Escherichia coli O157:H7 is one of the most dangerous zoonotic pathogens of meat. The present investigation was done to study the prevalence and antibiotic resistance of E. coli O157:H7 strains isolated from raw meat samples. A total of 458 meat samples were collected. Samples were cultured using what? After which sorbitol negative isolates were analyzed for rfbO157 and flicH7 genes. Thirty-six out of 458 meat samples were positive for sorbitol negative strains of E. coli (7.86%). All of the sorbitol negative strains were also positive for rfbO157 and flicH7 genes. Prevalence of E. coli O157:H7 strains were 7.86%. The prevalence of E. coli O157:H7 in chicken meat was higher than the other samples (16.25%). The genes that encode resistance to ampicillin (CITM) (100%), gentamicin (aac(3)-IV) (94.44%) and tetracycline (tetA) (61.11%) had the highest prevalence. Escherichia coli O157:H7 strains from raw meat samples from ruminants and poultry had the highest resistance to ampicillin (100%), tetracycline (83.33%) and gentamicin (83.33%) respectively. Strains of antibiotic resistant E. coli 0157:H7 found in this present study are of public health importance.
Food pathogens cause more than three-hundred diseases from simple diarrhea to death 1, 2. Foodborne diseases cause about 75 million illnesses, 320,000 hospitalizations, and 4,000 deaths in the United States annually 2, 3, 4. Access to hygienic and healthy food samples is an important issue particularly in Iran where basic principles of meat inspection are not applied in some slaughterhouses. Food samples with animal origin and especially meat play an important role in the transmission of foodborne pathogens to humans 5, 6, 7, 8.
Escherichia. coli (E. coli) O157:H7 is an important foodborne pathogen of public health importance 5, 6, 7, 8. E. coli is a gram-negative, non-sporulating, rod-shaped, facultative anaerobe and Shiga toxin-producing E. coli (STEC) is a subdivision of enterohemorrhagic E. coli (EHEC) 9, 10, 11. Outbreak of food poisoning and foodborne diseases are associated with certain STEC O-serogroups and O157 is the most important serogroup associated with intensive clinical syndromes like lethal hemolytic uremic syndrome (HUS), bloody and non-bloody diarrhea, thrombotic thrombocytopenic purpura (TTP) and hemorrhagic colitis (HC) 9, 10, 11. Human infection with E. coli O157:H7 serotype has been associated with contaminated food samples, water, and person-to person transmission 9, 10, 11. Meats from ruminants and poultry are considered to be the primary reservoirs of E. coli O157:H7 9, 10, 11.
High levels of resistance in E. coli O157:H7 is an important factor which can increase the pathogenicity of bacterium. Food samples with animal origin and especially meat have been found to harbor E. coli 0157:H7 with high levels of resistance against commonly used groups of antibiotics including quinolones, aminoglycosides, macrolides, cephalosporins, sulfonamides, fluoroquinolones and tetracycline 9, 10, 11, 12, 13, 14, 15. Some antibiotic resistance genes including the genes that encode resistance to ampicillin (CITM), fluoroquinolone (qnr), gentamicin (aac(3)-IV), cephalothin (blaSHV), trimethoprim (dfrA1), sulfonamide (sul1), tetracycline (tetA and tetB), chloramphenicol (cat1 and cmlA) and aminoglycosides (aadA1 have been found to be responsible for antibiotic resistance in STEC strains 9, 10, 11, 12, 13, 14, 16, 17, 18.
Regarding an uncertain prevalence of E. coli O157:H7 in raw meat samples, the present research was carried out to study the prevalence and distribution of antibiotic resistance genes and antibiotic resistance pattern of E. coli O157:H7 strains isolated from raw bovine, ovine, caprine, camel, chicken, turkey and quail meat samples.
Verification of this research project and the licenses related to sampling process were approved by Dr. Zohreh Mashak.
2.2. SamplesFrom September 2015 to December 2015, a total of 458 raw meat samples including cows (n= 70), sheep (n= 68), goats (n= 60), camel (n= 60), chicken (n= 80), turkey (n= 60), and quail (n= 60) were collected and immediately transferred to the laboratory in cooler with ice-packs. Samples were randomly collected from the various parts of Alborz province, Iran. All meat samples showed normal physical characters including odor, color and density.
2.3. Escherichia coli O157:H7 IsolationTwenty-five grams of each meat sample was aseptically transferred to 225 ml of Trypticase Soy Broth (TSB, Merck, Frankfurt, Germany) supplemented with 0.5 mg/ml novobiocin and incubated at 37°C for 24 hrs 10, 16. Enriched culture was plated onto Sorbitol MacConkey agar (SMAC, Merck, Frankfurt, Germany) supplemented with cefixime (0.05 mg/ml) and potassium tellurite (2.5 mg/L). All plates were then incubated at 37°C for 24 hrs. Then, non-sorbitol fermented colonies were selected from the SMAC plates and streaked onto plates containing Eosin Methylene Blue agar (EMB, Merck, Frankfurt, Germany) and were incubated at 37°C for 24 hrs. These isolates, with typical E. coli green metallic shine on EMB agar were biochemically tested for growth on triple sugar iron agar (TSI, Merck, Frankfurt, Germany) and lysine iron agar (LIA, Merck, Frankfurt, Germany), oxidative/fermentative degradation of glucose, citrate utilization, urease production, indole production, tryptophan degradation, glucose degradation (methyl red test, Merck, Frankfurt, Germany), Voges Proskauer (VP, Merck, Frankfurt, Germany), lysine decarboxylase and motility tests 10, 16.
