Performance, Carcass Variables, and Meat Quality of Broilers Supplemented with Dietary Mexican Oregano Oil

R Cázares-Gallegos R Silva-Vázquez CA Hernández-Martínez JG Gutiérrez-Soto JR Kawas-Garza ME Hume GM Méndez-Zamora About the authors

ABSTRACT

The current study was conducted to evaluate the dietary supplementation of Mexican oregano essential oil (MOO; Lippiaberlandieri Schauer) on broiler performance, carcass variables, meat quality, and sensory evaluation. One-day-old mixed-sex broilers were distributed in the following treatment groups, according to MOO supplementation levels: 0 = control diet; 200 = diet + 2200 mg of MOO/kg; 400 = diet + 4200 mg of MOO/kg; 600 = diet + 6200 mg of MOO/kg; 800 = diet + 8200 mg of MOO/kg; 1000 = diet + 1000 mg of MOO/kg. MOO affected (p<0.05) body weight, feed and water intake, and feed conversion ratio. The 200 and 400 mg/kg formulations gave better results at 7, 14 and 28 d than the other diets. MOO at 1000 mg/kg increased (p<0.05) slaughter weight and hot carcass yield, and decreased meat pH and cooking loss. The 200 and 400 treatments increased breast meat redness (a*), but reduced yellowness (b*). Meat hardness, cohesiveness and resilience were affected (p<0.05) by MOO, but not (p>0.05) the sensory parameters evaluated. Mexican oregano oil presents positive qualities as a plant-derived performance enhancer in broiler diets and improves of the meat quality of broilers at the levels of 200, 400 and 600 mg/kg of diet.

Keywords:
Body weight; breast; sensory; texture

INTRODUCTION

Resistance of pathogenic bacteria to antibiotics used in broilers is widely known. Human health can be directly affected by residues of antibiotic growth promoters (AGP)in the meat or by the development of antibiotic-resistant pathogenic bacteria that may spread to humans (Chowdhury et al., 2018Chowdhury S, Prasad Mandal G, Kumar Patra 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 2018;236: 86-97.). In recent years, natural strategies are being studied for application in poultry production.

Leaves of the oregano plant and its essential oils are considered phytogenic replacers for AGPs in broiler diets (Toghyani et al., 2011Toghyani M, Toghyani M, Gheisari A, Ghalamkari G, Eghbalsaied S. Evaluation of cinnamon and garlic as antibiotic growth promoter substitutions on performance, immune responses, serum biochemical and haematological parameters in broiler chicks. Livestock Science 2011;138(1-3):167-173.), as well as growth promoters, natural antibiotics, and improvers of broiler meat quality. Two plants commonly used fall under the common name oregano. There are the oregano varieties Origanum spp. (common name Greek oregano, a member of the mint family Lamiaceae), which are native to Eurasia and the Mediterranean. There is also the oregano variety Lippiaberlandieri Schauer (common name Mexican oregano, a member of family Verbenaceae), which is native to Mexico, Central America, and southwestern United States. The dried leaves and inflorescences of Mexican oregano, similar to the Greek varieties, are used as condiments and treatment for respiratory and digestive diseases (Rivero-Cruz et al., 2011Rivero-Cruz I, Duarte G, Navarrete A, Bye R, Linares E, Mata R. Chemical composition and antimicrobial and spasmolytic properties of Poliominthalongifloraand Lippiagraveolens essential oils. Journal of Food Science 2011;76(2):C309-C317.). The main constituents of essential oils from Mexican oregano are carvacrol, thymol, b-myrcene, a-terpinene, ɤ-terpinene, p-cymene and ceneol (Silva Vazquez & Dunford, 2005Silva Vazquez SR, Dunford NT. Bioactive components of Mexican oregano oil as affected by moisture and plant maturity. Journal of Essential Oil Research 2005;17(6):668-671.).

Some studies have evaluated the performance and meat quality of broilers given diets supplemented with natural extracts (Cho et al., 2014Cho JH, Kim IH, 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 2014;160:82-88.; Park et al., 2014Park JH, Kang SN, Chu GM, Jin SK. Growth performance, blood cell profiles, and meat quality properties of broilers fed with Saposhnikovia divaricata, Lonicera japonica, and Chelidonium majus extracts. Livestock Science 2014;165:87-94.; Mpofu et al., 2016Mpofu DA, Marume U, Mlambo V, Hugo A. The effects of Lippiajavanica dietary inclusion on growth performance, carcass characteristics and fatty acid profiles of broiler chickens. Animal Nutrition 2016;2(3):160-167.; Chowdhury et al., 2018Chowdhury S, Prasad Mandal G, Kumar Patra 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 2018;236: 86-97.), and Greek (OEO) and Mexican (MOO) oregano essential oils (Silva Vázquez et al., 2015Silva Vázquez R, Durán Meléndez LA, Santellano Estrada E, Rodríguez ME, Villalobos VG, Méndez-Zamora G, et al. Performance of broiler chickens supplemented with Mexican oregano oil (Lippiaberlandieri Schauer). Revista Brasileira de Zootecnia 2015;44(8):283-289.; Peng et al., 2016Peng QY, Li JD, Li Z, Duan ZY, Wu YP. Effects of dietary supplementation with oregano essential oil on growth performance, carcass traits and jejunal morphology in broiler chickens. Animal Feed Science and Technology 2016;214:148-153.; Méndez-Zamora et al., 2017Méndez-Zamora G, Durán Meléndez LA, Hume ME, Silva-Vázquez R. Performance, blood parameters, and carcass yield of broiler chickens supplemented with Mexicano regano oil. Revista Brasileira de Zootecnia 2017;46(6):515-520.; Reyer et al., 2017Reyer H, Zentek J, Männer K, Youssef IMI, Aumüller T, Weghuber J, et al. Possible molecular mechanisms by which an essential oil blend from star anise, rosemary, thyme, and oregano and saponins increase the performance and ileal protein digestibility of growing broilers. Journal of Agricultural and Food Chemistry 2017;65(32):6821-6830.), demonstrating their effects on feed intake, growth promotion, blood profile, and meat quality. Origanum vulgare L. and Origanumonites sp. and A. sativum L. are the most frequently phytogenic additives used in broiler production. However, a limited number of studies have been reported regarding Mexican oregano essential oils from Lippiaberlandieri in broiler diets (Méndez-Zamora et al., 2015a, 2015b; Silva-Vazquez et al., 2015; Méndez-Zamora et al., 2017). The use of Mexican oregano essential oils may be a value-added phytogenic alternative to traditional antibiotics in broiler production.

