Reptiles and zoonoses
Reptiles and Zoonoses by Vet .Dr .L. Sch****** (1)
Cohabitation between mankind and animals has always been a risky business as far as sanitary risks are concerned .Captive Reptile care and breeding cannot escape this rule :reptiles carry many pathogenic agents which are likely to infest or infect people and are potential vectors of various zoonoses .
However ,this risk must not be overestimated ,for contracting a zoonosis is conditioned by several factors :the more or less anthropomorphic links between the owner and his or her pet reptile , the hygiene and salubrity of the captive surroundings of the animal ,as well as its geographic origin .
• *According to the WHO definition ,zoonoses are diseases and infections which are naturally transmitted from vertebrate animals to people ,and reciprocally .
-Bacterial zoonoses :
Salmonellosis is the most frequent disease transmitted by reptiles [1,2,5,6,8,12,15,19,25].It is known in people under two different forms :non-typhic salmonellosis infection ,and typhoid fever .
Salmonellosis sp . is an anaerobic Gram – optional bacillus of the Enterobacteriaceae family ,generally a flagellate ,and widely spread around the world .Salmonella nomenclature is particularly complex ,as it is subject to perpetual controversies .Nowadays ,the classification of the Salmonella genus comprises two species : S. enterica and S. bongori, and six subspecies of S. enterica  :
- S. enterica enterica (sub-group I)
- S. enterica salamae (sub-group II)
- S. enterica arizonae (sub-group III)
- S. enterica diarizonae (sub-group IIIb)
- S. enterica houtenae (sub-group IV)
- S. enterica indica (sub-group V)
Salmonella enteritidis, Salmonella paratyphi, Salmonella typhi and Salmonella typhimurium are mere serovars of the subspecies Salmonella enterica enterica (Salmonella enteritidis, Salmonella paratyphi A, Salmonella typhi, Salmonella typhimurium).
Sub-group I is the most frequently isolated one among humans whereas othersubspecies are generally isolated from poikilothermous animals and from their surroundings [13,17].Serovar identification in sub-group I is called after thier geographic localities (ex : S.e.e. san diego, S.e.e. panama, S.e.e.tenessee) ,and for other subgroups according to its antigenic formula (ex : “H3 flagellate antigens ,"O" somatic heat –stable antigens , antigens "Vi" thermolabile capsular antigens – Vi for virulence) . 2435 different serovars are currently described within the genus Salmonella ,of which a great majority belongs to group I .The subspecies arizonae and diarizonae ,the most frequently isolated ones among reptiles ,own respectively 94 and 321 serovars .
In more than 80% of reported cases ,human salmonelloses are caused by food .They are linked to the consumption of insufficiently cooked meat ,(ranking among the MFTI ,Mass Food Toxi-Infections ) and /or to bad hygienic conditions in developing countries .But food and drinking water are not the sole sources of contamination for people .Indeed ,almost 90% of captive reptiles are healthy carriers of various serotypes of salmonella ,which they inconstantly defecate .These saprophyte opportunist bacteria are particularly well tolerated in poikilothermous animals ,providing they are well-fed and housed ,but they can also provoke septicaemia ,coelomites ,lung pathologies ,lethal gastro-enteritis ,in reptiles weakened by unsuitable captive conditions or by secondary infections [2,3,11,12,14,17].
The transmission risk of salmonella from reptiles to humans was particularly well studied in the USA in the 70’s ,considering the massive increase of cases among children ,as a parallel to the introduction of baby red –eared tortoises (Trachemys scripta elegans) in American households (15 million tortoises were sold every year in the 70’s in the US ) .Between 1963 and 1974 ,among the 2 million salmonellosis cases found on humans per year in the U.S. ,about 280 000 cases per year were described in children aged under 10 owning a tortoise (which represents a 14% incidence on annual cases ) )[13,17] .Facing the unfruitlful attemps to create in breeding farms "Salmonella-free"tortoises in 1975 ,the American authorities have declared as illegal the sale of red-eared tortoises of less than 4 inches ( shell length) .Indeed ,smaller tortoises generate more manipulations from children ,and the excretion of salmonella seems more important during the three first years of life .This measure has enabled a decrease of 77% of salmonellosis cases induced by these animals to take place  .Today ,in the States ,reptiles would be responsible for 3 to 5% of human salmonellosis cases [13,17] .
