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

Epidemiological, molecular characterization and antibiotic resistance of Salmonella enterica serovars isolated from chicken farms in Egypt

Authors: Hanem El-Sharkawy, Amin Tahoun, Abd El-Galiel A. El-Gohary, Moshira El-Abasy, Fares El-Khayat, Trudi Gillespie, Yukio Kitade, Hafez M. Hafez, Heinrich Neubauer, Hosny El-Adawy

Published in: Gut Pathogens | Issue 1/2017

Login to get access

Abstract

Background

Salmonella is one of major causes of foodborne outbreaks globally. This study was conducted to estimate the prevalence, typing and antibiotic susceptibilities of Salmonella enterica serovars isolated from 41 broiler chicken farms located in Kafr El-Sheikh Province in Northern Egypt during 2014–2015. The clinical signs and mortalities were observed.

Results

In total 615 clinical samples were collected from broiler flocks from different organs (liver, intestinal content and gall bladder). Salmonella infection was identified in 17 (41%) broiler chicken flocks and 67 Salmonella isolates were collected. Recovered isolates were serotyped as 58 (86.6%) S. enterica serovar Typhimurium, 6 (9%) S. enterica serovar Enteritidis and 3 (4.5%) were non-typable. The significant high mortality rate was observed only in 1-week-old chicks. sopE gene was detected in 92.5% of the isolates which indicating their ability to infect humans. All S. enterica serovar Enteritidis isolates were susceptible to all tested antimicrobials. The phenotypically resistant S. enterica serovar Typhimurium isolates against ampicillin, tetracycline, sulphamethoxazole and chloramphenicol were harbouring BlaTEM, (tetA and tetC), (sul1 and sul3) and (cat1 and floR), respectively. The sensitivity rate of S. enterica serovar Typhimurium to gentamycin, trimethoprim/sulphamethoxazole and streptomycin were 100, 94.8, 89.7%, respectively. The silent streptomycin antimicrobial cassettes were detected in all Salmonella serovars. A class one integron (dfrA12, orfF and aadA2) was identified in three of S. enterica serovar Typhimurium strains.

