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Medicinal plants of the genus Anthocleista - A review of their ethnobotany,
phytochemistry and pharmacology
Article in Journal of ethnopharmacology · October 2015
DOI: 10.1016/j.jep.2015.09.032
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Journal of Ethnopharmacology 175 (2015) 648–667
Contents lists available at ScienceDirect
Journal of Ethnopharmacology
journal homepage: www.elsevier.com/locate/jep
Review
Medicinal plants of the genus Anthocleista—A review of their
ethnobotany, phytochemistry and pharmacology
Gabriel O. Anyanwu a,c, Nisar-ur-Rehman a,n, Chukwu E. Onyeneke b, Khalid Rauf a
a
Department of Pharmacy, COMSATS Institute of Information Technology, Abbottabad 22060, K.P.K., Pakistan
Department of Biochemistry, University of Benin, Benin City, Edo State, Nigeria
c
Department of Biochemistry, Bingham University, Karu, Nasarawa State, Nigeria
b
art ic l e i nf o
a b s t r a c t
Article history:
Received 25 May 2015
Received in revised form
26 September 2015
Accepted 28 September 2015
Ethnopharmacological relevance: The genus Anthocleista of the Gentianaceae family contains 14 species of
trees and shrub-like plants distributed in tropical Africa, in Madagascar and on the Comoros. Traditionally, they are commonly used in the treatment of diabetes, hypertension, malaria, typhoid fever,
obesity, diarrhea, dysentery, hyperprolactinemia, abdominal pain, ulcer, jaundice, asthma, hemorrhoids,
hernia, cancer, wounds, chest pains, inflammations, rheumatism, STDs, infertility and skin diseases. They
serve as an anthelmintic, laxative, diuretic and contraceptive. This review aims to provide for the first
time a repository of ethnopharmacological information while critically evaluating the relation between
the traditional medicinal uses, chemical constituents and pharmacological activities of the Anthocleista
species so as to unveil opportunities for future research.
Materials and methods: A search for relevant information on Anthocleista species was performed on
scientific databases (Pubmed, Google Scholar, SciFinder, Web of Science, Scopus, PubChem and other web
sources such as The Plant List, Kew Botanical Garden and PROTA) and books, PhD and MSc dissertations
for un-published resources.
Results: Out of the 14 species of Anthocleista, 6 have been reported in literature to be widely used in traditional
medicine for the treatment of various ailments. The six species include: A. djalonensis, A. vogelii, A. nobilis, A.
grandiflora, A. schweinfurthii, and A. liebrechtsiana. The chemical compounds isolated from Anthocleista species
fall into the class of phytochemicals such as secoiridoids, nor-secoiridoids, xanthones, phytosterols, triterpenes,
alkaloids, and others of which majority of the compounds were isolated from A. djalonensis and A. vogelii. The in
vitro and in vivo pharmacological studies on the crude extracts, fractions and few isolated compounds of Anthocleista species showed antidiabetic, antiplasmodial, antimicrobial, hypotensive, spasmogenic, anti-obesity,
antiulcerogenic, analgesic, anti-inflammatory, antioxidant, antitrypanosomal, anthelmintic, fertility, diuretic and
laxative activities which supports most of their uses in traditional medicine. However, the bulk of the studies
where centered on the antidiabetic, antiplasmodial and antimicrobial activities of Anthocleista species, although
the evidence of its antiplasmodial effect was not convincing enough due to the discrepancies between the in
vitro and in vivo results.
Conclusion: A. djalonensis and A. vogelii are potential antidiabetic and antibacterial agents. The antibacterial
potency relates to infections or diseases caused by E. coli, S. typhi and S. aureus such as urinary tract infections,
typhoid, diarrhea, skin diseases, and food poisoning. Pharmacological research on this genus is quite elementary and limited, thus, more advanced research is necessary to isolate and determine the activities of
bioactive compounds in vitro and in vivo, establish their mechanisms of action and commence the process of
clinical research.
& 2015 Elsevier Ireland Ltd. All rights reserved.
Keywords:
Anthocleista
Gentianaceae
Traditional uses
Antidiabetic
Antiplasmodial
Antiobesity
Chemical compounds studied in this article:
1-hydroxy-3,7-dimethoxyxanthone (PubChem CID: 5488808)
3-oxo-Δ4′5-sitosterone (PubChem CID:
9801811)
6-ketobauerenone (not found)
7α-hydroxysitosterol (PubChem CID:
161816)
anthocleistenolide (not found)
anthocleistin (not found)
anthocleistol (not found)
bauerenol (PubChem CID: 111220)
bauerenone (not found)
caryophyllene oxide (PubChem CID:
6604672)
D-(þ )-bornesitol (PubChem CID: 440078)
decussatin (PubChem CID: 5378284)
de-O-methyllasiodiplodin (PubChem CID:
14562693)
djalonenol (not found)
djalonenoside (not found)
djalonensin (PubChem CID: 5360741)
djalonensone (PubChem CID:5359485)
Abbreviations: ACE inhibitors, Angiotensin-converting enzyme inhibitors; ALP, alkaline phosphatase; ALT, alanine transaminase; AST, aspartate aminotransferase; ATCC,
American Type Culture Collection; ATPase, adenosine triphosphatase; b.w, body weight; CCl4, carbon tetrachloride; COX, cyclooxygenase; DPPH, 2,2-diphenyl-1-picrylhydrazyl; EC50, half maximal effective concentration; ED, effective dose; Hb, hemoglobin; HCD, high carbohydrate diet; HDL-C, high-density lipoprotein cholesterol; IC50,
compound inhibition (50% inhibition); LD50, median lethal dose, LDL-C, low-density lipoprotein cholesterol; MCH, mean corpuscular hemoglobin; MDA, Malondialdehyde;
MIC, minimum inhibitory concentration; PCV, Packed cell volume; STDs, sexually transmitted diseases; STIs, sexually transmitted infections (STIs); TC, total cholesterol; TG,
triglycerides; WBC, white blood cells
n
Corresponding author.
E-mail addresses: anyanwugo@ciit.net.pk, gabrielanyanwu@binghamuni.edu.ng (G.O. Anyanwu), nisar@ciit.net.pk (Nisar-ur-Rehman),
bumkel@yahoo.com (C.E. Onyeneke), khalidrauf@ciit.net.pk (K. Rauf).
http://dx.doi.org/10.1016/j.jep.2015.09.032
0378-8741/& 2015 Elsevier Ireland Ltd. All rights reserved.
G.O. Anyanwu et al. / Journal of Ethnopharmacology 175 (2015) 648–667
649
fagaramide (PubChem CID: 5281772)
gentianine (PubChem CID: 354616)
grandiflorol (not found)
grandifloroside (not found)
hexadecanoic acid (PubChem CID: 985)
humulene epoxide II (PubChem CID:
10704181)
irlbacholine (PubChem CID: 177983)
lichexanthone (PubChem CID: 5358904)
lupenone (PubChem CID: 92158)
methyl grandifloroside (not found)
schweinfurthin (PubChem CID: 643463)
scopoletin (PubChem CID: 5280460)
secologanin (PubChem CID: 161276)
sitosterol (PubChem CID:222284)
sitosterol 3-O-β-D-glucopyranoside (PubChem CID: 70699351)
stigmasterol (PubChem CID: 5280794)
sweroside (PubChem CID:161036)
swertiamarin (PubChem CID: 442435)
swertiaperennin (PubChem CID: 5281653)
ursolic acid (PubChem CID: 64945)
vogeloside (not found)
α-humulene (PubChem CID: 5281520)
β-caryophyllene (PubChem CID: 5281515)
Contents
1.
2.
3.
4.
5.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
The classification, botanical description and distribution of Anthocleista . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Ethnomedicinal uses . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Chemical constituents . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Pharmacological activities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
5.1.
Antidiabetic activity. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
5.2.
Antiplasmodial activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
5.3.
Antimicrobial activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
5.4.
Antihypertensive and antihypotensive activities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
5.5.
Spasmolytic and spasmogenic activities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
5.6.
Anti-obesity activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
5.7.
Antiulcerogenic/analgesics, wound healing and anti-inflammatory activities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
5.8.
Antioxidant activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
5.9.
Antitrypanosomal activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
5.10. Anthelmintic activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
5.11. Fertility activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
5.12. Diuretic and laxative activities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
6. Toxicity studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
7. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
1. Introduction
The Anthocleista species are trees and shrub-like plants presently in the Gentianaceae family, and formerly of the Loganiaceae
family, in the major group Angiosperms. The genus Anthocleista
contains about 14 species distributed in tropical Africa, in Madagascar and on the Comoros (Leeuwenberg, 1973, 1992; Leeuwenberg and Leenhouts, 1980; De Wilde, 2011).
The tribe Potalieae includes the genera Anthocleista, Fagraea
and Potalia. The African genus Anthocleista has 15 species, Fagraea has about 35 species in Southeast Asia, tropical Australia
and the Southwest Pacific; and the American genus Potalia is
monotypic (Punt, 1978). Although Punt (1978) mentioned that
Anthocleista had 15 species, the 14 accepted species in
Anthocleista genus include: Anthocleista amplexicaulis Baker,
Anthocleista djalonensis A. Chev., Anthocleista grandiflora Gilg,
649
650
650
654
654
654
657
657
660
661
661
662
662
663
663
663
663
663
664
665
665
Anthocleista laxiflora Baker, Anthocleista liebrechtsiana De Wild.
& T. Durand, Anthocleista longifolia (Lam.) Boiteau, Anthocleista
madagascariensis Baker, Anthocleista microphylla Wernham,
Anthocleista nobilis G. Don, Anthocleista obanensis Wernham,
Anthocleista procera Lepr. ex Bureau, Anthocleista scandens
Hook.f., Anthocleista schweinfurthii Gilg, and Anthocleista vogelii
Planch (http://www.theplantlist.org/).
Anthocleista are generally called “cabbage tree” in English language. This is because the stem of some species are unbranched or
branched only at the top with huge leaves clustered at the end of
the shoot (Keay, 1989). A large proportion of the names used to
describe Anthocleista species seemed to be within the areas or
regions of the country in which they are found. For example, in the
Ijebu land of the western part of Nigeria, Anthocleista spp is called
Sapo sapo (Richards, 1939; Ross, 1954). The Hausas (Northern Nigeria) call it ‘Kwari’ (quiver), the Yorubas (Western Nigeria) call it
650
G.O. Anyanwu et al. / Journal of Ethnopharmacology 175 (2015) 648–667
‘Apa oro’ (Keay Onochie et al., 1964) or sapo and the Ibos (Eastern
Nigeria) call it ‘Mpoto’ (Anyanwu et al., 2013). The local name for A.
vogelii in Cameroon is Kewanten (Neba, 2006). Also, it is called
Ekoka ngowa (Bakweri) in the Southwest and Littoral region of
Cameroun (Jiofack et al., 2010). It is commonly known as ‘AwudifoAkete’ (murderer’s mat) by the Ashante people in Ghana (Irvine,
1961).
