Salmonella enterica in reptiles of German and Austrian origin.

Captive reptiles are routinely identified as reservoirs of Salmonella spp. and the number of reports about reptile-associated salmonellosis is increasing. In the present study, Salmonella were detected in 86 of 159 (54.1%) faecal reptile samples cultured. The percentage of Salmonella positive samples was significantly lower in turtles as compared with lizards and snakes, as Salmonella were only detected in one sample from a single turtle out of 38 turtles investigated. In all, 42 different Salmonella serovars were found. All isolated Salmonella belonged to the species enterica, predominantly to the subspecies I (n=46) and IIIb (n=30), but also to subspecies II (n=3), IIIa (n=6) and IV (n=2). All isolates were sensitive to the antimicrobials examined. A comparison between the reptile owners indicated that either no Salmonella were found, or that Salmonella could be isolated from all or nearly all animals of the respective owners. A significantly higher percentage of Salmonella positive reptiles was detected in the group of owners who purchase reptiles in comparison with pure breeders. A total of 88.9% of Salmonella isolates were found in samples of reptiles bought in pet shops and 58.8% in samples from wild-caught animals. The high percentage of Salmonella in reptiles in our study confirms the risk for the transmission of the infection to humans.     

In vitro inhibition of Salmonella organisms isolated from reptiles by an inactivated culture of microcin-producing Escherichia coli

OBJECTIVE: To determine whether an inactivated culture of a microcin-producing avian Escherichia coli was capable of killing Salmonella isolates from reptiles in an in vitro test system. SAMPLE POPULATION: 57 Salmonella isolate from reptiles. PROCEDURE: A wild-type avian E. coli electrotransformed with a plasmid coding for the production of microcin 24 was tested in an in vitro microassay system for its ability to kill 57 Salmonella spp isolated from reptiles. The reptile population included snakes, iguana, frilled lizards, turtles, other lizards, and unspecified reptiles. RESULTS: 44 of the Salmonella isolates were inhibited strongly, compared with the in vitro assay controls; 12 had weak inhibition, and 1 was not inhibited by the microcin-producing E. coli. Thirteen of the 57 isolates had resistance to at least 1 antibiotic, primarily streptomycin. There were 9 O serogroups identified in the 57 isolates, with serogroup H being the most prevalent (18 to 57). CONCLUSION AND CLINICAL RELEVANCE: Antibiotics are not recommended to eliminate Salmonella organisms from reptiles because of the development of antibiotic resistance. Further studies are necessary to determine whether the use of microcin-producing bacteria will be effective in controlling Salmonella infections in companion reptiles.     

Prevalence of Salmonella spp. in pet reptiles in Japan

From November 2000 to July 2002, 112 fecal samples from pet reptiles, including 18 turtles, 71 lizards and 23 snakes, sold at a pet shop were examined for the prevalence of Salmonella spp. in Japan. Salmonella spp. were isolated from 83 (74.1%) of 112 samples, and a total of 112 Salmonella isolates were identified as subspecies I to IV. The majority of isolates (62.5%) belonged to subspecies I and 54 isolates could be identified as any of 28 serovars. The predominant serovars were found to be S. Bardo, S. Newport and S. Panama, which cause human salmonellosis. These results indicate that pet reptiles may be a potential infectious source of human salmonellosis in Japan.     

Prevalence and antimicrobial resistance of Salmonella spp. in pet mammals, reptiles, fish aquarium water, and birds in Trinidad

