Journal of Agriculture and Food Research 8 (2022) 100293

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Journal of Agriculture and Food Research

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Evaluation of the sensory attributes of pepper soup beef hides and

determination of the preservative potential of the spices used for
its preparation
T.C.L. Maguipa a, P.D. Mbougueng b, *, H.M. Womeni a
a
University of Dschang-Cameroon, Department of Biochemistry, Cameroon
b
University of Ngaoundere-Cameroon, Department of Food Processing, Cameroon

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

Keywords: This study aimed to determine the best spice formulations used in the preparation of pepper soup beef hides and
Sensory evaluation to evaluate the antioxidant and antimicrobial activities of their aqueous extract. Sensory properties of pepper
Antimicrobial soup beef hides prepared from the spice’s formulations were evaluated with the 9-point hedonic scale. Proximate
Antioxidant
composition of formulations’ powders was analyzed using official methods (AOAC, 2005). Total phenols and
Proximate analyses
Spices
flavonoids contents were determined. Antioxidant activities from the spice’s formulations and their spices were
Pepper soup determined. The broth micro-dilution assay was used to evaluate the antimicrobial activities of the extracts.
Sensory evaluation of sixteen (16) pepper soups revealed that soups from formulations 456, 322, and 491 were
the most preferred in terms of flavor, odor, consistency, color, and overall acceptability. The extracts from
formulations 456 and 491 with the highest total phenols and flavonoids contents had shown the strongest
antioxidant activity. For the antibacterial activity, the aqueous extract from formulation 456 was the strongest
active against methicillin-resistant staphylococcus aureus, Enterobacter cloacae, Shigella flexieri, Escherichia coli, and
Salmonella typhi, with minimum inhibitory concentration (MIC) values ranging of 3.125–25 mg/ml compared to
those from formulations 491 and 322. Garlic aqueous extract exerted a bactericidal effect against methicillin-
sensitive Staphylococcus aureus, with a minimum bactericidal concentration (MBC) of 50 mg/ml. These in­
vestigations indicated that the aqueous extracts from the formulations could be considered natural sources of
antioxidant substances and antimicrobial agents for food preservation.

1. Introduction
In African countries, spices and herbs are generally added to foods
since ancient times to contribute to their taste and flavor, and also as
food preservatives and diseases remedies [1]. These characteristics are
associated with the phenolic compounds contained in the spices [2].
These spices are plants products that include seeds, kernels, bulbs,
stalks, roots, fruits, barks, leaves, pods or buds [3]. For their flavoring
and savoring characteristics, they are used as a whole, powder or
mixture of numerous spices [4], in small quantities as additives all over
the world [5].
The consumption of spices and aromatic herbs depends especially on
the socio-cultural groups, the food habits and their availability in the
zones of dwelling, [6]. In addition to their culinary role, spices and ar­
omatic herbs in the African context, confer to foods in which they are
incorporated, a nutritional role (contribution in lipids, carbohydrate,
proteins and mineral), functional properties and pharmacological vir­
tues [4].
Indeed, many spices have antimicrobial properties against numerous
gastroenteritis pathogenic bacteria such as Listeria, Staphylococci and
Escherichia coli [4]. This may explain why the use of spices is especially
prominent in meat processing (which is susceptible to decay). According
to Mah et al. [7], the mixture of garlic and other spices limited the
development of numerous microorganisms in Myeolchi-jeot, a Korean

Abbreviations: GAE, gallic acid equivalent; AAE, ascorbic acid equivalent; CE, catechin equivalent; TPC, total phenol content; FC, flavonoid content; DPPH, free
radical scavenging; FRAP, ferric reducing antioxidant power; HRSA, hydroxyl radical scavenging activity; ANOVA, Analysis of variance; MIC, Minimum Inhibitory
Concentration; MBC, Minimum Bactericidal Concentration.
* Corresponding author.
E-mail addresses: cmaguipa@yahoo.fr (T.C.L. Maguipa), pides_mbougueng@yahoo.fr (P.D. Mbougueng), womeni@yahoo.fr (H.M. Womeni).

