Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress 2023 EHA Congress 2023 ASCO Annual Meeting
Clinical Collections
Advances in Alzheimer’s

At a glance: The ONWARDS insulin icodec trials

A round-up of the ONWARDS phase 3 clinical trials evaluating the novel weekly insulin icodec in people with diabetes.
ADVANCED SEARCH
Log in
Top
Gut Pathogens
Published in: Gut Pathogens 1/2017

Open Access 01-12-2017 | Research

Occurrence of Salmonella enterica and Escherichia coli in raw chicken and beef meat in northern Egypt and dissemination of their antibiotic resistance markers

Authors: Amira A. Moawad, Helmut Hotzel, Omnia Awad, Herbert Tomaso, Heinrich Neubauer, Hafez M. Hafez, Hosny El-Adawy

Published in: Gut Pathogens | Issue 1/2017

Login to get access

Abstract

Background

The global incidence of foodborne infections and antibiotic resistance is recently increased and considered of public health concern. Currently, scarcely information is available on foodborne infections and ESBL associated with poultry and beef meat in Egypt.

Methods

In total, 180 chicken and beef meat samples as well as internal organs were collected from different districts in northern Egypt. The samples were investigated for the prevalence and antibiotic resistance of Salmonella enterica serovars and Escherichia coli. All isolates were investigated for harbouring class 1 and class 2 integrons.

Results

Out of 180 investigated samples 15 S. enterica (8.3%) and 21 E. coli (11.7%) were isolated and identified. S. enterica isolates were typed as 9 S. Typhimurium (60.0%), 3 S. Paratyphi A (20.0%), 2 S. Enteritidis (13.3%) and 1 S. Kentucky (6.7%). Twenty-one E. coli isolates were serotyped into O1, O18, O20, O78, O103, O119, O126, O145, O146 and O158. The phenotypic antibiotic resistance profiles of S. enterica serovars to ampicillin, cefotaxime, cefpodoxime, trimethoprim/sulphamethoxazole and tetracycline were 86.7, 80.0, 60.0, 53.3 and 40.0%, respectively. Isolated E. coli were resistant to tetracycline (80.9%), ampicillin (71.4%), streptomycin, trimethoprim/sulphamethoxazole (61.9% for each) and cefotaxime (33.3%). The dissemination of genes coding for ESBL and AmpC β-lactamase in S. enterica isolates included bla CTX-M (73.3%), bla TEM (73.3%) and bla CMY (13.3%). In E. coli isolates bla TEM, bla CTX-M and bla OXA were identified in 52.4, 42.9 and 14.3%, respectively. The plasmid-mediated quinolone resistance genes identified in S. enterica were qnrA (33.3%), qnrB (20.0%) and qnrS (6.7%) while qnrA and qnrB were detected in 33.3% of E. coli isolates. Class 1 integron was detected in 13.3% of S. enterica and in 14.3% of E. coli isolates. Class 2 integron as well as the colistin resistance gene mcr-1 was not found in any of E. coli or S. enterica isolates.

