Lipid oxidation, total volatiles, and sensory evaluation of cooked chicken meat treated with Origanum syriacum L. essential oil

Marwan Al-Hijazeen

doi:10.3136/fstr.FSTR-D-21-00300

Abstract

The effect of Origanum syriacum L. essential oil (OE) on lipid oxidation, total volatiles, and sensory evaluation of cooked chicken meat was investigated. The treatments applied were 1) Control; 2) 200 ppm oregano essential oil (OE_L1); 3) 250 ppm (OE_L2); 4) 150 ppm sodium nitrite (E-250); and 5) 14 ppm butylated hydroxyanisole (BHA) mixed with ground chicken thigh meat. The raw meat was cooked, stored under refrigeration, and analyzed for lipid oxidation and total volatiles after 0, 4, and 8 days. In addition, cooked thigh meat patties were prepared separately for evaluation of specific sensory attributes. Generally, OE_L2 was the most comparable additive to the synthetic E-250 regarding TBARS values. The total volatile (TV) profile showed that E-250 and OE_L2 were the most effective at decreasing off odor volatiles (p < 0.05). Sensory data also revealed the greatest improvement in overall meat acceptability with the use of OE_L2. The recommended level of OE in cooked chicken meat is approximately 250 ppm.

Introduction

The idea of using natural instead of synthetic meat preservatives has been established and developed over the last two decades (Abdel-Hamied et al., 2009; Kumar et al., 2015; Fruet et al., 2020). There are several rationales behind this approach; for example, using synthetic antioxidants (SA) as food preservatives (BHA, butylated hydroxyanisole; BHT, butylated hydroxytoluene; TBHQ, tertiary butyl hydroquinone; etc.) may cause cancers and have a toxicological effect with long-term human consumption (Velasco and Williams, 2011; Kumar et al., 2015; Manessis et al., 2020). In addition, increasing consumer demand for natural and organic food products is also encouraging meat scientists to meet this goal (Taghvaei and Jafari, 2015; Manessis et al., 2020). Researchers have investigated many natural additives, such as medicinal plants (sage, rosemary, thyme, green tea, and oregano) and their extracts (Al-Hijazeen, 2019; Al-Hijazeen and Al-Rawasheh, 2019; Beya et al., 2021; Nieto, 2020). Oregano essential oil (OE) was found at the top of this list of additives and can have a significant direct effect as a meat preservative (Zheng and Wang, 2001; Al-Hijazeen, 2019; Hać-Szymańczuk et al., 2019). However, Origanum syriacum L. (Grown in Jordan; commonly known Za'atar) contains unique polyphenolic compounds that support this application compared with other species (Daouk et al., 1995; Tepe et al., 2004; Ibrahim et al., 2012a, b). Generally, preparing meat products without using synthetic sodium nitrite (E-250) could be the most difficult and challenging method in the meat safety and preservation sector. However, reduction of E-250 addition or partial substitution with natural additives (NA) could be a possible solution. Despite their positive effects, E-250 may negatively affect human health if not used in the appropriate way, causing the formation of nitrosamines (N-Nitroso compounds), which are considered carcinogenic initiators (Sebranek and Bacus, 2007; Oostindjer et al., 2014; Karwowska and Kononiuk, 2020). However, many difficulties appear to determine the best recommended OE level for industrial purposes (Al-Hijazeen, 2019; Nieto, 2020). For example, the variation in antioxidant activity is affected by several factors, such as genetics, the season, temperature, moisture, soil, and daylight length (Ceylan et al., 2003; Viuda-Martos et al., 2010; Ibrahim et al., 2012b; Kosakowska et al., 2021). The oregano herb plant is found as a variety of species all over the world, which differ in their essential oil percentage and composition (Ibrahim et al., 2012b; Kosakowska et al., 2021). Origanum syriacum L. (Wild Jordanian species) essential oil was analyzed and reported as a strong natural antioxidant source that can improve meat preservation compared with other species (Al-Hijazeen, 2019; Al-Hijazeen, 2022a, b). In addition, a unique and strong antioxidant effect of Origanum syriacum L. compared with that of other species (e.g., Origanum vulgare, Origanum onties, and Origanum majorana L.) was also documented (Daouk, et al., 1995; Berna'th, 1997; Baser, 2002; Sahin et al., 2004; Al-Hijazeen, 2022a). Very few studies have been conducted to evaluate the effect of adding Jordanian oregano (Origanum syriacum L.) essential oil on lipid oxidation, volatile compound formation (volatile profile), and sensory attributes at the recommended level. Several volatiles were formed during storage of cooked meat, affecting their odor, flavor, and shelf life. For example, aldehydes (e.g., hexanal, pentanal, propanol), sulfuric (e.g., dimethyl disulfide, carbon disulfide) ketones, and other hydrocarbon (hexane, heptane, octane, cyclohexane) compounds play major roles in cooked meat quality (Al-Hijazeen et al., 2016a; Al-Hijazeen et al., 2016b; Insausti et al., 2021). In addition, the quantity and quality of these volatiles gives a good indication and is well correlated with lipid oxidation (TBARS) and other sensory attributes such as off-odor and -flavor (Al-Hijazeen et al., 2016a; Mancinelli et al., 2021). The development of lipid auto-oxidation, primary lipid oxidation, and secondary compounds formed along with antioxidant additives needs further investigation. However, an excellent conclusion could be obtained if it was connected with the major volatiles that affect rancidity development in cooked meat. Thus, the current study was conducted to 1) evaluate the effect of adding different levels of Origanum syriacum L. essential oil on lipid oxidation, the total volatile profile, and sensory attributes of cooked broiler meat and 2) compare this unique level with the synthetic antioxidant (E-250) currently used in the meat processing industry.

