South African Journal of Botany 129 (2020) 106–112

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South African Journal of Botany

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

Potential substitution of the root with the leaf in the use of Moringa
oleifera for antimicrobial, antidiabetic and antioxidant properties
T. Tshabalala a,b, A.R. Ndhlala a,d, B. Ncube a,d, H.A. Abdelgadir c,d, J. Van Staden d,⁎
a
Agricultural Research Council (ARC), Vegetable and Ornamental Plants (VOP), Private Bag X923, Pretoria 0001, South Africa
b
School of Agricultural, Earth and Environmental Sciences, University of KwaZulu-Natal Pietermaritzburg, Private Bag X01, Scottsville 3209, South Africa
c
Faculty of Animal Production and Pasture Sciences, Eldaien University, Eldaien, Sudan
d
Research Centre for Plant Growth and Development, University of KwaZulu-Natal Pietermaritzburg, Private Bag X01, Scottsville 3209, South Africa

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

Article history: A study was conducted to assess variation in antioxidant, antimicrobial, antidiabetic and phytochemical prop-
Received 5 December 2018 erties between the leaves, and the main and lateral roots of Moringa (Moringa oleifera). Standard antioxidant
Received in revised form 16 January 2019 models including the DPPH scavenging, ferric reducing power (FRAP) as well as α-glucosidase inhibitory
Accepted 21 January 2019
activity were used to evaluate and compare their bioactivity. Antimicrobial efficacy was also tested against
Available online 25 February 2019
Gram-positive (Staphylococcus aureus; Bacillus subtilis) and Gram-negative (Escherichia coli) strains and the
Edited by NE Madala yeast-like fungus Candida albicans using the microdilution method. Acetone extracts of all plant parts exhib-
ited good antibacterial activity (MIC b 1 mg/mL) against E. coli, B. subtilis and S. aureus, except for lateral root
Keywords: which exhibited weak activity against E. coli (MIC values N 1 mg/mL). However, all the plant part extracts
Flavonoids exhibited low activity against C. albicans (MIC values b 1 mg/mL). Variation in the antioxidant activity was
Medicinal plant observed, with the main and lateral roots exhibiting better activity than the leaves. All the plant parts had
Phytochemicals better antioxidant activity than the reference compound ascorbic acid. Leaf extracts had significantly good
Tannins antidiabetic activity as compared to the reference compound, acarbose. Variations were observed in the
Total Phenolics
total phenolic, condensed tannins and flavonoid contents among the different plant parts tested. The leaf
extracts exhibited the highest amount of total phenolics, while the lateral roots had higher amounts of
condensed tannins and flavonoid contents. The roots can be used as a better source of antioxidants than
the leaves. All the leaf extracts had significantly good antidiabetic and antimicrobial activity as compared
to the roots. This study ascertains that these different plant parts of Moringa can be suitable candidates for
antimicrobial, antioxidant and antidiabetic supplementations, particularly as it is already frequently used in
animal and human diets.
© 2019 SAAB. Published by Elsevier B.V. All rights reserved.

1. Introduction The leaves are particularly used for traditional medicine, and
human and livestock nutrition (Popoola and Obembe, 2013). Moringa
Moringa (Moringa oleifera Lam.) of the family Moringaceae is a fast leaves are added to foods to increase food shelf life as the leaves are
growing and drought tolerant plant widely cultivated in the tropical high in natural antioxidants (Siddhuraju and Becker, 2003). Antioxi-
and subtropical areas (Anwar et al., 2007). The tree grows in a wide dants found in Moringa leaves include ascorbic acid, flavonoids and
range of rainfall and soil conditions. Common names given to the phenolics (Anwar et al., 2007). These antioxidant agents/compounds
tree include horse-radish tree because of the taste of its roots and is protect cells from free radicals and decrease the oxidative damage of
also known as drumstick tree because of the shape of the pods on molecular compounds such as lipids, proteins and nucleic acids. On
the tree. Interestingly, Moringa is commonly known as a “miracle” the other hand, the roots (Fig. 1) of the Moringa tree have been re-
tree, because all the plant parts of the tree have multi-purpose uses, ported to contain alkaloids, flavonoids, saponins, terpenoids, steroids
including use as medicinal and functional foods (Ashfaq et al., 2012). and tannins (Raj et al., 2011). The root possesses antimicrobial activ-
The “miracle” tree has been reported to prevent a number of ailments ities against Gram-negative bacteria (Salmonella enteritica and Vibrio
(Anwar et al., 2007) and has the ability to purify water (Kumar and parahaemolyticus) (Dalukdeniya et al., 2016) and is also reported to
Gopal, 1999). have antiulcer activities (Choudhary et al., 2013), cure gout and con-
tain a cardiac stimulant. However, there is still anecdotal evidence on
⁎ Corresponding author. the comparison of medicinal properties of different plant parts of
E-mail address: rcpgd@ukzn.ac.za (J. Van Staden). Moringa, such as leaves, lateral and main roots. Additionally, there