The current study was carried out to evaluate the effects of the MOO supplementation in broiler diets on their growth performance, carcass traits, and meat physicochemical variables, texture analysis and meat sensory evaluation.

MATERIALS AND METHODS

Birds and experimental diets

The study was carried out at the Marin Experimental Farm of the Universidad Autonoma de Nuevo Leon (UANL), located at Marin, Nuevo Leon, Mexico. The study site is located between 25° 45’ and 26° 2’ N and 99° 48’ 100° 6’ W, at an altitude between 200 and 1500 m, with a mean temperature 21°C, annual precipitation between 600-800 mm, and is in a semi-warm sub humid climate (INEGI, 2017).

The experimental procedures complied with the Mexican standards on animal use (NOM-062-ZOO, 1999), and were approved by the local animal care and welfare committee of the Universidad Autonoma de Nuevo Leon.

In total, 360 one-day-old Ross308 mixed-sex broiler chicks (49.92 ± 1.33 g) were obtained from a local hatchery and distributed into 30 floor pens with 12 birds each (1.20 x 1.20 x 0.80 m) on fresh wood-shavings litter. Five pens were randomly assigned to one of six treatments (diets): 0 = control diet (CD), no MOO; 200 = CD + 200 mg of MOO/kg; 400 = CD + 400 mg of MOO/kg; 600 = CD + 600 mg of MOO/kg; 800 = CD + 800 mg of MOO/kg; and 1000 = CD + 1000 mg of MOO/kg.

The Mexican oregano oil was prepared by steam distillation of dry leaves (Natural Solutions Company SMI, Jimenez, Chihuahua, Mexico), and was incorporated into the diets with canola oil as carrier and by mixing for 8 min. The main components of MOO (60.02% carvacrol, 23.63% 1,8-cineole, 9.57% p-cymene, 3.96% thymol, 0.11%gamma-terpinene, and 2.71% others) were determined by gas chromatography (Clarus 600 and MS SQ8 PerkinElmer Inc., Waltham, MA, USA), according to Silva-Vazquez et al. (2017Silva-Vazquez R, Duran-Melendez LA, Mendez-Zamora G, Estrada ES, Xie M, Dunford TN, et al. Antioxidant activity of essential oils from various Mexican oregano ecotypes and oil fractions obtained by distillation. JSM Chemistry 2017;5(3):1046.).

Starter (1-21 d) and finisher (22-40 d) diets were formulated according to the NRC (1994NRC. Nutritional requirements of poultry. 9th ed. Washington: National Academy Press; 1994.) and as used by Silva-Vázquez et al. (2015Silva Vázquez R, Durán Meléndez LA, Santellano Estrada E, Rodríguez ME, Villalobos VG, Méndez-Zamora G, et al. Performance of broiler chickens supplemented with Mexican oregano oil (Lippiaberlandieri Schauer). Revista Brasileira de Zootecnia 2015;44(8):283-289.) and Méndez-Zamora et al. (2017Méndez-Zamora G, Durán Meléndez LA, Hume ME, Silva-Vázquez R. Performance, blood parameters, and carcass yield of broiler chickens supplemented with Mexicano regano oil. Revista Brasileira de Zootecnia 2017;46(6):515-520.). The ingredients and analyzed chemical composition of the control starter and finisher diets are shown in Table 1. Feed and water were provided ad libitum throughout the experiment. Husbandry practices were applied according to above-mentioned authors. House temperature was set at 34°C on the first day, followed by 32°C over the remainder of the first week, and then was reduced by 3°C per week until it reached 23°C. The relative humidity fluctuated between 65 and 85%. Lighting was provided 22 h/d.

Table 1
Ingredients of the starter and finisher diets for broilers.

Growth performance evaluation

The initial body weight (IBW; g) was determined at the beginning of the experiment. Broiler body weight (BW), feed intake (FI; g intake of feed per week/number of broilers per pen), and water intake (WI; g intake of water per week/number of broilers per pen) were evaluated on d 7, 14, 21, 28, 35, and 40. These variables were used to estimate weekly body weight gain (WBWG; g (BWcurrent-BWprevious)/day) and feed conversion ratio (FCR; FI/WBWG) and were determined at the same periods. Offered and rejected feed weights were recorded to estimate these variables.

Slaughter variables

The slaughter process was carried out according to the Official Mexican Standard (NOM-033-SAG/ZOO, 2014) and the method of Méndez-Zamora et al. (2015aMéndez-Zamora G, García-Macías JA, Durán-Meléndez LA, Herman-Lara E, Santellano-Estrada E, Silva-Vazquez R. Aceite esencial de orégano (LippiaberlandieriSchauer) en variables de calidad de la canal de pollo. Ecosistemas y Recursos Agropecuarios 2015a;2(4):41-51.). Thirty 40-day-old chicks from each treatment (six birds per pen) were randomly selected for slaughter by cervical dislocation. Slaughter weight (SW), and hot (HCW; after removal of the head, feathers, and internal organs) and cold (CCW; 24 h post mortem) carcass weights were recorded to calculate hot (HCY; (HCW/SW)×100) and cold (CCY; (CCW/SW)×100)carcass yields. Breast meat yield (BY = (BrW/SW)×100) was estimated as breast meat weight (BrW) relative to SW (two birds per pen per treatment).

