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The combination effect of adding rosemary extract and oregano essential oil on ground chicken meat quality

Abstract

Preservative effect of oregano essential oil (OE) and rosemary extract (RE) on ground chicken meat stored at different refrigeration time had been evaluated. Six treatments were prepared: T1) Control (No additives); T2) Combination (CM1) of 100 ppm OE and 300 ppm RE; T3) CM2: 100 ppm OE + 350 ppm RE; T4) CM3: 150 ppm OE + 300 ppm RE; T5) CM4: 150 ppm OE + 350 ppm RE; T6) 14 ppm of butylated hydroxyanisole (BHA). Meat patties were individually packaged in oxygen-permeable bags stored at 4 °C, and analyzed for lipid and protein oxidation, and CIE color values at 0, 4, and 7 days. Individual cooked thigh meats were used to evaluate different sensory attributes. All additives showed significant (P < 0.05) antioxidant effect delaying lipid and protein oxidation after day 4 comparing to the control treatment samples. However, the highest significant (P < 0.05) effect among all treatments was by CM4. The CM4 was the highest stabilizing raw meat color, and preventing meat discoloration. In addition, it showed (CM4) highest overall acceptability scores values regarding sensory evaluation. Based on current results, both OE and RE had a potential antioxidant activity; however, this could be stronger if used together.

Keywords:
oregano essential oil; rosemary extract; protein oxidation; lipid oxidation; ground meat

1 Introduction

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In Jordan, these extracts are widely available in the local market (at low concentration) which applies for different purposes, such as food flavor, pharmaceutical uses, and human health etc (Oran & Al-Eisawi, 1998Oran, S., & Al-Eisawi, D. (1998). Check-list of medical plants in Jordan. Dirasat. Medical and Biological Sciences, 25(2), 84-112. Retrieved from http://vlibrary.emro.who.int/imemr/check-list-of-medicinal-plants-in-jordan
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). Generally, the antioxidant effect of these plants extracts are based on their phenolic compounds (Brewer, 2011Brewer, M. S. (2011). Natural Antioxidants: sources, compounds, mechanisms of action, and potential applications. Comprehensive Reviews in Food Science and Food Safety, 10(4), 221-247. http://dx.doi.org/10.1111/j.1541-4337.2011.00156.x.
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). For instance, antioxidant activity of oregano oil linked with their carvacrol and thymol (78-82%) and the other polyphenolic constituents (Adam et al., 1998Adam, K., Sivropoulou, A., Kokkini, S., Lanaras, T., & Arsenakis, M. (1998). Antifungal activities of Origanum vulgare subsp. hirtum, Mentha spicata, Lavandula angustifolia, and Salvia fruticosa essential oils against human pathogenic fungi. Journal of Agricultural and Food Chemistry, 46(5), 1739-1745. http://dx.doi.org/10.1021/jf9708296.
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). In addition, they are main components giving their antimicrobial effect against several food borne diseases (Ultee et al., 2002Ultee, A., Bennik, M., & Moezelaar, H. J. (2002). The phenolic hydroxyl group of carvacrol is essential for action against the food-borne pathogen Bacillus cereus. Applied and Environmental Microbiology, 68(4), 1561-1568. http://dx.doi.org/10.1128/AEM.68.4.1561-1568.2002. PMid:11916669.
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). Chouliara et al. (2007)Chouliara, E., Karatapanis, A., Savvaidis, I. N., & Kontominas, M. G. (2007). Combined effect of oregano essential oil and modified atmosphere packaging on shelf-life extension of fresh chicken breast meat, stored at 4 °C. Food Microbiology, 24(6), 607-617. http://dx.doi.org/10.1016/j.fm.2006.12.005. PMid:17418312.
http://dx.doi.org/10.1016/j.fm.2006.12.0...
found an improvement on chicken meat freshness, shelf life, and decreasing of their microbes (lactic acid bacteria, TVC, pseudomonas spp., yeast) by direct adding oregano essential oil. Rosemary extract had been analyzed of their phenolic constituent’s, and it found that carnosic acid, carnosol, rosmanol, rosmariquinone and rosmaridiphenol, ursolic acid, and caffeic acid (Aruoma et al., 1992Aruoma, O. I., Halliwell, B., Aeschbach, R., & Löligers, J. (1992). Antioxidant and pro-oxidant properties of active rosemary constituents: carnosol and carnosic acid. Xenobiotica, 22(2), 257-268. http://dx.doi.org/10.3109/00498259209046624. PMid:1378672.
http://dx.doi.org/10.3109/00498259209046...
; Basaga et al., 1997Basaga, H., Tekkaya, C., & Acikel, F. (1997). Antioxidative and free radical scavenging properties of rosemary extract. Lebensmittel-Wissenschaft + Technologie, 30(1), 105-108. http://dx.doi.org/10.1006/fstl.1996.0127.
http://dx.doi.org/10.1006/fstl.1996.0127...
) are causing their antioxidant and antimicrobial activities. In addition, RE had been documented to have anti-inflammatory, anti-diabectic and anti-cancer activities (Moreno et al., 2006Moreno, S., Scheyer, T., Romano, C. S., & Vojnov, A. A. (2006). Antioxidant and antimicrobial activities of rosemary extract linked to their polyphenol composition. Free Radical Research, 40(2), 223-231. http://dx.doi.org/10.1080/10715760500473834. PMid:16390832.
http://dx.doi.org/10.1080/10715760500473...
; Khalil et al., 2012Khalil, O. A., Ramadan, K. S., Danial, E. N., Alnahdi, H. S., & Ayaz, N. O. (2012). Antidiabetic activity of Rosemarinus officinalis and its relationship with the antioxidant property. African Journal of Pharmacy and Pharmacology, 6(14), 1031-1036.; Moore et al., 2016Moore, J., Yousef, M., & Tsiani, E. (2016). Anticancer effect of rosemary (Rosmarinus officinalis L.) extract and rosemary extract polyphenols. Nutrients, 8(11), 731. http://dx.doi.org/10.3390/nu8110731. PMid:27869665.
http://dx.doi.org/10.3390/nu8110731...
). Ninety percent of RE antioxidant properties is originated from both carnosic and carnosol constituent’s (Aruoma et al., 1992Aruoma, O. I., Halliwell, B., Aeschbach, R., & Löligers, J. (1992). Antioxidant and pro-oxidant properties of active rosemary constituents: carnosol and carnosic acid. Xenobiotica, 22(2), 257-268. http://dx.doi.org/10.3109/00498259209046624. PMid:1378672.
http://dx.doi.org/10.3109/00498259209046...
; Erkan et al., 2008Erkan, N., Ayranci, G., & Ayranci, E. (2008). Antioxidant activities of rosemary (Rosmarinus Officinalis L.) extract, blackseed (Nigella sativia L.) essential oil, carnosic acid, rosmarinic acid and sesamol. Food Chemistry, 110(1), 76-82. http://dx.doi.org/10.1016/j.foodchem.2008.01.058. PMid:26050168.
http://dx.doi.org/10.1016/j.foodchem.200...
). However, the suitable level of RE that should be use in meat system is still under investigation and affected by several factors (Al-Hijazeen & Al-Rawashdeh, 2019Al-Hijazeen, M., & Al-Rawashdeh, M. (2019). Preservative effects of rosemary extract (Rosmarinus officinalis L.) on quality and storage stability of chicken meat patties. Food Science and Technology, 39(1), 27-34. http://dx.doi.org/10.1590/1678-457x.24817.
http://dx.doi.org/10.1590/1678-457x.2481...
; Duoxia et al., 2020Duoxia, X., Zhanqun, H., Guorong, L., Yanping, C., Atikorn, P., Hang, X., & Will, D. (2020). Influence of rosemary extract addition in different phases on the oxidation of lutein and WPI in WPI-Stabilized lutein emulsions. Journal of Food Quality, 2020, 5894646. http://dx.doi.org/10.1155/2020/5894646.
http://dx.doi.org/10.1155/2020/5894646...
). Furthermore, there were no research study investigate the combination effect of Rosmarinus officinalis Linn. extract and Origanum syriacum L. essential oil (grown in Jordan), and their level, on ground chicken meat. In addition, this combination may have synergistic effect preventing rancidity development and improve meat shelf life. The objectives of current research were: 1) to evaluate the effect of adding different combination of RE and OE on broiler meat quality; 2) compare their effect with the synthetic antioxidant BHA; 3) determine the best combination level that could be use in the meat industry.