https://doi.org/10.1016/j.sajb.2019.01.029
0254-6299/© 2019 SAAB. Published by Elsevier B.V. All rights reserved.
 T. Tshabalala et al. / South African Journal of Botany 129 (2020) 106–112 107

months from transplanting. Leaves were randomly sampled from

the 10 plants and divided into 3 samples (n = 3). Both lateral and
main roots were harvested and randomly divided into three samples
(n = 3), respectively.

2.2. Chemicals and reagents

2,2-Diphenyl-1-picrylhydrazyl (DPPH), neomycin and α-glucosi-

dase were purchased from Sigma–Aldrich (Sigma Chemical Co.,
Steinheim, Germany); butylated hydroxytoulene (BHT) and potassium
ferricyanide from BDH Chemicals Ltd. (Poole, England, UK); trichloro-
acetic acid, ascorbic acid, ferric chloride (FeCl3) and methanol from
Merck KGaA (Darmstadt, Germany). The rest of the chemicals used in
this study were obtained locally (South Africa) and were of analytical
grade.

2.3. Sample preparation

The leaves and roots (main and lateral roots) of Moringa were
first oven dried for 48 h at 50 °C. This was followed by grinding
the leaves and root samples into fine powders; ethanol, 50% aque-
ous methanol, acetone and water were used as extracting solvents
in an ultrasonic bath for 1 h. The extracts were filtered through
Whatman's No. 1 filter paper with the aid of a vacuum. Then a
rotary pressure was used to concentrate the extracts in 50% of
aqueous methanol, ethanol and acetone at 30 °C and a stream of
air was used to completely dry the samples. Water extracts were
freeze-dried. Acetone, ethanol and water extracts were used for an-
timicrobial assays while only water extracts were used for antidia-
betic assay. For all the antioxidant assays, the dried extracts of
50% aqueous methanol were used. All phytochemical analyses
Fig. 1. Morphology of Moringa oleifera roots system, a white swollen tuberous main root
with very sparse lateral roots.
were done from extracts prepared using 50% aqueous methanol
without drying.