2.4. PCR Confirmation of Escherichia coli O157:H7Sorbitol negative E. coli strains were subjected to DNA extraction and PCR amplification of rfbO157 and flicH7 targets. Sorbitol negative colonies were sub-cultured on Luria-Bertani broth (LBB, Merck, Frankfurt, Germany) and further incubated for 48 h at 37 °C. Genomic DNA was extracted from bacterial colonies using the DNA extraction kit (Thermo Fisher Scientific, Frankfurt, Germany) according to manufacturer’s instruction. The DNA extraction was done according 4 different stages of growth of bacteria, sample preparation, lysis of cell walls, purification of DNA and finally DNA condensation. The concentrations of extracted DNA of meat samples were previously determined by measuring absorbance of the sample at 260 nm using spectrophotometer 19. Table 1 shows the primer sequence and PCR cycling program used for the amplification of the rfbO157 and flicH7 genes. The PCR reactions were performed in a total volume of 25 μL, including 1.5 mM MgCl2, 50 mM KCl, 10 mM Tris-HCl (pH 9.0), 0.1% Triton X-100, 200 μM dNTPs each (Thermo Fisher Scientific, Frankfurt, Germany), 2.5 μL PCR buffer (10X), 25 pmoL of each primer (Table 1) 20, 21, 1.5 U of Taq DNA polymerase (Thermo Fisher Scientific, Frankfurt, Germany) and 5 μL (40-260 ng/μL) of the extracted DNA template of the E. coli isolates. Escherichia. coli O157:H7 (ATCC 35150) and sterile distilled water were used as t positive negative controls respectively 20, 21.
2.5. PCR Amplification of Antibiotic Resistance GenesEscherichia. coli O157:H7 strains were tested for presence of antibiotic resistance genes using PCR method and Table 2 shows the list of primers, program and condition of each reaction used for detection of antimicrobial resistant genes 11, 22. Programmable DNA thermo-cycler (Eppendorf Flexrcycler, Eppendorf AG Barkhausenweg, Hamburg, Germany) was used in all PCR reactions. The PCR amplification products (15 μl) were subjected to electrophoresis in a 1.5% agarose gel in 1X TBE buffer at 80 V for 30 min, stained with SYBR Green (Thermo Fisher Scientific, Frankfurt, Germany). All runs included a negative DNA control consisting of PCR grade water and strains of E. coli O157:K88ac:H19, CAPM 5933 and E. coli O159:H20, CAPM 6006 were used as positive controls.
2.6. Antimicrobial Susceptibility TestingAntibiogram test of E. coli strains against 13 commonly used antibiotics was determined according to the guidelines described by Clinical and Laboratory Standards Institute (950 West Valley Road, Suite 2500 Wayne, PA 19087 USA) 23. For this purpose, tetracycline (30 µg), ampicillin (10 µg), cefotaxime (30 µg), gentamycin (10 µg), ciprofloxacin (5 µg), amikacin (30 µg), imipenem (30 µg), cotrimoxazole (30 µg), enrofloxacin (5 µg), sulfamethoxazole (25 µg), trimethoprim (5 µg), streptomycin (10 µg), and chloramphenicol (30 µg) (Oxoid, Wade Road Basingstoke Hampshire RG24 8PW, United Kingdom). Plates were incubated at 37°C for 18-24 h and results were interpreted as described by CLSI (2012) 23.
Statistical analysis was performed using the SPSS/20.0 software and chi-square and fisher exact test for significant relationships. The prevalence of antibiotics resistance properties of E. coli O157:H7 isolated from various types of raw meat samples were statistically analyzed. Statistical significance was regarded at a P value < 0.05.
Table 3 represents the prevalence of E. coli and also O157:H7 serotype in different types of raw meat samples. Thirty-six out of 458 (7.86%) raw meat samples were positive for sorbitol negative bacteria. All of the sorbitol negative bacteria harbored both rfbO157 and flicH7 genes in the PCR reaction. Therefore, the prevalence of the E. coli O157:H7 strains in raw meat samples were 7.86%.
Figure 1 shows the results of the gel electrophoresis for the rfbO157 and flicH7 genes. We found that chicken meat samples had the highest (16.25%) prevalence of E. coli O157:H7, while caprine meat samples had the lowest (3.33%). Statistically significant difference was seen between the prevalence of E. coli O157:H7 and type of samples (P <0.05).
Table 4 represents the distribution of antibiotic resistance genes among the E. coli O157:H7 strains recovered from raw meat samples. We found that the genes that encode resistance against ampicillin (CITM) (100%), gentamicin (aac(3)-IV) (94.44%) and tetracycline (tetA) (61.11%) had the highest prevalence. E. coli O157:H7 strains isolated from chicken meat samples had the highest and the most diverse prevalence of antibiotic resistance genes. Statistically significant difference was seen between the prevalence of antibiotic resistance genes and type of samples (P <0.05). E. coli O157:H7 strains isolated from chicken, bovine and turkey had the highest prevalence of antibiotic resistance genes.
Table 5 represents the total prevalence of antibiotic resistance among the E. coli O157:H7 strains isolated from various types of raw meat samples. We found that E. coli O157:H7 strains of our study harbored the highest levels of resistance against ampicillin (100%), tetracycline (83.33%), gentamicin (83.33^), amikacin (58.33%) and sulfamethoxazole (58.33%). E. coli O157:H7 strains isolated from chicken meat samples had the highest and the most diverse prevalence of antibiotic resistance. Statistically significant difference was seen between the prevalence of antibiotic resistance and type of samples (P <0.05). Prevalence of resistance against imipenem (2.77%) and chloramphenicol (11.11%) antibiotics were low.