France had to wait September 1993 to apply a regulation on the importation of red-eared tortoises on its territory ,and September 1997 for its prohibition .The prophylaxis of reptile-induced salmonellosis cases is mainly based on sanitary recommendations : washing hands before and after manipulations ,and the respect of some basic hygienic rules are sufficient to avoid this zoonosis (see framed section ) [2,13] .Vaccination against typhoid exists(i.e. : Vaccine Typhim Vi) ,but only protects against the infection of Salmonella enterica enterica serovar typhi.
Many mycobacteria species ,said to be pathogenic for humans ,have been isolated on apparently healthy or sick reptiles (i.e.: Mycobacterium tuberculosis, M. avium, M. marinum) [3,4,7,13]. Reptiles infected with tubercolosis show chronical injuries ,sometimes granulomatous ,on the lungs ,liver ,spleen ,skin ,central nervous system ,buccal mucous membranes and gonades .Humans can become sick either through the inhalation of buccal or respiratory secretions of an infected reptile ,or by a contamination through a skin cut ,while cleaning the terrarium ,manipulating the animal or after a bite .
Wearing gloves ,glasses and a mask is a good preventive reflex against this zoonose .The treatment of a tuberculous reptile is not advisable ,because of the risks runned by other individuals around it ,humans or reptiles  .
Aeromonas sp is a Gram – bacillus of the Pseudomonadaceae Family .It is an opportunist pathogenic germ belonging to the saprophyte flora of reptiles ,among which it is thought to be responsible of many potentially fatal infectious diseases (pneumopathies, “Mouth Rot”, enteritis, septicaemias …). This bacteria is commonly found in the wild in freshwater inhabited by reptiles ,fishes and amphibians (lakes ,ponds...) ,but also in captive conditions ,in water bowls ,in the basins of vivaria with or without an aquatic area .Contamination to humans is usually made through the contact of infected water with a small skin wound .It can also happen after having been clawed by a tortoise .As far as Aeromonas sp. (and particularly Aeromonas hydrophila) is found among the usual oro-pharyngian microfauna ,every bite from a reptile can be a source of aeromonosis .Likewise ,many bacteria located in the buccal cave such as Serratia, Klebsiella, Enterobacter, Providencia, Citrobacter, Campylobacter, Proteus, Bacteroïdes and Pseudomonas (ex: P. aeruginosa) [7,12,13] can cause similar infections .All these bacteria ,also found in the digestive tractus of reptiles ,are likely to create gastro-intestinal disorders in humans of the “infectious gastro –enteritis type” through oro-fecal contamination ,particularly among children [13,23] . Enterobacter cloacae and Klebsiella pneumoniae are even considered as frequent sources of uro-genital infections for humans living alongside with reptiles . Yersinia enterocolitica is mainly responsible for gastro-enteritis with fever on humans ,which can be misleaded with an appendocitis false symptom . Yersinia pseudotuberculosis ,a bacteria often found in reptiles fed with wild rodents ,is responsible for mesenteric adenites and septicaemias on humans .
Human parasitoses originating from reptiles are not uncommon in South East Asia and in Africa ,areas in which the behaviour and cooking habits favour theses zoonoses .
• Pentastomidosis (or linguatulosis).
Pentastomids ,also called porocephales or linguatulids ,are worm-shaped organisms different from helminths which are parasites ,often under a sub-clinic form ,the respiratory tractus of reptiles (see § Parasitology) [3,9,13,16,24].It is as an accidental host that a human being can infest his- or herself :drinking contaminated water holding pentastomid eggs ,manipulating without hygienic measures a parasited reptile ,or eating raw or insufficiently cooked reptile meat [3,9,13]. The genus Armillifer (ex: A. moniliformis, A. armillatus) is the main agent responsible for human porocephalosis . After having being eaten and after having hatched ,these eggs release larvae which migrate towards the liver and lungs ,where they can cause ,according to their localisation ,damages like hepatic cirrhosis, icteria, purulent pneumonia , peritonitis, meningitis or pericarditis .Then ,these larvae enkyst themselves ,die and calcify in less than two years in different areas of the body .At this stage ,they can be detected through X-ray photos [3,9].No medical treatment enables to eradicate it until now ,neither in reptiles nor in humans .In reptiles ,the only solution is extraction through endoscopy , [9,16] and in humans ,extracting calcified larvae kysts require to be removed with a surgery act .Prevention of this zoonose consists of a parasitologic fecal examination of every wild-caught reptile newly acquired .Embryoned eggs ,eliminated through saliva or feces ,are easy to identify [9,16,24].