Conclusions

To the best of our knowledge, this study considered first report discussing the prevalence, genotyping, antibiotic susceptibility and public health significance of S. enterica serovars in broilers farms of different ages in Delta Egypt. Further studies are mandatory to verify the location of some resistance genes that are within or associated with the class one integron.
Literature
1.
Hafez H. Salmonella infections in poultry: diagnosis and control. Period Biol. 2001;103:103–14.
2.
3.
Omwandho C, Kubota T. Salmonella enterica serovar Enteritidis: a mini-review of contamination routes and limitations to effective control. Jpn Agric Res Q. 2010;44:7–16.CrossRef
4.
Bäumler A, Tsolis R, Ficht T, Adams L. Evolution of host adaptation in Salmonella enterica. Infect Immun. 1998;66:4579–87.PubMedPubMedCentral
5.
Popoff M, Bockemühl J, Brenner F. Supplement 1998 (no. 42) to the Kauffmann–White scheme. Res Microbiol. 2000;151:63–5.CrossRefPubMed
6.
Abouzeed Y, Hariharan H, Poppe C, Kibenge F. Characterization of Salmonella isolates from beef cattle, broiler chickens and human sources on Prince Edward Island. Comp Immunol Microbiol Infect Dis. 2000;23:253–66.CrossRefPubMed
7.
Sheela R, Babu U, Mu J, Elankumaran S, Bautista D, Raybourne R, et al. Immune responses against Salmonella enterica serovar enteritidis infection in virally immunosuppressed chickens. Clin Diag Lab Immunol. 2003;10:670–9.
8.
Altekruse S, Bauer N, Chanlongbutra A, DeSagun R, Naugle A, Schlosser W, et al. Salmonella enteritidis in broiler chickens, United States, 2000–2005. Emerg Infect Dis. 2006;12:1848.CrossRefPubMedPubMedCentral
9.
Coble D, Sandford E, Ji T, Abernathy J, Fleming D, Zhou H, et al. Impacts of Salmonella enteritidis infection on liver transcriptome in broilers. Genesis. 2013;51:357–64.CrossRefPubMed
10.
Gast R. Salmonella infections and Paratyphoid infections. In: Calnek BW, editor. Diseases of Poultry. Ames: Iowa State University Press; 1997. p. 97–121.
11.
Hafez H. Salmonella infections in Turkeys. In: Barrow P, Methner U, editors. Salmonella in domestic animals. Wallingford: CABI Publishing; 2013. p. 193–220.CrossRef
12.
Kapperud G, Stenwig H, Lassen J. Epidemiology of Salmonella typhimurium O: 4–12 infection in Norway evidence of transmission from an avian wildlife reservoir. Am J Epidemiol. 1998;147:774–82.CrossRefPubMed
13.
OIE. Fowl typhoid and pullorum disease. In: Manual of standards for diagnostic tests and vaccines. 1996. p. 532–38.
14.
Shivaprasad H, Chin R. Pullorum disease and fowl typhoid American Association of Avian Pathologists. 2001.
15.
Majowicz S, Musto J, Scallan E, Angulo F, Kirk M, O’Brien S, et al. The global burden of nontyphoidal Salmonella gastroenteritis. Clin Infect Dis. 2010;50:882–9.CrossRefPubMed
16.
Newell D, Koopmans M, Verhoef L, Duizer E, Aidara-Kane A, Sprong H, et al. Food-borne diseases: the challenges of 20 years ago still persist while new ones continue to emerge. Int J Food Microbiol. 2010;139:S3–15.CrossRefPubMed
17.
Desmidt M, Ducatelle R, Haesebrouck F. Pathogenesis of Salmonella enteritidis phage type four after experimental infection of young chickens. Vet Microbiol. 1997;56:99–109.CrossRefPubMed
18.
Abd El-Ghany W, El-Shafii S, Hatem M. A survey on Salmonella species isolated from chicken flocks in Egypt. Asian J Anim Vet Adv. 2012;7:489–501.CrossRef
19.
Lister S. Salmonella enteritidis infection in broilers and broiler breeders. Vet Rec. 1988;123:350.CrossRefPubMed
20.
Padron M. Salmonella typhimurium outbreak in broiler chicken flocks in Mexico. Avian Dis. 1990;34:221–3.CrossRefPubMed
21.
Forsythe R, Ross W, Ayres J. Salmonellae recovery following gastro-intestinal and ovarian inoculation in the domestic fowl. Poult Sci. 1967;46:849–55.CrossRefPubMed
22.
Hogue A, White P, Guard-Petter J, Schlosser W, Gast R, Ebel E, et al. Epidemiology and control of egg-associated Salmonella Enteritidis in the United States of America [Review]. Rev Sci Tech. 1997;16:542–53.PubMed
23.
Barbour E, Jurdi L, Talhouk R, Qatanani M, Eid A, Sakr W, et al. Emergence of Salmonella enteritidis outbreaks in broiler chickens in the Lebanon: epidemiological markers and competitive exclusion control. Revue scientifique et technique. 1999;18:710–8.CrossRefPubMed
24.
Barrow P. Experimental infection of chickens with Salmonella enteritidis. Avian Pathol. 1991;20:145–53.CrossRefPubMed
25.
Rampling A, Upson R, Ward L, Anderson J, Peters E, Rowe B. Salmonella enteritidis phage type 4 infection of broiler chickens: a hazard to public health. Lancet. 1989;334:436–8.CrossRef
26.
Su L, Chiu C, Chu C, Ou J. Antimicrobial resistance in nontyphoid Salmonella serotypes: a global challenge. Clin Infect Dis. 2004;39:546–51.CrossRefPubMed
27.
