You are on page 1of 9

Livestock Science 207 (2018) 117–125

Contents lists available at ScienceDirect

Livestock Science
journal homepage: www.elsevier.com/locate/livsci

Effect of dietary supplementation with Pleurotus ostreatus on growth T


performance and meat quality of Japanese quail
R.D. Vargas-Sáncheza, G.R. Torrescano-Urrutiab, F.J. Ibarra-Ariasc, J.J. Portillo-Loeraa,

F.G. Ríos-Rincóna, A. Sánchez-Escalanteb,
a
Universidad Autónoma de Sinaloa (UAS), Facultad de Medicina Veterinaria y Zootecnia. Blvd., San Ángel s/n Predio Las Coloradas, Culiacán, Sinaloa 80236, México
b
Centro de Investigación en Alimentación y Desarrollo, A.C. (CIAD), Carretera a la Victoria Km 0.6, Hermosillo, Sonora 83000, México
c
Alta Tecnología Industrial para la Salud Animal, S.A. de C.V., Gabino Barreda 1290, Guadalajara, Jalisco 44430, México

A R T I C L E I N F O A B S T R A C T

Keywords: Pleurotus ostreatus is an edible mushroom that possesses antioxidant potential. The effect of dietary supple-
Pleurotus ostreatus mentation with Pleurotus ostreatus on performance, carcass, and meat quality attributes of Japanese quail was
Japanese quail investigated. The experiment involving a total of 288 quails 1-d-old, which were fed diets supplemented with P.
Meat quality ostreatus (0, 10 or 20 g/kg of diet) for 35 d, with feed and water for ad libitum consumption. Total polysaccharide
Feed additive
(TP), total phenolic and flavonoid content (TPC and TFC), antiradical DPPH• and ABTS•+ activity, as well as
polyphenols compositions of P. ostreatus extract were evaluated using high-performance liquid chromatography
(HPLC). The pH, color (L*, a* and b*), water holding capacity (WHC), cooking loss weight (CLW), texture and
oxidative stability (thiobarbituric acid reactive substances, TBARS; total phenolic content, TPC; antiradical
DPPH• and ABTS•+ activity) were measured in breast meat during storage (0, 5, 10 and 15 d; 4 °C without
illumination). Statistical differences were not detected on growth performance expressed as body weight gain
228.3 g, feed intake 467.9 g, feed conversion ratio 2.0, feed efficiency 0.49, live weight at the slaughter of the
birds 217.2 g, as well as carcass weight 133.0 g and yield 61.3 g of the quail breast (P > 0.05). At day 15 of meat
storage, the pH24 (9.0%), a* (14.7%), b* (9.3%), WHC (7.2%), TPC (40.0%), DPPH• (11.0%) and ABTS•+
(33.0%) values were increased in quails fed with P. ostreatus in comparison with the control group; while
parameter L* (9.0%), CLW (21.4%), texture (30.7%) and lipid oxidation-TBARS (33.5%) values were reduced
(P < 0.05), which could be associated with the presence of polysaccharide and phenolic constituents in this
edible mushroom. In conclusion, this edible mushroom has the potential for use in the feed of Japanese quail to
improve meat quality and to serve as an antioxidant that reduces lipid oxidation during storage.

1. Introduction of many essential nutrients for human health, including essential amino
acids (lysine, methionine, isoleucine, leucine, phenylalanine, threonine
The Japanese quail (Coturnix Coturnix japonica) is a small bird that and valine) as well as various monounsaturated (palmitoleic, C16:1;
has recently received greater attention in the poultry industry due to oleic acid, C18:1) and polyunsaturated fatty acids (linoleic acid, C18:2;
the increasing consumption of its meat and products (eggs, meatballs, and linolenic acid, C18:3), which are highly susceptible to oxidation
among others), mainly in European and Latin American countries. Also, processes (Genchev et al., 2008). Oxidative deterioration of poly-
the Japanese quail has become an important model animal for in- unsaturated fatty acid (PUFA) in muscles is one of the main causes of
vestigation due to its short life cycle and great resistance to many quality loss in any type of meat and leads to discoloration, nutrient and
poultry diseases (Ikhlas et al., 2011; Galíndez et al., 2010; Purohit et al., drip losses, the formation of toxic compounds and poor shelf life
2016). Although, for commercial purposes, its performance and meat (Falowo et al., 2014).
quality should be enhanced. The uncontrolled concentration and uses of synthetic antioxidants
The quail meat (breast and legs) is considered an important source such as butylated hydroxytoluene (BHT), butylated hydroxyanisole

Abbreviations: HPLC, high performance liquid chromatography; CP, crude protein; TPC, total phenolic content; DPPH•, 2,2-diphenyl-1-picrylhydrazyl; ABTS•+, 2,2′-azino-bis(3-
ethylbenzothiazoline-6-sulfonic acid); MDA, malondialdehyde; BW, body weight; FI, feed intake; FCR, feed conversion ratio; FE, feed efficiency; LWS, Live weight at slaughter; BHT,
butylated hydroxytoluene; BHA, butylated hydroxyanisole; TBHQ, tert-butylhydroxiquinone; PG, propyl gallate; SEM, standard error of the mean

Corresponding author.
E-mail address: armida-sanchez@ciad.mx (A. Sánchez-Escalante).

https://doi.org/10.1016/j.livsci.2017.11.015
Received 21 March 2017; Received in revised form 14 November 2017; Accepted 16 November 2017
1871-1413/ © 2017 Elsevier B.V. All rights reserved.
R.D. Vargas-Sánchez et al. Livestock Science 207 (2018) 117–125

