JOURNAL OF ADVANCEMENT IN
MEDICAL AND LIFE SCIENCES
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Open Access
Research Article
Phytochemical investigation and TLC screening for antioxidant activity of 24 plant species
consumed by the Eastern Lowland Gorillas (Gorilla beringei ssp. graueri: Hominidae,
Primates) endemic to Democratic Republic of the Congo
Koto-te-Nyiwa Ngbolua1,*, Kambale Saa-Sita Dalley-Divin1, Malekani M. Jean1, Kyungu Kasolene Jean-Claude2, Kasereka Kataomba Odilon3,
Maloueki Ulrich1, Musuyu Munganza Désiré4, Pius T. Mpiana1, Virima Mudogo1
1
Faculté des Sciences, Université de Kinshasa, BP 190 Kinshasa XI, République Démocratique du Congo
2
Université de Goma, Nord Kivu, République Démocratique du Congo
3
Université Officielle de Ruwenzori, Nord Kivu, République Démocratique du Congo
4
Faculté des Sciences pharmaceutiques, Université de Kinshasa, République Démocratique du Congo
*Corresponding author: Koto-te-Nyiwa Ngbolua
Associate Professor,
Department of Biology, Faculty of Science,
University of Kinshasa, P.O. BOX 190
Kinshasa XI, Democratic Republic of the Congo.
E-mail: jpngbolua@unikin.ac.cd
Tel.: +243 81 68 79 527
Received: May 1, 2014, Accepted: May 22, 2014, Published: May 22, 2014.
ABSTRACT
Humans and great apes (bonobos, chimpanzees, gorillas, and orangutans) share a common gut anatomy. Although, some
diseases that cause countless deaths in humans are ineffective or have minor non disturbing effects in apes. Because of their
phylogenetic closeness and common neural pathways of chemosensory perception, humans and great apes, when displaying
symptoms of illness could alter their foraging to ingest non-nutritive chemical as diet (pharmacophagy). The aim of the present
study was to evaluate the chemical composition and the radical scavenging activity of 24 plants consumed by Gorilla beringei ssp.
Graueri. Flavonoids and proanthocyanidins plant contents were evaluated by Aluminium nitrate method and vanillin-HCl assay
respectively. Antioxidant activity was carried out by TLC bioautography method using 1,1-diphényl1- 2-picrylhydrazyle radical as
model. The results of chemical screening revealed the presence of alkaloids, cardiotonic heterosids, tannins, quinones, flavonoids,
terpenoids and steroids. 12 plant species Begonia meyeri-johannis, Blotiella crenata, Cyathea manniana, Englerina
woodfordioides, Galiniera saxifraga, Mimulopsis excellens, Myrica mildbraedii, Neoboutonia macrocalyx, Piper capense,
Psychotria palustris, Solenostemon thyrsiflorum and Triumfetta cordifolia were found to contain flavonoids concentration higher
or to equalizes to 1 mg QE/g extract. These plants displayed antioxidant activity thus justifying the role of animal self-medicative
behaviour as source of possible epigenome modulators and may aid in the control of infectious diseases through the consumption
of non-nutritive phytochemicals by infected animals. The results suggest that zoopharmacognosy might be a promising and
complementary source of nutraceuticals for human health care including Sickle cell Disease; an ischemic disease causes by
reactive oxygen species.
