Gıda Kaynaklı Staphylococcus aureus İntoksikasyonlarının Kontrolünde Bakteriyofaj Uygulamaları

Yıl 2023, , 114 - 120, 20.06.2023

Yeşim Yonsul Tuncer , Naim Deniz Ayaz

https://doi.org/10.35864/evmd.1282730

Öz

Staphylococcus aureus ısıya dayanıklı enterotoksinleri, biyofilm oluşturabilmesi ve antibiyotiklere özellikle de metisiline karşı direnç geliştirmesi sebebiyle başlıca gıda kaynaklı intoksikasyon etkenlerindendir. S. aureus’un stafilokokkal enterotoksinler (SEs) ve stafilokkokkal enterotoksin benzeri toksinler (SEIs) olmak üzere tanımlanmış 28 toksini bulunmasına rağmen gıda kaynaklı intoksikasyonlarının yaklaşık %95’inden sorumlu tutulanlar SEA-SEE’dir. Çiftlikten çatala gıda güvenliği için HACCP, GHP ve GMP gibi uygulamaların yanı sıra gıdalardaki ve gıda işleme tesislerinde bakteriyel yükün azaltılması amacıyla S.aureus’a özgü litik bakteriyofaj kullanımı alternatif bir yöntem olarak karşımıza çıkmaktadır. Fajların özgüllük, etkinlik ve insanlarda toksik etkisinin bulunmaması gibi birçok avantajına rağmen kullanımı sınırlandıran birtakım dezavantajları da bulunmaktadır. Bu derlemede, S. aureus’un gıda intoksikasyonları açısından önemi ile gıdalarda biyokontrolüne yönelik bakteriyofaj uygulamalarının etkinliği kısaca ele alınmıştır.

Anahtar Kelimeler

bakteriyofaj, biofilm, biyokontrol, S.aureus, vaka

Destekleyen Kurum

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Proje Numarası

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Teşekkür

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Bacteriophage Applications in the Control of Foodborne Staphylococcus aureus Intoxications

Öz

Staphylococcus aureus is one of the main foodborne intoxication agents due to its thermostable enterotoxins, biofilm formation and resistance to antibiotics, especially methicillin. Although S. aureus has 28 identified toxins, including staphylococcal enterotoxins (SEs) and staphylococcal enterotoxin-like toxins (SEIs), SEA-SEE were found responsible for approximately 95% of food intoxications. In addition to applications such as HACCP, GHP and GMP for farm-to-fork food safety, the use of S.aureus-specific lytic bacteriophage is an alternative method to reduce bacterial load in foods and food processing facilities. Although phages have many advantages such as specificity, efficacy and non-toxicity in humans, there are also disadvantages that limit their use. In this review, the importance of S. aureus in terms of food intoxications and the effectiveness of bacteriophage applications for biocontrol in foods are discussed briefly

