Antimicrobial Resistance and Characterization of
Salmonellae Isolated From Chicken Meat and Its Products in Mansoura City, Egypt
AlaaEldin M.A. Morshdy1
, Boshra M. Nahla2*
, Saleh Shafik2
, and Mohamed A. Hussein1
1Food Control Dept., Faculty of Vet. Medicine, Zagazig University, Zagazig, 44519, Egypt.
2Animal Health Research Institute, Mansoura Lab., Mansoura, 35511, Egypt.
Purpose: This research aimed to evaluate the rate of resistance to antimicrobials and the recognition of Salmonella strains virulence-related genes in chicken meat and its products collected from various shops for poultry, and supermarkets with varying degrees of hygiene in Mansoura City, Egypt.
Methods: Three hundred chicken meat and its products samples were streaked on XLD agar plates followed by biochemical and serological identification of the isolates. 43 isolates from all examined samples were identified as Salmonella, assayed for susceptibility to 14 antimicrobials by the single diffusion method.
Results: The antimicrobial resistance percentages for the Salmonella isolates was the highest for streptomycin (100%) and lowest for gentamicin (2.3%). Out of the forty three isolates of Salmonella, thirty six (83.72%) displayed multiple antimicrobial resistance (MAR) for 3 or more antimicrobials. PCR identification of virulence genes for Salmonella strains showed that S. enteritidis, S. typhimurium,S. papuana,S.infantis, andS.virchowserovars were positive for stn, hilA and fimH genes. S. kentucky, S. wingrove, andS. bargnyserovars were positiveforhilA and fimH genes. S. tamaleserovarwas found to be positive forfimHandstngenes.
S.anatumserovarwas found to be positive forhilAandstngenes. S. larochelleserovar wasfound to be positive forfimH gene. S. typhimurium, S. kentucky, S. enteritidis, S. tamale, S. papuana, S. wingrove, S. anatum, S.
virchow, and S. larochelleserovars were positive for sopAgene.
Conclusion: The higher contamination of different chicken meat and its products with multidrug-resistant Salmonella indicates improper hygienic measures. Also, the higher MAR index and presence of virulence-related genes in Salmonella isolates has high risk potential for consumers.
Antimicrobial resistance, Salmonella, Chicken meat, Virulence genes, MAR.
Chicken and chicken products provide high biological value animal protein for consumers of all ages, where they provide all the necessary essential amino acids, a significant proportion of fatty acids that are unsaturated(Marangoni et al. 2015). Moreover, chicken meat continues to be incriminated in human salmonellosis outbreaks (Ravel et al. 2009). All chicken edible products are exposed to contamination from many sources inside and outside of the animal during the various stages of slaughter and processing. The detection of Salmonellae in the chicken production chain is therefore of great concern, particularly at retail level.
Owing to the appearance and spreading of antimicrobial-resistant and possibly more strains that are pathogenic, Salmonella is increasingly concerned (Furuya and Lowy 2006; Baker et al. 2018). Inappropriate use of antimicrobial agents as medicinal or preventative agents and its use for promotion of the growth in animal development can be the reason for the increase in resistant strains.
Effective antimicrobial agents are necessary in severe cases of human salmonellosis. Antimicrobial-resistant Salmonella strains are highly risky because they can impair the successful treatment for human salmonellosis (Berrang et al. 2009).
Many of the Salmonella strains expressed multiple virulence factors that
promote the pathogenicity and establish the method of transmission to the target
hosts and the severity of the infection (Hensel 2004). The objective of this
research was to recognize the rate of resistance to antimicrobials and the
recognition of Salmonella strains virulence-related genes in chicken meat and its
Results and Discussion
The obtained results in Table (1) revealed that forty-three isolates from all examined samples were identified as Salmonella. Among the isolates of Salmonella, eleven various serotypes have been identified.S. typhimurium (23.26%) was the most prevalent, thenS. kentucky (18.6%), S. enteritidis (16.28%), S. tamale (11.63%), S. infantis (6.98%), S. papuana (6.98%), S.
wingrove (4.65%), S. bargny (4.65%), S. Larochelle(2.33%), S. virchow (2.33%), and S. anatum(2.33%). These results were comparable to the findings provided by (Abd-Elghany et al. 2015)and (Morshdy et al. 2015).
