Meat Science 172 (2021) 108307

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Meat Science
journal homepage: www.elsevier.com/locate/meatsci

Agaricus bisporus mushroom as partial fat replacer improves the sensory T

quality maintaining the instrumental characteristics of beef burger
Iliani Patinhoa, Miriam Mabel Selanib, Erick Saldañac, Ana Clara Teixeira Bortoluzzia,
Juan Dario Rios-Meraa, Claudia Maria da Silvad, Marta Mitsui Kushidae,
Carmen J. Contreras-Castilloa,
⁎

a
Departamento de Agroindústria, Alimentos e Nutrição (LAN), Escola Superior de Agricultura “Luiz de Queiroz” (ESALQ), Universidade de São Paulo (USP), Piracicaba,
SP, Brazil
b
Centro de Ciências da Natureza, Campus Lagoa do Sino, Universidade Federal de São Carlos, Rod. Lauri Simões de Barros, Km 12, Buri, SP, Brazil
c
Facultad de Ingeniería Agroindustrial, Universidad Nacional de Moquegua (UNAM), Calle Ancash S/N, 18001 Moquegua, Peru
d
Lanali, Laboratório de Análise de Alimentos, BR 467, Km 110, Cascavel, PR, Brazil
e
Departamento de Engenharia de Alimentos (ZEA), Faculdade de Zootecnia e Engenharia de Alimentos (FZEA), Universidade de São Paulo (USP), Av. Duque de Caxias
Norte, 225, Pirassununga, SP, Brazil

ARTICLE INFO ABSTRACT

Keywords: The effect of Agaricus bisporus (AB) mushroom as a fat replacer in beef burgers was evaluated. Four treatments
Agaricus bisporus were compared: control (0% AB, 20% fat) and 3 treatments with partial fat replacement: AB 5% (5% AB, 15%
Fat reduction fat); AB 10% (10% AB, 10% fat); AB 15% (AB 15%, 5% fat). Mushroom addition increased moisture content and
Beef burger yield and decreased cooking loss and diameter reduction of the burgers. Formulations with the highest AB
Lipid oxidation
concentrations were lighter and redder than the control. AB incorporation affected texture, resulting in less hard
Texture profile analysis
and less chewy products. In general, lipid oxidation increased during the storage time, however the lowest values
Sensory profile
were observed in AB 15%, i.e. the lowest fat content and the presence of AB increased the oxidative stability. AB
10% and AB 15% had good overall liking and were sensorially characterized as juicy, tender and flavorsome
burgers. The partial replacement of animal fat by AB is a promising strategy for developing a low-fat burger.

1. Introduction important sources of proteins (mainly essential amino acids), vitamins,

Beef burgers are among the most attractive ready-to-serve foods
(Patinho et al., 2019; Rios-Mera et al., 2019; Soltanizadeh & Ghiasi-
Esfahani, 2014). In Brazil, because of their high consumption, burgers
have considerable importance in the economy, accounting for 13% of
total quick service restaurant sales.
In general, beef burgers are produced with a high fat content
(20–30%) (Feiner, 2006; Heck et al., 2019), which is a limiting factor
considering that consumers have become more aware of the relation-
ship between diet and health. According to the WHO (2020), total fat
intake should be less than 30% of the total energy intake to prevent
unhealthy weight gain in adults and the intake of saturated fats should
be less than 10% of the total energy intake to reduce the risk of de-
veloping noncommunicable diseases.
Thus, to obtain a balanced diet, the consumption of vegetables have
attracted attention of consumers (Liu et al., 2014). In addition to ve-
getables, mushrooms also represent a healthy alternative as they are
minerals, dietary fibers (especially β-glucan), and phenolic compounds
(Cardoso et al., 2019; Patinho et al., 2019; Rezaeian & Pourianfar,
2016). Because of the nutritional characteristics and the considerable
increase in mushroom production and consumption, scientific studies
have evaluated the nutritional quality and functional potential of dif-
ferent edible mushroom species. These studies have also focused on the
application of AB as an ingredient in different foods. For instance, in
our preliminary study, different technological strategies (fat/salt re-
duction, addition of natural antioxidants) were evaluated by the addi-
tion of AB into beef burger formulations (Patinho et al., 2019). Ac-
cording to the results, mushroom showed to be a possible substitute for
animal fat as it retained higher percentages of water and fat in beef
burgers, reducing the impact of fat reduction in the sensory properties
of the product.
From the technological standpoint, the development of low-fat meat
products is not always easy because meat replacement negatively im-
pacts the sensory characteristics of foods (Afshari, Hosseini, Mousavi

⁎
Corresponding author.
E-mail address: ccastill@usp.br (C.J. Contreras-Castillo).