Materials and Methods

Essential oil composition of Origanum syriacum L. The thymol and carvacrol composition of Oregano essential oil (OE) (four samples in duplicate) was measured at the Royal Scientific Society, Amman, Jordan research institute by the method of Zekovic et al. (2000). A High-Performance Liquid Chromatography (HPLC) isocratic system (Shimadzu, Japan) was used. The chromatographic system was equipped with a controller system: Shimadzu Corporation, CBM-20A, an Auto-Sampler (SIL-20AC), a variable wavelength ultraviolet/visible detector (Shimadzu, Model SPD-10Avp, Japan), an insulated column oven (CTO-20AC, Shimadzu Corporation, Tokyo, Japan), and a pumping system (LC-20AD, Shimadzu Corporation, Japan).

Preparation of meat samples Meat samples were prepared at Mutah University (Agriculture Collage/Department of Animal Production) according to the method of Al-Hijazeen and Al-Rawashdeh. (2019). First, broiler thigh meat was obtained from the animal research facility. All birds had been evaluated and veterinary checked before the slaughtering process. This study was the last stage (Phase III) in series of studies (Project number: 120/14/118), which also depends on previous results. Meat carcasses were immersed in ice water (4 °C) in a refrigerated cooling area. After cleaning, skin removal, and deboning protocols, the meat was immediately vacuum packaged in oxygen-impermeable plastic bags. The frozen meat was stored at −18 °C using fast freezing chambers until use. Subsequently, the lean meat was thawed and then double ground using 8-mm and 3-mm plates (Moulinex, Type DKA1, France) as per USDA standard guidelines for meat preparation. Five treatments were prepared, including 1) Control (without additives), 2) 200 ppm of OE_L1, 3) 250 ppm of OE_L2, 4) 150 ppm of sodium nitrite (E-250), and 5) 14 ppm of BHA. Oregano essential oil (OE) was purified and extracted by Green Field Factory for oils, Amman, Jordan (Certified by Jordan Food and Drug Administration-JFDA). Sodium nitrite (Gainland Chemical Company-GCC, factory road; UK) powder was solubilized using distilled water and then mixed with mineral oil to form a stock emulsion ready to be mixed with the ground meat.

