Salmonella Associated with Snakes (Suborder Serpentes)

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Etiology
The current classification of Salmonella is complex.The genus is divided into two major species: S. enterica and S. bongori (subspecies V). S. enterica is further divided into six distinct subspecies based on biochemical differences: enterica (subspecies I), salamae (subspecies II), arizonae (subspecies IIIa), diarizonae (subspecies IIIb), houtenae (subspecies IV), and indica (subspecies VI).Salmonella strains may be further classified by serology into over 2500 serotypes (serovars) using the Kauffman and White classification scheme.This scheme defines the serogroup according to the expression of somatic lipopolysaccharide O antigens (LPS), and the serotype based on the expression of flagellar H antigens (Barrow et al., 2010;Grimont & Weill, 2007;Mitchell & Shane, 2001).Besides serving for classification purposes, the variations in LPS structure provide each serotype a different degree of virulence (Paré et al., 2006).Serotypes may be referred to by a name or an antigenic formula.In this chapter, strains will be referred to by the genus followed by the serotype or the number of the subgroup: Salmonella enterica enterica serotype Typhimurium will be referred to as "S.Typhimurium", Salmonella enterica diarizonae 60:r:z 15 as "S.60:r:z 15 " , Salmonella enterica diarizonae (IIIb) as "S.IIIb", and so forth.
Distinct patterns of infection (pathovars) may also be used to classify serotypes.There are three pathovars: the first includes a few serotypes that produce severe systemic disease in healthy animals; the second pathovar comprises serotypes that affect young animals and pregnant or egg-laying females; the third pathovar includes serotypes that cause infection in immunocompromised animals (Barrow et al. 2010).
The classification of strains based on their host range (host-specific, host-restricted, ubiquitous) is controversial (Barrow et al., 2010).Clinical signs involving the digestive tract are the predominant manifestations of the infections by the generalist serotypes.These infections are characterized by high morbidity but low mortality.In contrast, infections caused by serotypes adapted to specific animal species or a restrict group of hosts will tend to present low morbidity and high mortality (Hoelzer et al., 2011).
In reptiles, Salmonella inhabits the distal small intestine and the colon (Carvalho, 2006); however its presence seldom produces primary disease, as the bacteria seem to be part of the indigenous gut flora of these animals (Mitchell, 2004).
The first reports of Salmonella isolation from reptiles date back to cases involving lizards in 1939.In 1944, the bacterium was first isolated from a Bull Snake (Pituophis catenifer) and in 1946 from a turtle.However it was not until 1953, when a human was shown to have probably acquired salmonellosis from a chelonian, that these isolations were considered relevant (Mathewson, 1979).Hinshaw & McNeil (1944, 1945, 1946, 1947) were two researchers that greatly contributed on the first Salmonella isolations from reptiles.
There is a very broad diversity of serotypes amongst reptiles (Pedersen et al., 2009).From all known serotypes, approximately 40% are predominantly associated with these animals (Hoelzer et al., 2011).Even though there are no reptile-specific serotypes, subspecies III is known to be the most common in snakes (Warwick et al., 2001).Other studies have also demonstrated that Salmonella enterica diarizonae (IIIb) corresponds to 92.8% of the serotypes Please use Adobe Acrobat Reader to read this book chapter for free.
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In the past it was generally believed that subspecies III was a part of the reptile normal gastrointestinal microbiota (Orós et al., 1996).While serotypes of all Salmonella subspecies have been isolated from snakes (Bemis et al., 2007), S. IIIa seems to be the most pathogenic for these animals as it is most frequently isolated in cases with clinical disease (Lamberski et al., 2002;Ramsay et al., 2002).It must be taken into account, however, that due to recent changes in the nomenclature and structure of antigenic formulas used to classify Salmonella strains it is often difficult to determine to what extent the previous reports involved the subspecies IIIa and IIIb (Bemis et al., 2007).In Brazil, the subgroup III (formerly classified as genus Arizona) was first isolated in snakes in 1973, by Moreno and colleagues.
The retrieval of Salmonella strains from a reptile does not per se elucidate its role as a disease or potential zoonosis, as clinically healthy snakes may host highly virulent serotypes (Johnson-Delaney, 2006).Furthermore, the development of disease depends on a variety of factors such as animal species, individual susceptibility, stress, and inoculated dose (Carvalho, 2006).