The prevalence of Salmonella spp. was determined in 970 animals comprising 423 pet birds, 485 fish aquaria water and 62 other pets (40 pet mammals, 14 reptiles, eight others - crustaceans, snail, stingray) from both pet shops and households throughout Trinidad. The serotypes of Salmonella spp. isolated were identified and the resistance to various antimicrobial agents was determined. Overall nine (0.9%) of 970 pet animals were positive for Salmonella spp. Six isolates of Salmonella spp. were recovered from all pet birds with two isolates of serotype Aberdeen and one isolate each of Thompson, Rubislaw, Panama and Newport. The prevalence of Salmonella spp. in birds was 0.9%. Four isolates of Salmonella spp. were recovered from fish aquaria water, serotypes included Panama (two isolates), Newport (one isolate) and Virchow (one isolate). Prevalence of Salmonella spp. from fish aquaria was 0.4%. No isolate of Salmonella spp. was detected in pet mammals sampled while two isolates were recovered from reptiles, S. Enteritidis and S. Montevideo. One isolate of Salmonella spp. was recovered from a stingray, serotype unknown. Antimicrobial resistance was present is all animal types. The highest prevalence of resistance was to streptomycin among isolates from birds (83.3%) and other pets (100.0%) while isolates from fish aquarium water exhibited comparatively high resistance to cephalothin (50.0%). It was concluded that the isolation of Salmonella spp. from apparently healthy birds, fish aquarium water and other pet animals may pose a health risk to their owners and contacts as all serotypes are known to be potentially pathogenic depending on the oral dosage of the organism and the immune status of those in contact. The high prevalence of resistance to antimicrobial agents among Salmonella isolates across pet species may pose chemotherapeutic consequences to their owners and contacts.     

Prevalence of the Salmonella plasmid virulence gene "spvD" in Salmonella strains from animals]

Strains of Salmonella isolated from animals in Germany (n = 878) were analysed for the presence of the spvD gene ("Salmonella plasmid virulence gene D") by DNA-DNA hybridization. The spvD gene was only detected in strains of serovars Typhimurium (93.3%), Enteritidis (97.1%), and Dublin (100%) as well as in two rough strains of Salmonella enterica. Salmonella isolates from mammals carried the gene more frequently (cattle 94.0%, horses 92.6%, pigs 73.7%) than those from birds (33.3%) or reptiles (4.5%). Due to its high prevalence in epidemiologically relevant salmonellae, the virulence factor spvD may represent a sensitive and specific target in various serovars for diagnostic or immunization strategies.     

Introducing reptiles into a captive collection: the role of the veterinarian

The successful introduction of reptiles into a captive collection depends on providing optimal husbandry and veterinary attention. An important role of the veterinarian in this process is the prevention of disease introduction, which may affect both the introduced and the resident animals. This review focuses on preventive veterinary medicine in reptiles, emphasising quarantine measures, disinfection and entry control for infectious agents. Agents discussed include those that are likely give rise to severe clinical problems on introduction into a collection of reptiles, or, in the case of Salmonella, those that pose a significant public health risk. Aetiology, clinical signs and diagnosis are discussed for the most relevant endo- and ectoparasites, bacteria and viruses including Cryptosporidium and Entamoeba, Salmonella, Dermabacter, Chlamydiales, Mycoplasma, Herpesvirus, Adenovirus, Paramyxovirus and inclusion body disease.     

Foodborne outbreak of Salmonella subspecies IV infections associated with contamination from bearded dragons

Approximately 1.4 million Salmonella infections and 400 deaths occur annually in the United States. Approximately 6% of human Salmonella cases are thought to be associated with reptiles; Salmonella enterica subspecies IV is primarily reptile-associated. During 1-4 December, 2009, three isolates of Salmonella IV 6,7:z4,z24:- with indistinguishable pulsed-field gel electrophoresis (PFGE) patterns were identified through Minnesota Department of Health laboratory-based surveillance. None of the three patients associated with the isolates reported reptile contact; however, all had attended the same potluck dinner. Dinner attendees were asked questions regarding illness history, foods they prepared for and consumed at the event, and pet ownership. Cases were defined as illness in a person who had eaten potluck food and subsequently experienced fever and diarrhoea (three or more loose stools in 24 h) or laboratory-confirmed infection with Salmonella IV matching the outbreak PFGE subtype. Nineteen days after the event, environmental samples were collected from a food preparer's house where two pet bearded dragons were kept. Sixty-six of 73 potluck food consumers were interviewed; 19 cases were identified; 18 persons reported illness but did not meet the case definition. Median incubation period was 19 h (range: 3-26 h). Median duration of illness was 5 days (range: 1-11 days). Consumption of gravy, prepared by the bearded dragons' asymptomatic owner, was associated with illness (16/32 exposed versus 1/12 unexposed; risk ratio: 6.0; exact P = 0.02). Salmonella Labadi was recovered from 10 samples, including from one bearded dragon, the bathroom door knob and sink drain, and the kitchen sink drain. The outbreak PFGE subtype of Salmonella subspecies IV was isolated from vacuum-cleaner bag contents. This foodborne outbreak probably resulted from environmental contamination from bearded dragons. Reptiles pose a community threat when food for public consumption is prepared in households with reptiles.     

