
==== Front
Vet Anim Sci
Vet Anim Sci
Veterinary and Animal Science
2451-943X
Elsevier

S2451-943X(24)00057-7
10.1016/j.vas.2024.100390
100390
Article
Artemisia afra essential oils inclusion in diets induces desirable effects on meat quality and fatty acid profiles of broilers chickens
Marume U. upenyu.marume@nwu.ac.za
ab⁎
Zvarivadza W. ab
Hugo A. c
a School of Agricultural Sciences, Faculty of Natural and Agricultural Sciences, North-West University, P Bag X 2046, Mmabatho, 2735, South Africa
b Food Security and Safety Niche area, Faculty of Natural and Agricultural Sciences, North-West University, P Bag X 2046, Mmabatho, 2735, South Africa
c Food Science Division: Microbial Biochemical and Food Biotechnology, Faculty of Natural and Agricultural Sciences, PO Box 339, Bloemfontein, 9300, South Africa
⁎ Corresponding author. upenyu.marume@nwu.ac.za
15 8 2024
9 2024
15 8 2024
25 100390© 2024 The Authors. Published by Elsevier Ltd.
2024

https://creativecommons.org/licenses/by-nc-nd/4.0/ This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
The effects of Artemisia afra (African wormwood) essential oil incorporation in diets on meat quality and fatty acid profilers of broilers was assessed. Four hundred Cobb500 day-old chicks were obtained and placed randomly into the following 4 diets replicated 10 times: NC-Negative control (broiler diet without antibiotics), PC-positive control (broiler diet with zinc bacitracin), AA1-broiler diet + 0.1 % A. afra essential oil and AA2 - broiler diet + 0.3% A. afra essential oil. A pen having 10 chicks was regarded as the experimental unit. From the results, all carcass traits were influenced (P < 0.01) by diet apart from the dressing out percentage. The highest slaughter weights (1846g) and hot carcass weight (1427.36g) were obtained in birds fed the AA1 diet. Highest ultimate pH value (6.24) was obtained from the birds fed the AA1 while the highest values for meat lightness (L*) were obtained in birds offered the AA1 and NC diets (55.73 and 55.82). Cooking loss was highest in birds fed the NC (31.01%) diet. Birds fed the AA2 diet (23.7mg/g)) had the highest intramuscular fat followed by the AA1 fed birds. Inclusion of A. afra essential oils in diets also increased the proportion of PUFAs, n-6 and n-3 fatty acids and the PUFA/SFA ratios. In conclusion, the incorporation of A. afra essential oil in diets improved meat quality and fatty acid composition of broiler meat for the benefit of consumers.

Keywords

Slaughter weight
Drip loss
Water holding capacity
Omega-6
Omega-3
==== Body
pmc1 Introduction

Poultry consumption is currently on a steady rise globally, particularly in resource poor areas of the developing world where most of the consumers are marginalised (Disetlhe et al., 2018; Mangwiro et al., 2013). The shift towards poultry meat consumption can be attributed to the fact that there are no religious or cultural connotations associated with poultry meat consumption, can effectively bridge the protein malnutrition gap, strengthen the economic endowments in the resource poor communities, and fits well in the animal production practices prevailing in Africa (Disetlhe et al., 2018; Mpofu et al., 2016). In poultry production systems, antibiotic use is prevalent. The utilisation of antibiotics particularly in broilers over the years effectively increased efficiency of production and gross margins. Nevertheless, consumers are increasingly becoming anxious about the associated health effects of the continuous use of the antibiotics. Consequently, prohibition of antibiotics use in animal production was effected in the European Union and other developed countries This stimulated intense efforts to explore alternative replacements including the utilisation of phytogenic plant essential oils.

Dietary alterations may influence post-mortem muscle biochemical pathways, subsequently inducing changes in meat quality and composition (Zhai et al 2018; Disetlhe et al., 2018; Gong et al., 2014). Inclusion of phytogenic plant essential oils in broiler diets may therefore improve meat quality in broilers. Phytogenic plants contain some essential oils that are composed of various aromatic compounds including carotenes, xanthophylls and flavonoids which were reported to have nutraceutical effects on the health of animals. The aromatics compounds have also been shown to desirably affect some important meat quality attributes including meat tenderness, pH and colour (Cázares-Gallegos et al., 2019; Mpofu et al., 2016; Ozbey et al., 2007). In addition, the aromatic compounds may alter the fatty acid composition of meat and improve the oxidative stability of the meat (Wenk, 2003; Ozbey et al., 2007; Qwele et al., 2013; Patil, et al., 2011). The bioactive compounds have also been acclaimed to depress the concentrations of serum cholesterol, reduce the levels density lipoproteins (LDL) and elevates the high-density lipoproteins (HDL) content of meat (Hong et al., 2012). Plant essential oils can also be used as natural preservatives by lowering lipid oxidation, that often cause the production of undesirable flavours and odours and hence prevent rapid meat deterioration (Kirkpinar et al., 2014). Phytogenic plant extracts can therefore be a viable alternative in replacing the synthetic preservatives that are often utilised as preservatives in the food industry (Muyima et al., 2002).

Artemisia afra (African wormwood) is one of the nutraceutical plants that are popular in many communities of South Africa (Viljoen, et al., 2006). It is widely used as an ethnomedicine in resource poor communities in South Africa and elsewhere to treat various health issues in humans and animals (Witkowska et al., 2019; Attia et al., 2019; Lim Ah Tock & Viljoen, 2024). In addition to nutraceutical properties, A. afra contains various secondary plant metabolites including artemisia ketones, cineole, camphor and thujone that may have desirable influences on the physiology and health of animals, productivity and ultimately meat quality (Viljoen, et al., 2006). Previous studies have shown that A. afra can improve growth and immunocompetences in broiler chickens (Zvarivadza & Marume, 2022; Trifan et al., 2022). In addition, Artemisia Annua was found to positively influence gut microbial balance and ultimately broiler performance (Panaite et al., 2019). While some information is available on the influences of some A. afra and other phytogenic plants on broiler performance (Cho et al., 2014; Park et al., 2014; Mpofu et al., 2016; Chowdhury et al., 2018, Zvarivadza & Marume, 2022), there is still no information of their effects of meat quality in broiler. Therefore, we postulate that the incorporation of A. afra essential oils (EO) in broiler diets may induce desirable effects on carcass attributes, meat quality and fatty acids profiles of broiler meat. This study assessed the effects of A. afra essential oil incorporation in diets on carcass meat quality and fatty acid composition of broiler chickens.

2 Materials and methods

2.1 Animal ethics and reagents

All reagents and solvents used in this study were sourced from Sigma-Aldrich (Pretoria, South Africa) and Merck Chemicals (Johannesburg, South Africa). The feeding trial and study protocols were assessed and certified by the Research Ethics Committee of the NWU (NWU-ANIMPROD REC) and the following ethics approval number was granted: NWU-00660-18A.