(BHA), tert-butyl hydroquinone (TBHQ) and propyl gallate (PG) is a Table 1


widespread practice for preserving meat. However, the use of synthetic Composition of experimental diets containing dried mushroom powder (g/kg).
antioxidants has shown potential health risks (i.e. carcinogenesis),
Item Starter diet (1–21 d) Finisher diet (21–35 d)
promoting strict regulations for their controlled use in foods. In pre-
vious investigations, natural antioxidants are commonly added directly CONa P10 P20 CON P10 P20
to meat or animal feed as additives (Kahl and Kappus, 1993; Madhavi
Ingredients
and Salunkhe, 1996; Poljsak et al., 2013). For animal feed supplements,
Corn 298.7 288.7 278.7 439.6 429.5 420.9
for example, the dietary administration of oil extract from rosemary Soybean meal 658.0 658.0 658.0 515.0 515.4 514.2
and sage was shown to enhance the oxidative stability of lipids in Dried mushroom 0.0 10.0 20.0 0.0 10.0 20.0
chicken meat and to reduce microsomal and cholesterol oxidation Sodium chloride 3.5 3.5 3.5 3.5 3.5 3.5
(López-Bote et al., 1998). Lábaque et al. (2013) reported that dietary Methionine 3.4 3.4 3.4 4.0 4.0 4.0
Threonine 0.0 0.0 0.0 1.5 1.2 1.0
supplementation with thymol, an efficient radical scavenger, may help
Fine limestone 14.0 14.0 14.0 14.0 14.0 14.0
reduce fear responses of female birds when exposed to stressful situa- Orthophosphate 11.0 11.0 11.0 11.0 11.0 11.0
tions, without affecting birds’ locomotor activity. Vitamins premixb 3.0 3.0 3.0 3.0 3.0 3.0
Edible mushrooms are another natural source of bioactive com- Minerals 0.6 0.6 0.6 0.6 0.6 0.6
Probiotic 2.5 2.5 2.5 2.5 2.5 2.5
pounds such as polysaccharides, which improves the intestinal health of
Adsorbent 3.0 3.0 3.0 3.0 3.0 3.0
broiler chickens. This effect occurs by reducing the pathogenic and Phytase 2.1 2.1 2.1 2.1 2.1 2.1
increasing the beneficial intestinal microbiota (Guo et al., 2004; Enzyme 0.25 0.25 0.25 0.25 0.25 0.25
Giannenas et al., 2010b). Lee et al. (2012) reported that Pleurotus eryngii Total (g) 1000 1000 1000 1000 1000 1000
stalk residues potentially could be used as an antioxidant to decrease Chemical analysis
Dry matter 883.1 884.1 885.1 883.9 885.0 886.0
lipid peroxidation and improve meat quality in broilers. Moreover,
CP (N × 6.25) 281.8 282.2 282.5 240.3 240.9 240.9
Pleurotus ostreatus is an edible mushroom which is collected and culti- Ether extract 24.7 24.7 24.6 26.9 26.9 26.8
vated worldwide as they are valued sources of organic nutrients, such as Crude fiber 24.9 26.1 27.2 23.5 24.7 25.9
proteins, carbohydrates, fiber and certain vitamins in addition to mi- Calculated analysis
Lysine 19.9 19.9 19.9 15.9 16.0 16.0
nerals and compounds that exert biological properties (Wang et al.,
Methionine 5.6 5.6 5.7 5.6 5.7 5.8
2014). P. ostreatus is popularly known as the oyster mushroom. This Cysteine 3.8 3.8 3.9 3.2 3.3 3.3
common edible fungus is a primary decomposer of hardwoods in North Threonine 10.7 11.0 11.2 10.3 10.3 10.3
America and, traditionally, has been used to treat various human dis- Tryptophan 3.3 3.3 3.3 2.7 2.7 2.7
eases. Also, P. ostreatus has been demonstrated to possess biological Calcium 9.5 9.7 9.8 9.1 9.2 9.4
Phosphorus 3.8 3.8 3.8 3.6 3.6 3.6
properties, such as immunomodulatory, antimutagenic, anti-in-
Linoleic acid 12.8 12.7 12.7 13.5 13.4 13.4
flammatory, antilipidemic, hyperglycemic, antibacterial and antiradical ME, kcal/kg 3110.5 3104.6 3098.6 3142.0 3140.4 3134.7
function (Patel et al., 2012). Thus, given that mushrooms possess an- Antioxidant levels
tioxidant compounds, the aim of this study was to evaluate the effect of TPC, mg GAE/kgc 35.0c 55.4b 78.1a 13.8c 35.6b 51.6a
DPPH• (%)d 50.8c 70.7b 75.4a 25.6c 34.7b 37.3a
dietary supplementation with P. ostreatus on the growth performance
ABTS•+ (%)e 9.0c 10.2b 15.8a 5.0c 6.4b 7.1a
and meat quality of the Japanese quail.
a
CON, P10 and P20 represent groups of quails fed a basal diet supplemented with
powder-dried Pleurotus ostreatus mushroom at the levels of 0, 10 and 20 g/kg, respec-
2. Materials and methods tively.
b
Supplying per kilogram of diet: vitamin A, 3.75 mg; cholecalciferol, 112 µg; toco-
pherol acetate, 30 mg; sodium bisulfide menadione, 3 mg; vitamin B1, 1.5 mg; riboflavin,
2.1. Birds and experimental diets
6 mg; pyridoxine, 3 mg; cyanocobalamin, 15 µg; folic acid, 1.5 mg; niacin, 55 mg; cal-
cium phantothenate, 15 mg; vitamin B8, 180 µg; choline, 600 mg; Mn, 75 mg; Zn, 75 mg;
Two hundred and eighty-eight 1-d-old quail chicks were randomly Fe, 75 mg; Mo, 900 µg; Co, 750 µg; Se, 105 µg; Banox (BHT+BHA), 120 mg.
allocated to three experimental treatments. Each treatment consisted of c
TPC, total phenolic content.
d
eight replicates with 12 quails per pen. The pens (90 × 90 cm) were 2,2-Diphenyl-1-picrylhydrazyl radical.
e
placed in a conventional poultry house (9 × 9 m) with cement floor at 2,2´-azino-bis-(3-ethylbenzothiazoline-6-sulfonic acid radical. Different letters within
the same row indicate significant differences (P < 0.05).
60 cm from the ground, and the floor of the pens was raised 60 cm upon
the cement floor. During the first three days, a feed plate (25 ×
17.5 cm) and an automatic water supplier (500 mL) were placed in each 2.2. Chemical analysis
cage. From day four, a feed plate hopper-type and an automatic water
supplier (1000 mL) were placed. The temperature was set between 21 2.2.1. Edible mushroom composition
and 36 °C during the experimental period, and relative humidity varied Before formulating the diets, the main feed ingredients (i.e., corn,
between 23.4–53.8%, with a lighting program of 23 h/light per day. soybean meal and dried mushroom) were analyzed for proximate che-
During the first week (day 1–7), all birds were reared in the floor of the mical composition: dry matter (method 934.01), total protein content
pens using an absorbent paper towel and after the floor of the pen left by Kjedahl method (method 968.06), crude fat content was extracted
uncovered for the remainder of the study. Mortality was recorded daily, with petroleum ether in a Soxhlet apparatus (method 985.01), crude
and the diets were prepared following the nutritional requirements for fiber content (method 962.09) was analyzed in a Dosi Fiber apparatus,
fattening (N.R.C, 1994). The feeding program consisted of an ad libitum an ash was measured by incinerating dried samples at 550 °C and
starter diet (1–21 d) and a finisher diet (21−35), which are shown in moisture by oven drying (A.O.A.C, 2005). The metabolizable energy
Table 1. The diets were based on corn-soybean meal and Pleurotus os- values of ingredients were then calculated using N.R.C (1994) re-
treatus was supplemented at the expense of corn (10 and 20 g/kg). commended formula.
Quails were not vaccinated. The experiment was approved by the An- In addition to basic chemical composition, the feed ingredients were
imal Care and Use Committee of the Universidad Autónoma de Sinaloa, analyzed for amino acid and fatty acid composition according to
UAS and was conducted at the Poultry Unit of the Faculty of Veterinary Vázquez-Ortiz et al. (1995) and NMX-F-490– (1999)-NORMEX (1999),
Medicine of the same university, located in Culiacán, Sinaloa, Mexico respectively. Briefly, 5 g of mushroom were hydrolyzed with 800 µL of
(24° 46′ 13′’ N and 107° 21′ 14′’ W). HCl 6 M at 150 °C for 24 h. Hydrolyzed samples were neutralized with
NaOH 6 M, and amino acids were derived with an O-phthalaldehyde

