Importance of Wild Species Kept in Captivity as Reservoirs of Salmonella Serotypes for Human in Petting Exhibitions and Zoo in Iran with Focus on Antimicrobial Resistance

Open access


Salmonella spp. is the leading cause of zoonotic enteric diseases wich represents a public health concern worldwide. The incidence of zoo-associated salmonellosis is rather high due to the high prevalence and shedding of this bacterium from wild animals specially kept in stressful conditions. To determine the potential public health risk presented by zoo animals in Semnan, we investigated the prevalence of Salmonella serovars Enteritidis and Typhimurium among wild animal species kept in the zoo and pet shops. Totally, 152 fecal samples from species in the zoo and pet shops were collected and Salmonella prevalence and identification was assessed via standard bacteriologic culture methods, serotyping, multiplex-PCR and antimicrobial susceptibility testing. Overall, 21% (32/152) of the samples were confirmed positive for Salmonella and serotyping showed 12.5% (19/32) Salmonella serovar Enteritidis and 8.5% (13/32) serovar Typhimurium, respectively. All the Salmonella isolates were sensitive to Chloramphenicole, Flurefenicole, Meropenem, Ceftizoxime, Imipenem and Ampicillin, while resistance was observed in the case of Nalidixic acid (78%) as the highest resistance, Streptomycin (28%), Oxytetracycline, Neomycin, Furazolidone (each one 15%) and Lincospectin (9.3%). The high occurrence of multidrug resistance Salmonella in zoo and pet animals represents a potential threat to public health and requires strict surveillance and application of hygienic criteria.

If the inline PDF is not rendering correctly, you can download the PDF file here.

  • 1. Pan Z. M. Geng S. Z. Zhou Y. Q. Liu Z. Y. Fang Q. Liu B. B. Jiao X. A. (2010). Prevalence and antimicrobial resistance of Salmonella spp. isolated from domestic animals in Eastern China. J Anim Vet Adv. 9 (17): 2290-2294.

  • 2. Herrera-León S. Ramiro R. Arroyo M. Díez R. Usera M. A. Echeita M. A. (2007). Blind comparison of traditional serotyping with three multiplex PCRs for the identification of Salmonella serotypes. Res Microbil. 158 (2): 122-127. PMid:17258433

  • 3. Mirzaie S. Hassanzadeh M. Ashrafi I. (2010). Identification and characterization of Salmonella isolates from captured house sparrows. Turk J Vet Anim Sci. 34 (2): 181-186.

  • 4. Centers for Disease Control and Prevention (CDC): Salmonella: Salmonella infection.

  • 5. Dallal M. M. S. (2014). Prevalence of Salmonella spp. in packed and unpacked red meat and chicken in south of Tehran. Jundishapur J Microbiol. 7 (4): e9254. PMCID: PMC4138620

  • 6. Staji H. Tonelli A. Zahraei Salehi T. Iorio M. Lopes F. (2015). Genetic Characterization of Salmonella Typhimurium isolates from faeces of children with gastroenteritis hospitalized in Baqiatollah-Azam Hospital Tehran Iran. J Med Microbiol Infect Dis. 3(1): 32-39.

  • 7. Staji H. Rezaei S. Rassouli M. Namroodi S. (2016). Prevalence and genetic characteristics of Salmonella strains in wild mallard ducks (Anas plathyrhincus) in Semnan suburb Iran. Bulg J Vet Med. Online First:

  • 8. Krawiec M. Kuczkowski M. Kruszewicz A. G. Wieliczko A. (2015). Prevalence and genetic characteristics of Salmonella in free-living birds in Poland. BMC Vet Res. 11 (1): 2-8. PMid:25636375 PMCid:PMC4316766

  • 9. Jamshidi A. Kalidari G. A. Hedayati M. (2010). Isolation and identification of Salmonella Enteritidis and Salmonella Typhimurium from the eggs of retail stores in Mashhad Iran using conventional culture method and multiplex PCR assay. J Food Safety. 30 (3): 558-568.

  • 10. Fudge A. M. (2001). Diagnosis and treatment of avian bacterial disease. Semin Avi Exot Pet Med. 10(1): 3-11.

  • 11. Tizard I. (2004). Salmonellosis in wild birds. Semin Avi Exot Pet Med. 13(2): 50-66.

  • 12. Peighambari S.M. Yazdani A. Hojjati P. (2011). Salmonella infection in birds kept in parks and pet shops in Tehran Iran. Iran J Vet Med. 5(3): 145-148.

