Journal of Functional Foods 33 (2017) 376–385

Contents lists available at ScienceDirect

Journal of Functional Foods

journal homepage: www.elsevier.com/locate/jff

Development and evaluation of African star apple (Chrysophyllum

albidum) based food supplement and its potential in combating oxidative
stress
Gibson Lucky Arueya ⇑, Grace Febechi Ugwu
Department of Food Technology, University of Ibadan, UI Post Office Road (Zip Code 200284), Ibadan, Nigeria

a r t i c l e i n f o a b s t r a c t

Article history: Africa Star apple (ASA) remains under-utilized. Development into an acceptable food supplement (FS)
Received 2 January 2017 with anti-stress potentials has not been explored.
Received in revised form 28 March 2017 ASA were washed, de-pulped, oven-dried (65 °C, 18 h) and milled (
180 mm). Possible bioactives were
Accepted 4 April 2017
investigated using Gas-Chromatography Mass-Spectrometry. Blending with pre-gelatinized starch (pulp:
starch, 7:3) followed, yielding the FS. Chemical parameters and sensory attributes were determined.
Impact on oxidative stress marker - malondialdehyde (MDA) and antioxidant enzymes (superoxide dis-
Chemical compounds studied in this article:
mutase and catalase) were monitored in Rats stressed and fed FS.
5-Hydroxymethylfurfural (PubChem CID:
237332)
FS had predominantly 5-Hydroxymethylfurfural (0.58 mg/kg) with high free radical scavenging capac-
2,5-Furandione, dihydro-3-methylene ity (DPPH, 86.23%). Mean Sensory (taste) scores for food supplemented with FS (5.5 ± 1.17) compared
(PubChem CID: 75110) favourably with the unsupplemented (6.2 ± 1.03). MDA was lower (0.92 ± 0.04nmole/ml) in Rats stressed
4H-Pyran-4-one, 2,3-dihyro-3, 5-dihydroxy- and fed the FS when compared to exclusively stressed groups (2.28 ± 0.09nmole/ml). FS also significantly
6-methyl (PubChem CID: 119838) (P = 0.05) enhanced (36–109%) the activities of antioxidant enzymes.
Catechin (PubChem CID: 9064) An acceptable FS with good anti-stress potential has been developed to further expand the utilization
Gallic acid (PubChem CID: 370) for ASA.
DPPH (PubChem CID: 2735032)
Ó 2017 Elsevier Ltd. All rights reserved.
Keywords:
African star apple
Food supplement
5-Hydroxymethylfurfural
Antioxidant
Anti-stress

1. Introduction ria and known by various local names: ‘‘agbalumo” by Yorubas,”

African star apple otherwise known as Chrysophyllum albidum
G. Don is a tropical fruit found in West, East and Central Africa. It
is a wild plant that belongs to the family of Sapotaceae and widely
distributed in the low land rain forest zones (Madubuike &
Ogbonnaya, 2003). It enjoys wide acceptability owing to its sweet
succulent fruits and diverse ethno-medical value (Amusa, Ashaya,
& Oladapo, 2003; Okoli & Okere, 2010). African star apple fruit is
a seasonal fruit, sometimes oval or rounded in shape with about
five seeds inside. It is pale orange when ruptured producing a
sweet milky sap from the pulp and is available during December
to April every year. The fruit is widely consumed in Southern Nige-
⇑ Corresponding author.
E-mail addresses: arueyagibson@yahoo.com (G.L. Arueya), febedestiny@yahoo.
com (G.F. Ugwu).
udara” by Igbos and ‘‘agwaluma” by Hausas in Nigeria. The fruit
is left to drop naturally to the forest floor from where they are
picked up (Amusa et al., 2003). Studies have shown that more than
30% postharvest losses of African star apple fruits are experienced
within five days as a result of the high tropical temperature and
humidity, poor post-harvest handling practices coupled with lack
of proper processing and preservation techniques (Amusa et al.,
2003).
The antimicrobial effects, nutritional value and potency of dif-
ferent parts of the plant against various ailments have long been
established. For instance the bark is used for treatment of yellow
fever and malaria while the leaves are used for skin irritation as
well as diarrhea and stomach aches (Adisa, 2000). The fruit is very
rich in vitamins, calcium and iron and also provides a good source
of flavorants to diet (Adisa, 2000; Chukumalume, Garba, Ijah, &
Agary, 2010). The ascorbic acid content of the fruit (1000–