Anthocleista has conservative and other traditional uses besides
its medicinal uses. They are a source of food for animals in the
forest, such as birds (turacos), ruminants and primates (gorillas
and chimpanzees) (Gautier-Hion et al., 1980; Dubost, 1984; Calvert, 1985; Basabose, 2002; Babalola et al., 2012). As a tree with
rough and coarse bark, Anthocleista is a preferred host for some
epiphytes in a tropical semideciduous forest of Ghana (Addo‐Fordjour et al., 2009), thereby providing support for this epiphytes
which are food and habitats for many of the animals inhabiting the
rainforest canopies. According to Burkill (1985c), the wood-ash of
A. vogelii is used in making dyes, stains, inks, tattoos and mordants; the wood is used in carpentry and related applications; the
trunk and branches are used in farming, forestry, hunting and
fishing apparatus; the leaf is used in the production of tobacco,
snuff, abrasives, cleaners, etc.
The traditional medicinal uses of Anthocleista is in the treatment of stomach ache, fever, constipation, inflammatory diseases,
diabetes, wounds, etc. (Dalziel, 1955; Ateufack et al., 2014). The use
of medical plants is still popular today because they are considered
safe, less expensive, easily available and effective. The social and
economic statuses of the people are no barrier to their patronage
of herbal medicines in different parts of the world, and most
especially in developing nations. This review aims to provide for
the first time a repository of ethnopharmacological information
while critically evaluating the relation between the traditional
medicinal uses, chemical constituents and pharmacological activities of the Anthocleista species so as to unveil opportunities for
future research.
2. The classification, botanical description and distribution of
Anthocleista
The tribe Potalieae is divided into three subtribes: Faroinae,
Lisianthiinae, and Potaliinae. The last subtribe, Potaliinae
(composed of Fagraea, Anthocleista, and Potalia), was formerly
circumscribed as tribe Potalieae within the family Loganiaceae
(Leeuwenberg and Leenhouts, 1980; Struwe et al., 1994). The
Potaliinae are aberrant in Gentianaceae in having fleshy berries
and a preponderance of large trees (Struwe et al., 2002). This
controversy on the family of Anthocleista either in the Loganiaceae or Gentianaceae has been on for decades in the past.
Bremer et al. (1994) and Struwe et al. (1994) had provided
further evidence that the hypothesis that Loganiaceae sensu
Leeuwenberg and Leenhouts (1980) are a paraphyletic assemblage with members showing closest relationships to other
families both within and outside of the Gentianales as reported
(Meszaros et al., 1996). As far as Gentianaceae is concerned,
Struwe et al. (1994) main conclusion is to formally include
Potalia Aubl., Fagraea Thunb. and Anthocleista Afzel. ex R. Br.
(tribe Potalieae of Loganiaceae sensu Leeuwenberg and
Leenhouts, 1980) in the Gentianaceae. This transfer had already
been proposed by Bureau (1856), then by Fosberg et al. (1980)
on the basis of gross morphology and later by Jensen (1992) on
the basis of the presence of advanced iridoid glucosides as
reported (Meszaros et al., 1996).
Anthocleista is presently under the Gentianaceae family but
its affinities were previously considered to be with the Loganiaceae (Leeuwenberg, 1992). The phytochemical, morphological and
molecular data of Anthocleista supports its transfer to the Gentianaceae (Jensen, 1992; Meszaros et al., 1996; Backlund et al., 2000).
Therefore, the suitable classification of the genus Anthocleista is
the family Gentianaceae of the order Gentianales.
Generally, Anthocleista is a genus of trees, 6–20 m high or more,
trunk 15–55 cm diameter, twigs with spines; leaves opposite, extremely large (up to 150 45 cm2), sessile or very shortly petiolate; lamina dark green and often glossy above; inflorescence
terminal, dichasial or otherwise, large, much-branched; sepals 4,
circular or broader than long. Corolla white (or creamy), actinomorphic, thick, fleshy; lobes 8–16, contorted in bud; ovary is superior and fruit a berry (Bruce, 1955; Leeuwenberg, 1983; De
Wilde 2011; Hyde et al., 2015). However, there are few disparities
among the species as observed in their morphology (Punt and
Nienhuis, 1976; Punt, 1978; Molina and Struwe, 2009; EdwinWosu et al., 2015), phylogenetics (Albach et al., 2001) chemotaxonomy (Jensen and Schripsema, 2002; Sonibare et al., 2007); and
chemical compounds (Jensen et al., 1975; Jensen, 1992).
Anthocleista species are present in tropical Africa, from Sierra
Leone in the west to Uganda in the north and to Angola in the
south (Leeuwenberg, 1983) including Zambia, and Kenya in the
East. Anthocleista species are found in lowland forest and/or
aquatic ecosystem. They are perennial trees with marked preference for tropical climates and prevalent in lowland secondary
rainforests. Anthocleista species are common seral plants on
abandoned farmland in the forest regions of tropical Africa (Keay,
1959). A. djalonensis and A. nobilis show preference for both normal terrestrial (low land dry rainforest) and wetland (seasonally
flooded) environments. A. vogelii shows a preference for normal
terrestrial habitat while A. liebrechtsiana prefers wetland or semi
aquatic habitats (Edwin-Wosu et al., 2015). A. grandiflora are riparian in habitat (Dowsett-Lemaire, 2008).
There is little information about the cultivation of Anthocleista
species, as the plants in this genus are not cultivated plants.
However, A. vogelii has been reported to be grown by traditional
medicine practitioners in Osun State, Nigeria (Alade et al., 2011).
Aside for its medicinal benefits, the reasons for cultivation of the
plant might not exactly be known as the authors did not specify;
however, it might not be far from one or all of the reasons mentioned in the study, which included: easily cultivated, frequently
used, very costly/scarce in the market, easily perishable and plants
that must be used fresh (Alade et al., 2011).
3. Ethnomedicinal uses
Out of the 14 species of Anthocleista, 6 have been reported in
literature to be widely used in traditional medicine for the treatment of various ailments. The six species include: A. djalonensis, A.
vogelii, A. nobilis, A. grandiflora, A. schweinfurthii, and A. liebrechtsiana. They are commonly used for treating constipation,
malaria fever, typhoid fever, hypertension, stomach aches, hemorrhoids, syphilis, diabetes, and used as a contraceptive, laxative
and purgative (Kadiri, 2009; Musa et al., 2010; Olubomehin et al.,
2013). The use of the bark and root of A. vogelii, A. nobilis and A.
schweinfurthii as purgative and antidote for snake bite; the barksap for ear and eye treatments; and the bark and root in the
healing of dropsy, swellings, edema, gout and venereal diseases
have been documented (Burkill, 1985a, b and c).
A. vogelii is widely used by traditional medicine practitioners
either singly or in combination with other plant materials to treat
several diseases or ailments in humans, including infertility problems both in male and female (Oladimeji Igbalaye, Coleshowers
2014). Many young women in Nigeria use A. vogelii and in combination with other plants as contraceptives usually preferred after
sexual intercourse and before pregnancy (Kadiri, 2009). Root
Table 1
Ethnomedicinal uses of Anthocleista species.
Scientific name
Country
Plant part used
Disease condition
Preparation form/ Ethnomedicinal receipe
Reference
Metabolic disorders
A. djalonensis
Bheino modyo (P)
Sapo (Y)
Sapo (Y)
Assoubobissaou (K)
Guinea
Nigeria
Nigeria
Togo
Diabetes
Diabetes
diabetes
diabetes
Decoction
Maceration with five other plants
ni
Decoction or powder, administrated by oral or anal rout
Diallo et al. (2012)
Soladoye et al. (2012)
Olowokudejo et al. (2008)
Tchacondo et al. (2012)
A. vogelii
Diabetes Mellitus
Decoction
A. nobilis
A. vogelii
Sapo (Y), Kwari (H),
Awudifo-Akete (As)
Ekoka ngowa (Bk)
Mpoto (I)
Konibou Kankan (M);
Artaninfiro (M)
uko nkirisi (I)
Nigeria, Ghana
Root
Bark
Bark, Leaves
Roots, the stem bark,
and the leaves
Root
Cameroun
Nigeria
Guinea
Stem bark, Leaves
Root bark
Stem bark
Diabetes
Obesity
Diabetes
Decoction
Maceration
Decoction
Ampofo, (1977), Abuh et al. (1990) and
Soladoye et al. (2012)
Jiofack et al. (2010)
Anyanwu et al. (2013)
Diallo et al. (2012)
Nigeria
Root bark
Diabetes Mellitus
Decoction
Madubunyi et al. (1994)
Ezenukpogan (B)
Nigeria
Leaves and root
Hypertension
Sapo (Y)
Nigeria
Roots
Hypertension
Assoubobissaou (K)
Togo
Benin rope (B) Kwari
(H)
Nigeria
Roots, the stem bark, Hypertension
and the leaves
Stem
Hypertension
Decoction of the grounded leaves and root with little
Gbolade (2012)
water and heat; one spoon taken trice daily
Maceration in combination C. Pilosa, S. Londepedunculata Olorunnisola et al. (2015)
and N. Latifolia/ 1tea spoon 3times daily
Decoction or powder, administrated by oral or anal rout Tchacondo et al. (2012)
Diuretic and purgative
A. djalonensis
Sapo (Y)
A. vogelii
ni
ni
Urugba (Ig)
A. liebrechtsiana Sapo (Y)
Nigeria
Africa region,
Cameroun
Nigeria
Nigeria
Nigeria
Fertility
A. djalonensis
Nigeria
A. vogelii
A. nobilis
A. schweinfurthii
Ohangbakire (Ig) Ibu
(In)
Sapo (Y)
Sapo (Y)
Assoubobissaou (K)
Sapo (Y)
Sapo (Y)
Moukoro (P)
Wudifokεtε/ Hohoroho
(A)
Wudifokεtε/ Hohoroho
(A)
Abanga'a
ni
Maceration; soaked in water for 3day; half glass cup
daily
Gbolade (2012)
ni
Stem bark
antidiuretic, purgative
purgative
ni
ni
Bark and stems
Root/ stem bark
Bark, Leaves
Purgative
Laxative, purgative
Purgative
ni
Boil and drink
ni
Lawal et al. (2010)
Dalziel, (1955) and Adjanohoun et al.
(1986)
Ariwaodo et al. (2012)
Okorie, (1976) and Igoli et al. (2005)
Olowokudejo et al. (2008)
Infertility (male)
Adjanahoun et al., (1991), Igoli et al.