https://doi.org/10.1016/j.meatsci.2020.108307
Received 18 December 2019; Received in revised form 27 May 2020; Accepted 2 September 2020
Available online 06 September 2020
0309-1740/ © 2020 Elsevier Ltd. All rights reserved.
I. Patinho, et al.
Khaneghah, & Khaksar, 2017; Moghtadaei, Soltanizadeh, & Goli, 2018).
Although there are several studies in the literature on the development
of burgers using fat substitutes, as well as studies with the incorporation
of powdered mushrooms (Kurt & Gençcelep, 2018; Pil-Nam et al., 2015;
Süfer, Bozok, & Demir, 2016) or mushroom extracts (Bao, Ushio, &
Ohshima, 2008; Dermiki et al., 2013; Mattar et al., 2018) in meat
products, as far as we know the incorporation of cooked mushrooms as
fat substitute in beef burgers has not been explored.
It is known that the replacement of animal fat by another healthier
lipid source affects the sensory quality of the meat product, often
leading to the consumer rejection (da Silva et al., 2019; Saldaña et al.,
2018). Faced with this challenge, sensory and consumer science pro-
vides different sensory techniques to meat scientists, allowing them to
obtain the sensory profile of healthier meat products (Saldaña et al.,
2020), as well as to assess their acceptance and purchase intention
(Ventanas, González-Mohino, Estévez, & Carvalho, 2019). In this re-
gard, the CATA questionnaire is one of the most outstanding sensory
techniques for sensory profiling of meat products, since it is quick to
implement by practitioners and easy to use by the respondents (Ares &
Jaeger, 2015). This technique has been extensively applied to char-
acterize different meat products, such as chicken burger with pink
pepper extract (Saldaña, Serrano-León, Selani, & Contreras-Castillo,
2020), bacon smoked with different Brazilian woods (Saldaña et al.,
2019), low-fat burger (Heck et al., 2017), restructured low-fat cooked
ham (Oliveira et al., 2018), low-fat Bologna sausage with flavor en-
hancers (dos Santos Alves et al., 2017), among others. The mathema-
tical association between the sensory profile and the liking of a product
to identify the sensory drivers of liking/disliking is an efficient way to
focus our attention on those salient sensory attributes (Ares, Dauber,
Fernández, Giménez, & Varela, 2014). For this reason, hedonic and
sensory measurements are commonly coupled to the same test, which is
called “Ideal Profile” (Saldaña et al., 2019; Worch, Lê, Punter, & Pagès,
2013). The use of the Ideal Profile in the development of meat products
is scarce, which demonstrates the novelty of this study from a sensory
perspective.
Based on the previous theorical framework, the aim of this study
was to investigate the impact of different levels of cooked mushroom as
an animal fat replacer on the physicochemical properties and ideal
profile of beef burger.
2. Material and methods
2.1. Materials
The mushrooms (Agaricus bisporus) were supplied by Zucca
Cogumelos (Salto/SP, Brazil) and the condiments (black pepper, onion
powder, garlic powder) and additives (sodium erythorbate (anti-
oxidant), sodium tripolyphosphate and monosodium glutamate, which
were used within the limits allowed by Brazilian legislation) were do-
nated by Ibrac (Rio Claro/SP, Brazil). Three different batches of beef
meat (Quadriceps femoris from Angus cattle) from animals slaughtered
on different days were supplied by VPJ Alimentos (Pirassununga/SP,
Brazil). After boning, the meat was kept frozen until its further use,
which occurred between 13 and 17 days after slaughtering. The animal
fat used was pork back fat purchased in three different days at a local
market (Piracicaba/SP, Brazil) and stored under freezing until use,
which occurred between 3 and 5 days after slaughtering.
2.2. Mushroom preparation
The mushrooms were prepared following the recommendations of
Ng and Tan (2017). Firstly, mushrooms were washed and portions
(100 g) were cooked in 100 mL of distilled water using microwave oven
(800 W, ME21S, Electrolux, Manaus, Brazil) for 1.5 min in an open
container. The content was filtered using a 1-mm sieve and the mush-
room was ground for 30 s in a multiprocessor (Philco, PMX600, China).
2
Meat Science 172 (2021) 108307
The cooked mushroom (93.47% moisture, 2.8% protein, 0.06% lipid,
0.5% ash, 2.37% fiber, 0.8% carbohydrates) was the material added to
the burger formulation.
2.3. Burger formulation
Three beef burger formulations were manufactured varying the
animal fat and Agaricus bisporus (AB) contents: AB 5% (5% AB and 15%
fat); AB 10% (10% AB and 10% fat); AB 15% (AB 15% and 5% fat).
Additionally, a control treatment containing a standard content of fat
(20%) was prepared. The minimum and maximum levels of each factor
were based on our previous study (Patinho et al., 2019).
Beef and fat were ground in a grinder (P33003, Hermann SA), with
5 and 3 mm plates, respectively. Then, beef (70%) was manually mixed
with salt (2.0%) and water (7.0%) for 3 min to extract myofibrillar
proteins. Subsequently, the other ingredients were added in the fol-
lowing order: sodium erythorbate (0.05%), monosodium glutamate
(0.05%), mushroom (0, 5, 10 and 15%), black pepper (0.05%), onion
powder (0.2%), garlic powder (0.3%), sodium tripolyphosphate (0.3%),
pork fat (5, 10, 15 and 20%) and were manually mixed for 7 min. After
obtaining the meat batter, 100 g portions were weighed, molded (10 cm
diameter and 1 cm thick molds) and the burgers were stored at −18 °C
for 2 h before being packed to prevent sample deformation. After that,
burgers were packed in low density polyethylene bags and stored at
4 °C with incidence of white light (fluorescent lamp, light flow 800 lm).
The pH, color, water activity and the lipid oxidation of the burgers were
evaluated for 16 days. For sensory evaluation, the samples were con-
ditioned at −18 °C until the analysis, which occurred after micro-
biological analysis (15 days after processing).
2.4. Physicochemical analysis of beef burgers
2.4.1. Water activity (Aw), color and pH measurement
Water activity (Aw) was determined on raw burgers using a standard
hygrometer (AquaLab 4TE, Decagon Devices, Pullman, USA). Color
measurement was determined directly on the raw burgers using a
Konica Minolta colorimeter (Chroma Meter, CR-400, Mahwah, NJ,
USA) with D65 illuminating source, measuring area 8 mm diameter,
viewing angle 10°. The coordinates determined were: L* (lightness), a*
(redness) and b* (yellowness). The pH was measured on the raw bur-
gers using a potentiometer (Hanna instruments, HI98163, Romania)
coupled to a glass electrode. Measurements were performed on 3 bat-
ches of each treatment, with 3 readings on each sample, after 1, 4, 8, 12
and 16 days of storage at 4 °C.
2.4.2. Determination of thiobarbituric acid reactive substances (TBARS)
TBARS value was determined in triplicate using the method Cd
19–90, described by the American Oil Chemists' Society (AOCS, 1990),
with modifications. An aliquot of 7 g of burger was added with 0.015 g
of ethylenediamine tetra-acetic acid (EDTA), 0.015 g of propyl gallate
and 15 mL of a 7.5% trichloroacetic acid solution. The content was
vortexed (1800 rpm, 1 min) and 15 mL of a 7.5% trichloroacetic acid
solution were added and vortexed again. The mixture was filtered
(qualitative #4, 125 mm filter paper) and 2.5 mL of the filtrate was
