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IBDReview2010 JexoticPet PDF
IBDReview2010 JexoticPet PDF
Abstract
A disease called inclusion body disease (IBD) is seen worldwide in snakes that are
members of the families Boidae and Pythonidae. Snakes affected by this disease
often have neurological signs. A diagnosis is based on light microscopic examina-
tion of tissues for the presence of intracytoplasmic inclusions that consist of a
unique protein that has been termed inclusion body disease protein (IBDP). In some
cases, inclusions are found exclusively in the central nervous system, whereas in
others they may be diffusely disseminated in multiple tissues. In a few cases, the
IBD inclusions have overlapped in appearance with other types of nonviral intra-
cytoplasmic inclusions. The specific etiologic agent of IBD remains unknown.
Because the underlying cause of IBD is unknown, recent research has focused on
understanding the formation and nature of IBDP. A monoclonal antibody has been
developed against IBDP and is currently being used in immunodiagnostic assays to
develop a reliable diagnostic test for IBD. This monoclonal antibody is going
through rigorous validation testing and will provide more specificity and sensitivity
than currently available routine histological diagnostics. Because large numbers of
boas and pythons are being bred and sold for the pet trade, better diagnostic tests
are needed to help develop IBD-free breeding colonies of these snakes. Further,
because IBD is one of the few worldwide diseases of captive snakes, there is
concern in many countries (e.g., Australia, where it has been identified in captive
pythons) that it will become established in native wild populations. Thus, there is
conservation value in developing better diagnostic tools for screening snakes
intended for release as part of reintroduction programs. Copyright 2010 Elsevier
Inc. All rights reserved.
Key words: Boa; IBD; IBDP; monoclonal antibody; protein sequencing; python
S
nakes make up approximately 19% of all rep-
tiles maintained as pets in the U.S.1 Of these,
various boid snakes (members of the families From the Department of Small Animal Clinical Sciences, College of
Boidae and Pythonidae) are bred in large numbers Veterinary Medicine, University of Florida, Gainesville, FL USA.
for the pet trade. Although accurate numbers are Address correspondence to: Elliott Jacobson, DVM, PhD, Dip.
ACZM, Department of Small Animal Clinical Sciences, Box
not available, it is believed that several million of
100126, College of Veterinary Medicine, University of Florida,
these snakes are classified as pets or maintained in Gainesville, FL 32610. E-mail: jacobsone@vetmed.ufl.edu.
breeding operations within the United States. Of © 2010 Elsevier Inc. All rights reserved.
illnesses affecting boid snakes, inclusion body dis- 1557-5063/10/1903-$30.00
ease (IBD) has surfaced as the most important world- doi:10.1053/j.jepm.2010.07.014
216 Journal of Exotic Pet Medicine, Vol 19, No 3 ( July), 2010: pp 216 –225
Inclusion Body Disease 217
wide disease, a condition characterized by the for- an eastern king snake (Lampropeltis getula) that was
mation of intracytoplasmic inclusions.2 In Australia, housed with boa constrictors,4 and in a zoological
where IBD has been identified in captive pythons,3 collection of palm vipers (Bothriechis marchi).8 How-
and in other countries where boid snakes are being ever, the correlation of the inclusions in the king
bred for release to the wild, there is concern that this snake and viper cases to IBD has not been confirmed
disease will become established in native wild popu- with molecular techniques or immunological re-
lations. Boid snakes with IBD may have a subclinical agents.
infection. It is not known what percentage of in-
fected snakes will develop clinical signs of disease in
relation to those that will appear unaffected. It is
Clinical Signs
possible that latent infections can persist for long
From the late 1970s and extending into the mid-
periods of time. Currently, a presumptive diagnosis
1980s, Burmese pythons were the most common
of IBD is based on the light microscopic identifica-
boid snake seen with IBD. Clinical signs of the dis-
tion of intracytoplasmic inclusions in one or more
ease in Burmese pythons primarily involved CNS
tissues. However, some snakes have very few inclu-
abnormalities (e.g., torticollis, disequilibrium, opis-
sions in tissue sections because they are easy to over-
thotonos, inability to right itself when placed in dor-
look, especially if limited to the central nervous sys-
sal recumbency, flaccid paralysis).2 Beginning in the
tem (CNS). Although several viruses, including ret-
early 1990s, more cases were diagnosed in boa con-
roviruses,4 have been identified and isolated from
strictors in relation to Burmese and other pythons.
