Volume 9, Issue 4 (December 2022)                   J. Food Qual. Hazards Control 2022, 9(4): 215-225 | Back to browse issues page


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Sadek O, Koriem A. Multidrug Resistance and Virulence Factors of Enterococci Isolated from Milk and Some Dairy Desserts. J. Food Qual. Hazards Control 2022; 9 (4) :215-225
URL: http://jfqhc.ssu.ac.ir/article-1-1039-en.html
Department of Food Hygiene, Assiut Lab., Animal Health Research Institute (AHRI), Agricultural Research Center (ARC), Egypt , onsi_2000@yahoo.com
Abstract:   (448 Views)
Background: Enterococci spp. bacteria especially Enterococcus faecalis and E. faecium have the ability to acquire antibiotic-resistance pattern and causing life-threatening hospital-acquired infections. So, the aim of this study was to count and isolate of E. faecalis and E. faecium from milk and dairy desserts consumed in Assiut city, Egypt.
Methods: A total of 100 raw milk, ice cream, mehallabia, and milk rice samples were collected from dairies shop in Assiut city, Egypt and were bacteriologically examined for the presence and count of Enterococcus spp. Then, identification of enterococci isolates by conventional and Polymerase Chain Reaction (PCR) methods, performance of antibiotic sensitivity assay, and some virulence genes in the Multi Drug Resistant (MDR) isolates were identified.
Results: The prevalence of counted Enterococcus spp. in raw milk, ice cream, mehallabia, and milk rice samples were 76, 44, 20, and 32%, respectively. The prevalence of E. faecalis in raw milk, ice cream, mehallabia, and milk rice samples were 64, 0, 0, and 8%, while for E. faecium were 12, 44, 20, and 24%, respectively. E. faecalis isolates were resistant to vancomycin, ciprofloxacin, gentamicin, erythromycin, and tetracycline with the rate of 72.2, 88.9, 88.9, 94.4, and 77.8%, respectively, while for the resistance rates of E. faecium were 16, 40, 16, 84, and 20%, respectively. E. faecalis and E. faecium were MDR in rate of 88.9 and 32%, respectively.
Conclusion: This study revealed that milk, ice cream, mehallabia, and milk rice could be a source of enterococci to consumers in Assiut, Egypt. Moreover, E. faecalis had higher MDR and Resistant Index (RI) than E. faecium.

DOI: 10.18502/jfqhc.9.4.11376
Full-Text [PDF 660 kb]   (212 Downloads)    
Type of Study: Original article | Subject: Special
Received: 22/08/14 | Accepted: 22/11/29 | Published: 22/12/29

References
1. Abd El-Tawab A.A., Mohamed S.R., Kotb M.A.M. (2019). Molecular detection of virulence and resistance genes of Enterococci spp. isolated from milk and milk products in Egypt. Nature and Science. 17: 77-83. [DOI: 10.7537/marsnsj170919.10]
2. Al-Shammary A.H.A. (2019). Run-off patterns of vancomycin resistant enterococci (VRE clones) in cows raw milk and imported milk powders at Baghdad markets. The Iraqi Journal of Veterinary Medicine. 43: 65-70. [DOI: 10.30539/ iraqijvm.v43i2.532] [DOI:10.30539/iraqijvm.v43i2.532]
3. Bouymajane A., Filali F.R., Oulghazi S., Ed-Dra A., Benhallam F., El Allaoui A., Anissi J., Sendide K., Ouhmidou B., Moumni M. (2018). Occurrence, molecular and antimicrobial resistance of Enterococcus spp. isolated from raw cow's milk trade by street trading in Meknes city, Morocco. Germs. 8: 77-84. [DOI: 10.18683/germs.2018.1134] [DOI:10.18683/germs.2018.1134] [PMID] [PMCID]
4. Chajęcka-Wierzchowska W., Zadernowska A., García-Solache M. (2020). Ready-to-eat dairy products as a source of multidrug-resistant Enterococcus strains: phenotypic and genotypic characteristics. Journal of Dairy Science. 103: 4068-4077. [DOI: 10.3168/jds.2019-17395] [DOI:10.3168/jds.2019-17395] [PMID]
5. Ch'ng J.-H., Chong K.K.L., Lam L.N., Wong J.J., Kline K.A. (2019). Biofilm-associated infection by enterococci. Nature Reviews Microbiology. 17: 82-94. [DOI: 10.1038/s41579-018-0107-z] [DOI:10.1038/s41579-018-0107-z] [PMID]
6. Clinical and Laboratory Standards Institute (CLSI). (2018). Performance standards for antimicrobial susceptibility testing. 28th edition. CLSI Supplement M100, Wayne, Pennsylvaniya. URL: https://clsi.org/media/1930/m100ed28_sample.pdf.
