Tiny Turtles Purchased at Pet Stores are a Potential High Risk for Salmonella Human Infection in the Valencian Region,Eastern Spain

Abstract

Turtles may be considered unsafe pets, particularly in households with children. This study aimed to assess Salmonella carriage by turtles in pet stores and in private ownership to inform the public of the potential health risk, enabling informed choices around pet selection. During the period between September and October 2013, 24 pet stores and 96 private owners were sampled in the Valencian Region (Eastern Spain). Salmonella identification procedure was based on ISO 6579: 2002 recommendations (Annex D). Salmonella strains were serotyped in accordance with Kauffman–White–Le-Minor technique. The rate of isolation of Salmonella was very high from pet store samples (75.0% ± 8.8%) and moderate for private owners (29.0% ± 4.6%). Serotyping revealed 18 different serotypes among two Salmonella enterica subspecies: S. enterica subsp. enterica and S. enterica subsp. diarizonae. Most frequently isolated serotypes were Salmonella Typhimurium (39.5%, 17/43) and Salmonella Pomona (9.3%, 4/43). Serotypes identified have previously been reported in turtles, and child Salmonella infections associate with pet turtle exposure. The present study clearly demonstrates that turtles in pet stores, as well as in private owners, could be a direct or indirect source of a high risk of human Salmonella infections. In addition, pet stores should advise their customers of the potential risks associated with reptile ownership.

Introduction

Salmonellosis is one of the most prevalent zoonosis worldwide (European Food Safety Authority 2012). It was estimated that nontyphoidal Salmonella causes around 59,153 deaths each year worldwide (Havelaar et al. 2015). More than 1 million cases of foodborne salmonellosis have been estimated to occur annually in the United States (Scallan et al. 2011). In Europe, over 100,000 laboratory-confirmed cases are reported each year (European Food Safety Authority 2012). Currently, at a global level, salmonellosis represents an important public health problem and controlling the disease has become a challenge in most countries (European Food Safety Authority 2012).

Although humans usually become infected with Salmonella through ingestion of Salmonella-contaminated food, 6% of Salmonella infections overall are acquired from direct or indirect contact with turtle (Mermin et al. 2004). The most popular reptiles are chelonians, although there are also a large number of lizards and snakes kept as pets (Lafuente et al. 2013). Wild and pet reptiles are generally known to be asymptomatic carriers and natural reservoirs of several Salmonella serotypes (Mermin et al. 2004, Nakadai et al. 2005, Hidalgo-Vila et al. 2007, Marin et al. 2013).

From a public health point of view, turtles commonly shed Salmonella and are, therefore, unsafe pets, particularly in households with children (Harris et al. 2010). Nevertheless, as the proportion of worldwide salmonellosis infections in humans transmitted by reptiles is low (Editorial team et al. 2008, Cooke et al. 2009, Lafuente et al. 2013, Pees et al. 2013), it is considered sporadic. Moreover, the popularity and number of exotic reptiles kept as pets have risen, leading to an increase in the number of reptile-associated zoonotic pathogen infections, especially in vulnerable patients such as infants, young children, the elderly, or immunocompromised adults (Schröter et al. 2004; Hernández et al. 2012, Centers for Disease Control and Prevention 2012).

Based on this information, many countries have recognized the risk of the increasing number and popularity of pet reptiles (Lukac et al. 2015) and it has been recognized as a significant public health issue in Europe and the United States (Editorial team et al. 2008, Centers for Disease Control and Prevention 2012). Multiple reports since 2004 suggest that exposure to small pet turtles is a persistent source of salmonellosis in young children (Voetsch et al. 2004).

The objective of the present study is to assess Salmonella carriage by turtles in pet stores and private owners to inform the public of the potential health risk and allow them to make informed choices around pet selection.

Materials and Methods

This project is included in the LIFE+Biodiversity section, which aims to develop innovative projects or demonstrations that contribute to the implementation of the objectives of the Commission communication (COM (2006) 216 final) “Halting the loss of Biodiversity for 2010 and beyond.”

