ORIGINAL_ARTICLE 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. https://macvetrev.mk/Files/Article/2019/10.1515/macvetrev-2017-0025/macvetrev-2017-0025.pdf 2017-10-15T09:00:00 167 175 10.2478/macvetrev-2017-0025 Salmonella wild species in captivity serotyping multiplex-PCR antimicrobial resistance false 1 LEAD_AUTHOR Hamid Staji hstaji@semnan.ac.ir false 2 Department of Pathobiology, Faculty of Veterinary Medicine, Semnan University, Semnan, Iran AUTHOR Ladan Zandiar false 3 Veterinary Medicine Laboratory Student, Semnan University, Semnan, Iran AUTHOR 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. 1 10.3923/javaa.2010.2290.2294 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 2 10.1016/j.resmic.2006.09.009 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. 3 Centers for Disease Control and Prevention (CDC):Salmonella:Salmonella infection. https://www.cdc.gov/salmonella/index.html 4 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 5 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. 6 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: http://tru.uni-sz.bg/bjvm/H.%20Staji%20OnFirst.pdf 7 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 8 10.1186/s12917-015-0332-x 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. 9 Fudge, A. M. (2001). Diagnosis and treatment of avian bacterial disease. Semin Avi Exot Pet Med. 10(1):3-11. 10 10.1053/saep.2001.19542 Tizard, I. (2004). Salmonellosis in wild birds. Semin Avi Exot Pet Med. 13(2):50-66. 11 10.1053/j.saep.2004.01.008 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. 12 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 13 10.3201/eid1301.060480 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. 14 Sharifi-Rad, J., Van Belkum, A., Fallah, F., et al. (2016). Rising antimicrobial resistance in Iran. Der Pharm Lett. 8 (7):31-33. 15 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 16 10.1111/1755-0998.12031 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 17 10.1111/j.1863-2378.2007.01061.x 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 18 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. 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 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. 21 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 22 10.2460/javma.248.9.1050 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 23 10.1089/vbz.2016.2000 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 24 10.4142/jvs.2008.9.2.177 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. 25 10.1016/S0022-3476(98)70307-5 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 26 10.2460/javma.2004.224.1105 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 27 10.1089/fpd.2016.2185 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 28 10.1017/S0950268899004379 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 29 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 30 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 31 10.7589/0090-3558-44.3.585 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 32 10.1080/03079450903349170 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 33 10.1128/AAC.02536-15 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 34 10.1089/fpd.2016.2228 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 35 10.1080/00480169.2002.36306 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 36 10.1017/S0950268802007021 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 37 10.1089/fpd.2014.1744 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 38 10.1093/jac/dks387 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 39 10.1017/S0950268813001829 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 40 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 41 10.1542/peds.2008-1942 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 42 10.1111/j.1863-2378.2012.01531.x