Meat physicochemical variables

Breast meat (pectoralis major) pH, color, water holding capacity (WHC), and cooking loss (CL) were measured 24 h post mortem. These variables were measured in duplicate in ten breasts from each treatment, randomly selected, two breasts/pen/treatment. Meat pH was determined with a puncture electrode (HI 99163, Hanna Instruments WoonSocket, RI, USA). Meat color values for lightness (L*), redness (a*), yellowness (b*), Chroma (saturation index) and Hue angle were measured with a colorimeter (CR-400 Konica Minolta®, Tokyo, Japan; Illuminant/Observer: D65/10), set on the CIE Lab System (CIE, 1976) on the breast surfaces. Values for L*, a* and b* were used to estimate total color change (∆E) and browning index (BI), according to Ledesma et al. (2016Ledesma E, Laca A, Rendueles M, Díaz M. Texture, colour and optical characteristics of a meat product depending on smoking time and casing type. LWT-Food Science and Technology 2016;65:164-172.), using the colorimeter calibration values L*0 = 94.18, a*0 = -0.43 and b*0 = 3.98. The equipment was calibrated with a standard white plate. Breast meat WHC was determined using the compression method according to Tsai & Ockerman (1981Tsai TC, Ockerman HW. Water binding measurement of meat. Journal of Food Science 1981;46(3):697-701.) and Méndez-Zamora et al. (2015bMéndez-Zamora G, García Macías JA, Santellano Estrada E, Durán Meléndez LA, Silva Vázquez R. Aceite de orégano sobre la calidad de pechuga de pollos de engorda. Investigación y Ciencia 2015b;23(65):5-12.). Approximately 300 ± 0.1 mg of meat sample were placed between two pieces of filter paper, between two acrylic-plastic plates, applying a force of 4 kg for 20 min, and obtaining the final weight: WHC=100{[(initialweightfinalweight)/initialweight]x100}. To determine CL, the breast meat was vacuum-packed (Koch 800, Kansas City, MO, USA) in vacuum bags (Zubex Industrial SA de CV, Monterrey, Nuevo Leon, Mexico) and cooked by immersion in water at 75.0 ± 0.1°C for 1 h. Then the samples were cooled by immersion in water at 4°C for 20 min. The pieces were removed from the bags, carefully drained, and weighed. Raw and cooked weights of each breast meat sample were recorded to evaluate CL percentage as [(rawweightcookedweight)/rawweightpiece]×100.

Meat texture analysis

Breast meat shear force (SF) and texture profile analysis (TPA) were carried out with a TA.XT.Plustexturometer (Stable Micro Systems, Serrey, England) in two sections per replicate (2 breasts/pen/treatment). SF (N, Newtons) was measured using a Warner-Bratzler shear blade with a triangular slot cutting edge. Rectangular meat slices (3.5 cm long x 1.0 cm wide x 1.0 cm high for each breast) were used to evaluate SF. Samples were cut parallelly to the direction of the muscle fibers. Test conditions used in the instrument were velocities of 2 mm/s pre-test, 2 mms/s during the test, 10 mm/s post-test, and a distance of 15 mm. The SF value was calculated from the maximum point of the curve generated. TPA was determined using standardized cylinders (1.5 cm high and 2.5 cm in diameter), oriented perpendicular to the direction of the muscle fibers. A cylindrical piston (75 mm in diameter) was used to compress the sample during two test cycles, compressing the sample up to 60% of the original height within a time span of 5 s between the cycles. Force-time curves of deformation were obtained from the conditions established in the texturometer. The velocities used were 2.0 mm/s pre-test, 5.0 mm/s during the test, and 5.0 mm/s post-test. The following parameters were recorded according to Bourne (1978Bourne MC. Texture profile analysis. Food Technology 1978;35:62-67.): hardness (Hard; N), adhesiveness (Adhes; g/s), springiness (Spring; mm), cohesiveness (Cohes; dimensionless), gumminess (Gum; g), chewiness (Chew; g mm), and resilience (Resil; dimensionless).

Sensory evaluation

The most important meat attributes are appearance and texture, since they exert the most influence on consumer initial selection and ultimate satisfaction with traditional poultry meat products (Fletcher, 2002Fletcher DL. Poultry meat quality. World's Poultry Science Journal 2002;58(2):131-145.). An affective sensory test of breast meat attributes was conducted to measure the satisfaction level of 30 consumers. The breasts (1 breast/pen/treatment) were vacuum-packed and cooked by immersion in water at 75.0 ± 0.1°C for 1 h. Each consumer evaluated four 1.5-cm cut cubes chosen at random per treatment. Samples for evaluation were maintained at 30°C and were presented in small plastic cups codified with three random numbers. The attributes evaluated were odor, taste, tenderness and overall acceptability. A 7-point hedonic scale was used, where 7 = liked very much and 1 = disliked very much (Anzaldúa-Morales, 1994Anzaldúa-Morales A. La evaluación sensorial de los alimentos en la teoría y la práctica. Zaragoza: Acribia;1994. 220 p.; Meilgaard et al., 2006Meilgaard M, Civille GV, Carr TB. Affective tests consumer tests and in-house panel acceptance tests. In: Meilgaard M, Civille GV, Carr TB, editors. Sensory evaluation techniques. Boca Raton: CRC Press; 2006. p 231-251.).

Statistical analysis

The growth performance data were analyzed using the MIXED procedure of SAS (2006) and the following statistical model (Wang & Goonewardene, 2004Wang Z, Goonewardene AL. The use of MIXED models in the analysis of animal experiments with repeated measures data. Canadian Journal of Animal Science 2004;84:1-12.): yijk=µ+Ƭi+δj+(Ƭδ)ij+Фk(ij)+λ+Ԑijk;where yijk = production variables measured during the experiment, µ = general mean, Ti = effect of the ith treatment (0, 200, 400, 600, 800, and 1000), dj = effect of the jth day of fattening (7, 14, 21, 28, 35 and 40 d), (Ƭd)ij = fixed effect of the interaction between ith treatment and jth day of fattening, Фk(ij) = nested effect of the ith treatment in each pen where the chickens remained for the jth day of fattening, λ = effect of the covariate IW, and Ԑijk = random error normally distributed with mean zero and variance σ2Ԑijk ~ N (0, σ2). A significance level of p<0.05 was used to detect significant statistical difference, and when the p-value was less than 0.05 in fixed effects and its interaction, the means were compared using Adjust = Tukey (SAS, 2006).

