Antibiotic resistance profiles of Salmonella serotypes isolated from animals in Iran: a meta-analysis

Document Type : Full paper (Original article)


1 Department of Microbiology, School of Medicine, Zabol University of Medical Sciences, Zabol, Iran

2 Student Research Committee, School of Medicine, Shahid Saddoughi University of Medical Sciences, Yazd, Iran

3 Biotechnology Research Center, Pharmaceutical Technology Institute, Mashhad University of Medical Sciences, Mashhad, Iran, and Neurogenic Inflammation Research Center, Mashhad University of Medical Sciences, Mashhad, Iran

4 Department of Microbiology, School of Medicine, Ardabil University of Medical Sciences, Ardabil, Iran



Background: Salmonella infection (salmonellosis) is a zoonotic bacterial disease. Widespread use of antibiotics in livestock and poultry production for different purposes such as treatment and growth promotion has led to the emergence of antibiotic-resistant Salmonella, causing treatment of Salmonella infections more difficult with each passing year. Aims: To determine the antibiotic resistance prevalence of Salmonella serotypes isolated from animals in different provinces of Iran. Methods: To find eligible articles, we searched the international and national electronic databases using appropriate keywords in English and Persian. Results: After applying predefined criteria, 54 articles reporting antibiotic resistance profiles of Salmonella serotypes were included. Salmonella isolates were mostly resistant against nalidixic acid (67%), tetracycline (66.9%), and streptomycin (49.6%), followed by trimethoprim/sulfamethoxazole (41.6%) and kanamycin (23.6%). The highest sensitivity was observed against imipenem, meropenem, and cefepime with 1.7%, 1.4%, and 1.9% of all isolates being resistant, respectively. Conclusion: Results revealed that the prevalence of resistant isolates to nalidixic acid, tetracycline and streptomycin is high and their use must be restricted. In addition, resistance to other antibiotics such as chloramphenicol, ampicillin, cephalothin, cefixime, and enrofloxacin is at an alarming level that calls for attention in the future infection control and antibiotic stewardship programs.


Main Subjects

Ahmadi, M; Talebi, A; Mansouri, S and Rahman, B (2013). Antimicrobial resistance pattern and plasmid profile of Salmonella isolates from poultry. J. Vet. Microbiol., 9: 117-128.
Akbarmehr, J (2012). Antimicrobial resistance in Salmonella isolated from broiler chicken carcasses. Afr. J. Microbiol. Res., 6: 1485-1488.
Amini, K (2016). Prevalence of antibiotic resistance genes in Salmonella Enteritidis isolated from animal and human and determining their antibiotic resistance patterns. J. Comp. Pathobiol., 12: 1733-1740.
Antonelli, P; Belluco, S; Mancin, M; Losasso, C and Ricci, A (2019). Genes conferring resistance to critically important antimicrobials in Salmonella enterica isolated from animals and food: a systematic review of the literature, 2013-2017. Res. Vet. Sci., 126: 59-67.
Asadpour, Y; Mohammadi, M and Rasa, M (2014). Isolation, serotyping and antibiotic resistance of Salmonella isolated from chicken carcasses in Guilan province. Iran. Vet. J., 9: 5-13.
Asgharpour, F; Rajabnia, R; Shahandashti, EF; Marashi, MA; Khalilian, M and Moulana, Z (2014). Investigation of class I integron in Salmonella Infantis and its association with drug resistance. Jundishapur J. Microbiol., 7: 1-5.
Azizpour, A (2018a). Determining the antibiotic resistance patterns of isolated Salmonella from broiler flocks to 28 antimicrobial agents used in Iran. J. Comp. Pathobiol., 15: 2411-2420.
Azizpour, A (2018b). A survey on prevalence of Salmonella Enteritidis and Salmonella Typhimurium serotypes in broiler flocks of Ardabil province and determination of their antibiotics resistance to five antibacterial agents widely used in the Iranian medical field. J. Health. 9: 143-151.
Bush, K and Jacoby, G (2010). Updated functional classification of β-lactamases. Antimicrob. Agents Chemother., 54: 969-976.
Dallal, M; Doyle, M; Rezadehbashi, M; Dabiri, H; Sanaei, M and Modarresi, S (2010). Prevalence and antimicrobial resistance profiles of Salmonella serotypes, Campylobacter and Yersinia spp. isolated from retail chicken and beef, Tehran, Iran. Food Cont., 21: 388-392.
Doosti, A; Mahmoudi, E; Jami, M and Mokhtari-Farsani, A (2016a). Prevalence of aadA1, aadA2, aadB, strA and strB genes and their associations with multidrug resistance phenotype in Salmonella Typhimurium isolated from poultry carcasses. Thai Vet. Med., 46: 691-697.
Doosti, A; Zohoor, A; Chehelgerdi, M and Mokhtari-Farsani, A (2016b). Distribution of TEM-1 gene in Salmonella enterica isolated from poultry carcasses in Iran. Thai Vet. Med., 46: 9-15.
Doulatyabi, S and Peyghambari, S (2017). Survey of Salmonella infections in broiler farms around Sanandaj. Sci. J. Ilam Uni. Med. Sci., 25: 70-78.
Egger, M; Smith, GD; Schneider, M and Minder, C (1997). Bias in meta-analysis detected by a simple, graphical test. BMJ. 315: 629-634.