Sample collection

During the period between September and October 2013, 24 pet stores and 96 private owners were sampled in the Valencian Region (Eastern Spain). The Conselleria de Infraestructuras, Territorio y Medio Ambiente (regional administration) gave permission to take samples in the pet stores. Private owners were contacted by advertising the project through the University community (CEU Cardenal Herrera University, University of Valencia, and Polytechnic University of Valencia). As bacteria excretion is not continuous, water samples were taken after 2 days without filtration or water changes according to Marin et al. (2013). Water samples were collected in sterile 0.5-L polypropylene bottles filled by hand in the deepest part of the aquariums. Samples from the pet stores were collected by veterinary inspectors. Private owners personally brought samples to the laboratory. In both cases, all samples were processed within 6 h of collection. Each of the participants was provided with a questionnaire that was completed and submitted together with the samples to the laboratory. The questionnaire containing specie, number of animals in the aquarium, age of the animal, aquarium volume, and housing (indoor vs. outdoor) was completed.

Detection of Salmonella spp.

The procedure was based on ISO 6579: 2002 recommendations (Annex D). Samples were pre-enriched in 1: 10 vol/vol Buffered Peptone Water 2.5% (BPW; Scharlau^®, Barcelona, Spain) and then incubated at 37°C ± 1°C for 18 ± 2 h. The pre-enriched samples were transferred onto Semi-Solid Modification Rappaport Vassiliadis agar plate (MSRV; Difco^®, Valencia, Spain) and incubated at 41.5°C ± 1°C for 24–48 h. The culture obtained in MSRV was inoculated onto Xylose–Lysine–Deoxycholate (XLD; Liofilchem^®, Valencia, Spain) and Xylose–Lysine–Tergitol-4 (XLT4; Biokar Diagnostics^®, Pantin Cedex, France) and incubated at 37°C ± 1°C for 24–48 h. After incubation, five typical colonies were streaked onto the surface of predried nutrient agar plates (Scharlau^®, Barcelona, Spain) at 37°C ± 1°C for 24 ± 3 h. Then, a biochemical test using API (API-20^®; bioMérieux, Madrid, Spain) was performed to confirm Salmonella spp. Salmonella strains isolated were serotyped by the Ministry of Agriculture, Fisheries and Food Reference Laboratory (Algete, Madrid, Spain) in accordance with Kauffman–White–Le-Minor technique.

Statistical analysis

Data relative to number of animals in the aquarium, age of the animals, and aquarium volume were analyzed using a General Linear Model (GLM) with sample origin (pet store and private owner [indoor and outdoor]) as a fixed factor. In addition, a GLM, which assumed a binomial distribution for Salmonella shedding, was fitted to the data to determine whether there was an association with sample origin (pet store and private owner). Analyses were performed with SPSS 21.0 software package (SPSS, Inc., Chicago, IL, 2002). Values were considered statistically different at p < 0.05. Results are reported as least square mean with standard error of the mean (SEM).

Results

During the study, 120 samples (Table 1) were evaluated. They were distributed as follows: 20.0% (24/120) from pet stores and 80.0% (96/120) from private owners. The private owners housing distribution was as follows: 62.4% (77/96) from indoor turtles and 15.8% (19/96) from outdoor turtles. Details of sample origin, number of animals in the aquarium, age of the animals, aquarium volume, and housing are provided in Table 1. A total of 35 number of species of turtles were identified (Table 2). The 10% of the samples were obtained from aquariums with turtles of different species. In the pet stores, the most common species identified were, in decreasing order: Graptemys pseudographica (45.8%), Pseudemys rubriventris (12.5%), and Pseudemys nelsoni (8.3%). In the private owners, the most common species identified were, in decreasing order: Chelydra serpentina (34.4%), Trachemys scripta elegans (19.8%), Macrochelys temminckii (5.2%), and P. nelsoni (4.2%). All turtles in the pet stores were kept indoors. Pet store showed a significant higher number of animals in the aquarium (30 ± 3.1) compared to outdoor private owner aquariums (6 ± 3.4, p < 0.001) and indoor private owner aquariums (2 ± 1.7, p < 0.001). Pet stores also had much younger turtles (2 ± 10.6 months, p < 0.001) compared to private owners (131 ± 11.7 and 39 ± 5.9 months for outdoor and indoor private owner, respectively). In addition, pet store showed significant differences in the aquarium volume (43 ± 109.0, p < 0.001) compared to outdoor private owner aquariums (705 ± 134.6, p < 0.001) and indoor private owner aquariums (8 ± 80.24, p < 0.001).

Table 1.