The high incidence of Salmonellae in chicken and chicken products reflected the public health hazards that could result from subsequent mishandling, improper cooking, and cross-contamination.
The isolated 43 Salmonella strains were assayed for susceptibility to 14 antimicrobials as displayed in Table (2). The antimicrobial resistance percentages for the Salmonella isolates was the highest for streptomycin (100%) followed by erythromycin (90.7%), norocillin (83.7%), cephalothin (72.1%), penicillin G (69.8%), nalidixic acid (62.8%), cephradine (51.1%), sulphamethoxazol (37.2%), clindamycin (32.5%), tetracycline (20.9%), ampicillin (11.6%), amikacin (9.3%), doxycycline (4.7%), and gentamicin (2.3%).
Antimicrobial resistance profile ofthe isolated 43 Salmonella strains revealed in Table (3). Out of Salmonella 43 isolates, 36 (83.72%) showed multiple antimicrobial resistance (MAR) for 3 or more antimicrobials. It was clear that the MAR index ranged from 1 to 0.071 with an average of 0.469. Multiple antimicrobial resistant Salmonella is recognized as an environmental hazard to the food supply and human health.
Nearly similar results were recorded by (Abd-Elghany et al. 2015).Higher
results of 100% multi-resistant Salmonella strains were isolated by
(Carramiñana et al. 2004) fromavian slaughterhouse in Spain, (KasimogluDogru, Ayaz, and Gencay 2010) from chicken carcasses in Turkey, (Shrestha et al. 2010) from poultry in Nepal, (Yildirim et al. 2011) from raw chicken carcasses in Turkey, and (Álvarez-Fernández et al. 2012) from poultry in Spain. Also, (Abd-Elghany et al. 2015) recorded 92·8% isolated multi- resistant strains of Salmonella from chickens and giblets in Egypt with a MAR index average of 0.582.
Lower results of multi-resistant Salmonella strains were isolated by (Nastasi, Mammina, and Cannova 2000) with a percentage of 2.3% in Southern Italy,(Antunes et al. 2003)with a percentage of 75% from poultry products in Portugal,(Abdellah et al. 2009)with a percentage of 75.43% in carcasses and giblets of chicken in Morocco, and 65.2% in Korea from poultry (Hur et al.
Nearly 90% of antimicrobials used in poultry, provided either prophylactically at subtherapeutic concentrations or to promote growth. Antimicrobial usage has long been documented to modify the genes of antimicrobial resistance. The microbial population encoded (resistome) and the influences of resistant bacteria persists for decades after antimicrobial usages has ended (Sommer and Dantas 2011).
The evidence that S. typhimurium has been among the serovars that have the highest meanantimicrobial resistance in this research is a disturbingreport, because S. typhimurium has more significant effects onhuman health than other serotypes of Salmonella.
Results shown in Table (4) revealed PCR identification of enterotoxin (stn),
hyper-invasive locus (hilA), and fimbrial (fimH) virulenceSalmonella genes. The
results showed thatS. enteritidis,S. typhimurium,S. papuana,S.infantis,
andS.virchowserovars were positive for stn, hilA and fimH genes. S. kentucky, S.
wingrove, andS. bargnyserovars were positiveforhilA and fimH genes. S.
tamaleserovarhadstnand fimH genes. S.anatumserovarhadstnand hilA genes. S.
larochelleserovarhad the fimH gene.
Results shown in Table (4) revealed PCR identification of sopA virulence gene of Salmonella species. The results showed that S. typhimurium, S. kentucky, S.
enteritidis, S. tamale, S. papuana,S. wingrove, S. anatum, S. virchow, and S.
larochelleserovars were positive for sopAgene. From the other side, S. infantis, and S. bargnyserovars were negative for sopA gene.
Comparable results have been reported in other studies, including (EL-Hanafy 2019) who found that S. enteritidis, S. kentucky and S. typhimurium were positive for stn, hilA and fimH genes, S. infantis and S. takoradi were positive for fimH gene, and S. papuana was positive for hilA gene, (Abd-Elghany et al.