118
R.D. Vargas-Sánchez et al. Livestock Science 207 (2018) 117–125

(OPA) solution before HPLC analysis. The chromatographic separation ethanolic: aqueous extract (100 µL, 100 μg/mL) was mixed with 100 µL
was carried out in an HPLC 1260 series using a Poroshell 120 EC-C18 (3 of DPPH• solution (300 μM, abs 1.0 nm) and incubated for 30 min in
× 100 mm, 2.7 µm; Agilent Inc., Palo Alto, CA, USA) column. A gra- darkness at room temperature. After, the absorbance was measured at
dient run was developed at a flow rate of 0.42 mL/min using Na2HP04 517 nm. The RSA was calculated using the following equation: %RSA =
10 mM, Na2B4O7 10 mM, NaN3 5 mM, pH 8.2 (solvent A) and acet- [(ADPPH – AS)/ADPPH] × 100, where AS is the absorbance of the solution
onitrile/methanol/DI (45:45:10, v/v) (solvent B). The gradient was 2% when the sample extract has been added at a particular level and ADPPH
B (0–0.35 min), 2–57% B (0.35–13.4 min), 100% B (13.5–15.7 min) is the absorbance of the DPPH• solution. After, the ABTS•+ radical ca-
and 2% B (15.7–16 min). Each peak was monitored using a diode array tion assay was evaluated mixing 10 µL of ethanolic: aqueous extract
detector set at 338 nm with a wavelength reference of 390 nm. (100 µg/mL) with 990 µL of ABTS•+ (absorbance of 0.8 nm), which is
Fatty acid composition was determined according to the method considered to be stable for free radicals derived from the reaction of
described by NMX-F-490– (1999)-NORMEX (1999). Fatty acid compo- 2,2′-azino-bis(3-ethylbenzothiazoline-6-sulfonic acid) with ammonium
sition of Pleurotus ostreatus was evaluated by fat extraction with persulfate. The samples were incubated for 30 min in darkness, and the
chloroform (CHCl3): methanol (MeOH) mixture 2:1 (Folch et al., 1957). absorbance was measured at 730 nm. The results were expressed as
The extract was centrifuged, the supernatant filtered, dried over an- inhibition percentages.
hydrous sodium sulfate, concentrated in a rotary evaporator under
vacuum, weighed and identified as the polar lipid extract. The lipid 2.2.4. Phenolic composition
extract was methylated with BF3-MeOH. After, fatty acid methyl esters An HPLC system (model 1100 series, Agilent Technologies,
(FAME) were analyzed with a gas chromatography chamber (Hewlett Waldbronn, Germany) with a UV–Vis detector, equipped with a re-
Packard Model 6890; Avondale, PA) equipped with a flame-ionization versed-phase C18 column (125 × 4.0 mm, 5 mm; Agilent Inc., Clara,
detector and capillary column 100 × 0.25 mm (SP-2560 Supelco Inc. Calif., U.S.A.) maintained at 30 °C, was used for analysis of phenolic
Bellefonte, PA) using He as a carrier gas 1.0 mL/min, in splitless mode. compounds (Hernández et al., 2007). The mobile phase consisted of
The injector and detector were maintained at 260 °C. The oven tem- water with formic acid (5%; solvent A) and methanol (abs, solvent B).
perature increased from 150 to 175 °C, at 2 °C/min for 60 min The gradient was 0% B (0 min), 30% (10–20 min), 40% (20–30 min),
(Pedneault et al., 2007). FAME internal standard (C11:0, Supelco Bel- 45% (30–50 min), 60% (50–52 min), 80% (52–65 min), 100%
lefonte, PA) was used to quantified FA composition, and FA identifi- (65–70 min) and 0% (70–71 min). The ethanolic: aqueous extract in-
cation was made by comparing the relative retention times of FAME jection volume was set to 10 µL at a flow rate of 1.0 mL/min. The UV-
peaks from samples with standards. detection wavelengths were 340 nm and 280 nm. The phenolic acids
used as standards were: caffeic acid phenethyl ester, p-coumaric, gallic,
2.2.2. Mushroom extract preparation and composition protocatechuic, and ferulic; as well as flavonoids compounds: acacetin,
The hydrophilic bioactive compounds of Pleurotus ostreatus (20 g) apigenin, chrysin galangin, kaempferol, luteolin, naringenin, pino-
were extracted by ultrasound (1 h at 30 °C) using 180 mL of ethanolic: banksin, pinocembrin, pinostrobin, and quercetin. The concentrations
aqueous (1:1). Then, the extracts were filtered through Whatman No. 1 used as standards ranged from 50 to 500 ppm. All standard curves
filter paper and concentrated under reduced pressure at 60 °C in a ro- showed high degrees of linearity (r2 > 0.99). Phenolic compounds were
tary evaporator (Yamato RE-301 BW). The extract was lyophilized in a identified by the retention times of each standard and were quantified
freeze dryer (Yamato DC401) and stored at − 20 °C under darkness by their peak areas related with those of standard curves.
until use (Soares et al., 2009). The yield of ethanol: water-soluble
polysaccharide extract was determined according to Guo et al. (2004). 2.3. Performance and carcass processing
The carbohydrate content was determined by the sulfuric acid-UV
method (Albalasmeh et al., 2013). An aliquot of 0.25 mL of ethanolic: At 14 and 35 d of age, the performance of the quail was determined
aqueous extract (5 mg/mL) and 0.125 mL of 5% aqueous solution of by measuring the body weight (BW) in each bird and the feed intake at
phenol were rapidly mixed with 0.625 mL of concentrated sulfuric acid the pen level (n = 8); the body weight gain and feed efficiency were
in a test tube for 30 s. Afterwards, the solution was cooled in ice for then calculated. At 35 d of age, quails were weighed (LWS, live weight
2 min and brought to room temperature. Finally, UV-light absorption at slaughter) underwent a fasting period of 3 h with water provided ad
was read at 315 nm using a spectrophotometer (Thermo Scientific, libitum. At the end of fasting, 32 male quails per treatment (four birds
Multiskan Go) and results were expressed as mg of glucose equivalent/g per replicate) were randomly selected for sampling and then weighed
extract. and euthanized by cervical dislocation for carcass processing according
The phenolic content was measured by the Folin-Ciocalteu (F-C) to the "Humane Killing of Wild and Domestic Animals" (Norma Oficial
method described by Mau et al. (2001). The ethanolic: aqueous extract Mexicana, 1995) and weighed to obtain the carcass weight and yield.
(10 µL, 5 mg/mL) was transferred into each well of a flat, 96-well mi- The carcasses were washed and sanitized in cold water (50 ppm hy-
croplate and diluted with 160 µL distilled water, 40 µL F-C reagent pochlorite), and they were pre-cooled in containers with crushed ice
(0.25 N) and 60 µL Na2CO3 solution (7%). The reaction mixture was (3 °C/30 min). The carcasses were then placed in plastic bags and
homogenized and incubated in darkness (at room temperature, 25 °C) stored at 4 °C for 24 h; after this period, each carcass was individually
for 1 h. The absorbance was measured at 750 nm and results expressed placed in a vacuum bag and frozen (−20 °C) until analysis. From each
as mg of gallic acid equivalent/g extract. Total flavonoid content was carcass, the breast (Pectoralis major) muscle was dissected, according to
measured based on the formation of aluminum chloride complexes the protocol described by Genchev and Mihaylov (2008), and six
(Popova et al., 2004). The extracts (10 µL, 5 mg/mL) were diluted with breasts from each treatment were placed on a styrofoam tray. The
130 µL of methanol, and 10 µL AlCl3 5% (w/v) were added. The mix- polystyrene trays with breasts were wrapped with polyvinyl chloride
ture was incubated for 30 min (25 °C), and the absorbance was read at film (17,400 cm3 O2/m2/24 h at 23 °C) and subjected to refrigerated
412 nm. The results were expressed as mg quercetin equivalent/g ex- storage at 4 °C without illumination for 0, 5, 10 and 15 d for subsequent
tract. analysis.

2.2.3. Antiradical assay 2.4. Meat quality measurements


The antiradical assays were carried out according to the method
described by Huang et al. (2011) and Carlsen et al. (2010), with slight The color of the surface of the breasts was assessed using a spec-
modifications. The radical-scavenging activity (RSA) was evaluated by trophotometer (model CM 508d, Konica Minolta Inc.), according to the
the DPPH• (2,2-diphenyl-1-picrylhydrazyl radical) method. The methodology of the Commission Internationale de l′Eclairage C.I.E