Even if reptiles are frequently carriers of digestive protozoans (ex: Entamoeba sp., Cryptosporidium sp., Giardia sp., Trichomonas sp…), blood protozoans (ex: Plasmodium sp., Trypanosoma sp.) or urinary (ex: Hexamita sp.),they have never been reckoned as directly responsible for human protozooses .These microscopic single-celled organisms are generally speaking specific to ectothermous animals ,and sometimes exclusively of reptiles .
Humans can mainly suffer from two larval cestodo-zoonoses ,sparganosis and mesocestoidosis ,after the consumption of the raw meat of a reptile hosting taenia larvae as a second intermediate host .
Ophidians can host in their underskin conjunctive tissues plerocercoïd larvae (called "sparganum") of Spirometra sp.,a pseudophyllidian cestod of the Diphyllobothridae Family ,of which the definitive hosts are wild canidae or felidae .Snakes take part in the evolutive cycle of the parasite while ingesting a small copepod crustacean (the first intermediary host ) or a prey which has been infested with larvae [3,13,24]. Humans can also accidentally host plerocercoid larvae :in Asia ,some popular beliefs claim that the consumption of snake flesh can cure arthrosis ,tuberculosis ,and sexual impotence .The « miracle meat » is even sometimes used directly as a cataplasm on inflammatory wounds of all kinds ,thus enabling parasite larvae to penetrate into the body through a skin cut and to conceal in miscellaneous parts of the body .Human sparganosis is clinically noticed through ocular symptoms (with the total destruction of the eye ) and overall (linked to the migrations of larvae within the body ) [13,24].
Humans can become infested with cestodes of the Diplopylidium and Mesocestoides Genus called “tetrathyridia” ,while eating meat or innards from a reptile which have been insufficiently cooked (i.e. raw liver ,heart ) .These cestod larvae have been found in the liver ,on the mesenterium ,within the coelomic cavity and myocarde of some snakes and lizards (rattlesankes ,king snakes ,iguanids ) ,intermediary hosts of a parasitic cycle which have birds and wild or domestic carnivores as definitive hosts .
The only reptile nematods likely to parasite humans are larvae of some worms of the Superfamily Spiruroïdea :spirurudae (ex: Spirura sp.) and gnathostomatidae (ex : Tanqua sp.). The zoononse can occur ,in South –East Asia ,through the ingestion of reptile meat when it holds ,as a second intermediary host ,larval forms of parasites .These larvae get through the intestinal wall ,colonize the bladder and conceal behind the eyes .
The famous gamasiform and blood-eating acarians of snakes of the Genus Ophionyssus (O. natricis) are able to infest human skin during long and repeated contacts with heavily infested animals .Nevertheless ,a sole case of pruriginous dermitis ,papulo-vesicular and bubbling ,was reported in 1975 in several membres of the same family hosting an infested snake .Considering the number of reptile hobbyists owning ophidians which carry ectoparasites in the world ,this case is merely anecdotical and the risk is very low .Likewise ,humans can host ixodiformic acarians of the Hyalomma or Ixodes Genus ,as well as prostigmatic acarians of the Trombiculidae Family (ex : Trombicula, Eutrombicula) . But much more than the possible skin wounds caused by bites of all these acarians ,the risks of transmission of infectious agents from reptile hosts do represent a zoonotic threat for mankind .Indeed ,as an example ,Ixodes pacificus ,an external parasite of some colubridae and of some lizards from the Pacific coast of the United States ,can inoculate the agent of tularemia (Francisella tularensis) or of the Lyme disease (Borrelia burgdorferi). The situation is similar with Ixodes ricinus ,the European tick ,an occasional parasite of some lacertidae , Amblyomma nuttalli ,the agent of “Q fever “ provoked by Coxiella brunetii  or Ornithodoros turicata ,a vector of human leptospirosis with Leptospira pomona .
Prophylaxia and sanitary rules aimed at minimizing the zoonosis risks when in contact with reptiles :
-Wash carefully and systematically your hands with warm water and soap after having manipulated a reptile or after having touched any item of its enclosure .
-Do not settle any reptile enclosure in a room aimed at storing food or eating (kitchen ,living room ,cellar ) .
-Disinfect regularly with bleach the whole of the enclosure (using single-use gloves ,and ,if possible ,a protection mask ,and never use kitchen tools during this cleaning ) .
-Never clean the water dish or vivaria furnishings in the sink where the washing-up is done or in the bathroom sink .
-Always favour hygiene to the aesthetic aspect when building and arranging a reptile enclosure .To enable an efficient disinfection ,a simple setting ,easy to clean ,must be designed .
-Do not drink ,eat nor smoke while handling reptiles or while cleaning its enclosure .