2015) who reported that S. typhimurium,S. enteritidis, S. kentucky, S.
anatum,andS. virchow were positive for stn gene, and (Ahmed, El-Hofy, and Shafik 2016) who recorded that stn gene was identified in all isolates of S.
typhimurium of human and chicken origin at Mansoura city, Egypt.
Detection of genes of virulence in isolated Salmonella strains clarified the high prevalence of related virulence genes among isolated strains and added extraevidence of the hazard of virulent salmonellosis posed by chicken and its products to humans.
Conclusion and Recommendations
These results have established that chicken meat is a major multi-resistant Salmonella reservoir, and concluded that effective antimicrobial treatment of salmonellosis caused by chicken-origin strains is difficult to accomplish.
Chicken meat and its products therefore pose a major concern for the health of
the public, and this directs for proper control of antimicrobials to minimize the
inappropriate usage of antimicrobial drugs in the food sector. To ensure food safety before consumption, an improper method of cooking of chicken meat and inadequate hygiene procedures before consumption should be avoided.
Materials and Methods (1) Samples Collection
A sum of 300 samples of chicken meat and its products including raw thigh, frozen thigh, raw breast, frozen breast, gizzard, liver, heart, pane, luncheon, and burger (30 of each) were collected from various poultry shops and supermarkets with varying hygiene levels in Mansoura, Egypt. Samples collected were packed, described, transported to the ice box as quickly as possible and processed at the Research lab of Animal Health Research Institute, Mansoura.
(2)Isolation and Identification of Salmonellae
The applied technique was recommended by (Vassiliadis 1983).Twenty five grams of every hard sample were homogenised into 225 ml of buffered peptone water (BPW) under aseptic conditions for 2 min. by using sterile homogenizer.
All of the samples were incubated at 35˚ C for 24 ± 2 hours. One ml from the
pre-enrichment was added to 10 ml of the Rappaport Vassiliadis (RV)
enrichment broth and was incubated at 41 ± 1˚ C for 24 hours. Loopfuls of RV
broth enrichment were independently streaked onto xylose lysine deoxycholate
(XLD) agar and were incubated at 37˚ C for 24 hours. Two or three of typical or
suspected colonies (red colonies with or without a black centre on XLD) were
chosen from every selective medium and were streaked onto nutrient agar slope
which incubated at 37˚ C for 24 hours for more identification. Suspected isolates
of Salmonella organisms were subjected to morphological identification
(International Standards Organization “ISO”, 2013), biochemical
identification (Holt 1984)and serological identification(Kauffman 1974).
(3) Antibiotic Resistance of isolated Salmonellae species (Antibiogramme) Susceptibility to antimicrobials has been evaluated viathe single diffusion method in accordance with (Srivani 2011) for Salmonellae. Discs of sensitivity with different concentrations have been used to evaluate the susceptibility of the isolated Salmonella strains (Oxoid Limited, Basingstoke, Hampshire, UK).
The Multiple Antibiotic Resistance Index (MAR) for every strain was determined on the basis of the formula specified by Singh et al. (2010) as follows:
MAR index= Resistance No. (Isolates categorized as intermediate were assumed to be sensitive to MAR index)/Total No. of antibiotics tested.