Conclusions

This study showed high prevalence of S. enterica and E. coli as foodborne pathogens in raw chicken and beef meat in Nile Delta, Egypt. The emergence of antimicrobial resistance in S. enterica and E. coli isolates is of public health concern in Egypt. Molecular biological investigation elucidated the presence of genes associated with antibiotic resistance as well as class 1 integron in S. enterica and E. coli.
Literature
1.
Helmy Y, El-Adawy H, Abdelwhab E. A comprehensive review of common bacterial, parasitic and viral zoonoses at the human–animal interface in Egypt. Pathogens. 2017;6:33.CrossRefPubMedCentral
2.
Pitout J, Laupland K. Extended-spectrum beta-lactamase-producing Enterobacteriaceae: an emerging public-health concern. Lancet Infect Dis. 2008;8:159–66.CrossRefPubMed
3.
Bush K, Jacoby GA. Updated functional classification of β-lactamases. Antimicrob Agents Chemother. 2010;54:969–76.CrossRefPubMed
4.
5.
Pfeifer Y, Cullik A, Witte W. Resistance to cephalosporins and carbapenems in Gram-negative bacterial pathogens. Int J Med Microbiol. 2010;300:371–9.CrossRefPubMed
6.
Abd-Elghany SM, Sallam KI, Abd-Elkhalek A, Tamura T. Occurrence, genetic characterization and antimicrobial resistance of Salmonella isolated from chicken meat and giblets. Epidemiol Infect. 2015;143:997–1003.CrossRefPubMed
7.
Gharieb RM, Tartor YH, Khedr MH. Non-typhoidal Salmonella in poultry meat and diarrhoeic patients: prevalence, antibiogram, virulotyping, molecular detection and sequencing of class I integrons in multidrug resistant strains. Gut Pathog. 2015;7:15–81.CrossRef
8.
Ahmed HA, El-Hofy FI, Shafik SM, Abdelrahman MA, Elsaid GA. Characterization of virulence-associated genes, antimicrobial resistance genes, and class 1 integrons in Salmonella enterica serovar Typhimurium isolates from chicken meat and humans in Egypt. Foodborne Pathog Dis. 2016;13:281–8.CrossRefPubMed
9.
Abdallah HM, Reuland EA, Wintermans BB, Al Naiemi N, Koek A, Abdelwahab AM, et al. Extended-spectrum β-lactamases and/or carbapenemases-producing Enterobacteriaceae isolated from retail chicken meat in Zagazig, Egypt. PLoS ONE. 2015;10:e0136052.CrossRefPubMedPubMedCentral
10.
Ahmed AM, Shimamoto T. Molecular analysis of multidrug resistance in Shiga toxin-producing Escherichia coli O157:H7 isolated from meat and dairy products. Int J Food Microbiol. 2015;193:68–73.CrossRefPubMed
11.
Andriole VT. The quinolones: past, present, and future. Clin Infect Dis. 2005113-19.
12.
Flach CF, Boulund F, Kristiansson E, Larsson DJ. Functional verification of computationally predicted qnr genes. Ann Clin Microbiol Antimicrob. 2013;12:34.CrossRefPubMedPubMedCentral
13.
Guan X, Xue X, Liu Y, Wang J, Wang Y, Wang K, et al. Plasmid-mediated quinolone resistance—current knowledge and future perspectives. J Int Med Res. 2013;41:20–30.CrossRefPubMed
14.
Robicsek A, Jacoby GA, Hooper DC. The worldwide emergence of plasmid-mediated quinolone resistance. Lancet Infect Dis. 2006;6:629–40.CrossRefPubMed
15.
Hanau-Bercot B, Podglajen I, Casin I, Collatz E. An intrinsic control element for translational initiation in class 1 integrons. Mol Microbiol. 2002;44:119–30.CrossRefPubMed
16.
Rowe-Magnus DA, Guerout AM, Mazel D. Bacterial resistance evolution by recruitment of super-integron gene cassettes. Mol Microbiol. 2002;43:1657–69.CrossRefPubMed
17.
Tzouvelekis L, Markogiannakis A, Piperaki E, Souli M, Daikos G. Treating infections caused by carbapenemase-producing Enterobacteriaceae. Clin Microbiol Infect Dis. 2014;20:862–72.CrossRef
18.
Sun S, Negrea A, Rhen M, Andersson D. Genetic analysis of colistin resistance in Salmonella enterica serovar Typhimurium. Antimicrob Agents Chemother. 2009;53:2298–305.CrossRefPubMedPubMedCentral
19.
Popoff MY, Bockemuhl J, Gheesling LL. Supplement 2002 (no. 46) to the Kauffmann–White scheme. Res Microbiol. 2004;155:568–70.CrossRefPubMed
20.
Bauer AW, Kirby WM, Sherris JC, Turck M. Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol. 1966;45:493–6.PubMed
21.
CLSI. Performance standards for antimicrobial susceptibility testing; twenty-first informational supplement: CLSI document M100-S21. CLSI. 2011;31:42–51.
