Occurrence of multidrug-resistant Salmonella enterica serovar Enteritidis isolates from poultry in Iran

Document Type: Original Articles


Department of Microbiology, Razi vaccine and Serum Research Institute, Karaj, Iran


Salmonella enterica is recognized as one of the major food-borne pathogens with more than 2,500 serotypes
worldwide. The present study addresses antimicrobial resistance of Salmonella enterica serovar Enteritidis
isolates in Iran. A collection of 151 Salmonella spp. isolates collected from poultry were serotyped to
identify Salmonella Enteritidis. Sixty-one Salmonella Enteritidis were subsequently tested against 30
antimicrobials. A high frequency of antimicrobial resistance was observed against nitrofurantoin (n=55,
90.2%) followed by nalidixic acid (n=41, 67.2%), and cephalexin (n=23, 37.7%). Multi-drug resistance
were observed in 35 (57.4%) out of 61 isolates. Twenty-six antimicrobial resistance patterns were observed
among the 61 Salmonella Enteritidis. All isolates were susceptible to ofloxacin, imipenem, enrofloxacin,
chloramphenicol, gentamicin, and 3rd and 4th generation cephalosporins. In conclusion, our results revealed
that implementing new policies toward overuse of antimicrobial drugs in Iranian poultry industry are of
great importance.


Main Subjects

Article Title [French]

L’occurrence d’isolats multirésistants de Salmonella enterica serovar Enteritidis chez les volailles iraniennes

Abstract [French]

Salmonella enterica est reconnue comme l’un des principaux pathogènes d’origine alimentaire comptant plus de 2500 sérotypes à travers le monde. Cette étude a pour objectif d’évaluer la résistance antimicrobienne des isolats de Salmonella enterica serovar Enteritidis en Iran. Une collection de 151 espèces de Salmonella infectant les volailles ont fait l’objet d’un sérotypage afin d’identifier S. Enteritidis. Soixante et un isolats de S. Enteritidis ont été ensuite testés contre 30 agents antimicrobiens. Les plus fortes résistances antimicrobiennes ont été observées contre le nitrofurantoine (n=55, 90.2%), suivi par l’acide nalidixique (n=41, 67.2%), et la céphalexine (n=23, 37.7%). Trente cinq des 61 isolats testés étaient multirésistants. Cette étude a révélé 26 patterns différents de résistance antimicrobienne dans les 61 isolats analysés. Tous les isolats montraient une susceptibilité vis-à-vis de l’ofloxacine, l’imipenème, l’enrofloxacine, le chloramphénicol, la gentamicine, et la céphalosporine de troisième et quatrième générations. En conclusion, nos résultats reflètent la nécessité d’adopter de nouvelles politiques pour limiter l’emploi excessif de certains agents antimicrobiens dans l’industrie avicole iranienne.

Keywords [French]

  • Résistance antimicrobienne
  • Profile de résistance
  • multirésistance
  • Salmonella enterica
Abdollahi, A., Najafipour, S., Kouhpayeh, S.A., Meshkibaf, M., 2011. Salmonlla Enterica:Serotyping, Drug Resistance & Extended Spectrum of B-Lactamase (ESBLs). J. Fasa Univ. Med.Sci. 1, 38-44.

Angulo, F.J., Nargund, V.N., Chiller, T.C., 2004. Evidence of an association between use of anti-microbial agents in food animals and anti-microbial resistance among bacteria isolated from humans and the human health consequences of such resistance. J Vet Med B Infect Dis Vet Public Health 51, 374-379.

Anonymous, 2012a. Antimicrobial Resistance. In: Organization, W.H. (Ed.), (World Health Organization). World Health Organization, World Health Organization.

Anonymous, 2012b. Clinical&Laboratory-Standard-Institute, Twenty-Second Informational Supplement performance standards for antimicrobial susceptibility testing, Wayne, PA, USA, p. 188.

Ashtiani, M.T., Monajemzadeh, M., Kashi, L., 2009. Trends in antimicrobial resistance of fecal Shigella and Salmonella isolates in Tehran, Iran. Indian J Pathol Microbiol 52, 52-55.

Bennish, M.L., Salam, M.A., 1992. Rethinking options for the treatment of shigellosis. J Antimicrob Chemother 30, 243-247.

Braden, C.R., 2006. Salmonella enterica serotype Enteritidis and eggs: a national epidemic in the United States. Clin Infect Dis 43, 512-517.

Broughton, E.I., Heffernan, H.M., Coles, C.L., 2010. Salmonella enterica serotypes and antibiotic susceptibility in New Zealand, 2002-2007. Epidemiol Infect 138, 322-329.

Crump, J.A., Barrett, T.J., Nelson, J.T., Angulo, F.J., 2003. Reevaluating fluoroquinolone breakpoints for Salmonella enterica serotype Typhi and for non-Typhi salmonellae. Clin Infect Dis 37, 75-81.

Davies, P., Turkson, P., Funk, J., Nichols, M., Ladely, S., Fedorka-Cray, P., 2001. Comparison of methods for isolating Salmonella bacteria from faeces of naturally infected pigs. Journal of applied microbiology 89, 169-177.

Eshraghi, S., Dalall, M.M.S., Fardsanei, F., Salehi, T.Z., Ranjbar, R., Nikmanesh, B., Aminharati, F., Abdosamadi, Z., Akbari, A., 2010. Salmonella Enteritidis and antibiotic resistance patterns: a study on 1950 children with diarrhea. Tehran University Med J 67, 876-881.