2 Materials and methods

2.1 Meat preparation

All meat were deboned, cleaned, and stored as described by Al-Hijazeen & Al-Rawashdeh (2019)Al-Hijazeen, M., & Al-Rawashdeh, M. (2019). Preservative effects of rosemary extract (Rosmarinus officinalis L.) on quality and storage stability of chicken meat patties. Food Science and Technology, 39(1), 27-34. http://dx.doi.org/10.1590/1678-457x.24817.
http://dx.doi.org/10.1590/1678-457x.2481...
. Chicken thigh meat was purchased from a local slaughtering plant and ground (twice) a through a 8-mm plate then a 3-mm plate (Moulinex, Type DKA1, France). Prepared treatments were including: T1) Control (No additives); T2) Combination (CM1) of 100 ppm OE and 300 ppm RE; T3) CM2: 100 ppm OE + 350 ppm RE; T4) CM3: 150 ppm OE + 300 ppm RE; T5) CM4: 150 ppm OE + 350 ppm RE; T6) 14 ppm of butylated hydroxyanisole (BHA). Oregano essential oil (OE) and RE concentration were chosen based on several preliminary and original meat quality studies considering their antioxidant activities (Al-Hijazeen & Al-Rawashdeh, 2019Al-Hijazeen, M., & Al-Rawashdeh, M. (2019). Preservative effects of rosemary extract (Rosmarinus officinalis L.) on quality and storage stability of chicken meat patties. Food Science and Technology, 39(1), 27-34. http://dx.doi.org/10.1590/1678-457x.24817.
http://dx.doi.org/10.1590/1678-457x.2481...
; Al-Hijazeen, 2018Al-Hijazeen, M. (2018). Effect of direct adding oregano essential oil (Origanum syriacum L.) on quality and stability of chicken meat patties. Food Science and Technology, 38(1, Suppl. 1), 123-130. http://dx.doi.org/10.1590/1678-457x.17117.
http://dx.doi.org/10.1590/1678-457x.1711...
). Oregano essential oil (Origanum syriacum L.) was purchased from a certified company (Green Fields Factory for oils, Amman/Jordan) using the most efficient purification, extraction, and steam distillation methods. The HPLC analysis (Royal Scientific Society, Jordan, Amman research institution (RSS)) of the OE showed that 76.39% of the essential oil was carvacrol. Rosemary extract (Extracted from cultivated rosemary in Jordan) was obtained from the same source, and the HPLC analysis (RSS) of the RE was measured as described by the method of Okamura et al. (1994)Okamura, N., Fujimoto, Y., Kuwabara, S., & Yagi, A. (1994). High performance liquid chromatographic determination of carnosic acid and carnosol in Rosmarinus officinalis and Salvia officinalis. Journal of Chromotagraphy A, 679(2), 381-386. http://dx.doi.org/10.1016/0021-9673(94)80582-2.
http://dx.doi.org/10.1016/0021-9673(94)8...
, and it was containing 26 ± 3% as the average of phenolic diterpenes (4% carnosol and 6% carnosic acid and other phenolic constituents). The BHA powder, RE, and OE were dissolved in 10 mL of 100% ethanol, and then mixed with 50 mL mineral oil (Sant Cruz Biotechnology, Dallas, TX, USA) to prepare their stock solution. The ethanol mixed with mineral oil was split out using a rotary evaporator (Heidolph, Model Laborota 4001-effecient) at (70 °C, 175 mbar vacuum pressure) before adding the stock to the meat mixture. All supplements were added to the ground meat, and then mixed for 4 min in a bowl mixer individually. However, they were supplemented using same quantity of mineral oil to get the same experimental conditions. The individual prepared meat patties (approximately 100 g each/4 replicate of each treatment) were packaged in oxygen-permeable bags (polyethylene, Size: 11 × 25 cm, Future for Plastic Industry, Al- Moumtaz bags, Co. L.T.D, Jordan), stored at 4 °C cooler for up to 7 days, and analyzed for lipid and protein oxidation, and CIE color values at 0, 4, and 7 days. In the cooked section, the raw meat samples were first packaged in oxygen impermeable vacuum bags (Albalabki-Jordan, Malcom SRL, Milano, Italy), and the meat were cooked in-bag in a 90 °C water bath (Memmert, WNB 14; GMbH + Co. KH, D-91107 Schwabach, Germany) until the internal temperature of the meat patties reached to 75 °C. After cooling to room temperature, meat samples (cooked) was transferred to a new oxygen-permeable bag (polyethylene, Size: 11 × 25 cm, Future for Plastic Industry, Al-Moumtaz bags, Co. L.T.D, Amman, Jordan), and stored at 4 °C for up to 7 days to be analyzed for quality parameters. Same preparation method was done for all sensory analysis treatments samples. However, the ground (raw) meat patties stored at 4 °C up to 4 days before cooking and for each evaluation session.

2.2 Color measurement

In the meat lab (Department of Animal Production); Konica Minolta Meter (CR-400, Konioca Minolta, Osaka, Japan) was used to measure meat color. The colorimeter was calibrated using an illuminant source C (Average day light) on a standard ceramic tile enveloped with the same plastic bag used for meat samples. The color values were expressed as CIE L*- (lightness), a*- (redness), and b*- (yellowness) values (American Meat Science Association, 2012American Meat Science Association – AMSA. (2012). Meat color measurement guidelines (pp. 1-117). Champaign: AMSA. Retrieved from http://www.meatscience.org
http://www.meatscience.org...
). The un-uniform (defects) color area where excluded from the targeted measurements. An average of two random readings on the top of the sample surface was used for statistical analysis.

2.3 Thiobarbituric acid-reactive substances (TBARS) measurement

Lipid oxidation in ground meat sample was determined using a TBARS method (Ahn et al., 1998Ahn, D. U., Olson, D. G., Jo, C., Chen, X., Wu, C., & Lee, J. I. (1998). Effect of muscle type, packaging, and irradiation on lipid oxidation, volatile production and color in raw pork patties. Meat Science, 49(1), 27-39. http://dx.doi.org/10.1016/S0309-1740(97)00101-0. PMid:22063182.
http://dx.doi.org/10.1016/S0309-1740(97)...
) with minor modification as described by Al-Hijazeen et al. (2016a)Al-Hijazeen, M., Lee, E. J., Mendonca, A., & Ahn, D. U. (2016a). Effect of Oregano essential oil (Origanum vulgare subsp.hirtum) on the storage stability and quality parameters of ground chicken breast meat. Antioxidant, 5(2), 18. http://dx.doi.org/10.3390/antiox5020018. PMid:27338486.
http://dx.doi.org/10.3390/antiox5020018...
. All chemicals, stock solution, and equipment were prepared before starting chemical analysis. The TBARS number was expressed as mg of malon-dialdehyde (MDA) per kg of meat.

2.4 Protein oxidation

Protein oxidation (DNPH: 2.4-Dinitrophenylhydrazine) values was estimated using the general method of total carbonyl value described by Lund et al. (2008)Lund, M. N., Hviid, M. S., Claudi-Magnussen, C., & Skibsted, L. H. (2008). Effects of dietary soybean oil on lipid and protein oxidation in pork patties during chill storage. Meat Science, 79(4), 727-733. http://dx.doi.org/10.1016/j.meatsci.2007.11.008. PMid:22063036.
http://dx.doi.org/10.1016/j.meatsci.2007...
and as reported and modified by Al-Hijazeen (2018)Al-Hijazeen, M. (2018). Effect of direct adding oregano essential oil (Origanum syriacum L.) on quality and stability of chicken meat patties. Food Science and Technology, 38(1, Suppl. 1), 123-130. http://dx.doi.org/10.1590/1678-457x.17117.
http://dx.doi.org/10.1590/1678-457x.1711...
. The carbonyl content was calculated as nmol/mg protein using absorption coefficient of 22,000/M/cm as described by Levine et al. (1994)Levine, R. L., Williams, J. A., Stadtman, E. R., & Shacter, E. (1994). Carbonyl assays for determination of oxidatively modified proteins. Methods in Enzymology, 233, 346-357. http://dx.doi.org/10.1016/S0076-6879(94)33040-9. PMid:8015469.
http://dx.doi.org/10.1016/S0076-6879(94)...
.

