Antimicrobial efficiency of rosemary, thyme and clove essential oils on the preservation of marinated chicken breasts (fillets)

• Pelin Demir Fırat University, Faculty of Veterinary Medicine, Department of Food Hygiene and Technology. Elazig, Türkiye
• Mehmet Emin Aydemir Harran University, Faculty of Veterinary Medicine, Department of Food Hygiene and Technology. Sanliurfa, Türkiye
• Selçuk Alan Kafkas University, Faculty of Veterinary Medicine, Department of Veterinary, Food Hygiene and Production. Kars, Türkiye
• Gülsüm Öksüztepe Fırat University, Faculty of Veterinary Medicine, Department of Food Hygiene and Technology. Elazig, Türkiye

DOI: https://doi.org/10.52973/rcfcv-e34346

Keywords: Essential oil compounds, marination, chicken breast, preservation, quality parameters

Abstract

Essential oils can be used as natural preservatives in the poultry meat industry. The aim of this research was to determine the effect of some essential oils on the microbial, physicochemical, and sensory properties of marinated chicken breast. For this purpose, rosemary, thyme, and clove essential oils were used at doses of 125 mg·kg^-1 and 250 mg·kg^-1 while marinating chicken breasts. After the marinated chicken breasts were divided into groups, they were stored in the refrigerator at 4°C. The results showed that 250 mg·kg^-1 doses of essential oils, especially at 24 h, and rosemary had more inhibitory effects on some microbial (total mesophilic aerobic, total psychrophilic aerobic, and yeast–mold) parameters. However, the sensory groups with the addition of 125 mg·kg^-1 were more accepted. Among these groups, the most acceptable group was the group that added 125 mg·kg^-1 of thyme essential oil. The study shows that the use of thyme essential oil as an alternative to chemical preservatives may be beneficial both in extending the shelf life of marinated chicken breasts and in terms of consumer taste.

References

İnal T. Besin hijyeni: Hayvansal gıdaların sağlık kontrolu [Food Hygiene, Health Controls on Animal Source Food]. 2nd ed. Istanbul (Türkiye): Final Ofset; 1992. 783 p. Turkish.

Ergezer H, Gokce R. Comparison of marinating with two different types of marinade on some quality and sensory characteristics of Turkey breast meat. J. Anim. Vet. Adv. [Internet]. 2011 [cited 08 Aug. 2023]; 10(1):60–67. Available in: https://goo.su/I9sui7

Chouliara E, Karatapanis A, Savvaidis IN, Kontominas MG. Combined effect of oregano essential oil and modified atmosphere packaging on shelf–life extension of fresh chicken breast meat, stored at 4°C. Food Microbiol. [Internet]. 2007; 24(6):607–617. doi: https://doi.org/cznj55

Sahin S, Kalin R, Arslanbas E, Mogulkoc MN. [Determination of some bacteria and indicator microorganisms in chicken meat offered for sale]. Manas J. Agric. Vet. [Internet]. 2017 [cited 12 Jul. 2023]; 7(1):47–56. Turkish. Available in: https://goo.su/ls5uV

Álvarez–Astorga M, Capita R, Alonso–Calleja C, Moreno B, García–Fernández C. Microbiological quality of retail chicken by–products in Spain. Meat Sci. [Internet]. 2002; 62(1):45–50. doi: https://doi.org/b97wtd

Can HY. Investigation of Pseudomonas species in chicken drumstick samples. Kocatepe Vet. J. [Internet]. 2022; 15(2):139–143. doi: https://doi.org/m3v5

Mahdavi–Roshan M, Gheibi S, Pourfarzad A. Effect of propolis extract as a natural preservative on quality and shelf life of marinated chicken breast (chicken Kebab). LWT. [Internet]. 2022; 155:112942. doi: https://doi.org/m3v6

Kozačinski L, Hadžiosmanović M, Zdolec N. Microbiological quality of poultry meat on the Croatian market. Vet. Arh. [Internet]. 2006 [cited 14 Aug. 2023]; 76(4):305–313. Available in: https://goo.su/f6f9Y

Magdelaine P, Spiess MP, Valceschini E. Poultry meat consumption trends in Europe. World's Poult. Sci. J. [Internet]. 2008; 64(1):53–64. doi: https://doi.org/bs4rtq