2.4. Bioassays
are high conservation concerns when the roots of the tree are har-
vested. Hence, there is a need to investigate the properties for the 2.4.1. Total phenolics, condensed tannins and flavonoids
justification of use for different tree parts. In this study, we investi- Following the method described by Makkar (1999), with slight mod-
gated the variations in the antioxidant activity using the DPPH (2, ification by Ndhlala et al. (2007) the total amounts of phenolics were
2-diphenyl-1-picrylhydrazyl) radical scavenging assay, ferric-reducing determined using the Folin–Ciocalteu (Folin C.) assay. The standard
power (FRAP) and antidiabetic α-glucosidase inhibitory activity, as for this assay was gallic acid. The vanillin-HCl assay was used to deter-
well as properties of the leaves and the main and lateral roots of mine flavonoids found in the roots and leaves of Moringa, this was
Moringa. Additionally, colourimetric methods were used to investi- done following Hagerman (2002) as slightly modified by Ndhlala et al.
gate the variations of phenolic contents of the leaves and the main (2007).
and lateral roots.
2.4.2. Antifungal microdilution bioassay
Anticandidal activity was determined by minimum inhibitory con-
2. Materials and methods centration (MIC), this was tested against the fungus Candida albicans
using the microdilution assay (Eloff, 1998) but modified for the antifun-
2.1. General gal assay (Masoko et al., 2007). An antifungal amphotericin B was used
as a positive control in this study. Acetone, ethanol and water were used
Moringa plants were cultivated at the Agricultural Research Coun- as negative and solvent controls.
cil (ARC) experimental farm in Roodeplaat, Pretoria, South Africa
(25°36′1.85″S; 28°21′54.78″E). Vegetation of the area is described 2.4.3. Diphenyl-1-picrylhydrazyl (DPPH) radical scavenging activity
as Savanna biome (Mucina and Rutherford, 2006) and as Sourish Following the method described by Karioti et al. (2004) with
Mixed Bushveld (Acocks, 1988). Daily mean temperature varies some modifications, diphenyl-1-picrylhydrazyl (DPPH) radical scav-
from 11 °C to 27.2 °C with a minimum of 2.3 °C in winter and a max- enging assay was carried out. Methanolic extracts (50% v/v) from
imum of 30 °C in summer. The experimental farm receives an aver- the leaves and roots (diluted in absolute methanol) were mixed
age rainfall of 650 mm per annum, with most precipitation in with DPPH solution (750 μL, 50 μM in methanol) in a reaction mix-
summer. The farm is situated at an elevation of 1160 m a.s.l., on the ture, under a dimmed light and incubated for 30 min at room tem-
Roodeplaat Igneous Complex belonging to the Post-Waterberg For- perature. This was done in a dark room and readings of the
mation (Panagos et al., 1998). absorbance of the mixtures were read at 517 nm using a UV–vis
Ten moringa plants were randomly selected from a field plot, with a spectrophotometer (Varian Cary 50, Varian Australia Pty. Ltd., Syd-
spacing of 1 × 1 m. Plants were treated to routine maintenance such as ney, Australia). Methanol was used as a blank mixture. Ascorbic
weeding, cultivation, irrigation three times a week and no fertiliser was acid, a known antioxidant was used as a positive control. The exper-
applied to the plants. The plants were harvested in December, two iment was repeated three times. The decolouration of the DPPH
108 T. Tshabalala et al. / South African Journal of Botany 129 (2020) 106–112

solution determined the free radical scavenging solution, using the Statistical Package for the Social Sciences (SPSS) v 25.0 for Windows
formula: (Chicago, IL, USA).
  