(2005) and Erhabor et al. (2013)
Olowokudejo et al. (2008)
Soladoye et al. (2014)
Tchacondo et al. (2012)
Decoction
ni
Steeping
Decoction
Sharaibi et al. (2014)
Omobuwajo et al. (2008)
Akoué et al. (2013)
Diame (2010)
Ghana
Bark
Decoction
Diame (2010)
Cameroon, Gabon,
Equatorial Guinea
Congo
Bark
Impotence
Female infertility
female infertility and male
infertility
Hyperprolactinemia
Menstrual Dysfunction
Sexual dysfunction
Protrusion retention during
pregnancy
Abdominal pains during pregnancy; menstrual disorders
Ovarian problems
A concoction of the three plants is taken once daily.
Decoction of roots and leaves
ni
ni
Decoction or powder, administrated by oral or anal rout
Nigeria
Nigeria
Gabon
Ghana
Leaves, Roots and
leaves
Bark, Leaves
Bark
Roots, the stem bark,
and the leaves
Bark
Leaf
Root
Bark; leaf
Decoction
Bark
female infertility
Decoction
Kerharo, (1974) and Christophe et al.
(2015)
Schmelzer (2008), Bouquet (1972) Christophe et al. (2015)
Nigeria
Nigeria
Togo
G.O. Anyanwu et al. / Journal of Ethnopharmacology 175 (2015) 648–667
Hypertension
A. djalonensis
Local name (ethnic)
651
652
Table 1 (continued )
Scientific name
Contraceptive
A. vogelii
A. nobilis
Malaria
A. djalonensis
A. vogelii
A. nobilis
A. schweinfurthii
Country
Plant part used
Disease condition
Preparation form/ Ethnomedicinal receipe
Reference
ni
Wudifokεtε/Hohoroho
(A)
Nigeria
Ghana
Roots
Bark/leaf
Contraceptive
Contraceptive
Maceration with three other plants
Decoction
Kadiri et al. (2009)
Diame (2010)
ni
Samatlo (Br)
Mbabaigana (KL)
Nigeria
Mali
Côte-d’Ivoire
Nigeria
Nigeria
Guinea
Ghana
Côte d'Ivoire
Guinea
Southern Africa
South Africa
Tanzania
Malaria
Malaria
Malaria
Malaria fever
malaria
malaria
Malaria
Malaria
Malaria
Malaria
Malaria
Malaria
ni
Decoction (leaves) or Maceration (roots)
Decoction
Decoctions with five other plants
Decoction
Decoction
Decoction
Body smeared with mashed bark
Decoction
Decoctions
Decoction
Decoction
Ajibesin et al. (2008)
Diarra et al. (2015)
Zirihi et al. (2010)
Okorie, (1976) and Igoli et al. (2005)
Madubunyi et al. (1994)
Baldé et al. (2015)
Asase and Oppong-Mensah(2009)
Malan et al. (2015)
Traore et al. (2013)
Palmer and Pitman (1972)
Bapela et al. (2014)
Nondo et al. (2015)
ni
Tanzania
Leaves, stem bark
Leaves, roots
Stem bark
Leaves/ stem bark
Root bark
Root
Stem bark and root
Bark
Stem bark
Bark
Stem bark and leaves
Leaves, stem bark
and roots
Root Bark and leaves
Malaria
Decoction
N.Transvaal
Bark
Malaria
Decoction
Kerharo (1974), Burkill (1995), Fowler
(2006), and Christophe et al. (2015)
Fowler (2006)
Nigeria
Roots
diarrheoa, dysentery
Decoction
Stem bark
ni
Bark
Stem bark
Gastro-intestinal disorders, stomach ache, abdominal pains
Ulcer
Stomach aches
Decoction
Decoction
Urugba (Ig)
uko nkirisi (I)
ni
Odeefuor kete (S)
ni
Bomon (G)
ni
Stomach disorders
A. djalonensis
ni
Akubue et al. (1983), and Nweze and
Ngongeh (2007)
Dalziel (1955) and Adjanohoun et al.
(1986)
Odukoya et al. (2012)
Etonde and Ekwalla (1997), Kerharo
(1974) and Christophe et al. (2015)
Adongo et al. (2012)
A. vogelii
ni
A. nobilis
A. schweinfurthii
A. grandiflora
Epo sapo (Y)
Bopolopolo (D)
Africa region,
Cameroun
Nigeria
Cameroon
Murigurigu (C)
Kenya
Stem bark
ameba
ni
Anthelmintic conditions
A. djalonensis
Nigeria
Roots
Worms
Decoction
A.
A.
A.
A.
Cameroun
Nigeria
Kenya
Tanzania
ni
Root bark
Stem bark
Root Bark and leaves
Intestinal worms
gastrointestinal worms
worms
worms
ni
Decoction
ni
Decoction
Nigeria
Togo
STDs
syphilis
ni
Kayode et al. (2004)
Decoction or powder, administrated by oral or anal rout Tchacondo et al. (2012)
STDs
Gonorrhea Syphilis
Syphilis/gonorrhea
Jiofack et al. (2010)
Omobuwajo et al. (2008)
Okorie (1976) and Igoli et al. (2005)
Kerharo, (1974) and Christophe et al.
vogelii
nobilis
grandiflora
schweinfurthii
ni
uko nkirisi (I)
Murigurigu (C)
ni
Sexually transmitted diseases
A. djalonensis
Sapo (Y)
Assoubobissaou (K)
A. vogelii
A. nobilis
A.
Ekoka ngowa (Bk)
Sapo (Y)
Urugba (Ig)
Cameroun
Nigeria
Nigeria
Root
Roots, the stem bark,
and the leaves
Stem bark, Leaves
Leaf Root
Root
Sapo (Y)
Sapo (Y)
Wudifokεtε/ Hohoroho
(A)
Abanga'a
Nigeria
Nigeria
Stem
Root
Gonorrhea
STIs
STDs (Gonorrhea)
Decoction
ni
Scrape and squeeze or macerate inner root bark, add salt
and take.
ni
ni
Decoction
Cameroon, Gabon,
Bark
venereal disease
Decoction
Akubue et al. (1983), and Nweze and
Ngongeh (2007)
Dibong et al. (2011)
Madubunyi et al. (1994)
Adongo et al. (2012)
Kerharo (1974), Burkill, (1995), Fowler
(2006) and Christophe et al. (2015)
Olukoya et al. (1993)
Gbadamosi (2014)
Diame (2010)
G.O. Anyanwu et al. / Journal of Ethnopharmacology 175 (2015) 648–667
A. grandiflora
Local name (ethnic)
schweinfurthii
Equatorial Guinea
Pain, wounds and inflammations
A. djalonensis
Sapo (Y)
Sapo (Y)
A. vogelii
A. nobilis
A. grandiflora
A. schweinfurthii
Bark, Leaves
Stem bark
antipyretic
Asthma
ni
Cold infusion with 8 other plants/ two tablespoon daily
Cameroun
Nigeria
Guinea
Nigeria
Côte d'Ivoire
Kenya
Tanzania
Stem bark, Leaves
Leaves
Root
Bark
Root
Stem bark
Bark and leaves
Wounds, Inflammations
Wounds
Inflammatory diseases
Wounds
Rheumatism
Chest pains
wound healing
Decoction
Applied as poultice on swellings and to cleanse wound
Decoction
Hot infusion
Topical application with crushed roots
ni
Decoction
Nigeria
Nigeria
Ghana
Leaves
Root
Bark/leaf
Typhoid fever
Throat problems
Candidiasis/white
Decoction
ni
Decoction
Musa et al. (2010)
Omobuwajo et al. (2008)
Diame (2010)
Nigeria
Kenya
Cameroon, Gabon,
Equatorial Guinea
Congo
Tanzania
Bark, Leaves
Stem bark
Bark
antimicrobial
cold
bronchitis
Ni
ni
Decoction
Stem bark
Bark and leaves
Mycosis
Fever
Crushing
Decoction
Olowokudejo et al. (2008)
Adongo et al. (2012)
Kerharo (1974) and Christophe et al.
(2015)
Ngbolua et al. (2014a)
Kerharo (1974), Burkill (1995), Fowler
(2006) and Christophe et al. (2015)
Sapo (Y)
Sapo (Y)
Nigeria
Nigeria
Bark, Leaves
Bark, Leaves
Skin diseases – rashes and eczema ni
Skin infection
Ni
Olowokudejo et al. (2008)
Olowokudejo et al. (2008)
Sapo (Y)
uko nkirisi (I)
Nigeria
Nigeria
ni
Root bark
Jaundice
Jaundice, liver protecting effects
Lawal et al. (2010)
Madubunyi et al. (1994)
Assoubobissaou (K)
Togo
Decoction or powder, administrated by oral or anal rout Tchacondo et al. (2012)
Sapo (Y)
Wudifokεtε/Hohoroho
(A)
Nigeria
Ghana
Roots, the stem bark, hemorrhoids
and the leaves
Bark
Hemorrhoid
Leaves
Hemorrhoids, piles
Assoubobissaou (K)
Togo
Decoction or powder, administrated by oral or anal rout Tchacondo et al. (2012)
Wudifokεtε/ Hohoroho
(A)
ni
Ghana
Roots, the stem bark, Hernia
and the leaves
Leaves
hernia
Infusion/decoction
Diame (2010)
Congo
Bark
Hernia
Decoction
Schmelzer (2008), Bouquet (1972) and
Christophe et al. (2015)
Sapo (Y)
Nigeria
Leaves
Cancer
Decoction
Soladoye et al. (2010b)
Ekoka ngowa (Bk)
Odogwu (Ia)
ni
Epo sapo (Y)
ni
Murigurigu (C)
ni
Hemorrhoids
A. djalonensis
A. nobilis
Hernia
A. djalonensis
A. nobilis
A. schweinfurthii
Cancer
A. nobilis
ni
Decoction
Decoction and maceration
Infusion/Decoction
Olowokudejo et al. (2008)
Borokini et al., (2013), and Sonibare and
Gbile (2008)
Jiofack et al. (2010)
Musa et al. (2010)
Baldé et al. (2015)
Odukoya et al. (2012)
Malan et al. (2015)
Adongo et al. (2012)
Kerharo, (1974), Burkill (1995), Fowler
(2006) and Christophe et al. (2015)
Soladoye et al. (2010a)
Diame (2010)
G.O. Anyanwu et al. / Journal of Ethnopharmacology 175 (2015) 648–667
Nigeria
Nigeria
Microbial infections
A. vogelii
Odogwu (Ia)
Sapo (Y)
A. nobilis
Wudifokεtε/ Hohoroho
(A)
A. liebrechtsiana Sapo (Y)
A. grandiflora
Murigurigu (C)
A. schweinAbanga'a
furthii
Mpuku mpuku (Kg)
ni
Skin diseases
A. djalonensis
A. liebrechtsiana
Jaundice
A. djalonensis
A. nobilis
(2015)
A: Akan; As: Ashante; B: Benin; Bk: Bakweri; Br: Bambara; C: Chuka; D: Douala; G: Guerzé; H: Hausa; I: Igbo; Ia: Igala; Ig: Igede; In: Ifa Nkari; K: Kotokoli; Kg: Kikongo; KL: Kagera and Lindi regions; M: Maninka; P: Pular; P: Pygmy;
S: Southern Ghana; T: Tumu Fang; Y: Yoruba; ni: not indicated.