Carcass parameters and meat physicochemical and texture variables were analyzed with the GLM procedure (SAS, 2006), according to the following statistical model: yij=µ+Ƭi+λ+Ԑij; where yij = variables evaluated; µ = general mean; Ti = effect of the i th treatment (0, 200, 400, 600, 800, and 1000); λ = effect of the covariate IW, and Ԑij = random error normally distributed with mean zero and variance σ2ij ~ N (0, σ2)). When the fixed effect had significant effect (p<0.05), the means were compared using the Tukey’s test (SAS, 2006).

The sensorial data were analyzed with a complete random block design according to the statistical model yij=µ+Ƭi+βj+Ɛj. The treatments (Ƭi) represented the fixed effects and each consumer was the block (βj). A significance level of p<0.05 was used to assess significant differences among treatment applying Tukey’s test (SAS, 2006).

RESULTS

The statistical model was significant (p<0.001) for growth performance variables, and the interaction effect was statistically significant (p<0.001) for WBWG and FCR. Specifically, treatments were different (p<0.05) and days were significant (p<0.001) for performance variables.

Body weight and feed intake

On d 28, BW was different (p<0.05) among treatments, with 400 mg/kg being highest and 800 mg/kg lowest (Table 2). At 40 d, BW was not different (p>0.05) by treatment, although the400 mg/kg treatment BW was slightly higher. BW did increase for all treatments over time, being highest at 40 d. FI was affected (p<0.05) at 7, 14 and 21 d (starter period), presenting higher FI with 0, 400, and 600(at 21 d) mg/kg, while200, 600 (at 7 and 14 d), 800, and 1000 mg of MOO/kg showed lower values (Table 2). Somewhat similar performance values were found over the fattening period (1-40 d); however, broilers given 400mg/kg did consumed more feed (FI), although at levels not significantly different from broilers given the other MOO formulations. Due to the period between 35 d and 40 d accounting for only 5 d and not 7 d, the FI values statistically and numerically were lower more specifically when compared to 28 d and 35 d. Overall, FI increased (p<0.05) incrementally during the period from 7 d to 35 d. WI was different (p<0.05) at 28 d and 1-40 d. During these periods, 400 and 600 mg/kg promoted the highest (p<0.05) WI, while that 200 and 800 mg/kg presented lower (p<0.05) WI values.

Table 2
Performance parameters of broilers supplemented with Mexican oregano essential oil.

Weekly body weight gain and feed conversion ratio

Production efficiencies of broilers fed MOO in the diet are given in Table 3. Effects of MOO levels on WBWG were different (p<0.05) at 21 and 28 d, with higher values obtained with400 and 600 mg/kg (p<0.05). At 21 d (starter period), birds fed 200 mg/kg had the lowest (p<0.05) WBWG value and at 28 d (finisher period), those fed 800 mg/kg had the lowest (p<0.05) value. During the other evaluated periods, there were no WBWG differences (p>0.05). Throughout the trial (1-40 d), there were no WBWG or FCR differences (p<0.05) among treatment groups. There were FCR differences (p<0.05) among treatments during the starter period (7 to 21 d), when the control group (0 mg/kg) presented the highest FCR. However, at 14 and 21 d, the FCR of the control group was not different (p>0.05) from those of groups 200, 400, and 1000mg of MOO/kg.

Table 3
Production efficiency of broilers supplemented with Mexican oregano essential oil.

Slaughter variables

The effects of MOO on slaughter variables are shown in Table 4. SW and HCY were affected (p<0.05) by MOO levels, with the highest SW in broilers given 400 mg/kg. Although, the 400 mg/kg treatment promoted the highest (p<0.05) comparative SW, its value was similar to those presented by broilers given MOO at 0, 200 and 600 mg/kg. The highest HCY values (p<0.05) were obtained in broilers given 0 and 200 mg/kg and the lowest (p<0.05) in broilers given 400 mg of MOO/kg. However, the HCY obtained with the 0 and 200 mg/kg treatments and the 400 mg/kg treatment were not statistically different (p>0.05) from the 600 to 1000 mg/kg treatments. CCY and BY values were not different (p>0.05) among treatments.

Table 4
Slaughter variables of broilers supplemented with Mexican oregano essential oil.

Breast meat physicochemical properties

Table 5 presents the effects of MOO on breast meat physicochemical properties. The pH values were different (p<0.05), with broilers given 0 mg/kg MOO having the highest (p<0.05) and those given 1000 mg/kg the lowest (p<0.05) values. WHC values were not different among treatments (p>0.05); however, there was an increasing trend to hold water as the level of MOO increased. Broilers fed 400 of MOO mg/kg had the highest (p<0.05) CL, while those fed 1000 mg/kg had the lowest (p<0.05) CL. However, CL was not different (p>0.05) among broilers given 0 to 800 mg of MOO /kg, and between broilers given 1000 mg/kg and the other treatments, with the exception of the 400 mg/kg treatment.

Table 5
Breast meat pH, water holding capacity and cooking loss in breast meat from broilers supplemented with Mexican oregano essential oil.

Broiler breast meat color parameters were affected (p<0.05) by dietary MOO concentrations (Table 6). Parameters L* and Hue angle were higher (p<0.05) in 1000 mg/kg breast meat samples than for the other concentrations, although L* values for 0 and 1000 mg/kg were not different (p>0.05). Otherwise, no single MOO concentration across b*, Chroma, ∆E, and BI color parameters demonstrated consistent statistically high or low values.

