The source of vomiting in the emerald tree boa (corallus caninus)

(c) Graham P. Oxtoby 2007/2008 Journal of the British Herpetological Society 2008

THE OCCURRENCE OF PSITTACOSIS IN THE
EMERALD TREE BOA (CORALLUS CANINUS) OF
SOUTH AMERICA

GRAHAM P. OXTOBY
[Abstract]
Corallus caninus – the emerald tree boa of South America – is renowned for the many difficulties it may
present whilst kept in captivity. The problems which may occur vary from stress-related symptoms and the
refusal to feed and endoparasitic diseases (worm infestations and infections caused by flagellate colonies in
the intestines), to the vomiting of prey, also known as ‘regurgitation’.
Corallus caninus – the emerald tree boad of S. America (Photo by author).
Swan & Weidner [2002] describe this chronic condition as the Emerald Vomiting Syndrome or EVS. This
vomiting or regurgitation of prey has often been attributed to stress-related factors or imbalances between
humidity and temperatures in the captive environment. As rightly pointed out in a publication by Swan &
Weidner [2002], the term 'regurgitation' is perhaps not an appropriate way to describe these symptoms since
regurgitation is usually referred to as a condition in which animals store food in a crop or in their esophagus
for later retrieval in order to feed their offspring. This is seen, for example, in numerous species of bird.
Vomiting, on the other hand, is a term generally used to describe the abrupt involuntary evacuation of the
contents of the stomache after the break-down process of food mass in the stomache has begun, as is
typically the case in specimens of Corallus caninus exhibiting symptoms the Emerald Vomiting Syndrome
[EVS].

(c) Graham P. Oxtoby 2007/2008 Journal of the British Herpetological Society 2008
Further studies under clinically defined laboratory Many claim that this syndrome – EVS - is generally conditions with the use of sampled specimens will be caused by stress or in part by the imbalance of required in order to assert these assumptions; these humidity and temperature in the captive environment were conditions which could not be provided by Swan of Corallus caninus. However, recent studies, amongst & Weidner [2002] at the time their own studies were others by Swan & Weidner [2002], suggest that the undertaken. Even so, their claims may have great symptoms are only manifest in captive specimens of significance and therefore warrant further scientific the emerald tree boa that orginate from exporting investigation by specialists in this field. locations where birds (in particular parrots) are kept for later exportation and introduction into the international pet trade. Swan & Weidner mention this Psittacosis is a common and potentially serious disease in their paper [2002] in which they also describe occurring in avians, mammals and humans. The disease is not fully understood and there is still a lot to be learned about the condition. The causal organism, After conducting studies in captive caught specimens Chlamydia psittaci, has recently been renamed of Corallus caninus, Swan and Weidner [2002] suspect Chlamydophia psittaci and is found in a wide variety of that the organism known as Chlamydophia psittaci is (tropical) birds, but may also occur in mammals, the cause of this condition. The authors also state that including humans causing serious illness. their findings are by no means based on true ‘scientific’ This species of organism is now sub-divided into many subspecies, each affecting a different animal. For example, the type which will affect cats produces an The same applies to this current paper. It is merely a eye-infection called conjunctivitis or blepharitis collection and summary of data and information (inflammation/infection of the eyelids). In sheep, the widely available in literature on this subject, but, at the disease is said to result in premature abortion and in same time, poses the important question regarding humans, it has been established that this disease will whether EVS is, in fact, a manifest form of Psittacosis most probbaly cause atypical pneumonia. The organism producing a genital/venereal disease in humans has now been classified as a separate genus: in Corallus caninus, the emerald tree boa of S. America, or that regurgitation (EVS) can be attributed to a much wider spectrum of disorders (both phyisical The generic term for the disease produced by and environmental) in Corallus caninus. Chlamydophia psittaci affecting all species – both avian and mammalian - is chlamydiosis. When this disease is The studies conducted by Swan & Weidner revealed exhibited in avians, it is called ornithosis. When that, whilst a certain percentage of specimens collected exhibited specifically in psittacine birds, it is for the pet trade exhibited symptoms of Psittacosis designated as psittacosis, a designation also used to (also known as the Parrot Disease), others