119
R.D. Vargas-Sánchez et al. Livestock Science 207 (2018) 117–125

(1978). The recorded values were luminosity (L∗), red index (a∗), high carbohydrates content (> 600.0 g/kg) and nitrogen-free extract
yellow index (b∗), chroma (C∗) and hue (h∗). The pH of breasts was (> 700.0 g/kg). The amount of insoluble a soluble fiber of P. ostreatus
measured according to the methodology described by Torrescano et al. was ~ 160.0 g/kg and ~ 18.0 g/kg, respectively. The yield of ex-
(2003). Samples were homogenized in distilled water (1:10), and pH tractable polysaccharide content (~ 340.0 g/kg) and sugar content (~
was determined using a potentiometer (Model pH211, Hanna Instru- 120.0 g/kg), as well as the total phenolic (~ 30.0 g/kg) and flavonoid
ments Inc., Woonsocket, R.I., U.S.A.) with automatic temperature (~ 25.0 g/kg), were determined and expressed based on the dry matter
compensation. The water holding capacity (WHC) of breasts was de- of the intact mushroom. Also, P. ostreatus contained some biological
termined according to the methodology described by Castellini et al. compounds such as essential and non-essential amino acids and es-
(2002), with slight modifications. Samples (1 g) were placed on a fine sential fatty acids, as well as secondary plant metabolites, including
mesh nylon, inserted into 50 mL tubes with a screw cap and then polysaccharides, phenolic acids, and flavonoid compounds. Moreover,
centrifuged at 1500 × g at 4 °C for 5 min. The water remaining after the results showed that P. ostreatus exert in vitro good antiradical DPPH•
centrifugation was quantified by drying the samples at 70 °C for 24 h. and ABTS•+ levels (> 50.0% and 15.0% of radical inhibition, respec-
The WHC (%) was then calculated using the following formula: WHC = tively). As shown in Table 1, the inclusion of P. ostreatus (10 and 20 g/
[(weight after centrifugation - weight after drying) / initial weight)] × kg) in the quail feed increased the total phenolic content (TPC) 55.2%
100. The cooking loss weight (CLW) was determined using the meth- and antiradical DPPH• and ABTS•+ levels of the diet (32.6% and 43.0%
odology described by Torrescano et al. (2003), with slight modifica- of radical inhibition, respectively) when compared with the basal diet.
tions. Frozen samples (Pectoralis profundus) were thawed at 4 °C over- The obtained values for growth performance such as body weight
night, and 1 cm3 of the breast was cut for determination of cooking loss gain (BWG), feed intake (FI), feed conversion ratio (FCR), feed effi-
weight. Afterwards, samples were cooked in a water bath at 85 °C for ciency (FE) and carcass characteristics (live weight at slaughter, LWS;
10 min to achieve a core temperature of approximately 71 °C in the carcass weight, CW; and yield) are shown in Table 3. Initial average
geometric center of the muscle (temperature was measured by a ther- bird weight in all groups was 14.6 g (P > 0.05), and the performance
mocouple). Then, the samples were cooled at room temperature and during 21 and 35 d of age were evaluated. The result showed no sig-
chilled another 12 h at 4 °C. The CLW (%) was calculated using the nificant effects (P > 0.05) on BWG (110.4 and 228.3 g, respectively), FI
following formula: CLW = [(initial weight - final weight)/initial (196.4 and 467.9 g), FCR (2.0 approximately), FE (0.5 approximately),
weight)] × 100. A texture instrumental analysis of breast samples was LWS (217.2 g), CW (133.0 g) and yield (61.4%). Also, no quail mor-
performed using the Volodkevich method described by Wakefield et al. tality was observed throughout the experiment.
(1989). The breasts were stored at 4 °C for 24 h, cooked in a water bath The proximate composition of quail meat (breasts) following sup-
at 71 °C (internal temperature) and then cut into strips (0.5 × 0.5 × plementation with P. ostreatus for 35 days is shown in Table 4. No
1.0 cm) perpendicular to the length of the muscle fiber. A knife was significant differences (P > 0.05) were observed in moisture 72.7%,
used to measure the maximum cutting effort (Kg-f). Lipid oxidation protein 22.2% and ash content 1.4%, among the treatments. The crude
(Lox) of breasts was measured by the TBARS method (Pfalzgraf et al., fat content of quail breasts significantly decreased 22.2% in birds
1995). Meat samples (5 g) were homogenized with 10 mL TCA (10%) supplemented with the edible mushroom when compared with the
for 1 min, centrifuged at 2300 × g for 10 min at 4 °C and filtered control group (P < 0.05).
through Whatman No. 1 filter paper. Subsequently, 2 mL of the filtered As shown in Table 5, the results of the meat quality parameters pH,
material was mixed with 2 mL TBA solution for 1 min in test tubes and color (L*, a*, b*), water holding capacity (WHC), cooking loss weight
then placed in a water bath at 97 °C for 20 min. After cooling, the ab- (CLW), texture (WBSF) and lipid oxidation (TBARS) showed that
sorbance was read at 531 nm. TBA values were expressed as mg mal- treatment x storage time effect was significant (P < 0.05). The treat-
ondialdehyde (MDA)/kg of meat. The antioxidants of meat samples ment vs. storage time effect on pH values were significant (P = 0.004).
(5 mg/mL), stored for 15 d, were extracted with ethanol and distilled The pH values of breasts at 24 h post-slaughter (pH24) ranged between
water and then by sonication at room temperature during 30 min. The 5.7 and 6.0 and gradually decreased over storage time for the CON
extracts were centrifuged at 2300 × g for 10 min, and the supernatant group. At day 15 of storage, there was a significant (P < 0.05) decrease
was used to assay the total phenolic content using the Folin-Ciocalteau in pH values (9.0% approximately) in the quail breasts from CON when
colorimetric method and the antiradical DPPH• and ABTS•+ methods compared with P10 and P20 treatments. The treatment x storage time
(Mau et al., 2001; Carlsen et al., 2010; Huang et al., 2011). effect on L* (lightness), a* (redness) and b* (yellowness) values were
significant (P < 0.001). The average values for L*, a* and b* of breasts
2.5. Statistical analysis at 24 h post-mortem storage were 46.1, 10.9 and 8.3, respectively. At
day 15 of storage, L* and b* values were significantly increased
The data were analyzed using NCSS statistical package v2007 (P < 0.05) for the CON group over storage time by 8.5% and 37.3%,
(Kavyille, Utah, USA). The results of quail performance and carcass respectively; while a* value was significantly decreased by 23.0% in
characteristics were analyzed by a completely randomized design, with comparison with the P. ostreatus treatments. Also, the treatment x sto-
three treatments and eight replicates of 12 birds each, respectively. rage time effect on WHC (P = 0.045), CLW (P = 0.049) and texture (P
Data on meat quality were subjected to two-way ANOVA including the = 0.038) values were significant. The results showed that thought
main effects of dietary treatment (three levels) and storage time (four storage time the WHC values were significantly increased in quail
levels) as well as interactions between two factors. The homogeneity of breast supplemented with P. ostreatus treatments (7.2%, respectively);
variance was tested by Bartlett´s and Tukey´s tests and was carried out while CLW and texture values were reduced for the same samples by
to assess any significant differences at the probability level of P < 0.05 21.4% and 30.7%, respectively, when compared with CON group. In
among the experimental treatments. addition, the treatment x storage time effect on TBA values were sig-
nificant (P < 0.001). The initial TBA values remained below 0.1 mg
3. Results malondialdehyde (MDA)/kg of meat for all treatments and these values
were significantly increased for the CON group by 83.6% (> 0.5 mg
The dried Pleurotus ostreatus powder used in the present study was MDA/kg). At day 15 of storage, the dietary P. ostreatus supplement
donated by ATISA (Alta Tecnología en Investigación para la Salud group displayed reduced MDA formation by 68% (< 0.2 mg MDA/kg)
Animal). As shown in Table 2, the results of chemical analyses showed in breast meat when compared with the CON group at day 15.
that this edible mushroom possess low moisture (< 15.0 g/kg), ether No detectable treatment x storage effects were observed on TPC (P
extract (< 35.0 g/kg), and ash content (~ 50.0 g/kg); as well as a key = 0.110), DPPH• (P = 0.960) and ABTS•+ (P = 0.920) values of breast
source of crude protein (~ 100.0 g/kg), crude fiber (~ 130.0 g/kg), meat extracts obtained with ethanol as solvent (data are not shown);

120
R.D. Vargas-Sánchez et al. Livestock Science 207 (2018) 117–125

Table 2
Chemical composition of Pleurotus ostreatus powder and extracta.

Dried powder composition (n = 6)

Chemical analysis Amino acid composition

Dry matter, g/kg 870.0 Aspartic acid, g/kg 6.95 Leucine, g/kg 1.53
Total protein (N × 6.25), g/kg 123.0 Arginine, g/kg 4.96 Lysine, g/kg 3.98
Ether extract, g/kg 33.4 Alanine, g/kg 2.25 Methionine, g/kg 7.92
Crude fiber, g/kg 134.7 Glutamic acid, g/kg 12.62 Phenylalanine, g/kg 10.31
Ash, g/kg 52.0 Glycine, g/kg 1.33 Serine, g/kg 9.06
Carbohydrates, g/kg 643.7 Histidine, g/kg 7.79 Threonine, g/kg 24.84
Nitrogen-free extract, g/kg 766.9 Isoleucine, g/kg 22.99 Valine, g/kg 0.25
Phosphorus, g/kg 4.1 Fatty acid composition
Calcium, g/kg 14.0 16:00 (%) 5.0 18:3n−3 (%) 12.6
Insoluble dietary fiber, g/kg 166.0 18:00 (%) 0.6 MUFA 12.2
Soluble dietary fiber, g/kg 17.8 18:1n−9 (%) 10.5 PUFA 14.5
18:2n−6 (%) 12.6 SFA 6.8
Dried extract composition (n = 6)
Chemical analysis Phenolic composition
Yield of polysaccharide, g/kg 342.0 Compound Rt (min) g/kg
Total sugar content, g GE/kg 128.3 Gallic acid 1.9 23.3
Total phenolic content, g GAE/kg 34.2 Protocatechuic acid 2.7 2.6
Total flavonoid content, g QE/kg 26.3 Cinnamic acid 3.4 (-)
p-coumaric acid 7.8 (-)
Ferulic acid 8.7 (-)
Antioxidant levels Naringenin 27.3 (-)
DPPH• (%) 59.5 Quercetin 30.8 (-)
ABTS•+ (%) 16.0 Luteolin 36.4 (-)
Kaempferol 37.2 (-)
Apigenin 40.6 (-)
Pinocembrin 44.5 (-)
Pinobanksin 45.8 (-)
CAPE 49.0 (-)
Chrysin 47.9 0.7
Galangin 52.4 (-)
Acacetin 57.0 (-)
Pinostrobin 62.9 (-)

a
Dried powder values are reported in dried matter basis, while phenolic composition values are expressed in dried matter basis of the ethanolic: aqueous extract; MUFA, mono-
unsatured fatty acids; PUFA, polyunsaturated fatty acids; SFA, saturated fatty acids. 16:00, palmitic acid; 18:00, stearic acid; 18:1n-9, oleic acid; 18:2n-6, linoleic acid; 18:3n-3, linoleic
acid.

