Clonal relatedness and antimicrobial susceptibility of Salmonella serovars isolated from humans and domestic animals in Iran: a one health perspective

Document Type : Full paper (Original article)


1 Department of Pathobiology, Faculty of Veterinary Medicine, Garmsar Branch, Islamic Azad University, Garmsar, Iran

2 Ph.D. Student in Bacteriology, Department of Pathobiology, Faculty of Veterinary Medicine, Ferdowsi University of Mashhad, Mashhad, Iran

3 Department of Pathobiology, Faculty of Veterinary Medicine, Ferdowsi University of Mashhad, Mashhad, Iran

4 Department of Microbiology and Immunology, Faculty of Veterinary Medicine, University of Tehran, Tehran, Iran


Background: Salmonellosis is one of the most important zoonotic diseases in humans and animals worldwide. Aims: The main objective of this study was to report serovars, clonal relatedness, and antimicrobial resistance of Salmonella strains isolated from human, different animal hosts including pigeons, broilers, cattle, camel, parrots, and hamsters in different regions of Iran. Methods: Twenty-four Salmonella isolates were confirmed at the genus level by biochemical tests and polymerase chain reaction (PCR) by showing the presence of invA gene. Serovars were determined and their clonal relatedness was assessed by RAPD-PCR and antibiotic resistance profiles. Results: Overall, Salmonella Typhimurium was the most prevalent serovar (45.8%, 11/24), which was recovered from humans, pigeons, and camels. Salmonella Enteritidis (29.2%, 7/24) was the second common serovar that was recovered from cattle, broilers, humans, and hamsters. Salmonella Infantis (12.5%, 3/24) belonged only to broiler sources, and Salmonella Seftenberg (12.5%, 3/24) was isolated from eggs and a parrot. The major RAPD pattern was VI (33.3%) in which the two S. Typhimurium isolates (belonged to humans and pigeons) exhibited similarity in both RAPD pattern and resistance profile. Antimicrobial susceptibility test showed full resistance to tylosin and erythromycin (100%, 24/24). All isolates (100%, 24/24) were susceptible to ceftriaxone, cefixime, and gentamicin. In total, 75% of the isolates were multi-drug resistant (MDR) and revealed 15 different antimicrobial resistance profiles (R-type). Conclusion: This study supports the potential transmission of Salmonella serovars via animal contacts. Thus, it is necessary to establish a national systematic monitoring program with one health approach for controlling Salmonella infections.