Abs517 nm Sample 3. Results
RSA ð%Þ ¼ 1−  100
Abs517 nm Neg Control
3.1. Total phenolics, condensed tannin and flavonoid content
where:
RSA is the Free Radical Scavenging Activity. The leaf of the Moringa plant had significantly (p ≤ .05) higher total
Abs517 sample is the absorbance of the mixture containing the leaf, phenolic compounds compared to both the main and lateral roots
root extracts or the positive control solution. (Table 1). There were significantly (p ≤ .05) more flavonoids in the lat-
Abs517 Neg control is the absorbance of the negative control. eral roots than in the main roots and leaf (Table 1). Lateral roots of
The EC50 (effective concentration) values, representing the amount Moringa had the highest amount of condensed tannins of dry mass,
of extract required to decrease the absorbance of DPPH by 50% was cal- which was approximately three times more than the condensed tannins
culated from the percentage radical scavenging activity. found in the main roots and seven times more (p ≤ .05) than those
found in the leaves (Table 1).
2.4.4. Antibacterial microdilution assay
Antibacterial activity determined by minimum inhibitory concentra- 3.2. Antimicrobial activity
tion (MIC), was tested against Bacillus subtilis, Escherichia coli and Staph-
ylococcus aureus using the microdilution technique in 96-well (Greiner The antibacterial and antifungal MIC values for the Moringa extracts
Bio-one GmbH, Frickenhausen, Germany) microtitre plates (Eloff, 1998) of the leaves, lateral and main roots are presented in Table 2. Generally,
for water, acetone and ethanol extracts. A standard antibiotic, neomy- the leaf samples exhibited better antibacterial activity compared to the
cin, was used as a positive control. Water, acetone and ethanol were root extracts against B. subtilis, E. coli and Staphylococcus aureus (MIC b
used as the negative and solvent controls. The assay was repeated 1 mg/mL) (Table 2). All the extracts indicated good activity against
three times with two replications in each case. S. aureus with no activity difference among the plant parts. The extracts
from the main and lateral roots demonstrated weak activity against
2.4.5. Antidiabetic α-glucosidase inhibitory activity B. subtilis and E. coli, except for the acetone extracts. All the extracts
Antidiabetic activity of the M. oleifera leaf and root extracts was done exhibited weak activity against the fungus C. albicans.
following the method by Tao et al. (2013) as modified by Rengasamy
et al. (2013). Firstly, an enzyme solution was made by dissolving α-glu-
3.3. DPPH radical scavenging activity
cosidase (0.1 Unit/mL) in 0.1 M potassium phosphate buffer (pH 6.8).
The phosphate buffer was used as the negative control. The positive
The EC50 values for the DPPH radical scavenging potential of the leaf,
control was acarbose dissolved in dimethyl sulphoxide (DMSO). The fol-
main and lateral roots of Moringa are shown in Table 3. The EC50 value
lowing equation was used to calculate percentage inhibition:
of Ascorbic acid (Vitamin C) which was used as the positive control was
Acontrol −Asample 69.28 μg/mL. Ideally, the lower the EC50 value the greater the antioxi-
Percentage inhibition ð%Þ ¼  100 dant potency of the tested extract, therefore the plant extracts with
Asample
EC50 values less than or equal to the reference represented high antiox-
idant potential. In this study, all three plant parts (leaves, main and lat-
where:
eral roots) had a DPPH radical scavenging ability better than the
Acontrol is the absorbance of the control.
reference compound (ascorbic acid, Vitamin C). The main and lateral
Asample is the absorbance of the sample.
roots had the highest activity of antioxidants (Table 3). The DPPH radi-
We determined the IC50 for each sample, which was the concentra-
cal scavenging ability from the Moringa leaves was three times more
tion of the inhibitor reduced by half. The experiment was repeated three
than the reference compound, while the roots were 70 times more
times each with two replications.
(Table 3).
2.4.6. Ferric-reducing antioxidant power (FRAP) assay
Ferric-reducing power of the leaf and roots of the Moringa plants 3.4. Ferric-reducing power assay activity
was carried out following the method of Lim et al. (2009). Briefly, ex-
tracts of the plant parts (50 μL) at 6.25 mg/mL and the positive control The ability of different concentrations of extracts found in Moringa
butylated hydroxytoluene (BHT) were added to a 96-well microtitre. leaves and roots in reducing Fe3+ complex to Fe2+, is shown in Fig. 2.
40 μL of potassium phosphate buffer (0.2 M, pH 7.2) and 40 μL of potas- As the concentration of all extracts from leaves and roots increased,
sium ferricyanide (1% in phosphate buffer, w/v) were then added to the the reducing power also increased. The antioxidants in the leaf extracts
well and this was incubated for 20 min at 50 °C. Soon after incubation,
40 μL trichloroacetic acid (10% in phosphate buffer, w/v), 150 μL distilled
water and 50 μL FeCl3 (0.1% in phosphate buffer, w/v) were added. A Table 1
microtiter reader (Opsys MRTM, Dynex Technologies Inc., Palm City, Total phenolic compounds, condensed tannins and flavonoids in the leaves, main and lat-
FL, USA) was used to measure the absorbance at 630 nm of the Fe2+ eral roots of Moringa oleifera. Flavonoid and total phenolics values expressed as gallic acid
produced from the reduction of the Fe3+/ferricyanide complex. equivalent (GAE), condensed tannins in leucocyanidin equivalent (LE) and catechin equiv-
alents (CAT) per gram of dry weight (DW), respectively.