653
654
G.O. Anyanwu et al. / Journal of Ethnopharmacology 175 (2015) 648–667
decoctions of A. djalonensis, A. vogelii and A. kerstingii are used in
Nigeria and Ghana by herbalists for the treatment of diabetes
mellitus (Ampofo, 1977). A summary of the ethnomedicinal uses of
Anthocleista species with their local names and methods of preparation are presented in Table 1.
4. Chemical constituents
Previous studies on Anthocleista showed the presence of alkaloids, xanthones, secoiridoids, terpenes, and phthalides (Irvine,
1961; Chapelle, 1976). Important phytochemicals such as saponins,
flavonoids, terpenoids, alkaloids, and steroids are present in the
leaf, stem–bark and root bark of A. vogelii (Jegede et al., 2011;
Anyanwu et al., 2013; Gboeloh et al., 2014; Ngbolua et al., 2014c).
Reducing sugar, tannin, phlobatanins, glycosides were found to be
absent in both the leaf and the stem bark of the Anthocleista
species (Njayou et al., 2008; Jegede et al., 2011; Oladimeji Igbalaye,
Coleshowers, 2014), however, tannins are present in the root bark
(Anyanwu et al., 2013) and anthraquinones in the leaves (Oladimeji Igbalaye, Coleshowers, 2014).
It has been reported that complex indole alkaloids appear to be
absent in Anthocleista, while secoiridoids and alkaloids derived
from these during the isolation procedure are present (Jensen,
1992). The secoiridoids found in Anthocleista are typical of those
found in Gentianaceae species, namely sweroside (1) and swertiamarin (2). Secoiridoid glycosides are responsible for the bitter
taste of the species. A compilation of the chemical compounds
isolated from Anthocleista species, their structures and class of
phytochemicals which include; secoiridoids, nor-secoiridoids,
xanthones, phytosterols, triterpenes, alkaloids, and others is found
in Fig. 1.
The presence of tetraoxygenated xanthones and the secoiridiod
glycosides, sweroside (1) and vogeloside, have been reported in
the leaves and roots of A. vogelii (Chapelle, 1976). Sweroside has
revealed significant anti-inflammatory activity (Baba and Usifoh,
2011). Tene et al. (2008) was the first to report the isolation and
structural elucidation of a rearranged nor-secoiridoid, anthocleistenolide from the stem bark of A. vogelii. Other chemical compounds isolated from A. vogelii include: secologanin (3), decussatin
(4), swertiaperennin (6), 1-hydroxy-3,7-dimethoxyxanthone (7),
7α-hydroxysitosterol (8), stigmasterol (9), hexadecanoic acid (10),
sitosterol 3-O-β-D-glucopyranoside (11), fagaramide (18) and triterpenes (Chapelle, 1974; Okorie, 1976; Kojima et al., 1990; Guerriero et al., 1993; Monte et al., 2001; Valentão et al., 2002; Tene
et al., 2008; Alaribe, et al., 2012). Decussatin has demonstrated
very weak antiplasmodial activity (Alaribe et al., 2012). Anthocleistenolide has revealed low antibacterial activities against S.
aureus and E. faecalis while 1-hydroxy-3,7-dimethoxyxanthone
and 1-hydroxy-3,7,8-trimethoxyxanthone showed antifungal activity against Candida parapsilosis (Tene et al., 2008).
Bierer et al. (1995) reported the isolation and structure elucidation of the then novel plant metabolite, 1,22-bis[[[2-(trimethylammonium) ethoxy]phosphinyl]oxy]docosane, which they
named Irlbacholine (23), from the plant species Irlbachia alata and
A. djalonensis. Irlbacholine revealed potent in vitro activity against
three pathogenic fungi: C. albicans, C. neoformans, and A. fumigatus
(Biere et al. 1995). Ogunwande et al. (2013) pioneering work on the
volatile oil contents of A. djalonensis revealed sesquiterpene
compounds (82.5%) are the dominant class of the 49 compounds
in A. djalonensis, and the main compounds are α-humulene (20), βcaryophyllene (21), humulene epoxide II (22) and caryophyllene
oxide (24). A monoterpene diol, djalonenol have been isolated
from A. djalonensis and the isolation of dibenzo-α-pyrone, djalonensone (27) from a plant source and it’s structurally elucidation
as tetrahydro-3-hydroxy hydroxymethylene-4-(3-hydroxymethylene
prop-1-ene)-2H-pyran-2-one was reported for the first time (Onocha
et al., 1995). The isolation of sweroside (1), djalonenoside, lichexanthone (5), stigmasterol (9), 3-oxo-Δ4′5-sitosterone (12), sitosterol
(13), ursolic acid (14), djalonensin (25) and D-(þ)-bornesitol (26)
from A. djalonensis have also been reported (Okorie, 1976; Onocha
et al., 1995).
Two iridoid glucosides, grandifloroside and methyl grandifloroside, one coumarin, scopoletin (27) and the secoiridoid
sweroside (1) were found in A. grandiflora (Chapelle, 1973, 1976).
Some compounds which have been isolated from the stem bark of
A. grandiflora are grandiflorol, bauerenol (15), bauerenone, 6-ketobauerenone; scopoletin (28) and (þ)-de-O-methyllasiodiplodin
(29); while lupenone (16) and the iridoid sweroside (1) were additional compounds isolated from the root bark (Mulholland et al.,
2005). Within the other species of Anthocleista much work with
regards to isolation has not been done. The investigation of the
occurrence of secoiridoids in methanol extract of the root bark of
A. nobilis by Madubunyi et al. (1994), led to the isolation and
identification of anthocleistol. The secoiridoid swertiamarin (2)
have been isolated from A. liebrechtsiana (Cornelis and Chapelle,
1976) and bauerenone and bauerenol (15) schweinfurthin (19)
from the roots of A. schweinfurthii (Mbouangouere et al., 2007).
Although no literature was found on the traditional use of A.
procera, phytochemical research on the plant revealed the isolation of the secoiridoid swertiamarin (2), the alkaloid gentianine
(17) and anthocleistin, a triterpene (Koch et al., 1964; Lavie and
Taylor-Smith, 1963; Taylor-Smith, 1965).
5. Pharmacological activities
5.1. Antidiabetic activity
In African traditional medicine, the leaves, stems and roots of A.
djalonensis, A. vogelii and A. nobilis are prepared as a decoction or
macerated in water or alcohol, and the solution is given orally as a
treatment for diabetes in Guinea, Nigeria, Togo, Ghana and Cameroun (Ampofo, 1977; Abuh et al.,1990; Madubunyi et al., 1994;
Olowokudejo et al., 2008; Jiofack et al., 2010; Diallo et al., 2012;
Soladoye et al., 2012; Tchacondo et al., 2012).
The hypoglycemic effect of the leaves, stem bark and roots of A.
djalonensis and A. vogelii, and roots of A. schweinfurthii has been
scientifically proven by in vitro and in vivo studies (Abuh et al.,
1990; Olagunju et al., 1998; Mbouangouere et al., 2007; Okokon
et al., 2012; Olubomehin et al., 2013; Osadebe et al., 2014a, 2014b;
Sunday et al., 2014). The leaves, stem barks and roots of A. djalonensis and A. vogelii revealed α-amylase inhibitory activity at 1mL
of 250 mg/mL concentration of their aqueous methanol extracts
(Olubomehin et al., 2013), although, A. djalonensis had the better
activity which indicated that it might contain more of the active
principles necessary for the management of diabetes. Alpha-glucosidase has been effectively inhibited by schweinfurthin, bauerenone and bauerenol isolated from the dichloromethane/methanol extracts of the roots of A. schweinfurthii (Mbouangouere et al.,
2007). The inhibition of α-glucosidase and α-amylase by A. djalonensis, A. vogelii and A. schweinfurthii prevents the digestion of
carbohydrates (starch and table sugar), thus serving as potent antidiabetic agents.
In the in vivo studies, while Olubomehin et al. (2013) reported
hypoglycemic activity of a high dose (1000 mg/kg) of A. djalonensis
extracts, Okokon et al. (2012) showed the dose- dependent activity
of same plant at lower doses (37 mg/kg, 74 mg/kg and 111 mg/kg).
All the doses for other in vivo hypoglycemic studies fell within 37–
1000 mg/kg (Abuh et al., 1990; Olagunju et al., 1998; Osadebe
et al., 2014b; Sunday et al., 2014), however, results of the various
studies showed that the extracts/fractions of A. djalonensis and A.
G.O. Anyanwu et al. / Journal of Ethnopharmacology 175 (2015) 648–667
655
Iridoids and secoiridoids
Sweroside (1)
Swertiamarin (2)
Secologanin (3)
Lichexanthone (5)
Swertiaperennin (6)
Xanthones
Decussatin (4)
1-hydroxy-3,7-dimethoxyxanthone (7)
Phytosterol
7α-hydroxysitosterol (8)
Stigmasterol (9)
Hexadecanoic acid (10)
Sitosterol 3-O-β-D-glucopyranoside (11)
3-oxo-Δ4'5-sitosterone (12)
Sitosterol (13)
Fig. 1. Chemical structures and names of compounds reported from Anthocleista species.
vogelii produced a dose dependent antidiabetic effect (at 100 mg/
kg p.o minimum dose) which could justify the use of these plants
traditionally to manage diabetes.
The antidiabetic activity of A. nobilis is yet to be reported despite its traditional use in Guinea (Diallo et al., 2012) and Nigeria
(Madubunyi et al., 1994). From the existing antidiabetic studies of
A. djalonensis and A. vogelii, the use of solvent fractions of the
plants make it is difficult to know which class of phytochemical
compounds may be responsible for their antidiabetic effect, except
based on polarity. Also, more active compounds should be isolated
from the Anthocleista species for the purpose of testing their antidiabetic activity. The mechanisms of action of the extracts/fractions of these plants are not yet known and no study has been
done on it. Further research is needed to understand how the
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G.O. Anyanwu et al. / Journal of Ethnopharmacology 175 (2015) 648–667
Triterpenes
Ursolic acid (14)
Bauerenol (15)
Lupenone (16)
Alkaloids
Gentianine (17)
Steriod
Fagaramide (18)
Schweinfurthin (19)
Volatile oil contents
α-humulene (20)
Plant metabolite
Irlbacholine (24)
β-caryophyllene (21)
Humulene epoxide II (22)
Caryophyllene oxide (23)
Phthalide
Oligosaccharide
Djalonensin (25)
D-( + )-bornesitol (26)
dibenzo-α-pyrone
Coumarin
Polyketides
Djalonensone (27)
Scopoletin (28)
de-O-methyllasiodiplodin (29)
Fig. 1. (continued)
plants exert their blood glucose lowering activities; either by increasing the amount of insulin secreted by the pancreas, increasing the sensitivity of target organs to insulin, and/or decreasing
the rate at which glucose is absorbed from the gastrointestinal
tract. So basically research on diabetes for this species is still at its
crude form.