Prevalence
One of the first estimates of Salmonella prevalence among snakes was performed by Chiodini & Sundberg in 1981, who described rates of infection ranging from 16 to 92%.Another study conducted by Chiodini (1982), found that 55 out of 56 snakes (98%) were naturally infected with Salmonella.Several other studies determined the prevalence of these bacteria in snakes throughout the world: 92.5% and 69.2% in Australia (Iveson et al., 1969;Scheelings et al., 2011), 24% in Austria (Pfleger et al., 2003), 64.7% in Brazil (Bastos et al., 2008), 71.6% in Germany and Austria (Geue & Löschner, 2002), 69.7% in Taiwan (Chen et al., 2010), and 15% in Trinidad (Gopee et al., 2000).Prevalence is generally high in snakes; however it is important to consider these numbers may vary broadly depending on the evaluation methods (Johnson-Delaney, 2006).
The most prevalent Salmonella strains in snake fecal samples may vary over time (Schröter et al., 2004), however such fluctuations have yet to be understood (Schröter et al., 2006), but it has been suggested that failures of the isolation methods and intermittent elimination of the bacteria in the feces may be involved (Chiodini & Sundberg, 1981).

Sources of infection
Fecal shedding is well documented in snakes (Ramsay et al., 2002) however other potential sources of infection must be considered (Warwick et al., 2001).The bacteria may be present in the oral cavity and there is a remote possibility of transmission through bites (see Treatment).The bacteria can also be eliminated via the cloaca in the eggs, feces, urine, and possibly other secretions.Ramsay et al. (2002) reported that in a colony of rattlesnakes, some of which presented Salmonella-associated osteomyelitis, contaminated wood shaving substrate might have been a Please use Adobe Acrobat Reader to read this book chapter for free.
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source of infection when snakes were transferred among cages.The transmission of Salmonella through inanimate objects has been well described in a Salmonella outbreak in Komodo Dragons (Varanus komodoensis) held captive at a zoo (Friedman et al., 1998).Furthermore, considering the natural tongue-flicking behavior of snakes, the ingestion of substrate during prey consumption is probably not necessary to cause infection, as the briefest contact of the tongue with a contaminated surface could be sufficient to acquire Salmonella.Although the bacterium is frequently present in the environment, large outbreaks in humans are rarely caused solely due to environmental contamination (Friedman et al., 1998).Some reptiles may inoculate Salmonella through bites and claw scratches.It is also possible that humans could be infected through ear or eye contact with feces, urine or water from the snakes' cages (Warwick et al., 2001).A snake may become infected when maintained in poor hygiene conditions, in cages or exhibits with accumulation of excrements (Fornazari & Teixeira, 2009).

Methods of transmission
Transmission occurs primarily through the fecal-oral route, but may also occur through the ingestion of contaminated food or water.Bacteria present in inanimate surfaces or in the animals may also be transmitted indirectly (Carvalho, 2006).Snake prey, whether wild animals captured by free-ranging snakes or laboratory animals used to feed captive snakes, may present distinct species-specific characteristics that influence the acquisition of Salmonella.This bacterium has been frequently retrieved from wild rodents (Hoelzer et al., 2011) and other vertebrates upon which free-ranging snakes feed, however its prevalence tends to be generally lower in wild than in captive reptiles (Gray, 2011).
Although most snakes feed on vertebrates, some have specialized on invertebrate-based diets.Mollusks and crustaceans may also be consumed by snakes and it is believed that they may be a source of Salmonella to humans and other animals.Information is yet insufficient to confirm whether they could be potential sources of infection for snakes, but it has been suggested that they could maintain these bacteria in natural environments (Minette, 1984).
The indirect transmission from reptiles may occur because Salmonella can retain its virulence for several days or months in the environment.This has been shown to be particularly important for small children, as they may often become infected without ever touching the pet reptile (Bays, 2005;Hoelzer et al., 2011).Mermin et al. (2004) reported that Salmonella can been isolated from the aquarium water of chelonians several weeks following contamination, and the bacteria can be recovered from the reptiles' feces even several months after defecation.It is likely that strains from semiaquatic snakes may persist for several weeks in the water of their cages.
Salmonella has been used for several decades in an unusual manner: as a rodenticide.Even nowadays these products are still produced in some countries, despite the risk they are known to pose to human health (Painter et al., 2004).Such rodenticides are prepared using Salmonella Typhimurium and S. Enteritidis (Hoelzer et al., 2011).In addition to the unnecessary risk of transmission to humans, the strains used in these products may infect food, livestock and wildlife.