Main Subjects

Asadpour, Y; Mohammadi, M; Pourbakhsh, SA and Rasa, M (2014). Isolation, serotyping and antibiotic resistance of Salmonella strains isolated from chicken carcasses in Guilan province. Iran. Vet. J., 9: 5-13.
Askari Badouei, M; Vaezi, H; Nemati, A; Ghorbanyoon, E; Firoozeh, F; Jajarmi, M and Peighambari, SM (2021). High prevalence of clonally related multiple resistant Salmonella Infantis carrying class 1 integrons in broiler farms. Vet. Ital., 57: 181-188. doi: 10.12834/VetIt.2269. 13773.1.
Besharati, S; Sadeghi, A; Ahmadi, F; Tajeddin, E; Mohammad Salehi, R; Fani, F; Pouladfar, G; Nikmanesh, B; Majidpour, A; Soleymanzadeh Moghadam, S and Mirab Samiee, S (2020). Serogroups, and drug resistance of nontyphoidal Salmonella in symptomatic patients with community-acquired diarrhea and chicken meat samples in Tehran. Iran. J. Vet. Res., 21: 269-278.
Cao, ZZ; Xu, JW; Gao, M; Li, XS; Zhai, YJ; Yu, K; Wan, M and Luan, XH (2020). Prevalence and antimicrobial resistance of Salmonella isolates from goose farms in Northeast China. Iran. J. Vet. Res., 21: 287-293.
Carramiñana, JJ; Rota, C; Agustin, I and Herrera, A (2004). High prevalence of multiple resistance to antibiotics in Salmonella serovars isolated from a poultry slaughterhouse in Spain. Vet. Microbiol., 104: 133-139.
Dallal, MM; Ehrampoush, MH; Aminharati, F; Tafti, AA; Yaseri, M and Memariani, M (2020). Associations between climatic parameters and the human salmonellosis in Yazd province, Iran. Environ. Res., 187: 109706.
Emadi, CS; Hasanzadeh, M; Bozorg, MM and Mirzaei, S (2009). Characterization of the Salmonella isolates from backyard chickens in north of Iran, by serotyping, multiplex PCR and antibiotic resistance analysis. Arch. Razi Inst., 64: 77-83.
Ezatpanah, E; Moradi Bidhendi, S; Khaki, P; Ghaderi, R; Seydan Jasebi, E and Meghtedaeifar, S (2013). Detection, determination of serovars and antibiotic resistance patterns of Salmonenlla strains isolated from
Arak city poultry. Iran. Vet. J., 9: 88-96.
Fadl, AA; Nguyen, AV and Khan, MI (1995). Analysis of Salmonella Enteritidis isolates by arbitrarily primed PCR. J. Clin. Microbiol., 33: 987-989.
Fallah, SH; Asgharpour, F; Naderian, Z and Moulana, Z (2013). Isolation and determination of antibiotic resistance patterns in nontyphoid Salmonella spp isolated from chicken. Int. J. Enteric. Pathog., 1: 17-21.
Gould, LH; Walsh, KA; Vieira, AR; Herman, K; Williams, IT; Hall, AJ and Cole, D (2013). Surveillance for foodborne disease outbreaks—United States, 1998–2008. MMWR CDC Surveill. Summ., 62: 1-34.
Grimont, PA and Weill, FX (2007). Antigenic formulae of the Salmonella serovars. WHO collaborating centre for reference and research on Salmonella. 9: 1-66.
Hendriksen, RS; Vieira, AR; Karlsmose, S; Lo Fo Wong, DM; Jensen, AB; Wegener, HC and Aarestrup, FM (2011). Global monitoring of Salmonella serovar distribution from the World Health Organization Global Foodborne Infections Network Country Data Bank: results of quality assured laboratories from 2001 to 2007. Foodborne Pathog. Dis., 8: 887-900.
Heuvelink, AE; Van de Kar, NC; Meis, JF; Monnens, LA and Melchers, WJ (1995). Characterization of verocytotoxin-producing Escherichia coli O157 isolates from patients with haemolytic uraemic syndrome in Western Europe. Epidemiol. Infect., 115: 1-3.
Hu, Y; Cheng, H and Tao, S (2017). Environmental and human health challenges of industrial livestock and poultry farming in China and their mitigation. Environ. Int., 107: 111-130.
Khaltabadi, RF; Shahrokhi, N; Ebrahimi-Rad, M and Ehsani, P (2019). Salmonella Typhimurium in Iran: Contribution of molecular and IS 200 PCR methods in variants detection. PLoS One. 14: e0213726.
Khan, SA; Imtiaz, MA; Sayeed, MA; Shaikat, AH and Hassan, MM (2020). Antimicrobial resistance pattern in domestic animal-wildlife-environmental niche via the food chain to humans with a Bangladesh perspective; a systematic review. BMC Vet. Res., 16: 302.