Table 3 Table 4
Effect of P. ostreatus supplementation on the growth performance and carcass char- Effect of P. ostreatus supplementation on proximate composition of quail breast meata.
acteristics of Japanese quail at 35 days of agea.
Item Treatments
Item CONb P10 P20 SEMc P-value
CONb P10 P20 SEMc P-value
Initial weight (g) 14.52 14.54 14.54 0.326 0.999
7–14 d 110.30 110.27 110.51 1.186 0.988 Moisture 72.6 73.10 72.32 0.353 0.316
BW gain (g) 95.78 95.74 95.97 1.254 0.990 Protein 22.07 22.43 22.17 0.137 0.180
FI (g) 194.28 183.45 201.45 8.471 0.330 Fat 1.84a 1.38b 1.42b 0.034 < 0.001
FCR 2.04 1.92 2.10 0.093 0.368 Ash 1.40 1.54 1.39 0.054 0.121
FE 0.51 0.48 0.52 0.002 0.467
a
14–35 d 244.88 241.93 241.74 3.653 0.794 Results are given as means of groups (n = 6) and expressed as a percent (%).
BW gain (g) 230.35 227.40 227.20 3.711 0.800 b
CON, P10 and P20 represent groups of quails fed a basal diet supplemented with
FI (g) 476.08 467.17 460.27 14.122 0.733 powder-dried Pleurotus ostreatus mushroom at the levels of 0, 10 and 20 g/kg, respec-
FCR 2.07 2.05 2.02 0.005 0.932 tively.
FE 0.49 0.49 0.50 0.001 0.829 c
SEM, standard error of the mean. Different letters within the same row indicate
LWS (g)d 217.80 221.28 212.40 3.545 0.207 significant differences (P < 0.05).
CW (g)e 131.60 136.87 130.56 2.192 0.100
Yield (%) 60.45 62.07 61.46 0.738 0.281
ABTS•+ (P = 0.002) were significant (P < 0.05). At day 15 of storage,
BW, body weight; FI, feed intake; FCR, feed conversion ratio; FE, feed efficiency. the values of TPC, DPPH• and ABTS•+ were lower in the CON group
a
Results are given as means per group (n = 8). (40.0%, 11.0% and 33.0%, respectively, at day 15) when compared
b
CON, P10 and P20 represent groups of quails fed a basal diet supplemented with with breasts of birds supplemented with P. ostreatus (P < 0.05).
powder-dried Pleurotus ostreatus mushroom at the levels of 0, 10 and 20 g/kg, respec-
tively.
c
SEM, standard error of the mean. 4. Discussion
d
LWS, live weight at slaughter.
e
Carcass weight.
The results presented in this study showed that P. ostreatus possess
nutritional components such as carbohydrates, protein, fat, fiber (in-
the average values for these antioxidant parameters were 2.4 mg GAE/g soluble and soluble) and minerals (phosphorus and calcium), as well as
of meat, 53.0% and 25.6% of radical inhibition, respectively. sugars, essential amino acids (histidine, isoleucine, leucine, lysine,
Meanwhile, for the aqueous meat extracts (Table 6), the treatment x methionine, phenylalanine, threonine, and valine) and fatty acids (li-
storage time effect on TPC (P = 0.036), DPPH• (P < 0.001), and noleic and linolenic acid). Besides, some compounds such as

121
R.D. Vargas-Sánchez et al. Livestock Science 207 (2018) 117–125

Table 5
Effect of storage time and P. ostreatus supplementation on meat quality of Japanese quaila.

ITEM Treatmentb Storage time (Days) P-level

0 5 10 15 Trat Time Trat*Time

L* CON 47.60aB 45.30bB 48.20aB 52.00aA 0.011 0.013 < 0.001


P10 46.03bA 47.38aA 46.59bA 47.90bA
P20 44.71cA 45.80bA 44.78cA 47.40bA
a* CON 10.76aA 10.00bA 9.11bB 8.29bB < 0.001 < 0.001 < 0.001
P10 11.32aA 10.01bB 10.20aB 10.10aB
P20 10.56bA 11.03aA 10.40aA 10.94aA
b* CON 9.60aC 9.40bC 13.80aB 15.32aA < 0.001 < 0.001 < 0.001
P10 8.21bD 9.77bC 11.20bB 13.50bA
P20 7.13cC 11.90aB 10.62bB 13.40bA
pH CON 5.80aB 5.80aB 5.80cB 5.61bA < 0.001 < 0.001 0.004
P10 5.80aC 5.92aB 6.00aA 6.10aA
P20 5.80aC 5.91bB 5.90bB 6.21aA
WHC (%)c CON 62.68aA 61.16bB 60.09bB 57.80bC 0.017 0.023 0.045
P10 62.38aA 62.03aA 62.84aA 62.70aA
P20 62.26aA 62.20aA 62.27aA 61.80aA
CLW (%)d CON 11.42aB 11.42aB 14.18aA 14.10aA 0.003 0.050 0.049
P10 11.73aB 10.50cA 10.11bA 10.53bA
P20 11.92aB 10.91bB 10.20bA 10.10bA
Texture (Kg–f) CON 0.88bB 1.00aA 0.91aA 1.30aA 0.037 0.048 0.038
P10 1.00aA 1.05aA 1.10aA 0.92bB
P20 1.00aA 1.09aA 0.98aA 0.90bB
TBARSe CON 0.07aC 0.10aB 0.41aA 0.60aA < 0.001 < 0.001 < 0.001
P10 0.02bC 0.04bB 0.20bA 0.20bA
P20 0.02bB 0.03bB 0.21bA 0.20bA

Different letters (a–c) within the same column indicate significant differences (P < 0.05).
Different letters (A–C) within the same row indicate significant differences (P < 0.05).
a
Results are given as means of groups (n = 6).
b
CON, P10 and P20 represent groups of quails fed a basal diet supplemented with powder-dried Pleurotus ostreatus mushroom at the levels of 0, 10 and 20 g/kg, respectively.
c
Water holding capacity.
d
Cooking loss weight.
e
Thiobarbituric acid reactive substances (mg MDA/kg meat).

Table 6
Effect of storage time and P. ostreatus supplementation on meat oxidative stability of Japanese quaila.

ITEM Treatmentb Storage time (days) P-level

0 5 10 15 Trat Time Trat*Time

c bA bB bB bC
TPC CON 5.8 4.3 4.2 2.5 < 0.001 < 0.001 0.036
P10 6.6aA 4.6aB 4.8aB 4.1aC
P20 6.5aA 4.7aB 4.8aB 3.9aC
DPPH• (%)d CON 60.4bA 60.7aA 59.0aA 56.6bB < 0.001 < 0.001 < 0.001
P10 63.6aA 60.2aB 59.8aB 58.8aC
P20 62.4aA 60.3aB 58.9bC 58.1aC
ABTS•+ (%)d CON 41.0aA 30.5bB 32.4bB 31.7bB < 0.001 < 0.001 0.002
P10 43.6aA 41.2aB 42.4aB 40.0aB
P20 40.3aA 39.7aA 41.6aA 41.1aA

Different letters (a-b) within the same column indicate significant differences (P < 0.05).
Different letters (A-B) within the same row indicate significant differences (P < 0.05).
a
Results are given as means of groups (n= 6).
b
CON, P10 and P20 represent groups of quails fed a basal diet supplemented with powder-dried Pleurotus ostreatus mushroom at the levels of 0, 10 and 20 g/kg, respectively.
c
Total phenolic content (mg eq. gallic acid/g).
d
Expressed as percentage inhibition of the respective radical.

polysaccharides and phenolic constituents (gallic acid, protocatechuic information is available regarding the influence of dietary supple-
acid, and chrysin) which are associated with the biological properties of mentation with P. ostreatus powder for Japanese quail. So, the present
the edible mushroom were identified. This chemical profile is com- study was designed to evaluate the potential application of P. ostreatus
parable to those reported in other studies (Chirinang and Intarapichet, (0, 10 and 20 g/kg of diet) in the diet of Japanese quail, as this
2009; Lee et al., 2012). The composition and biological properties of mushroom is rich in polysaccharide and phenolic compounds, P. os-
these elements vary within and among mushrooms species, and the treatus can be employed as a functional ingredient with potential to
maturity of the fruiting body can also play a role (Chirinang and improve performance, meat quality and antioxidant stability.
Intarapichet, 2009; Roupas et al., 2012). Environmental factors and The results obtained in this study showed that P. ostreatus supple-
cultivation method can also have an impact on the abundance of spe- mentation no increase body weight gain (average 239.0 g) and feed
cific compounds in edible mushrooms, which may then be added to the intake (average 468.0 g) values for Japanese quail among the treat-
diets of animals to enhance their oxidative status and reduce oxidative ments (CON, P10 and P20) and periods (14 and 35 d of age).
reactions (Guillén-Navarro et al., 1998; Lee et al., 2012). However, no Meanwhile, the values for the carcass characteristics LWS, CW and