2.2 Artemisia afra oil extraction and analysis

A. afra essential oil was sourced from the Highland Essential Oils (HEO, South Africa) involved in commercial plant essential oils production for the cosmetic and food industry. A gas chromatography integrated to a mass spectroscopy detector (Liu et al., 2009) was used to profile the different components of the essential oils. The major bioactive compounds profiled are presented in Table 1 while fatty acid profiles are presented in Table 2.Table 1 Major components of A. afra essential oil (%).

Table 1Component	Proportion (%)	
Tricylene	0.2	
Fenchene	1	
Camphene	3.9	
Sabinene	2.6	
Myrcene	1.1	
1,8 Cineole	27.9	
Artemisia ketone	41.9	
α-Thujone	2.9	
α-Terpineol	2.7	
α-copaene/camphor	27.1	

Table 2 Fatty acid composition (mg/g) of A. afra essential oil.

Table 2Fatty Acids	Amount	
Palmitic acid	113.2 ± 4.1	
Stearic acid	31.8 ± 3.2	
Arachidic acid	13.6 ± 3.2	
Behenic acid	10.4 ± 0.19	
Tricosylic acid	38.2 ± 2.3	
Lignoceric acid	16.2 ± 3.6	
∑SFA	223.4 ± 3.1	
Palmitoleic acid	64.6 ± 3.2	
Oleic acid	91 ± 2.5	
∑MUFA	155.6 ± 2.8	
Linoleic acid	372.3 ± 4.7	
Stearidonic acid	58.6 ± 4.9	
g- Linolenic acid	38.3 ± 3.9	
α-Linolenic acid	13.4 ± 3.2	
Eicosadienoic acid	122.4 ± 2.8	
Arachidonic acid	26.9 ± 3.9	
∑PUFA	631.1±3.9	
∑UFA	786.7±3.3	

2.3 Animals, treatments and experimental arrangement

Four diets were developed with the inclusion of antibiotics and essential oils as follows: a negative control (NC, no antibiotics), positive control (PC, inclusion of zinc bacitracin in diet). The other 2 treatments were formulated with the inclusion of A. afra essential oils in place of zinc bacitracin at 0.1% (AA1) and 0.3% (AA2) respectively giving 10g/kg feed (AA1) and 30g/kg feed (AA2) crude essential oil extract. The dose calculations were based on artemisia ketone (AK) concentrations, which is the major bioactive component constituting 41% of the essential oil extract. Hence, the AA1 treatment contained 4.1gAK/kg feed and AA2 treatment contained 12.3gAK/kg feed. The formulated dietary treatments and ingredients are presented in in Table 3. A total of 400 day-old Cobb500 broiler chicks with an initial weight of 40g ± 0.21 (mean ± SD) were obtained from Mimosa Chicks (SA) and randomly allotted to the four (4) diets. Each diet had 10 replicate pens and a pen with 10 birds was regarded as the experimental unit in a completely randomised design (CRD). The design (3.5 × 1.0 × 1.85 m) of the pens was done in accordance with the welfare requirements of growing chick including provision of brood environment. A normal feeding program for commercial broilers was applied following the 3 feeding phases (starter phase day 1-7; grower- day 8-21 and finisher- day 22-35). Feed and water were freely provisioned, and mortalities were recorded.Table 3 Ingredients composition of experimental diets for starter, grower and finisher phases.

Table 3	Dietary treatments	
Ingredients	Starter	Grower	Finisher	
	PC	NC	AA1	AA2	PC	NC	AA1	AA2	PC	NC	AA1	AA2	
Yellow Maize-Fine	63.2	63.2	63.2	63.2	69.9	69.9	69.9	69.9	76.2	76.2	76.2	76.2	
Prime Gluten 60 (Yellow)	1.2	1.2	1.2	1.2	1.8	1.8	1.8	1.8	1.3	1.3	1.3	1.3	
Fullfat Soya	0.0	0.0	0.0	0.0	5.1	5.1	5.1	5.1	1.5	1.5	1.5	1.5	
Soyabean Meal (Local)	31.7	31.7	31.7	31.7	19.7	19.7	19.7	19.7	18.0	18.0	18.0	18.0	
Limestone Powder-Fine	1.62	1.62	1.62	1.62	1.45	1.45	1.45	1.45	1.30	1.30	1.30	1.30	
MCP/Mono Cal KK	0.90	0.90	0.90	0.90	0.72	0.72	0.72	0.72	0.50	0.50	0.50	0.50	
Salt-Fine	0.34	0.34	0.34	0.34	0.32	0.32	0.32	0.32	0.33	0.33	0.33	0.33	
Koeksoda	0.18	0.18	0.18	0.18	0.17	0.17	0.17	0.17	0.13	0.13	0.13	0.13	
Choline Powder	0.075	0.075	0.075	0.075	0.075	0.075	0.075	0.075	0.075	0.075	0.075	0.075	
Lysine	0.250	0.250	0.250	0.250	0.279	0.279	0.279	0.279	0.262	0.262	0.262	0.262	
L-Threonine	0.048	0.048	0.048	0.048	0.041	0.041	0.041	0.041	0.030	0.030	0.030	0.030	
Methionine	0.231	0.231	0.231	0.231	0.187	0.187	0.187	0.187	0.161	0.161	0.161	0.161	
PX P2 Br Grower with Phytase	0.167	0.167	0.167	0.167	0.167	0.167	0.167	0.167	0	0	0	0	
PX P3 Br Finisher with Phytase	0	0	0	0	0	0	0	0	0.167	0.167	0.167	0.167	
Coxistac	0	0	0	0	0.05	0	0	0	0.05	0	0	0	
Olaquindox	0.05	0.05	0.05	0.05	0.04	0	0	0	0.04	0	0	0	
A. afra	0	0	0.1	0.3	0	0	0.1	0.3	0	0	0.1	0.3	
NC -Negative control (commercial broiler diet without antibiotics). PC-positive control (commercial broiler diet). AA1-commercial diet without antibiotics + 0.1% A. afra essential oil inclusion and AA2- commercial diet without antibiotics + 0.3 % A. afra essential oil inclusion.

2.4 Slaughter procedures and carcass traits

The feeding trial ran over a period of 35 days, At the end of the trial, the birds were taken off-feed for a 13-hour period to allow for the emptying of the crop (Disetlhe, 2017; Ari et al., 2013). The birds were grouped according to dietary treatments subsequently transported to Rooigrond abattoir (Mahikeng, SA) for slaughter. At slaughter the birds were stunned and bled immediately for approximately 2 minutes, followed by de-feathering and evisceration. After evisceration, the feet and head were removed, and the carcasses were weighed immediately to obtain the hot carcass weights (HCW). The carcasses were then moved to a cold room and chilled over night for 24 h and subsequently reweighed to determine the cold carcass weights (CCW). The dressing out percentage was then determined as the ratio of the HCW over the slaughter weight. The internal organs were individually packed in plastics and taken to the Dept of Animal Science lab for determination of morphometric measurements. Following the HCW and CCW measurements, the breast, quota leg, thigh and drumsticks were surgically removed and weighed to obtain the weights of different cuts and the breast and thigh indices were calculated. The internal organs (gizzards, livers, hearts and spleens) were also weighed, and lengths of the intestines (duodenum jejunum and ileum) were recorded. The breast muscles (pectoralis major muscle) of the broilers were obtained and used for the assessment of meat quality traits and fatty acid compositions.

