Akure, Нигерия
Introduction. Diabetes is a common disease all over the world that is often a cause of mortality. Ice cream is popular in many countries. However, sugar and fat in its composition makes ice cream a high-caloric product. Soursop (Annona muricata L.) and moringa (Moringa oleifera L.), African medicinal plants, contain natural sugars and are rich in phytochemicals. We aimed to produce ice cream with these plants and evaluate its remedial properties. Study objects and methods. The study featured ice cream purchased in a local store (control sample) and soursop ice cream with moringa leaf powder (experimental samples). The experimental ice cream samples included ice cream with soursop, ice cream with soursop and 0.1 g of moringa, and ice cream with soursop and 1 g of moringa. The antioxidant properties, glycemic indices, amylose and amylopectin contents, as well as α-amylase and α-glucosidase inhibitory properties of the samples were determined using the standard methods. Results and discussion. Comparing with the other samples, ice cream with 1 g of moringa showed the highest total phenol and flavonoid contents, ABTS scavenging ability, DPPH radical scavenging ability, hydroxyl scavenging ability, ferric reducing antioxidant properties, and lowest glycemic index. Sensory evaluation revealed a lower overall acceptability of the experimental samples compared to the control ice cream. This could be due a peculiar taste of moringa (the formulation did not include sugar). Conclusion. Ice cream based on soursop and moringa can be a good alternative to sugar-sweetened ice cream due to its antioxidant properties, low glycemic index, and acceptable sensory attributes.
Ice cream, diabetes, antioxidant properties, glycemic index, phenolic compounds, α-amylase, α-glucosidase
INTRODUCTION
The World Health Organization reported that by
2035 the number of people with diabetes, a major cause
of mortality worldwide, will account for 471 million [1].
Cheap snacks and products with high energy content are
risk factors in diabetes development [2, 3]. One of the
most popular high energy snacks is ice cream, which
mainly contains milk or cream and sugar. Ice cream is
a homogenized mixture of milk, flavorings, colorings,
and stabilizers frozen at the temperature that is lower
than the freezing point to avoid the formation of large ice
crystals.
There are many varieties of ice cream, but generally
ice cream contains 10% of milk fat, less than 10%
of non-milk fat (caseins, whey proteins, lactose),
13–20% of sweeteners, 0.1–0.7% of stabilizers and
emulsifiers, and about 64% of water [4]. Ice cream
has become a popular product due to its cooling
properties and the enormous amount of energy it
supplies. However, a high amount of carbohydrates
fats in ice cream can increase bad cholesterol
deposition around the belly and have become one
of the leading causes of obesity and such diseases
as diabetes, atherosclerosis, and hypertension [5].
All these diseases caused by ice cream consumption
have been found to result from excess energy deposition,
which is a central factor to hyperglycemia. Despite a
high demand for ice cream, there has been little effort to
improve its nutritional and medicinal properties. Hence,
there is a need to develop functional ice cream without
the mentioned disadvantages which would treat a wide
array of metabolic diseases.
Herbs are widely available, effective, safe, and
acceptable raw materials which can be used as
functional plants in the food industry [6]. Various types
of plants that have been used in the treatment of heart related diseases have shown promising therapeutic
potential. Soursop (Annona muricata L.) is a tropical
plant popular in ethnomedicine due to its antioxidant
properties [7]. Soursop is rich in phytochemicals such
as flavonoids, phenolic acids, phytosterols, saponins,
and cardiac glycosides [7, 8]. Moringa oleifera L.
(Moringaceae family) is a fast growing plant of
economic and medical importance widely distributed
in Africa, America, and Asia [9–11]. Some of the
phytochemicals present in moringa leaf, which have
medicinal potential, are mainly natural antioxidants
such as flavonoids, carotenoids, vitamins, and phenolic
acids [12–17].
Therefore, this study aimed to produce soursopbased
ice cream enriched with moringa leaf powder and
then assess its antioxidant properties, glycemic index,
amylose and amylopectin contents, as well as α-amylase
and α-glucosidase inhibitory properties.
STUDY OBJECTS AND METHODS
Soursop (Anona muricata L.) and moringa (Moringa
oleifera L.) leaves were collected from the botanical
garden at the Federal University of Technology, Akure.
The moringa leaves were washed, air dried, and finely
powdered using a stainless steel blender. The powdered
samples were kept dry at room temperature for further
analysis.