Chen S, Zhao S, White D, Schroeder C, Lu R, Yang H, et al. Characterization of multiple-antimicrobial-resistant Salmonella serovars isolated from retail meats. Appl Environ Microbiol. 2004;70:1–7.CrossRefPubMedPubMedCentral
28.
Lynne A, Rhodes-Clark B, Bliven K, Zhao S, Foley S. Antimicrobial resistance genes associated with Salmonella enterica serovar Newport isolates from food animals. Antimicrob Agents Chemother. 2008;52:353–6.CrossRefPubMed
29.
Blair J, Webber M, Baylay A, Ogbolu D, Piddock L. Molecular mechanisms of antibiotic resistance. Nat Rev Microbiol. 2015;13:42–51.CrossRefPubMed
30.
Okeke I, Laxminarayan R, Bhutta Z, Duse A, Jenkins P, O’Brien T, et al. Antimicrobial resistance in developing countries. Part I: recent trends and current status. Lancet Infect Dis. 2005;5:481–93.CrossRefPubMed
31.
Ma M, Wang H, Yu Y, Zhang D, Liu S. Detection of antimicrobial resistance genes of pathogenic Salmonella from swine with DNA microarray. J Vet Diagn Investig. 2007;19:161–7.CrossRef
32.
Malorny B, Bunge C, Helmuth R. Discrimination of d-tartrate-fermenting and-nonfermenting Salmonella enterica subsp. enterica isolates by genotypic and phenotypic methods. J Clin Microbiol. 2003;41:4292–7.CrossRefPubMedPubMedCentral
33.
Agron P, Walker R, Kinde H, Sawyer S, Hayes D, Wollard J, et al. Identification by subtractive hybridization of sequences specific for Salmonella enterica serovar Enteritidis. Appl Environ Microbiol. 2001;67:4984–91.CrossRefPubMedPubMedCentral
34.
Alvarez J, Sota M, Vivanco A, 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
35.
O’Regan E, McCabe E, Burgess C, McGuinness S, Barry T, Duffy G, et al. Development of a real-time multiplex PCR assay for the detection of multiple Salmonella serotypes in chicken samples. BMC Microbiol. 2008;8:1.CrossRef
36.
Prager R, Rabsch W, Streckel W, Voigt W, Tietze E, Tschäpe H. Molecular properties of Salmonella enterica serotype paratyphi B distinguish between its systemic and its enteric pathovars. J Clin Microbiol. 2003;41:4270–8.CrossRefPubMedPubMedCentral
37.
Bauer A, Kirby W, Sherris J, Turck M. Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol. 1966;45:493.PubMed
38.
EUCAST. Breakpoint tables for interpretation of MICs and zone diameters. ed.: version 2015.
39.
Guard-Petter J, Parker C, Asokan K, Carlson R. Clinical and veterinary isolates of Salmonella enterica serovar Enteritidis defective in lipopolysaccharide O-chain polymerization. Appl Environ Microbiol. 1999;65:2195–201.PubMedPubMedCentral
40.
Shah D, Zhou X, Addwebi T, Davis M, Orfe L, Call D, et al. Cell invasion of poultry-associated Salmonella enterica serovar Enteritidis isolates is associated with pathogenicity, motility and proteins secreted by the type III secretion system. Microbiology. 2011;157:1428–45.CrossRefPubMedPubMedCentral
41.
Hafez H, Stadler A, Kosters J. Surveillance on Salmonella in turkey flocks and processing plants. Dtsch Tierarztl Wochenschr. 1997;104:33–5.PubMed
42.
Pieskus J, Franciosini M, Proietti PC, Reich F, Kazeniauskas E, Butrimaite-Ambrozeviciene C, et al. Preliminary investigations on Salmonella spp. incidence in meat chicken farms in Italy, Germany, Lithuania and the Netherlands. Int J Poult Sci. 2008;7:813–7.CrossRef
43.
Snow L, Davies R, Christiansen K, Carrique-Mas J, Cook A, Teale C, et al. Survey of the prevalence of Salmonella on commercial broiler farms in the United Kingdom, 2005/06. Vet Rec. 2008;163:649–54.CrossRefPubMed
44.
Van Hoorebeke S, Van Immerseel F, Schulz J, Hartung J, Harisberger M, Barco L, et al. Determination of the within and between flock prevalence and identification of risk factors for Salmonella infections in laying hen flocks housed in conventional and alternative systems [Research Support, Non-U.S. Gov't]. Prev Vet Med. 2010;94:94–100.CrossRefPubMed
45.
Van Overbeke I, Duchateau L, De Zutter L, Albers G, Ducatelle R. A comparison survey of organic and conventional broiler chickens for infectious agents affecting health and food safety. Avian Dis. 2006;50(2):196–200.
46.
47.
Clayton D, Bowen A, Hulme S, Buckley A, Deacon V, Thomson N, et al. Analysis of the role of 13 major fimbrial subunits in colonisation of the chicken intestines by Salmonella enterica serovar Enteritidis reveals a role for a novel locus. BMC Microbiol. 2008;8:1.CrossRef
48.
Girón J. Role of flagella in mucosal colonization. Colonization of mucosal surfaces. Boston: American Society of Microbiology; 2005. p. 213–36.CrossRef
49.
Tahoun A, Jensen K, Corripio-Miyar Y, McAteer S, Corbishley A, Mahajan A, et al. Functional analysis of bovine TLR5 and association with IgA responses of cattle following systemic immunisation with H7 flagella. Vet Res. 2015;46:1.CrossRef
50.
Hopkins K, Threlfall E. Frequency and polymorphism of sopE in isolates of Salmonella enterica belonging to the ten most prevalent serotypes in England and Wales. J Med Microbiol. 2004;53:539–43.CrossRefPubMed