122
R.D. Vargas-Sánchez et al. Livestock Science 207 (2018) 117–125

Yield were not significant (P > 0.05). In agreement with our in- of pH from 5.8 to 6.3. Those values may be used as a reference for quail
vestigation, it has been reported an adverse effect on quail performance breasts, and may result from good animal welfare conditions, which
when some oil´s extract from Mentha spicata was supplemented in quail may reduce pre-slaughter stress and thus glycogen consumption
feed (Ghazaghi et al., 2014). In another work, Giannenas et al. (2010a) (Castellini et al., 2002). In this case, pH values are related to glycogen
reported that body weight, weight gain, feed intake and feed conversion content in muscle, and glycogen stores are strongly influenced by lo-
ratio values were not affected by Agaricus bisporus inclusion at 10 and comotor activity and the presence of stress factors in the pre-slaughter
20 g/kg. Previous studies have shown that inclusion of natural sources process. After slaughter, the pH values of muscle immediately were
of antioxidants such as Pleurotus eryngii in the diet conferred growth reduced during the post-mortem period, and the rate of pH decline often
performance (i.e. body weight gain and feed efficiency) in broiler affects meat quality parameters (Genchev and Mihaylov, 2008).
chickens (Lee et al., 2012). In some studies where a positive effect has Meanwhile, high breast pH produces conditions that create a dark-co-
been found on growth performance of chickens, results indicate that the lored appearance associated with water retention, due to an increase in
action of growth factors is mediated by an antibacterial effect (Guo muscle fiber density and compaction (Barbut et al., 2005).
et al., 2004). These results suggest that edible mushroom species and In poultry meat, color is an important quality attribute that influ-
chemical composition could play a specific role in growth performance ences consumer acceptance since consumers often reject products with
of birds (Lee et al., 2012). a color that varies from the expected, typical appearance (Qiao et al.,
The results obtained for the proximate composition of quail breast 2001). In our study L*, a* and b* color values were found by Allen et al.
meat showed higher protein (~ 20.0%) and moisture content (~ (1998) and Genchev et al. (2008) studies, who associated dark meat
70.0%) and lower fat content (~ 1.5%). The protein content in quail breast to values of L* < 50.0, a* > 4.5 and b* < 10.0. In the last day of
breast is higher than the reported value for chicken breast 16.5% (Du sampling, an increase in L* and b* values were observed for the CON
and Ahn, 2002), which indicate that quail meat, like most poultry, is a group when compared with P. ostreatus treatments. Those color changes
valuable source of protein. Our results showed that fat content was can be associated with a decrease in a* value (red index) and pH values
23.9% higher in birds from the CON group, compared with the birds (Debut et al., 2003). The lowest L* (47.6) and b* (13.5) values, as well
supplemented with P. ostreatus, which could be associated with the as the highest a* (> 10.0) values were obtained in quails supplemented
antioxidant components of the edible mushroom, i.e. polysaccharides with P. ostreatus treatment, which confirm the efficacy of this edible
and phenolic compounds. In agreement with this, Dong et al. (2007) mushroom against color changes of meat.
reported that supplementation of 0.06% of alfalfa extract (characterized Moreover, water loss is of great commercial importance, as it can
by having 18.6% polysaccharides, 5.6% triterpenoid saponins and 5.9% generate economic losses when theses exceed 10.0% (Allen et al.,
flavonoids) in broiler chickens diets during six weeks, decreased 35.3% 1998). The results of the current investigation indicate that at day 15,
the abdominal fat deposition. Also, Lee et al. (2012) reported that the the dietary mushroom supplementation led to decreased water loss
crude fat content was significantly decreased in the breast (15.1%) and after cooking (8.0%) and reduced the texture (10.0%) and increased the
thigh (19.4%) of broiler chickens supplemented with 0.5%, 1.0% and WHC (7.1%) in comparison with the breasts of the CON group. In
2.0% of Pleurotus eryngii stalk residue rich in antioxidant components, agreement with our work, Mehdipour et al. (2013) reported a sig-
i.e. polysaccharides and phenolic compounds. While Kamboh et al. nificant increase in the WHC (5.0%) in quail breast meat of birds sup-
(2017) reported that supplementation with 5 mg of soy (genistein) and plemented with cinnamon oil (200 mg/kg) as a natural antioxidant.
20 mg citrus flavonoids (hesperidin) of broiler diets during 42 days, However, no significant differences were observed in the water loss
significantly decreased the fat content of breast meat (2.7% and 12.4%, parameter. In a previous study, Debut et al. (2003) reported that water
respectively). These results were associated with the components of the loss and WHC of raw chicken meat was significantly higher for the birds
natural extract, mainly polysaccharides, and phenolic compounds. It with high initial rates of pH decline. These unfavorable pH values are
has been reported that supplementation of low-density chitosan (50 g/ associated with negative environmental factors and may lead to pale,
kg) in the chicken diet for 3 weeks, reduce the fat content of chickens by soft, and exudative conditions. After slaughter, a fast development of
inhibiting the absorption of dietary fat in the small intestine via the rigor mortis is known to affect the structure of myofibrils. The oxidation
suppression of lipase activity due a reduction in the levels of bile acids of myofibrils involves the loss of essential amino acids and the gen-
(Kobayashi et al., 2002). The supplementation of 25 mg/kg of oligo- eration of oxidation products, such as cross-links (disulfide bonds and
saccharides in the diet of animal models (rats) reduces fat deposition by di-tyrosines), amino acid-oxidized derivatives, and protein carbonyls.
reducing lipid uptake via the suppression of the enzyme activity of Those chemical changes lead to shrinkage of contractile fibers and
pancreatic lipase (Kang et al., 2012). Also, Biswas and Wakita (2001) weaker bonds with protein muscles and thereby reducing the water-
reported that 0.5% of polyphenols supplemented in the broiler chickens binding ability of breasts (i.e., leading to an increase in liquid outflow
diets reduce abdominal fat traits by inhibiting hepatic lipogenesis. and loss of soluble nutrients) and increasing light scattering and hard-
Also, Genchev et al. (2008) reported that the fat content of quail ness of the meat (Dransfield and Sosnicki, 1999; Warris, 2001). The
breast is 2.5% which is a high value in comparison with our study. Also, results obtained in our investigation could be attributed to the presence
this work indicate that high proportions of fat content subsequent in- of phenolic compounds since they been reported to reduce protein
creased lipid oxidation, which conferring many negative characteristics oxidation by radical-scavenging and metal-chelating mechanism
on the physicochemical, sensory and technological properties of meat. (Estévez et al., 2008), which led to reduce water loss and increase WHC
So, the meat industry uses additive of synthetic origin to reduce this (Mehdipour et al., 2013).
oxidative process. However, the uncontrolled use of synthetic anti- Malondialdehyde (MDA) is a biomarker commonly used to measure
oxidants has shown potential health risks such as cancer (Kahl and the level of lipid oxidation (Lox) in poultry meat through the reaction
Kappus, 1993; Poljsak et al., 2013). Several natural products are po- with thiobarbituric acid-TBA: TBA + MDA → TBA-MDA adduct (Salih
tential alternatives to synthetic antioxidants and have begun to receive et al., 1987). The lipid oxidation levels were increased for all treatments
considerable attention in the food industry, as they may extend the trough storage time and indicated that MDA formation occurred from
shelf-life of foods, improve food quality and be directly incorporated the day 0 (< 0.1 mg MDA/kg). At day 15 of storage, the lowest MDA
into the food matrix or through diet (Shahidi and Zhong, 2010; Lábaque values were obtained in P. ostreatus treatments when compared with
et al., 2013). CON group. These results can be associated with the presence of
In this study, pH values of breasts at 24 h post-slaughter (pH24) polysaccharide and phenolic compounds found in P. ostreatus powder,
ranged between 5.7 and 6.0 and gradually decreased over storage time which can act as inhibitors of aldehydic Lox products, especially MDA,
for the CON group. Similar pH values were found by others authors that are transferred to and/or accumulated in meat (Patel et al., 2012;
(Genchev et al., 2008; Mehdipour et al., 2013), reporting normal values Lin et al., 2004). Also, the high MDA formation founded in CON