https://doi.org/10.1016/j.jafr.2022.100293
Received 25 November 2021; Received in revised form 7 March 2022; Accepted 8 March 2022
Available online 18 March 2022
2666-1543/© 2022 Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
T.C.L. Maguipa et al.
salted anchovy. In addition, spices and aromatic plants are abundant
sources of components that have antioxidants and natural antibacterial
substances for food processing factories [8]. They are known to prevent
the formation of free radicals, delay the oxidization of lipids and prolong
the shelf life of food [9].
Several countries have recommended their usage as alternatives to
salt for seasoning foods, thereby reducing sodium intake [10]. Their
properties to increase both flavor and taste have made them common
condiments and ingredients in every cuisine. In Nigeria, some spices are
used as a seasoning in certain soups preparations which are delicacies
and also recommended for cold and malaria fever [11].
Cameroon has a rich flora with more than 13,000 species of plants
identified and its multi-cultural background exposes its population to a
variety of well-spiced diets that even in the absence of a refrigerator
hardly go sour because of their antioxidant properties [12]. These spices
are readily available, at a low cost and to boost flavor, they form the
major ingredients in soup preparation. Moreover, there are as many
varieties of traditional soups as tribes. The taste and quality differ from
one soup to another depending on the type of spices used in their
preparation. Hence, some of the commonly consumed spices must be
screened for reactive oxygen species scavenging activity [12]. Pepper
soup is one of the traditional foods which can be classified as an appe­
tizer, warm food during cold and sickness. Pepper soup beef hides is a
soup made from beef hides, simmered with various other ingredients.
According to Maguipa et al. [13] five major ingredients are used in the
preparation of pepper soup beef hides (Allium sativum, Allium cepa, Piper
nigrum, Afrostyrax lepidophyllus and Ricinodendron heudelotii). The
studies conducted on these spices showed that Allium sativum [14] and
Allium cepa [15] used for the preparation of this soup have antibacterial
efficacy and seasoning. Afrostyrax lepidophyllus seeds used as spices in
African cuisine show antibacterial activity against Gram-positive bac­
teria and Gram-negative bacteria [16]. The paste of ground kernels of
Ricinodendron heudelotii is used to thicken soup and stew [17]. White
Piper nigrum, possesses non-negligible phytochemical and antioxidant
properties [18]. When spices are mixed properly, they play an important
role in the sensory viewpoint, by boosting a particular taste and flavor of
a meal. This establishes the relationship between spices and sensory
attributes [19]. Indeed the mixture of spices requires the determination
and use of the appropriate quantity of each entity because each spice
provides particular compounds that stimulate a particular sensory re­
ceptor [20].
The aim of this study was to determine the antioxidant properties of
spices widely used in the preparation of pepper soup beef hides in the
west Cameroon Region. Their combined effect as antioxidants on
selected pathogenic microorganisms was used to predict their effect as
food preservation agents.
2. Materials and methods
2.1. Materials
The biological materials used for this study were:
➢ Garlic (Allium sativum), Onion (Allium cepa), White pepper (Piper
nigrum), country onion (Afrostyrax lepidophyllus), and Djansang
(Ricinodendron heudelotii). These spices were bought from a local
market in Dschang, West Cameroon. All the spices used were chosen
based on a survey with housewives achieved by Maguipa et al. [13].
➢ The soups prepared from the formulations of spices mentioned
above, that were used in the sensory evaluation
➢ The spices formulations retained after the sensory evaluation
2
Journal of Agriculture and Food Research 8 (2022) 100293
2.2. Methods
2.2.1. Spices formulations for the preparation of different pepper soup beef
hides
Mean ratings of the spices or ingredients identified as important by
respondents were used to prepare the formulations. Quantification of
the proportions of these spices to properly situate the lower and upper
intervals for the mixture design was done during an investigation.
Sixteen (16) pepper soup spices formulations of varying proportions
were obtained by mixture design using Design Expert 12, were labelled
and defined as stated in (Table 2). In addition to the fundamental
constraint, the present study imposes upper and lower limits on each
spice (Table 1). These constraints have the effect of reducing the
experimental range of study. The proportions of ingredients used in
pepper soup beef hides preparation are given in Table 4 and for each
formulation, the sum of the component proportions was equal to a
hundred percent.
2.2.2. Sensory properties
2.2.2.1. Preparation of the pepper soup beef hides. The preparation of
pepper soup beef hides was done using five local ingredients and the
unit’s operations used in this process are expressed below:
For each formulation, 2 kg of beef hides, 1.5 l of drinking water, and
0.5 l of beef broth were used. Once the quantities in grams of the
powdered Piper nigrum, Afrostyrax lepidophyllus, Ricinodendron heudelotii
and the fresh Allium sativum and Allium cepa bulbs of the sixteen for­
mulations were weighed, the mixture of the ingredients was crushed and
the resulting product was used as a seasoning during cooking. After pre-
cooking beef hides, they were cut into smaller pieces and then washed.
For the preparation of pepper soup beef hides, the mixture of all the
inputs (ground mixed spices for seasoning, palm oil and smaller pieces of
beef hides) was done in a pot that contained water and cooked on a gas
stove for 30 min. At the end of the preparation, each soup was put in
small containers and then in vacuum flasks (thermos) to keep the soups
at the same temperature for the sensory evaluation.
2.2.2.2. Sensory evaluation of the pepper soup beef hides. Sensory eval­
uation was carried out on pepper soup beef hides samples. A total of
thirty (30) untrained panelists of men and women were recruited among
non-students and students of the University of Dschang in Cameroon. A
randomized complete block design was used whereby each panelist
evaluated all the samples prepared and this in one sensory session.
Panelists selection criteria were that they should be regular consumers
of beef hides and not present any allergy to beef hides-related foods.
Panelists were asked to evaluate flavor, color, consistency, odor, and
overall acceptability of the pepper soup beef hides. The consumer
expressed their degree of liking or disliking using the 9-point hedonic
scale ranging from “like extremely”: 9 to “dislike extremely”: 1. All
samples were labelled with a three-digit code when they were served in
a random sequence to panelists. During the evaluation, panelists were
provided water to rinse their mouths after every sample and were also
invited to freely fill the questionnaires given to them. In addition, they
were not to make comments during evaluation to influence other
panelists.
Table 1
Variables for the design of spice blends.
Variables quantities (g)
Minimum Maximum
Ricinodendron heudelotii 17 18
Piper nigrum 2 3
Allium sativum 25 27
Allium cepa 51 54
Afrostyrax lepidophyllus 1 2
T.C.L. Maguipa et al. Journal of Agriculture and Food Research 8 (2022) 100293

Table 2
Composition of spices formulations as generated by Design-Expert software.
Order of tests Formulations Code Components

Djansang (g) White pepper (g) Garlic (g) Onion (g) Country onion (g)

1 410 17.1 2 25.78 54 1.12

2 330 17 2 26.5 52.5 2
3 343 17.84 2.59 25 53.57 1
4 322 17.43 2.21 27 51.92 1.44
5 360 17.51 2.59 26.23 51.67 2
6 158 18 2 26.46 52.54 1
7 512 18 2 27 51 2
8 491 17 2.65 25 53.47 1.88
9 414 18 3 25 52 2
10 329 17.33 3 25.72 52.55 1.40
11 346 17.90 3 27 51.1 1
12 469 17.80 2 25 53.40 1.80
13 456 17 3 27 51 2
14 215 17 2.69 26.77 52.54 1
15 255 17.51 2.59 26.23 51.67 2
16 550 18 257 26.28 51.62 1.53

