as crocodilians) in which the heart lies farther back in the coelomic cavity. Cardiac location varies in snakes according to species, but usually is found at the junction of the first and second quarter of the animal's body length. Typically arboreal snakes' hearts are found more cranially in the body than in terrestrial animals. Snake's hearts are fairly mobile within the coelomic cavity helping to facilitate the ingestion of large prey items.

The cardiac structure of reptiles is significantly different from that of mammals. Please note that the following descriptions are very general, and that significant variation exists between species. Most reptiles have three chambered hearts with two atria and one common ventricle. The right atrium receives blood returning from the systemic circulation via the sinus venosus, which is formed by the confluence of the right and left precaval veins and the single postcaval vein. The walls of the sinus venosus contain cardiac muscle and the pacemaker of the heart. The left atrium receives oxygenated blood from the lungs via the pulmonary vein(s). The atrioventricular valves are bicuspid, membranous structures. Under normal conditions the three chambered heart functions much like a four chambered structure, therefore relatively little mixing of oxygenated and de-oxygenated blood occurs. Three cavities exist within the ventricle and can be functionally separate; the cavum venosum, cavum arteriosum and the cavum pulmonale. These cavities are partially separated by two muscular ridges found within the ventricle. These ridges vary in prominence in different species, but are generally well-developed in chelonians. The muscular ridge divides the cavum pulmonale and the cavum venosum. The vertical ridge divides the cavum venosum and cavum arteriosum. The cavum pulmonale receives blood from the right atrium through the cavum venosum and directs flow into the pulmonary circulation. The cavum arteriosum receives blood from the pulmonary veins and then directs oxygenated blood to the cavum venosum. The paired aortic arches arise from the cavum venosum and lead to the systemic circulation. The right and left aortic arches come together to form a single aorta at variable distances caudal to the heart. Differential blood flow and separation of oxygenated and de-oxygenated blood is maintained by pressure differences of the outflow tracts and the muscular ridges that partially divide the ventricle. In most non-crocodilian reptiles the ventricle function as a single pump, meaning that the same pressures are generated by both the cavum pulmonale and cavum venosum. This is not the case in monitor lizards and at least one species of python in which significantly higher pressures are generated in the cavum venosum and thus the systemic arches.

Due the unique anatomy, both right to left and left to right shunts are possible in the reptilian heart. Shunting does occur during apnea, though all the details regarding the exact purpose of shunts are unclear. Multiple theories exist regarding the purpose of right to left cardiac shunting in reptiles including the conservation of cardiac energy, facilitation of warming, reduction of plasma filtration into the lungs, reduction of carbon dioxide flux into the lungs and the metering of oxygen stores from the lung(s) during apnea. Theories to explain the purpose of left to right shunting include facilitation of carbon dioxide elimination from the lung(s), minimization of ventilation/perfusion mismatches and improvement of systemic oxygen transport. In times of oxygen deprivation (diving in some reptiles, consumption of large prey in snakes), reptiles can shunt blood away from the lungs. Right to left cardiac shunting in the non-crocodilian heart can be facilitated by an increase in pulmonary vascular resistance and action of the muscular and vertical ridge. Resumption of breathing results in a decrease in pressures within the pulmonary vasculature and restoration of pulmonary blood flow.

Crocodilians are the only reptiles which possess four chambered hearts comparable to mammals. Even so, crocodilian cardiac anatomy is quite different from what is seen in birds and mammals. Crocodilians possess two aortas; the right arising from the left ventricle and the left from the right ventricle. Both aortas route blood to the systemic circulation. The right and left aortas are connected near the base of the heart by the foramen of Panizza. The foramen allows blood from the right ventricle to bypass the pulmonary circulation when necessary. A valve exists at the opening of the pulmonary artery which has interdigitating muscular projections, hence the commonly used name "cog-wheel valve". When the animal holds its breath, the cog-wheel valve closes and blood that would have normally entered the pulmonary circulation is diverted into the left aorta. It should be noted that most veterinary texts incorrectly report that the location of the foramen of Panizza is in the ventricular septum or atrial septum.