Information Obtained by Questionnaire

Sample origin	n	Number of animals in the aquarium	Age of the animals (months)	Aquarium volume (liters)
Pet stores	24	30 ± 3.1^a	2 ± 10.6^c	43 ± 109.0^b
Private owner
Outdoor	19	6 ± 3.4^b	131 ± 11.7^a	705 ± 134.6^c
Indoor	77	2 ± 1.7^b	39 ± 5.9^b	8 ± 80.24^a

n, number of samples collected. Numbers within columns with different superscripts differ (p≤0.05).

Table 2.

Percentages of Salmonella spp. Isolated from Private Owners and Pet Store Turtles for the Different Species Analyzed

Sample origin	Turtle species	No. of samples (%)	No. of isolates (%)
Pet store
Only	Graptemys pseudographica pseudographica	11 (45.8)	7 (38.9)
Only	Pseudemys floridana	1 (4.2)	1 (5.6)
Only	Pseudemys nelsoni	2 (8.3)	1 (5.6)
Only	Pseudemys peninsularis	1 (4.2)	0 (0.0)
Only	Pseudemys rubriventris	3 (12.5)	3 (16.7)
Mix	G. pseudographica and Graptemys ouachitensis	1 (4.2)	1 (5.6)
Mix	G. pseudographica and P. rubriventris	2 (8.3)	2 (11.1)
Mix	P. nelsoni and Trachemys gaigeae	1 (4.2)	1 (5.6)
Mix	Trachemys scripta elegans and G. pseudographica	1 (4.2)	1 (5.6)
Mix	T. scripta elegans and P. nelsoni	1 (4.2)	1 (5.6)
	Total	24 (20.0)	18 (75.0)
Private owners
Indoor
Only	Chelydra serpentina	32 (41.6)	13 (61.9)
Only	Chrysemys picta marginata	1 (1.3)	1 (4.8)
Only	Emydura subglobosa	1 (1.3)	0
Only	Emys orbicularis	1 (1.3)	0
Only	Graptemys ouachitensis	1 (1.3)	0
Only	G. p. Pseudographica	3 (3.9)	0
Only	Kinosternon carinatus	2 (2.6)	1 (4.8)
Only	Kinosternon leucostomum	1 (1.3)	0
Only	Macrochelys temminckii	4 (5.2)	0
Only	Mauremys leprosa	1 (1.3)	0
Only	Pelusios niger	1 (1.3)	1 (4.8)
Only	Pseudemys concinna	1 (1.3)	0
Mix	P. concinna and T. scripta elegans	1 (1.3)	1 (4.8)
Only	P. Nelsoni	4 (5.2)	2 (9.5)
Only	P. Peninsularis	1 (1.3)	0
Only	Terrapene Carolina	2 (2.6)	0
Only	T. scripta elegans	17 (22.1)	1 (4.8)
Only	Trachemys scripta scripta	1 (1.3)	0
Only	Trachemys scripta troostii	1 (1.3)	1 (4.8)
	Total	77 (62.4)	21 (27.3)
Outdoor
Only	C. Serpentina	1 (5.3)	0
Only	Chrysemys picta dorsalis	1 (5.3)	0
Only	Clemmys guttata	1 (5.3)	1 (14.3)
Only	Cuora amboinensis kamarona	3 (15.8)	2 (28.6)
Mix	C. a. kamarona, C. mouhotii obsti	2 (10.5)	1 (14.3)
Mix	C. amboinensis, Terrapene carolina triunguis, Cuora flavomarginata and Terrapene carolina major	1 (5.3)	0
Only	Graptemys koni	1 (5.3)	0
Mix	G. koni, Chrysemys picta belli and C. p. marginata	1 (5.3)	0
Mix	Kinosternon baurii and K. subrurum	1 (5.3)	1 (14.3)
Only	Kinosternon carinatum	1 (5.3)	0
Only	M. Temminckii	1 (5.3)	0
Only	P. concinna	1 (5.3)	0
Only	P. Rubriventris	1 (5.3)	1 (14.3)
Only	T. s. Scripta	1 (5.3)	1 (14.3)
	Total	19 (15.8)	7 (36.9)

The location of sample collection was significantly associated with Salmonella carriage, with frequency of carriage higher for samples from pet stores (75.0% ± 8.8% vs. 29.0% ± 4.6%, for pet stores versus private owners' samples, respectively, p < 0.001). When we compared private owners' indoor and outdoor enclosure, no significant differences were observed (37.0 ± 11.1% vs. 27.0% ± 5.1%, for outdoor vs. indoor samples, respectively, p < 0.001).