2.5. Statistical analysis Plant part Phytochemical

Total phenolics Condensed tannins Flavonoids

One-way analysis of variance (ANOVA) was carried out on the data (mg GAE/g DW) (mg LE/g DW) (mg CAT/g DW)
to determine the differences in means (± SE) of the phytochemical Leaves 0.97 ± 0.05a 0.06 ± 0.00a 0.09 ± 0.00a
and antioxidant properties between the leaf and root of Moringa. The Main roots 0.11 ± 0.01b 0.15 ± 000b 0.16 ± 0.07a
post hoc-Duncan's multiple range test was used to separate the bioactiv- Lateral roots 0.19 ± 0.01b 0.44 ± 0.01c 0.36 ± 0.06b
ity property means (±SE), with p-values less than 0.05 being statisti- Mean values (±SE) in the same column with different letters are significantly different (p
cally significant. All statistical analyses were carried out using the IBM ≤ .05; n = 3) due to Duncan's Multiple Range test.
 T. Tshabalala et al. / South African Journal of Botany 129 (2020) 106–112 109

Table 2 0.25
Leaves
Antimicrobial activities (Minimum Inhibitory Concentration – MIC mg/mL) of Moringa
0.20 Main Root

Ab 630 nm Fe2+
oleifera leaves and roots (main and lateral) extract on various micro-organisms as deter-
mined by the microdilution method. Lateral Root
0.15 BHT
Micro-organism (MIC mg/mL)
0.10
Plant part Solvent Bs Ec Sa Ca
Leaves Acetone 0.78 0.78 0.78 3.13
0.05
Ethanol 0.78 0.78 0.39 3.13
Water 1.56 0.78 0.78 3.13
0.00
Main roots Acetone 0.78 0.78 0.78 6.25
0 1 2 3 4
Ethanol 1.56 1.56 0.39 3.13
Concentration (mg/ml)
Water 1.56 3.12 0.78 6.25
Lateral roots Acetone 0.78 1.56 0.78 6.25
Ethanol 1.56 1.56 0.78 6.25 Fig. 2. Ferric reducing activity of the leaves, main and lateral root extracts of Moringa
Water 1.56 3.12 0.78 6.25 oleifera. BHT- butylated hydroxytoluene was used as positive control.
Neomycin 1.6 × 10−3 0.8 × 10−3 1.6 × 10−3
Amphotericin B 9.77 × 10−3