G.O. Anyanwu et al. / Journal of Ethnopharmacology 175 (2015) 648–667
5.2. Antiplasmodial activity
Malaria is a major health problem in Africa caused by Plasmodium species transmitted by mosquitos. The Anthocleista species
are used to treat malaria in countries like Nigeria, Mali, Côte-d’Ivoire, Guinea, South Africa and Tanzania, of which the mode of
preparation is decoction/maceration and administered orally (Table 1), except in Côte-d’Ivoire where the bark of A. nobilis is mashed and smeared on the body (Malan et al., 2015).
Both in vitro and in vivo antiplasmodial studies have been carried out on Anthocleista. While the in vivo results were positive, the
in vitro results were negative or not impressive among the species.
In two different in vitro studies by Zirihi et al. (2005) and Zirihi
et al. (2010), A. djalonensis was inactive against Plasmodium falciparum in culture with IC50 value 450 μg/mL at a concentration of
10 mg/mL. Similarly, Bapela et al. (2014) reported that 10 mg/mL of
dichloromethane and methanol extracts of A. grandiflora showed
no in vitro antiplasmodial activity (IC50 450 μg/mL). Again,
among the 31 plants tested for in vitro antiplasmodial activity by
Nondo et al. (2015), ethanol extracts of A. grandiflora at 100 μg/mL
was among the least active with growth inhibition rate of less than
30% against chloroquine-resistant Plasmodium falciparum Dd2
strains. The in vitro antiplasmodial studies on the species seems
inadequate as most where not dose dependent, variation of extraction solvents from nonpolar to polar, and the laboratory
techniques were not exhaustive. No in vitro antiplasmodial studies
were found to be reported on A. vogelii and A. nobilis.
As in Table 2, the different plant parts of A. djalonensis, A. vogelii
and A. grandiflora at doses ranging from 50–3000 mg/kg have all
revealed in vivo antiplasmodial activities against Plasmodium falciparum or Plasmodium berghei in a dose dependent manner
(Bassey et al., 2009; Alaribe et al., 2012; Odeghe et al., 2012a; Okon
et al., 2014; Gboeloh et al., 2014; Ogbuehi et al., 2014). The work by
Alaribe et al. (2012) revealed a variation in the route of administration, where the petroleum ether leaf extracts (50, 100, 250 mg/
kg) of A. vogelii produced a dose dependent reduction in parasite
density compared to the control group when given intraperitoneally. But, there was no reduction when the extract was
administered orally at 100–1250 mg/mL in chloroquine sensitive
Plasmodium berghei infected mice. It is possible that petroleum
ether was not efficient in extracting most of the active principles
from the plant compared to more polar solvents like ethanol, for
which antiplasmodial activity was reported when the extracts
were given orally.
Odeghe et al. (2012b) reported the effectiveness of the methanol
extract of A. grandiflora in increasing the hematological values (PCV,
Hb, WBC, platelets, lymphocyte, neutrophils and monocyte) and decreasing the levels of AST and ALT activities of malaria parasite infected rodents. This indicated that the extract possess the ability to
enhance blood component to phagocytose, delay or prevent the incidence of anemia, protect the liver by its free radical scavenging
activities and improve the disease progression.
Typical of herbal medicines all over the world, is the combination of several plants to treat a particular disease condition,
which is a function of the understanding that the active principles
in the different plants work synergistically to elicit the expected
healing. The combination of A. nobilis, Nauclea latifolia and Napoleona imperialis and the individual plants exerted antiplasmodial
effect in varying degrees at 125, 250 and 500 mg/kg concentrations; however their combination gave improved symptomatic
relief from malaria and extended the mean survival time of the
treated mice (Ogbuehi et al., 2014). Similarly, A. vogelii in combination with Ficus exasperata has been shown to be effective against
P. berghei berghei (Okon et al., 2014).
An isolated compound decussatin (4), from pet ether leaf extract of A. vogelii, demonstrated very weak reduction in parasite
657
density at 10 mg/kg in P. berghei infected mice. Also, the extract
and decussatin demonstrated good iron chelating ability at
1 mg/mL concentration which might contribute in its antiplasmodial activities (Alaribe et al., 2012). So far, decussatin is the
only isolated compound from the Anthocleista species that has
been tested for antiplasmodial activity. However, the results of the
in vivo studies support the traditional use of the Anthocleista
species in the treatment of malaria.
The variation of in vitro and in vivo antiplasmodial results calls
for further research while modifying the extraction solvents or
standard techniques used for the in vitro antiplasmodial studies in
order to determine the most adequate or appropriate. However,
the positive in vivo results, and weak/negative in vitro antiplasmodial results is not a new phenomenon, as such weak/negative results are referred to as false negatives. According to
Walker (1987), several examples already exist of nucleoside antiviral agents which in vitro show weak or negative activity but
work very well in vivo. Furthermore, the identification of the
bioactive components in the species responsible for the antiplasmodial activity should be investigated with the aim of elucidating their mechanism of action and exploring the species for
new malaria drugs.
5.3. Antimicrobial activity
The Anthocleista species have been useful in the healing of
certain diseases caused by microbial infections such as typhoid,
candidiasis, mycosis, bronchitis and fever (Table 1). Also, the
treatment of sexually transmitted diseases by Anthocleista species
is a common herbal practice in countries like Nigeria, Togo, Cameroun, Gabon and Equatorial Guinea (Kerharo, 1974; Okorie,
1976; Olukoya et al., 1993; Igoli et al., 2005; Omobuwajo et al.,
2008; Kayode et al., 2004; Diame, 2010; Jiofack et al., 2010;
Tchacondo et al., 2012; Gbadamosi 2014; Christophe et al., 2015).
More so, skin diseases such as rashes and eczema are being treated
with Anthocleista species (Olowokudejo et al., 2008). Usually, the
plants are soaked in water or macerated before drinking (Table 1).
Anthocleista species have demonstrated antibacterial activity
against disease causing microorganisms like Escherichia coli, Salmonella typhi, Staphylococcus aureus, Klebsiella pneumoniae and
Corynebacterium diphtheriae. E. coli is the main causal agent of
urinary tract infection, also causes food poisoning. S. aureus causes
boils, impetigo cellulitis, abscesses, wound infections, toxic shock
syndrome, pneumonia, and food poisoning. S. typhi is the major
cause of typhoid, and sometimes accompanied with weakness,
headache, abdominal pain and constipation, and in rare cases
vomiting and diarrhea. K. pneumoniae causes pneumonia and infections in the urinary tract while C. diphtheriae causes diphtheria.
These explain the use of Anthocleista species by locals and traditional healers in the treatment of typhoid, diarrhea, skin diseases
and other infections.
Studies have provided scientific evidence for the long use of
these plants in the treatment of microbial infections (Table 2). A.
djalonensis have been shown to possess notable growth inhibitory
activities against E. coli, E. faecalis, S. typhi, S. aureus, Bacillus subtilis, Pseudomonas aeruginosa, Proteus spp., and Shigella spp. (Atindehou et al., 2002; Okoli and Iroegbu, 2004; Chah et al., 2006;
Akinyemi and Ogundare, 2012; Leke, 2012), but weak antifungal
activity against Candida albicans and Cladosporium cucumerinum
(Atindehou et al., 2002). The folkloric claim that A. djalonensis are
potent in the management of tuberculosis and leprosy was investigated in a sensitivity screening study by Esimone et al. (2009).
The methanol leaf and root extracts of A. djalonensis showed antimycobacterial activity (MIC ¼125 μg/mL), while the aqueous extracts of the same parts exhibited no inhibitory activity against
Mycobacterium smegmatis (Esimone et al., 2009). This suggests
658
Table 2
Pharmacological activities of Anthocleista species.
Pharmacological activities
Scientific name
Part used
Extract/fraction
Dosage/duration
Model
used
Type of effect
References
Antidiabetic activity
Anthocleista
djalonensis
Leaves, stem
bark and roots
Same
Roots
Aqueous methanol (E), hexane (F), ethyl acetate
(F)
same
Ethanol (E), methanol (F), chloroform (F), ethyl
acetate (F)
Isosaline (E)
1 mL of 250 mg/mL
in vitro
alpha-Amylase inhibitory
Olubomehin et al. (2013)
1 g/kg 7 days
in vivo
37,74, 111 mg/kg 7 h and in vivo
15 days
15 days
in vivo
Hypoglycemic
Hypoglycemic
Olubomehin et al. (2013)
Okokon et al. (2012)
Olagunju et al. (1998)
Aqueous methanol (E)
1 mL of 250 mg/mL
Hypoglycaemic, hypolipaemic,
hypocholestero-laemic activities
alpha-amylase inhibitory
Methanol (E), chloroform (F), ethyl acetate (F),
acetone (F) and water (F)
Ethanol (E and F)
Aqueous (E)
Dichloromethane (E), methanol (E)
200 and 400 mg/kg
in vivo
6 hrs
100, 200 and 400 mg/kg in vivo
100, 400 and 800 mg/kg in vivo
Hypoglycemic
Osadebe et al. (2014b)
Antidiabetic/ Toxicity
Hypoglycaemic
α-Glucosidase inhibition
Sunday et al. (2014)
Abuh et al. (1990)
Mbouangouere et al. (2007)
Aqueous (E), Methanol (E)
1-Hydroxy-3,7,8-trimethoxyxanthone (AV) isolated from the methanol extract
Ethanol (F)
0.13–8.00 mg/mL
2.50 10 2–1.60 μg/mL
in vitro
in vitro
Spasmogenic
Spasmogenic
Ateufack et al. (2010)
Ateufack et al. (2007)
0.06–0.31 mg/ml
in vitro
Spasmolytic
Madubunyi and Asuzu
(1996)
Aqueous (E), alcohol-insoluble fraction of the
aqueous extract
Aqueous (E), dichloromethane (E), cardiac glycoside type compounds (F)
Up to 1 mL/kg
in vitro
Hypotensive Activity
Duwiejua (1983)
in vitro
Vasoconstrictor and inotropic
effects
Ngombe et al. (2010)
in vivo
Hematological and biochemical
Indices
Antiplasmodial activity
Odeghe et al. (2012b)
Antiplasmodial activity
Antiplasmodial activity
Antiplasmodial activity schizontocidal activity
Bapela et al. (2014)
Nondo et al. (2015)
Bassey et al. (2009)
Leaves
Anthocleista vogelii
Spasmogenic activity
Cardiovascular effect
Antimalarial Activity
Olubomehin et al. (2013)
Anthocleista vogelii
Stem bark
Stem bark
Anthocleista nobilis
Root bark
Anthocleista nobilis
Root bark
Anthocleista
Schweinfurthii
Root bark
Anthocleista
grandiflora
Stem barks
Methanol (E)
Stem barks
Methanol (E)
Stem bark
Stem bark
Leaf Stem bark
Dichloromethane (E) and aqueous (E)
Ethanol (E)
Ethanol (E)
Stem back
Ethanol (E)
300, 500, 700 mg/kg 12
days
300, 500, 700 mg/kg 12
days
10 mg/mL
100 μg/mL
1000–3000 mg/kg/day
220–660 mg/kg/day
10 mg/mL
Root
175–1 000 mg/kg; 250
and 500 mg/kg
100,200, 400 mg/kg
in vivo
Stem back
Ethanol (E) Chloroform (F), ethyl acetate (F) and
methanol (F)
Ethanol (E)
Leaf
Petroleum ether (E)
in vivo
Stem bark
Decussatin
Ethanol (E)
in vivo
in vivo
Antiplasmodial effect
Antiplasmodial effect
Alaribe et al. (2012)
Gboeloh et al. (2014)
Anthocleista nobilis
Root
Methanol (E)
100–1250 mg/kg p.o,
50–250 mg/kg i.p
10 mg/kg
100, 200, and 400 mg/
kg
125, 250 and 500 mg/kg
Antiplasmodial and antipyretic
activities
Antiplasmodial activities (in
combination with Ficus
exasperata)
Antiplasmodial effect
in vivo
Antiplasmodial effect in combination with two plants
Ogbuehi et al. (2014)
Anthocleista vogelii
Stem bark
1-hydroxy-3,7,8-trimethoxyxanthone of Methanol 1, 2, and 5 mg/kg
Anthocleista
djalonensis
Anthocleista vogelii
Antiulcerogenic activity
Root
Root
Root
in vitro
in vivo
in vitro
in vitro
in vivo
in vitro
in vivo
in vivo
Odeghe et al. (2012a)
Zirihi et al. (2005) and Zirihi
et al. (2010)
Akpan et al. (2012)
Okon et al. (2014)
Alaribe et al. (2012)
Ateufack et al. (2014)
G.O. Anyanwu et al. / Journal of Ethnopharmacology 175 (2015) 648–667
Anthocleista
Schweinfurthii
Leaves, stem
bark and roots
Stem bark
(E)
Aqueous (E), hexane (E), acetone (E), Methanol (E) 500 mg/kg
in vivo
in vivo
in vivo
Anthocleista vogelii
Root bark
Root bark
Ethanol (E)
Ethanol (E)
500 mg/kg 28 days
500 mg/kg 28 days
Antiobesity
Liver function, antioxidant
activity
Anyanwu et al. (2013)
Anyanwu Sangodele et al.