added to 2.5 mL of an aqueous thiobarbituric acid (TBA) solution
(46 mM). The samples were kept in a water bath with boiling water
(95 ± 5 °C) for 35 min and then cooled in an ice bath. Absorbance
(532 nm) was measured using a spectrophotometer (Shimadzu, UV–Vis
mini 1240, Chiyoda-ku, Tokyo, Japan). TBARS values were calculated
from a standard curve of 1,1,3,3 tetraethoxypropane and expressed in
mg malonaldehyde (MDA)/Kg sample. Analyzes were performed in
triplicate after 1, 4, 8, 12 and 16 days of storage at 4 °C.
2.4.3. Proximate composition
To determine the proximate composition of raw burgers, the fol-
lowing analyzes were performed: moisture was assessed by drying the
I. Patinho, et al.
samples in an oven at 105 °C until constant weight (AOAC, 2000); crude
protein was estimated by measuring total nitrogen using the Kjeldhal
method (Nx6.25) (ISO. (1871:2009) (n.d.)); ash was determined by
calcination of the organic matter in the muffle furnace at 550 °C (AOAC,
2000); total lipids were extracted using hexane and the Soxhlet method
(ISO. (1443,2010) (n.d.)). The contents of proteins and lipids were
performed in duplicate, while the contents of moisture and ash were
estimated in triplicate. Results were calculated on a wet basis and ex-
pressed as percentage (%).
2.4.4. Sodium content
The sodium content of beef burgers was determined as described by
AOAC (2016). Four grams of each raw sample were taken to the muffle
at 525 °C until the crude ash was obtained. Subsequently, the ash was
cooled to room temperature and solubilized in 15 mL of diluted nitric
acid, HNO3 (250 mL of HNO3 in 750 mL of distilled water), filtered and
then transferred to a 100 mL volumetric flask. A blank sample was used
as a control. The readings were taken in a flame photometer (brand
Digimed, model DM63, São Paulo, Brazil) in duplicate.
2.4.5. Theoretical value of dietary fibers in beef burgers
The estimated dietary fiber content of burgers was obtained from
the fiber content of the cooked mushroom (2.37%) added in each for-
mulation (5, 10 and 15%), according to Eq. 1.
%of mushroom added to the burger × 2.37
%Dietary fiber =
100 (1)
2.4.6. Cooking properties
Samples were cooked in an electric hot plate at 150 °C, until the
internal temperature of the burgers reached 75 °C, and then the burgers
were cooled to 25 °C.
Cooking loss (CL) corresponds to the weight of the burger before
and after cooking, which was expressed as a percentage and calculated
according to Eq. 2.
Raw burger weight (g)–Cooked burger weight (g) x 100
CL (%) =
Raw burger weight (g) (2)
The diameter reduction (DR) of the samples was measured before
and after cooking in 3 replicates and calculated according to Eq. 3
(Sánchez-Zapata et al., 2010).
Raw burger diameter (cm)–Cooked burger diameter (cm) x 100
DR (%) =
Raw burger diameter (cm)
(3)
2.4.7. Texture profile analysis
Texture profile analysis (TPA) was performed using a TA-XT texture
analyzer (Stable Micro Systems, Godalming, UK) based on the para-
meters defined by Rios-Mera et al. (2020) and Selani et al. (2016).
Samples were molded using a circular stainless-steel cutter. Nine
cylinders (2.5 cm in diameter) per treatment were compressed to 75%
of their original height using a P–35 probe (long axis, regular base) at a
speed of 3.3 mm/s. Nine measurements were performed in 3 batches of
each treatment. The parameters determined were: hardness, cohesive-
ness, chewiness and springiness, as described by Saldaña et al. (2015)
and Bourne (1978).
2.5. Microbiological analysis
Microbiological analysis were determined in duplicate, as described
by da Silva et al. (2017). Burger samples (25 g) were placed in sterile
sampling bags containing 225 mL of sterile buffered peptone water and
then homogenized in a Stomacher (MA440, Marconi, Piracicaba,
Brazil). Then, the necessary dilutions were made using lactose broth for
presence/absence test, or peptone water for quantitation tests. Counts
3
Meat Science 172 (2021) 108307
of total mesophilic bacteria (PCA, Merck, Darmstadt, Germany), molds
and yeasts (DRBC, Merck, Darmstadt, Germany), Escherichia coli
(Compact Dry™ EC, Nissui Pharmaceutical Co., Ltd., Tokyo, Japan),
Staphylococcus aureus (Compact Dry™ XSA, Nissui Pharmaceutical Co.,
Ltd., Tokyo, Japan) and Salmonella sp. (BAX System™, Dupont/Qua-
licon, Wilmington, USA) were enumerated. As a consequence of the
analysis undertaken under Brazilian legislation, the burger samples
were deemed safe for presentation to sensory panels.
2.6. Sensory analysis: the ideal profile
Sensory analysis was performed in a single session, following the
recommendations and procedures described by Saldaña et al. (2019).
Data were collected using Compusense Cloud software (Compusense
Inc., Guelph, Canada) using tablets (Samsung Galaxy Table E T560). All
participants completed an informed consent form, which was pre-
viously approved by the ethics committee (CAAE
98168118.4.0000.5395).
2.6.1. Consumers
Two hundred and nine regular burger consumers (58% women and
42% men, aged between 18 and 61 years) were recruited from students,
staff and visitors of the Escola Superior de Agricultura “Luiz de Queiroz”,
Universidade de São Paulo (ESALQ/USP).
2.6.2. Familiarization
Before starting the test, participants were familiarized using a
15 min session, in which the use of Compusense software and the Check-
all-that-apply (CATA) questions was fully explained. Afterwards, con-
sumers were installed in individual sensory booths under artificial
white light.
2.6.3. Ideal profile
Samples (~10 g) were served monadically at 50 °C in coded dis-
posable plastic plates following a Williams Latin Square Design
(Wakeling & MacFie, 1995). Consumers rated their overall liking using
a 9-point hedonic scale, ranging from “disliked extremely” (1) to “liked
extremely” (9). Then, consumers indicated which sensory descriptors
characterized better each sample (CATA questions). The list consisted
of 12 descriptors related to appearance, aroma, taste and texture. The
sensory terms used in this study were based on previous studies
(Patinho et al., 2019; Rios-Mera et al., 2020, 2019; Selani et al., 2016).
Water and biscuit were offered to consumers to clean the palate be-
tween samples.
2.7. Data analysis
The experiment was conducted in a randomized complete block
design with 3 blocks (three independent processing). All analyzes were
performed using R software, version 3.5.1.
2.7.1. Instrumental analysis
A mixed ANOVA was used considering treatment (T), storage time
(ST) and T*ST as fixed effects, while processing (P), T*P, and ST*P as
random factors. Then, means were compared using Tukey's test at 95%
confidence. The variables analyzed in the course of storage time were:
lipid oxidation due to antioxidant activity of AB mushroom, water ac-
tivity as a function of high AB water content, pH and color.
2.7.2. Sensory analysis: the ideal profile
For CATA questions, correspondence analysis (CA) was performed
using the frequency of terms that characterized each sample, con-
sidering the chi-square distances, as recommended by Vidal, Tárrega,
Antúnez, Ares, and Jaeger (2015). Data from the overall liking test were
analyzed using mixed ANOVA, considering sample (fixed) and con-
sumer (random) as sources of variation. When the difference between
I. Patinho, et al. Meat Science 172 (2021) 108307