Anahtar Kelimeler

bacteriophage, biocontrol, biofilm, cases, S.aureus

Proje Numarası

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Kaynakça

• Abdeen EE, Mousa WS, Salam SYA, Al-Maary KS, Mubarak AS, Mousa IM, Hemeng HA, Almuzaini AM, Alajaji AI, Alsubki RA, Elbehiry A, (2020). Antibiogram and phylogenetic diveristy of enterotoxigenic Staphylococcus aureus strains from milk and public health implications. Saudi Journal of Biological Sciences. 27(8),1968-1974. Al-Mebarik NF, El-Kersh TA, Al-Sheikh YA, Marie MA, (2016). A review of virulence factors, pathogenesis and antibiotic resistance in Staphylococcus aureus. Reviews in Medical Microbiology. 27(2), 50-56.
• Alves DR, Gaudion A, Bean JE, Perez-Esteban P, Arnot T C, Harper D R, Kot W, Hansen LH, Enright MC, A. Tobias A. Jenkins, (2014). Comined use of bacteriophage K and a novel bacteriophage to reduce Staphylococcus aureus biofilm formation. Apply Environmental Microbiology, 80 (21), 6694-6703.
• Asao T, Kumeda Y, Kawai T, Shibata T, Oda H, Haruki K, Nakazawa H., Kozyki S, (2003). An extensive outbreak of staphylococcal food poisoning due to low-fat milk in Japan: estimation of enterotoxin A in the incriminated milk and powdered skim milk. Epidemiol.İnfect. 130, 33-40.
• Bueno E, García P, Martínez B, Rodríguez A, (2012). Phage inactivation of Staphylococcus aureus in fresh and hard-type cheeses. International Journal of Food Microbiology. 158, 23–27.
• Cha Y, Son B, Ryu S, (2019). Effective removal of staphyloococcal biofilms on various food contact surfaces by Staphylococcus aureus phage endolysin LysCSA13. Food microbiology. 84, 103245.
• Chang Y, Kim M, Ryu S, (2017). Characterization of a novel endolysin LysSA11 and its utility as a potent biocontrol agent against Staphylococcus aureus on food an utensils. Food Microbiology. 68,112-120.
• Cristobal-Cueto P. Garcia-Quintanilla A, Esteban J, Garcia-Quintanilla M, (2021). Phages in food industry biocontrol and bio –remediation. Antibiotics. 10(7), 786.
• Denayer S, Delbrassinne L, Nia Y, Botteldoorn N, (2017). Food-borne outbreak investigation and molecular typing: high diversity of Staphylococcus aureus strains and importance of toxin detection. Toxins. 9(12), 407.
• Dakheel KH, Rahim RA, Neela VK, Al-Obaidi JR, Hun TG, Isa MNM, Yusoff K, (2019). Genomic analyses of two novel biofilm-degrading methicillin resistant Staphylococcus aureus phages. BMC microbiology, 19(1),1-23.
• Duc HM, Son HM, Ngan PH, Sato J, Masuda Y, Honjoh KI, & Miyamoto T, (2020). Isolation and application of bacteriophages alone or in combination with nisin against planktonic and biofilm cells of Staphylococcus aureus. Applied Microbiology and Biotechnology. 104, 5145-5158.
• El Haddad L, Roy JP, Khail GE, St-Gelais D., Champagne CP, Labrie S, Moineau S, (2016). Efficacy of two Staphylococcus aureus phage cocktails in cheese production. İnternational Journal of Food Microbiology. 217, 7-13.
• Fernandez L, Gutierrez D, Garcia P, Rodriquez A, (2019). The perfect bacteriophage for the theraupetic applications-a quick guide. Antibiotics.8(3),126.
• Fetsch A, Contzen M, Hartelt K, Kleiser A, Maassen S, Rau J, Kraushaar B, Layer F, Strommenger B, (2014). Staphylococcus aureus food poisoning outbreak associated with the consumption of ice-cream. International Journal of Food Microbiology. 187, 1-6.
• Fetsch A, Johler S, (2018). Staphylococcus aureus as a foodborne pathogen. Current Clinical Microbiology Reports. 5, 88-96.
• Galie S, Garcia-Gutierrez C, Miguelez EM, Villar CJ, Lombo F, (2018). Biofilms in the food industry:health aspects and control methods. Frontiers in Microbiology. 9, 898. doi10.3389/fmcb.2018.00898.
• Garcia P, Madera C, Martinez B, Rodriguez A, (2007). Biocontrol of Staphylococcus aureus in curd manufacturing processes using bacteriophages. International Dairy Journal. 17(10), 1232–1239.
• Gencay YE, Ayaz ND, Doğru AK, (2010). Enterotoxin gene profiles of Staphylococcus aureus and other staphylococcal ısolates from various foods and food İngredients. Erciyes Üniversitesi Veteriner Fakültesi Dergisi. 7(2), 75-80.
• Gencay YE, Brondsted L, (2019). Bacteriophages for biological control of foodborne pathogens. Doyle MP, Diez-Gonzalez F, Hill C eds. Food Microbiology: Fundamental and Frontiers, Fifth edition, ASM press, Washington, p. 765-786.