7. Courvalin P. (2006). Vancomycin resistance in gram-positive cocci. Clinical Infectious Diseases. 42: S25-S34. [DOI: 10.1086/ 491711] [DOI:10.1086/491711] [PMID]
8. Cunha S., Soares R., Maia M., Igrejas G., Silva F., Miranda C., Poeta P. (2021). Presence of antibiotic-resistant Enterococcus faecalis in colostrum supplied to calves?. Antibiotics. 68.
9. Donlan R.M., Costerton J.W. (2002). Biofilms: survival mechanisms of clinically relevant microorganisms. Clinical Microbiology Reviews. 15: 167-193. [DOI:10.1128/CMR.15. 2.167-193.2002] [DOI:10.1128/CMR.15.2.167-193.2002] [PMID] [PMCID]
10. Downes F.P., Ito K. (2001). Compendium of methods for the microbiological examination of foods. 4th edition. American Public Health Association, Washington, DC, USA. [DOI:10.2105/9780875531755]
11. El-Malt L., AbdelHameed K., Mohammed A. (2013). Microbiological quality assessment of ice cream products in Qena city, Egypt. Zagazig Veterinary Journal. 41: 775-783.
12. El-Zamkan M.A., Mohamed H.M.A. (2021). Antimicrobial resistance, virulence genes and biofilm formation in Enterococcus species isolated from milk of sheep and goat with subclinical mastitis. Plos One. 16: e0259584. [DOI: 10.1371/journal.pone.0259584] [DOI:10.1371/journal.pone.0259584] [PMID] [PMCID]
13. Fahmy N.F., Abdel-Gawad A.R., Rezk G.A.E.-G., Mahmoud E.A.-R. (2021). Characterization of Enterococci isolated from intensive care unit (ICU); distribution of virulence markers, virulence genes and antibiotic resistance pattern. Microbes and Infectious Diseases. 2: 725-735. [DOI: 10.21608/MID. 2021.76391.1158]
14. Fisher K., Phillips C. (2009). The ecology, epidemiology and virulence of Enterococcus. Microbiology. 155: 1749-1757. [DOI: 10.1099/mic.0.026385-0] [DOI:10.1099/mic.0.026385-0] [PMID]
15. Franz C.M.A.P., Stiles M.E., Schleifer K.H., Holzapfel W.H. (2003). Enterococci in foods-a conundrum for food safety. International Journal of Food Microbiology. 88: 105-122. [DOI: 10.1016/S0168-1605(03)00174-0] [DOI:10.1016/S0168-1605(03)00174-0] [PMID]
16. Freeman D.J., Falkiner F.R., Keane C.T. (1989). New method for detecting slime production by coagulase negative staphylococci. Journal of Clinical Pathology. 42: 872-874. [DOI: 10.1136/jcp.42.8.872] [DOI:10.1136/jcp.42.8.872] [PMID] [PMCID]
17. Fuka M.M., Maksimovic A.Z., Tanuwidjaja I., Hulak N., Schloter M. (2017). Characterization of Enterococcal community isolated from an artisan Istrian raw milk cheese: biotechnological and safety aspects. Food Technology and Biotechnology. 55: 368-380. [DOI: 10.17113/ftb.55.03.17.5118] [DOI:10.17113/ftb.55.03.17.5118] [PMID] [PMCID]
18. Gökmen M., Ektik N. (2022). Determination of virulence factors and antibiotic resistances of Enterococcus spp. identified from different stages of ripened (classical) white cheese production. Kocatepe Veterinary Journal. 15: 120-127. [DOI: 10.30607/kvj.1048982] [DOI:10.30607/kvj.1048982]