E. coli O157:H7 is the most commonly isolated serotype of EHEC group from ill persons and also cases of food infection in the Japan, United States and the United Kingdom 23, 24. The Centers for Disease Control and Prevention (CDC) has appraised that E. coli O157:H7 infections cause 75,000 illnesses, 2,500 hospitalizations, and 50 deaths annually in the United States 24. The annual cost of illness due to E. coli O157:H7 infections was 400 million dollars 24.
Raw ruminant and poultry meat are considered as substantial sources of E. coli O157:H7. Results of the present investigation showed that 36 samples out of 458 samples (7.86%) were contaminated with E. coli O157:H7 which was entirely high. Some of the most important causes for the high prevalence of E. coli O157:H7 in raw meat samples of our study are I: close contact of meat carcasses with each other and easily transmission of E. coli O157:H7; II: possibility for transmission of E. coli O157:H7 from the contents of digestive tract, blood, wool and external surface of body through the slaughter process; III: transmission of E. coli O157:H7 from the hands of the infected butchers and meat inspector to meat; IV: transmission of E. coli O157:H7 from animals like rats, cats, fox and birds which have been entered from outside the slaughterhouse to meat and environment; V: using from infected water for washing of meat carcasses; VI: transmission of E. coli O157:H7 from the contaminated equipment like knife and yeah used for cutting the head, skin and divided the carcasses to meat; VII: lack of attention to detailed meat inspection in some Iranian slaughterhouses.
Zarei et al. (2013) 25 reported that the prevalence of E. coli O157:H7 in the meat samples of beef, buffalo and lamb were 2.8%, 1.4% and 0%, respectively which was entirely lower than our findings. Hessain et al. (2015) 26 reported that the prevalence of E. coli O157:H7 in raw beef, chicken and mutton meat samples were 2%, 2.5% and 2.5%, respectively which was lower than our findings. They showed that the prevalences of E. coli O157:H7 in ground beef, beef burgers, beef sausage, ground chicken and chicken burgers were 5%, 10%, 0.0%, 5% and 0.0%, respectively. Momtaz et al. (2013) 10 indicated that 238 out of 820 meat samples (29.02%) were positive for presence of E. coli and of which 153 samples (64.28%) were STEC. They showed that sheep meat (35.45%) had the highest prevalence of E. coli, while camel meat (19.56%) had the lowest. They showed that the prevalence of O157 serogroup in the meat samples of beef, sheep, goat and camel were 31.34%, 28.57%, 36% and 25%, respectively. Previous study which was conducted in China 27 showed that of 551 samples studied, 21 (3.81%) were positive for E. coli O157 and seven (1.27%) for O157:H7. They showed that the highest prevalence rate was found in beef (13.32%), pork (6.90%), chicken (3.28%) and duck (2.54%). Bekele et al. (2014) 28 reported that of 384 meat samples collected from Addis Ababa, 39 (10.2%) were positive to E. coli O157:H7. They reported that beef (13.30%), sheep (9.40%) and goat (7.80%) meat samples had the highest prevalence of E. coli O157:H7. E. coli O157:H7 can colonize the intestinal tract of many livestock and during slaughtering may contaminate the carcass, work surfaces and material used for processing of meat products. With good hygienic practices during skinning and eviscerating, the rate of carcass contamination should be significantly below the carriage rate. High differences of the prevalence of E. coli O157:H7 strains in different studies is due to the fact that maybe types of samples, number of samples collected, method of sampling, method of experiment, place of sampling and weather and climate of geographical zone of sampling were different. Differences in the levels of health care and hygiene, accuracy in meat inspection, hygiene of the slaughterhouses and finally levels of personal hygiene are other factors which may affected the prevalence of E. coli O157:H7 in each region.
Another important issue which is not proper observed in some Iranian farms is antibiotic prescription. Unfortunately, Iranian veterinary practitioners prescribed antibiotics in a highly irregular and unauthorized manner without any attentions to the results of disk diffusion method. Therefore, it was not surprising that the E. coli O157:H7 strains of our investigation had the high prevalence of resistance against ampicillin, tetracycline, gentamicin, amikacin and sulfamethoxazole antibiotics, which was covered by presence of antibiotic resistance genes. Goncuoglu et al. (2010) 29 showed that prevalence of resistance of E. coli O157:H7 isolated from meat in Turkey against cephalothin, streptomycin, sulfamethoxazole and sulfonamides were 36.36%, 9.09%, 14.28% and 7.14%, respectively. Zhang et al. (2015) 27 reported that E. coli O157:H7 isolates of raw meat in China were highly resistant to penicillin (100%), chloramphenicol (64.29%) and ampicillin (57.14%) which was similar to our findings. Momtaz et al. (2013) 10 reported that the most commonly detected antibiotic resistance genes in the raw beef meat samples were blaSHV (70.14%), aac(3)-IV (64.17%), tetA (58.20%), aadA1 (49.25%), CITM (46.26%) and dfrA1 (43.28%) which was similar to our findings. They showed that resistance against penicillin and tetracycline were high, while resistance against ciprofloxacin and nitrofurantoin were low. Our results showed that all of the E. coli O157:H7 strains harbored resistance at-least against two antibiotic agents. Our results were similar with those of South Africa 30, Korea 31 and Mexico 32. Momtaz et al. (2013) 22 reported that aac(3)-IV (68.03%), sul1 (82.78%), blaSHV (56.55%), aadA1 (60.65%) and tetA (51.63%) and also resistance against tetracycline (86.88%), penicillin (100%), gentamycin (62.29%) and streptomycin (54.91%) were the most commonly reported antibiotic resistance-based finding of STEC strains of diarrheic patients which was similar to our results.