• Gonzalez-Menendez E, Fernandez L, Gutierrez D, Rodriquez A, Martinez B, Garcia P, (2018). Compative analysis of different preservation techniques for the storage of staphylococus phages aimed for the industrial development of phage based antimicrobial products. PLos one. 13(10):e 0205728.
• Grispoldi L, Karama M, Armani A, Hadjicharalambous C, Cenci-Goga BT, (2021). Staphylococcus aureus enterotoxin in food of animal origin and staphylococcal food poisoning risk assessment from farm to table. Italian Journal of Animal Science. 20(1), 677-690, doı: 10.1080/1828051X.2020.1871428.
• Gutiérrez D, Ruas-Madiedo P, Martinez B, Rodriguez A, Garcia P, (2014). Effective removal of staphylococcal biofilms by the endolysin LysH5. PLoS one. 9(9):e107307.
• Gutiérrez D, Vandenheuvel D, Martinez B, Rodriguez A, Lavigne R, Garcia P, (2015). Two-phages phiIPLA-RODI and phiIPLA-C1C, lyse mono and dual-species staphylococcal biofilms. Applied and Environmental Microbiology. 81(10),3336-3348.
• Güngör C, (2022). Büyükbaş hayvan mezbahalarında Staphylococcus aureus’a özgü litik bakteriyofaj izolasyonu, karakterizasyonu ve kırmızı et modelinde biyokontrolünün araştırılması, Doktora Tezi, Erciyes Üniversitesi Sağlık Bilimleri Enstitüsü, Kayseri.
• Hagens S, Loessner MJ, (2010). Bacteriophage for biocontrol of foodborne pathogens: Calculations and considerations. Current Pharmaceutical Biotechnology, 11, 58-68.
• Hennekinne JA, (2018). Staphylococcus aureus as a leading cause of foodborne outbreaks worldwide. Fetsch A eds. Staphylococcus aureus, Academic Press, UK, p. 129-146,
• Igbinosa EO, Beshiru A, Igbinosa IH, Ogofure AG, Ekundayo TC, Okoh AI, (2023). Prevalance, multiple antibiotic resistance and virulence profile of methicillin-resistant Staphylococcus aureus (MRSA) in retail poultry meat from Edo, Nigeria. Fronteriers in Cellular and Infection Microbiology. 13,183.
• Ivanova T, Krumova-Valcheva G, Mateva G, Daskalov H, (2020). Characteristics of Staphylococcus aureus ısolated from a case of foodborne outbreak in Bulgaria. Macedonian Veterinary Review. 43(2),151-159.
• Kelly D, McAuliffe O, Ross RP, Coffey A, (2012). Prevention of Staphylococcus aureus biofilm formation and reduction in established biofilm density using a combination of phage K and modified derivatives. Letters in Apply Microbiology. 54, 286-291.
• Le HHHT, Dalsgard A, Andersen PS, Nguyen HM, Ta Yt, Nguyen TT, (2021). Large scale Staphyloccocus aureus foodborne disease poisoning outbreak among primary school children. Microbiology Research. 12(1),43-52.
• Leitie JA, Pereira HP, Borges CAV, Alves BRC, Ramos AIAP, Martins MF, Arcuri EF, (2019). Lytic bacteriophages as a potential alternative to control Staphylococcus aureus. Pesquisa Agropecuaria Brasileria. 54.
• Lv G, Jiang R, Zhang H, Wang L, Li L, Gao W, Zhang H, Pei Y, Wei X, Dong H, Qin L, (2021).Molecular characteristics of Staphylococcus aureus from food samples and food poisoning outbreaks in Shiijiazhuang, China. Fronteriers in Microbiology. 12,652276.
• Mahros MA, Abd-Elghany SM, Sallam KI, (2021). Multidrug-methicillin- and vancomycin resistan Staphylococcus aureus isolated from ready to eat meat sandwiches: An on going food and public health concern. İnternational Journal of Food Microbiology. 346,109165.
• Martinez B, Obeso JM, Rodriguez A. Garcia P, (2008). Nisin-bacteriophage crossresistance in Staphylococcus aureus. International Journal of Food Microbiology. 122(3), 253-258.
• Mekhloufi OA, Chieffi D, Hammoudi A, Bensefia SA, Fanelli F, Fusco V, (2021). Prevalance, enterotoxigenic potential and antimicrobial resistance of Staphylococcus aureus and Methicillin-Resistant Staphylococcus aureus (MRSA)isolated from Algerian ready to eat foods. Toxins. 13(2),835.
• Moye ZD, Woolston J, Sulakvelidze A, (2018). Bacteriophage applications for food production and processing. Viruses. 10(4), 205, doi:10.33901/v10040205.
• Ngassam-Tchamba C, Duprez JN, Fergestad M, De Visscher A, L’Abeee-Lund T, De Vliegher S, Wasteson Y, Touzain F, Blanchard Y, Lavigne R, Chanishvili N, Cassart D, Mainil J, Thiry D, (2020). İn vitro and in vivo assessment of phage therapy against Staphylococcus aureus causing bovine mastitis. Journal of Global Antimicrobial Resistance. 22, 762-770.
• O’Flaherty S, Coffey A, Meaney WJ, Fitzgerald GF, Ross RP, (2005). Inhibition of bacteriophage K proliferation on Staphylococcus aureus in raw bovine milk. Letters in Applied Microbiology. 41(3), 274-279.