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Another form of Salmonella infection is vertical transmission.Investigating chelonians, Kaufmann and colleagues (1972) reported that the first studies on this subject indicated transovarian infection may occur, but with unknown frequency and likely with less relevance than post-laying contamination of the eggs.Those authors did not succeed in isolating Salmonella from the ovarian tissues of the turtles as they had done before (Kaufmann & Morrison, 1966) and suggested their previous findings could be due to rapid bacterial penetration through the egg shell after oviposition, resulting in infected newborn animals.In the 1960s, it was already known that Salmonella quickly penetrated turtle eggs, contaminating them as they passed through the cloaca or were laid in contaminated soil (Chiodini & Sundberg, 1981).In the following decades, the isolation of Salmonella from turtle ovarian tissues and egg contents as had been performed by Kaufmann and Morrison (1966) was not reproduced (Kaufmann et al., 1972) nor investigated in other reptiles (Chiodini & Sundberg, 1981).Snake fetuses are not sterile, and the shedding of Salmonella by hatchlings does not necessarily occur even when the fetuses are already infected by that microorganism (Chiodini, 1982).Salmonella is only shed in the feces when the digestive tract of the fetus is infected, not in systemic or coelomic infections.Moreover, because Salmonella may be isolated in one fecal culture and not in another, it is possible that fetuses positive to S. arizonae may be delivered by a female that had negative fecal cultures during pregnancy (Chiodini, 1982).
In a study carried out in Germany, Schröter et al. (2006) observed 65% Salmonella prevalence in newborn snakes, suggesting that colonization may have occurred during pregnancy or upon birth.There seems to be no correlation between a specific serotype and its success in being transmitted to the host's progeny.
Discussions on the vertical transmission of a pathogen are generally focused on the female, whether it is an oviparous or viviparous species.The male is not often considered, either because it is not recognized as playing a significant role in vertical transmission or simply because it is forgotten.In certain snake species sperm transfer during copulation may be very prolonged, the cloacae remaining in intimate contact during this period, which may be sufficient for the exchange of bacteria between male and female.Moreover, it has been shown that some female snakes can store viable sperm from copulation for up to 6 years, a phenomenon called amphigonia retardata (Mader, 2006).There is research that can help us evaluating the possibility of sexual transmission of Salmonella from male to female, and the potential hazard for posterior vertical transmission to the progeny (Hidalgo-Vila, 2007, as cited in Pedersen et al., 2009).For instance, Chiodini (1982) did not succeed in isolating Salmonella from snake testes, whilst Ramsay et al. (2002) successfully isolated S. arizonae from the testes of a Crotalus willardi, and noted that active spermatogenesis occurred despite the presence of granulomatous infiltrates.
Behavioral characteristics may interfere with the acquisition and elimination of Salmonella by a snake.The high prevalence of Salmonella in terrestrial (ground-dwelling) snakes when compared to arboreal snakes may be explained by behavioral differences and by the higher risk for the terrestrial species to come in contact with contaminated excrements in the soil or substrate (Schröter et al., 2004).Semiaquatic snakes, which spend most of their time inside water, present a greater probability to acquire Salmonella by hydric transmission.This becomes particularly relevant for snakes in captivity, where the concentration of bacteria may become high depending on the maintenance routine and the characteristics of their Please use Adobe Acrobat Reader to read this book chapter for free.
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tank or artificial lake.There is a case report of fatal bacterial sepsis in Water Snakes (Helicops modestus) in which the lack of flowing water was considered a contributing factor for the contamination of the cages with Proteus vulgaris (Coutinho et al., 2001).
Although they often prefer to place their feces on a corner of the cage, snakes may defecate and urinate in various locations, including in watering bowls, particularly after ecdysis.Urine may be contaminated by fecal debris upon expelling through the cloaca.Some freshwater chelonians can drain water into the cloaca and release it at the nesting site to soften the soil and facilitate oviposition (Warwick et al., 2001), a behavior that may lead to the contamination of the nest and eggs.

Diagnostic techniques
The diagnostic method most frequently used to isolate Salmonella is microbiological culture (Mitchell, 2006).Isolation protocols and information on culture media are easily found in the vast scientific literature on this topic.The isolation of this bacterium generally involves: direct culture, enrichment, inoculation on culture plates, screening for suspect colonies and confirmation through biochemical and serological tests (Waltman, 2000).Most techniques and protocols used for the isolation of Salmonella from other sources are also used for its isolation from reptiles.