El-Sharkawy, H; Tahoun, A; El-Gohary, A; El-Abasy, M; El-Khayat, F; Gillespie, T and El-Adawy, H (2017). Epidemiological, molecular characterization and antibiotic resistance of Salmonella enterica serovars isolated from chicken farms in Egypt. Gut Path., 9: 1-12.

Emadi, CS; Hasanzadeh, M; Bozorg, M 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., 7: 35-41.
Eng, SK; Pusparajah, P; Mutalib, N; Ser, H; Chan, KG and Lee, LH (2015). Salmonella: a review on pathogenesis, epidemiology and antibiotic resistance. Front. Life Sci., 8: 284-293.
Eshraghi, S; Dalall, M; Fardsanei, F; Salehi, TZ; Ranjbar, R; Nikmanesh, B and Akbari, A (2010). Salmonella Enteritidis and antibiotic resistance patterns: a study on 1950 children with diarrhea. Tehran Uni. Med. J., 67: 876-882.
Ezatpanah, E; Moradi, BS; Khaki, P; Ghaderi, R; Seyedan, JE and Moghtadaee, FS (2013). Isolation, serotyping and antibiotic-resistance pattern of isolated Salmonella from chicken of Arak. Iran. Vet. J., 9: 88-96.
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.
Farahani, RK; Ehsani, P; Ebrahimi-Rad, M and Khaledi, A (2018). Molecular detection, virulence genes, biofilm formation, and antibiotic resistance of Salmonella enterica serotype Enteritidis isolated from poultry and clinical samples. Jundishapur J. Microbiol., 11: 1-9.
Fasaei, BN and Tamai, IA (2017). Detection of Salmonella spp. from zoo animals in Iran, determination of serovars, antibiotic susceptibility and genotyping by RAPD-PCR. J. Hellenic Vet. Med. Soci., 68: 377-384.
Firoozeh, F; Zahraei-Salehi, T; Shahcheraghi, F; Karimi, V and Aslani, MM (2012). Characterization of class I integrons among Salmonella enterica serovar Enteritidis isolated from humans and poultry. FEMS Immunol. Med. Microbiol., 64: 237-243.
Gal-Mor, O; Boyle, EC and Grassl, GA (2014). Same species, different diseases: how and why typhoidal and non-typhoidal Salmonella enterica serovars differ. Front. Microbiol., 5: 1-10.
Ghaderi, R and Moradi, S (2016). Occurrence of multidrug-resistant Salmonella enterica serovar Enteritidis isolates from poultry in Iran. Arch. Razi Inst., 71: 43-49.
Ghasemmahdi, H; Tajik, H; Moradi, M; Mardani, K; Modaresi, R; Badali, A and Dilmaghani, M (2015). Antibiotic resistance pattern and biofilm formation ability of clinically isolates of Salmonella enterica serotype Typhimurium. Int. J. Enteric. Pathog., 3: 1-6.
Ghazalibina, M; Farahani, RK; Mansouri, S; Meskini, M; Farahani, AHK and Khaledi, A (2019). Molecular detection of antibiotic resistance genes, and class I, and II integrons in Salmonella Enteritidis isolated from Iranian one-day-old chicks. Gene Rep., 16: 1-8.
Ghoddusi, A; Fasaei, BN; Karimi, V; Tamai, IA; Moulana, Z and Salehi, TZ (2015). Molecular identification of Salmonella Infantis isolated from backyard chickens and detection of their resistance genesby PCR. Iran. J. Vet. Res., 16: 293-297.
Ghorbani-Ranjbary, A; Ghorbani-Ranjbary, N and Ghorbani-Ranjbary, Z (2013). Survey on Salmonella infection horse rate in horses of some horse riding clubs Southern Iran. Am. J. Discovery Dev., 3: 181-187.