22.
Maalej S, Meziou M, Rhimi F, Hammami A. Comparison of disc diffusion, Etest and agar dilution for susceptibility testing of colistin against Enterobacteriaceae. Lett Appl Microbiol. 2011;53:546–51.CrossRefPubMed
23.
Zhao S, Blickenstaff K, Bodeis-Jones S, Gaines SA, Tong E, McDermott PF. Comparison of the prevalences and antimicrobial resistances of Escherichia coli isolates from different retail meats in the United States, 2002 to 2008. Appl Environ Microbiol. 2012;78:1701–7.CrossRefPubMedPubMedCentral
24.
Liu Y, Wang Y, Walsh T, Yi LX, Zhang R, Spencer J, et al. Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: a microbiological and molecular biological study. Lancet Infect Dis. 2016;16:161–8.CrossRefPubMed
25.
Braun S, Monecke S, Thurmer A, Ruppelt A, Makarewicz O, Pletz M, et al. Rapid identification of carbapenemase genes in gram-negative bacteria with an oligonucleotide microarray-based assay. PLoS ONE. 2014;9:e102232.CrossRefPubMedPubMedCentral
26.
Ejo M, Garedew L, Alebachew Z, Worku W. Prevalence and antimicrobial resistance of Salmonella isolated from animal-origin food items in Gondar, Ethiopia. Biomed Res Int. 2016;4290506:15–20.
27.
Hernandez T, Sierra A, Rodriguez-Alvarez C, Torres A, Arevalo MP, Calvo M, et al. Salmonella enterica serotypes isolated from imported frozen chicken meat in the Canary islands. J Food Prot. 2005;68:2702–6.CrossRefPubMed
28.
Capita R, Alonso-Calleja C, Prieto M. Prevalence of Salmonella enterica serovars and genovars from chicken carcasses in slaughterhouses in Spain. J Appl Microbiol. 2007;103:1366–75.CrossRefPubMed
29.
Tibaijuka B, Molla B, Hildebrandt G, Kleer J. Occurrence of Salmonellae in retail raw chicken products in Ethiopia. Berl Munch Tierarztl Wochenschr. 2003;116:55–8.PubMed
30.
Ahmed AM, Shimamoto T. Isolation and molecular characterization of Salmonella enterica, Escherichia coli O157:H7 and Shigella spp. from meat and dairy products in Egypt. Int J Food Microbiol. 2014;169:M405–10.
31.
Bosilevac JM, Guerini MN, Kalchayanand N, Koohmaraie M. Prevalence and characterization of salmonellae in commercial ground beef in the United States. Appl Environ Microbiol. 2009;75:1892–900.CrossRefPubMedPubMedCentral
32.
Trongjit S, Angkititrakul S, Tuttle RE, Poungseree J, Padungtod P, Chuanchuen R. Prevalence and antimicrobial resistance in Salmonella enterica isolated from broiler chickens, pigs and meat products in Thailand-Cambodia border provinces. Microbiol Immunol. 2017;61:23–33.CrossRefPubMed
33.
Adeyanju GT, Ishola O. Salmonella and Escherichia coli contamination of poultry meat from a processing plant and retail markets in Ibadan, Oyo State, Nigeria. Springerplus. 2014;3:139.CrossRefPubMedPubMedCentral
34.
Lee GY, Jang HI, Hwang IG, Rhee MS. Prevalence and classification of pathogenic Escherichia coli isolated from fresh beef, poultry, and pork in Korea. Int J Food Microbiol. 2009;134:196–200.CrossRefPubMed
35.
Momtaz H, Dehkordi FS, Hosseini MJ, Sarshar M, 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 Pathog. 2013;5:1757–4749.CrossRef
36.
Wang S, Meng Q, Dai J, Han X, Han Y, Ding C, et al. Development of an allele-specific PCR assay for simultaneous sero-typing of avian pathogenic Escherichia coli predominant O1, O2, O18 and O78 strains. PLoS ONE. 2014;9:e96904.CrossRefPubMedPubMedCentral
37.
Alexandre M, Prado V, Ulloa MT, Arellano C, Rios M. Detection of enterohemorrhagic Escherichia coli in meat foods using DNA probes, enzyme-linked immunosorbent assay and polymerase chain reaction. J Vet Med B Infect Dis Vet Public Health. 2001;48:321–30.CrossRefPubMed
38.
Larkin C, Poppe C, McNab B, McEwen B, Mahdi A, Odumeru J. Antibiotic resistance of Salmonella isolated from hog, beef, and chicken carcass samples from provincially inspected abattoirs in Ontario. J Food Prot. 2004;67:448–55.CrossRefPubMed
39.
Perugini AG, Carullo MR, Esposito A, Caligiuri V, Capuano F, Galiero G, et al. Characterization of antimicrobial resistant Salmonella enterica serovars Enteritidis and Typhimurium isolates from animal and food in Southern Italy. Vet Res Commun. 2010;34:387–92.CrossRefPubMed