Although microbiological culture may fail to detect some asymptomatic carriers (Bradley & Angulo, 2008), it may assist investigations concerning the transmission of Salmonella from reptiles to humans (Gray, 2011), while biomolecular assays such as pulsed-field gel electrophoresis (PFGE) provide additional confirmatory clues.
Tetrathionate, Rappaport-Vassiliadis and selenite broths are the selective-enrichment media used to isolate Salmonella.To isolate this bacterium from reptiles, Mitchell (2006) recommends selenite broth.After incubation, a small aliquot of the primary enrichment broth is transferred to a selective medium.Although the direct culturing of a sample is usually unsuccessful, Bastos et al. (2008) were able to isolate multiple Salmonella and other enterobacteria from intestinal mucosa swabs of Bothrops jararaca.
Most of the broad variety of selective media used to isolate Salmonella from other animals has already been tested for reptiles, and the XLT4 agar has been shown to provide the best results (Bastos et al., 2008;Mitchell, 2006).In spite of the morphologic similarity of Salmonella colonies with those of other Enterobacteriaceae in MacConkey agar, Bastos et al. (2008) isolated 7 colonies on this agar (poorly selective media) when compared to the 13 colonies obtained from the same samples using the XLT4 agar (highly selective media); MacConkey agar is seldom used to specifically isolate Salmonella.
Selective screening media are used to confirm or rule out suspect colonies.The most commonly used are lysine iron agar (LIA), urea and triple sugar iron agar (TSI), besides a variety of commercial biochemical test kits (Mitchell, 2006).
After confirmation of the Salmonella genus, colonies can be submitted for serotyping.Subsequently, the isolates may be further identified using molecular methods such as ribotyping and PFGE (Ghilardi et al., 2006;Nair et al., 2002).Non-culture diagnostic methods can also be used for the detection of Salmonella, such as enzyme-linked immunosorbent assays (ELISA) and polymerase chain reactions (PCR).Both techniques can detect low numbers of bacteria in a sample (Mitchell, 2006); however are seldom applied for reptiles.
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Knowledge on the dynamics of this bacterium may be obtained through antigenic characterization and molecular methods (Nair et al., 2002;Sá & Solari, 2001).However, studies on the virulence of Salmonella in snakes still lack appropriate infection models (Bernis et al., 2007).

Clinical signs
In reptiles, Salmonella gastroenteritis leads to diarrhea (Funk, 1996), particularly in acute form.Other clinical signs include coelomitis, pneumonia, and septicemia.Hypovolemic shock and death may also occur.The feces may become green-grayish and contain mucus or blood.Small hemorrhagic spots may appear on the mucous membranes and ventral scales in animals with sepsis.Reptiles in this condition may also exhibit muscle weakness (Messonnier, 1996).
Inappetance and regurgitation with blood and mucus were observed in a Rosy Boa (Lichanura trivirgata) with gastrointestinal lesions (Orós et al., 1996).Extra-intestinal salmonellosis may also occur.S. arizonae has been associated with extensive bone lesions on the vertebrae and ribs of snakes, leading to limited mobility and prostration.Severely affected animals lose their righting reflexes and fail to capture prey (Ramsay et al., 2002).Salmonella-associated pneumonias in Boa constrictor may also lead to dyspnea (Onderka & Finlayson, 1985).

Pathological findings
Several reports dating back to the 1940s demonstrated that snakes may harbor Salmonella, often without any clinical manifestations (asymptomatic carriers) or with clinical signs and lesions typically related to the disease.Although this does not occur frequently, the first descriptions reported hepatic lesions and intestinal inflammation (Page, 1966).Inflammation and necrosis are often present in many organs.However, Salmonella can occur in virtually any visceral tissue of clinically healthy snakes (Chiodini, 1982) and its implication in the death of snakes and other reptiles is uncommon.In snakes, salmonellosis may manifest as necrotizing subacute severe enteritis, normally involving the distal half of the intestines (Onderka & Finlayson, 1985).The intestinal tract of two Crotallus willardi that died from enteritis presented heterophilic necrotizing and granulomatous lesions (Ramsay et al., 2002).A Rosy Boa (Lichanura trivirgata) with gastrointestinal clinical signs presented diffuse thickening of the gastric wall with necrotic and fibrinonecrotic lesions (Orós et al., 1996).