http://dx.doi.org/10.1016/j.jff.2017.04.004
1756-4646/Ó 2017 Elsevier Ltd. All rights reserved.
 G.L. Arueya, G.F. Ugwu / Journal of Functional Foods 33 (2017) 376–385
3300 mg/100 g) is about 100times that of orange and 10times that
of guava or cashew (Amusa et al., 2003). The fruit is known also to
be high in antioxidants, total phenols and flavonoids (Oloyede &
Oloyede, 2014).
In view of the high postharvest losses and nutritional value, var-
ious uses have been proposed as possible outlets for the fruit. The
fleshy fruits are the potential source of a soft drink (Ugwu & Umeh,
2015). The juice of the fruit can be fermented for wine or produc-
tion of alcohols (Ajewole & Adeyeye, 1991). Fruit leathers/candies
manufacture have also been advocated using osmotic dehydration
(Falade & Aworh, 2004). The fruits are also suitable for the produc-
tion of fruit jams and jellies (Ureigho & Ekeke, 2010).
The foregoing notwithstanding, African star apple remains cur-
rently underutilized. The use in the formulation and production of
a food supplement based on its antioxidant properties has not been
explored. Therefore this study intends to explore this property in
developing a food supplement which may encourage increased uti-
lization and hence reduce postharvest losses.
2. Materials and method
2.1. Raw material sourcing and pre-processing
2.1.1. Raw material sourcing
The fruits of African star apple (Chrysophyllum albidum) were
purchased from Oje market in Ibadan, Oyo State, Nigeria. Food
grade corn starch was procured from Archkings Confectionery in
Ota, Ogun State Nigeria.
2.1.2. Preparation of African star apple pulp
The ripe African star apple fruits were first sorted and washed;
the exocarp and seeds were removed mechanically with the aid of
knife. The pulp was rinsed in distilled water and allowed to drain
for few minutes, dried at 65 °C for 18 h, pulverized and milled in
a hammer mill (Apex Construction,China) for chemical characteri-
zation as well as formulation of the food supplement.
2.1.2.1. Elucidation of structure of possible bioactive compounds in the
pulp. Sample extraction was first done using the method of Idu,
Obayagbona, Oshomoh, and Erhabor (2014). One hundred grams
of the powdered fruit pulp sample was soaked in 1000 ml of 95%
ethanol at room temperature for 24 h. The extracts were then fil-
tered through cheesecloth. The filtrate was collected and re-
filtered through Whatman paper No. 1. The resulting filterate
was evaporated under reduced pressure using a rotary evaporator
at low temperature of 40 °C until a dry extract was obtained. The
extract was collected and stored at 4 °C for elucidation of possible
bioactive compounds. Prior to the elucidation, the extract was re-
extracted with methanol before injection to gas chromatography
mass spectrometer (GCMS) (Model GC 7890A, MSD 5975C) from
Agilent Technologies Inc., CA, USA. The column (Agilent 190915-
433) specifications were length 30 m, internal diameter 0.35 mm
(i.d.) and thickness of 0.25 mm.
The elucidation of the identity of possible bioactive compounds
was carried out using the method of Kim et al. (2007) with slight
modification. Temperature range of the GCMS was initially at
50 °C for 5 min before increasing to 210 °C at a rate of 3 °C min1
and remained so for 10 min. It was further increased to 230 °C at
a rate of 3 °C min1 and held for 5 min. The temperature of the
injector was 250 °C and injection volume was 1.0 L. The flow rate
of the helium carrier gas (99.999% purity) was 1 milliliter per min-
ute. The ionization voltage of the mass spectrometer was70 eV and
the ion source temperature was 230 °C. An aliquot of 1.0 mL of the
extract solution stock (105 ml) was injected. The identification of
the components was done by comparing their Kovats GC retention
377
indices and mass spectra with those obtained from the correspond-
ing standards and data from the NIST MS library 11.
2.1.3. Production of pre-gelatinized corn starch
Pre-gelatinized starch was produced from the food grade corn
starch according to the method of Mohammed (2014) with little
modification. Two hundred and fifty grams of corn starch powder
was mixed with about 500 ml of distilled water to form a paste.
About 2 L of already boiled distilled water was added to the paste
and stirred until a homogenous starch mix was obtained. The pro-
duct formed was transferred to a stainless tray and dried at 60 °C to
10% moisture level. The dried product was milled to obtain small
particle sizes of about 180 mm.
2.2. Development of the African star apple based food supplement
2.2.1. Formulation of food supplement
The African star apple food supplement formulation was pro-
duced by blending African star apple pulp powder and pre-
gelatinized starch in different ratios - 9:1, 8:2, 7:3, 6:4, 5:5, 4:6,
3:7, 2:8, and 1:9 respectively. The mixed samples were separately
kept in uncapped plastic containers of 8.75 mm  2.14  0.2 cm
(height  width  thickness) at room temperature (27 ± 3 °C) and
relative humidity (70 ± 10%) for 72 h.
2.2.2. Moisture uptake of formulations
The change in weight as a result of moisture uptake was evalu-
ated. The increase in weight of different mixes of food supplement
as a function of moisture uptake were-{Pulp: starch(g)/ Moisture
uptake (mg)} were: 9:1/(340); 8:2/(246); 7:3/(149); 6:4/(185);
5:5/(214); 4:6/(209); 3:7/(185); 2:8/(140); 1:9/(132). The formula-
tion (7:3) with 70% of African star apple had lesser uptake of mois-
ture compared to others with high amount of pre-gelatinized
starch. Therefore the formulation with 70% African star apple
was adopted for this study.
2.3. Proximate and physico-chemical evaluation of the food
supplement
2.3.1. Proximate analysis of the food supplement
Moisture, crude protein, ash and Crude fibre were all deter-
mined according to standard methods (AOAC, 2010). Carbohydrate
was by difference.
2.3.1.1. Colour. The colour of African star apple food supplement
was measured by the method described by Arueya and
Osundahunsi (2015). The L, a, and b values of the powder were
determined with a HunterLab Colorimeter (CR-400/ 410; Konica
Minolta Sensing Inc., Osaka, Japan). The instrument was calibrated
using a standard white tile prior to use (L = 95.07, a = 0.73,
b = 3.75). The mean of the three measurements of the sample
was calculated.
Where ‘L’ indicates the lightness and varies from 100 for perfect
white to 0 for black