In addition, OE and BHA were dissolved in ethanol (100%) and then mixed with mineral oil to prepare working solutions. However, the ethanol was removed from the stock solution using a rotary evaporator (Heidoph, Model Laborota 4001-efficient) at 70 °C and a vacuum pressure of 175 mbar. All additives were mixed for 3 min with the ground meat using a bowl mixer (Model KM-331; Kenwood Limited, New Lane, Havant, PO9 2NH, UK). In addition, all treatments were batch prepared to contain the same amount of mineral oil and water before meat patty preparation. The ultimate pH and proximate composition of individual raw meat samples from each treatment batch were checked before cooking. In the cooking part, the raw meat patties were first packaged in oxygen-impermeable vacuum bags (Ehsan and Tahssin Baalbaki CO, Bayader Wadi Al-Seer, Amman, Jordan) and then cooked in-bag at 90 °C in a water bath (Memmert, WNB 14; GMbH + Co. KH, D-91107 Schwabach, Germany) to obtain an internal temperature of 75 °C. Finally, all meat patties (100 g) were cooled, transferred to new oxygen-permeable bags (polyethylene, Size : 11 × 25 cm, Future for Plastic Industry, Al-Moumtaz bags, Co. L.T.D, Amman, Jordan), and stored at 4 °C to be analyzed for TBARS and total volatiles at 0, 4, and 8 days. Separate samples were used to evaluate cooking loss percentage and sensory attributes according to the previous protocol (lipid oxidation part).

Cooking loss%, proximate composition, and ultimate pH of raw meat The proximate composition of all batches of (fresh) meat treatments were analyzed to determine the average percentages of fat, protein, water, and ash before cooking preparation. However, samples from each treatment (two sub-samples from each batch) (n = 4) were used and analyzed according to standard methods (AOAC, 2000). The final pH of raw meat and the cooking loss% were measured as reported by Al-Hijazeen and Al-Rawashdeh (2019).

Thiobarbituric acid-reactive substances (TBARS) for lipid oxidation Lipid oxidation of cooked meat samples was determined using a TBARS method with minor modifications as described by Ahn et al. (1998). The TBARS number was expressed as milligrams of malondialdehyde (MDA) per kilogram of meat.

Total volatiles (cooked thigh meat profile) Total volatile analysis was performed at the Royal Scientific Society, Department of Gas Laboratory, Amman, Jordan by experts and highly qualified specialists. Volatiles of cooked meat samples were analyzed using a GC-MS (QP2010_nc System, Shimadzu Corporation, Japan) connected to a purge and trap concentrator (O·I·Analytical, Eclipse; Model 4660), as described by Ahn et al. (2001). All treatment samples were obtained from the same meat patties, which were used for the TBARS test at each set time interval. The sample (2 g of cooked thigh meat) was placed in a 40-mL sample vial, flushed with helium gas (40 psi) for 3 s, and then capped airtight with a Teflon*fluorocarbon resin/silicone septum (ALWSCI, No. 16 Plant Building, Yuexing Technology Innovation Park, Binhai New City, Shaoxing 312366, Zhejiang PR, China) before starting the GC-MS operation. Treatments samples were randomly organized on refrigerated (4 °C) holding vials-tray, and purged with helium (40 mL/min) for 14 min at 20 °C. The identification of volatiles was based on stored Wiley Library software. The total peak area (total ion counts × 10⁴) was reported as an indicator of volatiles generated from the samples.

Sensory evaluation A highly trained panel of 10 panelists (Mu'tah University, students and staff) participated in the sensory evaluation of the chicken (cooked thigh) meat. Meat patties were evaluated using selected attributes, including egg like, spice, and oxidation odor, and finally, for its overall acceptability. Meat patties were prepared as described in the previous oxidation section, to study the effect of using different levels of OE compared with other synthetic antioxidants. Meat samples were subjected to 3 days of storage time and refrigerated at 4 °C before cooking and for each evaluation session. The sensory panel was served twice after cooling cooked meat to room temperature (25 °C) for all treatment samples. The panelists participated in three training (1 h) sessions to build up the final descriptive terms of all attributes used in the current evaluation. All sensory attributes were estimated using a line scale without numbers including nine units. The individual treatment samples (10 g/each) were placed in a small glass vials (20 ml volume) as a last step before the panelists recorded their scores. All procedures, preparation, estimation, and serving of meat samples was performed as described by Al-Hijazeen (2019).