snakes with IBD, the causative agent remains un-
Boa constrictors affected by IBD also regurgitated
known. Because the inclusions consist of a unique
food items within several days of feeding, in addition
protein (inclusion body disease protein, IBDP),5 un-
to the CNS disease signs described for pythons (Figs
derstanding the cause of IBD will be based on deter-
1 and 2). Although some snakes die within several
mining the composition and factors affecting the
weeks of first manifesting illness, others may survive
formation of this protein. To better understand the
for months. Other clinical signs observed in affected
nature of IBDP, this protein needs to be entirely or
snakes were stomatitis, regurgitation, pneumonia,
partially sequenced. Eventually the sequencing of
lymphoproliferative disorders, and round cell tu-
this protein will allow the creation of peptides that
mors. Regurgitation was not a disease sign identified
can be used in the development of better immuno-
in Burmese pythons.
diagnostic tests to screen individuals and colonies of
Hematological and selected biochemical analyte
snakes for IBDP.
values of acutely affected boa constrictors diagnosed
with IBD included leukocytosis, relative lymphocyto-
History, Hosts, and Geographic Range
In the 1970s, IBD was first identified in the United
States, where it affected multiple species of boid
snakes in private and zoological collections.2 When
first recognized, Burmese pythons (Python bivittatus)
were the most common boid snake diagnosed with
IBD. In 1998, IBD was reported in captive native
carpet (Morelia spilota variegata) and diamond py-
thons (M. spilota spilota) in Australia,3 in captive boa
constrictors in the Canary Islands, Spain,6 and sub-
sequently in Belgium.7 Beginning in the early 1990s,
more cases of IBD were diagnosed in boa constric-
tors than pythons, but the cause of this epidemio-
logic shift is unknown. Additional species diagnosed
with IBD include the green anaconda (Eunectes mu-
rinus), yellow anaconda (Eunectes notaeus), rainbow
boa (Epicrates cenchris), Haitian boa (Epicrates stria-
tus), Madagascan boa (Acranthophis madagascarien-
sis), Indian python (P. molurus molurus), reticulated
python (P. reticulatus), and ball python (P. regius). In Figure 1. Boa constrictor. Boidae. IBD. This abnormal posture is a
addition, a disease resembling IBD was diagnosed in sign of CNS disease.
218 Chang and Jacobson
Quarantining new animals is essential for risk re- mining exposure to a specific pathogen. Currently,
duction in relation to infectious disease. A quaran- demonstration of inclusions using H&E staining is
tine period of at least 90 days is recommended for the only diagnostic method being used to identify
new snake acquisitions and animals that have been cases of IBD. The sensitivity and specificity of this
to reptile swaps, although some new animals may staining technique for IBD have not been estab-
have to be quarantined for longer periods of time. lished. Second, there is the development of vaccines
Ideally, quarantined animals should be housed in a that can protect animals from infection and disease.
building that is separate from the main collection. A Unfortunately, there is no vaccine available for pro-
true quarantine, which is rarely done, takes place tection against IBD or any effective treatment. Vac-
when all new animals enter the facility on the same cine research and development are extremely costly,
day and leave on the same day, 90 days later. For IBD and the odds that the money will become available
evaluation, blood is the easiest diagnostic sample to for an IBD project are extremely low.
collect in snakes, and blood smears can be examined There are still options available to both veterinar-
for the presence of IBD inclusions in blood cells. If ians and owners to determine the IBD status of the
snake-keepers have the financial resources, biopsy animals they are presented with or own. Biopsy sam-
samples can be obtained from a snake’s tonsils, liver, ples and blood smears can be obtained from ex-
and kidneys. Collection of biopsy samples is not posed animals to screen for inclusions. If it is finan-
practical in all situations, but antemortem diagnostic cially impossible to obtain samples from all animals
testing improves the owner’s ability to identify an within a collection, then select a subset for evalua-
infected animal. In the end, the cost of recom- tion. Snakes showing signs of IBD should be imme-
mended quarantine programs and the use of diag- diately removed from the main collection and
nostic testing depend on either the owner’s financial placed in a separate room, or submitted for a micro-
situation or the importance they attach to such pre- scopic and/or necropsy evaluation. Cages of ill or
ventative medicine programs. dead animals should be disinfected with bleach and
Finally, snakes showing clinical signs of illness or allowed to dry in the sunlight for a few days. House-
anorexia and weight loss should never be added to hold bleach is the best overall disinfectant and must
an established collection. Only mite-free animals come into contact with cleaned surfaces. Although it
with a good appetite and excellent body condition will not kill every pathogen known to snakes and
should be added after the quarantine period is over. other reptiles, it is highly recommended.