51.
Rahman H, Streckel W, Prager R, Tschape H. Presence of sopE gene and its phenotypic expression among different serovars of Salmonella isolated from man and animals. Indian J Med Res. 2004;120:35–8.PubMed
52.
Prager R, Mirold S, Tietze E, Strutz U, Knuppel B, Rabsch W, et al. Prevalence and polymorphism of genes encoding translocated effector proteins among clinical isolates of Salmonella enterica. Int J Med Microbiol. 2000;290:605–17.CrossRefPubMed
53.
Han J, Gokulan K, Barnette D, Khare S, Rooney A, Deck J, et al. Evaluation of virulence and antimicrobial resistance in Salmonella enterica serovar Enteritidis isolates from humans and chicken- and egg-associated sources. Foodborne Pathog Dis. 2013;10:1008–15.CrossRefPubMed
54.
Gorham S, Kadavil K, Lambert H, Vaughan E, Pert B, Abel J. Persistence of Salmonella enteritidis in young chickens. Avian Pathol. 1991;20:433–7.CrossRefPubMed
55.
Bolder N, Janss L, Putirulan F, Wagenaar J. Resistance of broiler outbred lines to infection with Salmonella enteritidis. Avian Pathol. 2002;31:581–7.CrossRefPubMed
56.
Zishiri O, Mkhize N, Mukaratirwa S. Prevalence of virulence and antimicrobial resistance genes in Salmonella spp. isolated from commercial chickens and human clinical isolates from South Africa and Brazil. Onderstepoort J Vet Res. 2016;83:e1–11.CrossRefPubMed
57.
Maynard C, Fairbrother J, Bekal S, Sanschagrin F, Levesque R, Brousseau R, et al. Antimicrobial resistance genes in enterotoxigenic Escherichia coli O149: K91 isolates obtained over a 23-year period from pigs. Antimicrob Agents Chemother. 2003;47:3214–21.CrossRefPubMedPubMedCentral
58.
59.
60.
Yang H, Byelashov O, Geornaras I, Goodridge L, Nightingale K, Belk K, et al. Presence of antibiotic-resistant commensal bacteria in samples from agricultural, city, and national park environments evaluated by standard culture and real-time PCR methods. Can J Microbiol. 2010;56:761–70.CrossRefPubMed
61.
Dawes F, Kuzevski A, Bettelheim K, Hornitzky M, Djordjevic S, Walker M. Distribution of class 1 integrons with IS 26-mediated deletions in their 3′-conserved segments in Escherichia coli of human and animal origin. PLoS ONE. 2010;5:e12754.CrossRefPubMedPubMedCentral
62.
Randall L, Cooles S, Osborn M, Piddock L, Woodward M. Antibiotic resistance genes, integrons and multiple antibiotic resistance in thirty-five serotypes of Salmonella enterica isolated from humans and animals in the UK. J Antimicrob Chemother. 2004;53:208–16.CrossRefPubMed
63.
Boerlin P, Travis R, Gyles C, Reid-Smith R, Lim N, Nicholson V, et al. Antimicrobial resistance and virulence genes of Escherichia coli isolates from swine in Ontario. Appl Environ Microbiol. 2005;71:6753–61.CrossRefPubMedPubMedCentral
64.
Fonseca E, Mykytczuk O, Asensi M, Reis E, Ferraz L, Paula F, et al. Clonality and antimicrobial resistance gene profiles of multidrug-resistant Salmonella enterica serovar infantis isolates from four public hospitals in Rio de Janeiro, Brazil. J Clin Microbiol. 2006;44:2767–72.CrossRefPubMedPubMedCentral
65.
Zhao S, White D, Ge B, Ayers S, Friedman S, English L, et al. Identification and characterization of integron-mediated antibiotic resistance among Shiga toxin-producing Escherichia coli isolates. Appl Environ Microbiol. 2001;67:1558–64.CrossRefPubMedPubMedCentral
Metadata
Title
Epidemiological, molecular characterization and antibiotic resistance of Salmonella enterica serovars isolated from chicken farms in Egypt
Authors
Hanem El-Sharkawy
Amin Tahoun
Abd El-Galiel A. El-Gohary
Moshira El-Abasy
Fares El-Khayat
Trudi Gillespie
Yukio Kitade
Hafez M. Hafez
Heinrich Neubauer
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/s13099-017-0157-1

Other articles of this Issue 1/2017

Gut Pathogens 1/2017 Go to the issue

Research

Toll-like receptor-4 differentially mediates intestinal and extra-intestinal immune responses upon multi-drug resistant Pseudomonas aeruginosa association of IL10−/− mice with chronic colitis

Research

Single-nucleotide polymorphism typing analysis for molecular subtyping of Salmonella Tennessee isolates associated with the 2007 nationwide peanut butter outbreak in the United States

Research

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

Research

Multiple etiologies of infectious diarrhea and concurrent infections in a pediatric outpatient-based screening study in Odisha, India

Research

Genetic variants of Helicobacter pylori type IV secretion system components CagL and CagI and their association with clinical outcomes

Correction

Correction to: CRISPR-like sequences in Helicobacter pylori and application in genotyping

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