Statistical analysis Data from the current study were analyzed using the procedures of the generalized linear model (Proc. GLM, SAS program, version 9.3, 2012). Mean values and standard error of the means (SEM) were reported. The significance was defined at p < 0.05 and the Tukey test or Tukey's Multiple Range test were used to report whether there were significant differences between mean values.

Results and Discussion

Oregano essential oil composition The average percentage values of OE measured by HPLC showed that thymol (13.06%) and carvacrol (76.39%) represented the predominant components. This agreed with previous researchers, who reported that carvacrol is the major component of Origanum syriacum. L (Daouk et al., 1995, and Tepe et al., 2004; Ibrahim et al., 2012a, b). In addition, other dominant components were detected and reported in Origanum syriacum L., such as P-cymene, Trepinen-4-ol, carvone, aristolochic acid, and sabinene hydrate (Berna'th, 1997; Al-Bandak, 2007). These compounds, which form approximately 5–7% of the total oil, have minor effects on the total antioxidant activity (Adam et al., 1998; Yanishlieva et al., 1999). The essential oil (OE) content and quality are highly variable and affected by many factors, such as storage and harvesting conditions, the soil, the extraction method, and genetic and seasonal effects (Farooqi et al., 1999; Gonuz and Ozorgucu, 1999; Ceylan et al., 2003; Viuda-Martos et al., 2010). Thus, the unique composition of this oil will produce different antioxidant activity from that of other Origanum species. In addition, no research studies have evaluated these levels of OE in cooked chicken meat preservation.

Cooking loss%, proximate composition, and ultimate pH In terms of meat quality and freshness, it is very important to analyze the raw meat mixture in order to avoid any off-treatment effects. Based on current results (Table 1), it is clear that supplementation had no significant (p > 0.05) effect on meat cooking loss percentage, proximate composition, and their ultimate pH (raw meat) values. This finding confirmed that any oxidative variation during storage was due to the treatment effect. In addition, this was in agreement with Al-Hijazeen (2019), who reported that adding OE (Origanum syriacum. L) at levels of 100, 150, and 300 ppm to ground chicken meat had no significant (p > 0.05) effect on meat cooking loss%, and their ultimate pH values. Statistically, this confirms the univariate status (approximately equal starting numbers) for comparison of treatment effects during storage time.

Table 1. Cooking loss%, proximate analysis, and ultimate pH values of ground chicken thigh meat.

TRT*	Proximate Analysis
TRT*	Cooking Loss%	Fat%	Protein%	Water%	Ash%	U-pH Value
Control	0.196^a	6.64^a	18.53^a	73.94^a	0.90^a	6.05^a
OE_L1	0.184^a	6.78^a	18.53^a	73.79^a	0.91^a	6.11^a
OE_L2	0.177^a	6.48^a	18.68^a	73.94^a	0.90^a	6.14^a
E-250	0.184^a	6.76^a	18.54^a	73.77^a	0.93^a	6.12^a
BHA	0.187^a	6.77^a	18.58^a	73.75^a	0.90^a	6.11^a
SEM	0.0073	0.1197	0.096	0.154	0.021	0.0379

* Treatments: Control; OE_L1 (200 ppm); OE_L2 (250 ppm); E-250; and 14 ppm BHA; n = 4.

¹ Proximate analysis (PA) of fresh meat before cooking.

² Ultimate pH: 24 h after slaughtering.