‘a’ indicates redness when positive and greenness when
negative
‘b’ measures yellowness when positive and blueness when
negative.
2.3.1.2. pH. pH meter (Model 3520, Bibby scientific limited Dumow
Essex, UK) was used for the analysis. The pH meter was standard-
ized with pH 4.0 and pH 7.0 buffer solutions and the electrode was
rinsed properly with distilled water. Thereafter 1 g of sample was
mixed with 10 ml of distilled water and the pH determined.
378 G.L. Arueya, G.F. Ugwu / Journal of Functional Foods 33 (2017) 376–385
2.3.1.3. Water activity. The water activity (aw) of the food supple-
ment was determined by the method of Mathlouthi (2001) as equi-
librium relative humidity (ERH) using saturated sodium chloride
salt solution and a hygrometer in an air tight container.
aw ¼ ERH=100
2.3.1.4. Total phenol. The total phenol content of samples was ana-
lyzed by Folin-Ciocalteu colorimetric method (Arueya &
Osundahunsi, 2015). One milliliter of appropriate dilutions (10–
1000 lg/mL) of sample extract was oxidized with 1 ml of 10% Folin
C reagent. After 3 min 1 ml of saturated 15% sodium carbonate
(Na2CO3) solution was used to neutralize the reaction. The solution
was made up to 5 mL with distilled water. The absorbance of the
resulting mixture was read at a wave length of 760 nm in a UV–vis-
ible spectrophotometer (Spectrum lab 752s). Gallic acid was used
as standard.
2.3.1.5. Assay of total flavonoid. The assay of flavonoid content was
done colorimetricaly using the method described by Jia, Tan, and
Wu (1999) with some modifications. The sample was made up to
10–1000 lg/mL with distilled water. An aliquot (75 lL) of sodium
nitrite was added. Thereafter (5 min later), 150 lL of Aluminum
chloride was added. This was followed by the addition of 500 lL
of sodium hydroxide to the mixture and made up with 1.28 mL
of distilled water. The absorbance reading of the sample mixture
was taken at a wave length of 760 nm. Catechin was used as
standard.
2.3.1.6. Free radical scavenging ability. The hydrogen donating or
radical scavenging of the sample was determined using the stable
radical DPPH (2,2-diphenyl-2-picrylhydrazyl hydrate) according to
the method described by Oloyede and Oloyede (2014). A concen-
tration of 1 mg/ml of sample solution was prepared. One milliliter
of methanol was measured into the cuvette followed by addition of
1 ml DPPH reagent in the spectrophotometer and kept in the dark
for 30 min. The absorbance was read at 517 nm. This served as con-
trol. Also 1 ml of DPPH was added to 1 ml of sample, the resultant
mixture was kept in the dark for 30 min and thereafter absorbance
read at 517 nm. Catechin was used as control.
2.3.2. Functional properties
2.3.2.1. Water and oil absorption capacity. Water absorption capac-
ity and oil absorption capacity of the food supplement was deter-
mined by the method of Owuamanam, Ihediohanma, and
Nwanekezi (2010). One gram of the food supplement was mixed
with distilled water and oil, each in a centrifuge tube and made
up to 10 ml dispersion and allowed to stand at room temperature
for 30 min. The sample was centrifuged at 350g {G-force}. Water
absorption and Oil absorption capacities were expressed as gram
of water or oil bound per gram of food supplement.
2.3.2.2. Bulk density. The method of Owuamanam et al. (2010) was
followed to determine the bulk density. Ten grams of the sample
was weighed into 50 ml graduated cylinder and the initial volume
recorded. In determining packed bulk density, the cylinder was
tapped repeatedly for 100 times to constant volume and the final
volume recorded. The loosed bulk density was calculated by noting
the initial volume of the sample before tapping. The bulk density
was calculated as the mass of the sample divided by the volume
at the end of tapping.
2.4. Sensory evaluation
The sensory properties of the food supplement were evaluated
using thirty (30) panelists. Each panelist was presented with two
different coded samples of jollof rice with and without the African
star apple food supplement. Sensory evaluation was carried out by
rating each sample on a 9-point hedonic scale for taste, colour,
mouth feel, aroma, appearance and overall acceptability (where
9 = extremely liked and 1 = extremely disliked) according to the
method of Ihekoronye and Ngoddy (1985).
2.5. Animal study
2.5.1. Experimental design
Twenty-five Wistar albino rats (90–180 g) obtained from the
Animal house of Physiology Department, University of Ibadan were
used following, clearance from the Animal Care and Use Research
Ethics Committee of the University of Ibadan. They were randomly
separated into five groups and housed in standard cages containing
five rats per cage. Animals were maintained under controlled con-
ditions of temperature (25 ± 5 °C), relative humidity (55–60%) and
light (12 h light/darkcycles). The rats were acclimatized for
14 days. They were allowed to feed on standard pelleted rat diet
(Ladokun feed) and water ad libitum before the administration of
the food supplement (test diet). The African star apple based food
supplement was incorporated into the feed and pelletized.
2.5.2. Animal grouping and food supplement administration
These were assigned to groups as follows:
Group (1): Negative Control: Rats fed on standard Rat diet and
unstressed
Group (2): Positive Control: Rats fed on standard Rat diet and
stressed
Group (3): Treatment 1: Rats fed on 5% African star apple food
supplemented diet and stressed
Group (4): Treatment 2: Rats fed on 10% African star apple food
supplemented diet and stressed
Group (5): Treatment 3: Rats fed on 20% African star apple food
supplemented diet and stressed
2.5.3. Induction of oxidative stress
Oxidative stress was induced in the animals using immobiliza-
tion stress according to Al-Rejaie et al. (2012) with slight modifica-
tion. This was done by subjecting each treatment rat to restraint
stress in a plastic/well-ventilated cage of the same size
(2.5 in.  4 in.), whereas control rats were not restrained from
movement throughout the experimental period. Animals were
restrained for 2 h per day for five days in a week any time between
9 am and 12 noon. The experiment lasted for 4 weeks. During
stress induction, animals were deprived of food and water (Liu
et al., 1996). Body weight of each animal was recorded weekly.
2.5.4. Sample collection
Four millilitres of blood sample was collected by ocular punc-