Besides the digestive tract, the urinary tract and the liver were found to be frequently infected in a survey conducted by Chiodini (1982).In snakes, Salmonella septicemia produced hepatitis associated to granulomas (Onderka & Finlayson, 1985).
Lesions associated with S. arizonae are frequently observed in the gastrointestinal tract, spleen, liver, oviduct and ureter.Lesions in the respiratory tract are less common.Orós et al. (1996) observed tracheal necrosis and inflammation caused by S. arizonae in a double-headed Honduran Milksnake (Lampropeltis hondurensis) which had been found dead without previous clinical signals.Onderka & Finlayson (1985) reported fibrinous alveolar exudation and interstitial inflammatory infiltration in the lungs of a Boa constrictor deceased from a pneumonia caused by Salmonella.
In snakes with osteomyelitis, the bone lesions presented heterophilic-granulomatous inflammation, osteonecrosis and sequestra, periosteal bone proliferations in the form of exostoses accompanied by heterophilic-granulomatous inflammation, and trabecular and cortical osteopenia; oophoritis and salpingitis also occured (Ramsay et al., 2002).

Antibiotics
It is not possible to eliminate Salmonella from the digestive tract of reptiles.Experience has shown it is impossible to raise Salmonella-free reptiles (Association of Reptilian and Amphibian Veterinarians [ARAV], 2009), suggesting a participation of environmental contamination in the infection, and indicating that the animals may maintain latent infections (Mermin et al., 2004).
The administration of antimicrobial agents is not recommended for enteric salmonellosis in reptiles, as some studies have demonstrated that the course of the disease is not affected by the antimicrobial therapy.On the other hand, treatment of systemic salmonellosis should include intensive care and appropriate antimicrobial therapy (Hirsh, 2004).
Whenever possible, antibiotic choice should be based on antimicrobial sensitivity testing.When this is not possible, information from the literature may be useful: Salmonella strains isolated from snakes are generally sensitive to aminoglycosides, quinolones and trimethoprim-sulfamethoxazole, and are often resistant to ampicillin, cefoperazone, chloramphenicol, neomycin, streptomycin and tetracycline (Bastos et al., 2008;Chen et al., 2010;Gopee et al., 2000).Multi-resistant strains are uncommon.Bastos et al. (2008) demonstrated that Salmonella isolates from Jararacas were sensible to most antimicrobials tested.Salmonella strains carried by free-ranging snakes are also generally sensitive to antibiotics.Indiscriminate use of antibiotics can select resistant strains, however Jijón et al. (2007) pointed out that the emergence of drug-resistant bacteria is not mandatorily associated to prior antimicrobial therapy.
Several bacterial genera, including Salmonella, may be isolated from the mouth of snakes that are clinically healthy or with stomatitis (Mehler & Bennett, 2006).However, prophylactic antibiotic administration is not recommended for victims of ophidism if the snake species involved has venom lacking strong cytotoxic effects, such as is the case for South American Rattlesnakes (Crotalus durissus) (Nishioka et al., 2000).Although the incidence of abscesses on the bite wound area is approximately 12% for accidents involving South American Bothrops spp.(Ribeiro & Jorge, 1990, 1997), the specific involvement of Salmonella is clearly not a problem (Andrade et al., 1989;Jorge et al., 1990).This also applies to large constrictor snakes Please use Adobe Acrobat Reader to read this book chapter for free.
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It is likely that the bacterial diversity found in the snake oral microbiota reflects the variation in the fecal microbiota of the live prey they ingested, particularly as the prey often defecates while it is being killed and consumed (Goldstein et al., 1979).These researchers mentioned that live rodents were used to feed the studied captive snakes, however oftentimes the studies on differences in the microbiota of wild and captive snakes do not specify which food items were offered to the animals.Another important consideration is that food and stress may alter the snake oral microbiota depending on the lifetime spent in captivity.

Probiotics and prebiotics
The capacity of the microbial flora to prevent the multiplication of a given microorganism is called competitive exclusion (Schneitz & Mead, 2000).Probiotics act in this manner: they are live microorganisms that provide beneficial effects to their host's health that go beyond their inherent nutritional value.Studies demonstrate that only a few organisms truly act as probiotics (Myers, 2007).