The soursop was peeled and seeds were separated
from the pulp. Whipping cream (600 g) was stirred for
15 min using a mixer. Thereafter, 600 g of the soursop
pulp was mixed together with the whipping cream
for another 15 min. The mixture was divided into
three parts and frozen (Fig. 1). This produced three
experimental samples of soursop-based ice cream: with
no moringa, with 0.1 g of moringa, and with 1 g of
moringa. Ice cream purchased at a local store served as
control.
Sensory analyses were conducted in well illuminated
odorless laboratory booths. Water was provided for
mouth rinsing in between successive evaluation. Sample
attributes (color, texture, taste, aroma, etc.) were rated
from 1 to 7, where 1 = very poor and 7 = excellent.
Panelists made their responses on score sheets which
were designed in line with the test procedures [18].
The total phenol content was determined according
to the method reported by Singleton et al. and calculated
as gallic acid equivalent (GAE) [19].
The total flavonoid content was determined
using a slightly modified method reported by Meda
et al. [20]. The absorbance of the reaction mixture
was subsequently measured at 415 nm, and the total
flavonoid content was subsequently calculated.
DPPH free radical scavenging ability was evaluated
as described by Gyamfi et al. [21]. Ice cream samples
(0.05 mL) were incubated in the dark for 30 min with
1 mL of 0.4 mM DPPH after thorough mixing. The
absorbance was measured at 516 nm, and the radical
scavenging ability was subsequently calculated as
percentage of the control.
ABTS radical scavenging ability was determined
according to the method described by Re et al. [22].
The radicals were generated by adding 7 mmol/L ABTS
aqueous solution to a reaction mixture containing
2.45 mmol/L K2S2O8, keeping in the dark for 16 h,
and adjusting the absorbance to 0.700 with ethanol at
734 nm. 0.2 mL of appropriate dilution of the ice cream samples was added to 2.0 mL of ABTS solution
and absorbance was measured at 734 nm after 15 min.
The radical scavenging ability and Trolox equivalent
antioxidant capacity were subsequently calculated.
Ferric reducing antioxidant property of the samples
was determined by assessing its ability to reduce FeCl3
solution as described by Pulido et al. [23]. The reducing
property was subsequently calculated using ascorbic
acid equivalent.
Hydroxyl radical scavenging ability was determined
using the method of Halliwell and Gutteridge [24]. The
reaction mixture contained 1–100 μL of the ice cream
samples, 400 μL of 0.1 M phosphate buffer, 120 μL of 20
mM deoxyribose, 40 μL of 20 mM hydrogen, and 40 μL
of 500 M FeSO4. The mixture was incubated at 37°C for
30 min. Thereafter, 0.5 mL of 2.8% TCA (trichloroacetic
acid) and 0.4 mL of 0.6% TBA (thiobarbituric acid)
solution were added. The tubes were subsequently
incubated in boiling water for 20 min. The absorbance
was measured at 532 nm using a spectrophotometer.
α-amylase activity assay. The reaction mixture
contained the sample dilution (500 μL) and 0.5 mg/mL
α-amylase in 500 μL of 0.02 M sodium phosphate buffer
(pH 6.9 with 0.006 M NaCl). The mixture was incubated
for 10 min at 25°C. 500 μL of a 1% starch solution in
0.02 M sodium phosphate buffer (pH 6.9 with
0.006 M NaCl) was then added to the reaction
mixture and incubated for another 10 min at 25°C.
Dinitrosalicylic acid (DNSA) was used to stop
the reaction before incubating for 5 min at room
temperature. Absorbance was measured at 540 nm, and
the percentage enzyme inhibitory was calculated [25].
The α-glucosidase inhibitory activity was
determined by the method of Apostolidis et al. [26].
The reaction mixture contained 100 μL of α-glucosidase
solution (EC 3.2.1.20; 1.0 U/mL) in 0.1 M phosphate
buffer (pH 6.9). Ice cream samples (50 μL each) were
put in the mixture and incubated at 25°C for 10 min.
50 μL of 5 mM pnitrophenyl-α-D-glucopyranoside
solution was added, and the reaction mixture was
incubated for 5 min at 25°C. The absorbance was read at
405 nm.
Glycemic index and starch hydrolysis rate in vitro
were determined according to the method of Goni
et al. [27]. Each ice cream sample (50 mg) was incubated
with pepsin (1 mg) in 10 mL of HCl-KCl buffer
(pH 1.5) at 40°C for 60 min. 2.5 mL of phosphate buffer
(pH 6.9) and 5 mL of α-amylase solution were added to
the reaction mixture. The mixture was incubated at 37°C
in a shaking water bath. To activate the enzyme, we
were taking 0.1 mL of the mixtures every 30 min during
three hours and boiled. The residual starch was digested
to glucose by the addition of 3 mL of α-glucosidase and
incubated at 60°C for 45 min. The glucose concentration
was assayed by the addition of 200 mL of DNSA. After
stopping the reaction by boiling, 5 mL of distilled water
was added and absorbance read at 540 nm.