did not. describe the disease occurring in mammals, including They attribute this to the fact that some wild-caught specimens of Corallus caninsus are housed in close proximity to numerous species of tropical bird, for example parrots, before being exported and introduced into the international pet trade. In their article, reference is made to a trapper who kept specimens of Corallus caninus segregated from avians whilst awaiting exportation and that it was found that the disease did not occur in those specimens. Specimens of Corallus caninus which were not housed in close proximity to birds whilst awaiting exportation, were not affected by this disease and did not exhibit Fluorescent antibodies associated with infection by
the characteristic symptoms of Psittacosis or EVS. Chlamydia psittaci, 40X. Courtesy of Dr. Jean
The disease was observed only in specimens that had Sander & Merck Veterinary Manual
been kept in close proximity to avians after capture. Other species susceptible to this disease include red- The organism itself is unusual in that it possesses tailed boa constrictors and anacondas collected for the certain characteristics of both bacteria and viruses. It is relatively large and also highly sensitive to antibiotics. It resembles viruses in that it can only develop and (c) Graham P. Oxtoby 2007/2008 Journal of the British Herpetological Society 2008
multiply within the cells of its host. The damage is compounds. The conventional fumigation of caused by the rupture and further destruction of these quarantine confinements with the use of formaldehyde cells and the release of toxins into the host’s biologic gas (formalin and potassium permanganate) has system. Chlamydia appear to infect and multiply in proven to be highly effective against this organism, most cell-types, thus resulting in a widely variable provided that surfaces have first been adequately The natural occurrence of this infection is world-wide and it has been estimated that 1% of all wild birds are infected and therefore also act as carriers. Many avians can retain the organism in their bodies in a latent state without immediately showing signs of the disease - these birds are carriers and are a persistent risk to other birds and other animals susceptible to the disease. It appears that the infection or disease is most predominant when external stress-related factors occur, i.e. capture, loss of food sources, change of Elementary bodies associated with infection of
habitat, transportation, quarantine and relocation. The Chlamydia psittaci, 100X. Courtesy of Dr. Jean
disease is therefore most commonly observed after Sander & Merck Veterinary Manual
recent capture, relocation and importation into the pet trade, particularly in avians. This is also the time when In Corallus caninus, it is said to cause the destruction most wild caught animals are stressed, thus resulting in of HCl-producing cells needed for the break-down of the weakening of their natural biologic resistance. This brings the current discussion to the points made The organism is also able to survive outside the host by Swan & Weidner [2002], where the authors explain for approximately one month if protected by cell the dangers which may exist when other species are debris and protein material (i.e. droppings, nasal held in confinements in close proximity to infected discharge etc.). An important aspect of control of the avians in their countries of origin or during and after disease is therefore cleanliness and disinfection to transit, such as is the case in wild-caught Corallus remove such debris from confinements in which the caninus (the emerald tree boa) collected in particular in Guyana, Surinam and other regions of S. America. These are regions where avians are also collected for Members of the Chlamydiaceae are so-called nomotile, exportation and introduction into the international pet gram-negative, obligate intracellular organisms that possess a unique developmental cycle consisting of metabolically inactive infectious elementary bodies When kept in confinements awaiting further (EBs) and metabolically active, but non-infectious transportation, carriers of Chlamydophila produce reticulate bodies (RBs). Chlamydiae, on the other droppings containing the organisms. Avians and other hand, replicate in the cytoplasm of host cells within an animals are often kept in close proximity with each endosomalvacuole which appears under light other in these conditions and due to the extremely microscopy as an intercellular inclusion (see image contagious nature of the disease are therefore highly susceptible to the organism and resulting infection. The disease may therefore spread very rapidly. Chlamydophia psittaci is considered a dangerous Contracting is generally by airborne contact with organism to handle under laboratory conditions. For inhaled fecal dust from dried feces or