19. Golińska E., Tomusiak A., Gosiewski T., Więcek G., Machul A., Mikołajczyk D., Bulanda M., Heczko P.B., Strus M. (2013). Virulence factors of Enterococcus strains isolated from patients with inflammatory bowel disease. World Journal of Gastroenterology. 19: 3562-3572. [DOI: 10.3748/wjg.v19. i23.3562] [DOI:10.3748/wjg.v19.i23.3562] [PMID] [PMCID]
20. Golob M., Pate M., Kušar D., Dermota U., Avberšek J., Papić B., Zdovc I. (2019). Antimicrobial resistance and virulence genes in Enterococcus faecium and Enterococcus faecalis from humans and retail red meat. BioMed Research International. 2019. [DOI: 10.1155/2019/2815279] [DOI:10.1155/2019/2815279] [PMID] [PMCID]
21. Gorgy S.F., ElAsuoty M.S., Saber A.S., Ali A.H. (2016). Prevalence of enterococci and streptococci in raw milk and some dairy products and the subsequent alteration on quality. Egyptian Journal of Chemistry and Environmental Health. 2: 500-515. [DOI: 10.21608/ejceh.2016.254610] [DOI:10.21608/ejceh.2016.254610]
22. Gundogan N., Ataol O., Torlak F.O. (2013). Determination of some virulence factors in Staphylococcus aureus, Enterococcus faecalis and Enterococcus faecium isolated from meat and milk products. Journal of Food Safety. 33: 387-393. [DOI: 10.1111/jfs.12062] [DOI:10.1111/jfs.12062]
23. Hammad A.M. (2015). Bacteriocin production and probiotic properties of Enterococcus spp. isolated from raw milk. Assiut Veterinary Medical Journal. 61: 80-86. [DOI: 10. 21608/avmj.2015.170216] [DOI:10.21608/avmj.2015.170216]
24. Hammad A.M., Aly S.S., Hassan H.A., Abbas N.H., Eltahan A., Khalifa E., Shimamoto T. (2022). Occurrence, phenotypic and molecular characteristics of vancomycin-resistant enterococci isolated from retail raw milk in Egypt. Food-borne Pathogens and Disease. 19: 192-198. [DOI: 10.1089/ fpd.2021.0054] [DOI:10.1089/fpd.2021.0054] [PMID]
25. Hamzah A.M., Kadium H.K. (2018). Isolation and identification of Enterococcus fecalis from cow milk samples and vaginal swab from human. Journal of Entomology and Zoology Studies. 6: 218-222.
26. Harely J.P. (2016). Laboratory exercises in microbiology. 10th edition. McGraw-Hill Education, USA.
27. Harrigan W.F. (1998). Laboratory methods in food microbiology. 3rd edition. Gulf Professional Publishing, Houston, Texas.
28. Hartman P.A., Deibel R.H., Sieverding L.M. (2001). Enterococci. In: Downes F.P., Ito K. (Editors). Compendium of methods for the microbiological examination of foods. 4th edition. American Public Health Association, Washington, DC., USA. pp: 83-87 [DOI:10.2105/9780875531755ch09]
29. Hassan G.M., Afifi S.A. (2016). Bacteriological quality assessment of some locally manufactured dairy desserts sold in Beni-Suef city, Egypt and molecular detection of Staphylococcus aureus enterotoxin genes. Zagazig Veterinary Journal. 44: 91-100. [DOI: 10.21608/zvjz.2016.7851] [DOI:10.21608/zvjz.2016.7851]
30. Horiuk Y.V., Kukhtyn M.D., Vergeles K.M., Kovalenko V.L., Verkholiuk M.M., Peleno R.A., Horiuk V.V. (2018). Characteristics of enterococci isolated from raw milk and hand-made cottage cheese in Ukraine. Research Journal of Pharmaceutical, Biological and Chemical Sciences. 9: 1128-1133.