Goswami M, Pathak V, Bharti SK, Chappalwar AM, Ojha S, Singh S, Singh S. Effect of low temperature preservation on quality characteristics of meat. JAFST. [Internet]. 2019 [cited 14 Aug. 2023]; ;7(1):41–46. Available in: https://goo.su/XQp5dB

The might of marinades [Internet]. Prepared Foods. 2003 [cited 22 Jul. 2023]. Available in: https://goo.su/JGkcq4

Lytou AE, Nychas GJE, Panagou EZ. Effect of pomegranate based marinades on the microbiological, chemical and sensory quality of chicken meat: A metabolomics approach. Int. J. Food Microbiol. [Internet]. 2018; 267:42–53. doi: https://doi.org/gczthv

Parks SS, Reynolds AE, Wicker L. Aqueous apple flavoring in breast muscle has physical, chemical, and sensory properties similar to those of phosphate–marinated controls. Poult. Sci. [Internet]. 2000; 79(8):1183–1188. doi: https://doi.org/m3x2

Nisiotou A, Chorianopoulos NG, Gounadaki A, Panagou EZ, Nychas GJ. Effect of wine–based marinades on the behavior of Salmonella Typhimurium and background flora in beef fillets. Int. J. Food Microbiol. [Internet]. 2013; 164(2–3):119–127. doi: https://doi.org/f43rt6

Thanissery R, Smith DP. Marinade with thyme and orange oils reduces Salmonella Enteritidis and Campylobacter coli on inoculated broiler breast fillets and whole wings. Poult. Sci. [Internet]. 2014; 93(5):1258–1262. doi: https://doi.org/f53c36

Jarvis N, O'Bryan CA, Ricke SC, Crandall PG. The functionality of plum ingredients in meat products: A review. Meat Sci. [Internet]. 2015; 102:41–48. doi: https://doi.org/f6zsv4

Bayaz M. [Essential oils: antimicrobial, antioxidant and antimutagenic activities]. Akad. Gida. [Internet] 2014 [cited 08 Aug. 2023]; 12(3):45–53. Turkish. Available in: https://goo.su/Jhet

Rice–Evans CA, Miller NJ, Paganga G. Structure–antioxidant activity relationships of flavonoids and phenolic acids. Free Radic. Biol. Med. [Internet]. 1996; 20(7):933–956. doi: https://doi.org/cdx3jv

Burt S. Essential oils: their antibacterial properties and potential applications in foods–a review. Int. J. Food Microbiol. [Internet]. 2004; 94(3):223–253. doi: https://doi.org/fh92fg

Hammer KA, Carson CF, Riley TV. Antimicrobial activity of essential oils and other plant extracts. J. Appl. Microbiol. [Internet]. 1999; 86(6):985–990. doi: https://doi.org/bh8w9x

Pizzale L, Bortolomeazzi R, Vichi S, Überegger E, Conte LS. Antioxidant activity of sage (Salvia officinalis and S. fruticosa) and oregano (Origanum onites and O. indercedens) extracts related to their phenolic compound content. J. Sci. Food Agric. [Internet]. 2002; 82(14):1645–1651. doi: https://doi.org/bkxcdd

Güran S, Öksüztepe G. Effects of chitosan and some essential oils (thyme, clove, roemary), individually or in combination, on inactivation of Salmonella Typhimurium in raw meatball (Turkish raw meatball). F. Ü. Sağ. Bil. Vet. Derg. [Internet]. 2014 [cited 14 Aug. 2023]; 28(3):117–122. Available in: https://goo.su/Yww9

EFSA Panel on Food Additives and Nutrient Sources added to Food (ANS). Scientific opinion on the use of oregano and lemon balm extracts as a food additive. EFSA J. [Internet]. 2010 [cited 18 Aug. 2023]; 8(2):1514. Available in: https://goo.su/SN6o

Damien Dorman HJ, Deans SG, Noble RC, Surai P. Evaluation in vitro of plant essential oils as natural antioxidants. J. Essent. Oil Res. [Internet]. 1995; 7(6):645–651. doi: https://doi.org/m3x4