Lipid oxidation Lipid oxidation produces primary (hydroperoxide-ROOH) and secondary compounds (volatiles such as ketones, aldehydes, and hydrocarbons) formed during storage, considered the major components responsible for causing meat deterioration, rancidity development, and off-odor flavor and reducing meat shelf-life (Lee and Ahn, 2005; Ahn et al., 2009; Domínguez et al., 2019). In addition, TBARS is considered the most common method used to evaluate lipid oxidation in meat. It is correlated well with secondary compounds (e.g., hexanal shown in Table 6), sensory characteristics (off-odors/flavors), and meat freshness (Du et al., 2003; Ahn et al. 2009; Al-Hijazeen and Al-Rawashdeh, 2019; Domínguez et al., 2019). In the current study, there was no significant antioxidant (p > 0.05) effect among all treatment additives at day 0 of the storage period (Table 2).

Table 2. TBARS values of cooked chicken (thigh) meat at different storage times at 4 °C.

Time	Control	OE_L1	OE_L2	E-250	BHA	SEM
		TBARS (mg/kg) meat
Day 0	1.148^az	1.134^ay	1.112^ay	1.124^ay	1.144^az	0.0658
Day 4	3.504^ay	1.437^by	1.300^by	1.395^by	1.421^ay	0.0687
Day 8	7.420^ax	2.509^bx	2.194^bx	2.311^bx	2.491^bx	0.0756
SEM	0.0342	0.0796	0.0607	0.1013	0.0562

a–c Values with different letters within a row are significantly different (p < 0.05); n = 4.

x–z Values with different letters within a column are significantly different (p < 0.05).

* TBARS value in mg malonaldehyde/kg meat.

Treatments: Control; OEL1; OE_L2; E-250; BHA: 14 ppm BHA.

This was due to the low amount of free radicals formed at the beginning of the storage time as reported by Al-Hijazeen (2016a, b). However, OE_L1, OE_L2, and E-250 showed a significant (p < 0.05) effect by reducing the amount of malonaldehyde formed at day 4 compared with the control and BHA treatments. The antioxidant mechanism of OE was explained previously regarding its composition of phenolic compounds such as carvacrol and thymol (Al-Bandak, 2007; Hać-Szymańczuk et al.; 2019; Simirgiotis et al., 2020). These compounds delayed the auto-oxidation process through their ability to act as hydrogen donors (Maral, 2017; Hać-Szymańczuk et al., 2019; Yildiz et al., 2021). These results agreed with Al-Hijazeen (2019), who reported that adding OE to ground chicken meat at the level of 150 ppm decreased TBARS values during storage. However, no research studies indicate the best level that can be recommended for the meat processing industry. All treatment additives showed a significant (p < 0.05) effect, reducing the TBARS values at day 8 compared with the control treatment. However, OE_L2 exhibited the highest antioxidant activity, showing the lowest TBARS values during the storage period (0–8 days). Furthermore, the antioxidant effect of oregano (OE_L1) and BHA was very comparable during the storage time. Thus, oregano (OE_L2) could be a promising substitution for E-250 and other synthetic meat preservatives. Finally, the level that is practical for use in the meat industry should consider all parameters in the current study. In addition, this research followed and considered previous studies regarding the preservation effect of OE, and a thorough investigation was performed to recommend final compatible level.

Total volatiles in cooked meat samples Depending on previous research, raw meat was excluded from the current study because it produced low volatiles (aldehydes, ketones, and sulfur compounds) during storage time (Lee and Ahn, 2005; Al-Hijazeen et al., 2016a; Al-Hijazeen et al., 2016b; Kosowska et al., 2017). On the other hand, a higher quantity of total volatiles (TV) was detected by GC-MS when cooked meat was evaluated for a similar storage time (Ahn et al., 1998; Al-Hijazeen et al., 2018). Generally, researchers reported a positive relation (correlation) between aldehydes (e.g., hexanal, pentanal, butanal, and heptanal) and the TBARS values during storage using different meat sources (Ahn et al., 2000; Jo et al., 2006; Ahn et al., 2009). In addition, this was in agreement with the current results (Table 7). Generally, the TV in aerobically packaged broiler meat samples increased rapidly (5–6-fold) during refrigerated storage (Table 3–5). This agreed with previous studies comparing aerobically packaged with vacuum packaged meat samples (Du et al., 2000; Al-Hijazeen et al., 2018). In the present study, no significant differences (p > 0.05) were found among mean values of all volatiles regarding all treatments at day 0 of storage time (Table 3). However, a small numerical variation could be due to free radicals and initial lipid peroxidation of raw ground meat samples. In addition, there was a minor amount of volatiles (such as ethyl propionate, ethyl acetate, S-methyl ethane, 2-butanone) detected inconsistently and not reported in the present tables.