ture from each of the experimental animal using capillary tube
and was dispensed into commercially prepared heparin containers.
Blood was centrifuged at 2000g for 15 min. The supernatant was
stored at 18 °C and used for all the assays.
2.6. Biochemical assays
2.6.1. Estimation of malondialdehyde (MDA)
The malonaldehyde was estimated by method described by Al-
Rejaie et al. (2012). Two milliliter of plasma was mixed with 1 ml
of 10%trichloroacetic acid and placed on boiling water bath for
20 min. The mixture was cooled and centrifuged at 4000g for
15 min. One milliliter supernatant was mixed with 2 ml of 0.67%
2-thiobarbituric acid and the supernatant was measured at
532 nm using spectrophotometer. The malondialdehyde (MDA)
 G.L. Arueya, G.F. Ugwu / Journal of Functional Foods 33 (2017) 376–385
level was calculated using the molar extinction coefficient of
1.56  105 M1 cm1 and results reported in MDA equivalents
(Ohkawa, Ohishi, & Yagi, 1979).
2.6.2. Measurement of antioxidant marker enzymes activity
2.6.2.1. Determination of superoxide dismutase activity. Superoxide
dismutase was assayed by the method described by Oyedemi,
Bradley, and Afolayan (2010). The reaction mixture contained
0.5 ml of hepatic PMS, 1 ml of 50 mM sodium carbonate, 0.4 ml
of 25 lg nitrobluetetrazolium and 0.2 ml of freshly prepared
0.1 mM hydroxylamine hydrochloride. It was mixed quickly by
inversion followed by the addition of clear supernatant of 0.1 ml
of plasma (10% w/v). The change in absorbance was recorded at
560 nm.
2.6.2.2. Determination of catalase activity. Catalase activity was
determined according to the method described by (Onyeka,
Aligwekwe, Nwakanma, Bakare, & Ofoego, 2012). Decrease in
absorbance due to the decomposition of H2O2 was recorded at
240 nm using spectrophotometer. The reaction mixture (3 ml) con-
tained 0.1 ml of serum in phosphate buffer (50 mM, pH 7.0) and
2.9 ml of 30 mM H2O2 in phosphate buffer pH 7.0. An extinction
coefficient of 40.0 M1 cm1 for H2O2 degradation was used for cal-
culation. The specific activity of catalase was expressed as moles of
H2O2 reduced per minute per mg. protein.
2.6.3. Liver function tests
The activities of Aspartate aminotransferase (AST), Alanine
aminotransferase (ALT) and Alanine phosphates (ALP) were esti-
mated according to the standard procedures described by Burtis,
Ashwood, and Bruns (2007, chap. 19) using Randox diagnostic kit
(Randox Laboratories, USA).
2.7. Statistical analysis
Data obtained were analyzed using one-way analysis of vari-
ance (ANOVA) SPSS Version 17.0 computer software. The mean
were separated using Duncan’s multiple range tests (p < 0.05)
and presented as Mean ± standard deviation.
3. Results and discussions
3.1. Elucidation of the possible bioactive compounds in the dried pulp
extract
The identified Bioactive components of the dried pulp extract
were 5-Hydroxymethylfurfural (5-HMF) (0.83 mg/kg); 2,5-furan
dione,dihydro-3-methylene (0.09 mg/kg); 4H-Pyran-4-one, 2,3
dihydro-3,5-dihydroxy-6-methyl- (0.02 mg/kg) (Table 1). These
Table 1
Major bioactives identified in African star apple.
RT Name of compound
9.072 2,5-Furandione,dihyro-3-methylene-
18.773 4H-Pyran-4-one, 2,3-dihyro-3,5-dihydroxy-6-methyl-
23.684 5-Hydroxymethylfufural
379
contributed about 86.71%, 9.86% and 3.43% respectively of the peak
areas of the chromatogram (Fig 1). Furfural derived compounds are
closely linked with thermal processes and prolonged storage
(Manyi-Loh, Clarke, & Ndip, 2011). They do not occur naturally
but are created in sugar-containing food such as fruits during heat
treatment processes enhanced by high concentration of saccha-
rides (mainly hexoses), low pH values, presence of organic acids
and low water activity (Matić et al., 2009).
The activities of the bioactives are a function of sub-units of
their structural moieties (Table 1). The furfural – 5HMF has a furan
ring oxygen with affinity for electrons as well as an allylic hydroxyl
group with hydrogen donating potential. Double bonds with
attraction for Non-free-radical singlet oxygen (O12) and an aldehyde
oxygen atom together make up the remaining features. These were
reported to have largely accounted for In Vitro antioxidative activity
(dose/time dependent) of the 5-HMF Isolate from marine Red alga
against free radical species (DPPH, hydroxyl, alkyl and superoxide
anions (Li, Li, Qian, Kim, & Kim, 2009). In evaluating the structure
of another component namely 2,5-furandione 3-methyl- (Table 1)
the lone pair electrons associated with the carbonyl oxygen at posi-
tions 2 and 5 cannot be ignored. They make good H-bonds acceptor
sites and could effectively neutralize a number of free radicals. These
may have contributed to their antioxidative property as also
observed by Shukla, Sharma, Pathak, and Bajpai (2016) with the
methanolic extract of Grewia Asiatica fruit. Also noteworthy is the
dual degree of hydroxylation (positions 3 and 5) and its attendant
hydrogen donating potential as obtained in 4H-Pyran-4-one, 2,3-di
hydro-3,5-dihydroxy-6-methyl, the third bioactive identified. Indeed
the position and degree of hydroxylation are critical in determining
antioxidant activity (Gulcin, 2012). The potential contribution of this
latter bioactive compound to oxidative stability of foods has since
been recognized (Kanzler, Haase, Schest, & Kroh, 2016).
While the antioxidative effect of these Maillard reaction prod-
ucts have been applauded as beneficial to human health, various
concerns have been expressed for and against their safety. It must
be stated that no case reports or epidemiological studies so far
links exposure to Maillard reaction products with cancer develop-
ment in humans (Kowalski, Lukasiewicz, Duda-Chodak, & Ziec,
2013). Regulatory authorities in some countries have prescribed
maximum permissible limit of 20 mg/kg for 5-HMF containing
foods (pasteurized juices, bread, coffee, confectioneries etc.) osten-
sibly as a precautionary measure (Matić et al., 2009). It is instruc-
tive that Maillard Reaction Products as evaluated in the Dried Pulp
under consideration as well as the food supplement developed
thereof were all less than 1 mg/kg [5-HMF (0.58 mg/kg), 2,5 fura-
dione, dihydro-3-methylene (0.06 mg/kg), 4H-Pyran-4-one, 2,3-di
hydro-3,5-dihydroxy-6-methyl-(0.02 mg/kg)].
Peak area Molecular structure Molecular weight
9.86 112.0843
3.43 144.1253
86.71 126.1100
380 G.L. Arueya, G.F. Ugwu / Journal of Functional Foods 33 (2017) 376–385