2.5 Meat quality parameters

A Corning Model 4 pH-temperature meter with an attached in-gold spear-type electrode (Corning Glass Works, Medfield, MA) was used for Meat pH (pHu) and temperature measurements 24 hours’ post-slaughter, while a Minolta colour-guide (Konika Minolta Spectrophotometer CM 2500c, Osaka, Japan) was used for measurement of the meat colour coordinates for lightness (L*), Redness (a*) = and = Yellowness (b*). Calibration of the pH meter was done using a set of standards for calibration including pH 4.00 / 7 / 10 while the standard colour calibration was done using a white tile at initial test and on subsequent meat colour measurements. Meat pH and colour measurements were done in triplicate at different locations on the breast muscle. For determination of the water holding capacity (WHC), a procedure developed by Grau and Hamm (1957) was used. Freshly cut breast muscle slices (5-6 grams) were placed in between two filter papers and held under a weight of 60 kg. The breast sliced were subsequently reweighed to determine the weight of slices after press. The WHC was then determined as follows:WHC(%)=(initialweight−−weightafterpressing)initialweight×100%

For drip loss measurements, meat strips weighing ∼ 2 grams (wet weight, w1) were obtained from the breast muscles and suspended in a sample bottle while hooked on the bottle cap using wire steel. The sample bottles were subsequently sealed tightly with the strips avoiding the edges of the bottles. The sample bottles were then placed in a chiller at 4°C for 72 hours. When the storage period elapsed, the strips were retrieved and reweighed to obtain weight after drip (w2). The drip loss was determined using the following equation:Driploss(%)=(W1−−W2)W1×100%

For cooking loss breast muscle samples weighing approximately 80 g were obtained and individually weighed to get the initial weight (w1). The samples were then placed in foil plates and oven broiled (dry heating) for 30 minutes at 180°C to a core temperature of 70°C. Broiled breast samples were then cooled for 20 minutes and subsequently weighed to obtain the weight after cooking (w2). The losses due to cooking were determined as follows:Cookingloss(%)=(W1−−W2)W1×100%

2.6 Proximate fat compositions

Folch extraction was used for gravimetrical extraction of total fat (Folch et al., 1957). Transmethylation was performed following the procedures described by Sukhija and Palmquist (1988) and modified by Jenkins (2010). Brief, 2 mL of 0.5 N sodium methoxide and 3 mL of 5% methanolic HCl reagents were used to methylate 10 mg of the extracted lipids followed by a 10 min incubation in a water baths (Thermo Scientific, Waltham, MA, USA) at 50 and 80°C respectively. 1 mg of c-10-heptadecenoic acid (c10–17:1) methyl ester/mL toluene was used (standard no. U-42 M form Nu-Check Prep Inc., Elysian, MN, USA) for standardisation. The Varian 430 flame ionization gas chromatography was used for the quantification of the fatty acid methyl esters (FAMEs) from meat samples. The GC had an integrated silica capillary column, (Chrompack, CPSIL 88, length - 100 m, ID - 0.25 mm, film thicknesses - 0.2 μm) for the quantification of FAMEs. The FAME samples were subsequently identified by comparing the retention times of FAME peaks from samples with the Supelco reference standards (Supelco 37 Component Fame Mix 47885-U) and UC-59M for conjugated linoleic acid (CLA) isomers (Nu-Check Prep Inc., Elysian, MN, USA) and expressed mg/100g of muscle tissue (Vahmani et al., 2017). Nutritional indices were determined as the sum of different fatty acids combination as follows: omega-3 (n-3), omega-6 (n-6), total saturated fatty acids (SFA), total monounsaturated fatty acids (MUFA), polyunsaturated fatty acids (PUFA), PUFA/SFA ratio (P/S) and n-6/n-3 ratio. All fatty acids were expressed as a proportion t (w/w) per 100 g muscle tissue.

2.7 Statistical analysis

The effect of dietary treatment on carcass traits internal organ morphometrics, meat quality and fatty acid composition of broiler meat was assessed using the Proc GLM procedure of SAS (2010). The initial weight of the birds and the birds within pens were used as random variables. Proc Univariate (SAS, 2010) was used to test for normality. Where the effects of diets were significant, differences among treatments were assessed using the PDIFF option of SAS (2010). The level of significance was set at P < 0.05 for all tests. The following statistical model was used:Yij=μ+Di+εij

Where: Yij = observations (carcass and meat quality traits), µ = overall mean, Di = dietary effect, and εij = error term.

3 Results

3.1 Carcass traits

The influences of essential oil inclusion in diets on carcass parametes of broilers are shown in Table 4. From the table, all carcass traits were significantly (P < 0.05) affected by diet with the exception of dressing out percentage. Average slaughter weight (1846g), HCW (1427.36g), and CCW (1407.50g) were highest in broilers given the AA1 diet. Similarly, the birds offed the AA1 diet also obtained the highest (P < 0.05) breast weight and breast muscle index. For all carcass parameters, the least values were consistently obtained in birds offered the NC diet followed by those fed the AA2 diet.Table 4 The effect of A. afra essential oil inclusion in diet on carcass characteristics of broiler chickens.

Table 4	1Dietary treatments	
Parameters	NC	PC	AA1	AA2	SEM	P-value	
Final body weight (g)	1550a	1818b	1846b	1677a	0.91	0.001	
Hot carcass weight (g)	1192.80a	1396.60ab	1427.36b	1211.60a	29.40	0.015	
Cold carcass weight (g)	1171.88a	1376.20b	1407.50b	1183.04a	29.35	0.006	
Dressing %	76.85	77.19	80.15	74.54	3.54	0.096	
Average Breast weight (g)	272a	367b	388b	298b	10.90	0.005	
Average Quota leg weight (g)	253a	279.04b	297.58b	245.20a	6.54	0.001	
Average Thigh weight (g)	171.08a	190.92b	187.79b	173.20a	5.14	0.014	
Average Drumstick weight (g)	80.92a	88.80b	103.67c	90.84b	2.46	0.001	
Breast muscle ratio	0.23a	0.26b	0.27b	0.25ab	0.01	0.001	
Thigh muscle ratio	0.14	0.14	0.13	0.13	0.01	0.061	
1 Dietary treatments: NC -Negative control (commercial broiler diet without antibiotics). PC-positive control (commercial broiler diet). AA1-commercial diet without antibiotics + 0.1% A. afra essential oil inclusion and AA2- commercial diet without antibiotics + 0.3 % A. afra essential oil inclusion.