Table 3 Table 4
Mean sensory attributes of the formulated pepper soups beef hides. Proximate estimation of the retained formulations (% of dry weight).
Formulations Flavor Odor Consistency Color Overall Formulations Parameters
Code acceptability
Lipid Protein Ash Carbohydrate Moisture
410 4.63b 5.17b 5.17a ± 5.27a 5.37b ± 1.27 (%) (%) content (%) content
± 1.90 ± 1.23 0.99 ± 1.53 (%) (%)
330 4.83b 5.20b 5.30a ± 5.40a 5.30b ± 2.02
322 2.85 2.40 ± 4.94 ± 89.81 ± 0.47a 61.45 ±
± 2.00 ± 1.47 1.56 ±1.30
± 0.05a 0.32a 0.01a
343 4.03b 5.17b 5.03a ± 5.13a 5.07b ± 1.66
0.06a
± 1.81 ± 0.75 1.90 ± 1.57
491 3.21 1.99 ± 4.27 ± 90.53 ± 0.55a 70.69 ±
322 6.23a ± 6.37a 6.20a ± 5.70a 6.80a ± 1.42
± 0.15a 0.32a 0.20b
1.10 ± 1.00 1.10 ± 1.56
0.00b
360 4.03b 5.20b 5.13a ± 4.47a 5.07b ± 1.39
456 2.76 2.24 ± 4.30 ± 90.70 ± 0.22a 77.88 ±
± 1.58 ± 1.06 0.94 ± 1.81
± 0.05a 0.23a 0.43c
158 4.93b 5.17b 5.53a ± 5.40a b
5.27 ± 1.65
0.06a
± 1.74 ± 1.32 1.38 ± 1.28
512 4.80b 5.20b 5.53a ± 5.43a 5.23b ± 1.70 Values are means ± SD of triplicate determination. Formulations with different
± 1.65 ± 1.29 1.74 ± 1.77 superscripts in the same column were significantly different (p < 0.05).
491 6.17a ± 6.30a 6.23a ± 5.10a a
6.73 ± 0.94
1.26 ± 1.18 1.07 ± 1.40
414 4.57b 5.13b 5.17a ± 5.03a 5.00b ± 1.86 ⁃ The raw materials Allium sativum, Allium cepa, Piper nigrum, Afros­
± 1.85 ± 1.82 1.72 ± 1.81 tyrax lepidophyllus and Ricinodendron heudelotii were carefully
329 4.97b 5.20b 5.67a ± 5.37a 5.37b ± 1.27 selected manually. Piper nigrum, Afrostyrax lepidophyllus and Ricino­
± 1.88 ± 1.49 1.58 ± 1.87
346 4.73b 5.17b 5.87a ± 5.53a 5.40b ± 1.79
dendron heudelotii were sorted to remove debris, stones as well as
± 1.87 ± 1.37 2.01 ± 1.70 spoiled seeds.
469 4.47b 5.13b 5.20a ± 5.13a 5.20b ± 1.86 ⁃ After washing these seeds, they were dried at 45 ◦ C for 48 h and then
± 1.98 ± 1.54 1.42 ± 1.72 reduced to a powder for Piper nigrum, Afrostyrax lepidophyllus and a
456 6.33a ± 6.37a 6.20a± 1.00 5.50a 6.73a ± 1.17
paste in the case of Ricinodendron heudelotii.
1.35 ± 1.32 ± 1.48
215 4.73b 5.20b 5.83a ± 5.53a 5.27b ± 1.87 ⁃ Allium sativum and Allium cepa were later purchased from a market in
± 1.80 ± 1.80 1.91 ± 1.78 Dschang, fresh skins of Allium sativum and Allium cepa bulbs were
255 4.87b 5.20b 5.07a ± 4.90a 5.17b ± 1.84 peeled out, washed with distilled water to avoid product contami­
± 1.59 ± 1.21 1.53 ± 1.45 nation and sliced. Pieces of Allium sativum and Allium cepa were then
550 4.50b 5.17b 5.27a ± 5.20a 5.27b ± 1.55
± 1.61 ± 0.70 1.62 ± 1.83
ground in an electric blender to get a paste sample.
⁃ 100 g of individual spices were extracted separately with 1000 ml of
Values are mean ± SD of scores of 30 panelists. Formulations with different distilled water
superscripts within the same column were significantly different (p < 0.05).
⁃ Regarding the formulation of mixed spices, powdered samples of
Piper nigrum, Afrostyrax lepidophyllus, Ricinodendron heudelotii were
2.2.3. Proximate composition of the powdered formulations weighed, mixed to the ground mixture of Allium sativum and Allium
Analysis of formulations’ powders for lipid, protein, ash and mois­ cepa, and macerated in distilled water (1000 ml) at room tempera­
ture contents were determined according to standard AOAC methods ture for 48 h.
[21]. The carbohydrate content was determined by difference. ⁃ The individual and the formulation extracts were then centrifuged
(3000 rpm, 10 min) and filtered through a Whatman N◦ 1 filter paper.
2.2.4. Determination of phytochemical contents and biological activities The filtrate was stored at 4 ◦ C.
⁃ The different samples were subjected to various assays to determine
2.2.4.1. Aqueous extracts preparation from formulations of mixed spices the TPC, FC, antioxidant and antibacterial activities.
and their ingredients. The samples studied were prepared according to
their nature and were based on unit operations. 2.2.4.2. Phytochemical contents
2.2.4.2.1. Determination of total phenols contents (TPC). The amount