2.5 Sensory panel evaluation

Highly trained sensory panels (10 panelists) were used to evaluate certain sensory attributes of the ground chicken (cooked thigh) meat similarly (Same procedure, scale, and preparation method for all attributes used) as described by Al-Hijazeen & Al-Rawashdeh (2019)Al-Hijazeen, M., & Al-Rawashdeh, M. (2019). Preservative effects of rosemary extract (Rosmarinus officinalis L.) on quality and storage stability of chicken meat patties. Food Science and Technology, 39(1), 27-34. http://dx.doi.org/10.1590/1678-457x.24817.
http://dx.doi.org/10.1590/1678-457x.2481...
.

2.6 Statistical analysis

Data were analyzed using the procedures of generalized linear model (Proc. GLM, SAS program, version 9.3, 2012). Mean values and standard error of the means (SEM) were reported (SAS Institute, 2012SAS Institute. (2012). Base SAS® 9.3 procedures guide. Cary: SAS Institute.). The significance was defined at P < 0.05 and Tukey test or Tukey’s Multiple Range test were used to determine the significant differences between the mean values.

3 Results and discussion

Generally, both RE and OE have no significant effect on the ultimate pH of raw meat, and cooking loss %, as it reported in previous studies (Al-Hijazeen & Al-Rawashdeh, 2019Al-Hijazeen, M., & Al-Rawashdeh, M. (2019). Preservative effects of rosemary extract (Rosmarinus officinalis L.) on quality and storage stability of chicken meat patties. Food Science and Technology, 39(1), 27-34. http://dx.doi.org/10.1590/1678-457x.24817.
http://dx.doi.org/10.1590/1678-457x.2481...
; Al-Hijazeen, 2019Al-Hijazeen, M. (2019). Preservative effect of Origanum syriacum L. essential oil on stability and quality of cooked chicken meat. Brazilian. Journal of Poultry Science, 21(1), eRBCA-2019-0719. http://dx.doi.org/10.1590/1806-9061-2017-0719.
http://dx.doi.org/10.1590/1806-9061-2017...
). This enhance the univariate analysis between treatments especially lipid and protein oxidation measurements. Therefore, any treatments variation in this study will be due to treatments additive effect. In addition, current study is a part of meat quality and safety evaluation project (GN: 120/14/118) which designed to evaluate both OE and RE antioxidant/ antimicrobial effect using ground chicken meat.

3.1 Lipid oxidation

Among all treatments tested by TBARS method (Ahn et al., 1998Ahn, D. U., Olson, D. G., Jo, C., Chen, X., Wu, C., & Lee, J. I. (1998). Effect of muscle type, packaging, and irradiation on lipid oxidation, volatile production and color in raw pork patties. Meat Science, 49(1), 27-39. http://dx.doi.org/10.1016/S0309-1740(97)00101-0. PMid:22063182.
http://dx.doi.org/10.1016/S0309-1740(97)...
) there were no significant differences (P > 0.05) at day 0 for both raw and cooked meat mean values. However, all treatments additives showed significant antioxidant effect (P < 0.05) compared to the control samples after day 4 (Table 1). This was in agreement with previous studies (Liu et al., 2009;Liu, D. C., Tsau, R. T., Lin, Y. C., Jan, S. S., & Tan, F. J. (2009). Effect of various levels of rosemary or Chinese mahogany on the quality of fresh chicken sausage during refrigerated storage. Food Chemistry, 117(1), 106-113. http://dx.doi.org/10.1016/j.foodchem.2009.03.083.
http://dx.doi.org/10.1016/j.foodchem.200...
Kahraman et al., 2015Kahraman, T., Issa, G., Bingol, E. B., Kahraman, B. B., & Dumen, E. (2015). Effect of rosemary essential oil and modified-atmosphere packaging (MAP) on meat quality and survival of pathogens in poultry fillets. Brazilian Journal of Microbiology, 46(2), 591-599. http://dx.doi.org/10.1590/S1517-838246220131201. PMid:26273279.
http://dx.doi.org/10.1590/S1517-83824622...
; Al-Hijazeen et al., 2016aAl-Hijazeen, M., Lee, E. J., Mendonca, A., & Ahn, D. U. (2016a). Effect of Oregano essential oil (Origanum vulgare subsp.hirtum) on the storage stability and quality parameters of ground chicken breast meat. Antioxidant, 5(2), 18. http://dx.doi.org/10.3390/antiox5020018. PMid:27338486.
http://dx.doi.org/10.3390/antiox5020018...
; Al-Hijazeen & Al-Rawashdeh, 2019Al-Hijazeen, M., & Al-Rawashdeh, M. (2019). Preservative effects of rosemary extract (Rosmarinus officinalis L.) on quality and storage stability of chicken meat patties. Food Science and Technology, 39(1), 27-34. http://dx.doi.org/10.1590/1678-457x.24817.
http://dx.doi.org/10.1590/1678-457x.2481...
; Al-Hijazeen, 2019Al-Hijazeen, M. (2019). Preservative effect of Origanum syriacum L. essential oil on stability and quality of cooked chicken meat. Brazilian. Journal of Poultry Science, 21(1), eRBCA-2019-0719. http://dx.doi.org/10.1590/1806-9061-2017-0719.
http://dx.doi.org/10.1590/1806-9061-2017...
), tested different level of OE and RE using ground chicken meat. In addition, the effect of adding OE was positively extends chicken meat shelf life, decrease off-odor flavor, and delay rancidity development (Chouliara et al., 2007Chouliara, E., Karatapanis, A., Savvaidis, I. N., & Kontominas, M. G. (2007). Combined effect of oregano essential oil and modified atmosphere packaging on shelf-life extension of fresh chicken breast meat, stored at 4 °C. Food Microbiology, 24(6), 607-617. http://dx.doi.org/10.1016/j.fm.2006.12.005. PMid:17418312.
http://dx.doi.org/10.1016/j.fm.2006.12.0...
; Fasseas et al., 2008Fasseas, M. K., Mountzouris, K. C., Tarantilis, P. A., Polissiou, M., & Zervas, G. (2008). Antioxidant activity in meat treated with oregano and sage essential oils. Food Chemistry, 106(3), 1188-1194. http://dx.doi.org/10.1016/j.foodchem.2007.07.060.
http://dx.doi.org/10.1016/j.foodchem.200...
; Kumar et al., 2015Kumar, Y., Yadav, D. N., Ahmad, T., & Narsaiah, K. (2015). Recent trend in the use of natural antioxidants for meat and meat products. Comprehensive Reviews in Food Science and Food Safety, 14(6), 796-812. http://dx.doi.org/10.1111/1541-4337.12156.
http://dx.doi.org/10.1111/1541-4337.1215...
; Manessis et al., 2020Manessis, G., Kalogianni, A. I., Lazou, T., Moschovas, M., Bossis, I., & Gelasakis, A. I. (2020). Review: Plant-Derived natural antioxidants in meat and meat products. Antioxidants, 9(12), 1215. http://dx.doi.org/10.3390/antiox9121215. PMid:33276503.
http://dx.doi.org/10.3390/antiox9121215...
).

Table 1
* * TBARS value in mg malonaldehyde/kg meat. Treatments: Control (No additives); CM1:100 OE and 300 RE; CM 2:100 OE + 350 RE; CM3:150 OE + 300 RE; CM4: 150 OE + 350 RE; BHA: 14 ppm of butylatedhydroxyanisole; SEM: Standard error of the means. a-cValue with different letters within a row are significantly different (P < 0.05). n=4. x-zValue with different letters within a column are significantly different (P < 0.05). TBARS values of ground thigh meat at different storage time at 4 °C.