Data are means of 10 replicate pens with 10 birds per pen

3.2 Internal organs

Table 5 presents the influence of A. afra essential oil incorporation in diets on internal organs of broiler chickens. Significant (P < 0.05) dietary effects were observed on internal organs (large intestines, gizzard, liver, spleen, and heart) and intestinal length (duodenum and ileum). The heaviest (P < 0.05) gizzard (60.25g) were obtained in broilers offered the AA2 diets. Conversely, the birds given the AA1 diet obtained the highest (P < 0.05) heart and spleen weights compared with other broilers. The birds offered the AA2 diet (90.82g) had the heaviest (P < 0.05) intestinal weights while those fed NC diet (79.90g) had the lightest. With regards to intestinal length, birds given the AA1 diet had the shortest (P <0.05) intestines compared to all other diets.Table 5 The effect of A. afra essential oil inclusion in diet on internal organs of broiler chickens.

Table 5	1Dietary treatments	
Parameters	NC	PC	AA1	AA2	SEM	P-value	
Gizzard (g)	43.23a	46.11a	43.59a	50.25b	1.64	0.001	
Heart (g)	8.24a	8.62a	9.08b	8.19a	0.27	0.016	
Spleen (g)	1.85b	1.76b	1.90b	1.50a	1.21	0.012	
Liver (g)	27.60a	32.30b	31.48b	28.03a	0.82	0.001	
Large Intestines (g)	79.90a	80.64b	83.59b	90.82c	2.32	0.041	
Duodenum (cm)	27.78a	33.65b	29.03a	37.12c	0.91	0.014	
Jejunum (cm)	71.91	71.15	70.98	74.16	1.16	0.116	
Ileum (cm)	66.90a	70.72b	64.15a	72.57b	1.30	0.001	
Intestinal pH	7.64	7.81	7.59	7.24	0.06	0.071	
1 Dietary treatments: NC -Negative control (commercial broiler diet without antibiotics). PC-positive control (commercial broiler diet). AA1-commercial diet without antibiotics + 0.1% A. afra essential oil inclusion and AA2- commercial diet without antibiotics + 0.3 % A. afra essential oil inclusion.

3.3 Meat quality

Table 6 presents the influences of A. afra essential oil dietary inclusion on meat quality parameters in broilers. Significant (P < 0.05) effects of diet were observed on all meat quality traits except for the drip loss. Highest ultimate pH value (6.24) was obtained from the birds given the AA1 diet while meat from birds offered the PC diet had the lowest (6.02). The meat colour coordinates were also affected by the diet with the highest (P < 0.05) lightness (L*) value obtained in birds given the AA1 and NC diets (55.73 and 55.82) while the birds offered the AA2 diet obtained the lowest (52.95). On the contrary, the AA2 treatment group obtained the highest (P < 0.05) value for redness (a*) whilst those fed NC diet obtained the lowest value. Yellowness (b*) values were highest in birds fed the PC (13.14) diet. With regards to the water holding capacity (WHC), meat from the birds fed the NC (16.61%) group had the lowest WHC followed by those fed PC diet. The birds fed the AA2 diet (26.78%) had the highest WHC showing greater potential of the breast muscle to retain more water in contrast with the other treatments. Meat from the broilers fed the NC (31.01%) diet also had the highest cooking loss whilst those fed the PC (24.69%) diet had the lowest.Table 6 The effect of A. afra essential oil inclusion in deit on meat quality measurements of broiler chickens.

Table 6	1Dietary treatments	
Parameters	NC	PC	AA1	AA2	SEM	P-value	
Ultimate pH	6.17b	6.02a	6.24b	6.17b	0.05	0.001	
Ultimate Temperature (°C)	17.08ab	19.16b	16.42a	16.08 a	0.32	0.001	
Meat colour							
L*	55.82b	53.14a	55.73b	52.95 a	0.76	0.011	
a*	0.33a	0.53a	0.71b	1.22c	0.28	0.014	
b*	10.77a	13.14b	11.76a	11.79a	0.53	0.001	
							
Water-holding capacity (WHC) (%)	16.61a	20.04b	24.79c	26.78c	1.50	0.003	
Drip loss %	1.73	1.46	1.46	2.34	0.33	0.426	
Cooking loss (%)	31.01b	24.69a	25.83a	28.50 b	0.87	0.016	
1 Dietary treatments: NC -Negative control (commercial broiler diet without antibiotics). PC-positive control (commercial broiler diet). AA1-commercial diet without antibiotics + 0.1% A. afra essential oil inclusion and AA2- commercial diet without antibiotics + 0.3 % A. afra essential oil inclusion.

3.4 Fatty acid profiles

The influences of A. afra essential oil incorporation in diets on fatty acid profiles of broiler meat are presented in Tables 7, Table 8, Table 9. An increase in intramuscular fat was apparent with the incorporation of the essential oil in the diet (Table 7). Birds fed the AA2 diet (2.37) obtained the highest (P < 0.05) levels of intramuscular fat followed by those offered the AA1 diet. Birds offered the PC diet had the least IMF content, while those fed the AA1 diet obtained the greatest concentration of fat free dry matter (FFDM). With regards to individual fatty acids, the major fatty acids observed in all diets included the oleic, palmitic, stearic, palmitoleic and vaccenic acids in order of abundance (Table 8). The essential oil fed birds appeared to have lower levels of palmitic, and oleic acid compared with the PC fed birds. However, when compared to the control, diets containing essential oils obtained higher (P < 0.05) levels of some important n-6 and n-3 fatty acids (Linoleic, α-Linolenic, Eicosadienoic and Docosahexanoic). Results on total nutritional indices (Table 8,9 reflected some desirable influenced of incorporation of essential oils in diets. Birds offered the essential oil containing diets obtained lower (P < 0.05) SFAs compared to the control. In contrast, the birds fed essential oil diets had greater (P < 0.05) amounts of PUFAs, total n-6 and n-3 fats, and higher PUFA: SFA ratio. The n-6/n-3 ratio was lowest (P <0.05) in the birds receiving the AA1 diet.Table 7 The effect of A. afra essential oil inclusion in diet on proximate fat composition (mg/g) in breast muscle of broiler chickens.

Table 7	1Dietary treatments	
2Parameter	NC	PC	AA1	AA2	SEM	P-Value	
IMF	21.2a	20.2a	23.2b	23.7b	1.31	0.002	
FFDM	208.3a	210.1ab	212.5b	199.7a	4.52	0.001	
Moisture	770.4ab	769.7a	764.2a	776.5b	2.45	0.016	
1 Dietary treatments: NC -Negative control (commercial broiler diet without antibiotics). PC-positive control (commercial broiler diet). AA1-commercial diet without antibiotics + 0.1% A. afra essential oil inclusion and AA2- commercial diet without antibiotics + 0.3 % A. afra essential oil inclusion.