Of the 46 Salmonella isolates, 43 could be identified as 18 serotypes. Salmonella enterica subspecies represented 95.3% (41/43) of all isolates (Table 3). Most frequently isolated serotypes were Salmonella Typhimurium (39.5%, 17/43) and Salmonella Pomona (9.3%, 4/43). Among the 12 serotypes isolated from pet stores, three were also isolated from private owners: Salmonella Pomona, Salmonella Urbana, and Salmonella Thompson.

Table 3.

Salmonella Serotypes Isolated from Private Owners and Pet Store Turtles

Sample origin	n	Subspecies	Serovar
Pet store	3	enterica	Pomona 28: y: 1, 7
	1	enterica	Rubislaw 11: r: e,n,x
	1	diarizonae	50: z52: z35
	2	enterica	Paratyphi B 4, 12:b 1, 2
	1	enterica	Thompson 6, 7: k: 1, 5
	2	enterica	Sandiego 4, 12: e,h: e,n,z15
	2	enterica	Braenderup 6, 7: e,h: e,n,z15
	1	enterica	Poona 13, 22: z: 1, 6
	1	enterica	Urbana 30: b: e,n,x
	1	enterica	Bareilly 6, 7: y: 1, 5
	1	enterica	Hvittingfoss 16: b: e,n,x
	1	enterica	Montevideo 6, 7: g,m,s: —
Private owner
Indoor	17	enterica	Typhimurium 4, 12: i: 1, 2
	1	diarizonae	61: c: 1, 5, 7
	1	enterica	Pomona 28: y: 1, 7
	1	enterica	Saint paul 4, 12: e,h. 1, 2
	2	enterica	Thompson 6, 7: k: 1, 5
	1	enterica	Kintambo 1, 13, 23: m,t:—
Outdoor	1	enterica	Stanley 4, 12: d: 1, 2
	1	enterica	Urbana 30: b: e,n,x
	1	enterica	Agoueve 13, 22: z29: —

n, number of strains isolated.

Discussion

The present study clearly demonstrates that turtles in pet stores, as well as in private owners, could be a direct or indirect source of human Salmonella infections. The percentage of isolation of Salmonella was high from pet store samples (75%) and lower for private owners (29%), consistent with those of other countries such as Japan (Nakadai et al. 2005). This finding was not unexpected if we take into account that reptiles and amphibians have long been known to harbor Salmonella (Caldwell and Ryerson 1939) and to cause human infection (Door 1958). Effectively, Mermim et al. (2004) estimated that 74,000 Salmonella infections, during the 1996–1997, in the United States were associated with reptile or amphibian contact. Consistent with this, recent studies clearly demonstrates the association of reptile-associated salmonellosis with hospitalization and invasive disease at young age (Meyer Sauteur et al. 2013, Murphy and Oshin 2015, Walters et al. 2016), in particular infants <6 months of age (Meyer Sauteur et al. 2013). Because turtles are slow moving and are perceived to be gentle pets, they are more likely than other reptiles to be given to infants or young children (de Jong et al. 2015), who in turn handle small turtles more closely than they might handle other reptiles, including kissing the turtles or putting them in their mouths (de Jong et al. 2015). In addition, turtle terrariums frequently contain a reservoir of water that serves as a site of amplification of Salmonella bacteria (D'Aoust et al. 1990); children might play with a turtle in the terrarium and splash the contaminated water, increasing their risk of infection. The difficulty in enforcing children's good hygiene practices, including adequate handwashing immediately after contact with a reptile, compounds this problem (Harris et al. 2010).