Failure to detect Salmonella species in a population of wild tuatara (Sphenodon punctatus)

AIM: To assess the prevalence of faecal excretion of Salmonella serovars by wild tuatara (Sphenodon punctatus) on Stephens Island, New Zealand. METHODS: One hundred cloacal swabs obtained as part of health-screening for the translocation of adult tuatara from Stephens Island were subjected to general aerobic culture and enrichment, and cultured specifically for Salmonella spp. RESULTS: No Salmonella spp were cultured from any of the cloacal samples, which suggests that, at the 95% confidence interval, the maximum prevalence of tuatara in the island population that were shedding Salmonella spp not detected by our sample size was 1.5%. Mixed bacteria were grown from the 70 cloacal swabs cultured aerobically. A predominant organism was evident in 30 cultures, and these were identified as Hafnia alvei type 1 (n=16) and type 2 (n=7), Corynebacterium spp (n=4), Klebsiella oxytoca (n=2), and Moraxella spp (n=1). CONCLUSIONS: The absence of intestinal carriage of Salmonella spp by the tuatara sampled in this study may indicate either lack of exposure, or an innate resistance to intestinal colonisation in tuatara. The significance of the other bacteria cultured as potential pathogens to the tuatara and as zoonotic risks is also uncertain. Wildlife managers should screen translocated reptiles for Salmonella spp, and thereby avoid exposing wild and managed populations to infection.     

Salmonella Prevalence Among Reptiles in a Zoo Education Setting

Clinically healthy reptiles may shed Salmonella and therefore act as a potential zoonotic threat. Most people in Northern European countries are rarely exposed to reptiles, but many zoos have education departments where children have direct contact with this group of animals. The objectives of this study were to determine the prevalence and serotype distribution of Salmonella among reptiles in the Education Department (n = 55) at Copenhagen Zoo and compare it to the Zoo’s main reptile collection (n = 145) to evaluate the zoonotic risk. Salmonella was isolated from cloacal swabs by selective enrichment, and a single isolate from each positive sample was further identified by biochemical tests and serotyped. The overall prevalence was 35% (69/200) with significant difference between the Education Department (64%, 35/55) and the main reptile collection (23%, 34/145). A total of 28 serotypes were detected. Ten serotypes were isolated from more than one specimen and four from more than one species. Salmonella enterica subsp. enterica serovar Eastbourne was the predominant serotype (32%, 22/69) and was also the serotype isolated from most reptile species (n = 7). Transmission of serotypes from one department to another was very limited indicated by the serotype distribution. Despite the relative high prevalence observed among the reptiles in the Zoo’s Education Department compared to the reptiles in the Zoo’s main reptile collection, no Salmonella cases have been linked to the Zoo, and Salmonella ser. Eastbourne is very rarely isolated from humans in Denmark. Simple hygienic procedures such as hand washing which is consistently carried out following handling of reptiles at the Education Department may reduce the risk and therefore contribute to this low prevalence.     

Outbreak of salmonellosis in a zoologic collection of lorikeets and lories (Trichoglossus,Lorius, and Eos spp.)

During August 2001, a syndrome characterized by acute lethargy and dyspnea was observed in a population of 45 lorikeets and lories in an open-air zoologic exhibit. The first death occurred on August 10, and within the next 12 days, nine more birds died (22% mortality rate). Hepatomegaly, reddening and congestion of the lungs, and injection of the serosal surface of the intestines were the common gross findings. Histologic changes, including fibrinonecrotic hepatitis and splenitis, bacterial emboli (liver, spleen, lung, kidney, proventriculus), pulmonary congestion and hemorrhage, and enteritis, were indicative of an acute, overwhelming bacterial septicemia. Salmonella typhimurium, with the same antibiogram, was isolated from four birds. Several birds had attacked and killed a snake on July 24, and Salmonella serogroup B (untypeable) was isolated from intestine and kidney samples of a garter snake caught in the open-air exhibit on August 28. Salmonella was also isolated from environmental samples of the exhibit but not from food preparation areas. After antimicrobial therapy, Salmonella spp. was not isolated from the surviving birds. The source of Salmonella in this outbreak remains unknown, but infection either directly or indirectly from snakes in the exhibit is possible. Contact between captive psittacine populations and reptiles should be avoided to prevent the risk of salmonellosis.     