40.
Oueslati W, Rjeibi MR, Mhadhbi M, Jbeli M, Zrelli S, Ettriqui A. Prevalence, virulence and antibiotic susceptibility of Salmonella spp. strains, isolated from beef in Greater Tunis (Tunisia). Meat Sci. 2016;119:154–9.CrossRefPubMed
41.
M’Ikanatha NM, Sandt CH, Localio AR, Tewari D, Rankin SC, Whichard JM, et al. Multidrug-resistant Salmonella isolates from retail chicken meat compared with human clinical isolates. Foodborne Pathog Dis. 2010;7:929–34.CrossRefPubMed
42.
Brichta-Harhay DM, Arthur TM, Bosilevac JM, Kalchayanand N, Shackelford SD, Wheeler TL, et al. Diversity of multidrug-resistant Salmonella enterica strains associated with cattle at harvest in the United States. Appl Environ Microbiol. 2011;77:1783–96.CrossRefPubMedPubMedCentral
43.
Ahmed AM, Shimamoto T, Shimamoto T. Molecular characterization of multidrug-resistant avian pathogenic Escherichia coli isolated from septicemic broilers. Int J Med Microbiol. 2013;303:475–83.CrossRefPubMed
44.
Laarem M, Barguigua A, Nayme K, Akila A, Zerouali K, El Mdaghri N, et al. Occurrence of plasmid-mediated quinolone resistance and virulence genes in avian Escherichia coli isolates from Algeria. J Infect Dev Ctries. 2017;11:143–51.CrossRefPubMed
45.
Medina A, Horcajo P, Jurado S, De la Fuente R, Ruiz-Santa-Quiteria JA, Dominguez-Bernal G, et al. Phenotypic and genotypic characterization of antimicrobial resistance in enterohemorrhagic Escherichia coli and atypical enteropathogenic E. coli strains from ruminants. J Vet Diagn Investig. 2011;23:91–5.CrossRef
46.
Rasmussen MM, Opintan JA, Frimodt-Moller N, Styrishave B. Beta-lactamase producing Escherichia coli isolates in imported and locally produced chicken meat from Ghana. PLoS ONE. 2015;10:e0139706.CrossRefPubMedPubMedCentral
47.
Qiao J, Zhang Q, Alali WQ, Wang J, Meng L, Xiao Y, et al. Characterization of extended-spectrum β-lactamases (ESBLs)-producing Salmonella in retail raw chicken carcasses. Int J Food Microbiol. 2017;248:72–81.CrossRefPubMed
48.
Ahmed AM, Shimamoto T. Genetic analysis of multiple antimicrobial resistance in Salmonella isolated from diseased broilers in Egypt. Microbiol Immunol. 2012;56:254–61.CrossRefPubMed
49.
Folster JP, Tolar B, Pecic G, Sheehan D, Rickert R, Hise K, et al. Characterization of blaCMY plasmids and their possible role in source attribution of Salmonella enterica serotype Typhimurium infections. Foodborne Pathog Dis. 2014;11:301–6.CrossRefPubMedPubMedCentral
50.
Al-Gallas N, Abbassi MS, Gharbi B, Manai M, Ben Fayala MN, Bichihi R, et al. Occurrence of plasmid-mediated quinolone resistance determinants and rmtB gene in Salmonella enterica serovar Enteritidis and Typhimurium isolated from food-animal products in Tunisia. Foodborne Pathog Dis. 2013;10:813–9.CrossRefPubMed
51.
Wang Y, Yang B, Wu Y, Zhang Z, Meng X, Xi M, et al. Molecular characterization of Salmonella enterica serovar Enteritidis on retail raw poultry in six provinces and two National cities in China. Food Microbiol. 2015;46:74–80.CrossRefPubMed
52.
Zhang Z, Meng X, Wang Y, Xia X, Wang X, Xi M, et al. Presence of qnr, aac(6′)-Ib, qepA, oqxAB, and mutations in gyrase and topoisomerase in nalidixic acid-resistant Salmonella isolates recovered from retail chicken carcasses. Foodborne Pathog Dis. 2014;11:698–705.CrossRefPubMed
53.
Li L, Ye L, Kromann S, Meng H. Occurrence of extended-spectrum B-lactamases, plasmid-mediated quinolone resistance, and disinfectant resistance genes in Escherichia coli isolated from ready-to-eat meat products. Foodborne Pathog Dis. 2017;14:109–15.CrossRefPubMed
54.
Hansen KH, Bortolaia V, Nielsen CA, Nielsen JB, Schonning K, Agerso Y, et al. Host-specific patterns of genetic diversity among IncI1-Igamma and IncK plasmids encoding CMY-2 B-lactamase in Escherichia coli isolates from humans, poultry meat, poultry, and dogs in Denmark. Appl Environ Microbiol. 2016;82:4705–14.CrossRefPubMedPubMedCentral
55.
Jafari RA, Motamedi H, Maleki E, Ghanbarpour R, Mayahi M. Phylogenetic typing and detection of extended-spectrum B-lactamases in Escherichia coli isolates from broiler chickens in Ahvaz, Iran. Vet Res Forum. 2016;7:227–33.PubMedPubMedCentral