To determine amylose-amylopectin content, 1 mL of
95% ethanol and 9 mL of 1 N NaOH were added to in
volumetric flasks containing 100 mg of each ice cream
sample. Thereafter, the reaction mixture was heated in
boiling water for 10 min. 1 mL of 1 N acetic acid and
2 mL of iodine solution were added to 5 mL portion of
the solution. After thorough shaking, the absorbance was
measured at 620 nm. Amylopectin content was derived
from the difference between the starch and amylose
contents [28, 29].
Statistical analysis. The results were expressed
as mean ± standard deviation (SD). One-way analysis
of variance (ANOVA) was used to analyze the results
followed by Turkey’s post hoc test, with levels of
significance accepted at P < 0.05.
RESULTS AND DISCUSSION
The results of the sensory evaluation of the control
(commercial ice cream) and experimental (soursopbased
ice cream enriched with moringa leaf powder)
samples are presented in Table 1. The control ice
cream had higher overall acceptability compared to the
soursop-based ice cream samples. The experimental
samples had no significant differences in their overall
acceptability.
Aroma, taste, color, flavor, texture, and general
acceptability of food have a significant effect on its
sensory quality, which is one of the major criteria
in food selection by consumers [30]. The overall
acceptability and aroma of the soursop-based ice cream
was not significantly different. However, moringa
leaf powder reduced such attributes as texture, taste,
and color. The ice cream samples with moringa
demonstrated reduced acceptability, which could be due
to a peculiar taste of moringa leaf powder (no sugar in
the formulation).
The soursop-based ice cream had a high amount of
phenolic and flavonoid content compared to the control
Table 1 Sensory attributes of soursop-based ice cream enriched with moringa leaf powder
Ice cream Texture Taste Color Aroma Overall acceptability
Commercial ice cream (control) 6.09 ± 0.04a 6.11 ± 0.03a 6.12 ± 0.07a 6.21 ± 0.04a 6.25 ± 0.05a
SS 5.37 ± 0.08b 5.89 ± 0.04b 5.92 ± 0.11a 5.91 ± 0.04b 5.82 ± 0.03b
SS + MLP (0.1 g) 5.11 ± 0.03c 5.71 ± 0.03c 5.71 ± 0.06b 5.82 ± 0.03b 5.78 ± 0.05b
SS + MLP (1g) 4.95 ± 0.04d 5.28 ± 0.04d 5.05 ± 0.07c 5.79 ± 0.06b 5.79 ± 0.04b
SS – soursop
MLP – moringa leaf powder
sample (Table 2). Our results consistent with the data
by Tungmunnithum et al. who studied phenolics and
flavonoids in medical plants [31]. The authors found
that these compounds are responsible for the biological
activity of the plants. Phenolic compounds, especially
flavonoids, are remarkable antioxidants which have
been widely researched for their medicinal properties
against various diseases. Phenolic compounds are good
iron chelators which scavenge free radicals, preventing
oxidative stress [32]. In this study, the sample with
moringa leaf powder (1 g) showed the highest total
phenol and flavonoid content compared to the other
samples.
Figure 2 demonstrates that the ice cream with
moringa leaf powder (1 g) had the highest DPPH
scavenging ability at all the concentrations (100–
400 mg/mL) among all the samples. Also, this ice cream
sample showed the highest ABTS scavenging ability
compared to the other samples (Fig. 3). The control ice
cream sample had the lowest both DHHP and ABST
scavenging activities.
The highest ferric reducing antioxidant properties
and hydroxyl radical scavenging ability belonged to
the experimental sample with moringa leaf powder
in the amount of 1 g (Figs. 4 and 5). Among the other
samples, these parameters decreased from ice cream
with moringa leaf powder (0.1 g) to the control sample
(without soursop and moringa powder).
Reducing property of the samples was assessed
based on their ability to reduce Fe3+ to Fe2+. The results
revealed that the control ice cream had significantly
lower reducing property compared to the soursop-based
samples. Similarly, the ice cream with 1 g of moringa
exhibited the highest hydroxyl radical scavenging ability
compared to the other soursop-based samples, while the
hydroxyl radical scavenging ability of the control ice
cream was comparably low.