Fig. 1. GCMS Chromatogram of major bioactives in African apple dried pulp extract.

3.2. Proximate and physico-chemical properties of the food Table 2

supplement Proximate and physico-chemical properties of African star Apple based Food
Supplement.

3.2.1. Proximate composition Parameters Amount

The moisture content of the African star apple food supplement Moisture (%) 8.27 ± 0.33
obtained in this study was 8.27%, a value comparable to the 8.10% Crude fat (%) 9.83 ± 0.57
reported for pineapple pulp (Ackom & Tano-Debrah, 2012) but Ash (%) 2.67 ± 0.58
Crude protein (%) 4.88 ± 0.25
lower than the 9.75% and 8.78% observed for apple pomace powder
Crude fibre (%) 3.45 ± 0.39
and carrot powder respectively (Humaira, Altaf, Heena, Saima, & Carbohydrate (%) 70.90 ± 0.21
Ambreen, 2013). The crude Fat (9.83%) observed for the supple- pH 3.10 ± 0.14
ment in this study is lower than 16.20% earlier reported for the Colour (Hunter L, a, b values) 30.51 ± 0.01; 7.77 ± 0.02;5.95 ± 0.01
Water activity 0.50
Chrysophyllum albidum fruit (Amusa et al., 2003), but higher than
Flavonoid (mg/100 g) 254.33 ± 4.04
1.48% crude fat content reported for pineapple pulp powder and Total phenol (mg/100 g) 2236.7 ± 15.28
3.12% for apple pomace powder. This indicates that C. albidum DPPH scavenging activity (%) 86.23 ± 2.83
fruits contain a moderately high level of crude fat. The ash content
of the food supplement was 2.67% (Table 2). This figure compares
favorably with those reported for African star apple fruit pulp by ciency causes growth retardation, abnormal swelling of the belly
Edem and Dosunmu (2011). This value is lower than 5.18% and collection of fluids in the body (Mounts, 2000). The crude fibre
reported for both processed pineapple pulp and 3.97% reported content is (3.45%), this value is lower than 4.45% obtained for Afri-
for apple powder but higher than 1.10% reported for the same fruit can star apple (Chrysophyllum albidum) fruit pulp (Edem &
(Gebhardt, Cutrufelli, & Matthews, 1982). The moderately high ash Dosunmu, 2011). The presence of fibre in diets assists in removal
content (2.67%) indicates the high mineral content of the food sup- of carcinogens, potential mutagens, steroids, bile acids and xenobi-
plement. The ash content can provide an estimate of the quality of otics by binding or absorbing these components and rapidly aid
the product. The protein content of African star apple was 4.88% a their excretion (Ayoola & Adeyeye, 2009). Increased crude fibre
figure lower than the 5.66% protein content reported by Edem and consumption also increase fecal bulk and rate of intestinal transit
Dosunmu (2011), 8.51% for pinapple pulp and 5.11% reported for and exerts prebiotic effects. The sample was high (70.90%) in car-
apple pomace powder. The result shows that C. albidum fruit is bohydrate content and can be good sources of energy. The value
very low in its protein content. Proteins are known to supply ade- is lower than (78.34%) obtained for African star apple pulp fruit
quate amount of required amino acids to the body. Protein defi-
 G.L. Arueya, G.F. Ugwu / Journal of Functional Foods 33 (2017) 376–385
but higher than (36.29%) for the same fruit (Abolaji & Adiaha, 2015;
Edem & Dosunmu, 2011).
3.2.2. Physico-chemical properties of the food supplement
The result of some selected physic-chemical properties of Afri-
can star apple based supplement is shown in Table 2. The pH of the
food supplement was 3.1; this low pH could assist in the preserva-
tion of the fruit. The low pH could be attributed to presence of
citric acid and ascorbic acid in African star apple (Dauda, 2014).
The colour attribute (reddish brown) of the food supplement mea-
sured before storage by the Hunter L, a, b, values was 30.51 ± 0.01,
7.77 ± 0.02, 5.95 ± 0.01. The drying could have affected the colour
by increasing the rate of maillard reaction thereby leading to low
L value and a positive a value. Colour is very important for con-
sumer’s acceptance. The Furfurals as products of heat treatment
of the pulp may have contributed to the colour of African star apple
based supplement. The moisture content and water activity of the
food supplement prior to storage were 8.27 and 0.50 respectively.
The moisture content of the supplement was within the recom-
mended moisture range (
12%) for dry products. Low moisture
content is essential during storage because it favours shelf stability
of powdered products (Eleazu, Eleazu, Awa, & Chukwuma, 2012).
Higher moisture content above 12% evidently promotes microbial
growth. Also the food supplement had a water activity below the
critical point (0.60) for microbial growth. It could reasonably be
concluded therefore, that the African star apple based supplement
possesses potential for good storage especially if properly
packaged.
The total phenolic contents in the African star apple fruit pulp
are as shown in Table 2. The pulp has considerable high amount
of phenol (2423 mg/100 g) and flavonoid (284 mg/100 g). These
values are less than 3146 mg/100 g phenol and 840 mg/100 g fla-
vonoid (Oloyede & Oloyede, 2014) and more than
(1070 mg/100 g) phenol and (60 mg/100 g) flavonoid
(Onyekwelu, Olufunmilola, Stimm, & Mosandl, 2011) for the same
fruit. The difference could be attributed to season of the year, soil,