Keyword: Gorilla beringei graueri, medicinal foods, zoo-pharmacognosy, TLC Bioautography, Virunga National Park,
Democratic Republic of the Congo
INTRODUCTION
Recent
findings
have
revealed
that
ethno-pharmacology plays a key role as source of new drugs [1,
2]. This approach using ethno-botanical surveys can provide
useful information as a pre-screen to select plant for experimental
studies. However, the ethno-pharmacological approach has some
limitations in its application particularly the reluctance of
traditional practitioners to disclose their secret and the lack of
J. of Advancement in Medical and Life Sciences
consensus among healers relating to the use of certain medicinal
plants. For this purpose, the alternative strategy uses
zoo-pharmacognosy approach for identifying bioactive agents
from plants or invertebrates [3]. It is a mean by which animal
self-heal. The self-medicative behaviour is well documented in
non-human primates’ practice. Indeed, because of their
phylogenetic closeness and common neural pathways of
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1
chemosensory perception, humans and great apes, when
displaying symptoms of illness learn to select some biological
resources as medicine [4, 5]. Great apes are a good model for
human pathology and physiology. The use of plants in
self-medication by the non-human primates was reported to be an
advantage in protecting them against diseases [6]. In order to
discover new effective molecules against human diseases, some
researchers have been studying for several years, the
self-medication behaviour in wild great apes in order to identify
compounds based plants they use for as medicine [5, 6]. The
biosynthesis of such secondary metabolites occurs in plants as a
result of selective pressure exerted by microbes, phytophagous
invertebrates and vertebrates. These compounds protect plant
species from predators and pathogens [7]. Surprisingly, some of
such non-nutritional metabolites are the major source of drugs for
human health care. This is the case of artemisinin, quinine, taxol,
morphine and codeine isolated from medicinal plants [8].
The aim of the present study was to evaluate the
phytochemical composition and antioxidant activity of 24 plant
species consumed by the Eastern Lowland Gorillas (Gorilla
beringei ssp. graueri: Hominidae, Primates) endemic to the
mountainous forest of eastern Democratic Republic of the Congo.
MATERIALS AND METHODS
Plant samples collection and identification
Specimens of twenty-four plant species included in the diet of
Eastern Lowland Gorillas (figure 1) were collected in December
2012 in the “Mont Tshiabirimu” (Virunga National Park) and
identified first with the help of the field assistants, and by
comparison with already identified herbarium specimens
collection at the herbarium of the Faculty of Science (University
of Kinshasa) with the help of INERA (Institut National d’Etudes
et de Recherches Agronomiques) botanist team, especially Mr.
Anthony Kikufi, Mr. Zamena Nsita Jonas, and Mr. Nlandu
Lukebakio Boniface. Voucher specimens are on deposit at the
same herbarium.The plants were collected in the Lubero territory,
located in DR Congo, between 0°30’ to 0°34’ N and 28°00’ to
29°30’ E.
Extraction and chemical screening
The dried and powdered plant material (10 g) was repeatedly
extracted by cold percolation with methanol (MeOH) (100 mL x
2) for 48 hours. Fractions were filtered and concentrated to
dryness under reduced pressure using a rotary evaporator.
Chemical screening was done using an established protocol as
previously reported [9, 10].
Antioxidant activity
The DPPH free radical (1,1-diphenyl-2- picrylhydrazyl )
scavenging assay was carried out by TLC bioautography method
as previously reported [11]. The radical scavenging activity of
extracts for DPPH free radical was measured on the principle that
antioxidants reduce the DPPH radical to a yellow-coloured
compound (diphenylpicrylhydrazin) and the extent of the reaction
will depend on the hydrogen donating ability of the antioxidant.
Plant extracts were spotted on silica gel sheets (Silica gel 60 F254
TLC plates) and developed in AcOEt-CH3COOH-HCOOH-H2O
(100: 11: 11: 27) and butanone-2 / toluène (4: 6 ; v/v). Plates were
sprayed with methanolic solution of DPPH radical (0, 2%).
Chlorogenic acid, cafeic acid, quecertin and isoquercitin were
used as reference controls. The active constituents were detected
as yellow smear or spots on a violet background. Only zones
J. of Advancement in Medical and Life Sciences
where their color turned from violet to yellow within the first 30
min (after spraying) were taken as positive results.