Chloramphenicol is a forbidden antibiotic. The high presences of resistance against chloramphenicol showed its irregular and unauthorized use in veterinary treatment and especially field of poultry in Iran. We found that the prevalence of resistance against chloramphenicol in the E. coli O157:H7 strains isolated from chicken and turkey meat samples were 23.07% and 12.50%, respectively with was entirely high. Practitioners of the field of poultry use from chloramphenicol antibiotic as a basic one. Therefore, in a very short period of time, antibiotic resistance will appear. High prevalence of resistance against chloramphenicol in the E. coli O157:H7 strains of meat samples have been reported from Iran 10, 22, USA 33, Turkey 28, UK 34 and Nigeria 35. High differences of the prevalence of antibiotic resistance in the E. coli O157:H7 strains in different studies is due to the fact that maybe availability of antibiotics, their cost and even idea of veterinarian for antibiotic prescription are different in each region. Therefore, various investigations reported different prevalence for antibiotic resistance. High prevalence of the tetA, CITM and aac(3)-IV antibiotic resistance genes and also high prevalence of resistance against tetracycline, ampicillin and gentamicin have also reported by other Iranian researchers 36, 37.
In conclusions, we identified a large number of antibiotic resistance genes and also antibiotic resistance in the E. coli O157:H7 strains isolated from bovine, ovine, caprine, camel, chicken, turkey and quail raw meat. The strains isolated from chicken, turkey and bovine meat samples, resistance against ampicillin, gentamicin and tetracycline antibiotics and finally presence of CITM, aac(3)-IV and tetA antibiotic resistance genes were the most commonly detected characters in the E. coli O157:H7 strains of raw meat. High prevalence of resistant E. coli O157:H7 bacteria in the samples showed insufficiency of meat inspection and also presence of cross contamination in Iranian slaughterhouses. Because of low levels of bacterial resistance against imipenem, cefotaxime, cotrimoxazole and streptomycin antibiotics, occurrence of food infections via consumption of meat contaminated with E. coli O157:H7 can be treated with their regular prescription. Complete cooking of meat before consumption can prevent from occurrence of E. coli O157:H7 infection in human.
The authors would like to thank Prof. Ebrahim Rahimi at the Department of Food Hygiene and Public Health, Islamic Azad University of Shahrekord, Shahrekord Iran and Prof. Afshin Akhondzadeh Basti at the Department of Food Hygiene and Quality Control, University of Tehran, Tehran, Iran for their important technical support.
| [1] | Gould, L.H., Walsh, K.A., Vieira, A.R., Herman, K., Williams, I.T., Hall, A.J. and Cole, D, ''Surveillance for foodborne disease outbreaks-United States, 1998-2008'', MMWR Surveill Summ, 62. 1-34. 2013. | ||
| In article | PubMed | ||
| [2] | Havelaar, A.H., Kirk, M.D., Torgerson, P.R., Gibb, H.J., Hald, T., Lake, R.J., Praet, N., Bellinger, D.C., De Silva, N.R. and Gargouri, N, “World Health Organization Global estimates and regional comparisons of the burden of foodborne disease in 2010”, PLoS Med, 12. e1001923. 2015. | ||
| In article | View Article PubMed | ||
| [3] | Control CfD and Prevention, “Surveillance for Foodborne Disease Outbreaks, United States, 2013, Annual Report”. Atlanta: US Department of Health and Human Services, 2014. | ||
| In article | |||
| [4] | Scallan, E., Hoekstra, R.M., Angulo, F.J., Tauxe, R.V., Widdowson, M.A., Roy, S.L., Jones, J.L. and Griffin, P.M, “Foodborne illness acquired in the United States-major pathogens”, Emerg Infect Dis, 17, 2011. | ||
| In article | View Article | ||
| [5] | Stewardson, A.J., Renzi, G., Maury, N., Vaudaux, C., Brassier, C., Fritsch, E., Pittet, D., Heck, M., van der Zwaluw, K. and Reuland, E.A, “Extended-Spectrum β-Lactamase-Producing Enterobacteriaceae in Hospital Food: A Risk Assessment”, Infection Control & Hospital Epidemiology, 35. 375-383. 2014. | ||
| In article | View Article PubMed | ||
| [6] | Luo, Y., Cui, S., Li, J., Yang, J., Lin, L., Hu, C., Jin, S., Ye, L., Zhao, Q. and Ma, Y, “Characterization of Escherichia coli isolates from healthy food handlers in hospital”, Microbial Drug Resistance, 17. 443-448. 2011. | ||
| In article | View Article PubMed | ||
| [7] | Dao, H.T.A. and Yen, P.T, “Study of Salmonella, Campylobacter, and Escherichia coli contamination in raw food available in factories, schools, and hospital canteens in Hanoi, Vietnam”, Annals of the New York Academy of Sciences, 1081. 262-265. 2006. | ||
| In article | View Article PubMed | ||
| [8] | Cooke, E.M., Kumar, P., Shooter, R., Rousseau, S. and Foulkes, A, “Hospital food as a possible source of Escherichia coli in patients”, The Lancet, 295. 436-437. 1970. | ||
| In article | View Article | ||