Rižnar K, Čelan Š, Knez Ž, ŠKerget M, Bauman D, Glaser R. Antioxidant and antimicrobial activity of rosemary extract in chicken frankfurters. J. Food Sci. [Internet]. 2006; 71(7):C425–C429. doi: https://doi.org/b69vk4

Harmankaya S, Vatansever L. The Effect of Essential Oils of Rosemary and Clove on Shelf Life Chicken Meat. Van Vet. J. [Internet]. 2017 [cited 14 Aug. 2023]; 28(1):11–19. Available in: https://goo.su/ZbupEJ

American Public Health Association (APHA). Standards Methods for the Examination of Dairy Products [Internet]. 14th ed. New York (USA): American Public Health Association; 1978 [cited 16 Aug. 2023]. 456 p. Available in: https://goo.su/mRBQ3mC

Harrigan WF. Laboratory methods in food microbiology [Internet]. 3rd ed. London (UK): Academic Press; 1998 [cited 16 Aug. 2023]. 520 p. Available in: https://goo.su/D0ft4m

USDA/FSIS. Laboratory Guidebook. Quantitative analysis of bacteria in foods as sanitary indicators [Internet]. 2015 [cited 14 Aug. 2023]; 18 p. Available in: https://goo.su/ZlEJZPn

International Organization for Standardization. ISO 4832:2006. Microbiology of Food and Animal Feeding Stuffs–Horizontal Method for the Enumeration of Coliforms–Colony–count Technique. Geneva (Switzerland): ISO; 2006. 6 p.

International Organization for Standardization. ISO 21528–2:2017. Microbiology of the food Chain–Horizontal method for the detection and enumeration of Enterobacteriaceae Part 2: Colony–count technique. Geneva (Switzerland): ISO; 2017. 15 p,

International Organization for Standardization. ISO 16649–1:2018. Microbiology of food and animal feeding Stuffs–Horizontal method for the enumeration of beta–glucuronidase–positive Escherichia coli. Part 1: Colony–count technique at 44 degrees C using membranes and 5–bromo–4–chloro–3–indolyl beta–D–glucuronide. Geneva (Switzerland): ISO; 2018. 11 p.

International Organization for Standardization. ISO 21527–1:2008. Microbiology of Food and Animal Feeding Stuffs–Horizontal Method for the Enumeration of Yeasts and Molds. Part 1: Colony Count Technique in Products with Water Activity Less Than or Equal to 0.95. Geneva (Switzerland): ISO; 2008. 8 p.

Halkman AK. [Food microbiology applications]. Ankara (Türkiye): Basak Printing; 2005. 358 p. Turkish.

International Organization for Standardization. ISO 6888–1:2021. Microbiology of food and animal feeding Stuffs–Horizontal method for the enumeration of coagulase–positive staphylococci (Staphylococcus aureus and other species). Part 1: Technique using Baird–Parker agar medium. Geneva (Switzerland): ISO; 2021.2 August 2023; 20 p.

AOAC International. Official methods of analysis of AOAC International. Horwitz W, Latimer GW, editors. 18th ed. 3rd Rev. Gaithersburg (USA): AOAC International; 2010. 540 p.

Qaziyani SD, Pourfarzad A, Gheibi S, Nasiraie LR. Effect of encapsulation and wall material on the probiotic survival and physicochemical properties of synbiotic chewing gum: study with univariate and multivariate analyzes. Heliyon [Internet]. 2019; 5(7):e02144. doi: https://doi.org/m3zd

Karagöz M. [Excel and SPSS Applied Biostatistics Methods]. 9th ed. Bursa (Türkiye): Ekin Publishing Distribution; 2015. 413 p. Turkish

Tsigarida E, Skandamis P, Nychas GJ. Behavior of Listeria monocytogenes and autochthonous flora on meat stored under aerobic, vacuum and modified atmosphere packaging conditions with or without the presence of oregano essential oil at 5 oC. J. Appl. Microbiol. [Internet]. 2000; 89(6):901–909. doi: https://doi.org/ftzm4x

Skandamis PN, Nychas GJ. Effect of oregano essential oil on microbiological and physico‐chemical attributes of minced meat stored in air and modified atmospheres. J. Appl. Microbiol. [Internet]. 2001; 91(6):1011–1022. doi: https://doi.org/dnggtp