2 Parameter: IMF = Intramuscular fat; FFDM = Fat free dry matter.

Table 8 The effect of A. afra essential oil inclusion in diet on fatty acid composition (mg/g) in breast muscle of broiler chickens.

Table 8	1Dietary treatments	
Fatty Acids	NC	PC	AA1	AA2	SEM	P-value	
Myristic (C14:0)	4.01	4.02	4.10	3.81	0.11	0.065	
Myristoleic (C14:1c9)	0.9	1.01	1.01	0.91	0.11	0.114	
Pentadecylic (C15:0)	0.21	0.11	0.21	0.32	0.12	0.189	
Palmitic (C16:0)	265.5ab	262.7a	262.3ab	253.2b	3.51	0.001	
Palmitoleic (C16:1)	58.4	59.1	60.7	54.5	3.42	0.367	
Margaric (C17:0)	0.4	0.41	0.42	0.51	0.11	0.776	
Heptadecenoic (C17:1)	1.42	1.01	1.53	1.11	0.23	0.157	
Stearic acid (C18:0)	71.4	69.9	69.6	68.3	4.20	0.115	
Oleic (C18:1)	334.1a	352.2b	337.1a	338.8a	6.91	0.006	
Elaidic (C18:1t9)	0.22	0.11	0.03	0.22	0.01	0.178	
Vaccenic (C18:1. 7)	40.9b	40.7b	35.1a	39.5ab	2.51	0.034	
Linoleic (C18:2. n-6)	180.3a	170.1a	185.7b	196.8c	5.81	0.019	
Arachidic (C20:0)	0.33	0.31	0.31	0.41	0.01	0.167	
γ-Linolenic	1.52	1.41	1.33	1.51	0.12	0.772	
α-Linolenic (C18:3 n-3)	10.0a	10.1a	11.3b	11.5b	0.31	0.041	
Eicosadienoic (C20:2. n-6)	1.41a	1.41a	1.72b	2.11c	0.22	0.112	
Erucic (C22:1)	4.71	4.71	4.82	4.91	0.41	0.871	
Arachidonic (C20:4 n-6)	21.9	18.9	20.1	19.7	0.23	0.145	
Eicosopentaenoic C20:5 n-3)	0.41	0.33	0.33	0.31	0.01	0.976	
Docosapentaenoic (C22:5 n-3)	1.81	1.42	1.61	1.33	0.02	0.887	
Docosahexanoic (C22:6 n-3)	0.41b	0.11a	0.44b	0.41b	0.37b	0.005	
1 Dietary treatments: NC -Negative control (commercial broiler diet without antibiotics). PC-positive control (commercial broiler diet). AA1-commercial diet without antibiotics + 0.1% A. afra essential oil inclusion and AA2- commercial diet without antibiotics + 0.3 % A. afra essential oil inclusion.

Table 9 The effect of A. afra essential oil inclusion in diet on total fatty acids indices (mg/g) in breast muscle of broiler chicken.

Table 9	1Dietary treatments	
2Parameter	NC	PC	AA1	AA2	SEM	P-value	
Total SFA	341.7b	337.2b	336.9a	336.4a	0.38	0.048	
Total MUFA	440.6	459	440.4	439.8	0.91	0.587	
Total PUFA	217.7b	203.7a	222.6c	233.7d	0.62	0.036	
Total n-6	205.1a	191.9a	208.9b	220.2c	0.73	0.028	
Total n-3	12.5a	11.9a	13.6b	13.5b	0.04	0.042	
PUFA: SFA	0.63a	0.61a	0.66ab	0.72b	0.12	0.016	
n-6/n-3	16.45b	16.15ab	15.33a	16.38b	0.21	0.045	
1 Dietary treatments: NC -Negative control (commercial broiler diet without antibiotics). PC-positive control (commercial broiler diet). AA1-commercial diet without antibiotics + 0.1% A. afra essential oil inclusion and AA2- commercial diet without antibiotics + 0.3 % A. afra essential oil inclusion.

2 Parameter: Total Saturated Fatty Acids =SFA; Total Mono Unsaturated Fatty Acids =MUFA; Total Poly Unsaturated Fatty Acids =PUFA; Total Omega- 6 Fatty Acids = n-6; Total Omega- 3 Fatty Acids = n-3; PUFA: SFA; n-6/n-3.

4 Discussion

4.1 Carcass traits

From the results the inclusion of A. afra in diets significant influenced the carcass parameters including the breast muscle indices. The breast muscle weight and the index are reflective of total amount of lean mass relative to the carcass weight (Disetlhe, 2017). The higher values for carcass parameters obtained in birds fed AA1 may be ascribed to the bio-stimulation effects A. afra oil extract on nutrient digestion efficiency and absorption (Zvarivadza & Marume, 2022), culminating in enhanced growth performance and muscle deposition as reported elsewhere in studies that used herbal plants of similar nature (Mpofu, 2016; Liu et al., 2009; Ozbey et al., 2007). A. afra contains a variety of bioactive compound including artemisia ketones, cineole, camphor and thujone that may influence gut microbial diversity, intestinal pH and permeability, and nutrient digestion, resulting in increased nutrient utilisation and ultimately growth rates and body weights of broiler chickens as observed elsewhere (Hong et al., 2012; Attia et al., 2011). The lack of dietary effects on dressing percentage is consonant with reports from previous studies (Disetlhe, 2017; Mpofu, 2016; Dotas et al., 2014; Moschini et al., 2005). Desirably, carcass parameters for birds fed the control diet and AA1 diet were comparable confirming the postulation that A. afra essential oils inclusion in diets can induce the same effect on feed utilisation and growth of broilers as conventional antibiotics. The inclusion of A. afra essential oil have the advantage of enhancing the quality of meat and excluding residues in meat as they are biodegradable natural plant products unlike antibiotics, ultimately meeting the consumer's requirements for safe and wholesome poultry products (Disetlhe, 2017; Hong et al., 2012; Attia et al., 2011; Engberg et al., 2000).

4.2 Internal organs

The observed effect of Artemisia afra oil extracts incorporation in diets in internal organ parameters in consistent with reports from other studies (Mpofu et al., 2016; Ahmad et al., 2011; Kirkpinar et al., 2011). The decline in intestinal length with the incorporation of A. afra essential oils in the diet might be indicative of increased nutrient utilization efficiency resulting in optimized growth in birds fed AA1 diets. Moreover, A. afra oil extracts have modulating effects on intestinal pH resulting in reduced viscosity of the gut contents while increasing the intestinal villus height, which contributes to the improvement of digestibility of nutrients as reported elsewhere (Afsharmanesh et al., 2016; Demir et al., 2008; Çabuk et al., 2006). Nonetheless, the observed high liver, heart and spleen weights in birds fed the A. afra containing diets could be reflective the influences of some antinutritional factors present in the essential oils which may need to be dealt with (Afolayan & Sunmonu., 2013; Patil, et al., 2011; Liu et al., 2009).