| [9] | Momtaz, H., Farzan, R., Rahimi, E., Safarpoor Dehkordi, F. and Souod, N, “Molecular characterization of Shiga toxin-producing Escherichia coli isolated from ruminant and donkey raw milk samples and traditional dairy products in Iran”, The Scientific World Journal, 2012. 1342. 2012. | ||
| In article | View Article | ||
| [10] | Momtaz, H., Dehkordi, F.S., Rahimi, E., Ezadi, H. and Arab, R, “Incidence of Shiga toxin-producing Escherichia coli serogroups in ruminant's meat”, Meat science, 95. 381-388. 2013. | ||
| In article | View Article PubMed | ||
| [11] | Dehkordi, F.S., Yazdani, F., Mozafari, J. and Valizadeh, Y, “Virulence factors, serogroups and antimicrobial resistance properties of Escherichia coli strains in fermented dairy products”, BMC research notes, 7. 1. 2014. | ||
| In article | View Article PubMed | ||
| [12] | Bai, X., Zhang, W., Tang, X., Xin, Y., Xu, Y., Sun, H., Luo, X., Pu, J., Xu, J. and Xiong, Y, “Shiga Toxin-Producing Escherichia coli in Plateau Pika (Ochotona curzoniae) on the Qinghai-Tibetan Plateau, China”, Frontiers in microbiology, 7. 2016. | ||
| In article | View Article | ||
| [13] | Dhaka, P., Vijay, D., Vergis, J., Negi, M., Kumar, M., Mohan, V., Doijad, S., Poharkar, K.V., Malik, S.S. and Barbuddhe, SB, “Genetic diversity and antibiogram profile of diarrhoeagenic Escherichia coli pathotypes isolated from human, animal, food samples and associated environmental sources”, Infection ecology & epidemiology, 6. 2016. | ||
| In article | View Article | ||
| [14] | Wang, J., Stanford, K., McAllister, T.A., Johnson, R.P., Chen, J., Hou, H., Zhang, G. and Niu, Y.D, “Biofilm Formation, Virulence Gene Profiles, and Antimicrobial Resistance of Nine Serogroups of Non-O157 Shiga Toxin-Producing Escherichia coli”, Foodborne pathogens and disease, 2016. | ||
| In article | View Article PubMed | ||
| [15] | Farshad, S., Ranijbar, R., Japoni, A., Hosseini, M., Anvarinejad, M. and Mohammadzadegan, R, “Microbial susceptibility, virulence factors, and plasmid profiles of uropathogenic Escherichia coli strains isolated from children in Jahrom, Iran”, Archives of Iranian Medicine, 15. 2012. | ||
| In article | View Article | ||
| [16] | Amézquita-López, B.A., Quiñones, B., Soto-Beltrán, M., Lee, B.G., Yambao, J.C., Lugo-Melchor, O.Y. and Chaidez, C, “Antimicrobial resistance profiles of Shiga toxin-producing Escherichia coli O157 and Non-O157 recovered from domestic farm animals in rural communities in Northwestern Mexico”, Antimicrobial resistance and infection control, 5. 1. 2016. | ||
| In article | View Article PubMed | ||
| [17] | Abdi, S., Ranjbar, R., Vala, M.H., Jonaidi, N., Bejestany, O.B. and Bejestany, F.B, “Frequency of bla TEM, bla SHV, bla CTX-M, and qnrA Among Escherichia coli Isolated From Urinary Tract Infection”, Archives of Clinical Infectious Diseases, 9. 2014. | ||
| In article | View Article | ||
| [18] | Momtaz, H., Karimian, A., Madani, M., Dehkordi, F.S., Ranjbar, R., Sarshar, M. and Souod, N, “Uropathogenic Escherichia coli in Iran: serogroup distributions, virulence factors and antimicrobial resistance properties”, Annals of clinical microbiology and antimicrobials, 12. 1. 2013. | ||
| In article | View Article PubMed | ||
| [19] | Sambrook, J. and Russell, D.W, “Molecular cloning: a laboratory manual. third”, Cold pring Harbor Laboratory Press, New York, 2001. | ||
| In article | |||
| [20] | Desmarchelier, P.M., Bilge, S.S., Fegan, N., Mills, L., Vary, J.C. and Tarr, P.I, “A PCR specific for Escherichia coli O157 based on the rfb locus encoding O157 lipopolysaccharide”, Journal of Clinical Microbiology, 36. 1801-1804. 1998. | ||
| In article | PubMed PubMed | ||
| [21] | Philpott, D. and Ebel, F, “E. coli: shiga toxin methods and protocols”, Springer Science & Business Media, 2003. | ||
| In article | View Article | ||
| [22] | Momtaz, H., Dehkordi, F.S., Hosseini, M.J., Sarshar, M. and Heidari, M, “Serogroups, virulence genes and antibiotic resistance in Shiga toxin-producing Escherichia coli isolated from diarrheic and non-diarrheic pediatric patients in Iran”, Gut pathogens, 5. 1. 2013. | ||
| In article | View Article PubMed | ||
| [23] | Wayne, P, “Clinical and Laboratory Standards Institute (CLSI) performance standards for antimicrobial disk diffusion susceptibility tests 19th ed”, approved standard, CLSI document M100-S19, 29. 2009. | ||
| In article | |||
| [24] | Mead, P.S., Slutsker, L., Dietz, V., McCaig, L.F., Bresee, J.S., Shapiro, C., Griffin, P.M. and Tauxe, R.V, “Food-related illness and death in the United States”, Emerging infectious diseases, 5. 607. 1999. | ||
| In article | View Article PubMed | ||
| [25] | Zarei, M., Basiri, N., Jamnejad, A. and Eskandari, M.H, “Prevalence of Escherichia coli O157: H7, Listeria monocytogenes and Salmonella spp. in beef, buffalo and lamb using multiplex PCR”, Jundishapur Journal of Microbiology, 6. 2013. | ||
| In article | View Article | ||