Bs- Bacillus subtilis; Ec- Escherichia coli; Sa- Staphylococcus aureus; Ca- Candida albicans. phytochemical analysis corroborates our findings showing that there
Values in bold are considered to be active (MIC b 1 mg/mL). is a better total flavonoid content in the roots than in leaves (Etejere
et al., 2015; Idowu and Oseni, 2015; Vyas et al., 2015). Flavonoids are
polyphenolic compounds consisting of a group of benzo-γ-pyrone
had better reducing strength than those in main and lateral root ex- structures and occur in almost every plant part, and they are responsible
tracts, respectively. for antimicrobial, anticancer and antiaging activities (Kumar and
Pandey, 2013). The flavonoids found in Moringa include myricetin,
3.5. The antidiabetic activity quercetin, kaempferol, isorhamnetin and rutin (Leone et al., 2015b).
Saini et al. (2016) and Siddhuraju and Becker (2003) reports that the
The leaf extracts and the control (acarbose) had significantly higher flavonoids, quercetin and kaempferol are predominantly found in the
(p ≤ .05) antidiabetic activity compared to both the main and lateral leaves and not in the roots. These flavonoids have potent antioxidant
roots (Table 3). The leaves had significantly similar antidiabetic activity properties (Saini et al., 2016). Additionally, flavonoids like quercetin
compared to the reference/positive control. In this study, this was con- have been attributed as antioxidants that bring about a scavenging ef-
sidered to be good activity. There was more evidence of antidiabetic ac- fect on ROS released from mitochondria, thereby protecting the beta
tivity detected in the leaf extracts compared to the main and lateral root cells and in turn keeping ailments such as hyperglycaemia controlled
extracts (Fig. 3). However, the leaves and both root plant extracts per- (Michalak, 2006; Al-Malki and El Rabey, 2015). The flavonoids found
formed below the acarbose which served as the control. in the leaves in our study explain the better performance of the antiox-
idant activity from leaves compared to roots (Fig. 2).
4. Discussion The variation in literature on the nutritional and bioactive com-
pounds found in Moringa (Shih et al., 2011; Ndhlala et al., 2014; Leone
4.1. Total phenolics, condensed tannin and flavonoid content et al., 2015a; Leone et al., 2015b) can be mainly attributed to the envi-
ronmental factors including soil conditions or fertiliser treatments
Plants produce phenolics to act as a defence mechanism against her- (Ncube et al., 2012; Dania et al., 2014), plant genetics and different ex-
bivory by animals or micro-organisms (Bhattacharya et al., 2010). The traction methods (Leone et al., 2015b), that affect the compound con-
results of this study corroborate with other studies, confirming that centrations at any given time. The findings in our study do support the
there are more total phenols in Moringa leaves than in the roots notion of knowing the nutritional and phenolic characteristics of
(Idowu and Oseni, 2015). Most of the Moringa nutrients are found in Moringa cultivated locally, prior to them being incorporated into nutri-
leaves (Leone et al., 2015a) and this entails that leaves are the most at- tional and pharmacological products.
tractive for herbivory, hence a need for more defence mechanisms being Condensed tannins, also known as proanthocyanidins, are defined
located in the leaves. Phenolics are ubiquitous plant compounds having as polymers of flavan-3-ols, classified into procyanidins and
at least one benzene ring (C6) and with one or more hydroxyl groups prodelphinidins which have two hydroxyl OH-groups and three OH-
(Bhattacharya et al., 2010). The phenolic hydroxyl groups are great re- groups in the B-ring, respectively (Francisco et al., 2014). Hagerman
ducing agents as they take part in a termination reaction which involves et al. (1998) report that an increase in the number of condensed tannins
the hydrogen-donating antioxidants reacting with reactive oxygen and results in higher antioxidant ability, because of the increase in hydroxyl
reactive nitrogen species, thereby reducing the cumulative generation groups taking part in the reduction of peroxyl radicals. The high DDPH
of reactive oxygen species (Valentão et al., 2002). scavenging activity of the roots reported in the current study (Table 3)
Congruent to this study, a somewhat similar flavonoid concentra-
tions were reported by Ndhlala et al. (2014). The literature on 100
Leaves
Antidiabetic activity

80 Lateral root
Table 3 Main Root
Antioxidant activity determined by the DPPH scavenging assay and antidiabetic activity as 60 Acarbose
(%)

determined by the α-glucosidase inhibitory activity assay of extracts from the leaf, main
and lateral root extracts of Moringa oleifera. Ascorbic acid (Vitamin C) was used as positive 40
control for the DPPH assay while acarbose was the control for the antidiabetic assay. Mean
values (±SE) in the same column with different letters are significantly different (p ≤ .05;
20
n = 3) due to Duncan's Multiple Range test.

Plant part DPPH activity (EC50) μg/ml Antidiabetic activity (EC50) μg/ml 0
0.0 0.5 1.0 1.5
a a
Leaves 20.54 ± 1.99 40.7 ± 5.2 Sample concentration (mg/ml)
Main roots 0.057 ± 0.03b 870.1 ± 12.0b
Lateral roots 1.23 ± 0.02b 560.7 ± 7.4b
Fig. 3. Antidiabetic activity of the leaves, main and lateral roots of Moringa oleifera.
Ascorbic acid 69.23 ± 1.14c 22.5 ± 0.3a
Acarbose was used as a positive control.
110 T. Tshabalala et al. / South African Journal of Botany 129 (2020) 106–112