3
T.C.L. Maguipa et al.
of total phenol compounds was determined according to the
Folin–Ciocalteu’s method of Sumczynski et al. [22] with slight modifi­
cations. To 100 μl of the extract (100 mg/ml), were added 800 μl of
distilled water, and 100 μl of Folin–Ciocalteu reagent (10% v/v). After 3
min, 100 μl of 10% aqueous sodium carbonate were added. After 40 min
of incubation at 40 ◦ C, the absorbance was measured at 760 nm and
compared to a Gallic acid calibration curve. TPC was expressed as gallic
acid equivalent (GAE) in milligrams per gram (mg GAE/g) of a sample.
2.2.4.2.2. Determination of flavonoids content (FC). The FC was
determined by the method described by Marinova et al. [23] with some
modifications. In 2 ml Eppendorf tubes, 0.1 ml of each extract (100
mg/ml) was mixed with 0.15 ml of 5% sodium nitrite. After 5 min at
room temperature, 0.15 ml of 10% aluminium chloride solution was
added. After an additional 6 min, 1 ml of 1 M sodium hydroxide solution
was added to the reaction mixture and absorbance was read at 510 nm
against the blank after 15 min of incubation. The FC was expressed as
catechin equivalent in milligram per gram (mg CE/g) of extract by
referring to the catechin (0–2.5 mg/ml) standard curve.
2.2.4.3. Determination of antioxidant activities
2.2.4.3.1. Determination of free radical scavenging activity on DPPH
assay. The free radical scavenging activity was determined using the
method of Brand-Williams et al. [24] with some modifications. A stock
solution of DPPH was freshly prepared by dissolving 6 mg of DPPH in
100 mL of methanol. 800 μL of this solution was introduced into test
tubes containing 200 μl different concentrations (1.25–20 mg/ml) of the
sample or standard ascorbic acid. 200 μl of distilled water treated under
similar conditions served as a control. The absorbance was measured at
517 nm against the blank after 30 min at room temperature. The free
radical scavenging activity was calculated as percent of inhibition ac­
cording to the following formula:
%DPPH inhibition = (A0-A1/A0) × 100
Where, A0 is the absorbance of the control, and A1 is the absorbance of
the sample or standard.
The results were expressed as IC50 determined by the exponential
regression equation.
2.2.4.3.2. Determination of ferric reducing antioxidant power (FRAP).
The FRAP of the sample extracts was estimated following the procedure
of Benzie and Strain [25], with slight modifications. An aliquot of 0.1 ml
of variable concentrations (0.57–9.09 mg/ml) of the sample prepared in
distilled water was mixed with 0.25 ml of phosphate buffer (0.2 M, pH
6.6) and 0.25 ml of 1% aqueous K3Fe (CN)6 solution, well shaken, and
incubated at 50 ◦ C in a water bath for 30 min. Centrifugation of the
mixture was done at 3000 rpm for 10 min after adding 0.25 ml of 10%
trichloroacetic acid. A 0.5 ml aliquot of supernatant from each sample
mixture was mixed with 0.5 ml of distilled water and 0.1 ml of 0.1%
FeCl3 solution in a test tube. After homogenization, reading of the
absorbance was taken at 700 nm. A higher absorbance indicated a
higher reducing power. The results were expressed as ascorbic acid
equivalent in milligram per gram (mg AAE/g) of extract by referring to
the ascorbic acid (0–0.6 mg/ml) standard curve.
2.2.4.3.3. Determination hydroxyl radical scavenging activity
(HRSA). The scavenging activity of extracts on the hydroxyl radical was
determined by the slightly modified method described by Nagulendran
et al. [26].
In test tubes, 0.5 ml of 1 mM FeCl2, 0.75 ml of 1 mM 1,10-phenan­
throline, 2 ml of 0.2 M phosphate buffer (pH 7.8), 0.5 ml of 0.17 M
hydrogen peroxide and 0.5 ml of variable concentrations (0.625–10 mg/
ml) of sample were mixed and well shaken. After 30 min of incubation at
room temperature, the absorbance was read at 510 nm against the
blank. Ascorbic acid treated under similar conditions served as a stan­
dard. An increase in the absorbance indicated an increase reducing of
hydroxyl radical. The hydroxyl radical scavenging activity (HRSA) was
calculated by the following equation:
4
Journal of Agriculture and Food Research 8 (2022) 100293
HRSA (%)= (A0-A1/A0) × 100
Where, A0 is the absorbance of the control, and A1 is the absorbance of
the sample or standard. The results were expressed as IC50 determined
by the exponential regression equation.
2.2.4.4. Antimicrobial activity evaluation
2.2.4.4.1. Bacterial isolates and culture media. The antibacterial ac­
tivities of the different extracts were tested against MRSA, MSSA, Ver­
bizi, ENT, ECB, and SERB. These bacteria were maintained on Mueller
Hinton Broth at 4 ◦ C and cultured on fresh appropriate agar plates 24 h
at 37 ◦ C before any antimicrobial test. Mueller Hinton Agar was used to
activate bacteria. The Mueller Hinton Broth was used for the determi­
nation of the MIC.
2.2.4.4.2. Determination of minimum inhibitory concentration (MIC)
and minimum bactericidal concentration (MBC). The method developed
by Mishra and Padhy [27] was followed and some modifications were
made. The concentrations of the extracts against the bacterial isolates
used for MICs ranged from 0.391 to 50 mg/ml. In brief, 0.1 ml of freshly
constituted bacterial inoculum in the sterile MHB previously introduced
into a well of the 96 microplates and 0.1 ml of 50 mg/ml of spice extract
was added in the first well and mixed well with micropipette followed by
process of homogenization and dilution to obtain other concentrations.
The positive control consisted of Ciprofloxacin (0.25–32 μg/ml).
An inoculum of 100 μl (equivalent to a 0.5 Mc Farland standard) of
MRSA, MSSA, Verbizi, ENT, ECB, and SERB was added into each of the
wells. The triplicates of each microplate were made and the procedure
was repeated for each test organism. The plates were then placed in an
incubator set at 37 ◦ C for 24 h. After incubation 40 μl of 0.2 mg/ml of
iodonitrotetrazolium (INT) was added in each of the wells and the plates
were examined after an additional 30 min of incubation. Viable bacteria
reduced the yellow INT dye to pink. The lowest sample concentration
required to inhibit visible microbial growth of the tested microorganism
was designated as the MIC value. To determine MBC [27], 0.1 ml of
suspension was taken from microplate wells that demonstrated no
growth and inoculated on agar plates. After incubation at 37 ◦ C for 48 h,
the plates were examined. The lowest concentration of extracts that
exhibited no bacterial growth was used to determine the MBC.
2.2.5. Statistical analysis
The significance of differences was determined by one-way analysis
of variance (ANOVA) with Student Newman-Keuls Multiple comparison
modules of the GraphPad Instat statistical software, version 5.0. Sig­
maPlot 12 version 12.1.15c (Systat Software, Inc.) was used for the
analysis of exponential regression curves necessary for the determina­
tion of IC50. The differences were considered statistically significant at p
< 0.05. Correlation analyses were performed using Pearson’s correlation
coefficient (r).
3. Results and discussion
3.1. Sensory evaluation of pepper soups beef hides
The results of the sensory evaluation of the pepper soups beef hides
are presented in Table 3 allowed us to see the specificity of the soups
based on the panel’s appreciation. It was observed that the soups from
formulations 456, 322, and 491 had the highest sensory attributes than
other test samples and the ANOVA result revealed no significant dif­
ference among these three test samples on organoleptic attributes
(p˂0.05). Flavor, odor, consistency, and color are sensory characteristics
of foods that influence food acceptability [28]. These characteristics
specifically influenced the decision that consumers make regarding their
preference for a food substance [29]. In this study, tasters evaluated
sixteen beef hide soups with different ingredient proportions.
According to Jayasena et al. [30], the flavor attribute can be
T.C.L. Maguipa et al.
developed during cooking, complex reactions, and also by the quantity
and quality of spices used. Thus, the highest flavor scores noted for soups