| [26] | Hessain, A.M., Al-Arfaj, A.A., Zakri, A.M., El-Jakee, J.K., Al-Zogibi, O.G., Hemeg, H.A. and Ibrahim, I.M, “Molecular characterization of Escherichia coli O157: H7 recovered from meat and meat products relevant to human health in Riyadh, Saudi Arabia”, Saudi journal of biological sciences, 22. 725-729. 2015. | ||
| In article | View Article PubMed | ||
| [27] | Zhang S, Zhu X, Wu Q, Zhang J, Xu X and Li H. Prevalence and characterization of Escherichia coli O157 and O157: H7 in retail fresh raw meat in South China. Annals of microbiology 2015; 65: 1993-1999. | ||
| In article | View Article | ||
| [28] | Bekele, T., Zewde, G., Tefera, G., Feleke, A. and Zerom, K, “Escherichia coli O157: H7 in raw meat in Addis Ababa, Ethiopia: prevalence at an abattoir and retailers and antimicrobial susceptibility”, International Journal of Food Contamination, 1. 4. 2014. | ||
| In article | View Article | ||
| [29] | Goncuoglu, M., Ormanci, F.S.B., Ayaz, N.D. and Erol, I, “Antibiotic resistance of Escherichia coli O157: H7 isolated from cattle and sheep”, Annals of microbiology, 60. 489-494. 2010. | ||
| In article | View Article | ||
| [30] | Iweriebor, B.C., Iwu, C.J., Obi, L.C., Nwodo, U.U. and Okoh, A,I, “Multiple antibiotic resistances among Shiga toxin producing Escherichia coli O157 in feces of dairy cattle farms in Eastern Cape of South Africa”, BMC microbiology, 15. 1. 2015. | ||
| In article | View Article PubMed | ||
| [31] | Kang, E., Hwang, S.Y., Kwon, K.H., Kim, K.Y., Kim, J.H. and Park, Y.H, “Prevalence and characteristics of Shiga toxin-producing Escherichia coli (STEC) from cattle in Korea between 2010 and 2011”, Journal of veterinary science, 15. 369-379. 2014. | ||
| In article | View Article PubMed | ||
| [32] | Castillo, F.Y.R., González, F.J.A., Garneau, P., Díaz, F.M., Barrera, A.L.G. and Harel, J, “Presence of multi-drug resistant pathogenic Escherichia coli in the San Pedro River located in the State of Aguascalientes, Mexico”, Frontiers in microbiology, 4. 2013. | ||
| In article | View Article | ||
| [33] | Tadesse, D.A., Zhao, S., Tong, E., Ayers, S., Singh, A., Bartholomew, M.J. and McDermott, P.F, “Antimicrobial drug resistance in Escherichia coli from humans and food animals, United States, 1950-2002”, Emerging infectious diseases, 18. 741. 2012. | ||
| In article | View Article PubMed | ||
| [34] | Schroeder, C.M., Zhao, C., DebRoy, C., Torcolini, J., Zhao, S., White, D.G., Wagner, D.D., McDermott, P.F., Walker, R.D. and Meng, J, “Antimicrobial resistance of Escherichia coli O157 isolated from humans, cattle, swine, and food”, Applied and Environmental Microbiology, 68. 576-581. 2002. | ||
| In article | View Article PubMed | ||
| [35] | Braoudaki, M. and Hilton, A.C, “Low level of cross-resistance between triclosan and antibiotics in Escherichia coli K-12 and E. coli O55 compared to E. coli O157”, FEMS microbiology letters, 235. 305-309. 2004. | ||
| In article | View Article PubMed | ||
| [36] | Hemmatinezhad, B., Khamesipour, F., Mohammadi, M., Safarpoor Dehkordi, F. and Mashak, Z, “Microbiological Investigation of O-Serogroups, Virulence Factors and Antimicrobial Resistance Properties of Shiga Toxin‐Producing Escherichia Coli Isolated from Ostrich, Turkey and Quail Meats”, Journal of Food Safety, 35. 491-500. 2015. | ||
| In article | View Article | ||
| [37] | Momtaz, H., Safarpoor Dehkordi, F., Taktaz, T., Rezvani, A. and Yarali, S, “Shiga toxin-producing Escherichia coli isolated from bovine mastitic milk: serogroups, virulence factors, and antibiotic resistance properties”, The Scientific World Journal, 2012. 1-9. 2012. | ||
| In article | |||
Published with license by Science and Education Publishing, Copyright © 2018 Zohreh Mashak
This work is licensed under a Creative Commons Attribution 4.0 International License. To view a copy of this license, visit
https://creativecommons.org/licenses/by/4.0/
| [1] | Gould, L.H., Walsh, K.A., Vieira, A.R., Herman, K., Williams, I.T., Hall, A.J. and Cole, D, ''Surveillance for foodborne disease outbreaks-United States, 1998-2008'', MMWR Surveill Summ, 62. 1-34. 2013. | ||
| In article | PubMed | ||
| [2] | Havelaar, A.H., Kirk, M.D., Torgerson, P.R., Gibb, H.J., Hald, T., Lake, R.J., Praet, N., Bellinger, D.C., De Silva, N.R. and Gargouri, N, “World Health Organization Global estimates and regional comparisons of the burden of foodborne disease in 2010”, PLoS Med, 12. e1001923. 2015. | ||
| In article | View Article PubMed | ||
| [3] | Control CfD and Prevention, “Surveillance for Foodborne Disease Outbreaks, United States, 2013, Annual Report”. Atlanta: US Department of Health and Human Services, 2014. | ||
| In article | |||
| [4] | Scallan, E., Hoekstra, R.M., Angulo, F.J., Tauxe, R.V., Widdowson, M.A., Roy, S.L., Jones, J.L. and Griffin, P.M, “Foodborne illness acquired in the United States-major pathogens”, Emerg Infect Dis, 17, 2011. | ||