Polyphenols quantification
Determination of total proanthocyanidin content
The proanthocyanidin content was determined
spectrophotometrically in the extracts by the vanillin-HCl assay as
previously described [12]. Briefly, 0.5 mL of plant extract
solution (0.1 mg/mL) was mixed with 3 ml of 4% de vanilline–
MeOH mixture and 1.5 mL of hydrochloric acid. The mixture was
allowed to stand for 15 min and the absorbance was monitored at
500 nm using a GENESYS 10S UV-Vis spectrophotometer. The
measurements were done in triplicate. For the cathechin standards,
a calibration curve (Pearson’s correlation coefficient: R2 = 0.999)
was constructed and the level of proanthocyanidin for each sample
was expressed as cathechin equivalents (mg CE/g extract). The
negative control solution consist of 0,5 mL of methanol instead of
plant extract.
Determination of flavonoid content
Total
flavonoid
content
was
determined
spectrophotometrically in the extracts according to the method
described by Rahmat et al. [13]. Briefly, 0.25 mL of methanolic
plant extract (1 mg/mL) and quecertin standard solution was
mixed with 1.25 mL of distilled water in a tube test, followed by
addition of 75 µL of a 5% (w/v) sodium nitrite solution. After 6
min, 150 µL of 10% (w/v) AlCl3 solution was added, and the
mixture was made up to 2.5 mL with distilled water and mixed
well. The absorbance was monitored at 510 nm using a
GENESYS 10S UV-Vis spectrophotometer. The measurements
were done in triplicate. The results of samples were expressed as
mg of quecertin equivalents of total extractable compounds (mg
QE/g extract). The negative control solution consists of 1 mL of
methanol instead of plant extract.
Figure 1: Gorilla beringei ssp. graueri (Hominidae,
Primates)
RESULTS AND DISCUSSION
Chemical screening
The results of chemical screening 24 plant species are presented in
Table 1. These plants are belonging to 19 families and 24 genera.
Asteraceae family is the most represented with four species
(16.67%) confirming that this family is one of the largest
angiosperm families [14].
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Table 1: Chemical screening of plant species consumed by Gorilla beringei graueri (Matschie, 1914)
It is deduced from the table 1 that on 24 investigated plants, only two (8, 3%) contain alkaloids (Ilex mitis and Xymalos monospora), six
plants (or 25%) contain
Plant species
Alkaloids
Flavonoids
Secondary
metabolites
Cardiotonc
heterosids
Quinones
Tanins
Terpenoids et steroids
1
Arundinaria alpina K Schum.
-
+
-
+
-
+
2
Basella alba L.
-
-
-
-
-
+
3
Begonia meyeri-johannis Engl.
-
+
-
+
-
+
4
Blotiella crenata (Alston) Schelpe
-
+
-
+
-
+
5
Pteridium centrali-africanum (Hieron. ex R.E. Fries)
Alston
-
+
+
-
+
6
Cyathea manniana Hook.
-
+
+
+
-
+
7
Englerina woodfordioides (Schweinf.) Balle
-
+
+
+
-
+
8
Galiniera saxifraga (Hochst.) Bridson
-
+
+
-
+
+
9
Gynura scandens O. Hoffm.
-
-
-
-
-
+
10
Ilex mitis (L.) Radlk.
+
+
-
-
-
-
11
Mikania cordata (Burm.f.) B.L.Rob.
-
-
-
-
-
+
12
Mikaniopsis sp.
-
-
-
-
-
+
13
Mimulopsis excellens Lindau
-
+
-
+
-
+
14
Myrica mildbraedii Engl.
-
+
+
-
+
+
15
Neoboutonia macrocalyx Pax
-
+
-
+
-
+
16
Piper capense L.f.
-
+
-
+
-
+
17
Psychotria palustris E.M.A.Petit
-
+
+
-
+
+
18
Rapanea melanophloeios(L) Mez
-
-
-
+
-
+
19
Rubus kirungensis Engl.
-
+
-
+
+
+
20
Solenostemon thyrsiflorum (Lebrun & L. Touss.) Troupin
-
+
-
+
-
+
21
Triumfetta cordifolia A. Rich.