56.
Bagheri M, Ghanbarpour R, Alizade H. Shiga toxin and beta-lactamases genes in Escherichia coli phylotypes isolated from carcasses of broiler chickens slaughtered in Iran. Int J Food Microbiol. 2014;177:16–20.CrossRefPubMed
57.
Kaase M. Carbapenemases in gram-negative bacteria. Current data and trends of resistance resulting from the work of national reference centres. Bundesgesundheitsbl Gesundheitsforsch Gesundheitsschutz. 2012;55:1401–4.CrossRef
58.
de Oca SAM, Talavera-Rojas M, Soriano-Vargas E, Barba-Leon J, Vazquez-Navarrete J. Determination of extended spectrum β-lactamases/AmpC B-lactamases and plasmid-mediated quinolone resistance in Escherichia coli isolates obtained from bovine carcasses in Mexico. Trop Anim Health Prod. 2015;47:975–81.CrossRef
59.
Del Rio-Avila C, Rosario C, Arroyo-Escalante S, Carrillo-Casas EM, Diaz-Aparicio E, Suarez-Guemes F, et al. Characterisation of quinolone-resistant Escherichia coli of 1997 and 2005 isolates from poultry in Mexico. Br Poult Sci. 2016;57:494–500.CrossRefPubMed
60.
Guerra B, Soto S, Helmuth R, Mendoza MC. Characterization of a self-transferable plasmid from Salmonella enterica serotype Typhimurium clinical isolates carrying two integron-borne gene cassettes together with virulence and drug resistance genes. Antimicrob Agents Chemother. 2002;46:2977–81.CrossRefPubMedPubMedCentral
61.
Ahmed AM, Ishida Y, Shimamoto T. Molecular characterization of antimicrobial resistance in Salmonella isolated from animals in Japan. J Appl Microbiol. 2009;106:402–9.CrossRefPubMed
62.
Ahmed AM, Shimabukuro H, Shimamoto T. Isolation and molecular characterization of multidrug-resistant strains of Escherichia coli and Salmonella from retail chicken meat in Japan. J Food Sci. 2009;74:1750–3841.CrossRef
63.
Antunes P, Machado J, Peixe L. Characterization of antimicrobial resistance and class 1 and 2 integrons in Salmonella enterica isolates from different sources in Portugal. J Antimicrob Chemother. 2006;58:297–304.CrossRefPubMed
64.
Doumith M, Godbole G, Ashton P, Larkin L, Dallman T, Day M, et al. Detection of the plasmid-mediated mcr-1 gene conferring colistin resistance in human and food isolates of Salmonella enterica and Escherichia coli in England and Wales. J Antimicrob Chemother. 2016;71:2300–5.CrossRefPubMed
65.
Quesada A, Ugarte-Ruiz M, Iglesias M, Porrero M, Martinez R, Florez-Cuadrado D, et al. Detection of plasmid mediated colistin resistance (MCR-1) in Escherichia coli and Salmonella enterica isolated from poultry and swine in Spain. Res Vet Sci. 2016;105:134–5.CrossRefPubMed
66.
Jayol A, Nordmann P, Lehours P, Poirel L, Dubois V. Comparison of methods for detection of plasmid-mediated and chromosomally encoded colistin resistance in Enterobacteriaceae. Clin Microbiol Infect Dis. 2017;S1198-743X:30291–4.
67.
Seidavi A, Mirhosseini SZ, Shivazad M, Chamani M, Sadeghi AA, Pourseify R. Detection and investigation of Escherichia coli in contents of duodenum, jejunum, ileum and cecum of broilers at different ages by PCR. Asia-Pac J Mol Biol Biotechnol. 2010;18:321–6.
68.
Alvarez J, Sota M, Vivanco AB, Perales I, Cisterna R, Rementeria A, et al. Development of a multiplex PCR technique for detection and epidemiological typing of Salmonella in human clinical samples. J Clin Microbiol. 2004;42:1734–8.CrossRefPubMedPubMedCentral
69.
Ahmed AM, Motoi Y, Sato M, Maruyama A, Watanabe H, Fukumoto Y, et al. Zoo animals as reservoirs of gram-negative bacteria harboring integrons and antimicrobial resistance genes. Appl Environ Microbiol. 2007;73:6686–90.CrossRefPubMedPubMedCentral
Metadata
Title
Occurrence of Salmonella enterica and Escherichia coli in raw chicken and beef meat in northern Egypt and dissemination of their antibiotic resistance markers
Authors
Amira A. Moawad
Helmut Hotzel
Omnia Awad
Herbert Tomaso
Heinrich Neubauer
Hafez M. Hafez
Hosny El-Adawy
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Gut Pathogens / Issue 1/2017
Electronic ISSN: 1757-4749
DOI
https://doi.org/10.1186/s13099-017-0206-9