maturity stage and climatic conditions (Palencia, 2006). It could
also be as a result of differences in drying temperatures; since
these compounds tend to degrade with increase in temperature
(Irina & Mohamed, 2012). Drying processes lead also to degrada-
tion of phenolic compounds. The proportion lost depends on the
drying method: freeze-drying being less aggressive as against hot
air drying which ultimately leads to major losses (Irina &
Mohamed, 2012).
Phenolic compounds are a large group of the secondary
metabolites widespread in the plant. The phenolic compounds of
African star apple, especially flavonoids and phenols have been
reported to possess significant antioxidant activity (Oloyede &
Oloyede, 2014), sometimes acting as free radical terminators (Om
Prakash & Tripathi, 2007 and Kumar, Kumarave, & Lalitha, 2010).
They possess diverse biological activities such as antioxidant,
anti-apoptosis, anti-aging, anti-carcinogen, anti-inflammation,
anti-atherosclerosis, cardiovascular protection, improvement of
the endothelial function, as well as inhibition of angiogenesis and
cell proliferation activity (Han, Shen, & Lou, 2007). They have the
ability to absorb, neutralize and to quench free radicals (Duh, Tu,
& Yen, 1999). Their ability as free radical scavengers could also
be attributed to their redox properties, presence of conjugated ring
structures and carboxylic group which have been reported to inhi-
bit lipid peroxidation (Rice-Evans, Miller, Bolwell, Bramley, &
Pridham, 1995). Phenolic compounds also have the ability to che-
late ferric ions which catalyze lipid peroxidation, and this is a good
therapeutic agent for free radical-linked pathologies (Said &
Zeinab, 2009). Flavonoids have been recognized to possess antiox-
idant activity and their effects on human health are considerable.
The mechanisms of action of flavonoids are through scavenging
381
or chelating process (Kessler, Ubeaud, & Jung, 2003). The high phe-
nolic content also indicates that the plant has high antioxidant
activity. The relatively high level of phenol and flavonoid content
might account for the strong activity observed against DPPH radi-
cals (Table 2). This could be due to the interaction between the
African star apple and the pre-gelatinized starch. The DPPH activity
was found to decrease in the food supplement (86.23%) compared
to the pulp (92.47%). The scavenging activities of 5-HMF on DPPH
radical have been observed to be time- and dose-dependent (Zhao
et al., 2013). The DPPH assay is commonly used for testing radical
scavenging activity of various food products (Elmastas, Isildak,
Turkekul, & Temur, 2007).
3.3. Functional properties of African star apple food supplement
The physical and functional properties of African star apple are
shown in Table 3. The water and oil absorption capacities are
154.00 ± 2.83 and 105.60 ± 1.24 respectively. These values indicate
that the product could be used in fatty foods and emulsion systems
without making them soggy with water or fat (Ackom & Tano-
Debrah, 2012). The loose and tapped bulk density is 0.57 and
0.42 respectively as indicated in Table 3. The values are similar
to that obtained from apple pomace powder 0.58 and 0.43
(Jakubczyka, Gondeka, & Tamborb, 2011). However, powders are
composed of particles and voids; therefore increase in bulk density
will cause particles to move relatively close to one another to
occupy space between particles during packaging.
3.4. Sensory evaluation
Sensory quality of two jollof rice sample was analyzed for taste,
colour, aroma, mouthfeel, appearance and overall acceptability on
a 9 point hedonic scale where 1 indicated extremely dislike and 9
extremely liked. The jollof rice with food supplement received
lower scores: taste (5.5 ± 1.17), colour (6.5 ± 0.97), appearance
(6.5 ± 1.08), aroma (6.2 ± 0.79), mouth feel (5.5 ± 0.84) and Overall
acceptability (5.8 ± 0.79) when compared to those for unsupple-
mented jollof rice: taste (6.2 ± 1.03), colour (6.5 ± 1.17), appear-
ance (6.6 ± 0.97), aroma (6.4 ± 0.84), mouthfeel (6.6 ± 1.26) and
Overall acceptability (6.4 ± 0.84). Although at p-value (p < 0.05)
the difference between the means of the two samples were
insignificant. The slight astringent taste of African star apple might
have contributed to this less preference.
3.5. Animal studies
3.5.1. Effect of African star apple food supplement on the weight gain
of rat
Four weeks of restraint-induced stress significantly (P < 0.05)
decreased the body weight of rats. African star apple supplementa-
tion to the stressed rats significantly (P < 0.05) increased the body
weights (23.05%, 25.37% and 28.97% in 5%, 10% and 20% supple-
mented diet group respectively) as compared to untreated stressed
animals (18.89%). The percentage gain of the control group
(26.67%) is higher than that stressed group. Exposure of rats to
repeated immobilization stress reduces their food and water intake
Table 3
Functional properties of African star apple based food
supplement.
Parameter Amount
2
Loose bulk density (g/cm ) 0.57 ± 0.01
Tapped bulk density (g/cm2) 0.42 ± 0.02
Water absorption capacity (%) 154.00 ± 2.83
Oil absorption capacity (%) 105.60 ± 1.24
382 G.L. Arueya, G.F. Ugwu / Journal of Functional Foods 33 (2017) 376–385