Studies from the 1980s and the early 1990s demonstrated that the successful colonization of the cecum of turkeys by bacteria such as Lactobacillus reuteri and Bacillus subtilis may provide protection against the establishment of Salmonella in the microbiota; these findings were accompanied by general improvements in viability, body mass, and feed conversion efficiency.Research on hens, however, have generally failed to reproduce those results and did not provide protection against the colonization by Salmonella (Hafez & Jodas, 2000).Recent studies have indicated some organisms that might be more successful in preventing Salmonella colonization in the ceca of hens, and Pascual and colleagues (1999) demonstrated that Lactobacillus salivarius strain CTC2197 may be an effective competitor against the establishment of S. Enteritidis in the intestinal epithelium of hens.
The administration of probiotics on the feed of Green Iguanas (Iguana iguana) is anecdotally said to eliminate Salmonella from their gastrointestinal tract.However, such effect was not demonstrated in Carpet Pythons (Morelia spilota), as the probiotics did not prevent the shedding of the bacterium in the feces (Holz & Middleton, 2002).Although at the moment no tests on the use of probiotics in snakes have produced successful results, efforts to characterize their intestinal microflora have been conducted aiming to identify microorganisms that may be used for the competitive exclusion of Salmonella (Gray, 2011).
Prebiotics are another group of substances intended to modify the intestinal environment, favoring the growth of beneficial microorganisms while preventing the proliferation of pathogens.Lactulose is a prebiotic with beneficial effects on the health of domestic animals, and has also been used to prevent the growth of Salmonella in their digestive tract (Holz & Middleton, 2005).This compound is used as a nutritional substrate, to promote the growth of desirable bacteria.Pathogenic bacteria, on the other hand, are unable to use this energetic substrate and their growth is suppressed by the acidification of the intestinal environment (Jankowski, 2009).Unfortunately, however, lactulose failed to prevent the elimination of Salmonella in the feces on studies conducted with Carpet Pythons (Morelia spilota) and Scrub Pythons (Morelia amethystina) (Holz & Middleton, 2005).
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Prevention and control
A number of measures may be taken to interrupt the proliferation of Salmonella in the environment, eliminate it whenever possible and prevent it from reaching specific areas: rigorous hygiene and disinfection of facilities and equipment, isolation of sick animals and asymptomatic carriers, measures of animal welfare, and the complete removal of organic matter to facilitate disinfectant action.Sodium hypochlorite (bleach) is an effective and lowcost disinfectant that may be used for the sanitation of exhibits and cages.It should also be kept in mind that asymptomatic carriers are important sources of infection (Carvalho, 2006), as infected animals are normally isolated and monitored, thus reducing transmission (Fornazari & Teixeira, 2009).
The general public is often unaware of the risks associated to salmonellosis, failing to take basic hygiene practices while handling reptiles.Simple hygiene procedures alone can considerably decrease the probability of transmission (Hoelzer et al., 2011).Friedman et al. (1998) demonstrated that washing hands after attending a reptile exhibit or before the next meal is sufficient to prevent reptile-associated salmonellosis.This hygiene routine oftentimes is not properly followed by children under the age of five, and as a result this age group is more prone to become contaminated (Centers for Disease Control and Prevention [CDC], 2010).
The release of animals to their natural habitats, as performed by wildlife rehabilitation centers, should be thoughtful to avoid spreading Salmonella to free-ranging populations (Jijón et al., 2007).
Table 2 presents a list of instructions cooperatively elaborated by the Association of Reptilian and Amphibian Veterinarians (ARAV) and the Center for Disease Control and Prevention (CDC) to reduce human exposure and disease development risks involving reptiles.Table 3 provides a client educational handout developed by the ARAV.
Veterinarians who treat reptiles should educate their clients who own reptiles about Salmonella and provide information on the recommended precautions for reducing the risk of transmission of Salmonella from reptiles to humans.This is especially important in households with infants and children under 5 years of age or with immunocompromised persons.The CDC recommends that households with children less than 5 years of age not own reptiles.
All veterinarians, staff and clients who handle reptiles should follow recommended precautions for reducing the risk of transmitting Salmonella from reptiles to humans.These precautions are also included in the ARAV client education handout and are based on good personal hygiene and not allowing reptiles to soil the owners' domicile.
All reptiles should be presumed to be carrying Salmonella in their intestinal tract and to be continuously or intermittently shedding it in their feces.Bacterial culture of fecal specimens from reptiles to determine Salmonella infection status is discouraged.If veterinarians are called upon to assist health officials in determining the cause of salmonellosis in a person, bacterial culture of combined fecal and cloacal specimens from reptiles with which that person has had direct or indirect contact are recommended.Serotyping of Salmonella isolates is usually needed to help discern the source of the Salmonella in human infections.