Cooking increase lipid oxidation (primary and secondary products) by disrupting cell membranes, and releasing more pro-oxidants (Ahn & Lee, 2002Ahn, D. U., & Lee, E. J. (2002). Production of off-odor vo.latiles from liposome-containing amino acid homopolymers by irradiation. Journal of Food Science, 67(7), 2659-2665. http://dx.doi.org/10.1111/j.1365-2621.2002.tb08795.x.
http://dx.doi.org/10.1111/j.1365-2621.20...
; Sampaio et al., 2012Sampaio, G. R., Saldanha, T., Soares, R. A., & Torres, E. A. (2012). Effect of natural antioxidant combinations on lipid oxidation in cooked chicken meat during refrigerated storage. Food Chemistry, 135(3), 1383-1390. http://dx.doi.org/10.1016/j.foodchem.2012.05.103. PMid:22953870.
http://dx.doi.org/10.1016/j.foodchem.201...
). Thus, the variation among cooked meat treatments is obvious and more significant compared to the raw meat (Ahn et al., 2009Ahn, D. U., Nam, K. C., & Lee, E. J. (2009). Lipid oxidation and flavor. In M. Du & R. J. McCormick (Eds.), Applied muscle biology and meat science (Chap. 12, pp. 227-246). Boca Raton: CRS Press. http://dx.doi.org/10.1201/b15797-13.
http://dx.doi.org/10.1201/b15797-13...
; Al-Hijazeen et al., 2016aAl-Hijazeen, M., Lee, E. J., Mendonca, A., & Ahn, D. U. (2016a). Effect of Oregano essential oil (Origanum vulgare subsp.hirtum) on the storage stability and quality parameters of ground chicken breast meat. Antioxidant, 5(2), 18. http://dx.doi.org/10.3390/antiox5020018. PMid:27338486.
http://dx.doi.org/10.3390/antiox5020018...
). Usually, cooking denatured the antioxidant enzymes, releasing the free iron to extracellular fluid, disrupt phospholipid bi-layer in cells membrane which make internal cell more susceptible for oxygen and catalysts (Gray et al., 1996Gray, J. I., Gomaa, E. A., & Buckley, D. J. (1996). Oxidative quality and shelf life of meats. Meat Science, 43, 111-123. http://dx.doi.org/10.1016/0309-1740(96)00059-9. PMid:22060645.
http://dx.doi.org/10.1016/0309-1740(96)0...
; Ahn & Lee, 2002Ahn, D. U., & Lee, E. J. (2002). Production of off-odor vo.latiles from liposome-containing amino acid homopolymers by irradiation. Journal of Food Science, 67(7), 2659-2665. http://dx.doi.org/10.1111/j.1365-2621.2002.tb08795.x.
http://dx.doi.org/10.1111/j.1365-2621.20...
). As in current study, there were no significant differences (P > 0.05) appeared between all additives at day 4 and 7 of storage time using raw thigh meat. On the other hand, CM3 and CM4 was showed the highest significant (P < 0.05) effect decreasing malonaldehyde formation in the meat samples. This may be due their high concentration (%) of both extract compared to other treatments. All combination treatments were showed higher significant (P < 0.05) effect compared to the synthetic antioxidant (BHA) at day 7 using cooked meat samples. However, synthetic BHA effect usually enhanced by adding another secondary (synergistic) antioxidant which should be considers later (Rowe et al., 2009Rowe, C. W., Pohlman, F. W., Brown, A. H. Jr., Baublits, R. T., & Johnson, Z. B. (2009). Effects of salt, BHA/BHT, and differing phosphate types on quality and sensory characteristics of beef Longissimus Muscles. Journal of Food Science, 74(4), S160-S164. http://dx.doi.org/10.1111/j.1750-3841.2009.01119.x. PMid:19490343.
http://dx.doi.org/10.1111/j.1750-3841.20...
; Sonam & Guleria, 2017Sonam, K. S., & Guleria, S. S. (2017). Review article: synergistic antioxidant activity of natural products. Annals of Pharmacology and Pharmacutics, 2(8), 1086.). This agreed with the several research studies which suggested that adding natural antioxidants in combination could be competitive to the effect of using synthetic additives (Honikel, 2008Honikel, K.-O. (2008). The use and control of nitrate and nitrite for the processing of meat products. Meat Science, 78(1-2), 68-76. http://dx.doi.org/10.1016/j.meatsci.2007.05.030. PMid:22062097.
http://dx.doi.org/10.1016/j.meatsci.2007...
; Smet et al., 2008Smet, K., Rases, K., Huyghebaert, G., Haak, L., Arnouts, S., & Smet, S. (2008). Lipid and protein oxidation of broiler meat as influenced by dietary natural antioxidant supplementation. Poultry Science, 87(8), 1682-1688. http://dx.doi.org/10.3382/ps.2007-00384. PMid:18648067.
http://dx.doi.org/10.3382/ps.2007-00384...
; Brewer, 2011Brewer, M. S. (2011). Natural Antioxidants: sources, compounds, mechanisms of action, and potential applications. Comprehensive Reviews in Food Science and Food Safety, 10(4), 221-247. http://dx.doi.org/10.1111/j.1541-4337.2011.00156.x.
http://dx.doi.org/10.1111/j.1541-4337.20...
; Oostindjer et al., 2014Oostindjer, M., Alexander, J., Amdam, G. V., Andersen, G., Bryan, N. S., Chen, D., Corpet, D. E., De Smet, S., Dragsted, L. O., Haug, A., Karlsson, A. H., Kleter, G., de Kok, T. M., Kulseng, B., Milkowski, A. L., Martin, R. J., Pajari, A.-M., Paulsen, J. E., Pickova, J., Rudi, K., Sødring, M., Weed, D. L., & Egelandsdal, B. (2014). The role of red and processed meat in colorectal cancer development: a perspective. Meat Science, 97(4), 583-596. http://dx.doi.org/10.1016/j.meatsci.2014.02.011. PMid:24769880.
http://dx.doi.org/10.1016/j.meatsci.2014...
; Hwang et al., 2014Hwang, K.-E., Kim, H.-W., Song, D.-H., Kim, Y.-J., Ham, Y.-K., Choi, Y.-S., Lee, M.-A., & Kim, C.-J. (2014). Enhanced Antioxidant Activity of Mugwort herb and vitamin C in combination on shelf-life of chicken nuggets. Han-gug Chugsan Sigpum Hag-hoeji, 34(5), 582-590. http://dx.doi.org/10.5851/kosfa.2014.34.5.582. PMid:26761491.
http://dx.doi.org/10.5851/kosfa.2014.34....
; Sonam & Guleria, 2017Sonam, K. S., & Guleria, S. S. (2017). Review article: synergistic antioxidant activity of natural products. Annals of Pharmacology and Pharmacutics, 2(8), 1086.). However, even the synergistic effect was not achieved, it was concluded that adding both OE and RE in combination (additive effect) will be better than using them separately. This antioxidant activity of these plant extract linked with the high content of poly phenolic compound (Brewer, 2011Brewer, M. S. (2011). Natural Antioxidants: sources, compounds, mechanisms of action, and potential applications. Comprehensive Reviews in Food Science and Food Safety, 10(4), 221-247. http://dx.doi.org/10.1111/j.1541-4337.2011.00156.x.
http://dx.doi.org/10.1111/j.1541-4337.20...
; Kumar et al., 2015Kumar, Y., Yadav, D. N., Ahmad, T., & Narsaiah, K. (2015). Recent trend in the use of natural antioxidants for meat and meat products. Comprehensive Reviews in Food Science and Food Safety, 14(6), 796-812. http://dx.doi.org/10.1111/1541-4337.12156.
http://dx.doi.org/10.1111/1541-4337.1215...
). Both OE and RE contain many phenolic compounds (carvacrol and thymol; carnosic and carnosol) decrease rancidity development and enhance chicken meat reducing capacity (Al-Hijazeen, 2018Al-Hijazeen, M. (2018). Effect of direct adding oregano essential oil (Origanum syriacum L.) on quality and stability of chicken meat patties. Food Science and Technology, 38(1, Suppl. 1), 123-130. http://dx.doi.org/10.1590/1678-457x.17117.
http://dx.doi.org/10.1590/1678-457x.1711...
; Al-Hijazeen & Al-Rawashdeh, 2019Al-Hijazeen, M., & Al-Rawashdeh, M. (2019). Preservative effects of rosemary extract (Rosmarinus officinalis L.) on quality and storage stability of chicken meat patties. Food Science and Technology, 39(1), 27-34. http://dx.doi.org/10.1590/1678-457x.24817.
http://dx.doi.org/10.1590/1678-457x.2481...
). The CM4 treatment showed the lowest TBARS values at day 7 using both raw and cooked meat. Finally, there was a questionable variation between many research studies evaluating RE and OE of their recommended level (Sebranek et al., 2005Sebranek, J. G., Sewalt, V. J. H., Robbins, K. L., & Houser, T. T. A. (2005). Comparison of a natural rosemary extract and BHA/BHT for relative antioxidant effectiveness in pork sausage. Meat Science, 69(2), 289-296. http://dx.doi.org/10.1016/j.meatsci.2004.07.010. PMid:22062821.
http://dx.doi.org/10.1016/j.meatsci.2004...
; Kahraman et al., 2015Kahraman, T., Issa, G., Bingol, E. B., Kahraman, B. B., & Dumen, E. (2015). Effect of rosemary essential oil and modified-atmosphere packaging (MAP) on meat quality and survival of pathogens in poultry fillets. Brazilian Journal of Microbiology, 46(2), 591-599. http://dx.doi.org/10.1590/S1517-838246220131201. PMid:26273279.
http://dx.doi.org/10.1590/S1517-83824622...
; Alhijazeen et al., 2016a; Al-Hijazeen & Al-Rawashdeh, 2019Al-Hijazeen, M., & Al-Rawashdeh, M. (2019). Preservative effects of rosemary extract (Rosmarinus officinalis L.) on quality and storage stability of chicken meat patties. Food Science and Technology, 39(1), 27-34. http://dx.doi.org/10.1590/1678-457x.24817.
http://dx.doi.org/10.1590/1678-457x.2481...
; Al-Hijazeen, 2019Al-Hijazeen, M. (2019). Preservative effect of Origanum syriacum L. essential oil on stability and quality of cooked chicken meat. Brazilian. Journal of Poultry Science, 21(1), eRBCA-2019-0719. http://dx.doi.org/10.1590/1806-9061-2017-0719.
http://dx.doi.org/10.1590/1806-9061-2017...
).