123
R.D. Vargas-Sánchez et al. Livestock Science 207 (2018) 117–125

samples could be associated with a high-fat deposition in the muscle of meat on microstructure, extractable proteins, and cooking of marinated fillets. Poult.
the birds (Kamboh et al., 2017). In agreement with the latter, Sci. 84, 797–802.
Biswas, A.H., Wakita, M., 2001. Effect of dietary Japanese green tea powder supple-
Mehdipour et al. (2013) reported a decrease in MDA formation from mentation on feed utilization and carcass profiles in broilers. J. Poult. Sci. 38 (1),
quail meat by an average of 26.9% when cinnamon oil was supple- 50–57.
mented in the diet. In a previous work, Giannenas et al. (2010a) re- Carlsen, M.H., Halvorsen, B.L., Holte, K., Bøhn, S.K., Dragland, S., Sampson, L., Willey, C.,
Senoo, H., Umezono, Y., Sanada, C., Barikmo, I., Berhe, N., Willet, W.C., Phillips,
ported that dietary supplementation of the mushroom A. bisporus at K.M., Jacobs Jr, D.R., Barikmo, I., 2010. The total antioxidant content of more than
both inclusion levels of the study (20 > 10 g/kg) reduced MDA pro- 3100 foods, beverages, spices, herbs and supplements used worldwide. Nutr. J. 9, 1.
duction in breast tissue (by approximately 33.3%). Additionally, Lee Castellini, C., Mugnai, C., Dal Bosco, A., 2002. Effect of organic production system on
broiler carcass and meat quality. Meat Sci. 60, 219–225.
et al. (2012) reported that MDA production slightly decreased (33.5%) Chirinang, P., Intarapichet, K.O., 2009. Amino acids and antioxidant properties of the
in broiler chickens supplemented with Pleurotus eryngii stalk residue oyster mushrooms, Pleurotus ostreatus and Pleurotus sajor-caju. Sci. Asia. 35, 326–331.
(mainly at 20 g/kg) compared with their basal diet. C.I.E, 1978. Recommendations of uniform color spaces-color difference equations psy-
chometric color terms. Supplement No. 2 to CIE Publication No. 15 (E-1.3.1) 1971/
Other methods used to evaluate the antioxidant stability of meat
(TC-1.3). Commision International de I´Eclairage, Paris.
extracts (ethanolic and aqueous) are the total phenolic (TPC) and an- Debut, M., Berri, C., Baeza, E., Sellier, N., Arnould, C., Guemene, D., Jehl, N., Boutten, B.,
tiradical DPPH• and ABTS•+ activity. The obtained results at the current Jego, Y., Beaumont, C., Le Bihan-Duval, E., 2003. Variation of chicken technological
investigation revealed that on last day of sampling the presence of meat quality in relation to genotype and preslaughter stress conditions. Poult. Sci. 82,
1829–1838.
phenolic constituents was > 35.9% and antiradical DPPH• > 3.7% and Dong, X.F., Gao, W.W., Tong, J.M., Jia, H.Q., Sa, R.N., Zhang, Q., 2007. Effect of poly-
ABTS•+ > 26.3% for quail breast of birds supplemented with P. os- savone (alfalfa extract) on abdominal fat deposition and immunity in broiler
treatus. A previous study indicated that free radical scavengers, such as chickens. Poult. Sci. 86 (9), 1955–1959.
Dransfield, E., Sosnicki, A.A., 1999. Relationship between muscle growth and poultry
phenolic compounds (Ar-OH), could inhibit the Lox cycle. The proposed meat quality. Poult. Sci. 78 (5), 743–746.
mechanism of oxidative reactions between an unsaturated fatty acid Du, M., Ahn, D.U., 2002. Effect of dietary conjugated linoleic acid on the growth rate of
(RH) and phenolic compounds (Ar-OH): RH → R• (free radical) + O2 → live birds and on the abdominal fat content and quality of broiler meat. Poult. Sci. 81
(3), 428–433.
ROO• + Ar-OH (antioxidant) → ROOH + Ar-O• (oxidized antioxidant) Estévez, M., Kylli, P., Puolanne, E., Kivikari, R., Heinonen, M., 2008. Oxidation of skeletal
(Falowo et al., 2014). This finding suggests that dietary mushrooms muscle myofibrillar proteins in oil-in-water emulsions: interaction with lipids and
exerted an antioxidant effect on breast meat. effect of selected phenolic compounds. J. Agric. Food Chem. 56, 10933–10940.
Falowo, A.B., Fayemi, P.O., Muchenje, V., 2014. Natural antioxidants against lipid–pro-
tein oxidative deterioration in meat and meat products: a review. Food Res. Int. 64,
5. Conclusion 171–181.
Folch, J., Lees, M., Sloanestanley, G.H., 1957. A simple method for the isolation and
purification of total lipids from animal tissues. J. Biol. Chem. 226, 497–509.
In conclusion, the results reported in this work showed an increase
Galíndez, R., De Basilio, V., Martínez, G., Vargas, D., Uztariz, E., Mejía, P., 2010. Effect of
in meat quality parameters and antioxidant stability of quail breast hatching month, egg physical characters and storage, on embryonic mortality in ja-
meat because of dietary mushroom supplementation. The inclusion of panese quails (Coturnix coturnix japonica). Zootec. Trop. 28, 17–24.
10 or 20 g of P. ostreatus/kg in the diet was effective in delaying the Genchev, A., Mihaylova, G., Ribarski, S., Pavlov, A., Kabakchiev, M., 2008. Meat quality
and composition in Japanese quails. Trakia J. Sci. 6, 72–82.
lipid oxidation of breasts and enhancing the color, pH, WHC, CLW, and Genchev, A., Mihaylov, R., 2008. Slaughter analysis protocol in experiments using
texture. These results could be associated to the presence of phenolic Japanese quails (Coturnix japonica). Trakia J. Sci. 4, 66.
constituents in meat samples, as well as to the antiradical DPPH• and Ghazaghi, M., Mehri, M., Bagherzadeh-Kasmani, F., 2014. Effects of dietary Mentha spi-
cata on performance, blood metabolites, meat quality and microbial ecosystem of
ABTS•+ values founded in P. ostreatus treatments when compared with small intestine in growing Japanese quail. Anim. Feed Sci. Tech. 194, 89–98.
control group. However, no significant effects of treatment were ob- Giannenas, I., Pappas, I.S., Mavridis, S., Kontopidis, G., Skoufos, J., Kyriazakis, I., 2010a.
served on performance and carcass characteristics. Future experiments Performance and antioxidant status of broiler chickens supplemented with dried
mushrooms (Agaricus bisporus) in their diet. Poult. Sci. 89, 303–311.
are required to elucidate the mechanisms of antioxidant activity and to Giannenas, I., Tontis, D., Tsalie, E., Chronis, E.F., Doukas, D., Kyriazakis, I., 2010b.
determine the individual components responsible for antioxidant Influence of dietary mushroom Agaricus bisporus on intestinal morphology and mi-
properties. These results indicate that edible mushrooms should be croflora composition in broiler chickens. Res. Vet. Sci. 89, 78–84.
Guillén-Navarro, G.K., Márquez-Rocha, F.J., Sánchez-Vázquez, J.E., 1998. Producción de
considered for use as an alternative to commercially available anti-
biomasa y enzimas ligninolíticas por Pleurotus ostreatus en cultivo sumergido. Rev.
oxidants that are currently used as a feed supplement or incorporated Iberoam. Micol. 15, 302–306.
directly into meat products. Guo, F.C., Williams, B.A., Kwakkel, R.P., Li, H.S., Li, X.P., Luo, J.Y., Li, W.K., Verstegen,
M.W.A., 2004. Effects of mushroom and herb polysaccharides, as alternatives for an
antibiotic, on the cecal microbial ecosystem in broiler chickens. Poult. Sci. 83,
Acknowledgments 175–182.
Hernández, J., Goycoolea, F.M., Quintero, J., Acosta, A., Castañeda, M., Domínguez, Z.,
Rey D. Vargas-Sánchez gratefully acknowledges the fellowship re- Robles, R., Vázquez-Moreno, L., Velázquez, E.F., Astiazaran, H., Lugo, E., Velázquez,
C., 2007. Sonoran propolis: chemical composition and antiproliferative activity on
ceived from CONACYT (2015, 1; 290941)for his postdoctoral work. We cancer cell lines. Planta Med. 73, 1469–1474.
are grateful to Carlos Bell Castro Tamayo, M.S., Dr. Ramón Ignacio Huang, B., He, J., Ban, X., Zeng, H., Yao, X., Wang, Y., 2011. Antioxidant activity of
Castillo López, FMVZ, Vladimir Martínez Cruz and Melesio Quiñones bovine and porcine meat treated with extracts from edible lotus (Nelumbo nucifera)
rhizome knot and leaf. Meat Sci. 87, 46–53.
for his technical support. Ikhlas, B., Huda, N., Noryati, I., 2011. Chemical composition and physicochemical
properties of meatballs prepared from mechanically deboned quail meat using var-
Conflict of interest ious types of flour. Int. J. Poult. Sci. 10, 30–37.
Kahl, R., Kappus, H., 1993. Toxicology of the synthetic antioxidants BHA and BHT in
comparison with the natural antioxidant vitamin E. Z. Lebensm. Unters. Forsch. 196,
There was no conflict of interest throughout the duration of the 329–338.
current investigation. Kamboh, A.A., Memon, A.M., Mughal, M.J., Memon, J., Bakhetgul, M., 2017. Dietary
effects of soy and citrus flavonoid on antioxidation and microbial quality of meat in
broilers. J. Anim. Physiol. Anim. Nutr. 1–6.
References Kang, N.H., Lee, W.K., Yi, B.R., Park, M.A., Lee, H.R., Park, S.K., Hwang, K.A., Park, H.K.,
Choi, K.C., 2012. Modulation of lipid metabolism by mixtures of protamine and
chitooligosaccharide through pancreatic lipase inhibitory activity in a rat model. Lab.
Albalasmeh, A.A., Berhe, A.A., Ghezzehei, T.A., 2013. A new method for rapid determi-
Anim. Res. 28, 31–38.
nation of carbohydrate and total carbon concentrations using UV spectrophotometry.
Kobayashi, S., Terashima, Y., Itoh, H., 2002. Effect of dietary chitosan on fat deposition
Carbohydr. Polym. 97, 253–261.
and lipase activity in digesta in broiler chickens. Br. Poult. Sci. 43, 70–273.
Allen, C.D., Fletcher, D.L., Northcutt, J.K., Russell, S.M., 1998. The relationship of broiler
Lábaque, M.C., Kembro, J.M., Luna, A., Marin, R.H., 2013. Effects of thymol feed sup-
breast color to meat quality and shelf-life. Poult. Sci. 77, 361–366.
plementation on female Japanese quail (Coturnix coturnix) behavioral fear response.
A.O.A.C, 2005. Official Methods of Analysis, 18th ed. Association of Official Analytical
Anim. Feed Sci. Tech. 183, 67–72.
Chemists, Gaitherburg, USA.
Lee, T.T., Ciou, J.Y., Chiang, C.J., Chao, Y.P., Yu, B., 2012. Effect of Pleurotus eryngii stalk
Barbut, S., Zhang, L., Marcone, M., 2005. Effects of pale, normal, and dark chicken breast
residue on the oxidative status and meat quality of broiler chickens. J. Agric. Food