Table 3. Volatile profiles of cooked meat inclusion with different antioxidants at day 0.

Total ion counts×10⁴
Compounds	Control	OE_L1	OE_L2	E-250	BHA	SEM
Pentane	3622.5^a	2890.5^a	2769^a	2606.5^a	3278^a	254.38
Carbon disulfide	6093^a	4208^a	4888.5^a	5095.5^a	5644.8^a	1335
2-Propanone	3254.5^a	3398^a	3252^a	3179^a	3546^a	245
1-Pentene	365.8^a	486^a	452^a	446.8^a	186.5^a	113.87
Hexane	15653^a	12386.8^a	12326^a	13075^a	13290^a	2147
Butanal	2339.5^a	2062^a	1982^a	2550^a	2048^a	229.67
Dimethyl disulfide	4582^a	4686^a	5011^a	4076^a	4507^a	416
Octane	1928^a	1803^a	1694^a	2050^a	2239^a	178.64
Propanal	3287^a	3319^a	3198^a	2953^a	3139^a	405.65
Hexanal	29464^a	29130^a	29689^a	28606^a	28592^a	482.45
Pentanal	4252^a	4228^a	3734^a	3985^a	4309^a	291.68
Nonanal	3501^a	2732^a	2586^a	2535^a	3171^a	279.59
Camphene	0^b	300^a	358^a	0^b	0^b	32.43
Limonene	0^b	74.75^a	106^a	0^b 0^b	13.06
γ-Terpinene	0^b	95.75^a	125^a	0^b	0^b	8.44
Sabinene	0^b	36^a	44^a	0^b	0^b	3.9

ab Values with different letters within a row are significantly different (p < 0.05); n = 4.

Treatments: Control; OE_L1; OE_L2; E-250; 14 ppm BHA.

Table 4. Volatile profile of cooked meat inclusion with different antioxidants at day 4.

	Total ion counts×10⁴
Compounds	Control	OE_L1	OE_L2	E-250	BHA	SEM
Pentane	5711^a	5409^a	5168^a	5026^a	4813^a	238
Carbon disulfide	3760^a	2686^ab	2501^b	2110^b	2949^ab	257.77
2-Propanone	12658^a	9798^a	9236^a	8909^a	9163^a	980.77
1-Pentene	1107^a	863^a	798^a	691^a	777^a	173.89
Hexane	17830^a	15216^ab	13569^b	13264^b	13515^b	721.26
Butanal	4939^a	4308^a	4104^a	3921^a	4275^a	329.34
Dimethyl disulfide	6418^a	4440^a	5753^a	4185^a	5501^a	750.64
Octane	3214^a	3056^a	2976^a	2707^a	2867^a	425.43
Propanal	9173^a	8141^a	7217^a	6179^a	8291^a	748.07
Hexanal	40859^a	37042^ab	35391^ab	33317^b	36208^ab	1433.22
Pentanal	7276^a	5498^a	5361^a	5152^a	5306^a	544.32
Nonanal	4802^a	3313^b	2671^c	2836^bc	3358^b	139.28
Camphene	0^b	317^a	321^a	0^b	0^b	19.25
Limonene	0^b	63^a	65^a	0^b	0^b	3.64
γ-Terpinene	0^b	97^a	103^a	0^b	0^b	8.4
Sabinene	0^b	40^a	49^a	0^b	0^b	3.49

ac Values with different letters within a row are significantly different (p < 0.05); n = 4.

Treatments: Control; OE_L1; OE_L2; E-250; 14 ppm BHA.

Table 5. Volatile profile of cooked meat inclusion with different antioxidants at day 8.