Table 6
Color parameters of breast meat from broilers supplemented with Mexican oregano essential oil.

Shear force and texture analysis

Breast meat SF and TPA from broilers supplemented with MOO are shown in Table 7. Values of SF, Adhes, Spring, Gum, and Chew did not present any differences (p>0.05) over the range of MOO concentrations in broiler feeds. However, there was a tendency for SF and adhesiveness values to decrease as the MOO concentration increased. In contrast, Hard, Cohes and Resilwere different (p<0.05) among treatments. Higher Hardvalues (p<0.05) were detected in the breast meat of broilers given 600, 800 and 1000 mg of MOO/kg, while the meat from the control treatment presented lower values (p<0.05), but not different from those obtained with 200 and 400 mg of MOO/kg. These results indicated that hardness improved with increasing MOO concentrations in broiler diets. Conversely, Cohes and Resil decreased (p<0.05) as MOO levels increased, to the extent that the values obtained in broilers fed 0 mg/kg were higher (p<0.05) than those at 1000 mg/kg.

Table 7
Shear force and texture analysis of breast meat from broilers supplemented with Mexican oregano essential oil.

Sensory attributes

The sensory attribute scores for odor (5.04 ± 0.18), taste (5.06 ± 0.21), tenderness (5.34 ± 0.23) and overall acceptability (5.34 ± 0.19) were not different (p>0.05) among treatments. However, numerically the consumers gave a higher overall score (5.23) for the breast meat of broilers supplemented with MOO than for those of the control group (5.04).

DISCUSSION

The null hypothesis (MOO treatment effects on breast meat quality are equal to the no-MOO control treatment) is based on the p-value according to a significance level determined ata = 0.05. Several studies have evaluated oregano essential oil supplementation at various levels (mg/kg) in feed: 300 (Alp et al., 2012Alp M, Midilli M, Kocabagli N, Yilmaz H, Turan N, Gargili A, et al. The effects of dietary oregano essential oil on live performance, carcass yield, serum immunoglobulin G level, and oocyst count in broilers. Journal of Applied Poultry Research2012;21(3):630-636.; Skoufos et al., 2016Skoufos I, Giannenas I, Tontis D, Bartzanas T, Kittas C, Panagakis P, et al. Effects of oregano essential oil and attapulgite on growth performance, intestinal microbiota and morphometry in broilers. South African Journal of Animal Science 2016;1(1):77-88.), 65 (Bozkurt et al., 2012Bozkurt M, Küçükyilmaz K, Ugur A, Özyildiz Z, Çinar M, Çabuk M, et al. Influences of an essential oil mixture supplementation to corn versus wheat-based practical diets on growth, organ size, intestinal morphology and immune response of male and female broilers. Italian Journal of Animal Science 2012;11(3):289-296.; Sun et al., 2015Sun Q, Liu D, Guo S, Chen Y, Guo Y. Effects of dietary essential oil and enzyme supplementation on growth performance and gut health of broilers challenged by Clostridium perfringens. Animal Feed Science and Technology 2015;207:234-244.), 125 (Hong et al., 2012Hong JC, Steiner T, Aufy A, Lien TF. Effects of supplemental essential oil on growth performance, lipid metabolites and immunity, intestinal characteristics, microbiota and carcass traits in broilers. Livestock Science2012;144(3):253-262.), 0, 60, 100 and 200 (Hashemipour et al., 2013Hashemipour H, Kermanshahi H, Golian A, Veldkamp T. Effect of thymol and carvacrol feed supplementation on performance, antioxidant enzyme activities, fatty acid composition, digestive enzyme activities, and immune response in broiler chickens. Poultry Science 2013;92(8):2059-2069.), 15-60 (Khattak et al., 2014Khattak F, Ronchi A, Castelli P, Sparks N. Effects of natural blend of essential oil on growth performance, blood biochemistry, cecal morphology, and carcass quality of broiler chickens. Poultry Science 2014;93(1):132-137.), 250 (Ghazi et al., 2015Ghazi S, Amjadian T, Norouzi S. Single and combined effects of vitamin C and oregano essential oil in diet, on growth performance, and blood parameters of broiler chicks reared under heat stress condition. International Journal of Biometeorology 2015;59(8):1019-1024.), 300 and 500 (Mohiti-Asli & Ghanaatparast-Rashti, 2015Mohiti-Asli M, Ghanaatparast-Rashti M. Dietary orégano essential oil alleviates experimentally induced coccidiosis in broilers. Preventive Veterinary Medicine 2015;120(2):195-202.), 400-1600 (Silva Vazquez et al., 2015Silva Vázquez R, Durán Meléndez LA, Santellano Estrada E, Rodríguez ME, Villalobos VG, Méndez-Zamora G, et al. Performance of broiler chickens supplemented with Mexican oregano oil (Lippiaberlandieri Schauer). Revista Brasileira de Zootecnia 2015;44(8):283-289.), 300 and 600 (Peng et al., 2016Peng QY, Li JD, Li Z, Duan ZY, Wu YP. Effects of dietary supplementation with oregano essential oil on growth performance, carcass traits and jejunal morphology in broiler chickens. Animal Feed Science and Technology 2016;214:148-153.) and 400 (Méndez-Zamora et al., 2017Méndez-Zamora G, Durán Meléndez LA, Hume ME, Silva-Vázquez R. Performance, blood parameters, and carcass yield of broiler chickens supplemented with Mexicano regano oil. Revista Brasileira de Zootecnia 2017;46(6):515-520.). These studies obtained significant effects with all the OEO levels evaluated in broilers regarding, for example, BW, FI and FCR.