droppings. The many years it was a major cause of laboratory- incubation period (the time between the moment of contracted infections. It generally resulted from contracting the organism to the manifestation of clear exposure to and the use of aerosols. The stability of the clinical signs) however, is extremely variable and can organism in a laboratory environment is also be confusing when attempts are made to determine the considered to be a potential danger, also to humans. exact source and cause of the infection. Disinfectants found to be highly effective against this The organism may also reside in the host in a latent state, only to be triggered at a later stage under stress- benzalkonium chloride and formaline-based (c) Graham P. Oxtoby 2007/2008 Journal of the British Herpetological Society 2008
related conditions (e.g. relocation, transport, new weight and appetite, diarrhoea, vomiting and confinement) to produce clinical signs. In the latter sometimes respiratory symptoms. These are only the case, the onset triggered by these stress factors and may therefore also occur long after the animals have been exported and been placed in their new homes The symptoms observed in EVD in Corallus caninus (e.g. at the location of the new owner). are very similar, but in EVS vomiting predominates (24-72 hours after ingestion of prey), together with the The minimum incubation period documented to date refusal to eat and gradual dehydration. There is also a is 10 days, although ongoing studies suggest that this marked weight loss due to continued or prolonged period may vary from between 10-45 days. The inappetance and vomiting after feeding and the well- maximum period may be from between 9-18 months being of the specimen affected rapidly diminishes. when in its latent state, i.e. long after exportation of the Proper clinical diagnosis of the disease is difficult since animals to other countries and into the pet trade, or at may of these same symptoms may also arise in reptilians as a result of stress and infections by other endoparasitic infections (including Cryptosporidiosis) This means that regulated quarantine periods have and not all of these signs may be present at any one little or no bearing on the recognition of the infection time. Systemic infections which may also produce or the time of onset of the infection. Animals may be many of the same symptoms include e.g. infections infected by the organism, but show no clinical signs cause by flagellates and worms, the common cold in throughout prolonged periods of quarantine exceeding reptilians and the initial stages of secondary pneumonia 3-6 months. This also makes it very difficult to resulting from loss of biologic resistance etc. which, in determine the actual source or time of the infection. many cases, may be purely stress-related. Outbreaks of the disease may therefore occur in populations of apparently healthy animals that have As pointed out by Kolins & White: ‘The classic previously shown no clinical signs of the disease for presentation of Cryptosporidium serpentis infection in months or even years. From this, it follows that, the snake is an animal which regurgitates its meal contrary to popular belief, avians brought into a within four days or less of ingestion. This regurgitation country and subjected to relatively long periods of occurs because of decreased gastric lumen size and quarantine (3-6 months) cannot be guaranteed to be mucosal irritation. Since the diameter of the stomach free from psittacosis. In the UK, for example, the has often increased, a noticeable swelling can be quarantine period for imported birds is 35 days, i.e. it visualized and palpated in the mid-body region. The ends 6-10 days before the probable maximum period snake may or may not be anorexic, depending on how of incubation of the organism is reached, not including far the disease has progressed. Often, a mucoid those specimens in which the organism may reside in a latent state. In many countries therefore, regulated minimum periods of quarantine are most probably It is important to differentiate Cryptosporidiosis from ineffective for the purpose of recognising the other causes of regurgitation and gastritis. Suboptimal temperatures, inappropriate prey size, stress, and foreign body obstructions are other potential causes of In an attempt to control psittacosis, in the US many regurgitation. Hibernation associated necrotizing quarantine stations administer the board-spectrum gastroenteritis, parasitism from other protozoa and anitibiotic Tetracycline to avians during their stay. This nematodes, viruses, Salmonella and other bacteria can is regulated by US law, but is not the case in many all cause similar signs, but the gastric swelling is other countries such as the UK and other EU member pathognomonic for Cryptosporidiosis.’ states. Although some importers in the UK will administer Tetracycline as a preventive measure, they are not obliged to do so. In addition, the use of From this, it follows that not all symptoms seen in Tetracycline does not reliably eliminate the disease or psittacosis can be attributed to the presence of Chlamydophia psittaci, which makes any positive diagnosis based upon symptoms alone far from conclusive. Any accurate diagnosis must therefore be supported by further clinical laboratory tests, Clinical signs are many and variable. They depend otherwise the assumption that these symptoms are largely on the species involved. Some animals, like cats, caused by Chlamydophia psittaci may only be are reported to develop serious eye infections like considered as speculative. In many cases, blood conjunctivitis or blepharitis (inflammation of the samples will only demonstrate antibodies, which only conjunctiva and swollen eye-lids). In avians and means that the reptile has been exposed to reptilians the symptoms most predominant are: loss of chlamydophila at some time. That in itself would (c) Graham P. Oxtoby 2007/2008 Journal of the British Herpetological Society 2008
support the theory by Swan & Weidner [2002] that the
too late or mistaken for other conditions which exhibit organism must have been contracted during its stay in similar symptoms, or if the infection has been present confinements in close proximity to avians before, Erythromycin is a macrolide antibiotic that has an In order to be of any relevance, blood tests would need antimicrobial spectrum similar to or slightly wider to be repeated 10-14 days later for the results to be than that of penicillin and has proven to be highly suggestive of recent infection. The organism can be effective in the treatment of acute outbreaks of identified in blood samples only during the multiplication stage of the organism and because this period is only limited, negative results would not According to Swan & Weidner [2002] 'The apparent always implicate that the specimen does not have the successful dose used for gastric Chlamydophilal disease. The most effective means of diagnosing the infection in emerald tree boas is 25mg/kg orally, daily infection in Corallus caninus would be a post-mortem (autopsy) examination of the carcas or immediate examination and laboratory analysis based upon Treatment for shorter periods of 5-10 days will often cultures of the organism collected from fresh feces or produce a rapid clinical improvement, but the reptile will not be cured and relapses may occur. The antibiotic only acts on organisms when they are Typical signs would be similar to those found in other growing and multiplying, and since the Chlamydophia septic infections: inflammation of the stomache and can exist dormant (i.e. in a latent state) in cells for destruction of the stomache lining cell structures, some time, the drug will be useless during these enlargement of the spleen and liver and inflammation of the membranes of the air sacs, heart and peritoneum, i.e. the transparent membrane that lines Additionally, the prolonged use of antibiotic can itself pose problems of imbalance of the normal intestinal flora, producing diarrhoea and malabsorption There are other tests available for detecting conditions, or secondary infection by opportunist Chlamydophila antigen in feces, e.g. ELISA (Enzyme fungi or yeasts. There may also be some immuno- Linked Immunosorbent Assay), which provides suppressive effects to the drug and it can be difficult to quicker results on samples that contain the organism. maintain therapeutically effective levels of the Other tests developed for testing for the presence of tetracycline within the cells. Tetracycline also reacts this organism include Latex Agglutination (L.A. ) and with calcium in the diet to limit its absorption, so diets Direct Flourescent Antibody (F.A. ). However, PCR with high calcium levels in animals undergoing technology using Chlamydophia psittaci- specific DNA treatment with the drug should be avoided. probes has proven to be the most effective method of Doxycycline is available as 'Vibramycin syrup' and is administered orally. This is probably preferable for single, handleable specimens of Corallus caninus. It The treatment of psittacosis may not be as simple as it may be administered by means of a catheter inserted may seem. The drug of choice in avians and reptilians into the esophagus. Since this technique involves is one of the Tetracycline group, to which the handling and therefore stressing the reptile at regular Chlamydial organism is sensitive. Doxycycline is a intervals, this may sometimes be impractical since it semi-synthetic tetracycline clinically developed in the may also contribute to additional stress. Injectable early 1960s by Pfizer Inc. and also marketed under the forms of the drug are also available but may cause brand name Vibramycin. Vibramycin received FDA irreparable muscle