mean values was significant at 5% significance, the Tukey's test was Table 1
performed. To correlate the frequency of sensory attributes with the Effect of adding Agaricus bisporus mushroom as a fat substitute on pH and water
liking rate of the burger samples, a Principal Coordinates Analysis activity of beef burger.
(PCoA) was perfomed. The degree of correlation between an attribute Source of variation Aw pH
and the liking is represented by the proximity between them, indicating
that attributes close to liking contribute to its increase, while those that Treatment
are distant contribute to its decrease (Saldaña, Cardoso Merlo, et al.,
Control 0.970b 5.78a
2020). AB 5% 0.970b 5.77a
AB 10% 0.972ab 5.73a
AB 15% 0.973a 5.72a
3. Results and discussion SEM 0.003 0.065

3.1. Physicochemical analysis of beef burger
3.1.1. Determination of thiobarbituric acid reactive substances (TBARS)
After microbial deterioration, lipid oxidation is the main cause of
sensory deterioration and shelf life reduction in burgers, as the oxida-
tion cascade generates malonaldehyde (MDA), a major decomposition
product of polyunsaturated fatty acid hydroperoxides (Damodaran,
Parkin, & Fennema, 2010; Zhang et al., 2019). Herein, the oxidative
stability of beef burgers was evaluated by measuring the MDA content.
The interaction between ‘storage time’ and ‘treatment’ was sig-
nificant for lipid oxidation (P < 0.05). According to Fig. 1, TBARS
values increased during the storage period and these differences per-
sisted until the 16th day.
Formulations manufactured with different mushroom content
showed lower lipid oxidation than the control (Fig. 1), representing a
significant reduction in TBARS of 21.84% (AB 5%), 36.62% (AB 10%)
and 51.40% (AB 15%). A similar trend was also reported in ground beef
added with dehydrated AB (Alnoumani, Ataman, & Were, 2017) and in
fish burger manufactured with fresh AB (Nayak, Raju, Lakshmisha,
Singh, & Sofi, 2015).
There was an inverse association between the mushroom content
and the TBARS values: samples with higher replacement (and conse-
quently with lower fat proportion) presented the lowest TBARS. Thus,
one of the reasons for the lower oxidative stability of the control is its
high fat content. Oxidation reactions in burgers occur through various
types of oxidizing agents in muscle tissue, at different stages during
processing (grinding, mixing, cooking) and storage (de Oliveira
Ferreira, Rosset, Lima, Stuelp Campelo, & de Macedo, 2019). The
content of bioactive compounds with alleged antioxidant activity in a
burger model is also involved in the oxidative stability of burgers added
with AB (Gąsecka, Magdziak, Siwulski, & Mleczek, 2018; Liu, Jia, Kan,
& Jin, 2013; Ng & Tan, 2017; Patinho et al., 2019).
Storage days Aw pH
1 0.970a 5.83a
4 0.970a 5.78ab
8 0.970a 5.65b
12 0.970a 5.73ab
16 0.970a 5.74ab
SEM 0.003 0.115
Different letters in the same column indicate significant differences (P < 0.05)
according to the Tukey's test. SEM: Standard error of the mean. Control (sample
without mushroom), AB 5% (addition of 5% Agaricus bisporus), AB 10% (ad-
dition of 10% Agaricus bisporus) and AB 15% (addition of 15% Agaricus bis-
porus).
According to the results, the formulation containing 15% mushroom
and 5% fat presented the highest oxidative stability among the treat-
ments. Additionally, this burger formulation presented similar TBARS
values compared to the other formulations in the 8th day. All samples
presented values below the MDA threshold for sensory acceptance,
since according to Trindade, Mancini-Filho, and Villavicencio (2009),
TBARS values above 2 mg MDA/kg sample in beef burger indicate
sensory quality loss because of the perception of oxidation reactions in
the food. In a recent study, Zhang et al. (2019) propose that beef re-
mains acceptable to consumers, even when its TBARS values reach le-
vels of 2.5 mg MDA/kg.
3.1.2. pH and water activity (Aw)
The AB used in our study had a mean pH of 6.61. Despite the pH
close to neutrality, the addition of mushroom to burgers did not cause
significant differences in this parameter (Table 1) and no interaction
effect was found. On the other hand, there was significant pH variation
during the 16 days of storage, which ranged from 5.65 to 5.83. Al-
though there was a pH difference during the storage time, changes were
marginal (0.18 variation between 16 days) and did not show a clear