Contrary to results in the current study, Skoufos et al. (2016Skoufos I, Giannenas I, Tontis D, Bartzanas T, Kittas C, Panagakis P, et al. Effects of oregano essential oil and attapulgite on growth performance, intestinal microbiota and morphometry in broilers. South African Journal of Animal Science 2016;1(1):77-88.) did not find any differences in BW of 28-d-old broilers fed0 or 15 mg oregano essential oil (OEO)/kg feed. Peng et al. (2016Peng QY, Li JD, Li Z, Duan ZY, Wu YP. Effects of dietary supplementation with oregano essential oil on growth performance, carcass traits and jejunal morphology in broiler chickens. Animal Feed Science and Technology 2016;214:148-153.) obtained higher BW in broilers fed 300 and 600 mg OEO /kg diet in the grower (1-21 d) and finisher (22-42 d) phases, which are similar to results observed in the current study with 200 to 1000 mg MOO/kg. Contrasting results were obtained by Sun et al. (2015Sun Q, Liu D, Guo S, Chen Y, Guo Y. Effects of dietary essential oil and enzyme supplementation on growth performance and gut health of broilers challenged by Clostridium perfringens. Animal Feed Science and Technology 2015;207:234-244.), who obtained lower BW and higher FI at 14 and 21 d in broilers fed 60 mg OEO /kg in broiler diets on BW and FI compared with results of the current study using MOO. Hence, similar to improvements with OEO, broiler performance can be improved with MOO from Lippiaberlandieri Schauer, which may translate into higher market value. Peng et al. (2016), using 600 mg/kg of supplement, did not find differences in FI at 1 to 21 d, while from 22 to 42 d and 1 to 42 d, the supplement promoted higher FI. In contrast, Hashemipour et al. (2016Hashemipour H, Khaksar V, Rubio LA, Veldkamp T, van Krimpen MM. Effect of feed supplementation with a thymol plus carvacrol mixture, in combination or not with an NSp-degrading enzyme, on productive and physiological parameters of broilers fed on wheat-based diets. Animal Feed Science and Technology 2016;211:117-131.) did observed any FI differences at 42 d in broilers fed 100 or 200 mg/kg of thymol+carvacrol, major components of OEO and MOO. The controversy represented by these results is whether treatment during the fattening period would result in higher production expenditures for growers, and therefore, much consideration is needed to determine the optimal OEO, including MOO, levels required to enhance broiler performance.

Few studies have reported and measured the effect on the water intake (WI) of broilers supplemented with OEO, and to a lesser degree with MOO. Differently from the results of the present study, Silva Vázquez et al. (2015Silva Vázquez R, Durán Meléndez LA, Santellano Estrada E, Rodríguez ME, Villalobos VG, Méndez-Zamora G, et al. Performance of broiler chickens supplemented with Mexican oregano oil (Lippiaberlandieri Schauer). Revista Brasileira de Zootecnia 2015;44(8):283-289.), evaluating two MOO levels in the starter and/or finisher broiler diets, did not obtainany WI differences in at overall period (0-39 d). These differences may be due to broilers’ physiological status, population density, room temperature, and feed intake (Manning et al., 2007Manning L, Chadd SA, Baines RN. Key health and welfare indicators for broiler production. World's Poultry Science Journal 2007;63(1):46-62.), as well as to the thymol and carvacrol levels in the MOO used as growth promoter (Silva Vázquez et al., 2015). Results from the current study again demonstrated that WI can be affected in broilers supplemented with dietary MOO.

Hashemipour et al. (2016Hashemipour H, Khaksar V, Rubio LA, Veldkamp T, van Krimpen MM. Effect of feed supplementation with a thymol plus carvacrol mixture, in combination or not with an NSp-degrading enzyme, on productive and physiological parameters of broilers fed on wheat-based diets. Animal Feed Science and Technology 2016;211:117-131.) found significantly higher average daily weight gain at 10, 24 and 42 d and throughout the experiment (0-42 d) when supplementing broiler diets with 100 and 200 mg of thymol + carvacrol /kg. Similarly, Mohiti-Asli & Ghanaatparast-Rashti (2015Mohiti-Asli M, Ghanaatparast-Rashti M. Dietary orégano essential oil alleviates experimentally induced coccidiosis in broilers. Preventive Veterinary Medicine 2015;120(2):195-202.) found higher weight gain at 28 din broilers supplemented with 300 and 500 mg of OEO/kg. These results are consistent with those in the current study with 200, 400 and 600 mg of MOO /kg. Ghazi et al. (2015Ghazi S, Amjadian T, Norouzi S. Single and combined effects of vitamin C and oregano essential oil in diet, on growth performance, and blood parameters of broiler chicks reared under heat stress condition. International Journal of Biometeorology 2015;59(8):1019-1024.), supplementing broilers with 250 mg of OEO/kg, obtained similar average daily weight gain and FCR throughout that trial (1-40 d) as those observed in the current study.

Slaughter variables results (p<0.05 for SW and HCY) of the current study do not agree with those of Alp et al. (2012Alp M, Midilli M, Kocabagli N, Yilmaz H, Turan N, Gargili A, et al. The effects of dietary oregano essential oil on live performance, carcass yield, serum immunoglobulin G level, and oocyst count in broilers. Journal of Applied Poultry Research2012;21(3):630-636.) and Kırkpınar et al. (2014), who fed broilers with up to 300 mg of OEO/kg and did not find any SW or carcass yield differences. In contrast, Méndez-Zamora et al. (2017Méndez-Zamora G, Durán Meléndez LA, Hume ME, Silva-Vázquez R. Performance, blood parameters, and carcass yield of broiler chickens supplemented with Mexicano regano oil. Revista Brasileira de Zootecnia 2017;46(6):515-520.), feeding broilers with 400 mg of OEO/kg, did not find SW or HCY differences, while Méndez-Zamora et al. (2015a) observe higher SW and HCY when using 400 and 800 mg of MOO/kg. According to these authors, increased levels of the active molecules carvacrol and thymol, as essential oil components, may have reduced offal weight. Khattak et al. (2014Khattak F, Ronchi A, Castelli P, Sparks N. Effects of natural blend of essential oil on growth performance, blood biochemistry, cecal morphology, and carcass quality of broiler chickens. Poultry Science 2014;93(1):132-137.) and Peng et al. (2016Peng QY, Li JD, Li Z, Duan ZY, Wu YP. Effects of dietary supplementation with oregano essential oil on growth performance, carcass traits and jejunal morphology in broiler chickens. Animal Feed Science and Technology 2016;214:148-153.) found higher CY and BY values with broiler diet supplementation of 0 to 500 g/t and 300 and 600 mg/kg of a natural blend of essential oils and OEO, respectively. The previous analyses and data from the current study revealed that the effects on CY and BY may be attributed to dietary essential oil concentrations, in addition to breed, sex and diet. In the current study, CCY and BY were not different among treatments, but CCY and BY were numerically higher when broilers were fed 0 and 200mg MOO/kg and 800 1000 mg MOO/kg, respectively, which may increase carcass market value.