  • 13. Chomel B.B. Belotto A. Meslin F. X. (2007). Wildlife exotic pets and emerging zoonoses. Emerg Infect Dis. 13 (1): 6. PMid:17370509 PMCid:PMC2725831

  • 14. Koochakzadeh A. Zahraei Salehi T. Nayeri Fasaei B. Askari Badouei M. Oskouizadeh K. (2015). Detection of Salmonella spp. from some wild captive herbivores in Iran and determination of serogroup antibiotic susceptibility and presence of invA gene in the isolated strains. Arch Razi Institute 70 (2): 81-87.

  • 15. Sharifi-Rad J. Van Belkum A. Fallah F. et al. (2016). Rising antimicrobial resistance in Iran. Der Pharm Lett. 8 (7): 31-33.

  • 16. Osmundson T.W. Eyre C.A. Hayden K.M. Dhillon J. Garbelotto M.M. (2013). Back to basics: an evaluation of NaOH and alternative rapid DNA extraction protocols for DNA barcoding genotyping and disease diagnostics from fungal and oomycete samples. Mol Ecol Resources. 13 (1): 66-74. PMid:23121735

  • 17. Zahraei Salehi T. Tadjbakhsh H. Atashparvar N. Nadalian M. Mahzounieh M. (2007). Detection and identification of Salmonella Typhimurium in bovine diarrhoeic fecal samples by immunomagnetic separation and multiplex PCR assay. Zoonoses Pub Health. 54 (6-7): 231-236. PMid:17803511

  • 18. Pan T.M. Liu Y.J. (2002). Identification of Salmonella enteritidis isolates by polymerase chain reaction and multiplex polymerase chain reaction. J Microbiol Immunol Infect. 35 147-151. PMid:12380786

  • 19. Patel J. Cockerill III. F. Alder J. Bradford P. Eliopoulos G. Hardy D. et al. (2014). Performance standards for antimicrobial susceptibility testing; twenty-fourth informational supplement. CLSI standards for antimicrobial susceptibility testing 34(1): 1-226.

  • 20. Marchant P. Hidalgo-Hermoso E. Espinoza K. Retamal P. (2016). Prevalence of Salmonella enterica and Shiga toxin-producing Escherichia coli in zoo animals from Chile. J Vet Sci. 17 (4): 583-586. PMid:27030195 PMCid:PMC5204038

  • 21. Namroodi S. Staji H. Mazandarani E. (2016). Epidemiological Survey of Salmonella in Rural Cats: A Survey of Serotype Presence of spv R and spv B Genes and Antibiotic Resistance Pattern. Iran J Epidemiol. 12 (3): 47-55.

  • 22. Clancy M.M. Davis M. Valitutto M.T. Nelson K. Sykes I.V.J.M. (2016). Salmonella infection and carriage in reptiles in a zoological collection. J Am Vet Med Assoc. 248 (9): 1050-1059. PMid:27074614

  • 23. Grigar M.K. Cummings K.J. Rodriguez-Rivera L.D. Rankin S.C. Johns K. Hamer G.L. et al. (2016). Salmonella surveillance among great-tailed grackles (Quiscalus mexicanus) and other urban bird species in Eastern Texas. Vector-Borne Zoonotic Dis. 16 (12): 752-757. PMid: 27827557

  • 24. Jang Y. Lee S. Lim J. Lee H. Kim T. Park J. et al. (2008). The rate of Salmonella spp. infection in zoo animals at Seoul Grand Park Korea. J Vet Sci. 9 (2): 177-181. PMid:18487939 PMCid:PMC2839095

  • 25. Friedman C.R. Torigian C. Shillam P.J. Hoffman R.E. Heltze D. Beebe J.L. et al. (1998). An outbreak of salmonellosis among children attending a reptile exhibit at a zoo. J Pediat. 132 (5): 802-807.

  • 26. Bender J.B. Shulman S.A. (2004). Reports of zoonotic disease outbreaks associated with animal exhibits and availability of recommendations for preventing zoonotic disease transmission from animals to people in such settings. J Am Vet Med Assoc. 224 (7): 1105-1109. PMid:15074855

  • 27. Conrad C.C. Stanford K. Narvaez-Bravo C. Callaway T. McAllister T. (2017). Farm fairs and petting zoos: A review of animal contact as a source of zoonotic enteric disease. Foodborne Pathog Dis. 14 (2): 59-73. PMid:27992253

  • 28. Uzzau S. Brown D.J. Wallis T. Rubino S. Leori G. Bernard S. et al. (2000). Host adapted serotypes of Salmonella enterica. Epidemiol Infect. 125 (2): 229-255. PMid:11117946 PMCid:PMC2869595