| In article | View Article | ||
| [5] | Stewardson, A.J., Renzi, G., Maury, N., Vaudaux, C., Brassier, C., Fritsch, E., Pittet, D., Heck, M., van der Zwaluw, K. and Reuland, E.A, “Extended-Spectrum β-Lactamase-Producing Enterobacteriaceae in Hospital Food: A Risk Assessment”, Infection Control & Hospital Epidemiology, 35. 375-383. 2014. | ||
| In article | View Article PubMed | ||
| [6] | Luo, Y., Cui, S., Li, J., Yang, J., Lin, L., Hu, C., Jin, S., Ye, L., Zhao, Q. and Ma, Y, “Characterization of Escherichia coli isolates from healthy food handlers in hospital”, Microbial Drug Resistance, 17. 443-448. 2011. | ||
| In article | View Article PubMed | ||
| [7] | Dao, H.T.A. and Yen, P.T, “Study of Salmonella, Campylobacter, and Escherichia coli contamination in raw food available in factories, schools, and hospital canteens in Hanoi, Vietnam”, Annals of the New York Academy of Sciences, 1081. 262-265. 2006. | ||
| In article | View Article PubMed | ||
| [8] | Cooke, E.M., Kumar, P., Shooter, R., Rousseau, S. and Foulkes, A, “Hospital food as a possible source of Escherichia coli in patients”, The Lancet, 295. 436-437. 1970. | ||
| In article | View Article | ||
| [9] | Momtaz, H., Farzan, R., Rahimi, E., Safarpoor Dehkordi, F. and Souod, N, “Molecular characterization of Shiga toxin-producing Escherichia coli isolated from ruminant and donkey raw milk samples and traditional dairy products in Iran”, The Scientific World Journal, 2012. 1342. 2012. | ||
| In article | View Article | ||
| [10] | Momtaz, H., Dehkordi, F.S., Rahimi, E., Ezadi, H. and Arab, R, “Incidence of Shiga toxin-producing Escherichia coli serogroups in ruminant's meat”, Meat science, 95. 381-388. 2013. | ||
| In article | View Article PubMed | ||
| [11] | Dehkordi, F.S., Yazdani, F., Mozafari, J. and Valizadeh, Y, “Virulence factors, serogroups and antimicrobial resistance properties of Escherichia coli strains in fermented dairy products”, BMC research notes, 7. 1. 2014. | ||
| In article | View Article PubMed | ||
| [12] | Bai, X., Zhang, W., Tang, X., Xin, Y., Xu, Y., Sun, H., Luo, X., Pu, J., Xu, J. and Xiong, Y, “Shiga Toxin-Producing Escherichia coli in Plateau Pika (Ochotona curzoniae) on the Qinghai-Tibetan Plateau, China”, Frontiers in microbiology, 7. 2016. | ||
| In article | View Article | ||
| [13] | Dhaka, P., Vijay, D., Vergis, J., Negi, M., Kumar, M., Mohan, V., Doijad, S., Poharkar, K.V., Malik, S.S. and Barbuddhe, SB, “Genetic diversity and antibiogram profile of diarrhoeagenic Escherichia coli pathotypes isolated from human, animal, food samples and associated environmental sources”, Infection ecology & epidemiology, 6. 2016. | ||
| In article | View Article | ||
| [14] | Wang, J., Stanford, K., McAllister, T.A., Johnson, R.P., Chen, J., Hou, H., Zhang, G. and Niu, Y.D, “Biofilm Formation, Virulence Gene Profiles, and Antimicrobial Resistance of Nine Serogroups of Non-O157 Shiga Toxin-Producing Escherichia coli”, Foodborne pathogens and disease, 2016. | ||
| In article | View Article PubMed | ||
| [15] | Farshad, S., Ranijbar, R., Japoni, A., Hosseini, M., Anvarinejad, M. and Mohammadzadegan, R, “Microbial susceptibility, virulence factors, and plasmid profiles of uropathogenic Escherichia coli strains isolated from children in Jahrom, Iran”, Archives of Iranian Medicine, 15. 2012. | ||
| In article | View Article | ||
| [16] | Amézquita-López, B.A., Quiñones, B., Soto-Beltrán, M., Lee, B.G., Yambao, J.C., Lugo-Melchor, O.Y. and Chaidez, C, “Antimicrobial resistance profiles of Shiga toxin-producing Escherichia coli O157 and Non-O157 recovered from domestic farm animals in rural communities in Northwestern Mexico”, Antimicrobial resistance and infection control, 5. 1. 2016. | ||
| In article | View Article PubMed | ||
| [17] | Abdi, S., Ranjbar, R., Vala, M.H., Jonaidi, N., Bejestany, O.B. and Bejestany, F.B, “Frequency of bla TEM, bla SHV, bla CTX-M, and qnrA Among Escherichia coli Isolated From Urinary Tract Infection”, Archives of Clinical Infectious Diseases, 9. 2014. | ||
| In article | View Article | ||
| [18] | Momtaz, H., Karimian, A., Madani, M., Dehkordi, F.S., Ranjbar, R., Sarshar, M. and Souod, N, “Uropathogenic Escherichia coli in Iran: serogroup distributions, virulence factors and antimicrobial resistance properties”, Annals of clinical microbiology and antimicrobials, 12. 1. 2013. | ||
| In article | View Article PubMed | ||
| [19] | Sambrook, J. and Russell, D.W, “Molecular cloning: a laboratory manual. third”, Cold pring Harbor Laboratory Press, New York, 2001. | ||
| In article | |||
| [20] | Desmarchelier, P.M., Bilge, S.S., Fegan, N., Mills, L., Vary, J.C. and Tarr, P.I, “A PCR specific for Escherichia coli O157 based on the rfb locus encoding O157 lipopolysaccharide”, Journal of Clinical Microbiology, 36. 1801-1804. 1998. | ||
| In article | PubMed PubMed | ||
| [21] | Philpott, D. and Ebel, F, “E. coli: shiga toxin methods and protocols”, Springer Science & Business Media, 2003. | ||