can be explained by the high content of condensed tannins in the mitochondrial metabolism and energy production, they are radicals,
Moringa roots. ions or molecules that have an unpaired electron in their outermost
shell of electrons, hence very reactive (Liou and Storz, 2010). These in-
4.2. Antimicrobial activity clude superoxide anion (O2−), hydrogen peroxide (H2O2), and hy-
droxyl radical (HO•) (Ray et al., 2012). Failure of the antioxidants to
Staphylococcus aureus, a Gram-positive bacterium normally found in deal with ROS culminates to oxidative stress which results in damage
the nasopharynx and the skin of humans, is known to cause skin infec- of DNA, protein, lipids (Jaiswal et al., 2013), and may lead to carcinogen-
tions, boils, abscesses (Singer and Talan, 2014) and lung infections lead- esis (Liou and Storz, 2010), diabetes (Fakhruddin et al., 2017), hyperlip-
ing to pneumonia (Nair and Niederman, 2011). Due to the incorrect use idaemia (Sangkitikomol et al., 2014), and ageing (Cui et al., 2012).
of antibiotics, the resistance of the bacteria has been reported to be on The high level of phenolic compounds found in the Moringa leaves
the increase, leading to a more resistant strain called methicillin-resis- (Table 1) could be responsible for the reduction reactions as they con-
tant Staphylococcus aureus (MRSA). The good activity shown by extracts tain free hydroxyl compounds which combat oxidation activity
from Moringa in this study may offer potential solutions against the (Valentão et al., 2002). In the current study, the antioxidant activity in
MRSA (Liu et al., 2011). We recommend future studies should explore the leaves and roots was lower than that of the reference compound bu-
the antimicrobial potential of Moringa against MRSA. tylated hydroxytoluene (BHT) (Fig. 2). However, the antioxidant activ-
Candida albicans is normally a non-harmful fungus found on the skin ity in Moringa has been reported to reduce oxidative stress and
and mucous membranes of the mouth, intestines and the vagina. The prevent degenerative disease such as diabetes through regular intake
pathogen becomes harmful when the optimum conditions of the body of leaves (Sangkitikomol et al., 2014).
change, which can be caused by overuse of antibiotics (Samonis et al.,
1994), taking a diet high in carbohydrates and in immunocompromised 4.4. Antidiabetic activity
individuals (Silva, 2010). Infections caused by C. albicans include
chronic mucocutaneous candidiasis, gastrointestinal tract candidiasis, Diabetes mellitus is a common chronic disease, with an estimated
oesophageal candidiasis, respiratory tract candidiasis and vulvovaginal 422 million people globally living with the disease (World Health
candidiasis. In the current study, none of the tested Moringa extracts Organization, 2016). The disease occurs either when the pancreas
showed any noteworthy activity against C. albicans. However, extracts does not produce sufficient insulin (Type 1 diabetes) or when the
from Moringa seeds have been reported to lower C. albicans activity body cannot efficiently use the insulin (Type 2 diabetes). Type 2 diabe-
(Rocha et al., 2014). tes accounts for about 90% of the diabetes cases globally (World Health
Organization, 2018). Type 2 diabetes is caused by a decreased insulin se-
4.3. Antioxidant activity cretion resulting in increased blood glucose which takes part in glycol-
ysis in the mitochondria of beta cells which then form reactive oxygen
Free radicals are reactive molecular species that contain an unpaired species (ROS) (Cerf, 2013). ROS results in oxidative stress, which leads
electron, making them take part in redox reactions (Cheeseman and to depletion of antioxidants in the body and promotes the generation
Slater, 1993). Free radicals are either internally generated in the of free radicals which cause apoptosis of pancreatic beta-cells and
human body, from mitochondria, peroxisomes and through phagocyto- hyperglycaemia (Pi et al., 2010; Gandhi et al., 2012). Managing diabetes
sis or can be exogenously derived from X-rays, cigarette smoking and air may involve inhibiting α-amylase and α-glucosidase enzymes which
pollutants (Bagchi and Puri, 1998). The role of antioxidant compounds are responsible for the conversion of dietary starch to glucose
is to combat the free radical mediated oxidation of other molecules, (Casirola and Ferraris, 2006).