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It is not recommended to treat healthy reptiles with antimicrobial agents with the intention of eliminating Salmonella from the intestinal tract.Clients who request treatment of healthy reptiles for Salmonella should be discouraged from such treatment and cautioned about the possibility of causing the emergence of antimicrobial-resistant Salmonella strains that might pose a greater health risk to humans (Bradley & Angulo, 2008).
Table 2. Salmonella and reptiles: veterinary guidelines Always wash your hands with hot, soapy water after handling reptiles, reptile cages and equipment, and the feces of reptiles.
Do not allow reptiles to have access to the kitchen, dining room, or any other area in which food is prepared or eaten.Also, do not allow reptiles to have access to bathroom sinks and tubs or to any area where infants are bathed.Consider keeping your reptiles caged or limiting the parts of the house where reptiles are allowed to roam free.Always wash your hands after coming into contact with any area where reptiles are allowed to roam free.Do not eat, drink, or smoke while handling reptiles, reptile cages, or reptile equipment.Do not kiss reptiles or share food or drink with them.
Do not use the kitchen sink, kitchen counters, bathroom sinks or bathtubs to bathe reptiles or to wash reptile cages, dishes or aquariums.Reptile owners may wish to purchase a plastic basin or tub in which to bathe or swim their reptiles.Waste water and fecal material should be disposed of in the toilet instead of the bathtub or household sink.
The CDC recommends that children less than five years of age avoid contact with reptiles and those households with children less than five years of age not own reptiles.The ARAV encourages reptile owners with young children to discuss steps to minimize risks associated with owning reptiles with their reptiles' veterinarian and their physician.Children should be supervised when they are handling reptiles to ensure that they do not place their hands or objects that a reptile has contacted in their mouths.Reptiles should not be kept in childcare centers.
Immunocompromised persons should avoid contact with reptiles.
Follow instructions from your reptile's veterinarian concerning proper diet and environment for your reptile.Healthy reptiles living in proper environments are less likely to shed Salmonella bacteria (ARAV, 2008).1% of the reported cases of human salmonellosis are caused by reptile-associated strains (Hoelzer et al., 2011).Moreover, many patients recover rapidly without having received any treatment, further increasing underreporting (Gray, 2011).
Human salmonellosis is most frequently associated with food ingestion, however direct or indirect contact with animals in public or private environments may also be sources of infection (Hoelzer et al., 2011).Reptile-associated human infections only occur if the reptile or a feces-contaminated object is placed in the mouth.Physical contact with a reptile alone is thus not sufficient to produce infection in humans (ARAV, 2008).
Immunological, biological and behavioral characteristics are probably the reason why human salmonellosis is most frequent in children, especially the youngest (Hoelzer et al., 2011), although the disease may also occur in other age groups, including healthy adults (Warwick et al., 2001).
Many reports associate human Salmonella infections with isolates from snakes.Four cases were selected for discussion here; these cases will be presented in chronological order and were chosen because they are representative, interesting and illustrate the diversity of manners in which these exposures may occur.It is important to note that the development of molecular assays and their incorporation to the set of diagnostic techniques results in chronologically-increasing precision in comparing isolates retrieved from humans and reptiles in each case.
In July 1977, for the first time, S. eingedi was isolated from a snake in Israel and from a child that had diarrhea shortly after that.That serotype was also isolated from another child with diarrhea in the same Israeli community (Cahan, 1980).
In 1997, Paton & Mirfattahi presented the case of a 5-month-old boy with bacterial meningitis.S. uzaramo was isolated from the cerebrospinal fluid, blood and stool samples of the patient.The same serotype was isolated from the feces of an Indian Python (Python molurus) and two Ball Pythons (P.regius); S. arizonae and an unidentified isolate were also cultured from the Ball Pythons.Jafari et al. (2002) reported S. Enteritidis infections resulting from a platelet donation.The apparently healthy donor had acquired an asymptomatic S. enterica bacteremia from his Boa Constrictor.Two patients receiving the platelet donation developed sepsis, and one of them died.The reptilian origin of the infection was confirmed through the determination of the serotype by PFGE.