after release from immobilized chamber (Bhatnagar, Vining, Iyer, & stress thereby leading to disorders in humans such as diabetes
Kinni, 2006). This in turn affects sympathetic activity by suppress- mellitus, arthritis, aging, carcinogenesis, and atherosclerosis
ing the levels of circulating growth hormones (Al-Rejaie et al., (Gangwar et al., 2014). Conversely the free radicals find usefulness
2012; Yoshihara & Yawaka, 2008). Thus, immobilization stress in the proper physiological functioning of the immune system
affects food intake and decreases body weight of the untreated (Bast, Haenen, & Doelman, 1991). However, lipid peroxidation is
group. The intake of African star apple ostensibly helped to allevi- beneficial and has been used by nature to destroy microorganisms
ate the effect of stress. This may be due to the high antioxidant as well as produce molecules that signal new cell growth (Uhegbu,
capacity of the supplement leading to improved activity of growth Nwoku, & Ude, 2013).
hormone.
3.5.3. Effect of African star apple food supplement on antioxidant
enzymes
3.5.2. Effect of African star apple food supplement on oxidative stress
The effect of African star apple food supplement on the activi-
marker
ties of antioxidant enzyme superoxide dismutase in the plasma
In this study the plasma level of malondialdehyde (MDA)
of control and experimental rats are shown in Fig. 3. This study
increased (P < 0.05) significantly in stressed animals (2.28 ± 0.08n-
showed a significant decrease (P < 0.05) in the activity of superox-
mole/ml) without supplementation compared to 0.85 ± 0.01nmole/
ide dismutase in the stressed animals compared to control and
ml in the control group (Fig. 2). There were also significant
supplemented groups: 11.67 ± 0.98 U/ml (control), 6.60 ± 0.80 U/
decrease (P < 0.05) in experimental animal groups on supple-
ml (stressed) group. The level of Superoxide dismutase in 5%,
mented feed (1.63, 1.24 and 0.92nmole/ml for 5%, 10%, and 20%
10% and 20% supplemented diet group increased by 35.9%, 38.3%
supplementation respectively) compared to non-supplemented
and 68.6% respectively compared to the stressed group. A similar
group (2.28nmole/ml). Evidently, 5-HMF the predominant bioac-
trend was observed with immobilized rats fed with black and
tive component in the supplement may have played a leading role
green tea (Al-Rejaie et al., 2012). Also rats fed with various ratios
in this reduction. Zhao et al. (2013) reported a similar pattern of
of dikanut Supplemented diet showed increase in SOD which is
MDA reduction following an increase of 5-HMF from 1.5 mM to
attributed to antioxidant activity of the nut. Supplementation with
24.0 mM during in Vitro experiments involving oxidative damage
African star apple based food supplement displayed a significant
of erythrocytes induced by free radical from 2,21- azobis (2-
increase (P < 0.05) in the activities of the antioxidant enzymes. This
amidino propane) dihydrocloride (AAPH).
may also be related to the activities of 5-HMF inherent in the food
Studies have shown that isolation housing of adult rats per se is
supplement since a similar conclusion was reached with erythro-
not stressful; indeed, rats need to be isolated from weaning to
cytes pretreated with 5-HMF (Zhao et al., 2013).
show signs of stress/anxiety (McDougall, Paull, Widdup, &
The increase in SOD activity indicates that the African star apple
Lawrence, 2000). Lipid peroxidation, an index of oxidative stress
based food supplement has the ability to improve the production
in vivo is often characterized by high concentration of malondi-
of the superoxide dismutase inside the body system of the exper-
aldehyde (MDA) (Aruoma, 1998). Space restraint induces both psy-
imental animal. This also suggests that the African star apple based
chological and physical stress (Al-Rejaie et al., 2012) which can
food supplement improved their in vivo antioxidant activities and
lead to production of MDA.
can offer effective protective mechanism against lipid peroxida-
Reactive oxygen species degrade polyunsaturated lipids, form-
tion. SOD enzyme protects cells against the toxic effects of reacting
ing malondialdehyde which is a reactive aldehyde (Del, Stewart,
oxygen species by catalyzing the rapid removal of the superoxide
& Pellegrini, 2005). This aldehyde is among the reactive elec-
radical (Moore & Roberts, 1998). Indeed, SOD limits the formation
trophile species that cause toxic stress in cells and form covalent
of reactive oxygen species and hence controls lipid peroxidation.
protein adducts referred to as Advanced Lipoxidation End products
Superoxide dismutase (SOD) and catalase (CAT) are among the
(ALE), in analogy to Advanced Glycation End Products (AGE)
key enzymes responsible for the body’s antioxidant defense. They
(Farmer & Davoine, 2007). The production of MDA is used as a bio-
constitute the first defense system of neutralization of reactive
marker to measure the level of oxidative stress in an organism
oxygen species, protecting cells from oxidative injuries (Wu &
(Omoge, Idokpesi, Josiah, Uhunmwangho, & Ajeigbe, 2010). An
Cederbaum, 2003). These enzymes are present in the peroxisomes
unfavourable imbalance between free radicals and antioxidants
of nearly all aerobic cells. Immobilization stress stimulates the pro-
in the body causes destruction of lipid, protein and DNA molecules
(Hazra, Santana, & Nripendranath, 2008). The formation of more
free radicals and neutralization of pro-oxidants result in oxidative 16.00

14.00
2.50
12.00
SOD activity (U/ml)
Malondialdehyde (nmole/ml)

2.00
10.00

1.50 8.00

6.00
1.00
4.00
0.50 2.00

0.00 0.00
Control Stress Stress + 5% Stress +10% Stress + 20% Control Stress Stress + 5% Stress +10% Stress +
ASA ASA ASA ASA ASA 20% ASA