1.6 Fig. 1. Thiobarbituric acid reactive sub-

1.5 Control AB 5% AB 10% AB 15% aA stances (TBARS) of beef burger during
16 days of storage at 4 °C.
1.4
Different lower-case letters indicate sig-
1.3
nificant difference between treatments and
TBARS (mg MDA/kg sample)

1.2 bA different upper-case letters indicate sig-

1.1 aB nificant difference between storage time
1.0 (days) according to Tukey's test (P < 0.05).
0.9 bB n = 3. Vertical bars represent the standard
0.8 aC cA error of the mean. Control (sample without
0.7
aC
cB mushroom), AB 5% (addition of 5% Agaricus
aD bC bisporus), AB 10% (addition of 10% Agaricus
0.6 dA
bD bisporus) and AB 15% (addition of 15%
0.5
Agaricus bisporus).
0.4 cD
aE dB
0.3 bE
0.2 dD cC
cE
0.1 dE
0.0
1 4 8 12 16

Storage time (days)

4
I. Patinho, et al. Meat Science 172 (2021) 108307

Table 2 Table 3
Effect of adding Agaricus bisporus mushroom as a fat substitute on color para- Centesimal composition and sodium content of beef burger added with Agaricus
meters (L*, a* and b*) of beef burger. bisporus mushroom.
Source of variation L* a* b* Treatment Sodium Protein Lipid Moisture Ash
(mg/100 g) (%) (%) (%) (%)
Treatment
Control 822.17a 16.72a 14.77a 65.60c 3.04b
Control 51.29a 14.66b 9.57a
AB 5% 49.09b 16.06ab 9.13a AB 5% 818.67a 16.14a 11.75b 69.00bc 3.05b
AB 10% 46.78c 16.66a 9.95a AB 10% 785.00a 15.83a 8.55c 70.93b 3.13a
AB 15% 43.37d 16.17a 9.93a AB 15% 827.17a 16.05a 3.97d 75.09a 3.11a
SEM 1.06 0.98 0.71 SEM 3.72 0.06 0.37 0.64 0.32

Storage days L* a* b*
1 46.98a 10.54c 9.09b
Different letters in the same column indicate significant differences (P < 0.05)
4 47.75a 12.59b 9.42ab according to the Tukey's test. SEM: Standard error of the mean. Control (sample
8 47.36a 14.06b 9.40ab without mushroom), AB 5% (addition of 5% Agaricus bisporus), AB 10% (ad-
12 48.24a 20.28a 9.90ab dition of 10% Agaricus bisporus) and AB 15% (addition of 15% Agaricus bis-
16 47.85a 21.96a 10.42a porus).
SEM 0.83 0.90 0.66