-
+
-
+
+
+
22
Urera hypselodendron (Hochst. ex A. Rich.) Wedd.
-
-
-
+
-
+
23
Vernonia ampla O. Hoffm.
-
-
-
+
-
+
24
Xymalos monospora Baill
+
+
-
-
+
-
-
cardiotonic heterosids; seven plant species (29,2%) contain the tanins; 14 plants (58,3%) contain quinones; 17 plants (70,8%) contain the
flavonoids and 21 plants (87,5%) contain terpenoids and steroids. In terms of the number of secondary metabolites, Basella alba,
Gynura scandens, Mikania cordata and Mikaniopsis sp. are the plants which contain less compounds, since they contain one chemical
group on the six identified ones. Figure 2 shows TLC profiling of plant extracts containing quinones as revealed by NaOH or NH4OH
10% (colored spots).
Figure 2 : TLC chromatogram of plant extracts containing quinones (butanone – 2/toluene, 40:60 ), obsercation under UV lamp at the
wavelength of 366 nm.
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Figure 3: TLC chromatogram of plant extracts displaying radical scavenging activity.
Figure 3 shows TLC bioautography chromatogram profiling of plant extracts containing quinones as revealed by the methanolic solution
of DPPH radical (0,2%).
It can deduce from this figure that the plant species Pteridium centrali-africanum, Galiniera saxifraga, Myrica mildbraedii,
Psychotria palustris, Rubus kirungensis, Triumfetta cordifolia and Xymalos monospora are displayed interesting radical scavenging
activity, as revealed by the yellow smear or spots on the bioautobiography TLC chromatograms. Other plants like Arundinaria alpina,
Begonia meyeri-johannis, Blotiella crenata, Gynura scandens, Ilex mitis, Neoboutonia macrocalyx, Piper capense and Solenostemon
thyrsiflorum showed a weak anti-oxidant activity.
The table 2 lists the plants species consumed by Gorilla beringei graueri in alphabetical order of their scientific names (in
italic), followed by their families, their Congolese vernacular names, the used parts and their phenolic content.
N°
Scientific names (Family)
Vernacular
names (Nande)
Used parts
Polyphenols content (mg/g DW)
Proanthocyanidins
Flavonoids
1 Arundinaria alpina K Schum. (Poaceae)
Mulonge
Leaves
0,1815 ± 0,006
0,726 ± 0,003
2 Basella alba L. (Basellaceae)
Ndenderu
Whole plant
0,087 ± 0,0001
No evaluated
3 Begonia meyeri-johannis Engl. (Begoniaceae)
Virererere
Leaves
0,3 ± 0,0001
1,638 ± 0,014
4 Blotiella crenata (Alston) Schelpe (Dennstaedtiaceae)
Pteridium centrali-africanum (Hieron. ex R.E. Fries) Alston
5 (Dennstaedtiaceae)
Muvale
Leaves
0,1 ± 0,0001
2,215 ± 0,0001
Kasula
Rhizomes
0,574 ± 0,0001
0,734 ± 0,003
6 Cyathea manniana Hook. (Cyatheaceae)
Kisembe
Leaves
0,106 ± 0,0001
1,414 ± 0,004
7 Englerina woodfordioides (Schweinf.) Balle (Loranthaceae)
Ngatikatika
Leaves
0,127 ± 0,002
1,087 ± 0,002
8 Galiniera saxifraga (Hochst.) Bridson (Rubiaceae)
Mulyangote
Stem bark
1,3655 ± 0,0006
0,69 ± 0,002
9 Gynura scandens O. Hoffm. (Asteraceae)
Kirimyamuliro
Whole plant
0,11 ± 0,0001
No evaluated
10 Ilex mitis (L.) Radlk. (Aquifoliaceae)
Mwise
Stem bark
0,052 ± 0,0001
0,2975 ± 0,0006