Little, CL; Richardson, JF; Owen, RJ; De Pinna, E and Threlfall, EJ (2008). Campylobacter and Salmonella in raw red meats in the United Kingdom: prevalence, characterization and antimicrobial resistance pattern, 2003-2005. Food Microbiol., 25: 538-543.
Madadgar, O; Salehi, TZ; Ghafari, MM; Tamai, IA; Madani, SA and Yahyareyat, R (2009). Study of an unusual paratyphoid epornitic in canaries (Serinus canaria). Avian Pathol., 38: 437-441.
Madadgar, O; Tadjbakhsh, H; Salehi, TZ; Mahzounieh, M and Feizabadi, M (2008). Evaluation of random amplified polymorphic DNA analysis and antibiotic susceptibility application in discrimination of Salmonella Typhimurium isolates in Iran. New Microbiol., 31: 211-216.
Markey, B; Leonard, F; Archambault, M; Cullinane, A and Maguire, D (2013). Clinical veterinary microbiology. 2nd Edn., Printed in China, Elsevier Health Sciences. PP: 239-274.
Pasmans, F; Baert, K; Martel, A; Bousquet-Melou, A; Lanckriet, R; De, Boever S; Van Immerseel, F; Eeckhaut, V; De Backer, P and Haesebrouck, F (2008). Induction of the carrier state in pigeons infected with Salmonella enterica subspecies enterica serovar Typhimurium PT99 by treatment with florfenicol: a matter of pharmacokinetics. Antimicrob. Agents. Chemother., 52: 954-961.
Peighambari, S; Morshed, R; Baziar, M; Sharifi, A and Sadrzadeh, A (2018). Salmonellosis in broiler flocks of Golestan province: frequency, serogroups and drug resistance patterns of Salmonella isolates. New Find. Vet. Microbiol., 1: 70-78.
Rahmani, M; Peighambari, SM; Svendsen, CA; Cavaco, LM; Agersø, Y and Hendriksen, RS (2013). Molecular clonality and antimicrobial resistance in Salmonella enterica serovars Enteritidis and Infantis from broilers in three Northern regions of Iran. BMC Vet. Res., 9: 66.
Ranjbar, R; Elhaghi, P and Shokoohizadeh, L (2017). Multilocus sequence typing of the clinical isolates of Salmonella enterica serovar Typhimurium in Tehran Hospitals. Iran. J. Med. Sci., 42: 443-448.
Rodrigues, GL; Panzenhagen, P; Ferrari, RG; Paschoalin, VM and Conte-Junior, CA (2020). Antimicrobial resistance in nontyphoidal Salmonella isolates from human and swine sources in Brazil: a systematic review of the past three decades. Microb. Drug Resist., 26: 1260-1270.
Sabat, AJ; Budimir, A; Nashev, D; Sá-Leão, R; Van Dijl, JM; Laurent, F; Grundmann, H; Friedrich, AW and ESCMID Study Group of Epidemiological Markers (ESGEM) (2013). Overview of molecular typing methods for outbreak detection and epidemiological surveillance. Euro Surveill., 18: 20380.
Salehi, TZ; Badouei, MA; Madadgar, O; Ghiasi, SR and Tamai, IA (2013). Shepherd dogs as a common source for Salmonella enterica serovar Reading in Garmsar, Iran. Turkish J. Vet. Anim. Sci., 37: 102-105.
Threlfall, EJ (2002). Antimicrobial drug resistance in Salmonella: problems and perspectives in food-and water-borne infections. FEMS Microbiol. Rev., 26: 141-148.
Vaez, H; Ghanbari, F; Sahebkar, A and Khademi, F (2020). Antibiotic resistance profiles of Salmonella serotypes isolated from animals in Iran: a meta-analysis. Iran. J. Vet. Res., 21: 188-197.
Wang, X; Wang, H; Li, T; Liu, F; Cheng, Y; Guo, X; Wen, G; Luo, Q; Shao, H; Pan, Z and Zhang, T (2020). Characterization of Salmonella spp. isolated from chickens in Central China. BMC Vet. Res., 16: 299.
Wayne, PA (2018). Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals (CLSI supplement VET08). 4th Edn., Clinical and Laboratory Standards Institute. Pennsylvania, USA, Clinical and Laboratory Standards Institute. PP: 14-138.
Yang, X; Huang, J; Zhang, Y; Liu, S; Chen, L; Xiao, C; Zeng, H; Wei, X; Gu, Q; Li, Y and Wang, J (2020). Prevalence, abundance, serovars and antimicrobial resistance of Salmonella isolated from retail raw poultry meat in China. Sci. Total Environ., 713: 136385.