3.2 Protein oxidation

This study was using chicken thigh meat instead of breast meat since it contain more fat and myoglobin causing more significant variation between treatments (Ahn et al., 2009Ahn, D. U., Nam, K. C., & Lee, E. J. (2009). Lipid oxidation and flavor. In M. Du & R. J. McCormick (Eds.), Applied muscle biology and meat science (Chap. 12, pp. 227-246). Boca Raton: CRS Press. http://dx.doi.org/10.1201/b15797-13.
http://dx.doi.org/10.1201/b15797-13...
; Al-Hijazeen, 2019Al-Hijazeen, M. (2019). Preservative effect of Origanum syriacum L. essential oil on stability and quality of cooked chicken meat. Brazilian. Journal of Poultry Science, 21(1), eRBCA-2019-0719. http://dx.doi.org/10.1590/1806-9061-2017-0719.
http://dx.doi.org/10.1590/1806-9061-2017...
). Among all treatments, there were no significant differences (P > 0.05) between total carbonyl mean values at day 0 for both raw and cooked meat samples (Table 2).

Table 2
Effect of adding different level of OE and RE on protein oxidation of ground chicken meat during storage time.

This may be due to the low amount of total carbonyl formed when evaluating raw meat as reported by Al-Hijazeen (2018)Al-Hijazeen, M. (2018). Effect of direct adding oregano essential oil (Origanum syriacum L.) on quality and stability of chicken meat patties. Food Science and Technology, 38(1, Suppl. 1), 123-130. http://dx.doi.org/10.1590/1678-457x.17117.
http://dx.doi.org/10.1590/1678-457x.1711...
and Al-Hijazeen & Al-Rawashdeh (2019)Al-Hijazeen, M., & Al-Rawashdeh, M. (2019). Preservative effects of rosemary extract (Rosmarinus officinalis L.) on quality and storage stability of chicken meat patties. Food Science and Technology, 39(1), 27-34. http://dx.doi.org/10.1590/1678-457x.24817.
http://dx.doi.org/10.1590/1678-457x.2481...
. Similar findings were reported by Xiao et al. (2011)Xiao, S., Zhang, W. G., Lee, E. J., Ma, C. W., & Ahn, D. U. (2011). Effect of diet, packaging, and irradiation on protein oxidation, lipid oxidation, and color of raw broiler thigh meat during refrigerated storage. Poultry Science, 90(6), 1348-1357. http://dx.doi.org/10.3382/ps.2010-01244. PMid:21597078.
http://dx.doi.org/10.3382/ps.2010-01244...
who also found low total carbonyl values (0.46 to 0.80 nmol/mg protein) using raw ground chicken meat. The total carbonyl results is also agreed with several studies conducted on different meat type where the values of raw meat arranged between 1-3 nmol/mg, and 5 nmol/mg protein of cooked meat, depending on several internal/external factors (Requena et al., 2003Requena, J. R., Levine, R. L., & Stadtman, E. R. (2003). Recent advances in the analysis of oxidized proteins. Amino Acids, 25(3-4), 221-226. http://dx.doi.org/10.1007/s00726-003-0012-1. PMid:14661085.
http://dx.doi.org/10.1007/s00726-003-001...
; Estévez, 2011Estévez, M. (2011). Protein carbonyls in meat system: a review. Meat Science, 89(3), 259-279. http://dx.doi.org/10.1016/j.meatsci.2011.04.025. PMid:21621336.
http://dx.doi.org/10.1016/j.meatsci.2011...
; Sun et al., 2010Sun, W. Q., Zhang, Y. J., Zhou, G. H., Xu, X. L., & Peng, Z. Q. (2010). Effect of apple polyphenol on oxidative stability of sliced cooked cured beef and pork hams during chilled storage. Journal of Muscle Foods, 21(4), 722-737. http://dx.doi.org/10.1111/j.1745-4573.2010.00215.x.
http://dx.doi.org/10.1111/j.1745-4573.20...
). However, all supplements were showed significant (P < 0.05) effect decreasing carbonyl formation after day 4 using both raw and cooked meat. This was in agreement with previous studies evaluation both OE and RE separately (Al-Hijazeen, 2018Al-Hijazeen, M. (2018). Effect of direct adding oregano essential oil (Origanum syriacum L.) on quality and stability of chicken meat patties. Food Science and Technology, 38(1, Suppl. 1), 123-130. http://dx.doi.org/10.1590/1678-457x.17117.
http://dx.doi.org/10.1590/1678-457x.1711...
; Al-Hijazeen & Al-Rawashdeh, 2019Al-Hijazeen, M., & Al-Rawashdeh, M. (2019). Preservative effects of rosemary extract (Rosmarinus officinalis L.) on quality and storage stability of chicken meat patties. Food Science and Technology, 39(1), 27-34. http://dx.doi.org/10.1590/1678-457x.24817.
http://dx.doi.org/10.1590/1678-457x.2481...
). During the experimental period there were no significant differences (P > 0.05) between both BHA and CM1 treatments of the total carbonyl means values. The antioxidant activity of RE and OE against the formation of carbonyl compounds are well documented (Estévez et al., 2005Estévez, M., Ventanas, S., & Cava, R. (2005). Protein oxidation in frankfurters with increasing levels of added rosemary essential oil: effect on color and texture deterioration. Journal of Food Science, 70(7), c427-c432. http://dx.doi.org/10.1111/j.1365-2621.2005.tb11464.x.
http://dx.doi.org/10.1111/j.1365-2621.20...
; Jongberg et al., 2013Jongberg, S., Torngren, M. A., Gunvig, A., Skibsted, L. H., & Lund, M. N. (2013). Effect of green tea or rosemary extract on protein oxidation in Bologna type sausages prepared from oxidatively stressed pork. Meat Science, 93(3), 538-546. http://dx.doi.org/10.1016/j.meatsci.2012.11.005. PMid:23273462.