Other articles of this Issue 1/2017

Gut Pathogens 1/2017 Go to the issue

Research

Acute ileitis facilitates infection with multidrug resistant Pseudomonas aeruginosa in human microbiota-associated mice

Letter to the Editor

Colistin resistant Escherichia coli carrying mcr-1 in urban sludge samples: Dhaka, Bangladesh

Genome Report

Prevailing clone (ST69) of Vibrio cholerae O139 in India over 10 years

Genome Report

Comparative genomic analysis of Clostridium difficile ribotype 027 strains including the newly sequenced strain NCKUH-21 isolated from a patient in Taiwan

Research

Anaerobic adaptation of Mycobacterium avium subspecies paratuberculosis in vitro: similarities to M. tuberculosis and differential susceptibility to antibiotics

Research

Exposure to environmental microbiota explains persistent abdominal pain and irritable bowel syndrome after a major flood

ACC 2024 Congress Coverage

Heart Failure Video

Year in Review: Heart failure and cardiomyopathies

Watch now

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

16-04-2024 Type 2 Diabetes News

Incentivised to exercise

11-04-2024 Lifestyle Modifications News

New intervention for STEMI-related cardiogenic shock

10-04-2024 Myocardial Infarction News

» View more highlights on the ACC 2024 congress hub page

Image Credits