Salmonella isolated from individual reptiles and environmental samples from terraria in private households in Sweden

Background

This study investigates Salmonella spp. isolated from privately kept reptiles and from environmental samples such as bedding materials or water from the floor of the enclosures (terraria). It also compares isolation of Salmonella using Modified Semisolid Rappaport-Vassiliadis (MSRV) medium or selective enrichment in Rappaport-Vassiliadis-Soya (RVS) pepton broth. Cloacal swabs or swabs from the cloacal area were collected from 63 individual reptiles belonging to 14 households. All reptiles were from different terraria and from 62 of these, environmental samples were also collected. Sampling were done by the reptile owners according to written instructions and sent by mail immediately after sampling. All but three samples were analyzed within 24 h after collection. Colonies suspected for Salmonella were tested for agglutination and serotyped using the White-Kauffmann-Le Minor scheme. The relative sensitivity (se) and specificity (sp) for MSRV compared with RVS, and the agreement coefficient kappa (κ) were calculated.

Results

Salmonella was isolated from 50/63 (80%) terraria, either from the reptiles (31/63; 49%) or from bedding material (39/62; 63%). The most common subspecies was Salmonella enterica subspecies enterica followed by S. enterica subspecies diarizonae. In reptiles, the most common S. enterica subspecies enterica serovars were Java (n = 4) and Fluntern (n = 4), compared with the serovars Tennessee (n = 10) and Fluntern (n = 10) in the environmental samples. The exact same set of Salmonella subspecies and serovars were not isolated from the individual reptiles and the environmental samples from any of the households. Isolation using MSRV yielded more Salmonella isolates 61/113 (54%) than enrichment in RVS 57/125 (46%). The se was 97.9% (95% Confidence Interval 93.9-100), the sp 78.5% (95% CI 68.5-88.5) and the κ 0.74, indicating substantial agreement between the tests.

Conclusions

Salmonella can be expected to be present in environments where reptiles are kept. This constitutes public health risks and should be considered during handling of the reptiles and during cleaning and disposal of bedding. A combination of different culturing techniques may be used to increase the isolation rate.     

Reptile‐Associated Salmonellosis in Minnesota, 1996–2011

Reptile‐associated salmonellosis (RAS) occurs when Salmonella is transmitted from a reptile to a human. This study describes the epidemiology of RAS in Minnesota during 1996–2011. All Minnesotans with confirmed Salmonella infections are reported to the Minnesota Department of Health (MDH). Case patients are interviewed about illness characteristics and risk factors, including foods eaten, drinking and recreational water exposures, contact with ill people, and animal contact. Willing RAS case patients can submit stool from the reptile for culture. Serotype and pulsed‐field gel electrophoresis (PFGE) subtype of Salmonella isolates from reptiles and case patients are compared. Of 8389 sporadic (not associated with an outbreak) non‐typhoidal salmonellosis case patients in Minnesotans during 1996–2011, 290 (3.5%) reported reptile exposure. The median age of case patients with reptile exposure was 11 years, 31% were under the age of 5 years and 67% were under the age of 20 years; 50% were female. The median illness duration was 8 days; 23% required hospitalization. The most commonly reported reptile exposures were lizard (47%), snake (20%), turtle (19%) and a combination of reptile types (14%). Eighty‐four per cent of isolates from case patients who reported reptile exposure were Salmonella enterica subspecies I. The three most common serotypes were Typhimurium (15%), Enteritidis (7%) and subspecies IV serotypes (7%). Of 60 reptiles testing positive for Salmonella, 36 (60%) yielded the same Salmonella serotype as the human isolate. Twenty‐six of 27 reptile isolates that were subtyped by PFGE were indistinguishable from the human isolate. Of these, 88% were subspecies I; the most common serotypes were Enteritidis (12%), Typhimurium (8%), and Bareilly (8%). RAS accounts for approximately 3.5% of salmonellosis cases in Minnesota, primarily affecting children. The majority of isolates from case patients and reptiles belonged to Salmonella subspecies I, suggesting that reptiles are a source of human infection with serotypes not traditionally considered to be reptile‐associated.     