Fletcher (2002Fletcher DL. Poultry meat quality. World's Poultry Science Journal 2002;58(2):131-145.) indicated that myoglobin content, its chemical state and pH contribute to broiler meat color. Broiler breast meat pH in the current study decreased with increasing MOO levels. Similar pH values in broiler breast meat were obtained by Kirkpinar et al. (2014Kirkpinar F, Ünlü HB, Serdaroglu M, Turp GY. Effects of dietary oregano and garlic essential oils on carcass characteristics, meat composition, colour, pH and sensory quality of broiler meat. British Poultry Science 2014;55(1):157-166.) and Méndez-Zamora et al. (2015bMéndez-Zamora G, García Macías JA, Santellano Estrada E, Durán Meléndez LA, Silva Vázquez R. Aceite de orégano sobre la calidad de pechuga de pollos de engorda. Investigación y Ciencia 2015b;23(65):5-12.), using 150 and 300 mg of Greek oregano and garlic essential oils/kg diet, and 1600 mg MOO/kg, respectively. The breast meat pH variation obtained in the current study could be explained according to Roofchaee et al. (2011Roofchaee A, Irani M, Ebrahimzadeh MA, Akbari MR. Effect of dietary oregano (Origanum vulgare L.) essential oil on growth performance, cecal microflra and serum antioxidant activity of broiler chickens. African Journal of Biotechnology 2011;10(32):6177-6183.), in which the high antioxidant activity of thymol, present in Greek and Mexican oregano essential oils, is due to the presence of phenolic OH groups, which act as hydrogen donors. Hence, increasing OEO or MOO dietary levels diets enhances the donation of OH groups, potentially lowering the pH value detected in breast meat. Méndez-Zamora et al. (2015b) indicated that the synergism between carvacrol and thymol in MOO could equilibrate the charge distributions in the breast meat.

Few studies have evaluated CL when supplementing essential oils in broiler diets. Park et al. (2014Park JH, Kang SN, Chu GM, Jin SK. Growth performance, blood cell profiles, and meat quality properties of broilers fed with Saposhnikovia divaricata, Lonicera japonica, and Chelidonium majus extracts. Livestock Science 2014;165:87-94.) did not find any influence of the inclusion of 0.2% (w/v) of three plant extracts in broiler diets on CL. In the current study, CL was significantly lower when broilers were fed 1000 mg MOO/kg diet relative to 400 mg MOO/kg.

Differences in L* and a* values when testing OEO and garlic essential oil were found by Kirkpinar et al. (2014Kirkpinar F, Ünlü HB, Serdaroglu M, Turp GY. Effects of dietary oregano and garlic essential oils on carcass characteristics, meat composition, colour, pH and sensory quality of broiler meat. British Poultry Science 2014;55(1):157-166.) obtained higher breast meat L* and a* values in broiler fed 150 mg garlic essential oil or OEO/kg and 300 mg of both EO/kg, respectively. However, these values are lower than those determined in the current study with MOO. The b* results of the current study were similar to those obtained by Young et al. (2003Young JF, Stagsted J, Jensen SK, Karlsson AH, Henckel P. Ascorbic acid, a-tocopherol, and oregano supplements reduce stress-induced deterioration of chicken meat quality. Poultry Science 2003;82(8):1343-1351.) with 3 % of Turkish oregano; however, Méndez-Zamora et al. (2015bMéndez-Zamora G, García Macías JA, Santellano Estrada E, Durán Meléndez LA, Silva Vázquez R. Aceite de orégano sobre la calidad de pechuga de pollos de engorda. Investigación y Ciencia 2015b;23(65):5-12.) found higher L* and b* values when feeding broilers with400, 800 and 1600 mg of MOO/kg. Those authors indicated that the increase in b* are likely due to high carotenoid content of MOO. This observation could explain the results obtained in the current study, because higher b* values were obtained at high MOO concentrations. Symeon et al. (2009Symeon GK, Zintilas C, Ayoutanti A, Bizelis JA, Deligeorgis SG. Effect of dietary oregano essential oil supplementation for an extensive fattening period on growth performance and breast meat quality of female medium-growing broilers. Canadian Journal of Animal Science 2009;89(3):331-334.) found significant statistical differences in a* and b* when 100 and 250 mg of OEO /kg were fed to broilers, and stated that these parameters may present inconsistent performance due to dosage or genetic effects. Few studies have reported data on ∆E and BI, variables that can help explain L*, a* and b* behavior in broiler breast meat as affected by OEO inclusion in the diet. The results of the current study indicate that the changes in color parameters may be attributed to the effects of 400 and 600 mg of MOO /kg on ∆E, and of 600 and 800 mg/kg on BI. Other authors (Hong et al., 2012Hong JC, Steiner T, Aufy A, Lien TF. Effects of supplemental essential oil on growth performance, lipid metabolites and immunity, intestinal characteristics, microbiota and carcass traits in broilers. Livestock Science2012;144(3):253-262.; Park et al., 2014Park JH, Kang SN, Chu GM, Jin SK. Growth performance, blood cell profiles, and meat quality properties of broilers fed with Saposhnikovia divaricata, Lonicera japonica, and Chelidonium majus extracts. Livestock Science 2014;165:87-94.), however, did not find any effect of broiler diet supplementation OEO on meat color parameters.