(4) Polymerase Chain Reaction (PCR) for isolated Salmonellae species
• Sequences of primers used for PCR identification:
Implementation of PCR for virulence factors identification for Enterotoxin (stn), hyper-invasive locus (hilA), fimbrial (fimH) and (sopA) genes was conducted essentially by the use of Primers (Pharmacia Biotech) as seen in the following Table. DNA Extraction using QIA amp kit by the method of (Shah et al. 2009):
gene Oligonucleotide sequence (5′ → 3′) Product
size (bp) References stn (F) 5′ CTTTGGTCGTAAAATAAGGCG ′3
260 (Makino et al. 1999) stn (R) 5′ TGCCCAAAGCAGAGAGATTC ′3
hilA (F) 5′ CTGCCGCAGTGTTAAGGATA ′3
497 (Guo, Chen, and Beuchat 2000) hilA (R) 5′ CTGTCGCCTTAATCGCATGT ′3
fimH (F) 5′ GGA TCC ATG AAA ATA TAC TC ′3
1008 (Menghistu 2009) fimH (R) 5′ AAG CTT TTA ATC ATA ATC GAC TC ′3
sopA (F) 5′ TGGACTGAGAACGCTGTGGA ′3
207 (Elabed et al. 2016) sopA (R) 5′ GTGGGCCAGTACGCTTACCA ′3
• DNA Amplification
Multiplex PCR for amplification of stn, hilA, and fimH virulence genes (Singh et al. 2010) and sopAgene (Elabed et al. 2016).
Conflict of Interest
Neither of the authors have had any conflicts of interest to specify.
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List of Tables
Table 1. Distribution of Salmonella strains (n = 43) among chicken meat and its products samples (30 of each).
T= thigh, B=breast, G=gizzard, L=liver, H=heart, P=pane, L=luncheon, B=burger, r=raw, and f= frozen.
Serotypes Tr Tf Br Bf G L H P L B Total No. %
S. typhimurium 3 1 1 - 2 1 - 1 1 - 10 23.26
S. kentucky 2 1 1 - 1 2 - 1 - - 8 18.6
S. enteritidis 1 - - - 4 1 1 - - - 7 16.28
S. tamale 1 2 - - - - 1 1 - - 5 11.63
S. infantis - - - 1 - - - - 1 1 3 6.98
S. papuana - 1 - 1 1 - - - 3 6.98
S. wingrove - - - 1 1 - - - 2 4.65
S. bargny - - - 1 1 - - 2 4.65
S. larochelle - - 1 - - - 1 2.33
S. virchow - - - - 1 - - - 1 2.33
S. anatum - - - 1 - 1 2.33
Table 2. Antimicrobial susceptibility of Salmonella strains isolated from the examined chicken meat and its products samples (n=43)
Sa Ib Rc
NO % NO % NO %
Streptomycin (S) - - - - 43 100
Erythromycin (E) - - 4 9.3 42 90.7
Norocillin (NO) 2 4.7 5 11.6 36 83.7
Cephalothin (CN) 7 16.3 5 11.6 31 72.1
Penicillin G (P) 10 23.2 3 7.0 30 69.8
Nalidixic acid (NA) 14 32.5 2 4.7 27 62.8
Cephradine (CE) 18 41.9 3 7.0 22 51.1
(SXT) 23 53.5 4 9.3 16 37.2
Clindamycin (CL) 29 67.4 - - 14 32.5
Tetracycline (T) 33 76.7 1 2.3 9 20.9
Ampicillin (AM) 35 81.4 3 7.0 5 11.6
Amikacin (AK) 37 86.0 2 4.7 4 9.3
Doxycycline (DO) 38 88.3 3 7.0 2 4.7
Gentamicin (G) 41 95.4 1 2.3 1 2.3
S: Susceptiblea I: Intermediate susceptibilityb R: Resistantc
Table 3. Antimicrobial resistance profile of Salmonella strains isolated from the examined chicken meat and its products samples (n=43).