| In article | View Article | ||
| [22] | Momtaz, H., Dehkordi, F.S., Hosseini, M.J., Sarshar, M. and Heidari, M, “Serogroups, virulence genes and antibiotic resistance in Shiga toxin-producing Escherichia coli isolated from diarrheic and non-diarrheic pediatric patients in Iran”, Gut pathogens, 5. 1. 2013. | ||
| In article | View Article PubMed | ||
| [23] | Wayne, P, “Clinical and Laboratory Standards Institute (CLSI) performance standards for antimicrobial disk diffusion susceptibility tests 19th ed”, approved standard, CLSI document M100-S19, 29. 2009. | ||
| In article | |||
| [24] | Mead, P.S., Slutsker, L., Dietz, V., McCaig, L.F., Bresee, J.S., Shapiro, C., Griffin, P.M. and Tauxe, R.V, “Food-related illness and death in the United States”, Emerging infectious diseases, 5. 607. 1999. | ||
| In article | View Article PubMed | ||
| [25] | Zarei, M., Basiri, N., Jamnejad, A. and Eskandari, M.H, “Prevalence of Escherichia coli O157: H7, Listeria monocytogenes and Salmonella spp. in beef, buffalo and lamb using multiplex PCR”, Jundishapur Journal of Microbiology, 6. 2013. | ||
| In article | View Article | ||
| [26] | Hessain, A.M., Al-Arfaj, A.A., Zakri, A.M., El-Jakee, J.K., Al-Zogibi, O.G., Hemeg, H.A. and Ibrahim, I.M, “Molecular characterization of Escherichia coli O157: H7 recovered from meat and meat products relevant to human health in Riyadh, Saudi Arabia”, Saudi journal of biological sciences, 22. 725-729. 2015. | ||
| In article | View Article PubMed | ||
| [27] | Zhang S, Zhu X, Wu Q, Zhang J, Xu X and Li H. Prevalence and characterization of Escherichia coli O157 and O157: H7 in retail fresh raw meat in South China. Annals of microbiology 2015; 65: 1993-1999. | ||
| In article | View Article | ||
| [28] | Bekele, T., Zewde, G., Tefera, G., Feleke, A. and Zerom, K, “Escherichia coli O157: H7 in raw meat in Addis Ababa, Ethiopia: prevalence at an abattoir and retailers and antimicrobial susceptibility”, International Journal of Food Contamination, 1. 4. 2014. | ||
| In article | View Article | ||
| [29] | Goncuoglu, M., Ormanci, F.S.B., Ayaz, N.D. and Erol, I, “Antibiotic resistance of Escherichia coli O157: H7 isolated from cattle and sheep”, Annals of microbiology, 60. 489-494. 2010. | ||
| In article | View Article | ||
| [30] | Iweriebor, B.C., Iwu, C.J., Obi, L.C., Nwodo, U.U. and Okoh, A,I, “Multiple antibiotic resistances among Shiga toxin producing Escherichia coli O157 in feces of dairy cattle farms in Eastern Cape of South Africa”, BMC microbiology, 15. 1. 2015. | ||
| In article | View Article PubMed | ||
| [31] | Kang, E., Hwang, S.Y., Kwon, K.H., Kim, K.Y., Kim, J.H. and Park, Y.H, “Prevalence and characteristics of Shiga toxin-producing Escherichia coli (STEC) from cattle in Korea between 2010 and 2011”, Journal of veterinary science, 15. 369-379. 2014. | ||
| In article | View Article PubMed | ||
| [32] | Castillo, F.Y.R., González, F.J.A., Garneau, P., Díaz, F.M., Barrera, A.L.G. and Harel, J, “Presence of multi-drug resistant pathogenic Escherichia coli in the San Pedro River located in the State of Aguascalientes, Mexico”, Frontiers in microbiology, 4. 2013. | ||
| In article | View Article | ||
| [33] | Tadesse, D.A., Zhao, S., Tong, E., Ayers, S., Singh, A., Bartholomew, M.J. and McDermott, P.F, “Antimicrobial drug resistance in Escherichia coli from humans and food animals, United States, 1950-2002”, Emerging infectious diseases, 18. 741. 2012. | ||
| In article | View Article PubMed | ||
| [34] | Schroeder, C.M., Zhao, C., DebRoy, C., Torcolini, J., Zhao, S., White, D.G., Wagner, D.D., McDermott, P.F., Walker, R.D. and Meng, J, “Antimicrobial resistance of Escherichia coli O157 isolated from humans, cattle, swine, and food”, Applied and Environmental Microbiology, 68. 576-581. 2002. | ||
| In article | View Article PubMed | ||
| [35] | Braoudaki, M. and Hilton, A.C, “Low level of cross-resistance between triclosan and antibiotics in Escherichia coli K-12 and E. coli O55 compared to E. coli O157”, FEMS microbiology letters, 235. 305-309. 2004. | ||
| In article | View Article PubMed | ||
| [36] | Hemmatinezhad, B., Khamesipour, F., Mohammadi, M., Safarpoor Dehkordi, F. and Mashak, Z, “Microbiological Investigation of O-Serogroups, Virulence Factors and Antimicrobial Resistance Properties of Shiga Toxin‐Producing Escherichia Coli Isolated from Ostrich, Turkey and Quail Meats”, Journal of Food Safety, 35. 491-500. 2015. | ||
| In article | View Article | ||
| [37] | Momtaz, H., Safarpoor Dehkordi, F., Taktaz, T., Rezvani, A. and Yarali, S, “Shiga toxin-producing Escherichia coli isolated from bovine mastitic milk: serogroups, virulence factors, and antibiotic resistance properties”, The Scientific World Journal, 2012. 1-9. 2012. | ||
| In article | |||
 and flicH7 (625 bp) genes, 2: Positive controls and 3: Negative control){kind=link}