11 Mikania cordata (Burm.f.) B.L.Rob. (Asteraceae)
Mukohya
Stem bark
0,08 ± 0,0001
No evaluated
12 Mikaniopsis sp. (Asteraceae)
Muhururu
Stem bark
0,101 ± 0,0001
No evaluated
13 Mimulopsis excellens Lindau (Acanthaceae)
Mughunda
Leaves
0,121 ± 0,0001
2,248 ± 0,0001
14 Myrica mildbraedii Engl. (Myricaceae)
Munzikili
Stem bark
1,4575 ± 0,0016
0,636 ± 0,002
15 Neoboutonia macrocalyx Pax (Euphorbiaceae)
Vyona
Whole plant
0,124 ± 0,002
2,011 ± 0,003
16 Piper capense L.f. (Piperaceae)
Matumbitumbi
Stem bark
0,142 ± 0,0001
2,3245 ± 0,0026
17 Psychotria palustris E.M.A.Petit (Rubiaceae)
Mutahitsya
Stem bark
0,3135 ± 0,0006
1,0925 ± 0,0027
18 Rapanea melanophloeios (L) Mez (Primulaceae)
Mungokwe
Stem bark
0,112 ± 0,0001
No evaluated
Mahwa
Leaves + Stem
0,166 ± 0,003
2,203 ± 0,004
Viryanzweve
Leaves
0,187 ± 0,0001
2,2835 ± 0,0006
19
Rubus kirungensis Engl. (Rosaceae)
Solenostemon thyrsiflorum (Lebrun & L. Touss.) Troupin
20 (Lamiaceae)
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21 Triumfetta cordifolia A. Rich. (Malvaceae)
Urera hypselodendron (Hochst. ex A. Rich.) Wedd.
22 (Urticaceae)
Kitembekali
Leaves
Rise
Leaves
23 Vernonia ampla O. Hoffm. (Asteraceae)
Mbatule
Stem bark
24 Xymalos monospora Baill (Monimaceae)
Kitinde
Stem bark
It is deduced from the table 2 that the plants Galiniera
saxifraga (1, 3655 ± 0, 0006 mg CE/g extract) and Myrica
mildbraedii (1, 4575 ± 0, 0016 CE mg/g extract) displayed high
amount of proanthocyanidins, but no significant difference were
observed between the two plants (P>0.05). Between the lowest
and the highest values, the difference was statistically significant
(P<0.05); the plant Urera hypselodendron having the lowest
proanthocyanidins concentration (0,099 ± 0, 0001 CE mg/g
extract) while Myrica mildbraedii revealed the highest
concentration of proanthocyanidins (1, 4575 ± 0, 0016 CE mg/g
extract). According to flavonoids content, the plants Begonia
meyeri-johannis (1,638 ± 0,014 mg QE/g extracr), Blotiella
crenata (2,215 ± 0,0001 mg QE/g extract), Cyathea manniana
(1,414 ± 0,004 mg QE/g extract), Englerina woodfordioides
(1,087 ± 0,002 mg QE/g extract), Mimulopsis excellens (2,248 ±
0,0001 mg QE/g extract), Neoboutonia macrocalyx (2,011 ± 0,003
mg QE/g extract ), Piper capense (2,3245 ± 0,0026 mg QE/g
extract), Psychotria palustris (1,0925 ± 0,0027 mg QE/g extract),
Rubus kirungensis (2,203 ± 0,004 mg QE/g extract),
Solenostemon thyrsiflorum (2,2835 ± 0,0006 mg QE/g extract)
and Triumfetta cordifolia (2,731 ± 0,025 mg QE/g extract) were
found to be rich in flavonoïds. Between the lowest (Ilex mitis: 0,
2975 ± 0, 0006 mg QE/g extract) and the highest flavonoids values
(Triumfetta cordifolia: 2,731 ± 0,025 mg QE/g extract), the
difference is also statistically significant (P<0.05). From the table
2, it can also deduce that leaves are rich in flavonoids followed by
the barks, while the proanthocyanidins were well represented in
Galiniera saxifraga (1, 3655 ± 0, 0006 mg CE/g extract) and
Myrica mildbraedii (1, 4575 ± 0, 0016 mg CE/g extract).