Gut Abraham Majak; Vasiljevic, T; Yeager, T and Donkor, O (2018). Salmonella infection-prevention and treatment by antibiotics and probiotic yeasts: a review. Microbiology (Reading). 164: 1327-1344.
Halimi, HA; Seifi, HA and Rad, M (2014). Bovine salmonellosis in Northeast of Iran: frequency, genetic fingerprinting and antimicrobial resistance patterns of Salmonella spp. Asian Pac. J. Trop. Biomed., 4: 1-7.
Hao, H; Sander, P; Iqbal, Z; Wang, Y; Cheng, G and Yuan, Z (2016). The risk of some veterinary antimicrobial agents on public health associated with antimicrobial resistance and their molecular basis. Front. Microbiol., 7: 1-11.
Hur, J; Jawale, C and Lee, JH (2012). Antimicrobial resistance of Salmonella isolated from food animals: a review. Food Res. Int., 45: 819-830.
Jadidi, A; Hosseni, SD; Homayounimehr, A; Hamidi, A; Ghani, S and Rafiee, B (2012). Simple and rapid detection of Salmonella sp. from cattle feces using polymerase chain reaction (PCR) in Iran. Afr. J. Microbiol. Res., 6: 5210-5214.
Jafari, R; Ghorbanpour, M and Jaideri, A (2007). An investigation into Salmonella infection status in backyard chickens in Iran. Int. J. Poult. Sci., 6: 227-229.
Jahantigh, M; Jafari, SM; Rashki, A and Salari, S (2015). Prevalence and antibiotic resistance of Salmonella spp. in Turkey. Open J. Med. Microbiol., 5: 113-117.
Jamali, H; Radmehr, B and Ismail, S (2014). Prevalence and antimicrobial resistance of Listeria, Salmonella, and Yersinia species isolates in ducks and geese. Poultry Sci., 93: 1023-1030.
Khademi, F; Vaez, H; Ghanbari, F; Arzanlou, M; Mohammadshahi, J and Sahebkar, A (2020). Prevalence of fluoroquinolone-resistant Salmonella serotypes in Iran: a meta-analysis. Path. Glob. Health. 114: 16-29.
Liberati, A; Altman, DG; Tetzlaff, J; Mulrow, C; Gtzsche, PC; Ioannidis, JP and Moher, D (2009). The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. PLoS Med., 6: 1-28.
Mahdavi, S; Azizi Dehbokri, M and Isazadeh, A (2018). Contamination of chicken meat with Salmonella spp distributed in mahabad city, Iran. Int. J. Enteric. Pathog., 6: 65-68.
Malidareh, NR; Firouzi, S; Malidareh, NR and Habibi, H (2013). In vitro and in vivo susceptibility of Salmonella spp. isolated from broiler chickens. Comp. Clin. Pathol., 22: 1065-1068.
Mehrabian, S and Jaberi, E (2007). Isolasion, identification and antimicrobial resistance patterns of Salmonella from meat products in Tehran. Pak. J. Biol. Sci., 10: 122-126.
Mir, R and Rashki Ghalehnoo, Z (2018). Frequency and antimicrobial resistance pattern of Salmonella spp in asymptomatic rural dog in Zabol. New Find. Vet. Microbiol., 1: 44-50.
Mirmomeni, M; Colagar, AH and Ghazaey, S (2007). Molecular study of Salmonella Enteritidis in poultry samples by PCR, plasmid curing, antibiotic resistance and protein pattern analysis. Pak. J. Biol. Sci., 10: 1562-1570.
Moradi, BS (2017). Investigation of antibiotic resistance in Salmonella Infantis isolated from poultry in Arak. Vet. Res., 13: 99-108.