In the present study, a higher proportion of positive samples were present in pet stores compared with private owners. A plausible explanation for the difference could be the fact that turtles from private owners are less or not even exposed to stress factors that increase shedding rates. Intermittent shedding of Salmonella in reptiles and the wide array of collection and sampling techniques have been proposed to be the main reasons for the variability in detection rates (Scheelings et al. 2011). We hereby used a protocol evaluated 2 years ago in our laboratory, with higher detection rates compared with cloacal swabs (Marin et al. 2013). In the cloaca of turtles, the presence of Salmonella is lower than in the intestinal content (Marin et al. 2013). Salmonella shedding from the gastrointestinal tract is facilitated by stress due to transport, overcrowding at pet stores, or incorrect and inadequate housing (Smith et al. 2012). It is possible that the high number of young pet turtles (>30 of about 2 months age) housing at the same aquarium resulted in a stress situation, resulting in more Salmonella excretion. It is known that the risk of transmission is increased in young reptiles kept indoors, living, that is, in breeding farms, and transported from farms to stores, where a high diversity and number of animals are kept in close contact (Mitchell and Shane 2000). Moreover, the primary transmission route for pathogens is through fecal–oral ingestion (Lamm et al. 1972) and perhaps, turtle-to-turtle transmission within aquarium will be extremely rapid, and the majority of turtles in a positive aquarium will be colonized within only a few days. More research is required to corroborate such hypotheses.

In the present study, two subspecies of S. enterica belonging to 18 different serotypes were isolated (S. enterica enterica [I] and S. enterica diarizonae [III]). The proportion of subspecies I serotypes was the highest (95.3%) and belonged to those most frequently seen in humans in the European Union, where Salmonella Enteritidis, Salmonella Typhimurium monophasic, Salmonella Typhimurium, Salmonella Infantis, and Salmonella Stanley were the top five serotypes associated with human illness in 2012 (Hugas and Beloeil 2014). In addition to the S. e. enterica subspecies, S. e. diarizonae has also been described as causative agents in human infections associated with direct or indirect contact with pet reptiles (Editorial team et al. 2008). The serotypes most frequently identified were Salmonella Typhimurium, Salmonella Pomona, Salmonella Thompson, and Salmonella Urbana isolated in both pet stores and privately owned turtles. All of these serotypes have previously been reported in turtles and child Salmonella infections associate with pet turtle exposure (Dessì et al. 1992, Xu et al. 2002, Brédart et al. 2007, Editorial team et al. 2008, Li et al. 2009, Kocianova et al. 2010, Centers for Disease Control and Prevention 2013, Walters et al. 2016), an exception of Salmonella Thompson that has been identified in turtles, but not directly related with infant infection (Marin et al. 2013). Centers for Disease Control and Prevention (2010) reported a multistate outbreak of human Salmonella Typhimurium infections associated with pet turtle exposure. Previously, Dessì et al. (1992) disclosed human salmonellosis transmitted by a domestic turtle. In addition, turtles and other reptiles are the major reservoirs of Salmonella Pomona, and most of human Salmonella Pomona infections were associated with turtles and other reptiles (Bertrand et al. 2008, Centers for Disease Control and Prevention 2013). Specifically, a case of a 4-month-old girl who suffered of septicemia due to Salmonella Pomona was described in 2007 (Editorial team et al. 2008). The source of infection was established to be the family's pet turtle (Brédart et al. 2007). In China, Salmonella Pomona was isolated from the feces of an infant in Shanghai in 2000 (Xu et al. 2002), and two further cases of Salmonella Pomona infection in humans were found in Guangzhou later (Li et al. 2009). Finally, Salmonella Urbana infection in a 2-year-old child was caused by pet water turtles (Kocianova et al. 2010).

In conclusion, we had found a high and moderate frequency of Salmonella positives in both pet store and private owners, respectively. In our study, serotypes most frequently identified (Salmonella Typhimurium, Salmonella Pomona, and Salmonella Urbana) have previously been reported in children. Salmonella infections associate with pet turtle exposure. More than half-century after the first reports of turtle-associated Salmonella in humans and the continued occurrence of turtle-associated salmonellosis indicate that existing prevention efforts need to be enhanced to protect the public health. Families with young children should be aware of the health risks associated with having a turtle as a family pet. In addition, pet stores should advise their customers of the potential risks associated with reptile ownership. The effectiveness of any potential intervention requires monitoring of the Salmonella status at breeding farms and transport from farms to stores to determine the source of infection.

Footnotes

Acknowledgments

This work was supported by the Conselleria de Infraestructuras, Territorio y Medio Ambiente with their assistance and financial support (Life09-Trachemys, Resolution 28/02/12 CITMA). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the article. The authors thank the technical support of Cristóbal Torres, Xema Gil, and all the members of the research group “Improvement of the Food Safety related with the Production System and Final Products” (Veterinary Faculty, University CEU-Cardenal Herrera).

Author Disclosure Statement

No competing financial interests exist.

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