Abstract
The breeding of exotic pets has become a popular practice in Chile and, within this group of animals, small mammals such as guinea pigs and hedgehogs have gained importance due to their docile behaviour. The most common exotic hedgehog species in Chile is the African pygmy hedgehog (Atelerix albiventris). It has been reported that these pets are reservoirs of some zoonotic pathogens, among which Salmonella enterica constitutes an important threat for the owners. This study aimed to detect the presence of Salmonella strains in faeces from hedgehogs (Atelerix albiventris) admitted to a veterinary clinic in Santiago, Chile, and to characterise the antimicrobial susceptibility of the isolated strains. From 200 animals sampled, S. enterica was detected in 5 hedgehogs, corresponding to serotypes Muenchen (2), Infantis (2) and IV43:z4,z23:- (1). Furthermore, phenotypic antimicrobial resistance was determined in all subsp. enterica isolates. These results suggest that in Chile these exotic pets constitute a potential hazard for public health, therefore, supporting educational campaigns about basic biosecurity measures is necessary, mostly aimed at pet owners and risk groups.
Downloads
References
- Alcaine S, Sukhnanand S, Warnick L, Su W, McGann P, et al. 2005. Ceftiofur-resistant Salmonella strains isolated from dairy farms represent multiple widely distributed subtypes that evolved by independent horizontal gene transfer. Antimicrob Agents Chemother 49, 4061-4067.
- Anderson TC, Marsden-Haug N, Morris JF, Culpepper W, Bessette N, et al. 2017. Multistate outbreak of human Salmonella typhimurium infections linked to pet hedgehogs - United States, 2011-2013. Zoonoses Public Health 64, 290-298.
- Aviv G, Cornelius A, Davidovich M, Cohen H, Suwand A, et al. 2019. The emerging Salmonella Infantis expresses lower levels of SPI-1 genes and causes milder colitis in mice and lower rates of invasive disease in humans than Salmonella typhimurium. J Infect Dis 220, 1071-1081.
- Bonardi S, Alpigiani I, Bruini I, Barilli E, Brindani F, et al. 2016. Detection of Salmonella enterica in pigs at slaughter and comparison with human isolates in Italy. Int J Food Microbiol 218, 44-50.
- Boore AL, Hoekstra RM, Iwamoto M, Fields PI, Bishop RD, et al. 2015. Salmonella enterica infections in the United States and assessment of coefficients of variation: A novel approach to identify epidemiologic characteristics of individual serotypes, 1996-2011. PLoS One 10, e0145416.
- Braun S, Spalloni W, Ferreccio F, Postigo J, Fernández A, et al. 2015. Salmonella spp. gastroenteritis associated to pet turtles in three infants. Rev Chil Infectol 32, 334-338.
- Chomel BB, Belotto A, Meslin FX. 2007. Wildlife, exotic pets, and emerging zoonoses. Emerg Infect Dis 13, 6-11.
- Craig C, Styliadis S, Woodward D, Werker D. 1997. African pygmy hedgehog-associated Salmonella tilene in Canada. Can Commun Dis Rep 23, 129-131; discussion 131-122.
- Draper ADK, James CL, Pascall JE, Shield KJ, Langrell J, et al. 2017. An outbreak of Salmonella Muenchen after consuming sea turtle, Northern Territory, Australia, 2017. Commun Dis Intell Q Rep 41, e290-e294.
- Ferrari RG, Rosario DKA, Cunha-Neto A, Mano SB, Figueiredo EES, et al. 2019. Worldwide epidemiology of Salmonella serovars in animal-based foods: a meta-analysis. Appl Environ Microbiol 85, e00591- e00519.
- Fredes F, Román D. 2004. Fauna parasitaria en erizos de tierra africanos (Atelerix albiventris). Parasitol latinoam 59, 79-81.
- Fresno M, Barrera V, Gornall V, Lillo P, Paredes N, et al. 2013. Identification of diverse Salmonella serotypes, virulotypes, and antimicrobial resistance phenotypes in waterfowl from Chile. Vector Borne Zoonotic Dis 13, 884-887.
- Gordon MA. 2008. Salmonella infections in immunocompromised adults. J Infect 56, 413-422.
- Handeland K, Refsum T, Johansen BS, Holstad G, Knutsen G, et al. 2002. Prevalence of Salmonella typhimurium infection in Norwegian hedgehog populations associated with two human disease outbreaks. Epidemiol Infect 128, 523-527.
- Hoelzer K, Moreno Switt AI, Wiedmann M. 2011. Animal contact as a source of human non-typhoidal salmonellosis. Vet Res 42, 34.
- Ichimi R, Yoshino A, Higashigawa M. 2018. Salmonella stanley bacteremia transmitted from a pet hedgehog. Pediatr Int 60, 606-607.
- Jackson BR, Griffin PM, Cole D, Walsh KA, Chai SJ. 2013. Outbreakassociated Salmonella enterica serotypes and food Commodities, United States, 1998-2008. Emerg Infect Dis 19, 1239-1244.