values) is related to oxidation and metmyoglobin pigment formation

Different letters in the same column indicate significant differences (P < 0.05)
according to the Tukey's test. SEM: Standard error of the mean. Control (sample
without mushroom), AB 5% (addition of 5% Agaricus bisporus), AB 10% (ad-
dition of 10% Agaricus bisporus) and AB 15% (addition of 15% Agaricus bis-
porus).
trend. All values obtained for the samples at different storage times are
within the limit established by the Brazilian legislation (≤ 6.4)
(BRASIL, 1997).
There was significant difference (P < 0.05) in Aw between treat-
ments, however this difference did not impact negatively in the product
quality (Table 1). The formulation containing 15% mushroom had si-
milar Aw compared to the AB 10% treatment and higher Aw than the
control and the AB 5% sample. Since mushrooms are characterized by a
high moisture content and high Aw (≥ 0.98) (Venturini, Reyes, Rivera,
Oria, & Blanco, 2011), their addition in concentrations of 15% pro-
moted a slight increase in water activity of beef burgers.
3.1.3. Instrumental color
Based on the results presented in Table 2, higher mushroom addi-
tion to the burgers caused a decrease in the instrumental lightness.
Accordingly, the highest L* value was found in the control sample and
the lowest value in burger with 15% AB. Depending on the color
properties of the added material, the lightness may vary (Kurt &
Gençcelep, 2018). Similarly, Kurt and Gençcelep (2018) observed a
reduction in L* in a meat emulsion by increasing the concentration of
AB mushroom powder in the formulation. Another factor that may have
affected our results is the amount of fat used. This ingredient, having a
clear color, may have increased the lightness of burgers. High-fat raw
burgers were also lighter than fat-reduced burgers added with pine-
apple pomace as fat substitute (Selani et al., 2016).
Regarding the a* value, there was a significant effect of treatment
and storage time, but no interaction effect was observed. The addition
of AB increased the a* values during storage. Increasing a* over time
indicates no discoloration, i. e., there was no oxidation of oxymyo-
globin (bright red OMb) and its transition to metmyoglobin (brown
MMb) (Cooper et al., 2016; Warner, 2014). The formation of MMb re-
sults from the action of free radicals produced during lipid oxidation in
the heme group of myoglobin, which initiates the oxidation of the
molecule and leads to the color loss of the product. Thus, free radicals
produced during lipid oxidation can damage muscle fiber structure and
reduce pigmentation (Morgado et al., 2011). The present study showed
the opposite behavior: there was an increase in a* values during the
storage period, indicating that oxymyoglobin remained stable.
The b* value was not affected by treatments, but there was a sig-
nificant increase during the burger storage. Since both yellowness and
redness intensity increased during storage, this may indicate that
myoglobin did not oxidize, as the opposite (reduction in a* and b*
(Hernández Salueña, Sáenz Gamasa, Diñeiro Rubial, & Alberdi
Odriozola, 2019). Similar results were reported by Kim, Son, Ha, & Lee,
2003 in fried surimi gel containing oyster mushrooms (Pleurotus eryngii)
and in pork burger added with mushroom (Tremella fuciformis) (Cha,
Heo, Lee, Lo, & Moon, 2014).
3.1.4. Proximate composition
The results of the proximate composition and the sodium content of
beef burgers with AB addition are shown in Table 3.
It has been well-known that NaCl is one of the most widely used
additives in meat products (Inguglia, Zhang, Tiwari, Kerry, & Burgess,
2017). In the present study, 2% NaCl was used in all treatments and no
significant difference (P < 0.05) in sodium content was found between
them. Similar values were reported in goat burger (900 mg/90 g)
(Almeida, 2011) and beef burger (780 mg/100 g) (Novello & Pollonio,
2013).
As expected, because of the different amounts of fat added to the
formulations, there was a significant difference in lipid content. In fat-
reduced samples, fat was replaced by mushroom (low lipid content).
Thus, the lipid content decreased as the percentage of mushroom in-
creased in the formulations. In contrast, the moisture content has in-
creased and this is explained by the addition of AB, which has a high
moisture content (> 90% dry basis) (Bach, 2017) and contains dietary
fibers, which have the ability to retain water (Selani et al., 2016). The
highest moisture content was observed in the formulation AB 15%
(75.09%) and the lowest in the control (65.60%).
Regarding protein content, no significant differences were found
between treatments. According to the estimated content of dietary fi-
bers, burgers with 5%, 10% and 15% AB contained about 0.12 g/100 g,
0.24 g/100 g and 0.36 g/100 g fiber. Mehta, Ahlawat, Sharma, and
Dabur (2013) reported that a higher content of dietary fibers can re-
inforce the three-dimensional structure of the meat batter (link between
water, protein and lipids). The addition of mushroom either at 10 or
15% caused an increase in ash content compared to control and AB 5%.
3.1.5. Cooking properties
In the present study, cooking losses (CL) and diameter reduction
(DR) were influenced by the addition of AB (Table 4). The highest CL
was obtained in the control burger. However, as the concentration of
AB increased, the CL decreased significantly. Similar results were re-
ported by Selani et al. (2016) in beef burger manufactured with pine-
apple pomace. These results have relevance for the food industry in the
search for technological solutions to improve the water retention of
meat products, since the loss of water, besides reducing the yield,
causes liquid accumulation in the packaging and as consequence,
changes the color, texture and finally the acceptance of the meat pro-
duct (Bastos et al., 2014).