from the three formulations could be due to the taste habit of the classic
soups. The significant variations noted between the flavor scores of
soups from formulations 456, 322, 491, and the rest of the formulations
could be due to the quantities of ingredients used. Indeed, Ekanem and
Achinewhu [31] reported that the essential oils contained in spices are
known for their aromatic and taste properties. These same authors and
also Hui et al. [32] mentioned that spices are used to enhance and
improve the flavor of foods.
Aroma is the nasal attraction that elicits consumer interest and
positive feelings about a food product. The high mean scores on the
aroma attribute for soups from formulations 456, 322, and 491 implied
that some spices could have produced some change in their aroma,
showing their acceptance by the panel members. However, no signifi­
cant difference (p > 0.05) noted between the attributes of the other
thirteen soups samples with the lowest ratings for odor, showed that the
tasters were not sensitive enough to detect differences between the
properties evaluated.
Although the use of spices in the preparation of soups is intended to
influence their flavor and odor as observed above, some could influence
their consistency such as Djansang. Given the small amounts used in the
spice formulations, no significant variation (p > 0.05) in the consistency
scores of all these soups.
Color is an indicator that could decide and influence consumer
choice. In addition, Ekanem and Achinewhu [31] reported that spices
are used to enhance the color of foods. In this study, color was judged
subjectively by the panel members based on their sense of sight and
given the small amounts of spices used in each formulation, a
non-significant difference in color preference of the different soups was
noted.
No significant (p > 0.05) difference was observed in the color and
consistency of the soups and this may be due to the spice blends resulting
in products that show the same level of preference for the characteristics
of these attributes. The results of the sensory analyses showed significant
differences in the flavor, taste, and overall acceptability of soups pre­
pared with different ingredients at different proportions. This could be
due to the concentration of ingredients used during cooking. Indeed,
Abisoye et al. [33] in their studies indicated, that phenolic compounds in
plants have health and nutritional benefits.
3.2. Proximate composition of formulations
In food systems, proximate analysis allows the quantitative analysis
of the different macronutrients found in a food product. In the present
study, the results of the proximate composition of the three retained
formulations are shown in Table 4. The moisture content ranged from
61.45 to 77.88% for formulations 322 and 456 as lowest and highest
respectively.
Also, the moisture content of all the three formulations showed a
significant difference (p < 0.05). Fresh onion and garlic have a high
amount of water; therefore, the high moisture contents of the samples
could be due to their use as they are fresh. The lipid content ranged from
2.76 to 3.21% with formulation 491 having the highest value. There was
a significant difference (p < 0.05) in the lipid content of these formu­
lations and it can be due to the varied quantity of species used. Since the
spices are rich in essential oils [34], lipid content noted in this study
shows the spices used in these formulations are good sources of flavor.
Dietary fats function in the increase in food’s palatability, by absorption
and retention of flavors. Indeed, a diet that can provide 1–2% of calorific
energy as fat is sufficient to humans since its excess is implicated in some
cardio-vascular ailments and ageing [35]. No significant differences
were observed for protein contents, even though formulations 322 and
456 presented higher values than formulation 491. In terms of total
carbohydrate content, no significant differences were observed between
formulations. Minerals are vital to the functioning of many physiological
5
Journal of Agriculture and Food Research 8 (2022) 100293
processes and play an important role in the living systems [36]. The ash
contents were not significantly different (p < 0.05) in the formulations,
the content ranged between 4.30% and 4.94%.
3.3. Total phenol and flavonoid contents
TPC and FC of aqueous extracts of Allium sativum, Allium cepa, Piper
nigrum, Afrostyrax lepidophyllus, and Ricinodendron heudelotii, and the
formulations (322, 456 and 491) are presented in Table 5. The results
showed that TPC and FC were significantly different (p˂0.05) in all with
values ranging from 29.92 to 249.44 mg GAE/g and from 2.01 to 15.35
mg CE/g for the TPC and FC respectively.
The extract of Afrostyrax lepidophyllus showed the highest TPC
(249.44 ± 0.08 mg GAE/g) and FC (10.92 ± 0.38 mg CE/g). The TPC of
Afrostyrax lepidophyllus extract found in this study is greater than that
found by Sokamte et al. [16]. They found that the TPC of the methanolic
extract of the seeds of Afrostyrax lepidophyllus was 160.77 mg GAE/g.
This difference could be due to different solvents extraction used.
Concerning the other spices, the decreasing ranking order for TPC
and FC was Ricinodendron heudelotii > Piper nigrum > Allium sativum >
Allium cepa. The results obtained for the TPC in this study with Allium
sativum (59.44 mg GAE/g fresh weight) were slightly higher than those
reported by Kohole Foffe et al. [37] (54.28 mg GAE/g extract) on water
extract. The TPC of Allium sativum found here was equally greater than
those reported by Womeni et al. [38] on methanolic extract with a value
of 1.34 mg GAE/g extract. This difference could be the result of the
solvent used for extraction. The variation in TPC and FC observed in this
work might be due to genotypic and environmental differences, deter­
mination methods, and the type of solvent used for extractions [39].
When these spices were mixed in variable proportions, an increase in
these contents was observed. Results showed that the amount of TPC and
FC of the aqueous extract from formulations 491 and 456 were higher
compared to formulation 322 and its ingredients except Afrostyrax lep­
idophyllus in the amount of TPC. This was probably due to the individual
contribution of each ingredient or spice in each formulation. An increase
in total phenolic and flavonoid contents in these formulations could also
be due to some chemical reactions during the mixing or blending pro­
cess, as reported by Seah et al. [40]. From observations, it was noticed
that the color and flavor of the mixed ingredients or spices changed
during the production of the formulations, thus confirming the occur­
rence of a chemical reaction. The highest TPC and FC were found in the
aqueous extract from formulation 491 (118.65 mg GAE/g spice powder
and 15.35 ± 0.04 mg CE/g respectively) followed respectively by
aqueous extracts of spices’ mixtures from formulations 456 and 322. In
agreement with the literature, the interactions between the phenolic
compounds and other constituents found in the other spices [41] could
explain these results. Moreover, phenolic compounds belong to different
classes which react differently [41].
Table 5
TPC and FC of individual spices and their mixture from three formulations.
Samples TPC (mg GAE/g) FC (mg CE/g)
Allium sativum (WM) 59.44 ± 0.33 a
2.01 ± 0.08a
Allium cepa (WM) 29.92 ± 0.03b 1.94 ± 0.11a
Afrostyrax lepidophyllus (DM) 249.44 ± 0.08c 10.92 ± 0.38a
Ricinodendron heudelotii (DM) 76.43 ± 0.07d 10.17 ± 0.07b
Piper nigrum (DM) 62.78 ± 0.02e 2.69 ± 0.35c
Formulation 322 (DM) 50.87 ± 0.03f 10.54 ± 0.31d
Formulation 491 (DM) 118.65 ± 0.04g 15.35 ± 0.19e
Formulation 456 (DM) 100.32 ± 0.05h 15.07 ± 0.03f
Values are means ± SD of triplicate determination. Samples with different su­
perscripts in the same column were significantly different (p < 0.05). WM:Wet
Matter; DM:Dry Matter; GAE: gallic acid equivalent CE: catechin equivalent.
T.C.L. Maguipa et al. Journal of Agriculture and Food Research 8 (2022) 100293