Heart rate of reptiles depends on species, size, temperature and activity/level of metabolic function. An equation employing metabolic scaling for determination of the "appropriate" heart rate in reptiles has been proposed: Heart rate = 33.4(Weight in kilograms-0.25 ). This equation assumes that the reptile is within its preferred optimal temperature zone.

Evaluation and Monitoring

The same principles that are used to evaluate and monitor the cardiovascular system in mammals can be used in reptiles. The difficulty lies in interpreting results of the physical examination and diagnostic tests when one is not familiar with the normal anatomy and physiology of the species in question. Occasionally, important studies describing normal cardiac parameters are published that can provide guidance to the clinician. However, always use caution when applying "normals" determined for a particular species across taxa.

Auscultation

The author does not find this to be a useful tool for evaluating and monitoring cardiac function in reptiles. I have never been able to effectively auscult heart sounds in any species of reptile (though some claim they can). Despite this fact, one should always take the time to at least attempt cardiac auscultation in case it does yield useful information.

Doppler Probes

Doppler probes are extremely useful for evaluating and monitoring cardiac function in reptiles. Doppler probes can be used to evaluate the flow of blood in various parts of the animal's body, aid in location of vessels for venipuncture, monitor heart rate and give subjective information about cardiac function. The sound created by the Doppler can vary according to its exact position over the heart, but typically there are three heart sounds heard during contraction of a reptilian heart. Doppler probe placement for cardiac sounds varies according to species. In chelonians, the probe can be placed between one of the forelimbs and the neck. With most lizards the probe functions best when placed in the lateral axillary region or even the caudal gular region. Monitor lizards' and crocodilians' hearts lie further back in the coelomic cavity and cardiac movement can usually be seen unless the animal is very large or obese. Cardiac movement can usually be seen or palpated in snakes.

Electrocardiography

The use of electrocardiography (ECG) in reptiles is hampered by lack of normal values for the variety of species encountered. Also, the small size (and resultant low amplitude of cardiac electrical impulses) and anatomy of many reptiles makes the use of ECG difficult. Despite these facts, ECG has occasionally proven useful in diagnosis of cardiac disease in reptiles and has applications in monitoring of anesthesia.

When using ECG for diagnostic purposes it is best to use a tracing from a healthy conspecific as a normal. It is paramount that the normal animal's recording be taken under the same conditions as the patient's since temperature and metabolic state can affect the results. When compared to a normal animal's ECG, those of reptiles with specific cardiac maladies often show the same changes as would be expected in a mammal. For anesthesia monitoring, trends can be observed that may be of use in directing the procedure. Clinicians should keep in mind that reptiles' hearts often continue to contract for long periods of time following death, so use caution interpreting ECG findings as an indication of life.

In larger chelonians, adhesive ECG leads attached to the carapace seem to work quite well. These adhesive leads can also be used in larger snakes with smooth scales that allow good contact. The author and many others typically place hypodermic needles into the subcutaneous space and attach alligator clip leads to them. Exact placement of the leads depends on size, shape and cardiac location. It is best to experiment a bit in novel species to find a lead placement scheme that provide a tracing with the greatest amplitudes.

Radiography

Radiography can be quite useful in evaluation of the cardiovascular system in reptiles. Much information can be gained regarding the size, shape and composition of the heart and vasculature. Once again, it is important to have a "normal" radiograph from a matched conspecific to compare to. Note that cardiac size varies considerable between taxa, with more "athletic" species possessing relatively large hearts.

Blood pressure

Measurement of blood pressure in reptiles is rarely performed by most clinicians, but is certainly possible. Two methods of measuring blood pressure are available; direct and indirect.

Direct measurement involves placement of an arterial catheter, which can be a challenge or impossible depending on the species of reptile. Certainly small species are not candidates for arterial catheterization, but larger animals can be catheterized surgically with relative ease. Snakes can be catheterized via the internal carotid arteries or one of the aortas. Lizards, chelonians and crocodilians can be catheterized via their carotid or femoral arteries.

Indirect measurement of blood pressure can be accomplished via use of a blood pressure cuff and oscillometric monitor. Cuffs can be placed on the tail or one of the legs. Though not as accurate as direct measurement, indirect measurement can provide the clinician with some information for ancillary cardiac diagnostics and anesthesia monitoring in some species. Certainly indirect blood pressure monitoring can alert the clinician to trends that may necessitate intervention.