4.3 Meat quality

Meat pH is one of the critical quality parameters measured in meat, which can affect all other quality parameters (Hofmann, 1996; Huff-Lonergan et al., 2002; Knight et al., 2019). The ultimate pH (pHu) values of broiler meat ranging from 6.0 to 6.2 reported in this study are above the values reported by Disetlhe et al., 2019 and Li et al. (2016). The discrepancies in observations can be attributed to the differences in the chemical components of the plant products used diets in the studies. Nevertheless, pH values obtained in the current study fell within the expected pH threshold (pH 5.5 to 6.5) reported by Ao et al. (2008) for nonruminant animals. In the current study, the terpenoids and other bioactive components in A. afra could have caused the observed reduction in lightness (L) and an incline in redness (a*) and yellowness (b*). Secondary plant metabolites often alter the physiological state and chemical composition of meat resulting in changes in meat colour (Bai et al., 2013). The volatile compound contained in A. afra oils have been shown to depress discolouration of β-carotene (Liu at el., 2009, Patil, et al., 2011, Qwele et al., 2013, Afolayan & Sunmonu, 2013). Moreover, these components have also been linked to an increase in concentrations of conjugated linoleic acid (Liu et al., 2009, Mapiye et al., 2011). The high WHC observed in broilers offered the AA2 diet could be reflective of the influence of A. afra essential oils incorporation in diets in improving the ability of the meat to retain as reported in other studies (Qwele et al., 2013). Water holding capacity is generally linked to the concentrations of lipid peroxides present in the muscle which can be influenced by concentration of volatile compound in the essential oils (Schaefer et al., 1995, Macit et al., 2003). Although no effect of diet on drip loss was observed in this study, high levels of drip loss is undesirable as it induces a decline in WHC and meat tenderness, ultimately affecting meat quality in general (Wang et al., 2012).

4.4 Fatty acid profiles

The high PUFAs, total n-6 fatty acids and total n-3 fatty acids proportions obtained in birds fed diets containing A. afra essential oil could be due to the presence of some important fatty acids in the essential oils and the activities of the bioactive components in the essential oil in eliciting the increased synthesis of beneficial fatty acids that enhance healthiness of meat for the benefit of consumers (Trifan et al., 2022; Lim Ah Tock & Viljoen, 2024). These observations are consonant with reports by Cui et al. (2019) showing that incorporation of some essential oils may improve fatty acid profiles in meat by raising the concentrations of unsaturated fatty acids, particularly the n-3 fatty acids with many desirable effects on human health. According to Disetlhe et al. (2019) and Cui et al. (2019), both n-3 and n-6 FAs in the meat are critical as they are the precursor molecules for the production of eicosanoids, leucotriens, and thromboxanes, which modulate the immunological and cardiovascular pathways in humans. Plant essential oils s have also been shown to alter the serum cholesterol and low-density lipoproteins levels and elevates the levels of high-density lipoproteins of meat (Hong et al., 2012). The PUFA: SFA and n-6/n-3 ratios are critical indices used to assess the nutritional quality of meat (Ahmed et al., 2015; Disetlhe et al., 2019; Cui et al., 2019). Results from the study therefore implied that the incorporation of A. Afra essential oil in the diets may increase in the PUFA: SFA ratios which is desirable. Nevertheless, the values PUFA: SFA ratios for all diets exceeded the recommended value of 0.4 (FAO/WHO, 2009). Generally, a low PUFA: SFA ratio in meat of less than 0.4 is regarded as poor and unfavourable as it can potentiate an escalation in cholesterolaemia (FAO/WHO, 2009). Although the n-6/n-3 ratios of all treatments were above the recommended ratio of 5, it appeared that the A. afra essential oil in diet at 0.1% (AA1) could have the effects of lowering the ratio as reflected by the lower ratio in birds feed the AA1 diet compared with the control. Therefore, inclusion of A. afra EO in diets elicited favourable effects on the composition of important FAs necessary for the enhancement of human health.

5 Conclusion

Major findings of the study indicated that the incorporation of A. afra essential oil in diet induced some desirable effects on the carcass characteristics and meat quality parameters of broilers. In particular, the inclusion of A. afra essential oil at 0.1% significantly improved the carcass indices and meat quality parameters. Inclusion of A. afra essential oil in broiler diets also improved the proportion of PUFAs, PUFA/SFA ratio, n-3 and n-6 fatty acids and the which are important indicators of nutritional value of meat. It can, therefore, be concluded that A. afra essential oil can be effectively included in diets at 0.1% (AA1) with beneficial effects meat quality in broilers. However, caution must be taken when including the A. afra oil in diet at levels beyond 0.1% as it may negatively affect broiler performance.

Ethics approval

The feeding trial and experimental protocols were evaluated and ratified by the North-West University Research Ethics Committee (NWU-ANIMPROD REC # NWU-00660-18A)

Data and model availability statement

The data used in this study can be availed by the corresponding author on request.

Financial support

No specific grant was obtained from funding agencies other than from the Department of Animal Science, NWU

CRediT authorship contribution statement

U. Marume: Writing – review & editing, Writing – original draft, Resources, Methodology, Funding acquisition, Formal analysis, Conceptualization. W. Zvarivadza: Writing – review & editing, Writing – original draft, Methodology, Conceptualization. A. Hugo: Writing – review & editing, Validation, Methodology.

Declaration of competing interest

The authors hereby confirm that there are no conflict of interest in the submission of this manuscript

Acknowledgments

The authors would like to thank the Department of Animal Science, NWU who provided the resources used for the research.
==== Refs
References