3.4. Antioxidant activities Table 6

Antioxidant activities of aqueous extract expressed in IC50 and mg AAE/g
Several mechanisms are often used to evaluate the antioxidant ac­ extract.
tivities of a substance or a complex mixture. DPPH, FRAP, and HRSA Samples IC50(mg/ml) (mg AAE/g extract)
tests were used to evaluate the antioxidant potential of aqueous indi­ DPPH HRSA FRAP
vidual spice and their mixture.
Formulation 322 5.70 ± 0.03a 0.59 ± 0.06a 0.89 ± 0.10a
Formulation 491 4.14 ± 0.05b 0.39 ± 0.07b 1.45 ± 0.14b
3.4.1. DPPH radical scavenging activity Formulation 456 5.08 ± 0.04c 0.94 ± 0.15c 1.02 ± 0.13a
DPPH is widely used to determine the antioxidant activity of foods Afrostyrax lepidophyllus 7.27 ± 0.08e 1.91 ± 0.1d 0.82 ± 0.12a
[42]. Fig. 1 presents the results of free radical scavenging activity in Allium sativum 8.52 ± 0.03f 2.02 ± 0.04d 0.63 ± 0.07a
percentage inhibition. It showed that all the extracts act in a Allium cepa 5.08 ± 0.02c 5.46 ± 0.13e 0.67 ± 0.03a
Ricinodendron heudelotii 3.91 ± 0.04h 2.89 ± 0.13f 0.97 ± 0.14a
concentration-dependent manner. The percentage of inhibition of the Piper nigrum 4.14 ± 0.07b 3.01 ± 0.11f 0.39 ± 0.09a
control ascorbic acid was higher than that of the aqueous extracts of Ascorbic acid 3.13 ± 0.03d 0.23 ± 0.11b ND
individual spices and formulations for all concentrations. The latter have
Samples in the same column with different superscripts were significantly different (p
inhibition percentages higher than 50% at concentrations 10 and 20
< 0.05). ND: Not Determined; 322, 491, 456 are various codes of retained formu­
mg/ml. Table 6 showed the antioxidant activities of aqueous extracts lations. AAE: ascorbic acid equivalent; IC50: Half maximal inhibitory concentration.
studies. From this table, the IC50 values of the known antioxidant:
ascorbic acid, was least (3.13 mg ml-1) followed by Djansang (Ricino­
dendron heudelotii) (3.91 mg/ml). These spices hence exhibited the
highest antiradical activity, compared to other individual spices ex­
tracts: country onion (7.27 mg/ml) and garlic (8.52 mg/ml) that had
higher IC50 values and therefore lowest antioxidant activity. These re­
sults corroborate those of Nuutila et al. [43] who reported the lowest
antioxidant activity on methanolic extract of the garlic.
Concerning, spices’ mixtures, aqueous extracts from formulations
491 (4.14 mg/ml) and 456 (5.08 mg/ml) with lower values of IC50,
showed the highest in DPPH activities, compared to aqueous extract
from formulation 322 (5.70 mg ml-1). These results could be attributed
to the high activity of the active compounds and/or the synergistic ac­
tion of different chemical compounds present in the spices and their
mixture. However, the highest phenol content and antioxidant activity
were observed in aqueous extracts from formulations 456 and 491, and
Fig. 2. Reducing power activity of ascorbic acid, spices, and its mixtures at
it could find its application as a powerful free radical scavenger.
different concentrations.