Fig. 2. Changes in oxidative stress marker malondialdehyde (MDA) by African star Fig. 3. Changes in plasma superoxide dismutase activity by African star apple
apple supplementation in rats. supplementation in rats.
 G.L. Arueya, G.F. Ugwu / Journal of Functional Foods 33 (2017) 376–385
ductions of free radicals in experimental rats (Davydov,
Zakharchenko, & Ovsyannikov, 2004) and decrease the activity of
antioxidant enzymes, such as superoxide dismutase and catalase
(Zaidi, Al-Qirim, & Banu, 2005).
The activity of catalase enzyme significantly (p < 0.05)
increased to 22.34 ± 4.84, 28.38 ± 2.13, and 33.04 ± 2.91 in experi-
mental rats fed on 5%, 10% and 20%African star apple based food
supplement respectively, whereas stressed group without supple-
mentation had 15.82 ± 0.81U/L as shown in Fig. 4. Catalase works
closely with superoxide dismutase to prevent free radical damage
to the body (Uhegbu et al., 2013). SOD catalyzes the rapid removal
of harmful superoxide radicals producing hydrogen peroxide
which is eliminated by catalase (Wu & Cederbaum, 2003). Catalase
protects the cell from harmful hydrogen peroxide by catalyzing its
decomposition into harmless molecular oxygen and water without
the production of free radicals (Nehru & Anand, 2005). The reduc-
tion of activity of this enzyme as shown in the stressed group may
lead to deleterious effects associated with assimilation of superox-
ide and hydrogen peroxide. In this study, there was a positive
increase in the activity of catalase in the experimental animals
fed on supplemented diet (Fig. 4). Thus, this indicates the antioxi-
dant potential of African star apple based food supplement against
free radicals in vivo.
3.5.4. 4Activities of liver enzymes
Three levels of the African star apple food supplement (5%, 10%
and 20%) were evaluated for their antioxidative and hepatoprotec-
tive activities in immobilized stressed rats. A significant increase
(P < 0.05) in the liver marker enzymes was observed in group 2
(stressed and untreated) rats when compared with control. The
effect of oxidative stress on AST, ALT and ALP was significantly
reduced (P < 0.05) in the plasma of rats fed on 5%, 10% and 20%
with African star apple based food supplement as shown in
Fig. 5. Undoubtedly, the identified bioactives in the supplement
viz 5-Hydroxymethylfurfural, 2,5-Furandione,dihyro-3-methy
lene-,and 4H-Pyran-4-one, 2,3-dihyro-3,5-dihydroxy-6-methyl
would have had a marked influence on this reduction owing to
their antioxidative properties.
The liver is very susceptible to damage by xenobiotics and non-
xenobiotics induced oxidative stress. Hepatocellular damage is
usually assessed through serum markers employed in the diagno-
sis of liver diseases (Pari & Kumar, 2002). Liver damage is mani-
fested in increased serum levels of Aspartate transaminase (AST),
Alanine transaminase (ALT) and Alkaline phosphatase (ALP)
located in cytosol and serum bilirubin, as well as pronounced
40.00
35.00
Catalase acvity (Unit/ml)
30.00
25.00
20.00
15.00
10.00
5.00
0.00
Control Stress Stress + 5%
ASA
Fig. 4. Changes in plasma catalase activity by African star apple supplementation in
rats.
383
60 ASP
ALT
50
ALP
Enzyme acvies (U/L)
40
30
20
10
0
Control Stress Stress + 5% ASA Stress +10% Stress + 20%
ASA ASA
Fig. 5. Effect of African star apple food supplement on activities of enzyme markers
of liver function.
necrosis of hepatic cells. The rats fed with African star apple based
food supplement had a significant decrease in serum ALP, AST and
ALT when compared with those of the normal control rats (Fig. 5).
The food supplement mediated reduction in levels of AST, ALT
and ALP. African star apple food supplement may well be consid-
ered to have a salutary effect on the functioning of the liver. ALT
is a cytoplasmic enzyme found in very high concentration in the
liver and an increase of this specific enzyme indicates hepato cel-
lular damage. High levels of AST on the other hand indicates that
the liver damage might be due to toxicant induction as well as car-
diac infection and muscle injury. Admittedly, ALT is more specific
to the liver than AST and is thus a better indicator of liver function
(Aliyu, Adebayo, Gatsing, & Garba, 2006; Williamson, Okpako, &
Evans, 1996). Increases in the serum level of ALP are due to
increased synthesis in presence of increasing biliary pressure
(Singh, Singh, Singh, & Gupta, 2009). These indicate that the African
star apple food supplement may have a hepatoprotective effect. Its
high intake showed a higher hepatoprotective activity than when
low. Studies have shown that some bioactive compounds present
in plant extracts do indeed enhance hepatoprotective activities
(Maheswari, Maryammal, & Venkatanarayanan, 2008).
4. Conclusion
This study showed that African star apple based food supple-
ment has free radical scavenging ability in Wistar rats induced
with immobilized oxidative stress. An increased production of
antioxidant enzymes (superoxide dismutase, catalase) and a
decreased liver function enzymes (ALP, ASP, and ALP) were evi-
dent. The food supplement holds great potential for combating
stress in humans while providing a veritable sustainable outlet
for the use of African star apple currently plagued with high post
harvest losses.
Declaration of interest
The authors declare no conflict of interest whatsoever before,
during or after this study.
Stress +10% Stress + 20% Funding
ASA ASA
This research did not receive any specific grant from funding
agencies in the public, commercial, or not-for-profit sectors.
384 G.L. Arueya, G.F. Ugwu / Journal of Functional Foods 33 (2017) 376–385

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