(2014)
Analgesics properties
Anthocleista vogelii
Anthocleista
djalonensis
Stem bark
Root
Aqueous (E)
Methanol (E)
125, 250 and 500 mg/kg in vitro
200, 400 and 800 mg/kg in vivo
Analgesic effect
Analgesic effect
Mbianctha et al. (2013)
Kagbo and Simon (2015)
Antimicrobial effects
Anthocleista vogelii
Leaf
Stem
Leaves
Anthocleista
Schweinfurthii
Anthocleista
liebrechtsiana
Anthocleista
djalonensis
stem bark and
leaves
stem bark and
leaves
Leaves
Aqueous (E), ethanol (E), chloroform (E)
Aqueous (E), Ethanol (E)
Acetone (E), ethanol (E), methanol (E), methylenedichloride (E), methanol:chloroform: water (E),
water (E)
n-hexane (F), dichoromethane (F), ethyl acetate
(F), and methanol (F)
n-hexane (F), dichoromethane (F), ethyl acetate
(F), and methanol (F)
Methanol (E), Petroleum ether (E), Aqueous (E)
12.5–100 mg/kg
ni
in vitro
in vitro
in vitro
Typhoid fever
Antimicrobial effect
Antimicrobial effect
Musa et al. (2010)
Olukoya et al. (1993)
Eloff (1998)
250–1.95 μg/mL
in vitro
Antibacterial
Ngbolua et al. (2014b)
250–1.95 μg/mL
in vitro
Antibacterial
Ngbolua et al. (2014c)
30–5.0 mg/mL
in vitro
Antidiarrhoeal effect
in vitro
Antimicrobial effect
Akinyemi and Ogundare
(2012)
Leke et al. (2012)
in
in
in
in
in
in
Antibacterial and antifungal
Antibacterial
Antibacterial
Treatment of STDs
Anti-mycobacterial
Antibacterial and antifungal
Atindehou et al. (2002)
Ikegbunam et al. (2014)
Chah et al. (2006)
Okoli and Iroegbu (2004)
Esimone et al. (2009)
Atindehou et al. (2002)
in vivo
in vitro
Newcastle disease virus
Antibacterial
Ayodele et al. (2013)
Annan and Dickson (2008)
Oladimeji Igbalaye and Coleshowers (2014)
Muanya and Odukoya
(2008)
Root
Anthocleista nobilis
Fertility
Anti-inflammatory activity
Antioxidant assay
vitro
vitro
vitro
vitro
vitro
vitro
Anthocleista vogelii
Leaves
Ethanol (E)
100, 200 mg/kg
in vivo
Improve female fertility
Anthocleista
djalonensis
Root
Ethanol (E)
1 mL
in vivo
Improve male fertility
Anthocleista
djalonensis
Root
Aqueous ethanol (E) and sweroside
100, 200 and 400 mg/kg in vivo
Root
Stem bark
Methanol (E)
Methanol (E)
0.2 mL of 20 mg/mL
33.3% w/w
in vitro
in vivo
Aqueous (E), ethanol (E)
2.5–40.0 mg/mL
in vitro
Abu et al. (2009)
Anthocleista
djalonensis
Anthocleista nobilis
Leaf, stem and
root
Stem back
Ethanol (E)
500–0.07 g/mL
in vitro
Atindehou et al. (2004)
Root bark
Ethanol (E)
80, 67, 40 mg/kg, i.p.
In vivo
Madubunyi and Asuzu
(1996)
Anthocleista
Schweinfurthii
Anthocleista
liebrechtsiana
Anthocleista
stem bark and
leaves
stem bark and
leaves
Leaves
Methanol (F)
0.1–1 mg/mL
in vitro
DPPH radical scavenging assay
Ngbolua et al. (2014b)
Methanol (F)
0.1–1 mg/mL
in vitro
DPPH radical scavenging activity
Ngbolua et al. (2014c)
Methanol (E)
100 μL/ various conc.
in vitro
Free radical scavenging activity
Awah et al., (2010)
Anthocleista nobilis
Antitrypanosomal activity
Hexane (F) Methanol (F), Chloroform (F), Aqueous Full length and 10%
(F)
dilution
Stem bark
Ethanol (E)
ni
Leaves
Methanol (E)
3000.00–21.87 mg/mL
Root
Methanol (E)
0.1 mL of 20 mg/mL
Root
Ethanol (E), cold and hot water (E)
100 μL l of 25 mg/mL
Leaves Root
Aqueous (E) Methanol (E)
20 mg/mL
Stem bark, root Ethanol (E)
ni
bark
Root
Ethanol (E)
0.5 mg/100 g for 28 days
Stem bark
Methanol (E)
20 μL aliquot of extract
Anthocleista vogelii
Baba and Usifoh (2011)
Wound healing properties
Wound healing activity
G.O. Anyanwu et al. / Journal of Ethnopharmacology 175 (2015) 648–667
Antiobesity activity
Ateufack et al. (2006)
Chah et al. (2006)
Annan and Dickson (2008)
659
Anyanwu et al. (unpublished thesis, 2015)
Nweze and Ngongeh (2007)
in vivo
250–500 mg/kg
Ethanol (E)
Anthocleista vogelii
Diuretic and Laxative
activity
Root bark
Anthocleista
djalonensis
Anthelmintic activity
Root
in vitro
25–200 mg/mL
Ethanol (E)
TBA reactivity
DPPH radical scavenging activity
in vitro
in vitro
–
50 μL of 10–100 μg/mL
djalonensis
Anthocleista nobilis
Bark
Stem bark
Ethanol (E)
Methanol (E)
Type of effect
Model
used
Dosage/duration
Extract/fraction
Part used
Scientific name
Pharmacological activities
Table 2 (continued )
Odukoya et al. (2012)
Annan and Dickson (2008)
G.O. Anyanwu et al. / Journal of Ethnopharmacology 175 (2015) 648–667
References
660
that the active principles in A. djalonensis are better extracted or
much more concentrated in alcoholic extracts.
Aqueous, ethanol and chloroform extracts of A. vogelii leaf and
stem bark have revealed antibacterial activity against S. typhi, K.
pneumoniae and C. diphtheriae (Olukoya et al., 1993; Musa et al.,
2010), while the methanol stem bark extracts of A. nobilis inhibited
the growth of S. aureus, B. subtilis, M. flavus, E. coli and P. aeruginosa
(Annan and Dickson, 2008). The extracts of the leaves and stem
barks of A. schweinfurthii and A. liebrechtsiana have shown antibacterial activity against S. aureus, but they were less sensitive to E.
coli (Ngbolua et al., 2014b, 2014c). Species like A. schweinfurthii
and A. liebrechtsiana have only been screened for fewer microorganisms, there is need to experiment with more microorganisms
in order not to limit the effect of the plants. Traditionally, A.
schweinfurthii is used to treat bronchitis and mycosis, but there is
yet to be scientific evidence to this practice.
Irlbacholine, isolated from A. djalonensis, revealed potent in
vitro activity against three pathogenic fungi: C. albicans, C. neoformans, and A. fumigatus, with minimum inhibitory concentrations (MIC) of 1.25, 0.04 and 0.08 pg/mL respectively (Biere et al.
1995).
Similarly,
Irlbacholine
showed
potent
activity
(MIC¼ 0.04 pg/mL) against the dermatophyte Trichophyton rubrum. Tene et al. (2008) evaluated the antibacterial and antifungal
activities of anthocleistenolide, 1-hydroxy-3,7-dimethoxyxanthone,1-hydroxy-3,7,8-trimethoxyxanthone and sitosterol 3-Oβ-D-glucopyranoside isolated from the stem bark of A. vogelii. The
results showed relatively low activity against Staphylococcus aureus (MIC ¼200 μg/mL) and against Enterococcus faecalis
(MIC¼ 100 μg/mL) for anthocleistenolide, while compounds 1-hydroxy-3,7-dimethoxyxanthone and 1-hydroxy-3,7,8-trimethoxyxanthone were active against Candida parapsilosis with MIC of
200 μg/mL and 25 μg/mL respectively. Sitosterol 3-O-β-D-glucopyranoside was inactive against all the bacterial and fungal species
used.
Although, the traditional use of Anthocleista species for the
treatment of STDs and skin diseases still remains to be proven
scientifically, their use in the treatment of bacterial and fungal
diseases have been sufficiently supported by the above scientific
studies. However, more work is essential to isolate the biologically
active components in the numerous extracts for antibacterial and
antifungal activities. Studies on antiviral activities of this species
were not found to be reported.