• Papadopoulus P, Papadopoulus T, Angelidis AS, Kotzamanidis C, Zdragas A, Papa A, Filioussis G, Sergelidis D, (2021). Prevalance, antimicrobial susceptibility and characterization of Staphylococcus aureus and methicilin resistant Satphylococcus aureus isolated from dairy indistrues in north-central and nort eastern Greece. İnternational Journal of Food Microbiology. 291, 35-41.
• Park JY, Seo KS, (2019). Staphylococcus aureus. Doyle MP, Diez-Gonzalez F, Hill C eds. Food Microbiology: Fundamental and Frontiers, Fifth edition, ASM press, Washington, p. 555-584.
• Rahman M, Kim S, Kim SM, Seol SY, Kim J, (2011). Characterization of induced Staphylococcus aureus bacteriophage SAP-26 and its anti-biofilm activity with rifampcin. Biofuling. 27, 1087-1093.
• Rajakrishnan S, Ismail MZH, Jamalulail SH, Alias N, Ismail H, Taib, S M, Cheng LS, Zakiman Z, Richai O, Silverdurai RR, Yusof, MP, (2022). Investigation of a foodborne outbreak at a mass gathering in Petaling District, Selangor, Malaysia. Western Pacific Surveillance and Response Journal: WPSAR. 13(1), 1.
• Rodriquez-Lazaro D, Onicuic EA, Garcia PG, Gallego D, Fernandez-Natal I, Dominquez-Gill M, Hernandez M, (2017). Detection and characterization of Staphylococcus aureus and methicillin- resistance S.aureus in foods confiscated in EU borders. Fronteriers in micrbiology. 8,1344.
• Saber T, Samir M, El-Mekkawy RM, Ariny E, El-Sayed SR, Enan G, Abdelatif SH, Askora A, Merwad AMA, Tartor YH, (2022). Methicillin- and Vancomycin-Resistant Staphylococcus aureus From Humans and Ready-To-Eat Meat: Characterization of Antimicrobial Resistance and Biofilm Formation Ability. Frontiers in Microbiology.12, 735494.
• Sass P, Bierbaum G, (2007). Lytic activity of recombinant bacteriophages Φ 11 and Φ12 endolysins on whole cells and biofilms of Staphylococcus aureus. Apply and Environmental Microbiology. 73(1), 347-352.
• Sillankorva SM, Oliveria H, Azeredo J, (2012). Bacteriophages and Their Role in Food Safety .İnternational Journal of Microbiology.doi:10.115/2012/8639.
• Son JS, Lee S J, Jun SY, Yoon SJ, Kang SH, Paik HR, Kang JO Choi YJ, (2010). Antibacterial and biofilm removal activity of Staphylococcus aureus bacteriophage SAP-2 and a derived recombinant cell-wall-degrading enzyme. Applied Microbiology and Biotechnology. 86, 1439-1449.
• Tahir A, Asif M, Abbas Z, ur Rehman S, (2017). Three bacteriophages SA, SA2 and SNAF can control growth of milk isolates Staphylooccal species. Pakistan J Zool, 49(2),493-496.
• Titze I, Lehnherr T, Lehnherr H, Krömker V, (2020). Efficacy of bacteriophages against Staphylococcus aureus isolates from bovine mastitis. Pharmaceuticals,13(3),35.
• Umeda K, Nakamura H, Yamamoto K, Nishina N, Yasufuku K, Hirai Y, Hirayama T, Goto K, Hase A, Ogasawara J, (2017). Molecular and epidemiological characterization of staphylococcal foodborne outbreak of Staphylococcus aureus harboring seg, sei, sem, sen, seo, and selu genes without production of classical enterotoxins. International Journal of Food microbiology. 256, 30-35.
• Umeda K, Ono, HK, Wada T, Motooka D, Nakamura S, Nakamura H, & Hu DL, (2021). High production of egc2-related staphylococcal enterotoxins caused a food poisoning outbreak. International Journal of Food Microbiology. 357, 109366.
• Vandersteegen K, Kropinski AM, Nash JH, Noben JP, Hermans K, Lavigne R, (2013). Romulus and Remus, two phage isolates representing a distinct clade within the Twortlikevirus genus, display suitable properties for phage therapy applications. Journal of Virology. 87(6), 3237-3247.
• Vázquez-Sánchez D, Rodríguez- López P, (2018). Biofilm formation of Staphylococcus aureus, Fetsch A eds. In:Staphylococcus aureus, Academic Press, UK, p. 87-103.
• Wang H, Shen J, Zhu C, Ma K, Fang M, Li B, Wang W, Xue, T, (2022). Antibiotics Resistance and Virulence of Staphylococcus aureus Isolates Isolated from Raw Milk from Handmade Dairy Retail Stores in Hefei City. China. Foods.11(15), 2185.
• Wen H, Yuan L, Li X, Ye JH, Li YJ, Yang ZQ, Zhou WY, (2023). Isolation and characterization of a broad spectrum phage Sap YZU11 and its potential application for biological control of Staphylococcus aureus. Quality Assurance and Safety of Crops&Foods, 15(2),32-48.
• Youssef O, Agun S, Fernandez L, Khalil SA, Rodriquez A, Garcia P, (2023). Impact of the calcium concentration on the efficacy of phage philPLA-RODI, LysRODI ΔAmi and nisin for the elimination of Staphylococcus aureus during lab-scale cheese production. International Journal of Food Microbiology.110227.