A large S. Typhimurium outbreak occurred in the United States in 2005 and 2006.Several people had direct or indirect contact with snakes that had been fed with commerciallyraised mice.The rodents had been captive raised, euthanized, vacuum-packed, frozen and sold through the internet.Cultures from three of those mice yielded pure isolates of S. Typhimurium that were indistinguishable by PFGE from the isolates obtained from the human cases, snakes, and environmental samples (Fuller et al., 2008).

Snake products as food items, folk remedies, and human salmonellosis
Despite the legal prohibitions and the risks of foodborne bacterial infections, many communities worldwide consume sea turtle meat and eggs.The raw or undercooked meat, Please use Adobe Acrobat Reader to read this book chapter for free.
Just open this same document with Adobe Reader.If you do not have it, you can download it here.You can freely access the chapter at the Web Viewer here.
often prepared in unsanitary conditions, may result in human salmonellosis (Aguirre et al., 2006).In an outbreak of salmonellosis that occurred in Australia in 1988 it was found that 62% of the victims had ingested green turtle meat.Several people were hospitalized, and S. chester was isolated from undercooked sea turtle meat samples and from fecal samples of the patients (O'Grady & Krause, 1999).
Similarly to the consumption of chelonians, snakes are also used for meat production (Magnino et al., 2009).Although in the USA and in some Asian countries there are specific breeding facilities for this purpose, snakes may also often be collected from the wild.The consumption of snake meat poses a risk to the development of salmonellosis due to the high prevalence of this microorganism in these animals, and also probably because oftentimes the adequate hygiene measures are not properly carried out.Snake powder and dried meat, especially those prepared from rattlesnakes, are often used in folk medicine.However, several reports have associated the consumption of these products to the development of salmonellosis in humans (Babu et al., 1990), as well as infections by other Enterobacteriacea.Most of these cases occur in Mexican-American patients.Consumers often ingest such products while presenting underlying chronic and immunosuppressive conditions such as cancer, diabetes, arthritis, systemic lupus erythematosus, or acquired immunodeficiency syndrome (AIDS) (Sharma et al., 1993;Waterman et al., 1990).These conditions further complicate the cases, as Salmonella infections will tend to produce much more severe clinical manifestations and complications.For example, patients with AIDS may present recurrent bacteremia (Babu et al., 1990) and patients with gastric cancer may develop peritonitis (Sharma et al., 1993).Not only many Salmonella serotypes can be isolated from such rattlesnake capsules (Cone et al., 1990) but it also seems likely that all types of folk medicine preparations generally involve poor conditions of hygiene during their preparation, which may be yet another factor for the contamination of these products.

Conclusion
Numerous authors argue that Salmonella is a normal component of the reptilian intestinal microbiota and that 90% or more of reptiles harbor Salmonella, however some European researchers do not share that opinion (Hassl & Benyr, 2003), and there is evidence in other continents that some serotypes may be considerably pathogenic for the snakes (Bemis et al., 2007;Ramsay et al., 2002).
Basic hygiene practices may be sufficient to prevent most cases of human salmonellosis (Mitchell, 2004), even when it is known that snakes are very likely to be infected by Salmonella in both domestic and natural environments (Mermin et al., 2004).
It is vital to acknowledge Salmonella as an inhabitant of the digestive tract of reptiles, as this basic understanding is a solid basis to interpret the disease it may cause, to improve the life quality of these animals in captivity, and to take appropriate prevention and control measures.

References
Aguirre, A.A. et al. (2006).Hazards associated with the consumption of sea turtle meat and eggs: a review for health care workers and the general public.
, and was proven to have caused Please use Adobe Acrobat Reader to read this book chapter for free.Just open this same document with Adobe Reader.If you do not have it, you can download it here.You can freely access the chapter at the Web Viewer here.

Table 3 .
Salmonella bacteria and reptiles: client educational handout

9. Zoonotic aspects 9.1 Snake-associated human salmonellosis
Animal transmitted-salmonellosis is thought to be underreported, and the registered cases are probably biased towards uncommon or unusual characteristics.For instance, less than Please use Adobe Acrobat Reader to read this book chapter for free.Just open this same document with Adobe Reader.If you do not have it, you can download it here.You can freely access the chapter at the Web Viewer here.
EcoHealth, Vol. 3, No.  3,Please use Adobe Acrobat Reader to read this book chapter for free.Just open this same document with Adobe Reader.If you do not have it, you can download it here.You can freely access the chapter at the Web Viewer here.