Blood pressure in reptiles does seem to respond much as one would expect to typical clinical procedures. Depth of anesthesia seems to affect blood pressure in reptiles as does positioning while anesthetized. Whereas it is probably safe to assume that reptiles are capable of withstanding much greater variation in blood pressure than mammals, clinicians are advised to pay attention to what is occurring in their reptile patients and not "push their luck".

Ultrasound

Ultrasonographic examination can be a useful tool for diagnosis of cardiac disease in reptilian patients. At least a few studies exist describing normal ultrasonographic appearance of snake hearts and suggest a standardized method for evaluation. For the myriad species that have not been described, examination of a matched conspecific is advisable before making a diagnosis. Whereas it is very difficult to evaluate certain parameters without normal ranges for comparison, at times a diagnosis can be made with some confidence. Insufficient valves, stenotic valves, endocarditis and thrombi should be reasonably apparent to practitioners familiar with reptilian cardiac anatomy. Most squamate reptiles (snakes and lizards) and crocodilians are easily examined as their anatomy creates few challenges. The scale structure of some animals, especially those possessing osteoderms, can make ultrasonographic examination very difficult. Chelonians' hearts can be imaged via the same window that is used for placement of a Doppler probe. Ultrasound coupling gel can be used, but some practitioners prefer to perform reptilian ultrasound exams with the body of the animal submersed in a tub of water. By submerging the animal, artifact caused by air trapped between or under scales can be minimized.

Capnography

The author uses capnography as a part of reptile anesthesia monitoring and usually observes reasonable agreement between ETCO2 and arterial CO2. However the clinician should remember that due to reptiles' ability to shunt blood past the lungs, end tidal CO2 can be quite different from the actual CO2 content of arterial blood.

Pulse oximetry

Pulse oximetry is often difficult to employ in reptiles since few of the commercially available probes are "reptile friendly". Another fact to consider is that reptiles often have relatively high circulating levels of methemoglobin in a normal state. This can potentially affect pulse oximeter readings and give an erroneously low reading. In some species, pulse oximeter readings correlated well with blood gas analysis. Clinicians are encouraged to use pulse oximetry in reptiles as it may alert them to trends in oxygen saturation.

Literature/Suggested Reading

1. Farrell AP, Gamperl AK, Francis ETB. 1998. Comparative aspects of heart morphology. In: Gans C, Gaunt AS. Biology of the reptilia, Visceral organs, Vol. 19, morphology G. SSAR, Ithaca, NY:375-424.

2. Hicks JW. 1998. Cardiac shunting in reptiles: mechanisms, regulation and physiological functions. In: Gans C, Gaunt AS. Biology of the reptilia, Visceral organs, Vol. 19, morphology G. SSAR, Ithaca, NY:425-483.

3. Murray MJ. 2006. Cardiology. In: Mader DR (ed.). Reptile medicine and surgery (2nd edition). WB Saunders, St. Louis, MO:181-195.

4. O'Malley B (ed.). 2005. Clinical anatomy and physiology of exotic species. Elsevier, New York, NY:17-93.

5. Schildger BJ, Caesares M, Kramer M, Sporle H, Gerwing M, Rubel A, Tenhu H, Gobel T. 1994. Technique of ultrasonography in lizards, snakes and chelonians. Seminars in Avian and Exotic Pet Med, 3:147-155.

6. Schillinger L., Tessier D., Pouchelon JL., Chetboul V. 2006. Proposed standardization of the two-dimensional echocardiographic examination in snakes. J Herp Med Surg, 16(3):76-87.

7. Snyder PS, Shaw NG, Heard DJ. 1999. Two-dimensional echocardiographic anatomy of the snake heart (Python molurus bivittatus). Vet Radiol Ultrasound, 40:66-72.

8. Wang T, Altimiras J, Klein W, Axelsson M. 2003. Ventricular haemodynamics in Python molurus: separation of pulmonary and systemic pressures. Journal of Exp Biol. 206:4241-4245.