The antioxidant properties of the sour-sop based ice
cream samples was directly proportional to increasing
moringa leaf powder proportion (Figs. 2–5). Therefore,
the antioxidant properties can be linked to phenolic
compounds that majorly present in the moringa and
the soursop. Furthermore, the ability of the samples to
scavenge DPPH radical could be due to the presence of
multiple hydroxyl groups in phenolic compounds, which
are able to donate their protons to finally break the chain
reaction of the free radicals [32].
ABTS is a water soluble free radical initiator that is
oxidized to form a stable green radical ABTS+ in the
presence of reactive oxygen [33]. All the soursop-based
ice cream samples exhibited a remarkable ABTS radical
scavenging ability, with the highest radical scavenging
ability in the sample containing 1 g of morings leaf
powder. This could also be explained by synergistic
effects of phenolic compounds present in moringa and
soursop [34, 35]. These results prove that moringa and
soursop increased the antioxidant properties of the
ice cream samples due to phenolic compounds in their
compositions. The correlation between antioxidant
properties and phenolic content has been established for
many food products [36].
The effect of moringa and soursop on the α-amylase
and α-glucosidase inhibitory activity of the ice cream
samples are presented in Figs. 6 and 7. The sample
with 1 g of moringa leaf powder showed the strongest
inhibition of α-amylase activity at the concentrations
tested (50–200 mg/mL) and the highest α-glucosidase
inhibitory ability compared to the other soursop-based
samples. The control sample demonstrated the lowest
α-amylase and α-glucosidase inhibitory activities.
In vitro estimated glycemic indices of the samples
are presented in Fig. 8. The results revealed that the
control ice cream had the highest glycemic index (61.24)
compared to the other samples (27.14–28.61). Figures 6
and 7 revealed that the sour-sop based ice cream samples
inhibited carbohydrate hydrolyzing enzymes.
The control ice cream had the lowest amylose content
(14.32%) compared to the soursop-based ice cream
(32.35–35.34%) (Table 3). There was no significant
difference in the amylopectin content of the samples
with soursop and moringa leaf powder (64.66–67.65%),
while the control ice cream had the highest amylopectin
content (85.68%).
A therapeutic and practical way to control
postprandial rise of glucose level in blood is the control
of carbohydrate hydrolyzing enzymes [37]. Starch
is converted to disaccharides and oligosaccharides
by pancreatic α-amylase, before further conversion
to glucose is catalyzed by intestinal α-glucosidase
[38, 39]. Therefore, inhibition of both α-amylase
and α-glucosidase activities would result in a reduction
of glucose absorbed into the blood. The ability of
the sour-sop based ice creams to inhibit the enzymes
could be of therapeutic benefit in the management of
hyperglycemia.
Interestingly, this tendency for enzyme inhibition
by the samples was similar to the tendency for total
phenolic and flavonoid contents [40]. In addition, the
synergistic contribution of phenolic compounds in
soursop and moringa leaves can make ice cream a potent
inhibitor of α-amylase and α-glucosidase activities.
Our previous studies showed the presence of phenolic
compounds, such as gallic acid, elagic acid, rutin,
quercetin, kaempferol, epicatechin and chlorogenic acid,
in soursop and moringa leaves [34, 35, 41].
The soursop-based ice cream samples had low
glycemic indices (Fig. 8) which can be attributed to a
number of factors. First, phenolic compounds in soursop
and moringa leaves are potent inhibitors of α-amylase
and α-glucosidase activities, which results in a slower
breakdown of starch into glucose [42]. This is further
evidenced by the fact that moringa powder increased
phenolic content and reduced glycemic indices. Second,
an amylose and amylopectin ratio in food products
have a significant effect on postprandial glucose
response [43]. Starchy products with a high amylopectin
to amylose ratio often digest faster and are absorbed
quicker than those with a low amylose to amylopectin
ratio and, consequently, produce a high postprandial
glucose and insulin response [34]. The control ice cream used in this study possessed a low amylose content and
high amylopectin content and, thus, the highest glycemic
index compared to the experimental ice cream samples,
which had a low amylopectin content and a high
amylose content.
CONCLUSION
Moringa leaf powder added into soursop-based ice
cream improved the antioxidant properties of the final
product, reduced its glycemic index, and enhanced
inhibition of carbohydrate hydrolyzing enzymes.
Soursop-based ice cream with moringa leaf powder
can be used to control postprandial hyperglycemia and
oxidative stress. The results revealed that moringaenriched
soursop-based ice cream could be an
alternative to the sugar-sweetened ice-cream. However,
further in vivo experiments and clinical trials are
recommended.
CONFLICT OF INTEREST
The author declares no conflict of interest regarding
the publication of this article.
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