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I. Patinho, et al. Meat Science 172 (2021) 108307

Table 4 had higher moisture content and less cooking losses. Similarly, Wan
Cooking properties of beef burger added with Agaricus bisporus mushroom. Rosli and Solihah (2012) and Wong et al. (2017) also reported hardness
Treatment Cooking losses Diameter reduction reduction in meat products supplemented with mushrooms.
(%) (%) Although the springiness and cohesiveness presented small changes
between treatments, statistical differences were found between them.
Control 25.65a 16.57a
Both parameters were directly proportional to the mushroom content
AB 5% 15.52b 13.14b
AB 10% 13.15c 10.46c
added to the formulation. This effect was observed in the study per-
AB 15% 10.23d 9.14d formed by Wan Rosli et al. (2011) on chicken burger added with
SEM 0.15 0.36 mushroom.
The chewiness parameter is the product of hardness x cohesiveness
Different letters in the same column indicate significant differences (P < 0.05)
x springiness. Among these 3 parameters, the hardness was the most
according to the Tukey's test. SEM: Standard error of the mean. Control (sample
affected by the addition of mushroom. Moreover, burgers added with
without mushroom), AB 5% (addition of 5% Agaricus bisporus), AB 10% (ad-
mushroom presented lower chewiness. Thus, because samples manu-
dition of 10% Agaricus bisporus) and AB 15% (addition of 15% Agaricus bis-
porus). factured with mushroom are softer, they need less energy to be chewed
until an adequate consistency for swallowing is obtained. Lower che-
Regarding DR, it was observed that the control sample decreased winess of chicken burger and sausage added with mushroom has been
16.57% after cooking; however, this reduction in diameter decreased reported in the literature (Syuhairah, Huda, Syahariza, & Fazilah, 2016;
significantly with increasing mushroom percentage, reaching 9.14% in (Wan Rosli et al., 2011).
burgers with 15% AB. The reduction in diameter is the result of muscle
protein denaturation caused by water and fat losses (Carvalho et al., 3.3. Microbiological analysis
2019). As the ability of meat product extenders to improve water and
fat retention determines the shrinkage level of meat products (Alakali, The microbiological results indicated that the burgers were ade-
Irtwange, & Mzer, 2010), the high water and moisture retention capa- quate for human consumption, according to the current Brazilian leg-
city of mushrooms seems to prevented the shrinkage in the diameter of islation, RDC 12/2001 (ANVISA, 2001). Control samples presented
beef burgers during cooking. Similar results were obtained by 2.6 × 104 CFU/mL of mesophiles, 3.5 × 101 CFU/mL of total coli-
Soltanizadeh and Ghiasi-Esfahani (2014), who used Aloe vera as a meat forms, absence of E. coli, 1.8 × 104 CFU/mL for mold and yeast,
substitute in burger and by Carvalho et al. (2019), who evaluated hy- 2.0 × 101 CFU/mL of Staphylococcus aureus and absence of Salmonella
drated wheat fiber as meat and fat substitute in beef burgers. sp. In the samples AB 5%, AB 10% and AB 15% the average counts were
4.6 × 104, 1.2 × 104 and 1.6 × 104 CFU/mL, respectively, for me-
sophiles, 4.6 × 102, 4.4 × 102 and 3.2 × 103 CFU/mL, respectively,
3.2. Texture analysis for total coliforms, absence of E. coli, 5.4 × 103, 4.5 × 103 and
1.5 × 102 CFU/mL, respectively, for mold and yeasts, 2.0 × 102,
According to Table 5, the use of AB significantly influenced all 5.7 × 102 and 5.0 × 102 CFU/mL, respectively, for Staphylococcus
texture parameters of beef burgers in relation to the control treatment. aureus and absence of Salmonella sp.
Clearly, replacing the fat content with the mushroom softened the
texture. The results suggested that increased AB substitution up to 15% 3.4. Sensory analysis: ideal profile
impacted on less compressive strength (hardness), greater springiness
after deformation, better preservation of the burger's structure after the The presence of AB as an animal fat substitute affected the ideal
first compression (cohesiveness) and lower energy required to chew the profile expressed as sensory profile and overall liking of beef burgers.
sample until swallowing (chewiness). Similar results were found in The addition of 10% and 15% AB positively affected the “juicy”,
previous studies (Afshari et al., 2017; Moghtadaei et al., 2018; Yilmaz, “brittle” and “dry” attributes when compared to the control, thus
Karaman, Dogan, Yetim, & Kayacier, 2012). showing that in these attributes are the main sensory changes. As
The textural properties of meat products are highly related to the shown in Fig. 2, significant differences were found between the mean
properties of myofibrillar proteins (Westphalen, Briggs, & Lonergan, overall liking scores of the samples, which ranged from 6.9 to 7.2 on a
2006). It seems that myofibrillar proteins and mushrooms compete for 9-point hedonic scale. Beef burgers with 5%, 10% and 15% AB received
water adsorption and influence the texture of the product, making the scores above 7 and showed similar liking. Only the control sample
food softer (Soltanizadeh & Ghiasi-Esfahani, 2014). According to Gao, obtained a lower score, but still all treatments showed good overall
Zhang, and Zhou (2014), hardness varies inversely with moisture re- liking. Muñoz, Civille, and Carr (1992) state that scores between 6 and
tention of the product. This explains the results of the present study, 9 on a 9-point hedonic scale are good predictors of sensory acceptance
since beef burgers manufactured with higher mushroom percentages in the marketplace.
Fig. 3A shows the representation of attributes and treatments in the
Table 5 first two dimensions of the CA. The first two dimensions accounted for
Instrumental texture of beef burger added with Agaricus bisporus mushroom. 97% of the original information. As already mentioned, the sensory
Treatment Hardness Springiness Cohesiveness Chewiness profile revealed that the 10% and 15% AB burgers were similar and
(g) (mm) (g.mm) were perceived as salty, juicy, tender and flavorsome. These attributes
were associated with samples with higher percentage of mushroom,
Control 13,191.56a 0.83d 0.32d 3776.88a
which have high moisture content. Mushrooms contain umami com-
AB 5% 12,743.89b 0.84c 0.33c 3575.48b pounds (aspartic acid, glutamic acid and 5′-nucleotides) (Dermiki,
AB 10% 10,749.91c 0.85b 0.36b 3093.24c Phanphensophon, Mottram, & Methven, 2013), which act to enhance
AB 15% 9369.58d 0.87a 0.37a 2539.92d salty taste. In addition, they enhance the food taste (Yamaguchi &
SEM 82.09 0.02 0.01 50.84
Ninomiya, 2000).
Different letters in the same column indicate significant differences (P < 0.05) The first dimension of the CA separated the treatments with the
according to the Tukey's test. SEM: Standard error of the mean. Control (sample addition of mushroom from the control, which was characterized by the
without mushroom), AB 5% (addition of 5% Agaricus bisporus), AB 10% (ad- fibrous, seasoned, dry, and rancid attributes. This last attribute shows
dition of 10% Agaricus bisporus) and AB 15% (addition of 15% Agaricus bis- that the fat reduction along with the incorporation of cooked mush-
porus). rooms inhibited the development of the rancid attribute resulting from