Firoozeh, F., Shahcheraghi, F., Zahraei Salehi, T., Karimi, V., Aslani, M., 2011. Antimicrobial resistance profile and presence of class I integrongs among Salmonella enterica serovars isolated from human clinical specimens in Tehran, Iran. Iran J Microbiol 3, 112-117.

Giraud, E., Baucheron, S., Cloeckaert, A., 2006. Resistance to fluoroquinolones in Salmonella: emerging mechanisms and resistance prevention strategies. Microbes Infect 8, 1937-1944.

Grimont, P.A., Weill, F.X., 2007. Antignenic formulas of the Salmonella serovars WHO Collaboration Center for Resistance and Research on Salmonella, Institute Pasteur, paris

Hald, T., Lo Fo Wong, D.M., Aarestrup, F.M., 2007. The attribution of human infections with antimicrobial resistant Salmonella bacteria in Denmark to sources of animal origin. Foodborne Pathog Dis 4, 313-326.

Hendriksen, R.S., 2003a. Global Salm-Surv A global Salmonella surveillance and laboratory support project of the World Health Organization- Identification of Salmonella. WHO.

Hendriksen, R.S., 2003b. Global Salmonella Surveillance, Laboratory protocols: identification of Salmonella. World Health Organization, pp. 1-21.

Hohmann, E.L., 2001. Nontyphoidal salmonellosis. Clin Infect Dis 32, 263-269.

Kiessling, C.R., Jackson, M., Watts, K.A., Loftis, M.H., Kiessling, W.M., Buen, M.B., Laster, E.W., Sofos, J.N., 2007. Antimicrobial susceptibility of Salmonella isolated from various products, from 1999 to 2003. J Food Prot 70, 1334-1338.

Majowicz, S.E., Musto, J., Scallan, E., Angulo, F.J., Kirk, M., O'Brien, S.J., Jones, T.F., Fazil, A., Hoekstra, R.M., International Collaboration on Enteric Disease 'Burden of Illness, S., 2010. The global burden of nontyphoidal Salmonella gastroenteritis. Clin Infect Dis 50, 882-889.

Malorny, B., Schroeter, A., Helmuth, R., 1999. Incidence of quinolone resistance over the period 1986 to 1998 in veterinary Salmonella isolates from Germany. Antimicrob Agents Chemother 43, 2278-2282.

Martin, L.J., Fyfe, M., Dore, K., Buxton, J.A., Pollari, F., Henry, B., Middleton, D., Ahmed, R., Jamieson, F., Ciebin, B., McEwen, S.A., Wilson, J.B., 2004. Increased burden of illness associated with antimicrobial-resistant Salmonella enterica serotype typhimurium infections. J Infect Dis 189, 377-384.

Molbak, K., 2004. Spread of resistant bacteria and resistance genes from animals to humans--the public health consequences. J Vet Med B Infect Dis Vet Public Health 51, 364-369.

Morshed, R., Peighambari, S.M. 2010. Drug resistance, plasmid profile and random amplified polymorphic DNA analysis of Iranian isolates of Salmonella enteritidis. New Microbiol 33, 47-56.

Ohmani, F., Khedid, K., Britel, S., Qasmaoui, A., Charof, R., Filali-Maltouf, A., El Aouad, R., 2010. Antimicrobial resistance in Salmonella enterica serovar Enteritidis in Morocco. J Infect Dev Ctries 4, 804-809.

Okeke, I.N., Laxminarayan, R., Bhutta, Z.A., Duse, A.G., Jenkins, P., O'Brien, T.F., Pablos-Mendez, A., Klugman, K.P., 2005. Antimicrobial resistance in developing countries. Part I: recent trends and current status. Lancet Infect Dis 5, 481-493.

Rad, M., Kalidari, G., SH., K., 2008. Identification of salmonella spp. In a native poultry breeding and improvement center. Pajouhesh & Sazandegi 81, 87-93.

Ranjbar, R., Naghoni, A., Panahi, Y., Izadi, M., 2008. Antimicrobial susceptibility pattern of salmonella strains isolated from clinical cases against 10 less ordinary prescribed antibiotics in salmonella infection treatment. Iranian Journal of Infectious Diseases and Tropical Medicine 46, 41-45.

Shapouri, R., Rahnema, M., Eghbalzadeh, S., 2009. Prevalence of Salmonella seroptypes in poultry meat and egg and determine their antibiotic sensitivity in Zanjan city The Quarterterly Journal of Biological Sciences 2, 63-71.

Uzzau, S., Brown, D.J., Wallis, T., Rubino, S., Leori, G., Bernard, S., Casadesus, J., Platt, D.J., Olsen, J.E., 2000. Host adapted serotypes of Salmonella enterica. Epidemiol Infect 125, 229-255.

Varma, J.K., Molbak, K., Barrett, T.J., Beebe, J.L., Jones, T.F., Rabatsky-Ehr, T., Smith, K.E., Vugia, D.J., Chang, H.G., Angulo, F.J., 2005. Antimicrobial-resistant nontyphoidal Salmonella is associated with excess bloodstream infections and hospitalizations. J Infect Dis 191, 554-561.

Zahraei Salehi, T., Mahzounieh, M., Saeedzadeh, A., 2005. The isolation of antibiotic-resistant Salmonella from intestine and liver of poultry in Shiraz province of Iran. pp. 320-322.