5.4. Antihypertensive and antihypotensive activities
In Nigeria and Togo, the leaf, bark and root of A. djalonensis and
A. vogelii are used to treat hypertension (Table 1). The root of A.
djalonensis is also macerated in combination with three other
plants (Crematogaster pilosa, Securidaca londepedunculata and
Nauclea latifolia) and one tea spoon is taken three times daily to
treat hypertension in Nigeria (Olorunnisola et al., 2015). Although,
no comprehensive ethnobotanical use of A. nobilis and A.
schweinfurthii for the management of hypertension was found,
Burkill (1985a and 1985b) had earlier documented the traditional
use of the leaf of A. nobilis for the treatment of spasm, and the leaf,
bark and root of A. schweinfurthii as medicines for arteries and
veins. The reason behind the tradition use of Anthocleista species
in the treatment of hypertension might not be farfetched as studies have suggested their action on adrenergic receptors, direct or
indirect activation of L-type calcium channels, antispasmodic effect, vasodilator action, inhibition of the Naþ pump, ganglionblocking and muscarinic effect (Lafon, 1966; Duwiejua, 1983; Ignesti et al., 1988; Ngombe et al., 2010).
The pharmacological effects of the aqueous extract and the
alcohol-insoluble fraction (crystalline compound) of the aqueous
extract of the root bark of Anthocleista nobilis was investigated on
G.O. Anyanwu et al. / Journal of Ethnopharmacology 175 (2015) 648–667
the arterial blood pressure of anaesthetized cat and on isolated
perfused rabbit heart by Duwiejua (1983). A dose-dependent depressor effect, which was slightly antagonized by atropine, was
observed in both models (in vitro and in vivo). The extract exerted
a resultant lowered tone of the muscles which could cause a drop
in the blood pressure. The hypotensive action of the root extract of
A. nobilis was reported to be due to a direct muscarinic effect,
ganglion-blocking effect and a non-specific depressant action on
both smooth and skeletal muscles.
Previously, Lafon (1966) reported that the aqueous and alcohol
extracts of A. nobilis possess antispasmodic effect, hypotensive
activity, neurotropic activity and vasodilator action. Also, aqueous
extract of A. nobilis has been reported to have inhibited the contraction induced by noradrenalin in the rat ductus deferens (Ignesti et al., 1988). Vasodilation involves the widening of arterial
and/or venous vessels, thus reducing systemic vascular resistance
and consequently leading to reduced blood pressure. The vasodilator effect of A. nobilis validates its traditional use for the management of hypertension or spasms.
Ngombe et al. (2010) investigated the cardiovascular effect of
three extracts (aqueous extract, dichloromethane extract and a
fraction enriched in cardiac glycoside type compounds) from the
root bark of A. schweinfurthii. The bolus injection of extracts produced a positive inotropic effect in isolated perfused frog heart.
Other results indicated that A. schweinfurthii contains substances
that promote vasoconstriction and increase cardiac contraction.
The effect of dichloromethane extract was only partially mediated
by inhibition of the Na þ pump while the mechanism of action of
aqueous extract and cardiac glycoside type compounds was distinct from the inhibition of the Na þ , K þ -ATPase pump, but could
involve adrenergic receptors, or either direct or indirect activation
of L-type calcium channels. The rise in concentration of Ca2 þ ions
within vascular smooth muscle cells results in vasoconstriction
(Capponi et al., 1985). Drugs/agents that cause vasoconstriction,
that is the narrowing of blood vessels (large arteries and small
arterioles) help to elevate blood pressure. Therefore, the vasoconstrictor effect of A. schweinfurthii suggests its possible use for
the treatment of hypotension.
Scientific reports supporting the traditional use of A. djalonensis
and A. vogelii for the management of hypertension was not available. Recent studies on the hypotensive properties of Anthocleista
species is lacking, and neither past nor the reported studies have
gone beyond fractions in their investigation of the species. This
spells out clearly that more work on the pharmacological activities
of the extracts, fractions and their isolated compounds is
necessary.
661
polar fraction of the extract. The spasmolytic activity of A. nobilis
supports its traditional use in the treatment of colic, stomachaches, diarrhea and constipation. Although, neither the compound
nor mechanism by which A. nobilis produces spasmolysis have
been investigated.
Ateufack et al. (2010) have reported the spasmogenic effect of
A. vogelii stem bark, where it’s aqueous and methanol extracts
produced a dose-dependent effect on the tone and force of the
spontaneous contraction of the rat ileal and stomach smooth
muscle fragments at concentrations ranging from 0.13 to
8.00 mg/mL. Also, xanthone, 1-hydroxy-3,7,8-trimethoxyxanthone
isolated from the methanol extract of the stem bark of A. vogelii
produced a dose-dependent effect on the tone and force of the
spontaneous contraction of the rat ileal and stomach smooth
muscle fragments at concentrations ranging from 2.50 10 2 to
1.60 mg/mL (Ateufack et al., 2007). These results point to a possible
stimulation of these muscle fragments through muscarinic receptors which increase Ca2 þ mobilization from both extra and
intramuscular medium, that is, the plant extracts or isolated
compound interfere with calcium metabolism in smooth muscle to
exert its effect. The spasmogenic activity of A. vogelii validates their
use in African traditional medicine for gastro-intestinal disorders,
stomach ache and as a purgative, and most especially for the
treatment of abdominal pains in Cameroon.
The suggestion by the authors that the spasmogenic effect of
aqueous and methanol extracts of A. vogelii is by stimulation of
muscarinic receptors needs further investigation to ascertain
which muscarinic receptor subtypes (M1–M5) and their location is
responsible for this function. Also, it is imperative to determine if
the stimulation of muscarinic receptors extends to other smooth
muscles like the heart, mesenteric arteries, veins, etc. This is important because, for instance, activation of M1 and M3 are known
to mediate a direct smooth muscle vasocontrictive effect which
consequently leads to elevated blood pressure (Medina et al., 1997;
Grekin and Hamlyn, 2003). But it is also possible that the aqueous
and methanol extracts of A. vogelii might act by stimulating M2
muscarinic receptors in the heart and aorta of animals thereby
producing hypotension. If such is the case, this action may also
lend support to the use of A. vogelii in the management of hypertension by traditional healers and locals (Table 1).
The evidences above support the use of A. nobilis and A. vogelii
for their folkloric use against stomach disorders, but no evidence
was available to support the traditional use of A. djalonensis for
diarrhea or dysentery; A. schweinfurthii for stomach aches or A.
grandiflora for stomach amoeba infections (Table 1).
5.6. Anti-obesity activity
5.5. Spasmolytic and spasmogenic activities
The traditional use of Anthocleista species in the treatment of
stomach disorders such as stomach ache, abdominal pains, ulcer,
diarrhea and dysentery has been reported (Dalziel, 1955; Akubue
et al., 1983; Adjanohoun et al., 1986; Nweze and Ngongeh, 2007;
Adongo et al., 2012; Odukoya et al., 2012; Christophe et al., 2015).
Generally, the relevant parts of A. djalonensis, A. vogelii, A. nobilis,
A. schweinfurthii, and A. grandiflora are prepared by decoction and
taken orally in Nigeria, Cameroun and Kenya (Table 1).
In evaluating the pharmacological properties of defatted ethanol root bark extract A. nobilis, Madubunyi and Asuzu (1996) tested its spasmolytic effect on smooth muscle, the isolated guineapig ileum. Out of six fractions obtained by chromatographic separation of the ethanol extract, only one fraction, which showed
one main compound (Rf 0.4) in chloroform:acetone:formic acid
(9:2:1) relaxed the guinea-pig ileum in a concentration-dependent
manner. This indicated that the active principle responsible for the
relaxation effect on the guinea-pig ileum was contained in the
The impact of ethanol extract of A. vogelii root bark on weight
reduction in high carbohydrate diet (HCD) induced obesity in male
wistar rats had been investigated. The ethanol extract of A. vogelii
of 500 mg/kg b.w significantly decreased food intake, body weight,
total fat mass, adiposity index, low density lipoprotein cholesterol,
glucose and leptin levels (Anyanwu et al., 2013). In an anti-lipideamic study in hyperglycemic rats, the ethanol root extracts (100,
200 and 400 mg/kg) and fraction (200 mg/kg) of A. vogelii exerted
a dose dependent significant decrease (Po 0.05) in TC, TG, LDL-C,
ALT, AST and an increase in HDL-C when compared to the control
(Sunday et al., 2014).
The ethanol extract of A. vogelii root bark showed positive effect
on liver function and antioxidant status of obese rats (Anyanwu
et al., 2014). The extract of 500 mg/kg b.w significantly decreased
ALT, AST and ALP activities; while it increased the catalase and
superoxide dismutase activities, and glutathione level, with no
significant difference in MDA level compared to the high fat diet
and high carbohydrate diet obese controls. Also, the numerous
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prominent fat deposits in the livers appeared relatively reduced
among the groups treated with the extract (Anyanwu et al., 2014).
These indicated that the ethanol extract of A. vogelii root bark was
helpful in preventing the progress of oxidative stress, fatty liver
and eventually obesity.
Although, the results of the antiobesity studies which were
limited to A. vogelii seemed interesting, none of the studies have
determined the antiobesity effect of Anthocleista species based on
the 5 categorized mode of action for antiobesity agents from
natural products. This means that the species need to be tested for
their ability to decrease energy intake, increase energy expenditure, decrease lipid absorption, decrease lipogenesis and increase lipolysis, and lastly to decrease pre-adipocyte differentiation and proliferation. Also, studies need to go beyond crude extracts and fractions of plants, beginning with in vitro studies which
are lacking if any meaningful antiobesity agents have to be discovered from this species.
5.7. Antiulcerogenic/analgesics, wound healing and anti-inflammatory activities
The antiulcerogenic effect of a drug often times is as a result of
its combined effect of decreasing both pain and inflammation. The
ethnomedicinal uses of A. vogelii in the treatment of stomach pain
have been validated by the findings that both aqueous and organic
extracts of the stem bark of A. vogelii possess potent antiulcer
properties. The aqueous and methanol extracts showed 87.91% and
100% inhibition respectively at a dose of 500 mg/kg when
screened for antiulcerogenic activity using HCl/ethanol gastric
necrotizing solution (Ateufack et al., 2006). Similarly, the aqueous
extract at a dose of 500 mg/kg significantly reduced indomethacin-induced gastric lesions by 78.62% while the methanol
extract at the same dose completely inhibited the action of indomethacin (Ateufack et al., 2006). Further investigations on the
action of the xathone (1-hydroxy-3,7,8-trimethoxyxanthone) obtained from the methanol extract of the A. vogelii stem bark prevented in a dose-dependent manner ulcers induced by HCl/ethanol (60.90–93.22%), Indometacin (46.86–89.68%), and pylorus ligation (0.00–70.69%) at the doses of 1, 2, and 5 mg/kg respectively
(Ateufack et al., 2014).