-Never kiss a reptile !
-Deter children and immunodepressive individuals from handling reptiles .
-Avoid contacts between reptiles and other pets living in the same place .
-Always disinfect and watch closely a wound caused by a reptile claw or bite .
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2.- ARVY C., 1997. Salmonelloses humaines liées aux tortues : une revue du problème et de son évolution. Bull. Soc. Herp. Fr. , (84) : 25-31.
3.- BROGARG J., 1987. Les reptiles et la santé humaine. In Les maladies des reptiles. Les Éditions du point Vétérinaire, Maisons-Alfort : 301-310.
4.- BROWNSTEIN DG, 1984. Mycobacteriosis. In HOFF GL, FRYE FL, JACOBSON ER (eds): Diseases of Amphibians and Reptiles. New York, Plenum Press, 1984, pp1-22.
5.- CHIODINI R.J., 1983. The pathogenicity of Salmonella in snakes. Proceedings of the First International Colloquium on Pathology of Reptiles and Amphibians (Vago and Matz), Presse de l'Université d'Angers, Angers : 45-48
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7.- COOPER J.E., 1981. Bacteria. In Diseases of the Reptilia. Academic Press, London, vol.1 : 165-191.
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9.- DRABICK JJ, 1987. Pentastomiasis. Rev. Inf. Dis. 9(6) : 1087.
10.- FOX JG, 1991. Campylobacter infections and salmonellosis. Semin Vet Med. Surg. (Small Anim), 6(3) : 212.
11.- FRYE, F.L., 1981.. Biomedical and Surgical aspects of Captive Reptile Husbandry. Veterinary Medicine Publishing Company : Edwardsville, KS : -
12.- FRYE, F.L., 1981. Infectious diseases. Fungal Actinomycete, bacterial, rickettsial and viral diseases. In Biomedical and Surgical aspects of Captive Reptile Husbandry. Veterinary Medicine Publishing Company : Edwardsville, KS : -
13.- JOHNSON DELANAY C.A., 1996. Reptile Zoonoses and threats to public health. In Mader : Reptile Medicine and Surgery. Philadelphia : W.B Saunders Company : 20-33.
14.- JOORIS R., 1993. Infections bactériennes et traitement antibiotique chez les serpents : un nouveau point de vue. Bull. Soc. Herp. Fr., 65-66 : 63-68.
15.- LAMM SH, TAYLOR A, GANGAROSA EJ et al, 1972. Turtle-associated salmonellosis. I. An estimation of the magnitude of the problem in the United States, 1970-1971. Am. J. Epidemiol., 95(6) : 511.
16.- MADER D.R., 2001. Pentastomidiasis in an indigo snake. Proceedings of the North American Veterinay Conference, Orlando (FL) : .
17.- MITCHELL M. A., 2001. Salmonella in reptiles. Proceedings of the North American Veterinay Conference, Orlando (FL) : 812.
19.- ONDERKA DK, FINLAYSON MC, 1985. Salmonellae and salmonellosis in captive reptiles. Can. J. Comp. Med. 49 (3) : 268.
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21.- SAEED AM, HARRIS NV, DIGIACOMO RF, 1993. The role of exposure to animals in the etiology of Campylobacter jejuni/coli enteritis. Am. J. Epidemiol. 137 (1) : 108.
22.- SCHULTZ H, 1975. Human infestation by Ophionyssus natricis snake mite. Brit. J. Dermatol. 93 : 695.
23.- SHAYEGANI M, STONE WB, DEFORGE I et al, 1986. Yersinia enterocolitica and related species isolated from wildlife in New York state. Appl. Environ. Microbiol. 52(3):420.
24.- SCHILLIGER L. Les affections parasitaires chez les reptiles. Etude bibliographique et expérimentale. Applications prophylactiques et thérapeutiques en terrariophilie. Th. Méd. vét. Nantes, 1990, 403 p.
25.- STAIR GM, TACAL JV Jr, LAWRENCE W et al, 1989. Association of Salmonella typhimurium infection with a household iguana. Calif. Morbidity, vol 42.
26.- YADAV MD, SETHI MS, 1979. Poikilotherms as reservoirs of Q Fever (Coxiella brunetii) in Uttar Pradesh. J. Wildl. Dis. 15 : 15.
(1) In France,the Vet professional code forbids any kind of advertising or personal data about vets being displayed.
Translation by Thorrshamri/Hervé Saint Dizier 2006,with kind permission for the original text of the Genus Boiga website :http://boiga.infos.st/
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