http://dx.doi.org/10.1016/j.meatsci.2012...
; Kumar et al., 2015Kumar, Y., Yadav, D. N., Ahmad, T., & Narsaiah, K. (2015). Recent trend in the use of natural antioxidants for meat and meat products. Comprehensive Reviews in Food Science and Food Safety, 14(6), 796-812. http://dx.doi.org/10.1111/1541-4337.12156.
http://dx.doi.org/10.1111/1541-4337.1215...
; Al-Hijazeen & Al-Rawashdeh, 2019Al-Hijazeen, M., & Al-Rawashdeh, M. (2019). Preservative effects of rosemary extract (Rosmarinus officinalis L.) on quality and storage stability of chicken meat patties. Food Science and Technology, 39(1), 27-34. http://dx.doi.org/10.1590/1678-457x.24817.
http://dx.doi.org/10.1590/1678-457x.2481...
). The antioxidant mechanism of these extracts (RE & OE) are highly depends on their content of phenols. These phenolic compounds surrounding by several OH group which work as hydrogen donor, and retarding the initial auto-oxidation process (Lee et al., 2003Lee, K. W., Everts, H., Kappert, H. J., Frehner, M., Losa, R., & Beynen, A. (2003). Effects of dietary essential oil components on growth performance, digestive enzymes and lipid metabolism in female broiler chickens. British Poultry Science, 44(3), 450-457. http://dx.doi.org/10.1080/0007166031000085508. PMid:12964629.
http://dx.doi.org/10.1080/00071660310000...
; Estévez et al., 2005Estévez, M., Ventanas, S., & Cava, R. (2005). Protein oxidation in frankfurters with increasing levels of added rosemary essential oil: effect on color and texture deterioration. Journal of Food Science, 70(7), c427-c432. http://dx.doi.org/10.1111/j.1365-2621.2005.tb11464.x.
http://dx.doi.org/10.1111/j.1365-2621.20...
; Manessis et al., 2020Manessis, G., Kalogianni, A. I., Lazou, T., Moschovas, M., Bossis, I., & Gelasakis, A. I. (2020). Review: Plant-Derived natural antioxidants in meat and meat products. Antioxidants, 9(12), 1215. http://dx.doi.org/10.3390/antiox9121215. PMid:33276503.
http://dx.doi.org/10.3390/antiox9121215...
). In addition, it is also correlated with the TBARS results as it agreed by Al-Hijazeen et al. (2016aAl-Hijazeen, M., Lee, E. J., Mendonca, A., & Ahn, D. U. (2016a). Effect of Oregano essential oil (Origanum vulgare subsp.hirtum) on the storage stability and quality parameters of ground chicken breast meat. Antioxidant, 5(2), 18. http://dx.doi.org/10.3390/antiox5020018. PMid:27338486.
http://dx.doi.org/10.3390/antiox5020018...
, bAl-Hijazeen, M., Lee, E. J., Mendonca, A., & Ahn, D. U. (2016b). Effects of tannic acid on lipid and protein oxidation, color, and volatiles of raw and cooked chicken breast meat during storage. Antioxidant, 5(2), 19. http://dx.doi.org/10.3390/antiox5020019. PMid:27304971.
http://dx.doi.org/10.3390/antiox5020019...
) done previously, and several related studies (Howell et al., 2001Howell, N. K., Herman, H., & Li-Chan, E. C. Y. (2001). Elucidation of protein-lipid interactions in lysozyme – Corn oil system by Fourier transform Raman spectroscopy. Journal of Agricultural and Food Chemistry, 49(3), 1529-1533. http://dx.doi.org/10.1021/jf001115p. PMid:11312891.
http://dx.doi.org/10.1021/jf001115p...
; Lund et al., 2011Lund, M. N., Heinonen, M., Baron, C. P., & Estévez, M. (2011). Protein oxidation in muscle food: a review. Molecular Nutrition & Food Research, 55(1), 83-95. http://dx.doi.org/10.1002/mnfr.201000453. PMid:21207515.
http://dx.doi.org/10.1002/mnfr.201000453...
; Estévez, 2011Estévez, M. (2011). Protein carbonyls in meat system: a review. Meat Science, 89(3), 259-279. http://dx.doi.org/10.1016/j.meatsci.2011.04.025. PMid:21621336.
http://dx.doi.org/10.1016/j.meatsci.2011...
).

Furthermore, the highest significant (P < 0.05) antioxidant effect were appeared using CM3 and CM4 additives compared to the other treatments using cooked meat samples at day 4 and 7. Overall, total carbonyl values were higher using cooked meat compared to the raw meat samples. This might be due to the loss of the antioxidant capacity and the denaturation of meat protein during cooking (Ahn & Lee, 2002Ahn, D. U., & Lee, E. J. (2002). Production of off-odor vo.latiles from liposome-containing amino acid homopolymers by irradiation. Journal of Food Science, 67(7), 2659-2665. http://dx.doi.org/10.1111/j.1365-2621.2002.tb08795.x.
http://dx.doi.org/10.1111/j.1365-2621.20...
; Fasseas et al., 2008Fasseas, M. K., Mountzouris, K. C., Tarantilis, P. A., Polissiou, M., & Zervas, G. (2008). Antioxidant activity in meat treated with oregano and sage essential oils. Food Chemistry, 106(3), 1188-1194. http://dx.doi.org/10.1016/j.foodchem.2007.07.060.
http://dx.doi.org/10.1016/j.foodchem.200...
; Serpen et al., 2012Serpen, A., Gokmen, V., & Fogliano, V. (2012). Total antioxidant capacities of raw and cooked meats. Meat Science, 90(1), 60-65. http://dx.doi.org/10.1016/j.meatsci.2011.05.027. PMid:21684086.
http://dx.doi.org/10.1016/j.meatsci.2011...
). This also explains why cooked meat showed more variation between treatments compared to the raw meat in current study.