124
R.D. Vargas-Sánchez et al. Livestock Science 207 (2018) 117–125

Chem. 60, 11157–11163. Poljsak, B., Šuput, D., Milisav, I., 2013. Achieving the balance between ROS and anti-
Lin, F., Wu, J., Abdelnabi, M.A., Ottinger, M.A., Giusti, M.M., 2004. Effects of dose and oxidants: when to use the synthetic antioxidants. Oxid. Med. Cell. Longev. 1–11.
glycosylation on the transfer of genistein into the eggs of the Japanese quail (Coturnix Popova, M., Bankova, V., Butovska, D., Petkov, V., Nikolova‐Damyanova, B., Sabatini,
japonica). J. Agric. Food Chem. 52, 2397–2403. A.G., Marcazzan, G.L., Bogdanov, S., 2004. Validated methods for the quantification
López-Bote, C.J., Gray, J.I., Gomaa, E.A., Flegal, C.J., 1998. Effect of dietary adminis- of biologically active constituents of poplar-type propolis. Phytochem. Anal. 15,
tration of oil extracts from rosemary and sage on lipid oxidation in broiler meat. Br. 235–240.
Poult. Sci. 39, 235–240. Purohit, A.S., Reed, C., Mohan, A., 2016. Development and evaluation of quail breakfast
Mau, J.L., Chao, G.R., Wu, K.T., 2001. Antioxidant properties of methanolic extracts from sausage. LWT-Food Sci. Tech. 69, 447–453.
several ear mushrooms. J. Agric. Food Chem. 49, 5461–5467. Qiao, M., Fletcher, D.L., Smith, D.P., Northcutt, J.K., 2001. The effect of broiler breast
Madhavi, D.L., Salunkhe, D.K., 1996. Toxicological aspects of food antioxidants. In: meat color on pH, moisture, water-holding capacity, and emulsification capacity.
Madhavi, D.L., Deshpande, S.S., Salunkhe, D.K. (Eds.), Food Antioxidants. Marcel Poult. Sci. 80, 676–680.
Dekker, New York, pp. 267–359 (of409 pp). Roupas, P., Keogh, J., Noakes, M., Margetts, C., Taylor, P., 2012. The role of edible
Mehdipour, Z., Afsharmanesh, M., Sami, M., 2013. Effects of dietary synbiotic and cin- mushrooms in health: evaluation of the evidence. J. Func. Foods 4, 687–709.
namon (Cinnamomum verum) supplementation on growth performance and meat Salih, A.M., Smith, D.M., Price, J.F., Dawson, L.E., 1987. Modified extraction 2-thio-
quality in Japanese quail. Livest. Sci. 154, 152–157. barbituric acid method for measuring lipid oxidation in poultry. Poult. Sci. 66,
NMX-F-490-1999-NORMEX, 1999. Alimentos para humanos. Determinación de la 1483–1488.
composición de ácidos grasos a partir de C6 por cromatografía de gases en aceites y Shahidi, F., Zhong, Y., 2010. Novel antioxidants in food quality preservation and health
grasas. Available In: 〈http://www.colpos.mx/bancodenormas/nmexicanas/NMX-F- promotion. Eur. J. Lipid Sci. Tech. 112, 930–940.
490-1987.PDF〉. Ene, 2017. Soares, A.A., de Souza, C.G.M., Daniel, F.M., Ferrari, G.P., da Costa, S.M.G., Peralta, R.M.,
N.R.C, 1994. National Research Council. Nutriment Requirements of Poultry. Nutrient 2009. Antioxidant activity and total phenolic content of Agaricus brasiliensis (Agaricus
requirements of ring-necked pheasants, 9th Rev. Japanese quail, and bobwhite quail, blazei Murril) in two stages of maturity. Food Chem. 112, 775–781.
National. Torrescano, G., Sánchez-Escalante, A., Jiménez, B., Roncalés, P., Beltrán, J.A., 2003.
Norma Oficial Mexicana, 1995. NOM-033-ZOO-1995, Sacrificio Humanitario de los Shear values of raw samples of 14 bovine muscles and their relation to muscle col-
Animales Domésticos y Silvestres. Available In: 〈http://www.cuautitlan.unam.mx/ lagen characteristics. Meat Sci. 64, 85–91.
descargas/cicuae/normas/Norma033.pdf〉. Ene, 2017. Vázquez-Ortiz, F.A., Caire, G., Higuera-Ciapara, I., Hernández, G., 1995. High perfor-
Patel, Y., Naraian, R., Singh, V.K., 2012. Medicinal properties of Pleurotus species (oyster mance liquid chromatographic determination of free amino acids in shrimp. J. Liq.
mushroom): a review. W. J. F. P. B. 3, 1–12. Chromatogr. Relat. Technol. 18, 2059–2068.
Pedneault, K., Angers, P., Avis, T.J., Gosselin, A., Tweddell, R.J., 2007. Fatty acid profiles Wang, X.M., Zhang, J., Wu, L.H., Zhao, Y.L., Li, T., Li, J.Q., Wang, Y.Z., Liu, H.G., 2014. A
of polar and non-polar lipids of Pleurotus ostreatus and P. cornucopiae var.‘citrino- mini-review of chemical composition and nutritional value of edible wild-grown
pileatus' grown at different temperatures. Mycol. Res. 111 (10), 1228–1234. mushroom from China. Food Chem. 151, 279–285.
Pfalzgraf, A., Frigg, M., Steinhart, H., 1995. Alpha-tocopherol contents and lipid oxida- Wakefield, D.K., Dransfield, E., Down, N.F., Taylor, A.A., 1989. Influence of post‐mortem
tion in pork muscle and adipose tissue during storage. J. Agric. Food Chem. 43, treatments on turkey and chicken meat texture. Int. J. Food Sci. Tech. 24, 81–92.
1339–4132. Warris, P.D., 2001. Meat Sci. An introductory Text. CABI Pub. Inc., New York.

125

You might also like