- Jensen AN, Sørensen G, Baggesen DL, Bødker R, Hoorfar J. 2003. Addition of Novobiocin in pre-enrichment step can improve Salmonella culture protocol of modified semisolid Rappaport-Vassiliadis. J Microbiol Methods 55, 249-55.
- Kagambega A, Lienemann T, Aulu L, Traore AS, Barro N, et al. 2013. Prevalence and characterization of Salmonella enterica from the feces of cattle, poultry, swine and hedgehogs in Burkina Faso and their comparison to human Salmonella isolates. BMC Microbiol 13, 253.
- Keeble E, Koterwas B. 2020. Salmonellosis in Hedgehogs. Vet Clin North Am Exot Anim Pract 23, 459-470.
- Lamas A, Miranda JM, Regal P, Vázquez B, Franco CM, et al. 2018. A comprehensive review of non-enterica subspecies of Salmonella enterica. Microbiol Res 206, 60-73.
- Lawson B, Franklinos LHV, Rodriguez-Ramos Fernandez J, Wend-Hansen C, Nair S, et al. 2018. Salmonella enteritidis ST183: emerging and endemic biotypes affecting western European hedgehogs (Erinaceus europaeus) and people in Great Britain. Sci Rep 8, 2449.
- MacDonald E, White R, Mexia R, Bruun T, Kapperud G, et al. 2019. The role of domestic reservoirs in domestically acquired Salmonella infections in Norway: epidemiology of salmonellosis, 2000-2015, and results of a national prospective case-control study, 2010-2012. Epidemiol Infect 147, e43.
- Malorny B, Hoorfar J, Bunge C, Helmuth R. 2003. Multicenter validation of the analytical accuracy of Salmonella PCR: towards an international standard. Appl Environ Microbiol 69, 290-296.
- Marus JR, Magee MJ, Manikonda K, Nichols MC. 2019. Outbreaks of Salmonella enterica infections linked to animal contact: Demographic and outbreak characteristics and comparison to foodborne outbreaks-United States, 2009-2014. Zoonoses Public Health 66, 370-376.
- Millanao A, Barrientos-Schaffeld C, Siegel-Tike C, Tomova A, Ivanova L, et al. 2018. Antimicrobial resistance in Chile and the one health paradigm: Dealing with threats to human and veterinary health resulting from antimicrobial use in salmon aquaculture and the clinic. Rev Chil Infectol 35, 299-308.
- Morse SS, Mazet JA, Woolhouse M, Parrish CR, Carroll D, et al. 2012. Prediction and prevention of the next pandemic zoonosis. Lancet 380, 1956-1965.
- Okada K, Kondo H, Sumi A, Kagawa Y. 2018. A retrospective study of disease incidence in African pygmy hedgehogs (Atelerix albiventris). J Vet Med Sci 80, 1504-1510.
- Olea A, Díaz J, Fuentes R, Vaquero A, García M. 2012. Vigilancia de brotes de enfermedades transmitidas por alimentos en Chile. Rev Chil Infectol 29, 504-510.
- Pignon C, Mayer J. 2011. Zoonoses of ferrets, hedgehogs, and sugar gliders. Vet Clin North Am Exot Anim Pract 14, 533-549. Riley PY, Chomel BB. 2005. Hedgehog zoonoses. Emerg Infect Dis 11, 1-5.
- Santana EM, Jantz HE, Best TL. 2010. Atelerix albiventris (Erinaceomorpha: Erinaceidae). Mamm Species 42, 99-110.
- Schielke A, Rabsch W, Prager R, Simon S, Fruth A, et al. 2017. Two consecutive large outbreaks of Salmonella Muenchen linked to pig farming in Germany, 2013 to 2014: Is something missing in our regulatory framework? Euro Surveill 22, 30528.
- Smith KF, Goldberg M, Rosenthal S, Carlson L, Chen J, et al. 2014. Global rise in human infectious disease outbreaks. J R Soc Interface 11, 20140950.
- Yang W, Chan O, Wu T, Chen C, Su L, et al. 2016. Development of ceftriaxone resistance in Salmonella enterica serotype Oranienburg during therapy for bacteremia. J Microbiol Immunol Infect 49, 41-45.
- Younus M, Wilkins MJ, Davies HD, Rahbar MH, Funk J, et al. 2010. The role of exposures to animals and other risk factors in sporadic, non-typhoidal Salmonella infections in Michigan children. Zoonoses Public Health 57, e170-e176.
- WHO. 2019. Critically important antimicrobials for human medicine. WHO, Geneva, Switzerland.
- Zare P, Ghorbani-Choboghlo H. 2015. Isolation and characterization of multidrug-resistant gram-negative bacteria found in free-ranging long-eared hedgehogs (Erinaceus concolor) from Tabriz, Iran. J Exot Pet Med 24, 235-239.