31. Jackson C.R., Fedorka-Cray P.J., Barrett J.B. (2004). Use of a genus- and species-specific multiplex PCR for identification of enterococci. Journal of Clinical Microbiology. 42: 3558-3565. [DOI: 10.1128/JCM.42.8.3558-3565.2004] [DOI:10.1128/JCM.42.8.3558-3565.2004] [PMID] [PMCID]
32. Kayser F.H. (2003). Safety aspects of enterococci from the medical point of view. International Journal of Food Microbiology. 88: 255-262. [DOI: 10.1016/S0168-1605(03)00188-0] [DOI:10.1016/S0168-1605(03)00188-0] [PMID]
33. Krumperman P.H. (1983). Multiple antibiotic resistance indexing of Escherichia coli to identify high-risk sources of fecal contamination of foods. Applied and Environmental Microbiology. 46: 165-170. [DOI: 10.1128/aem.46.1.165-170.1983] [DOI:10.1128/aem.46.1.165-170.1983] [PMID] [PMCID]
34. Lampert L.M. (1975). Modern dairy products. 3rd edition. Chemical Publishing Company., Inc., New York.
35. Magiorakos A.-P., Srinivasan A., Carey R.B., Carmeli Y., Falagas M.E., Giske C.G., Harbarth S., Hindler J.F., Kahlmeter G., Olsson-Liljequist B., Paterson D.L., Rice L.B., et al. (2012). Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clinical Microbiology and Infection. 18: 268-281. [DOI: 10.1111/ j.1469-0691.2011.03570.x] [DOI:10.1111/j.1469-0691.2011.03570.x] [PMID]
36. Margalho L.P., Van Schalkwijk S., Bachmann H., Sant'Ana A.S. (2020). Enterococcus spp. in Brazilian artisanal cheeses: occurrence and assessment of phenotypic and safety properties of a large set of strains through the use of high throughput tools combined with multivariate statistics. Food Control. 118: 107425. [DOI: 10.1016/j.foodcont.2020.107425] [DOI:10.1016/j.foodcont.2020.107425]
37. Nasiri M., Hanifian S. (2022). Enterococcus faecalis and Enterococcus faecium in pasteurized milk: prevalence, genotyping, and characterization of virulence traits. LWT - Food Science and Technology. 153: 112452. [DOI: 10.1016/j.lwt.2021. 112452] [DOI:10.1016/j.lwt.2021.112452]
38. Poh C.H., Oh H.M.L., Tan A.L. (2006). Epidemiology and clinical outcome of enterococcal bacteraemia in an acute care hospital. Journal of Infection. 52: 383-386. [DOI: 10.1016/ j.jinf.2005.07.011] [DOI:10.1016/j.jinf.2005.07.011] [PMID]
39. Poonia S., Singh T.S., Tsering D.C. (2014). Antibiotic susceptibility profile of bacteria isolated from natural sources of water from rural areas of East Sikkim. Indian Journal of Community Medicine. 39: 156-160. [DOI: 10.4103/0970-0218.137152] [DOI:10.4103/0970-0218.137152] [PMID] [PMCID]
40. Rathnayake I.U., Hargreaves M., Huygens F. (2012). Antibiotic resistance and virulence traits in clinical and environmental Enterococcus faecalis and Enterococcus faecium isolates. Systemic and Applied Microbiology. 35: 326-333. [DOI: 10.1016/j.syapm.2012.05.004] [DOI:10.1016/j.syapm.2012.05.004] [PMID]
41. Ristori C.A., Rowlands R.E.G., Bergamini A.M.M., Lopes G.I.S.L., De Paula A.M.R., De Oliveira M.A., Lima M.D.J.D.C., Tegani L.S., Watanabe A.H., Jakabi M., Zanella R.C. (2012). Prevalence and antimicrobial susceptibility profile of Enterococcus spp isolated from frozen chicken carcasses. Revista do Instituto Adolfo Lutz. 71: 237-243. URL: https:// docs.bvsalud.org/biblioref/ses-sp/2012/ses-26486/ses-26486-3791.pdf.