	Total ion counts×10⁴
Compounds	Control	OE_L1	OE_L2	E-250	BHA	SEM
Pentane	9746^a	7909^a	7131^a	6557^a	7234^a	1301.71
Carbon disulfide	2513^a	2086^b	2014^b	1909^b	2080^b	64.65
2-Propanone	20578^a	19749^a	18974^a	17648^a	18383^a	1369.04
1-Pentene	3422^a	2885^ab	2737^ab	2068^ab	1708^b	352.75
Hexane	30999^a	28696^ab	27753^ab	25731^b	26558^b	938.64
Butanal	13265^a	10794^ab	9429^b	7909^b	9310^b	746
Dimethyl disulfide	5622^a	4787^ab	3901^ab	2998^b	3956^ab	556.66
Octane	9299^a	8624^a	8263^a	7865^a	8207^a	1574.79
Propanal	14707^a	12684^ab	11914^b	10694^b	12013^b	615.68
Hexanal	60477^a	55732^ab	54449^ab	53233^b	54578^ab	1585.05
Pentanal	9931^a	7237^ab	6658^ab	6366^b	6816^ab	778.3
Nonanal	6981^a	4446^ab	4205^ab	3969^b	4247^ab	652.42
Camphene	0^b	290^a	300^a	0^b	0^b	10.57
Limonene	0^b	56^a	65^a	0^b	0^b	4.007
γ-Terpinene	0^b	90^a	100^a	0^b	0^b	5.86
Sabinene	0^b	44^a	56^a	0^b	0^b	2.98

Different letters (a–d) within a row are significantly different (p < 0.05); n = 4.

Treatments: Control; OE_L1; OE_L2; E-250; 14 ppm BHA.

Table 6. Pearson correlation coefficients (PCC) between volatiles and TBARS values of current control samples during the storage period.

Volatiles	PCC	Mean	STD
2-Propanone	0.95178*	12164	7639
1-Pentene	0.94772*	1632	1421
Hexane	0.94776*	21494	7243
Butanal	0.95977*	6848	5001
Hexanal	0.97979*	43600	13651
Propanal	0.96251*	9056	4988
Nonanal	0.96605*	5095	1555
Carbon disulfide	−0.90304*	4122	1632
Dimethyl disulfide	0.23408	5540	1517

* p < 0.05; Strongly significant.

Table 7. Sensory attribute means of cooked ground thigh meat patties.

Sensory attributes^b
TRT*	Egg Like	Spice	Oxidation	Overall
TRT*	Odor	Odor	Odor	Acceptability
Control	7.92^a	0.614^c	7.34^a	3.87^b
OE_L1	5.19^b	5.434^b	5.14^bc	6.43^a
OE_L2	4.93^b	6.632^a	4.28^c	6.948^a
E-250	5.25^b	0.572^c	4.71^bc	6.72^a
BHA	5.89^b	0.601^c	5.39^b	5.903^a
SEM	0.245	0.118	0.262	0.294

* Treatments: Control; OE_L1(200 ppm); OE_L2(250 ppm); E-250; and 14 ppm BHA; n = 10.

b Sensory attributes: Samples were evaluated on day 3.

SEM^c: Standard error of the means.

a–f Mean within same column with different superscripts are different (p < 0.05).

The GC-MS data of OE treatment samples (OE_L1 and OE_L2) showed unique terpenoids (e.g., limonene, sabinene, camphene, α-terpenene) connected with EO composition. These volatiles can significantly affect overall meat odor, flavor, and sensorial characteristics affecting cooked meat quality (Al-Hijazeen et al., 2018; Mancinelli et al., 2021). Both E-250 and OE_L2 showed a significant (p < 0.05) antioxidant effect by reducing the total volatiles (such as hexanal, pentanal, and dimethyl disulfide) compared with the control treatment at day 4 of storage time. Overall, the effect of E-250 was higher than that of other supplements during the storage period. Furthermore, until day 4 of the storage period, all additives showed a significant anti-deterioration effect among most volatiles compared with the control (Tables 3–4).