Once mites infest a large snake collection, they may A question that has been asked many times is
be impossible to totally eliminate. whether the agent causing IBD can be transmitted to
neonates of either live-bearing or egg-laying snakes. We
have very little information to determine whether ver-
Managing a Collection tical transmission of this disease is possible. There are
anecdotal reports that recently hatched ball pythons
Seeing a single lone IBD-positive snake in a collec-
were diagnosed with IBD, but microscopic slides were
tion is uncommon. Typically, where there is one case
not forwarded to the authors for substantiation. One
of IBD there are others. As mentioned before, sub-
of the authors (ERJ) received a series of neonate boa
clinical cases of IBD are common. So what should be constrictors that had an IBD-positive mother, but
done in a situation where IBD has been identified in inclusions of the disease were not found in the off-
a snake collection? In extreme cases, some people spring of that animal. The problem with trying to
have depopulated entire collections of susceptible determine if vertical transmission of IBD is possible
snakes where IBD had been diagnosed and where a is related to a lack of appropriate diagnostic tests;
large number of the snakes shared the same room or molecular-screening tools that typically have a high
had been in contact with one another. Other owners degree of sensitivity and specificity are currently not
will be in denial despite evidence that IBD exists in available. The conservative viewpoint is to assume
their collection. Snake owners in denial often decide that the agent can be transmitted to offspring; there-
to conduct business as usual. This wide range of fore, neonates from known IBD-positive females
owner responses is typical for any type of animal- should not be kept, sold, or given away.
breeding operation when a potential infectious dis-
ease has been identified.
What has made a difference in controlling and Present and Future Research Needs
managing infectious disease outbreaks in domestic
animals is 2-fold. First, there is the ability to develop A study by Wozniak and coworkers demonstrated
very sensitive and specific diagnostic tests for deter- that inclusion bodies in IBD are composed of an
224 Chang and Jacobson
If there is any hope or desire for IBD to be man- 2. Schumacher J, Jacobson ER, Homer B, et al: Inclu-
aged in breeding operations of snakes sold for the sion body disease of boid snakes. J Zoo Wildl Med
pet trade, the need for such molecular-based tests is 25:511-524, 1994
3. Carlisle-Nowak MS, Sullivan N, Carrigan M, et al:
clear. The main problem scientists have regarding Inclusion body disease in two captive Australian py-
IBD research is that research dollars needed to per- thons (Morelia spilota variegata and Morelia spilota spi-
form the investigations have been extremely limited. lota). Aust Vet J 76:98-100, 1998
Although several reptile expositions and a number 4. Jacobson ER, Oros J, Tucker S, et al: Partial char-
of private individuals have made contributions to acterization of retroviruses from boid snakes with
this work, the total number of dollars received has inclusion body disease. Am J Vet Res 62:217-224,
2001
been inappropriate for the studies needed to have a
5. Wozniak E, McBride J, DeNardo D, et al: Isolation
significant impact on determining the cause of IBD and characterization of an antigenically distinct
and developing timely, cost-effective, scientifically 68-kd protein from nonviral intracytoplasmic inclu-
validated diagnostic tests. sions in boa constrictors chronically infected with the
inclusion body disease virus (IBDV: Retroviridae).
Vet Pathol 37:449-459, 2000
Concluding Remarks 6. Oros J, Tucker S, Jacobson ER: Inclusion body dis-
ease in two captive boas in the Canary Islands. Vet
IBD is one of the few worldwide diseases of captive Rec 143:283-285, 1998
snakes. The ease at which snakes can be shipped 7. Vanncraeynest D, Pasmans F, Martel A, et al: Inclu-
around the world is probably responsible for its sion body disease in snakes: a review and description
spread. Because many IBD-positive snakes may be of three cases in boa constrictors in Belgium. Vet Rec
158:757-761, 2006
subclinically infected, infected snakes considered
8. Raymond JT, Garner MM, Nordhausen RW, et al: A
healthy have been sold. It is possible that subclinical disease resembling inclusion body disease of boid
IBD infections can persist for long periods. It is snakes in captive palm vipers (Bothriechis marchi). J
unknown where this disease originated because Vet Diagn Invest 13:82-86, 2001
there are no reports of IBD in wild populations. A 9. Jacobson ER: Viruses and viral diseases of reptiles, in
sensitive and specific blood-based immunodiagnos- Jacobson ER (ed): Infectious Diseases and Pathology
tic and/or molecular test is needed to screen blood of Reptiles: A Color Atlas and Text. Boca Raton, FL,
CRC Press, pp 395-460, 2007
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snakes. Maintaining healthy and disease-free animals pathogens using electron microscopy, in Jacobson
should be the primary responsibility for all who ER (ed): Infectious Diseases and Pathology of Rep-
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Acknowledgments mun 4:703-711, 1980
12. Garner MM, Raymond JT: Methods for diagnosing
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Edward Wozniak, and Ann Dongtao Fu for technical characterization of two closely related unclassifi-
help. able endogenous retroviruses in pythons (Python
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mic inclusions in corn snakes, Elaphe guttata, resem-
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