Increasing evidence accumulated over the last decade
indicates that reactive oxygen species (ROS) play a key role in the
pathophysiology of various ailments including parasitic, chronic
and neurodegenerative diseases [15]. The results outlined in this
paper, revealed the scavenging effects of some plant species
consumed by Gorilla beringei graueri indicating that such plant
species could protect them from these diseases. Indeed, great apes
constitute a reservoir for human pathogens and can serve as
sentinels for surveillance of emerging pathogens by providing
models for basic research [16]. Natural products were reported to
interact with the immune system to either up-regulated or
down-regulated specific aspects of the host response by modifying
the immune system to enhance the ability of organism to resist
invasion by infectious pathogens [17]. It could be hypothesized
that the animal self-medicative behavior may aid in the control of
infectious diseases through the consumption of non-nutritive
phytochemicals by infected animals [18]. So, infectious diseases
such as malaria does not seem cause any harm or illness to the
great apes like besides the case for the sickle cell disease trait [4,
19-21].
Recent findings indicate that phenolic antioxidants
such as flavonoids and proanthocyanidins function as potent
modulators of the mammalian epigenome-regulated gene
expression through regulation of DNA methylation, histone
acetylation, and histone deacetylation in human experimental
J. of Advancement in Medical and Life Sciences
0,3225 ± 0,0006
2,731 ± 0 ,025
0,099 ± 0,0001
No evaluated
0,128 ± 0,0001
No evaluated
0,2305 ± 0,0006
0,605 ± 0,004
models. Naturally occurring dietary polyphenols can modulate
signaling pathways mediated via NF-κB and MAP kinase, and
up-regulate glutathione biosynthesis genes through activation of
Nrf2. Polyphenols also down-regulate the expression of
pro-inflammatory mediators, matrix metalloproteinases and
adhesion molecules by inhibiting histone acetyltransferase
activity and activating histone deacetylases [22,23]. It is thus
possible that the consumption of antioxidant phenolics such as
flavonoids and proanthocyanidins by the great apes especially
Gorilla beringei graueri can modulate their epigenome in order to
protect them from neurodegenerative and/or infectious diseases.
CONCLUSION
The present study evaluated the phytochemical
composition and antioxidant activity of 24 plant species consumed
by the Eastern Lowland Gorillas. The extracts obtained from some
of these plants displayed antioxidant activity. This activity could
be due to phenolic compounds such as flavonoids and
proanthocyanidins. The ability of extracts from plants consumed
by the great apes to display antioxidant properties could partially
justify the role of self-medicative behaviour as source of
epigenome
modulators.
These
results
suggest
that
zoopharmacognosy might be a promising and complementary
source of nutraceuticals for human health care including Sickle
cell Disease, an ischemic disease causes by reactive oxygen
species.
Acknowledgments
This research was supported by the International
Foundation for Science (IFS, Stockholm, Sweden) and the
Organization for the Prohibition of Chemical Weapons (OPCW)
(IFS Research Grant N0 F/4921-2), research grant offered to Dr.
Koto -te- Nyiwa NGBOLUA.
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Citation: Koto-te-Nyiwa Ngbolua, et al (2014). Phytochemical investigation and TLC screening for antioxidant activity of 24 plant species consumed by the Eastern
Lowland Gorillas (Gorilla beringei ssp. graueri: Hominidae, Primates) endemic to Democratic Republic of the Congo. J. of Advancement in Medical and Life Sciences.
V1I3. DOI: 10.15297/JALS.V1I3.02
Copyright: © 2014 Koto-te-Nyiwa Ngbolua. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
J. of Advancement in Medical and Life Sciences
Volume1/Issue3
ISSN: 2348-294X
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