Afolayan A.J. Sunmonu T.O. Protective role of Artemisia afra aqueous extract on tissue antioxidant defense systems in streptozotocin-induced diabetic rats African Journal of Traditional, Complementary and Alternative Medicines 10 1 2013 15 20 10.4314/ajtcam.v10i1.3
Afsharmanesh M. Lotfi M. Mehdipour Z. Effects of wet feeding and early feed restriction on blood parameters and growth performance of broiler chickens Animal Nutrition 2 2016 168 172 10.1016/j.aninu.2016.04.002 29767053
Ahmad A. Khan A. Akhtar F. Yousuf S. Xess I. Khan L. Manzoor N. Fungicidal activity of thymol and carvacrol by disrupting ergosterol biosynthesis and membrane integrity against Candida European Journal of Clinical Microbiology and Infectious Diseases 30 2011 41 50 10.1007/s10096-010-1050-8 20835742
Ahmed S.T. Islam M.M. Bostami A.B.M.R. Mun H.S. Kim Y.J. Yang C.J. Meat composition, fatty acid profile and oxidative stability of meat from broilers supplemented with pomegranate (Punica granatum L.) by-products Food Chemistry 188 2015 481 488 10.1016/j.foodchem.2015.04.140 26041221
Ao T. Cantor A.H. Pescatore A.J. Pierce J.L. In vitro evaluation of feed grade enzymes activity at pH levels stimulating various parts of the avian digestive tract Animal Feed Science and Technology 140 2008 462 468 10.1016/j.anifeedsci.2007.04.004
Ari M.M. Ayanwale B.A. Ogah D.M. Effects of alkali treatment of Soya bean on carcass traits, intestinal morphology and cooking yield of broilers Trakia Journal of Sciences 2 2013 189 196 http://www.uni-sz.bg
Attia Y.A. Zeweil H.S. Alsaffar A.A. El-Shafy A.S. Effect of non-antibiotic feed additives as an alternative flavomycin on productivity, meat quality and blood parameters in broilers Arch Fur Geflugelkunde 75 2011 40 48
Attia Y.A. Al-Harthi M. El-Kelawy M. Utilization of essential oils as a natural growth promoter for broiler chickens Italian Journal of Animal Science 18 2019 1005 1012 10.1080/1828051X.2019.1607574
Bai H.X. Chang Q.F. Shi B.M. Shan A.S. Effects of fulvic acid on growth performance and meat quality in growing-finishing pigs Livestock Science 158 2013 118 123 10.1016/j.livsci.2013.10.013
Çabuk M. Bozkurt M. Alçiçek A. Çatl A.U. Başer K.H.C. The effect of a mixture of herbal essential oils, a mannan oligosaccharide or an antibiotic on performance of laying hens under hot climatic conditions South African Journal of Animal Science 36 2006 135 141
Cázares-Gallegos R. Silva-Vázquez R. Hernández-Martínez C.A. Gutiérrez-Soto J.G. Kawas-Garza J.R. Hume M.E. Méndez-Zamora Performance, Carcass Variables, and Meat Quality of Broilers Supplemented with Dietary Mexican Oregano Oil Brazilian Journal of Poultry Science 21 2019 1 10 10.1590/1806-9061-2018-0801
Cho J.H. Kim I.H. Kim I. Effects of phytogenic feed additive on growth performance, digestibility, blood metabolites, intestinal microbiota, meat color and relative organ weight after oral challenge with clostridium perfringens in broilers Livestock Science 160 2014 82 88 10.1016/j.livsci.2013.11.006
Chowdhury S. Mandal G.P. Patra K.A. Different essential oils in diets of chickens: 1. Growth performance, nutrient utilisation, nitrogen excretion, carcass traits and chemical composition of meat Animal Feed Science and Technology 236 2018 86 97 10.1016/j.anifeedsci.2017.12.002
Cui X. Gou Z. Fan Q. Li L. Lin X. Wang Y. Jiang S. Jiang Z. Effects of dietary perilla seed oil supplementation on lipid metabolism, meat quality, and fatty acid profiles in Yellow-feathered chickens Poultry Science 98 11 2019 5714 5723 10.3382/ps/pez358
Demir E. Kilinc K. Yildirim Y. Dincer F. Eseceli H. Comparative effects of mint, sage, thyme and flavomycin in wheat-based broiler diets Arch Zootechnica 11 2008 54 63
Disetlhe A.R.P. Marume U. Mlambo V. Hugo A. Effects of dietary humic acid and enzymes on meat quality and fatty acid profiles of broiler chickens fed canola-based diets Asian-Australas Journal of Animal Science 32 5 2019 711 720 10.5713/ajas.18.0408
Disetlhe A.R.P. Marume U. Mlambo V. Humic acid and enzymes inclusion in canola-based diets generate different responses in growth performance, protein utilization dynamics, and hemato-biochemical parameters in broiler chickens Poultry Science 97 8 2018 2745 2753 10.3382/ps/pey047
Dotas V. Bampidis V.A. Sinapis E. Hatzipanagiotou A. Papanikolaou K. Effect of dietary field pea (Pisum sativum L.) supplementation on growth performance, and carcass and meat quality of broiler chickens Livestock Science 164 2014 135 143 10.1016/j.livsci.2014.03.024
Engberg R.M. Hedemann M.S. Leser T.D. Jensen B.B. Effect of zinc bacitracin and salimomycin on intestinal microflora and performance of broilers Poultry Science 79 2000 1311 1319 10.1093/ps/79.9.1311
FAO/WHO Fats and fatty acids in human nutrition Proceedings of the Joint FAO/WHO Expert Consultation Geneva, Switzerland 55 2008 Annals of Nutritional Metabolism 5 300 November 10–14
Folch J. Lees M. Sloane Stanley G.H. A simple method for the isolation and purification of total lipids from animal tissues Journal of Biological Chemistry 226 1957 497 509 10.1016/S0021-9258(18)64849-5 13428781
Gong J. Yin F. Hou R. Yin Y.L. Chinese herbs as alternatives to antibiotics in feed for swine and poultry production: potential and challenges in application Review Canadian Journal of Animal Science 94 2014 223 241 10.1139/CJAS2013-144
Grau R. Hamm R. Measurement of water-holding capacity and juiciness in Meat, Poultry and Fish Products 105 1957 Zur Lebensmittel Untersuchungen Forschung 446 460
Hofmann K. What is quality? Definition, measurement and evaluation of meat quality Meat Focus International 3 1996 73 82
Hong J.C. Steiner T. Aufy A. Lien T.F. Effects of supplemental essential oil on growth performance, lipid metabolites and immunity, intestinal characteristics, microbiota and carcass traits in broilers Livestock Science 144 2012 253 262 10.1016/j.livsci.2011.12.008
Huff-Lonergan E. Baas T.J. Malek M. Dekkers J.C.M. Prusa K. Rothschild M.F. Correlations among selected pork quality traits Journal of Animal Science 80 2002 617 627 10.2527/2002.803617x 11892678
Jenkins T.C. Technical note: Common analytical errors yielding inaccurate results during analysis of fatty acids in feed and digesta samples Journal of Dairy Science 93 3 2010 1170 1174 10.3168/jds.2009-2509 20172237