Fernández–Pan I, Carrión–Granda X, Maté JI. Antimicrobial efficiency of edible coatings on the preservation of chicken breast fillets. Food Control. [Internet]. 2014; 36(1):69–75. doi: https://doi.org/m3zf

Karam L, Roustom R, Abiad MG, El–Obeid T, Savvaidis IN. Combined effects of thymol, carvacrol and packaging on the shelf–life of marinated chicken. Int. J. Food Microbiol. [Internet]. 2019; 291:42–47. doi: https://doi.org/m3zg

Al–Hijazeen M, Mendonca A, Lee EJ, Ahn DU, White S. Fate of natural bacterial flora, and artificially inoculated Escherichia coli O157:H7, Listeria monocytogenes, and Salmonella enterica in raw ground chicken meat with added oregano oil or tannic acid alone or combined. Food Control. [Internet]. 2022; 139:109059. doi: https://doi.org/m3zh

Mahrour A, Lacroix M, Nketsa–Tabiri J, Calderon N, Gagnon M. Antimicrobial properties of natural substances in irradiated fresh poultry. Radiat. Phys. Chem. [Internet]. 1998; 52(1–6):81–84. doi: https://doi.org/dpq76x

Kaya H, Ertaş Onmaz N, Gönülalan Z, Al S. [Detection of Staphylococcus aureus and Their Enterotoxins in Poultry Meats Consumed in Kayseri]. Erciyes Üniv. Vet. Fak. Derg. [Internet]. 2015 [cited 14 Jul. 2023]; 12(2):93–98. Available in: https://goo.su/ODvbsB7

Van Haute S, Raes K, Van Der Meeren P, Sampers I. The effect of cinnamon, oregano and thyme essential oils in marinade on the microbial shelf life of fish and meat products. Food Control. [Internet]. 2016; 68:30–39. doi: https://doi.org/m3zn

Petrou S, Tsiraki M, Giatrakou V, Savvaidis IN. Chitosan dipping or oregano oil treatments, singly or combined on modified atmosphere packaged chicken breast meat. Int. J. Food Microbiol. [Internet]. 2012; 156(3):264–271. doi: https://doi.org/f32tzh

Giatrakou V, Ntzimani A, Savvaidis IN. Combined chitosan–thyme treatments with modified atmosphere packaging on a ready–to–cook poultry product. J. Food Prot. [Internet]. 2010 [cited 14 May 2023]; 73(4):663–669. Available in: https://goo.su/7Huzb

Gill CO, Harrison JCL, Penney N. The storage life of chicken carcasses packaged under carbon dioxide. Int. J. Food Microbiol. [Internet]. 1990; 11(2):151–157. doi: https://doi.org/dndbrm

Soare C, Mazeri S, McAteer S, McNeilly TN, Seguino A. Chase–Topping M The microbial condition of Scottish wild deer carcasses collected for human consumption and the hygiene risk factors associated with Escherichia coli and total coliforms contamination. Food Microbiol. [Internet]. 2022; 108:104102. doi: https://doi.org/m3zp

Fernández‐Pan I, Mendoza M, Maté JI. Whey protein isolate edible films with essential oils incorporated to improve the microbial quality of poultry. J. Sci. Food Agric. [Internet]. 2013; 93(12):2986–2994. doi: https://doi.org/f46xmg

Fernández‐Pan I, Royo M, Maté JI. Antimicrobial activity of whey protein isolate edible films with essential oils against food spoilers and foodborne pathogens. J. Food Sci. [Internet]. 2012; 77(7):383–390. doi: https://doi.org/f34mw9

Conner DE, Beuchat LR. Effects of essential oils from plants on growth of food spoilage yeasts. J. Food Sci. [Internet]. 1984; 49(2):429–434. doi: https://doi.org/fjnpp5

Khanjari A, Karabagias IK, Kontominas MG. Combined effect of N,O–carboxymethyl chitosan and oregano essential oil to extend shelf life and control Listeria monocytogenes in raw chicken meat fillets. LWT– Food Sci. Technol. [Internet]. 2013; 53(1):94–99. doi: https://doi.org/m3zq