Salmonella enterica isolates from faeces of domestic reptiles and a study of their antimicrobial in vitro sensitivity

From October 2001 to February 2002, the faecal samples of 305 reptiles (165 saurians, 99 ophidians and 41 chelonians) were bacteriologically examined to detect Salmonella enterica. S. enterica was isolated from 73 (23.93%) faecal samples including 44 (60.27%) samples collected from saurians, 15 (20.55%) from chelonians and 14 (19.18%) from ophidians; considering the number of samples taken for each reptile group, S. enterica was isolated from the 36.58% of chelonians, 26.66% of saurians and 14.14% of ophidians. The isolates were distributed among 38 serotypes. Sixty-nine (94.52%) isolates were resistant to erythromycin. About one-third of the isolates was resistant to sulfisoxazole (35.61%), gentamycin (32.88%), amoxycillin (31.51%) and ampicillin (27.40%). All but one of the isolates were sensitive to chloramphenicol. A high percentages of isolates were sensitive to enrofloxacin (84.93%), nitrofurantoin (80.82%), trimethoprim (76.71%) and tetracycline (75.34%).     

Disease patterns in the Detroit Zoo: a study of reptilian and amphibian populations from 1973 through 1983

A retrospective study was conducted to determine disease patterns in reptilian and amphibian populations at the Detroit Zoo from 1973 through 1983. In the reptilian population (mean +/- SD = 285.2 +/- 28), overall annual mortality rates were 1% to 40%. Mortality rates were highest in the fall months (20%) and lowest in the winter months (6%). The most frequently affected reptiles were iguana (Iguana iguana), reticulated python (Python reticulatus), rattlesnakes (Crotalus spp), common boa (Constrictor constrictor), and lizards (various genera of suborder Lacertilia). Of the 1,300 reptilian deaths from 1973 through 1983, 36.6% were caused by microbial agents, 12% by parasites, 11.6% by trauma, and 9.3% by nutritional deficiencies. The main microbial organisms that caused death were Aeromonas spp, Salmonella spp, Pseudomonas spp, Proteus spp, and Edwardsiella spp. The main parasites that caused death were Entamoeba spp and lungworms. Among amphibians, frogs and toads were the most frequently affected, and starvation and trauma were the most frequent causes of death.     

A Multistate Investigation of Antibiotic‐Resistant Salmonella enterica Serotype I 4,[5],12:i:‐ Infections as Part of an International Outbreak Associated with Frozen Feeder Rodents

While most human Salmonella infections result from exposure to contaminated foods, an estimated 11% of all Salmonella infections are attributed to animal exposures, including both direct animal handling and indirect exposures such as cleaning cages and handling contaminated pet food. This report describes the epidemiologic, environmental and laboratory investigations conducted in the United States as part of the response to an international outbreak of tetracycline‐resistant Salmonella enterica serotype I 4,[5],12:i:‐ infections with over 500 illnesses occurring from 2008 to 2010. This investigation found that illness due to the outbreak strain was significantly associated with exposure to pet reptiles and frozen feeder rodents used as food for pet reptiles. Salmonella isolates indistinguishable from the outbreak strain were isolated from a frozen feeder mice‐fed reptile owned by a case patient, as well as from frozen feeder mice and environmental samples collected from a rodent producing facility (Company A). An international voluntary recall of all Company A produced frozen feeder animals sold between May 2009 and July 2010 occurred. Only 13% of cases in our investigation were aware of the association between Salmonella infection and mice or rats. Consumers, the pet industry, healthcare providers and veterinarians need to be aware of the potential health risk posed by feeder rodents, whether live or frozen. Frozen feeder rodent producers, suppliers and distributors should follow the animal food labelling requirements as described in 21 CFR §501.5, and all packages of frozen feeder rodents should include safe handling instructions. Persons should wash their hands thoroughly with soap and water after handling live or frozen feeder rodents, as well as reptiles or anything in the area where the animals live. Continued opportunities exist for public health officials, the pet industry, veterinarians and consumers to work together to prevent salmonellosis associated with pet food, pets and other animals.     

Comparison of phenotypic traits and genetic relatedness of Salmonella enterica subspecies arizonae isolates from a colony of ridgenose rattlesnakes with osteomyelitis.