42. Sattari-Maraji A., Jabalameli F., Node Farahani N., Beigverdi R., Emaneini M. (2019). Antimicrobial resistance pattern, virulence determinants and molecular analysis of Enterococcus faecium isolated from children infections in Iran. BMC Microbiology. 19: 156. [DOI: 10.1186/s12866-019-1539-y] [DOI:10.1186/s12866-019-1539-y] [PMID] [PMCID]
43. Shafeek M.Y., El-Malt L.M., AbdelHameed K.G., El-Zamkan M.A. (2018). Some virulence genes of pathogenic enterococci isolated from raw milk and some milk products. SVU-International Journal of Veterinary Sciences. 1: 102-113. [DOI: 10.21608/SVU.2018.17937] [DOI:10.21608/svu.2018.17937]
44. Sparo M., Urbizu L., Solana M.V., Pourcel G., Delpech G., Confalonieri A., Ceci M., Sánchez Bruni S.F. (2012). High‐level resistance to gentamicin: genetic transfer between Enterococcus faecalis isolated from food of animal origin and human microbiota. Letters in Applied Microbiology. 54: 119-125. [DOI: 10.1111/j.1472-765X.2011.03182.x] [DOI:10.1111/j.1472-765X.2011.03182.x] [PMID]
45. Šustáčková A., Nápravníková E., Schlegelová J. (2004). Antimicrobial resistance of Enterococcus spp. isolates from raw beef and meat products. Folia Microbiologica. 49: 411-417. [DOI: 10.1007/BF02931602] [DOI:10.1007/BF02931602] [PMID]
46. Teixeira L.M., Carvalho M.D.G.S., Facklam R.R (2007). Enterococcus. In: Murray P.R., Baron E.J., Jorgensen J.H., Landry M.L., Pfaller M.A. (Editors). Manual of clinical microbiology. 9th edition. American Society for Microbiology, Washington, DC. pp: 430-442.
47. Toledo-Arana A., Valle J., Solano C., Arrizubieta M.J., Cucarella C., Lamata M., Amorena B., Leiva J., Penadés J.R., Lasa I. (2001). The enterococcal surface protein, Esp, is involved in Enterococcus faecalis biofilm formation. Applied and Environmental Microbiology. 67: 4538-4545. [DOI: 10.1128/ AEM.67.10.4538-4545.2001] [DOI:10.1128/AEM.67.10.4538-4545.2001] [PMID] [PMCID]
48. Torres C., Alonso C.A., Ruiz-Ripa L., León-Sampedro R., Del Campo R., Coque T.M. (2018). Antimicrobial resistance in Enterococcus spp. of animal origin. In: Schwarz S., Cavaco L.M., Shen J. (Editors). Antimicrobial resistance in bacteria from livestock and companion animals. Wiley, Hoboken, New Jersey. pp: 185-227. [DOI: 10.1128/9781555819804. ch9]. [DOI:10.1128/9781555819804]
49. Vankerckhoven V., Van Autgaerden T., Vael C., Lammens C., Chapelle S., Rossi R., Jabes D., Goossens H. (2004). Development of a multiplex PCR for the detection of asa1, gelE, cylA, esp, and hyl genes in enterococci and survey for virulence determinants among European hospital isolates of Enterococcus faecium. Journal of Clinical Microbiology. 42: 4473-4479. [DOI: 10.1128/JCM.42.10.4473-4479.2004] [DOI:10.1128/JCM.42.10.4473-4479.2004] [PMID] [PMCID]
50. Výrostková J., Regecová I., Dudriková E., Marcinčák S., Vargová M., Kováčová M., Mal'ová J. (2021). Antimicrobial resistance of Enterococcus sp. isolated from sheep and goat cheeses. Foods. 10: 1844. [DOI: 10.3390/foods10081844] [DOI:10.3390/foods10081844] [PMID] [PMCID]
51. Wajda Ł., Ostrowski A., Błasiak E., Godowska P. (2022). Enterococcus faecium isolates present in human breast milk might be carriers of multi-antibiotic resistance genes. Bacteria. 1: 66-87. [DOI: 10.3390/bacteria1020007] [DOI:10.3390/bacteria1020007]
52. Williams S.P., Livingston W., Safarulla A. (2022). A case of early-onset sepsis with Enterococcus faecalis in a neonate born to a COVID-positive mother. Journal of Investigative Medicine. 70: 581. [DOI: 10.1136/jim-2022-SRMC.267]
53. Zoletti G.O., Siqueira J.F., Santos K.R.N. (2006). Identification of Enterococcus faecalis in root-filled teeth with or without periradicular lesions by culture-dependent and -independent approaches. Journal of Endodontics. 32: 722-726. [DOI: 10.1016/j.joen.2006.02.001] [DOI:10.1016/j.joen.2006.02.001] [PMID]
54. Zou J., Shankar N. (2015). Surface protein Esp enhances pro-inflammatory cytokine expression through NF-κB activation during enterococcal infection. Innate Immunity. 22: 31-39. [DOI: 10.1177/1753425915611237] [DOI:10.1177/1753425915611237] [PMID]

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