6
I. Patinho, et al. Meat Science 172 (2021) 108307

9
6.87 7.09 7.12 7.2

8
(a) (ab) (ab) (b)
7.07

7
Overall liking
6
5
4
3
2
1

Control AB 5% AB 15% AB 10%

Treatments
Fig. 2. Overall liking scores of the 4 treatments evaluated through a 9-point hedonic scale. Different letters indicate significant differences according to Tukey's test
(P < 0.05). Vertical bars represent the standard error of the mean.

lipid oxidation. On the other hand, the second dimension of the CA
separated the samples with 10 and 15% AB from that with 5% AB,
which was characterized by the fatty and fibrous attributes. According
to Fig. 3B, the aromatic,flavorsome, seasoned, grilled, tender, and juicy
attributes were the sensory drivers of liking, indicating that the pre-
sence of these characteristics was desired by consumers. It is worthy to
mention that the salty sensory attribute was relatively close to liking,
showing its moderate influence. However, other sensory attributes were
more salient for the consumers. This can be explained by the intermodal
interaction between the attributes and by the fact that the salt mole-
cules do not only modify the saltiness of the product, but also modulate
other attributes related to taste, flavor and texture (Rios-Mera et al.,
2019), as those mentioned above. It is also importante to note that beef
burgers containing AB presented the majority of the sensory drivers of
liking, explaining their elevated overall liking (Fig. 2).
In general, the sensory results (overall liking and CATA) indicate
that AB can be incorporated into beef burgers without negatively affect
their sensory drivers of liking. Therefore, this result provides scientific
support for the development of a beef burger added with AB, increasing
the use of this mushroom in human nutrition. In addition, the re-
placement of animal fat by AB in beef burger could have greater ac-
ceptance in the market, which could be perceived as a low-fat beef
burger.
4. Conclusions
The use of A. bisporus to replace animal fat in beef burgers can be
considered a technological, nutritional and sensory promising strategy.

0.8 0.4
B A
Fatty
Rancid
0.6 0.3
Fatty
Juicy
0.4 0.2
Dim 2 (17.99 %)

Tender AB 5%
0.2 0.1 Fibrous

Salty Dry
Tasty Seasoned Control
0 0
Salty Tender
-0.8 -0.6 -0.4 -0.2 0 0.2 0.4 0.6 0.8 1 Grilled Brittle
Overall liking Fibrous JuicyAB 10% Aromatic
Aromatic -0.2 -0.1 AB 15% Rancid
Brittle
Tasty Seasoned
Grilled -0.4 -0.2

Dry
-0.6 -0.3
-0.2 -0.1 0 0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9

Dim 1 (79.06 %)

Fig. 3. Correspondence analysis. A: Representation of samples and descriptors in the first two dimensions of CA of the CATA questions; B: Overall liking based on
sensory descriptors.

7
I. Patinho, et al.
Formulations with A. bisporus addition, especially the AB 15% treat-
ment (15% mushroom and 5% fat) showed higher oxidative stability
and moisture retention, lower lipid content and cooking losses, re-
sulting in a tender product. In addition, beef burgers containing A.
bisporus not only have good technological quality, but also present a
sensory profile with attributes that positively contribute to the overall
liking of the product. This combination could be used for commercial
purposes to change the nutritional properties of beef burgers.
Declaration of Competing Interest
None.
Acknowledgments
Iliani Patinho is grateful to CAPES (Coordenação de
Aperfeiçoamento de Pessoal de Nível Superior, Brazil, for the master
scholarship (process n° 1766129). Juan D. Rios-Mera received the
support of the CIENCIACTIVA programme, PhD scholarship contract n°
238-2018-FONDECYT. The authors would also like to thank Zucca
mushrooms Company, VPJ Foods, Ibrac Additives and Condiments and
Sealed Air Brazil, for donating ingredients, raw materials and packa-
ging.
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