which lead to various degenerative disorders such as mutagenesis, Natural products from plants are preferred in the regulation of glu-
type 2 diabetes, carcinogenesis and ageing (Singh and Singh, 2008). cose levels, because of less complications arising from side effects
The 2, 2-diphenyl-β-picrylhydrazyl (DPPH) radical scavenging activity (Ivorra et al., 1989).The results of this study corroborates with findings
assay represents the potential of antioxidant activity against free radi- from other studies where the levels of phenolic compounds have been
cals in the human body. DPPH is a stable free radical which can change reported to be positively correlated with α-glucosidase (Molan and
to a stable diamagnetic molecule when it accepts an electron (Bijaya Mahdy, 2016). Although phenolic compounds form part of a suite of
and Bikash, 2013). The EC50 value of the DPPH radical scavenging activ- phytochemical compounds in a plant extract, it is tempting to speculate
ity assay represents the concentration of a test sample needed to de- that the high amount of total phenolics recorded in the leaves in this
crease the initial concentration of DPPH by 50% (Atoui et al., 2005). study (Table 1), could, to some extent, account for higher antidiabetic
The higher DPPH radical scavenging ability observed in the and antioxidant activities of the leaf extract than those of the roots. Phe-
roots could be attributed to the condensed tannins found in the roots nolic compounds in Moringa contribute to the antioxidant properties
(Table 1) which contain hydroxyl groups (OH) which take part in anti- and these can combine with the ROS and prevent apoptosis of cells
oxidant reactions (Hagerman et al., 1998). Vitamin C, which was used (Jaiswal et al., 2013; Al-Malki and El Rabey, 2015).
as a reference compound in this study, is an essential nutrient needed
by humans for muscle tissue formation, to protect cellular damage, 5. Conclusions
boost the immune system and is a potent water-soluble antioxidant
(Padayatty et al., 2003). Studies have shown that Moringa can also pro- A comparative antioxidant, antimicrobial, antidiabetic and phyto-
vide seven times more Vitamin C than in orange fruits (Rockwood et al., chemical analysis of leaves, main and lateral roots of Moringa was car-
2013). Antioxidants occur naturally in foods and this study suggests that ried out. There were significant (p ≤ .05) variations in the observed
Moringa is potentially a better source of antioxidants, which can be in- medicinal properties amongst the different studied Moringa plant
corporated into diet plans, skin products and anti-ageing products. parts (leaves, main and lateral roots). All the plant parts had better an-
The ferric-reducing antioxidant power (FRAP) assay activity mea- tioxidant activity than the reference compound ascorbic acid. The roots
sures the ability of the antioxidants (reductants) to reduce the Fe3 + can be used as a better source of antioxidants than the leaves. Leaf ex-
complex of tripyridyltriazine (Fe(TPTZ)3+) to ferrous form Fe2+ com- tracts had significantly good antidiabetic activity when compared to
plex (Fe(TPTZ)2+). This action by the antioxidants is characterised by the reference compound (acarbose). The leaf extracts exhibited the
higher absorbance values at λ 630 nm after the donation of electrons highest amount of total phenolics, while the lateral roots had higher
(Steenkamp et al., 2006). In the human body, this assay can be trans- amounts of condensed tannins and flavonoid contents. The different
lated to the reduction of reactive oxygen species (ROS) by antioxidants plant parts of Moringa can be used as a natural source to fight against in-
to more stable products (Prior et al., 2005). ROS are bi-products of fectious diseases caused by various microorganisms, which are rapidly
 T. Tshabalala et al. / South African Journal of Botany 129 (2020) 106–112 111

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flammatory activity of polyphenols on dendritic cells. Polyphenols in Human Health
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This study was supported by the Department of Science and Tech- Leone, A., Spada, A., Battezzati, A., Schiraldi, A., Aristil, J., Bertoli, S., 2015b. Cultivation, ge-
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