Morshed, R and Peighambari, SM (2010). Drug resistance, plasmid profile and random amplified polymorphic DNA analysis of Iranian isolates of Salmonella Enteritidis. New Microbiol., 33: 47-56.
Mozajin, MN; Khaki, P and Noorbakhsh, F (2018). Antibiotic resistance of Salmonella enterica producing extended-spectrum β-lactamases (ESBLs) type CMY-2, in poultry. J. Gorgan Uni. Med. Sci., 20: 109-115.
Munn, Z; Moola, S; Lisy, K; Riitano, D and Tufanaru, C (2015). Methodological guidance for systematic reviews of observational epidemiological studies reporting prevalence and cumulative incidence data. Int. J. Evidence-Based Health. 13: 147-153.
Naghizadeh, S and Moradi, G (2017). Determination of antibiotic resistance and identification of tetracycline (tet) resistance genes in Salmonella Enteritidis strains isolated from food sources. Iran. J. Med. Microbiol., 11: 64-69.
Namroodi, S and Behine, K (2016). Frequency, serovars and antibiotic resistant pattern of Salmonella spp. isolated from sheep in golestan province, Iran. Iran. J. Rum. Res., 4: 21-36.
Namroodi, S; Staji, H and 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: 47-55.
Ochiai, RL; Acosta, CJ; Danovaro-Holliday, M; Baiqing, D; Bhattacharya, SK; Agtini, MD and Shin, S (2008). A study of typhoid fever in five Asian countries: disease burden and implications for controls. Bull. World Health Organ., 86: 260-268.
Ommi, D; Hemmatinezhad, B; Hafshejani, TT and Khamesipour, F (2017). Incidence and antimicrobial resistance of Campylobacter and Salmonella from houseflies (Musca domestica) in kitchens, farms, hospitals and slaughter houses. Proc. Natl. Acad. Sci. India Sect. B Biol. Sci., 87: 1285-1291.
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 Inst., 70: 81-87.
Paniel, N and Noguer, T (2019). Detection of Salmonella in food matrices, from conventional methods to recent aptamer-sensing technologies. Foods. 8: 1-38.
Peighambari, S; Akbarian, R; Morshed, R and Yazdani, A (2013). Characterization of Salmonella isolates from poultry sources in Iran. Iran. J. Vet. Med., 7: 35-41.
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.
Peighambari, S; Qorbaniun, E; Morshed, R and Haghbin Nazarpak, H (2019). A survey on Salmonella infection in broiler farms around Mashhad city: determination of serogroups and antimicrobial resistance pattern of the Salmonella isolates. Iran. Vet. J., 15: 34-43.
Peighambari, S; Sorahi, NM and Morshed, R (2015). Detection of Salmonella enterica serovar Infantis among serogroup C Salmonella isolates from poultry using PCR and determination of drug resistance patterns. Iran. Vet. J., 11: 53-60.
Peighambari, S; Yazdani, A and Hojjati, P (2011). Salmonella infection in birds kept in parks and pet shops in Tehran, Iran. Iran. J. Vet. Med., 5: 145-148.
Raeisi, E and Ghiamirad, M (2015). Survey on prevalence of Salmonella serogroups and antibiotics susceptibility pattern in chicken meat in Ardabil, Iran. J. Ardabil Uni. Med. Sci., 15: 320-329.