Meat texture is evaluated with textural profile analysis (TPA) and shear force (SF) as affected by myofibril structure. Recently, studies on the meat quality or carcass traits of broilers supplemented with plant extracts in diets have been carried out (Méndez-Zamora et al., 2015aMéndez-Zamora G, García-Macías JA, Durán-Meléndez LA, Herman-Lara E, Santellano-Estrada E, Silva-Vazquez R. Aceite esencial de orégano (LippiaberlandieriSchauer) en variables de calidad de la canal de pollo. Ecosistemas y Recursos Agropecuarios 2015a;2(4):41-51., 2015b; Hashemipour et al., 2016Hashemipour H, Khaksar V, Rubio LA, Veldkamp T, van Krimpen MM. Effect of feed supplementation with a thymol plus carvacrol mixture, in combination or not with an NSp-degrading enzyme, on productive and physiological parameters of broilers fed on wheat-based diets. Animal Feed Science and Technology 2016;211:117-131.; Mpofu et al., 2016Mpofu DA, Marume U, Mlambo V, Hugo A. The effects of Lippiajavanica dietary inclusion on growth performance, carcass characteristics and fatty acid profiles of broiler chickens. Animal Nutrition 2016;2(3):160-167.; Peng et al., 2016Peng QY, Li JD, Li Z, Duan ZY, Wu YP. Effects of dietary supplementation with oregano essential oil on growth performance, carcass traits and jejunal morphology in broiler chickens. Animal Feed Science and Technology 2016;214:148-153.; Sadeghi et al., 2016Sadeghi G, Karimi A, Shafeie F, Vaziry A ,Farhadi D. The effects of purslane (Portulaca oleracea L.) powder on growth performance, carcass characteristics, antioxidant status, and blood metabolites in broiler. Livestock Science 2016;184:35-40.; Soltani et al., 2016Soltani M, Tabeidian SA, Ghalamkari G, Adeljoo AH, Mohammadrezaei M, Saheb Fosoul SSA. Effect of dietary extract and dried areal parts of Rosmarinus officinalis on performance, immune responses and total serum antioxidant activity in broiler chicks. Asian Pacific Journal of Tropical Disease 2016;6(3):218-222.; Chowdhury et al., 2018Chowdhury S, Prasad Mandal G, Kumar Patra 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 2018;236: 86-97.), but with little attention have been given to TPA. Park et al. (2014Park JH, Kang SN, Chu GM, Jin SK. Growth performance, blood cell profiles, and meat quality properties of broilers fed with Saposhnikovia divaricata, Lonicera japonica, and Chelidonium majus extracts. Livestock Science 2014;165:87-94.) did not find effects on SF, Spring, Gum and Chew when evaluating 0.2% (w/v) of the inclusion of extracts of the plants Saposhnikoviadivaricata, Lonicera japonica and Chelidoniummajusin broiler diets. Compared with the current study, those authors found contrasting results for Adhes, but similar results for Hard, Cohes and Resil. Results obtained by Park et al. (2014) and data from the current study indicate that essential oil extracts in diets may influence texture properties of broiler meat. In the current study, 200, 400 and 600 mg/kg increased the Hard, Cohes and Resil qualities of broiler breast meat.

The main poultry meat quality attributes are appearance, texture, juiciness, flavor, and functionality (Fletcher, 2002Fletcher DL. Poultry meat quality. World's Poultry Science Journal 2002;58(2):131-145.). Contrary to the sensory results obtained in the breast meat of broilers fed MOO in the current study), Hong et al. (2012Hong JC, Steiner T, Aufy A, Lien TF. Effects of supplemental essential oil on growth performance, lipid metabolites and immunity, intestinal characteristics, microbiota and carcass traits in broilers. Livestock Science2012;144(3):253-262.) obtained lower tenderness and overall acceptability scores in broiler fed 125 mg of OEO/kg diet. In addition, those authors obtained lower (4.04-4.52) preference values compared with the current study, using a seven-point hedonic scale, indicating that the improved overall acceptability may be due to the antioxidant properties of polyphenols and flavonoids in OEO, which limit lipid and protein oxidation. Kirkpinar et al. (2014Kirkpinar F, Ünlü HB, Serdaroglu M, Turp GY. Effects of dietary oregano and garlic essential oils on carcass characteristics, meat composition, colour, pH and sensory quality of broiler meat. British Poultry Science 2014;55(1):157-166.) carried out a sensory evaluation with a trained panel of the breast meat from broilers supplemented with 300 mg of OEO and garlic/kg diet, where the panel detected significant statistical differences with slightly higher scores for oxidized flavor, juiciness, flavor and overall acceptability at 1, 15 and 30 d of broiler age. The authors stated that the essential oils in the diet may improve flavor and texture in breast meat. This observation may be reflected by the inclusion of 200 to 1000 mg of MOO/kg tested in the current study.

CONCLUSIONS

Mexican oregano essential oil from Lippiaberlandieri Schauer at 200 and 400 mg/kg diet as broiler dietary supplement improved body weight, feed and water intake, weekly body weight gain and feed conversion ratio at 7, 14 and 28 d. Furthermore, dietary Mexican oregano essential oil supplementation at 1000 mg/kg increased slaughter weight, hot carcass yield, and reduced breast meat pH and cooking loss. Mexican oregano oil influenced color parameters, hardness, cohesiveness and resilience, but did not have any adverse effects on the sensory evaluation.

ACKNOWLEDGEMENTS

This study was supported by the Programa para el Desarrollo Profesional Docente PRODEP (UANL-PTC-957) and Facultad de Agronomia, Universidad Autonoma de Nuevo Leon.

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Publication Dates

  • Publication in this collection
    09 May 2019
  • Date of issue
    Jan-Mar 2019

History

  • Received
    16 Apr 2018
  • Accepted
    12 Oct 2018
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