3.4.2. Ferric reducing antioxidant power (FRAP)

with free radicals to convert them to more stable products. Even
The FRAP assay measures the antioxidant effect of any substance in
reducing power activity in several plant extracts was recorded by
the reaction medium as its reducing ability [44] and was commonly used
Rice-Evans et al. [46]; Amarowicz et al. [47]; Pérez-Pérez et al. [48];
to study the antioxidant capacity of plant materials [45]. The antioxi­
Manian et al. [49]; Sen et al. [50]; Mannan et al. [51], and they have
dant potential of individual spices and their mixtures was estimated
been linked to the polyphenolic constituents of these extracts. The
from their ability to transform of Fe3+ to Fe2+ by electron-donating.
reducing power of extracts varied significantly (p < 0.05) and the
FRAP activity of spices in comparison to ascorbic acid is presented in
aqueous extract of spices’ mixture from formulations 491 (1.45 ± 0.14
Fig. 2. The results showed that the FRAP activity is
mg AAE/g) showed highest activity, followed respectively by 456 (1.02
concentration-dependent. The FRAP values estimated in milligrams of
± 0.13 mg AAE/g) and 322 (0.89 ± 0.10 mg AAE/g). Among, the
ascorbic acid equivalents/g spice powder was used to compare the
aqueous extract of the individual spices, the highest FRAP activity was
antioxidant capacity (Table 6). At all concentrations, all aqueous ex­
observed with Djansang (Ricinodendron heudelotii) (0.97 ± 0.14 mg
tracts studied has presented less antioxidant activity than the reference
AAE/g) and Country onion (Afrostyrax lepidophyllus) (0.82 ± 0.12 mg
used (ascorbic acid). Indeed, these extracts could be potent enough to
AAE/g). The lowest FRAP activity (0.39 ± 0.09 mg AAE/g) was
function as a good electron and hydrogen-atom donor which could react
observed in the Piper nigrum. In comparison with this study, Devi et al.
[52] indicated a poor FRAP activity. The highest value of FRAP activity
observed in the aqueous extract of spices’ mixture from formulations
may be due to the presence of hydroxyl group of phenolic compounds
such as flavonoids [44]. This high antioxidant activity of these aqueous
extracts could be attributed to their content of phenolic compounds and
flavonoids, which are bioactive compounds naturally found in plants
and are very important for human health [53]. Since antioxidants were
considered as reducers and inactivators of oxidants [44], then the
reducing power of each extract studied could depend on the quantity of
Iron (II) produces in the reaction medium.

3.4.3. Hydroxyl radical scavenging activity (HRSA)

Hydroxyl radicals are the most reactive oxygen species, causing lipid
oxidation and enormous biological damage. They are potent cytotoxic
agents, able to attack biological molecules such as proteins, DNA, and
polyunsaturated fatty acids in membranes [54]. Fig. 3 shows the inhi­
Fig. 1. DPPH free radical scavenging assay of ascorbic acid, spices, and
bition of the production of the HRSA from aqueous extracts at variable
its mixtures.

6
T.C.L. Maguipa et al. Journal of Agriculture and Food Research 8 (2022) 100293

is similar to the results previously reported by Refs. [59,60] that there is

no direct correlation between TPC and antioxidant activity. Moreover,
no significant correlation was also observed between the TPC and FC for
the DPPH test.