  • 29. Hernandez S.M. Keel K. Sanchez S. Trees E. Gerner-Smidt P. Adams J.K. et al. (2012). The epidemiology of Salmonella enterica spp. enterica serovar Typhimurium strain associated with a songbird outbreak. Appl Environ Microbiol. 78(20): 7290-7298. PMid: 22885752 PMCid: PMC3457103

  • 30. Crim S.M. Griffin P.M. Tauxe R. Marder E.P. Gilliss D. Cronquist A.B. et al. (2015). Preliminary incidence and trends of infection with pathogens transmitted commonly through food. Foodborne Diseases Active Surveillance Network 10 US sites 2006–2014. MMWR Morb Mortal Wkly Rep. 64(18) 495-499. PMid:25974634

  • 31. Hall A.J. Saito E.K. (2008). Avian wildlife mortality events due to salmonellosis in the United States 1985–2004. J Wildlife Dis. 44 (3): 585-593. PMid:18689643

  • 32. Madadgar O. Salehi T.Z. Ghafari M.M. Tamai I.A. Madani S.A. Yahyareyat R. (2009). Study of an unusual paratyphoid epornitic in canaries (Serinus canaria). Avian Pathology. 38 (6): 437-441. PMid:19937532

  • 33. Tadesse D.A. Singh A. Zhao S. Bartholomew M. Womack N. Ayers S. et al. (2016). Antimicrobial resistance in Salmonella in the United States from 1948 to 1995. Antimicrob Agent Chemo. 60 (4): 2567-2571. PMid:26856840 PMCid:PMC4808194

  • 34. Voss-Rech D. Potter L. Vaz C.S.L. Pereira D.I.B. Sangioni L.A. Vargas A.C. et al. (2017). Antimicrobial resistance in nontyphoidal Salmonella isolated from human and poultry-related samples in Brazil: 20-Year meta-analysis. Foodborne Pathog Dis. 14 (2): 116-124. PMid:27922763

  • 35. Alley M. Connolly J. Fenwick S. Mackereth G. Leyland M. Rogers L. et al. (2002). An epidemic of salmonellosis caused by Salmonella Typhimurium DT160 in wild birds and humans in New Zealand. New Zealand Vet J. 50 (5): 170-176. PMid:16032266

  • 36. Handeland K. Refsum T. Johansen B. Holstad G. Knutsen G. Solberg I. et al. (2002). Prevalence of Salmonella Typhimurium infection in Norwegian hedgehog populations associated with two human disease outbreaks. Epidemiol Infect. 128 (3): 523-527. PMid:12113498 PMCid:PMC2869850

  • 37. Pires S.M. Vieira A.R. Hald T. Cole D. (2014). Source attribution of human salmonellosis: an overview of methods and estimates. Foodborne Pathog Dis. 11 (9): 667-676. PMid:24885917

  • 38. Dolejska M. Villa L. Hasman H. Hansen L. Carattoli A. (2013). Characterization of IncN plasmids carrying blaCTX-M-1 and qnr genes in Escherichia coli and Salmonella from animals the environment and humans. J Antimicrob Chemo. 68 (2): 333-339. PMid:23060365

  • 39. Mughini-Gras L. Barrucci F. Smid J. Graziani C. Luzzi I. Ricci A. et al. (2014). Attribution of human Salmonella infections to animal and food sources in Italy (2002–2010): adaptations of the Dutch and modified Hald source attribution models. Epidemiol Infect. 142 (5): 1070-1082. PMid:23920400

  • 40. Dunn J.R. Behravesh C.B. Angulo F.J. (2015). Diseases transmitted by domestic livestock: perils of the petting zoo. Microbiology Spectrum 3(6): 227-234. PMid:27337283

  • 41. Pickering L.K. Marano N. Bocchini J.A. Angulo F.J. (2008). Exposure to nontraditional pets at home and to animals in public settings: risks to children. Pediatrics 122 (4): 876-886. PMid:18829816

  • 42. Erdozain G. KuKanich K. Chapman B. Powell D. (2013). Observation of public health risk behaviours risk communication and hand hygiene at Kansas and Missouri petting zoos–2010–2011. Zoonoses Pub Health. 60 (4): 304-310. PMid:22846186

Journal information
Impact Factor

CiteScore 2018: 0.45

SCImago Journal Rank (SJR) 2018: 0.193
Source Normalized Impact per Paper (SNIP) 2018: 0.328

All Time Past Year Past 30 Days
Abstract Views 0 0 0
Full Text Views 156 73 4
PDF Downloads 86 46 3