Reptiles are well-known sources of human Salmonella infections; however, little is known about the ability of Salmonella to cause disease in reptiles. Thirty-seven isolates of Salmonella enterica subspecies arizonae (S. arizonae) were obtained from retrospective and prospective studies of a closed colony of ridgenose rattlesnakes (Crotalus willardi) with osteomyelitis. All isolates (N = 7) from bone lesions were of a single serotype, 56:z4,z23, and this serotype was found on only 1 occasion among 8 other serotypes isolated from 21 cloacal and intestinal samples. The remainder (N = 7) of serotype 56:z4,z23 isolates were from other extraintestinal sites, including liver, ovary, blood, and testis. S. arizonae isolates were susceptible to most antimicrobials, and plasmid profiles did not correlate with serotype or antimicrobial resistance. Isolates of the 56:z4,z23 serotype (N = 14) formed a tight cluster with 95% similarity by XbaI macrorestriction analysis. Individual isolates of serotypes, 56:z4,z23, 38:(k)-z35, and 48:i-z invaded HeLa cells but an isolate of serotype 50:r-z did not. The same individual isolates of serotype 56:z4,z23 and 48:i-z also invaded viper heart cells. The Salmonella InvA gene was detected by polymerase chain reaction (PCR) in all S. arizonae serotypes tested, including 5 serotype 56:z4,z23 isolates and individual isolates of serotypes 48:i-z and 50:r-z. A source or possible explanation for increased virulence of S. arizonae serotype 56:z4,z23 in this unique host has not been found.     

Salmonella Isolations from Snakes and Other Reptiles

Bacteriological examination of faeces and swabs from fourteen species of reptiles predominantly constrictors, yielded six serotypes of Salmonella as well as Arizona hinshawii, Proteus species, Citrobacter freundii and Enterobacter species. Organisms isolated were identified using conventional bacteriological methods and yielded two serotypes of salmonellae not previously identified in Canada: Salmonella nima and Salmonella 58:a.     

Diseases of chelonians: (1) Necropsy survey of tortoises.

The results of necropsies of 144 tortoises of 17 species that died in captivity are presented. Intestinal and nutritional disorders (27.0 and 22.2 per cent respectively) were the most common causes of death. Nematode infestations were found in 43.8 per cent, but with exception of a few species the parasites were seldom pathogenic. Infestations with other helminths appear to be very unusual. Protozoan infections were relatively common (at least 22.9 per cent) but protozoa are probably seldom pathogenic. Bacterial infections occurred in 7.6 per cent and no fungal infections were diagnosed. It was tentatively concluded that infections with Salmonella spp are less important in tortoises than in other reptiles in this country. In 34.7 per cent of cases no diagnosis was made.     

杭州市2010～2012年野生动物救护情况分析

杭州市野生动物救护中心于2010～2012年救护野生动物98种491只,其中杭州市有分布的动物种类占84．7％,在救护动物种类和数量上鸟类最多,其次为爬行类、哺乳类,最少为两栖类。救护动物的成活率两栖类（93．8％）和爬行类（92％）均比较高,而兽类（54．5％）最低。3a期间救护动物月分布频次亦为鸟类最高,依次为爬行类、兽类、两栖类：救护动物高峰为4～6月、8月、10—11月。本文通过对这些救护动物的种类分布、数量、保护级别、成活率、救护病因、救护主体和救护频次等进行分析,讨论出了今后救护野生动物更有效的方法,旨在促进杭州市野生动物救护工作。     

The rate of Salmonella spp. infection in zoo animals at Seoul Grand Park, Korea

Salmonellosis is an important zoonotic disease that affects both people and animals. The incidence of reptile-associated salmonellosis has increased in Western countries due to the increasing popularity of reptiles as pets. In Korea, where reptiles are not popular as pets, many zoos offer programs in which people have contact with animals, including reptiles. So, we determined the rate of Salmonella spp. infection in animals by taking anal swabs from 294 animals at Seoul Grand Park. Salmonella spp. were isolated from 14 of 46 reptiles (30.4%), 1 of 15 birds (6.7%) and 2 of 233 mammals (0.9%). These findings indicate that vigilance is required for determining the presence of zoonotic pathogen infections in zoo animals and contamination of animal facilities to prevent human infection with zoonotic diseases from zoo facilities and animal exhibitions. In addition, prevention of human infection requires proper education about personal hygiene.