3.5. Antimicrobial activity of aqueous extracts of three formulations of

spice mixture and its ingredients

The MIC and MBC values of the aqueous extracts presented in Table 8
indicate that all the aqueous extracts analyzed had antibacterial effects
depending on the bacterial isolates applied. The reference antibiotic
ciprofloxacin tested showed higher antibacterial activity than the
different extracts studied. In general, we noted that the MIC values for
all the aqueous extracts were in the range of 3.125–50 mg/ml. It
Fig. 3. Hydroxyl radical scavenging activity of ascorbic acid, spices, and its
mixtures at different concentrations. appeared from the analyses that, the aqueous extracts of garlic, country
onion, and white pepper showed a stronger antibacterial activity against
MSSA with MIC values of 25 mg/ml, compared to MIC value of 50 mg/
concentrations compared to that of ascorbic acid respectively. Ascorbic
ml of these same extracts against MRSA, Verbizi, ECB and SERB. For the
acid (70.77%) activity was higher than that of aqueous extracts of spices
aqueous extracts of onion and Djansang, MICs of 50 mg/ml were ob­
mixture from formulations (322, 491, and 456) and the individual
tained on all isolates tested. In addition, extracts from formulations 456
spices. All the extracts showed more than 50% inhibition of hydroxyl
and 491 showed higher antibacterial activity than that of formulation
radicals at a concentration of 10 mg/ml (Fig. 3). The aqueous extracts of
322 Thus, extract from formulation 456 exerted high activities against
spices mixture from the three formulations showed higher activity than
MRSA, ENTB, Verbizi, ECB, and SERB with MIC values of 3.125 mg/ml,
the aqueous extracts of individual spices with a percentage inhibition of
12.5 mg/ml, 25 mg/ml and 25 mg/ml respectively. Extract from
62.45, 67.31, and 68.52, respectively at 10 mg/ml, which could suggest
formulation 491 was more active on MRSA and Verbizi with MIC value
that these extracts could function as an excellent scavenger of HRSA.
of 25 mg/ml than on MSSA, ENTB, ECB, and SERB (50 mg/ml). The
The HRSA of an extract was found to be in the order of 491 > 322>456
results of the study are similar to the work of Ankri and Mirelman [61]
for the studied extracts. Hydroxyl radical scavenging activity from for­
who showed that the plant extracts inhibited the bacteria tested to
mulations 491 and 322 extracts was higher than from formulation 456
varying degrees. Overall, strong antibacterial activities were noted with
extract (Table 6). However, hydroxyl radical scavenging activity from
the aqueous extracts of garlic, country onion, pepper (against MSSA),
formulation 322 extract showed a different pattern with different
and aqueous extracts of spice mixtures of formulations 456 (against
methods used such as DPPH and FRAP. It is interesting to mention that,
MRSA, ENTB, Verbizi, ECB, and SERB) and 491 (against MRSA and
antioxidant activity varied depending on the methods used [55,56] and
Verbizi). These results showed that the antimicrobial efficacy of an
each method has its limitation [55]. The IC50 value for the 491-formula­
extract is not always proportional to its phenolic compounds content but
tion extract was 0.39 ± 0.07 mg/ml, while for aqueous extract indi­
could depend on its nature. They could also be due to the synergistic
vidual spices was >1.50 mg/ml. Since the spices are used to impart
interaction that could exist between the bioactive phytochemicals pre­
flavor to the food, they are also known to exert their effect on lipid
sent in the extracts, which would give rise to greater antimicrobial
peroxidation by scavenging reactive oxygen species. So, these results
activity.
suggest that the extracts from formulations studied could possess po­
Once the MICs and MBCs are determined for the aqueous spice ex­
tential health benefits by inhibiting lipid peroxidation.
tracts as well as their mixture, the MBC/MIC ratio was calculated
(Table 9). The results revealed that this ratio is indeterminate for sam­
3.4.3.1. Relationship between assays. The analysis of the correlation
ples tested with MBCs above the initial stock solution concentration of
between antioxidant activities (DPPH, HRSA, and FRAP) and TPC and
100 mg/ml except for ciprofloxacin tested at 0.032 mg/ml. The aqueous
FC were carried out for all spices’ extracts (Table 7). Negatively high
spice extract with bactericidal effect is garlic because it has an MBC/
correlation was found between FC (r = -0.7387, p < 0.05) and HRSA. It
MIC = 1 ratio for the MSSA isolate. The bactericidal effect of the aqueous
demonstrated that increasing in FC caused decreasing in HRSA. More­
garlic extract (MBC/MIC = 1) only on MSSA, would be due to the allicin
over, a negative correlation could suggest that phenolic compounds and
that was derived from alliin under the action of the alliinase enzyme
more particularly flavonoids play a key role in the inhibition of HRSA in
during the crushing of garlic bulbs. The same findings were recorded by
different systems. This agrees with the results of Liu et al. [57] who
Cavallito and Bailey [62] who attributed the antimicrobial potential of
reported a negative correlation between FC and antioxidant activity. A
the allicin contained in the garlic. The results obtained for garlic extract
positively strong correlation was detected between FRAP values and FC
are inferior to those of Tagoe and Gbadago [63] reported that aqueous
(r = 0.8612, p < 0.05), indicating the implication of total flavonoids in
garlic extract had strong antimicrobial activity on Salmonella and
the donation of electrons. This result is consistent with the work of
Shigella with MICs of 150 and 50 mg/ml respectively. No bactericidal
Liazid et al. [58] who also observed a strong correlation between anti­
activity was recorded for the other aqueous extracts against the bacteria
oxidant activity and flavonoids. However, analysis between TPC and
tested.
antioxidant activity (DPPH, FRAP, and HRSA) was not significant. This
4. Conclusion
Table 7
Correlation coefficient (r) between antioxidant activities (DPPH, HRSA, and Findings in this study showed that soups issued from formulations
FRAP) and total flavonoids and total phenol for the aqueous extracts. 456, 322, and 491 were the most preferred in terms of flavor, odor,
consistency, color, and overall acceptability. The data showed that all
Antioxidant test Total flavonoids Total phenol
individual spices used in the formulations contained TPC and FC, with
r P-value r P-value
varying amounts of antioxidant activities. The aqueous extracts from
DPPH -0,2931 0,4810 0,0975 0,8184 formulations 456 and 491 showed very high levels of TPC, FC, DPPH,
FRAP 0,8612 0,0060 0,5110 0,1730 FRAP and HRSA scavenging activities. A positive and a negative rela­
HRSA -0,7387 0,0363 -0,5338 0,1956
tionship between flavonoid and antioxidant content FRAP and HRSA

7
T.C.L. Maguipa et al. Journal of Agriculture and Food Research 8 (2022) 100293

Table 8
MIC and MBC values of spice extracts and their mixture (mg/ml)).
Samples MRSA MSSA Verbizi ENTB ECB SERB

322 MIC 50 50 50 50 50 50
MBC >50 >50 >50 >50 >50 >50
491 MIC 25 50 25 50 50 50
MBC >50 >50 >50 >50 >50 >50
456 MIC 3125 50 25 12,5 25 25
MBC >50 >50 >50 >50 >50 >50
Country onion MIC 50 25 50 50 50 50
MBC >50 >50 >50 >50 >50 >50
Garlic MIC 50 25 50 50 50 50
MBC >50 50 >50 >50 >50 >50
Onions MIC 50 50 50 50 50 50
MBC >50 >50 >50 >50 >50 >50
Djansang MIC 50 50 50 50 50 50
MBC >50 >50 >50 >50 >50 >50
White Pepper MIC 50 25 50 25 50 50
MBC >50 >50 >50 >50 >50 >50
Ciprofloxacine MIC 0,0005 0,00025 0,00025 0,001 0,0005 0,0005
MBC 0,00025 0,00025 0,00025 0,00025 0,00025 0,00025

MRSA: Methicillin-resistant Staphylococcus aureus, MSSA: Methicillin-susceptible Staphylococcus aureus; Verbizi Enterobacter cloacae ENT: Shigella flexieri ECB: Escherichia
coli; SERB: Salmonella typhi.

on Bananas and Plantains (CARBAP) Dr NGOH NEWILAH Gérard, for

Table 9
granting us access to his lab. They would also like to acknowledge
Determination of the MBC/MIC ratio of aqueous spice extracts and their
KENDINE VEPOWO Cédric, TANGA MEKUIKO Germaine and DJUKAM
mixture.
CHOYEP Ange for proofreading and reviewing this article.
Samples MRSA MSSA Verbizi ENTB ECB SERB

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