damage when administered over a approval in 1967, becoming Pfizer's first once-a-day longer period. Injectable forms are therefore not broad-spectrum antibiotic. Other brand names include: Monodox, Periostat, Vibra-Tabs, Doryx, Currently, there has been success in the treatment of psittacosis using the newer quinolone antibiotics, such The drug needs to be administered according to a as enrofloxacin, also marketed under the name Baytril. regime which will produce an effective dose for a This drug is more palatable and stable in the drinking sufficient period of time. Provided that a precise water, and in its injectable form it is less likely to diagnosis is made quickly enough, treatment with Tetracycline or Erythromycin will usually produce a tetracyclines. It appears also that cure rates may be rapid response, but not if the condition is diagnosed obtained in 14-21 days. Baytril is widely available as an effective antibiotic for use in reptiles. (c) Graham P. Oxtoby 2007/2008 Journal of the British Herpetological Society 2008
The present author’s own findings seem to suggest that However, there is evidence to suggest that apparent the breakdown of prey in the stomache of Corallus 'cures' using any of these drugs described above are in caninus takes longer than is generally assumed. In a fact only clinical improvements and do not produce a collection of recently imported wild-caught Guyana long-term sustainable cure of the infection and full specimens, only one of the 10 specimens exhibited elimination of the organism. Additionally, execessive symptoms similar to those seen in psittacosis by or prolonged doses of these drugs in Corallus caninus vomiting prey 48-72 hours after being fed. The prey may, in many cases, prove to be fatal and should vomited was found to be more or less fully intact and therefore be administered with great caution and care - had not, after 72 hours, been substantially reduced by It was recorded that this vomiting occurred only after If EVS is in fact attributed to the presence of excessive spraying and misting in the confinement had psittacosis, other complications may occur in Corallus occurred. It did not affect other specimens kept and caninus, as explained by Swan & Weidner [2002]. cared for under exactly the same conditions and Since the infection, if left untreated for a longer period obtained from the same source in Guyana. On other of time, has a highly destructive effect on the cells walls occasions, this same individual would readily accept prey and produce healthy looking feces days after, of the stomache in Corallus caninus, this may result, without bone remnants present in the feces. over time, in the permanent loss of HCl producing stomache cells. These HCl-producing cells are needed Perhaps in this case, the vomiting may be attributed to during the first stages of food processing in the stress-related factors or increased sensitivity of the stomache of the snake, i.e. for the conversion of prey individual to the abrupt and relatively high degree of into a ‘slush’-like mass which is normally processed humidity caused by spraying. The specimen was not further along the alimentary tract (small intestines) before feces are produced. clinically diagnosed as having psittacosis and no treatment with antibiotics had yet been initiated after This would account for the bone remnants found in the symptoms were observed. Analysis of the feces proved negative for worm and flagellate infections [the excretions of feces by Corallus caninus as reported by specimen had recently been treated preventively for Swan & Weidner [2002], where food masses have not been full processed during this initial ‘slushing stage’ in the stomache. The ‘slushed food mass’ is the result of the effects of the break-down effect of HCl- producing cells in the stomache during the first few Whether we are dealing here with EVS or psittacosis, days following acceptance and presence of prey in the or even Cryptosporidiosis, it is most probably stomache. The destructive effect of psittacosis causes recommendable to carry out the following preventive permanent, irreparable damage to these HCl- treatment of specimens of wild-caught specimens of producing cells which are essential for the initial Corallus caninus when signs similar to those presented in psittacosis are observed. This preventive treatment would merely have the purpose of alleviating If this breakdown is not possible or substantially symptoms in an attempt to combat any possible impaired, prey accepted and taken by Corallus caninus infection by Chlamydophia psittaci. Whether it is cannot physically continue down the alimentary tract effective or not depends on the underlying cause. and is therefore vomited up as a result. Therefore, until Obviously, if symptoms diminish considerably or a positive diagnosis is obtained, specimens of Corallus disappear after treatment