Rahmani, M; Peighambari, SM; Svendsen, CA; Cavaco, LM; Agers, 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: 66-76.
Rajaeian, H; Firouzi, R; Jalaei, J and Heydari, DF (2003). Antibiotic resistance of several common bacterial species isolated from chickens in Shiraz area. J. Vet. Med., 58: 223-226.
Ranjbar, R; Giammanco, GM; Aleo, A; Plano, MRA; Naghoni, A; Owlia, P and Mammina, C (2010). Characterization of the first extended-spectrum β-lactamase–producing nontyphoidal Salmonella strains isolated in Tehran, Iran. Foodborne Pathog. Dis., 7: 91-95.
Ranjbar, R; Giammanco, GM; Farshad, S; Owlia, P; Aleo, A and Mammina, C (2011). Serotypes, antibiotic resistance, and class 1 integrons in Salmonella isolates from pediatric cases of enteritis in Tehran, Iran. Foodborne Pathog. Dis., 8: 547-553.
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. Turk. J. Vet. Anim. Sci., 37: 102-105.
Salehi, TZ; Mahzounieh, M and Saeedzadeh, A (2005). The isolation of antibiotic-resistant Salmonella from intestine and liver of poultry in Shiraz province of Iran. Int. J. Poult. Sci., 4: 320-322.
Sodagari, HR and Mashak, Z (2015). Prevalence and antimicrobial resistance of Salmonella serotypes isolated from retail chicken meat and giblets in Iran. J. Infect. Dev. Count., 9: 463-469.
Su, L and Chiu, C (2007). Salmonella: clinical importance and evolution of nomenclature. Chang Gung Med. J., 30: 210-219.
Tajbakhsh, F and Tajbakhsh, E (2013). Determination of antibiotic resistance in Salmonella spp isolated from raw cow, sheep and goat’s milk in Chaharmahal Va Bakhtiyari Provience, Iran. Glob. Vet., 10: 681-685.
Tajbakhsh, F; Tajbakhsh, E; Momeni, M; Rahimi, E and Sohrabi, R (2012). Occurrence and antibiotic resistance of Salmonella spp isolated from raw cow’s milk from Shahahrekord, Iran. Int. J. Microbiol. Res., 3: 242-245.
Velasquez, C; Macklin, K; Kumar, S; Bailey, M; Ebner, P; Oliver, H and Singh, M (2018). Prevalence and
antimicrobial resistance patterns of Salmonella isolated from poultry farms in southeastern United States. Poult. Sci., 97: 2144-2152.
Vtnair, D; Venkitanarayanan, K and Kollanoor Johny, A (2018). Antibiotic-resistant Salmonella in the food supply and the potential role of antibiotic alternatives for control. Foods. 7: 1-24.
Wang, Y; Yang, B; Wu, Y; Zhang, Z; Meng, X; Xi, M and Wang, D (2015). Molecular characterization of Salmonella enterica serovar Enteritidis on retail raw poultry in six provinces and two national cities in China. Food Microbiol., 46: 74-80.
Zare, P; Ghorbani-Choboghlo, H; Jaberi, S; Razzaghi, S; Mirzaei, M and Mafuni, K (2014). Occurrence and antimicrobial resistance of Salmonella spp. and Escherichia coli isolates in apparently healthy slaughtered cattle, sheep and goats in East Azarbaijan province. Int. J. Ent. Pathog., 2: 1-4.
Zare, P; Ghorbani-Choboghlo, H; Tolouei, M and Hadavi, J (2016). Evaluation of the occurrence of Salmonella serovars and its antibiotic susceptibility in apparently healthy domestic animals in rural areas of East Azerbaijan province. Iran. J. Med. Microbiol., 10: 88-92.