strains Antimicrobial resistance profile MARo index 1 S. typhimurium Sa, Eb, NOc, CNd, Pe, NAf, CEg, SXTh, CLi, Tj, AMk,
AKl, DOm, Gn
2 S. typhimurium Sa, Eb, NOc, CNd, Pe, NAf, CEg, SXTh, CLi, Tj, AMk 0.786 3 S. typhimurium Sa, Eb, NOc, CNd, Pe, NAf, CEg, SXTh, CLi 0.643 4 S. typhimurium Sa, Eb, NOc, CNd, Pe, NAf, CEg, SXTh, CLi 0.643 5 S. typhimurium Sa, Eb, NOc, CNd, Pe, NAf, CEg 0.500 6 S. typhimurium Sa, Eb, NOc, CNd, Pe, NAf 0.428
7 S. typhimurium Sa, Eb, NOc, CNd, Pe 0.357
8 S. typhimurium Sa, Eb, NOc 0.214
9 S. typhimurium Sa, Eb 0.143
10 S. typhimurium Sa, Eb 0.143
11 S. kentucky Sa, Eb, NOc, CNd, Pe, NAf, CEg, SXTh, CLi, Tj, AMk, AKl, DOm
12 S. kentucky Sa, Eb, NOc, CNd, Pe, NAf, CEg, SXTh, CLi, Tj 0.714 13 S. kentucky Sa, Eb, NOc, CNd, Pe, NAf, CEg, SXTh 0.571 14 S. kentucky Sa, Eb, NOc, CNd, Pe, NAf, CEg 0.500
15 S. kentucky Sa, Eb, NOc, CNd, Pe 0.357
16 S. kentucky Sa, Eb, NOc, CNd 0.286
17 S. kentucky Sa, Eb 0.143
18 S. kentucky Sa 0.071
19 S. enteritidis Sa, Eb, NOc, CNd, Pe, NAf, CEg, SXTh, CLi, Tj, AMk, 0.857
20 S. enteritidis Sa, Eb, NOc, CNd, Pe, NAf, CEg, SXTh, CLi 0.643 21 S. enteritidis Sa, Eb, NOc, CNd, Pe, NAf, CEg 0.500 22 S. enteritidis Sa, Eb, NOc, CNd, Pe, NAf 0.428
23 S. enteritidis Sa, Eb, NOc, CNd, Pe 0.357
24 S. enteritidis Sa, Eb, NOc 0.214
25 S. enteritidis Sa, Eb 0.143
26 S. tamale Sa, Eb, NOc, CNd, Pe, NAf, CEg, SXTh, CLi, Tj, AMk, AKl
27 S. tamale Sa, Eb, NOc, CNd, Pe, NAf, CEg, SXTh, CLi, Tj 0.714 28 S. tamale Sa, Eb, NOc, CNd, Pe, NAf, CEg, SXTh 0.571 29 S. tamale Sa, Eb, NOc, CNd, Pe, NAf 0.428
30 S. tamale Sa, Eb, NOc 0.214
31 S. infantis Sa, Eb, NOc, CNd, Pe, NAf, CEg, SXTh, CLi, Tj 0.714 32 S. infantis Sa, Eb, NOc, CNd, Pe, NAf, CEg 0.500
33 S. infantis Sa, Eb 0.143
34 S. papuana Sa, Eb, NOc, CNd, Pe, NAf, CEg, SXTh, CLi, Tj 0.714 35 S. papuana Sa, Eb, NOc, CNd, Pe, NAf 0.428
36 S. papuana Sa, Eb 0.143
37 S. wingrove Sa, Eb, NOc, CNd, Pe, NAf, CEg, SXTh, CLi 0.643 38 S. wingrove Sa, Eb, NOc, CNd, Pe, NAf, CEg 0.500 39 S. bargny Sa, Eb, NOc, CNd, Pe, NAf, CEg, SXTh, CLi 0.643
40 S. bargny Sa, Eb, NOc 0.214
41 S. larochelle Sa, Eb, NOc, CNd, Pe, NAf, CEg 0.500 42 S. virchow Sa, Eb, NOc, CNd, Pe, NAf 0.428
43 S. anatum Sa, Eb, NOc 0.214
Average 0.469 S:Streptomycina
E:Erythromycinb NA:Nalidixic acidf T:Tetracyclinej
NO:Norocillinc CE:Cephradineg AM:Ampicillink
AK:Amikacinl DO:Doxycyclinem G:Gentamicinn MAR: Multiple Antibiotic Resistanceo
Table 4. Occurrence of virulence genes of Salmonella species isolated from the examined samples of chicken meat and its products.
SalmonellaSerovars stn hilA fimH sopA
S. typhimurium + + + +
S. kentucky - + + +
S. enteritidis + + + +
S. tamale + - + +
S. infantis + + + -
S. papuana + + + +
S. wingrove - + + +
S. bargny - + + -
S. anatum + + - +
S. virchow + + + +
S. larochelle - - + +