Kirkpinar F. Ünlü H.B. Özdemir G. Effects of oregano and garlic essential oils on performance, carcase, organ and blood characteristics and intestinal microflora of broilers Livestock Science 137 2011 219 225 10.1016/j.livsci.2010.11.010
Kirkpinar F. Ünlü H.B. Serdaroğlu M. Turp G.Y. Effects of dietary oregano and garlic essential oils on carcass characteristics, meat composition, colour, pH and sensory quality of broiler meat British Poultry Science 55 2 2014 157 166
Knight M.I. Linden N. Ponnampalam E.N. Kerr M.G. Brown W.G. Hopkins D.L. Wesley I. Development of VISNIR predictive regression models for ultimate pH, meat tenderness (shear force) and intramuscular fat content of Australian lamb Meat Science 155 2019 102 108 10.1016/j.meatsci.2019.05.009 31102991
Li X.K. Wang J.Z. Wang C.Q. Zhang C.H. Li X. Tang C.H. Wei X.L Effect of dietary phosphorus levels on meat quality and lipid metabolism in broiler chickens Food chemistry 205 2016 289 296 10.1016/j.foodchem.2016.02.133 27006242
Lim Ah Tock M.J. Viljoen A.M. Investigating the quality of commercially available indigenous southern African plant oils and the need for quality regulation South African Journal of Botany 168 2024 595 609 10.1016/j.sajb.2024.03.046
Liu N.Q. Van der Kooy F. Verboort R. Artemisia afra: A potential flagship for African medicinal plants South African Journal of Botany 75 2009 185 195
Macit M. Aksakal V. Emsen E. Aksu M.I. Karaoglu M. Esenbuga N. Effects of vitamin E supplementation on performance and meat quality traits of Morkaraman male lambs Meat Science 6 2003 51 55 10.1016/s0309-1740(02)00052-9
Mangwiro T.N. Dhliwayo M. Nyamushamba G.B. Towards sustainable broiler production – Does use of processed velvet bean (Mucuna pruiens) as an adjunct protein substitute for soyabean affect broiler performance Scientific Journal of Animal Science 2 11 2013 296 303
Mapiye C. Chimonyo M. Dzama K. Hugo A. Strydom P.E. Muchenje V. Fatty acid composition of beef from Nguni steers supplemented with Acacia karroo leaf-meal Journal of Food Compositional Analysis 24 2011 523 528 10.1016/j.jfca.2011.01.018
Moschini M. Masoero F. Prandini A. Fusconi G. Morlacchini M. Piva G. Raw pea (Pisum sativum), raw faba bean (Vicia faba var. minor) and raw lupin (Lupinus albus var. multitalia) as alternative protein sources in broiler diets Italian Journal of Animal Science 4 2005 59 69 10.4081/ijas.2005.59
Mpofu D.A. Marume U. Mlambo V. The effects of Lippia javanica dietary inclusion on growth performance, carcass characteristics and fatty acid profiles of broiler chickens Animal Nutrition 2 3 2016 160 167 10.1016/j.aninu.2016.05.003 29767096
Muyima N.Y.O. Zulu G. Bhengu T. Popplewell D. The potential application of some novel essential oils as natural cosmetic preservatives in an aqueous cream formulation Flavour and Fragrance Journal 17 2002 258 266 10.1002/ffj.1093
Ozbey O. Esen F. The effects of breeding systems and stocking density on some blood parameters of rock partridges (Alectoris graeca) Poultry Science 86 2007 420 422 10.1093/ps/86.2.420
Panaite T.D. Criste R.D. Vlaicu P.A. Saracila M. Tabuc C. Olteanu M. Turcu R.P. Buleandră M. Influence of Artemisia Annua on broiler performance and intestinal microflora Brazilian Journal of Poultry Science 21 2019 4 10.1590/1806-9061-2019-1092
Park J.H. Kang S.N. Chu G.M. Jin S.K. Growth performance, blood cell profiles, and meat quality properties of broilers fed with Saposhnikovia divaricata, Lonicera japonica, and Chelidonium majus extracts Livestock Science 165 2014 87 94 10.1016/j.livsci.2014.04.014
Patil G.V. Dass S.K. Chandra R Artemisia afra and modern diseases Journal of Pharmacogenomics and Pharmacoproteomics 2 2011 105 10.4172/2153-0645.1000105
Qwele K. Muchenje V. Oyedemi S.O. Moyo B. Masika P.J Chemical composition, fatty acid contents and antioxidant potential of meat from goats supplemented with Moringa (Moringa oleifera) leaves, sunflower cake and grass hay Meat Science 93 2013 455 462 10.1016/j.meatsci.2012.11.009 23273450
SAS, 2010. Statistical Analysis System Institute Inc. Users Guide, Carry, NC, USA.
Schaefer D.M. Liu Q. Faustman C. Yin M.C. Supranutritional administration of vitamins E and C improves oxidative stability of beef Journal of Nutrition 125 1995 1792 1798
Sukhija P.S. Palmquist D.L. Rapid method for determination of total fatty acid content and composition of feedstuffs and feces Journal of Agricultural and Food Chemistry 36 6 1988 1202 1206 10.1021/jf00084a019
Trifan A. Zengin G. Sinan K.I. Sieniawska E. Sawicki R. Maciejewska-Turska M. Skalikca-Woźniak K. Luca S.V. Unveiling the phytochemical profile and biological potential of five Artemisia species Antioxidants 11 2022 1017 10.3390/antiox11051017 35624882
Vahmani P. Rolland D.C. McAllister T.A. Block H.C. Proctor S.D. Guan L.L. Prieto N. López-Campos Ó. Aalhus J.L. Dugan M.E.R. Effects of feeding steers extruded flaxseed on its own before hay or mixed with hay on animal performance, carcass quality, and meat and hamburger fatty acid composition Meat Science 131 2017 9 17 10.1016/j.meatsci.2017.04.008 28448838
Viljoen A.M. Van Vuuren S.F. Gwebu T. Demirci B. Baser K. Husnu C The geographical variation and antimicrobial activity of African wormwood (Artemisia afra Jacq.) essential oil Journal of Essential Oil Research 18 2006 19 25 10.1080/10412905.2006.12067114
Wang H. Wang L.S. Shi B.M. Shan A.S. Effects of dietary corn dried distillers grains with solubles and vitamin E on growth performance, meat quality, fatty acid profiles, and pork shelf life of finishing pigs Livestock Science 149 2012 155 166 10.1016/j.livsci.2012.07.009
Wenk C. Herbs and botanicals as feed additives in monogastric animals Asian-Australas Journal of Animal Science 16 2003 282 289 10.5713/ajas.2003.282
Witkowska D. Sowińska J. Murawska D. Matusevičius P. Kwiatkowska-Stenzel A. Mituniewicz T. Wójcik A Effect of peppermint and thyme essential oil mist on performance and physiological parameters in broiler chickens South African Journal of Animal Science 49 2019 1 10.4314/sajas.v49i1.4
Zhai H. Liu H. Wang S. Wu J. Kluenter A.M. Potential of essential oils for poultry and pigs Animal Nutrition Journal 4 2 2018 179 186 10.1016/j.aninu.2018.01.005
Zvarivadza W. Marume U. Growth performance and heamatobiochemical parameters of broilers fed diets containing Artemisia afra essential oil Canadian Journal of Animal Science 102 2 2022 382 391 10.1139/cjas-2020-0113