with an antibiotic like caninus should preferably be fed smaller meals in Baytril, there would be reason to suggest that an order to allow for the possible destruction of cell tissue infection was the probable cause, but not necessarily and loss of HCl-prducing cells in the lining of the caused by psittacosis. If symptoms persist after stomache. If the destruction of cell tissue is severe, treatment with an antibiotic, this would then suggest over time this will inevitabaly lead to the death of the that other causes for the symptoms are present and snake (in which case euthanasia may be considered). should therefore be investigated (e.g. flagellate However, if the destruction of HCl-producing cells is infections, worms, stress-related causes). In order to halted at a relatively early stage of the infection (by rule out infections by worms and/or flagellates, the effective therapy), the remaining HCl-producing cells recommended treatment would be as follows: would enable the snake to survive the infection, A - treatment (following analysis of feces or preventively) of worm infestations by administering (c) Graham P. Oxtoby 2007/2008 Journal of the British Herpetological Society 2008
Panacur (or similarly effective drug) to eliminate the storage and transport, whilst these animals await possiblity of worm infections as the underlying cause; exportation and introduction into the collections of private breeders, herpetologists and zoos. B – treatment of flagellate infections (either preventively or following positive results of feces analyses) by administering Flagyl (or similar drug) to eliminate a flagellate infection as the underlying cause. (This treatment should only be performed on the basis C – the oral administration of Baytril as a preventive measure, following the above regime in order to assist in elimination or alleviation of EVS in Corallus CONCLUSION
In summary, therefore, it may be concluded that psittacosis is a disease that has long been recognised, but is yet still not fully understood. Many symptoms observed in EVS show great similarity with the signs Literature
most predominant in psittacosis for which there is, to date, no known long-term cure. Preventive treatment Jacobson, Elliott R., DVM, PhD Jorge Orós, DVM Sylvia J.
with an effective antibiotic from the tetracycline group Tucker, BS David P. Pollock, BS Karen L. Kelley Robert J. of drugs seems to be the only remaining option in such Munn, MS Brad A. Lock , DVM Ayalew Mergia, PhD Janet K. cases, unless a positive diagnosis for psittacosis is Yamamoto , PhD , Partial characterization of retroviruses made. Even then, the prognosis for specimens of from boid snakes with inclusion body disease, American Corallus caninus exhibiting these symptoms fro Journal of Veterinary Research, February 2001, Vol. 62, No. 2, Pages 217-224
Jackson, Kate., Nathan J. Kley, Nathan J., & Brainerd,
Elizabeth L., How snakes eat snakes: the biomechanical Until further scientific studies are conducted under challenges of ophiophagy for the California kingsnake, controlled laboratory conditions, any assumptions that Lampropeltis getula californiae, Department of Zoology, EVS in Corallus caninus should be attributed to psittacosis may therefore only be considered as Jones, Alan K., Understanding Psittacosis (Parrot Fever)
speculative. Cryptosporidiosis caused by Kolins, D., & White, M. Randy, 1996, Cryptosporidiosis in
Cryptosporidium serpentis must also be ruled out. Oxtoby, G. P., Observations on Anorexia in African pythons,
Journal of the British Herpetological Society [June, 1986]
However, due to the severity of the condition and the Satie, Andréa & Karasaw, M., (incl. Reinaldo José da Silva,
high mortality rate observed in indivdual specimens of Luciene Maura Mascarini, Thoma Henrque Barrella*, Carlos Corallus caninus (and to some extent in e.g. Boa. c. Albertode Magalhães Lopes*, Occurrence of Cryptosporidium constrictor and Eunectes notaeus) captured for the pet trade, further comprehensive scientific investigation is in Crotalus durissus terrificus (Serpentes,Viperidae) in Brazil Swan & Weidner, 2002, The Source of Vomiting in the
Emerald Tree Boa (Corallus caninus) It is important to differentiate psittacosis and The Merck Veterinary Manual
Cryptosporidiosis from other causes of regurgitation and gastritis. Suboptimal temperatures, inappropriate prey size, stress, endoparasitic infections (caused by flagellates and worms) as well as foreign body obstructions in the alimentary tract are other potential causes of regurgitation. Additionally, strict hygiene, disinfection, longer periods of quarantine and isolation of all newly captured specimens of Corallus caninus are of paramount importance in controlling the disease, as is the segregation of avians from other wild-caught species in their countries of origin during and after

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