However, the effect of adding OE_L2 was very close and comparable to that of the synthetic E-250. The BHA treatment results were also very close to those of OE_L1 regarding total volatile mean values. Similar results were found among sulfuric volatiles (Dimethyl disulfide, Carbon disulfide) during the storage period. However, the TV sulfuric compounds decreased after day 4 in all sample vials, which explained by the escaping and/disappearance of these volatiles after 4–5 days of storage due to their high volatility (Nam et al., 2002; Lee et al., 2003; Nam et al., 2003; Al-Hijazeen et al., 2018). GC-MS analysis did not detect thymol or carvacrol, which are characterized by low volatility. Overall, the variation among treatments clearly appeared at day 8 of the storage period.

Oregano essential oil (OE_L1 and OE_L2) showed significant antioxidant activity regarding most aldehydes, sulfuric compounds, and hydrocarbons compared with the control samples. The highest antioxidant effect (against aldehydes and sulfuric compounds) was achieved by E-250 compared with the other additives. In addition, other additives (OR_L1 and OR_L2, BHA) showed comparable effects at reducing volatile-related lipid oxidation by the final day. However, OR_L2 was the best level could be use as natural substitution for E-250 additive. Finally, finding a good correlation and relationship between these volatiles and primary lipid oxidation compounds will help to reach a better conclusion (Table 6). This relation will assist other researchers using different plant extract that might be used in meat preservation.

Sensory evaluation As shown in Table 6, all treatment additives showed a positive effect on meat preservation. This appeared through all sensory attributes linked to lipid oxidation, and formation results compared to those of the control treatment. A significant (p < 0.05) spice odor was detected clearly using all meat samples mixed with OE. This agreed with the GC-MS results, in which several terpenoids (e.g., sabinene, camphene) were associated with the OE composition. Despite the superior effect of adding E-250 over lipid oxidation and TV data compared with the other treatments, OE_L2 showed the greatest improvement in overall acceptability. This was due to the ability of OE constituents to decrease free radical formation, rancidity development, off-odor volatiles, improve their sensory characteristics, and enhance meat shelf-life (Pavelkova et al., 2013; Vital et al., 2016; Al-Hijazeen, 2019).

However, OE antioxidant activity was variable and depended on different factors such as oregano species, source and method of extraction, method evaluation, and mixing method (Al-Hijazeen et al., 2018; Al-Hijazeen, 2019, 2022a, b). For example, Al-Hijazeen (2019) found that adding OE (Origanum syriacum L.) at the level of 150 ppm had a great effect on lipid and all sensory evaluation results. In addition, OE from another species (Origanum vulgare subsp. hirtum) showed a positive preservation effect on ground chicken meat at levels from 100 ppm to 400 ppm. They concluded that adding OE at levels higher than 100 ppm improves meat quality and decreases off-odor volatiles in cooked meat (Al-Hijazeen et al., 2016a). Finally, the variation in the recommended OE level can be resolved by combining all parameters related to lipid oxidation; sensory evaluation, and meat freshness data and then forming a strong scientific opinion.

Conclusion

All additives showed a significant (p < 0.05) preservation effect among all parameters compared with the control meat samples. In addition, E-250 showed the highest antioxidant effect regarding lipid oxidation and total volatile development. However, both E-250 and OR_L2 exhibited a comparable effect higher than that of either BHA or OR_L1. Oregano essential oil (OR_L2) showed the highest overall acceptability scores compared with the other treatments. An important relation was found between total volatile aldehydes and sulfuric compounds, and TBARS values during storage. Based on the current results, the optimal level of OE (Origanum syriacum L.) recommended for industrial uses is 250 ppm as a complete and/or partial replacement for synthetic antioxidants.

Acknowledgements This study was financially supported by the Deanship of Scientific Research at Mutah University, Al-Karak, Jordan. Grant number: 120/14/118 (2020). This funding is highly appreciated with my deep thanks to all other Animal Production Department staff for their help and advice.

Conflict of interest There are no conflicts of interest to declare.

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