3.3 Meat color

Chicken thigh meat were used to evaluate the antioxidant effect, since it contain high myoglobin and lipid percentage which give better significances compared to the breast meat (Al-Hijazeen, 2014Al-Hijazeen, M. (2014). Effect of oregano essential oil and tannic acid on storage stability and quality of ground chicken meat (Doctoral dissertation). Iowa State University, Ames. Retrieved from http://lib.dr.iastate.edu/etd/13966
http://lib.dr.iastate.edu/etd/13966...
). There were no significant differences (P > 0.05) among all treatments means values of all color parameters (a*, L*, and b*) at day 0 of storage time (Table 3). This confirms that there were no treatments direct-effects on myoglobin chemical status or color values after mixing. This finding agreed with Al-Hijazeen et al. (2016a)Al-Hijazeen, M., Lee, E. J., Mendonca, A., & Ahn, D. U. (2016a). Effect of Oregano essential oil (Origanum vulgare subsp.hirtum) on the storage stability and quality parameters of ground chicken breast meat. Antioxidant, 5(2), 18. http://dx.doi.org/10.3390/antiox5020018. PMid:27338486.
http://dx.doi.org/10.3390/antiox5020018...
and Al-Hijazeen & Al-Rawashdeh (2019)Al-Hijazeen, M., & Al-Rawashdeh, M. (2019). Preservative effects of rosemary extract (Rosmarinus officinalis L.) on quality and storage stability of chicken meat patties. Food Science and Technology, 39(1), 27-34. http://dx.doi.org/10.1590/1678-457x.24817.
http://dx.doi.org/10.1590/1678-457x.2481...
where OE, and RE additives used to evaluate its separate antioxidant effect. The L* and a* values were decreased significantly (P < 0.05) during storage time (0-7 days) among all samples of control treatment. This agreed with several research studies conducted on measuring fresh meat color (Chouliara et al., 2007Chouliara, E., Karatapanis, A., Savvaidis, I. N., & Kontominas, M. G. (2007). Combined effect of oregano essential oil and modified atmosphere packaging on shelf-life extension of fresh chicken breast meat, stored at 4 °C. Food Microbiology, 24(6), 607-617. http://dx.doi.org/10.1016/j.fm.2006.12.005. PMid:17418312.
http://dx.doi.org/10.1016/j.fm.2006.12.0...
; Al-Hijazeen et al., 2016aAl-Hijazeen, M., Lee, E. J., Mendonca, A., & Ahn, D. U. (2016a). Effect of Oregano essential oil (Origanum vulgare subsp.hirtum) on the storage stability and quality parameters of ground chicken breast meat. Antioxidant, 5(2), 18. http://dx.doi.org/10.3390/antiox5020018. PMid:27338486.
http://dx.doi.org/10.3390/antiox5020018...
; Al-Hijazeen & Al-Rawashdeh, 2019Al-Hijazeen, M., & Al-Rawashdeh, M. (2019). Preservative effects of rosemary extract (Rosmarinus officinalis L.) on quality and storage stability of chicken meat patties. Food Science and Technology, 39(1), 27-34. http://dx.doi.org/10.1590/1678-457x.24817.
http://dx.doi.org/10.1590/1678-457x.2481...
). The decrease in a* values during storage is based on what happen through discoloration process, and the increase in met-myoglobin pigment formation (Mancini & Hunt, 2005Mancini, R. A., & Hunt, M. C. (2005). Current research in meat color. Meat Science, 71(1), 100-121. http://dx.doi.org/10.1016/j.meatsci.2005.03.003. PMid:22064056.
http://dx.doi.org/10.1016/j.meatsci.2005...
; Keokamnerd et al., 2008Keokamnerd, T., Acton, J. C., Han, I. Y., & Dawson, P. L. (2008). Effect of commercial rosemary oleoresin preparations on ground chicken thigh meat quality packaged in a high-oxygen atmosphere. Poultry Science, 87(1), 170-179. http://dx.doi.org/10.3382/ps.2007-00066. PMid:18079467.
http://dx.doi.org/10.3382/ps.2007-00066...
). The L* values was significantly (P < 0.05) higher using CM4 compared to the control samples at day 4 and 7 of storage (at 4 °C) time. However, there were no significant differences (P > 0.05) appeared between all treatments additives at day 4 of storage time using L* value. The CM4 showed the highest stabilizing effect on the L* value of the ground chicken meat compared to the other treatments. Similar trend in a* values appeared, and there were no significant differences (P > 0.05) between these treatments additives. However the CM4 showed the highest effect maintaining meat color stability, and preventing their discoloration. The ability of RE and OE to maintain meat redness during storage are highly documented and well evaluated (Estévez et al., 2005Estévez, M., Ventanas, S., & Cava, R. (2005). Protein oxidation in frankfurters with increasing levels of added rosemary essential oil: effect on color and texture deterioration. Journal of Food Science, 70(7), c427-c432. http://dx.doi.org/10.1111/j.1365-2621.2005.tb11464.x.
http://dx.doi.org/10.1111/j.1365-2621.20...
; Keokamnerd et al., 2008Keokamnerd, T., Acton, J. C., Han, I. Y., & Dawson, P. L. (2008). Effect of commercial rosemary oleoresin preparations on ground chicken thigh meat quality packaged in a high-oxygen atmosphere. Poultry Science, 87(1), 170-179. http://dx.doi.org/10.3382/ps.2007-00066. PMid:18079467.
http://dx.doi.org/10.3382/ps.2007-00066...
; Kumar et al., 2015Kumar, Y., Yadav, D. N., Ahmad, T., & Narsaiah, K. (2015). Recent trend in the use of natural antioxidants for meat and meat products. Comprehensive Reviews in Food Science and Food Safety, 14(6), 796-812. http://dx.doi.org/10.1111/1541-4337.12156.
http://dx.doi.org/10.1111/1541-4337.1215...
; Al-Hijazeen et al., 2016aAl-Hijazeen, M., Lee, E. J., Mendonca, A., & Ahn, D. U. (2016a). Effect of Oregano essential oil (Origanum vulgare subsp.hirtum) on the storage stability and quality parameters of ground chicken breast meat. Antioxidant, 5(2), 18. http://dx.doi.org/10.3390/antiox5020018. PMid:27338486.
http://dx.doi.org/10.3390/antiox5020018...
; Al-Hijazeen & Al-Rawashdeh, 2019Al-Hijazeen, M., & Al-Rawashdeh, M. (2019). Preservative effects of rosemary extract (Rosmarinus officinalis L.) on quality and storage stability of chicken meat patties. Food Science and Technology, 39(1), 27-34. http://dx.doi.org/10.1590/1678-457x.24817.
http://dx.doi.org/10.1590/1678-457x.2481...
). This anti-discoloration ability is linked to their polyphenolic content as it discussed before. However, the antioxidant activity of natural RE or OE may enhance when adding them in combination (Georgantelis et al., 2007Georgantelis, D., Ambrosiadis, I., Katikou, P., Blekas, G., & Georgakis, S. A. (2007). Effect of rosemary extract, chitosan and α-tocopherol on microbiological parameters and lipid oxidation of fresh pork sausage stored at 4 °C. Meat Science, 76(1), 172-181. http://dx.doi.org/10.1016/j.meatsci.2006.10.026. PMid:22064204.
http://dx.doi.org/10.1016/j.meatsci.2006...
; Nieto, 2017Nieto, G. (2017). Review: biological activities of three essential oils of the lamiaceae family. Medicines, 4(3), 63. http://dx.doi.org/10.3390/medicines4030063. PMid:28930277.
http://dx.doi.org/10.3390/medicines40300...
; Sonam & Guleria, 2017Sonam, K. S., & Guleria, S. S. (2017). Review article: synergistic antioxidant activity of natural products. Annals of Pharmacology and Pharmacutics, 2(8), 1086.).

Table 3
*CIE Color value of ground chicken thigh meat with different level of OE and RE during storage at 4 °C.

Generally, natural antioxidant activity will increase with higher content of phenolic compounds (Kumar et al., 2015Kumar, Y., Yadav, D. N., Ahmad, T., & Narsaiah, K. (2015). Recent trend in the use of natural antioxidants for meat and meat products. Comprehensive Reviews in Food Science and Food Safety, 14(6), 796-812. http://dx.doi.org/10.1111/1541-4337.12156.
http://dx.doi.org/10.1111/1541-4337.1215...
; Al-Hijazeen, 2014Al-Hijazeen, M. (2014). Effect of oregano essential oil and tannic acid on storage stability and quality of ground chicken meat (Doctoral dissertation). Iowa State University, Ames. Retrieved from http://lib.dr.iastate.edu/etd/13966
http://lib.dr.iastate.edu/etd/13966...
; Botsoglou et al., 2003Botsoglou, N. A., Govaris, A., Botsoglou, E. N., Grigoropoulou, S. H., & Papageorgiou, G. (2003). Antioxidant activity of dietary oregano essential oil and alpha-tocopheryl acetate supplementation in long-term frozenstored turkey meat. Journal of Agricultural and Food Chemistry, 51(10), 2930-2936. http://dx.doi.org/10.1021/jf021034o. PMid:12720373.
http://dx.doi.org/10.1021/jf021034o...
). This may explain the higher effect of the combination (CM4) treatment maintaining meat color compared to the other additives. However, there were no significant differences (P > 0.05) between the CM4 and BHA treatment through a* and L* values at day 7 of storage time. Finally, there were no significant differences (P > 0.05) among all treatments at day 0, and 7 regarding b* values. In addition, b* values were increased significantly (P < 0.05) using all treatments (CM and BHA) levels during storage time.

3.4 Sensory evaluation

Among all treatments, BHA and CM4 showed the highest cooked color attribute scores compared to the other treatments (Table 4). This was due to the ability of these extracts decreasing lipid and protein oxidation which affect overall meat quality and their protein functionality (Estévez et al., 2005Estévez, M., Ventanas, S., & Cava, R. (2005). Protein oxidation in frankfurters with increasing levels of added rosemary essential oil: effect on color and texture deterioration. Journal of Food Science, 70(7), c427-c432. http://dx.doi.org/10.1111/j.1365-2621.2005.tb11464.x.
http://dx.doi.org/10.1111/j.1365-2621.20...
; Al-Hijazeen, 2014Al-Hijazeen, M. (2014). Effect of oregano essential oil and tannic acid on storage stability and quality of ground chicken meat (Doctoral dissertation). Iowa State University, Ames. Retrieved from http://lib.dr.iastate.edu/etd/13966
http://lib.dr.iastate.edu/etd/13966...
; Al-Hijazeen & Al-Rawashdeh, 2019Al-Hijazeen, M., & Al-Rawashdeh, M. (2019). Preservative effects of rosemary extract (Rosmarinus officinalis L.) on quality and storage stability of chicken meat patties. Food Science and Technology, 39(1), 27-34. http://dx.doi.org/10.1590/1678-457x.24817.
http://dx.doi.org/10.1590/1678-457x.2481...
).

Table 4
Sensory attributes means values of cooked ground thigh chicken meat.

The spice odor was more intense in all samples of CM1, CM2, CM3, and CM4 and significantly (P < 0.05) differ from the other treatments (BHA and Control). The panelists easily distinguish the odor of these plant extracts due to their volatile compounds. However, the highest spice odor was detected in CM4 treatment samples compared to the other additives (CM1-3). This connected with the effect of extracts concentration of both OE and RE among all treatments. Based on the sensory panel of the oxidation odor attribute, all treatments additives were showed lower significant (P < 0.05) values compared to the control. In addition, CM4 showed the highest effect decreasing the rancidity development and their off odor. This was in agreement with previous research studies which used different plants essential oils as meat preservation (Al-Hijazeen, 2014Al-Hijazeen, M. (2014). Effect of oregano essential oil and tannic acid on storage stability and quality of ground chicken meat (Doctoral dissertation). Iowa State University, Ames. Retrieved from http://lib.dr.iastate.edu/etd/13966
http://lib.dr.iastate.edu/etd/13966...
; Al-Hijazeen & Al-Rawashdeh, 2019Al-Hijazeen, M., & Al-Rawashdeh, M. (2019). Preservative effects of rosemary extract (Rosmarinus officinalis L.) on quality and storage stability of chicken meat patties. Food Science and Technology, 39(1), 27-34. http://dx.doi.org/10.1590/1678-457x.24817.
http://dx.doi.org/10.1590/1678-457x.2481...
; Al-Hijazeen, 2019Al-Hijazeen, M. (2019). Preservative effect of Origanum syriacum L. essential oil on stability and quality of cooked chicken meat. Brazilian. Journal of Poultry Science, 21(1), eRBCA-2019-0719. http://dx.doi.org/10.1590/1806-9061-2017-0719.
http://dx.doi.org/10.1590/1806-9061-2017...
). The antioxidant activity of OE and RE enhances meat shelf life by retarding the aldehydes, sulfuric, and hydrocarbons compounds which are responsible on the chicken meat rancidity and their off-odor volatiles (Ahn et al., 2009Ahn, D. U., Nam, K. C., & Lee, E. J. (2009). Lipid oxidation and flavor. In M. Du & R. J. McCormick (Eds.), Applied muscle biology and meat science (Chap. 12, pp. 227-246). Boca Raton: CRS Press. http://dx.doi.org/10.1201/b15797-13.
http://dx.doi.org/10.1201/b15797-13...
). Furthermore, phenolic compounds of both OE and RE delay or prevent the formation of new free radicals during the initiation step of auto-oxidation process (Moreno et al., 2006Moreno, S., Scheyer, T., Romano, C. S., & Vojnov, A. A. (2006). Antioxidant and antimicrobial activities of rosemary extract linked to their polyphenol composition. Free Radical Research, 40(2), 223-231. http://dx.doi.org/10.1080/10715760500473834. PMid:16390832.
http://dx.doi.org/10.1080/10715760500473...
; Keokamnerd et al., 2008Keokamnerd, T., Acton, J. C., Han, I. Y., & Dawson, P. L. (2008). Effect of commercial rosemary oleoresin preparations on ground chicken thigh meat quality packaged in a high-oxygen atmosphere. Poultry Science, 87(1), 170-179. http://dx.doi.org/10.3382/ps.2007-00066. PMid:18079467.
http://dx.doi.org/10.3382/ps.2007-00066...
; Kumar et al., 2015Kumar, Y., Yadav, D. N., Ahmad, T., & Narsaiah, K. (2015). Recent trend in the use of natural antioxidants for meat and meat products. Comprehensive Reviews in Food Science and Food Safety, 14(6), 796-812. http://dx.doi.org/10.1111/1541-4337.12156.
http://dx.doi.org/10.1111/1541-4337.1215...
). These finding is agreed and linked with the previous chemical analysis (TBARS and DNPH) results during refrigerated storage time. Over all, the CM3 and CM4 treatments showed the highest acceptability attribute scores compared to the other treatments. The positive effect of adding RE and OE on different sensory attributes had been reported in previous research studies done on different meat preparation (Thongtan et al., 2005Thongtan, K., Toma, R. B., Reiboldt, W., & Daoud, A. (2005). Effect of rosemary extract on lipid oxidation and sensory evaluation of frozen, precooked beef patties. Journal of Foodservice, 16(3-4), 93-104. http://dx.doi.org/10.1111/j.1745-4506.2005.00013.x.
http://dx.doi.org/10.1111/j.1745-4506.20...
; Al-Hijazeen, 2014Al-Hijazeen, M. (2014). Effect of oregano essential oil and tannic acid on storage stability and quality of ground chicken meat (Doctoral dissertation). Iowa State University, Ames. Retrieved from http://lib.dr.iastate.edu/etd/13966
http://lib.dr.iastate.edu/etd/13966...
; Feng et al., 2016Feng, L., Shi, C., Bei, Z., Li, Y., Yuan, D., Gong, Y., & Han, J. (2016). Rosemary extract in combination with Polylysine enhance the quality of chicken breast muscle during refrigerated storage. International Journal of Food Properties, 19(10), 2338-2348. http://dx.doi.org/10.1080/10942912.2015.1130053.
http://dx.doi.org/10.1080/10942912.2015....
; Al-Hijazeen & Al-Rawashdeh, 2019Al-Hijazeen, M., & Al-Rawashdeh, M. (2019). Preservative effects of rosemary extract (Rosmarinus officinalis L.) on quality and storage stability of chicken meat patties. Food Science and Technology, 39(1), 27-34. http://dx.doi.org/10.1590/1678-457x.24817.
http://dx.doi.org/10.1590/1678-457x.2481...
). Finally, CM4 could be a good replacement to the synthetic BHA, and it may have superior characteristics such as flavor, anti-deterioration effect, and more consumer acceptability.

4 Conclusions

Adding OE and RE were showed significant (P < 0.05) antioxidant effect when testing meat TBARS, DNPH, and color’s values. Adding these extracts improves both ground meat shelf life, freshness, and their quality. However, the inclusion of CM4 (150 ppm OE and 350 ppm RE) showed the highest antioxidant effect compared to the other treatments. Similar trend found by the CM4 among all sensory attributes used. Generally, The CM4 was the best compared to the other treatments regarding all parameters used. Overall, the combination of RE and OE could form a good promising in the future of meat industry. In addition, it could be a good natural replacement or partial substitution to the synthetic one. However, their interaction with different food system must consider for recommendation purposes.

Acknowledgements

The Author would like to thank all of the financially support by the Deanship of Scientific Research at Mutah University, Al-karak, Jordan. Grant number: 120/14/118. This funding is highly appreciated with my deep thankful to all other Animal Science Department stuff on their technical assistance and expert advices.

  • Practical Application: Improving ground meat shelf-life and their quality using combined natural plants extracts.

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Publication Dates

  • Publication in this collection
    26 Feb 2021
  • Date of issue
    2022

History

  • Received
    14 Oct 2020
  • Accepted
    06 Jan 2021
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