Anti-inflammatory agents/drugs make up about half of analgesics, because they remedy pain by reducing inflammation or
swelling. Traditionally, a cold infusion of the stem bark of A. djalonensis with 8 other plants is prepared and two table spoons is
taken daily for the treatment of Asthma in Nigeria (Sonibare and
Gbile, 2008; Borokini et al., 2013). For swellings, rheumatism and
wounds, the area affected is poulticed to relieve the soreness and
inflammation, and to cleanse the wound (Musa et al., 2010).
The action of A. djalonensis at central and peripheral sites to
inhibit neurogenic and inflammatory pains has been proposed by
Kagbo and Simon (2015), after investigation of the analgesic
properties on the methanol root extract of A. djalonensis in albino
rats using chemical, mechanical and thermal models of pain. The
response to neurogenic and inflammatory pains by the formalin
hind paw licking test was used to study chemically induced pain.
Mechanical pain was induced by exertion of pressure on inflamed
and hyperalgesic rat paw with an Analgesy-meter while thermally
induced pain was assessed by the supraspinally mediated tail flick
test. The extract showed a significant, dose dependent inhibition
of nociception in all the models of pain used.
The aqueous extract of A. vogelii stem barks at 125, 250 and
500 mg/kg, reduced the number of abdominal constrictions induced by acetic acid with 40.42%, 65.62% and 68.75% respectively
demonstrating its analgesics properties (Mbianctha et al., 2013). In
the formalin test of the same study, extract provoked 56.48%,
59.49% and 89.93% of inhibition respectively with the same doses;
while the second phase was marked by a higher activity of the
extract, with 94.16%, 97.47% and 100% of inhibition.
The ethanol-water (1:1) extract of A. djalonensis root showed
significant activity (p o0.05) at 400 mg/kg comparable to the reference drug, while the pure compound (sweroside) isolated from
the extract revealed significant anti-inflammatory activity
(p o0.05) at 100 mg/kg in animal model (Baba and Usifoh, 2011).
Chah et al. (2006) determined the wound healing properties of
methanol root extracts of A. djalonensis using the excision wound
model, and the extract proved wound healing properties (98.84%)
s
comparable with that of the standard drug cicatrin (100%) by the
17th day post-surgery in rats. Also, the methanol extracts of A.
nobilis revealed potent wound healing activity as evident from the
wound contraction, increased tensile strength and hydroxyproline
content in male rats using the excision wound model (Annan and
Dickson, 2008).
These findings support the traditional use of Anthocleista species, particularly A. djalonensis, A. vogelii and A. nobilis as pain
killers and in the treatment of wounds and inflammatory diseases.
Although, scientific evidence supporting the traditional use of A.
grandiflora and A. schweinfurthii for treatment of chest pains and
wounds respectively is lacking, based on evidence of other Anthocleista species as anti-inflammatory agents, there is need to
research their mode of action for reducing pain and/or inflammation, likewise the bioactive agents mediating these effects.
5.8. Antioxidant activity
Antioxidants are needed to prevent the formation and reduce
the level of reactive oxygen and nitrogen species, which are produced in vivo and cause damage to DNA, proteins, lipids, and other
biomolecules. Antioxidants are widely used in dietary supplements and have been investigated for the prevention of diseases
such as cancer, coronary heart disease and even altitude sickness
(Baillie et al., 2009). Plants produce a number of antioxidants for
their own protection and some that may also be useful to humans
such as vitamin E, vitamin C, carotenoids, flavonoids, etc. The
Anthocleista species are potential source of antioxidants which
could be responsible for their health benefits.
The methanol extract of A. djalonensis leaves showed a very
potent DPPH and O2 anion radical scavenging activities
(IC50¼ 8.69 70.95 μg/mL and 5.32 71.05 μg/mL respectively).
Also, the extract displayed significantly higher OH radical and nonenzymatic lipid peroxidation inhibitory potentials than that of
standard
antioxidants
(IC50 ¼33.06 75.65 μg/mL
and
59.147 4.64 μg/mL respectively), likewise, it inhibited the accumulation of nitrite in vitro (Awah et al., 2010). Annan and Dickson
(2008) reported the inhibition of lipid peroxidation, DPPH radical
scavenging activity and protection against oxidant injury to fibroblast cells as indications of A. nobilis potent antioxidant activity.
A. Schweinfurthii and A. liebrechtsiana had been shown to possess DPPH free radical scavenging activities (IC50 o 10 μg/mL)
(Ngbolua et al., 2014b, 2014c). And the ethanol extract of Anthocleista nobilis bark showed TBA reactivity by decreasing levels of
MDA and a reduction in lipid peroxides both in the raw and
cooked fish homogenate, but the antioxidant capacity was low
compared to other plants tested (Odukoya et al., 2012).
The extract of A. schweinfurthii showed no inhibition of microsomal lipid peroxidation using rat hepatic microsomes, but
revealed inhibition of carbonyl-group formation on bovine serum
albumin (BSA), that is, against protein oxidation. The results indicated that the antioxidant activities of A. schweinfurthii may be
due to their ability to scavenge free radicals involved in protein
oxidation, but not in microsomal lipid peroxidation (Njayou et al.,
2008). Nonetheless, the compounds within the plants that are
responsible for its antioxidant properties are yet to be identified.
G.O. Anyanwu et al. / Journal of Ethnopharmacology 175 (2015) 648–667
5.9. Antitrypanosomal activity
The antitrypanosomal activity of 101 crude ethanol extracts
derived from 88 medicinal plants from Cote d’Ivoire was determined in vitro using Trypanosoma brucei rhodesiense by Atindehou et al. (2004). A. djalonensis was one of the 56 plants that did
not show any activity at all (IC50 values 4 25 g/mL). Similarly, in a
previous study, the defatted ethanol root bark extract of A. nobilis
did not reduce the level of parasitaemia in mice infected with
Trypanosoma brucei brucei (Madubunyi and Asuzu, 1996). However, a different result was obtained in the in vitro antitrypanosomal studies of crude extracts of some Nigerian medicinal
plants by Abu et al. (2009). It was discovered that both aqueous
and ethanol extracts of the root bark of A. vogelii showed activity
at 40 and 20 mg/mL, but the stem bark had no activity at the test
concentrations. This could be indicative of species difference with
respect to presence or concentration of the bioactive components
in the part of the plants used.
5.10. Anthelmintic activity
Anthelmintic is any drug used in the treatment of infections
caused by parasitic worms (helminths). Helminths include tapeworms, roundworms and flukes. The Anthocleista species have
been used to kill or flush out worms in Tanzania, Nigeria, Cameroun and Kenya (Table 1). Majorly, the roots and stem barks of the
A. djalonensis, A. vogelii, A. nobilis, A. schweinfurthii, and A. grandiflora are prepared as a decoction and taken orally (Akubue et al.,
1983; Kerharo, 1974; Madubunyi et al., 1994; Burkill, 1995; Fowler,
2006; Nweze and Ngongeh, 2007; Dibong et al., 2011; Adongo
et al., 2012; Christophe et al., 2015).
The in vitro anthelmintic activity of the ethanol extract of A.
djalonensis was studied against L larvae of Heligmosomoides polygyrus (roundworm) at 25, 50, 100 and 200 mg/mL concentrations
(Nweze and Ngongeh, 2007). The extract had a concentrationdependent lethal action on H. polygyrus larvae. At a concentration
of 100 mg/mL, the extract recorded 98.45% mortality which was
equivalent to that of levamisole (the positive control) at 10 mg/mL.
This is indicative of the validity of its use traditionally against
worms and other internal parasites in the body, and thus, the
mode of action of the species on the worms needs to be
investigated.
5.11. Fertility activity
The Anthocleista species, particularly A. djalonensis, A. vogelii, A.
nobilis and A. schweinfurthii are a source of traditional recipes for
treatment of male and female fertility problems in Togo, Nigeria,
Ghana, Cameroon, Gabon, Equatorial Guinea and Congo (Table 1).
Traditionally, A. djalonensis is used in South West Nigeria to boost
libido, induce erection, increase sperm count and consequently
male fertility (Olowokudejo et al., 2008). Other examples include
the use A. vogelii for the treatment of menstrual dysfunction
(Omobuwajo et al., 2008) and A. schweinfurthii for ovarian problems (Kerharo, 1974; Christophe et al., 2015). In contrast to the
use of Anthocleista species to enhance fertility, the roots of A. vogelii and bark/leaf of A. nobilis are reported to be used as contraceptives or to induce abortion (Kadiri, 2009; Diame, 2010).
Reactive oxygen species are important mediators of sperm
dysfunction (Wang et al., 1997; Bansal and Bilaspuri, 2011). Production of MDA, an end product of lipid peroxidation, has been
reported in spermatozoa. Muanya and Odukoya (2008) studied the
effect of 9 medicinal plants on lipid peroxidation as an index of
male fertility. Lipid peroxidation in raw and cooked fish homogenates was measured as the amount of thiobabituric acid reactive
sample (TBARS) in nmol/mg. The A. djalonensis extract was the
663
most active in the inhibition of lipid peroxidation among the
9 plants tested. This indicates that A. djalonensis possess the ability
to improve sperm function thereby increasing male fertility, and
hereby it gives support to its traditional use in the treatment of
male fertility problems.
The ethanol extract of A. vogelii showed a statistically significant increase of estradiol concentration in the female rats, from
(184.65 730.06 pg/mL) in the control group compared to
(288.29 7 30.06 pg/mL) in the extract treated group (Oladimeji
Igbalaye, Coleshowers, 2014). In female reproductive system, estrogen plays a very important role especially in ovulation. The
evidence by Oladimeji Igbalaye and Coleshowers (2014) that A.
vogelii can induce estrogen production supports the claim on the
traditional use of the plant to enhance fertility in females.
The traditional use of A. djalonensis for the treatment of female
infertility has not been reported, likewise no report was found for
A. nobilis and A. schweinfurthii vis-à-vis its folkloric use for improving female fertility. Nevertheless, the evidence that A. djalonensis and A. vogelii improves male and female fertility respectively should trigger further investigation on the bioactive compounds in these plants in order to develop them into useable
therapeutic agents of fertility enhancers.
5.12. Diuretic and laxative activities
Traditionally, A. djalonensis, A. vogelii, and A. liebrechtsiana are
used as purgative by locals/natives in Nigeria, Cameroun and other
African regions (Dalziel, 1955, Okorie, 1976; Adjanohoun et al.,
1986; Igoli et al., 2005; Olowokudejo et al., 2008; Lawal et al.,
2010; Ariwaodo et al., 2012). The leaf, bark or roots are usually
boiled with water and drank to obtain its purgative/laxative effect.
The root of A. vogelii is traditionally used as a diuretic (Burkill,
1985c), however, Lawal et al. (2010) reported the use of A. djalonensis as an antidiuretic.
The diuretic and laxative activity of ethanol extracts of A. vogelii
root bark was studied in vivo in male wistar rats (Anyanwu et al
unpublished thesis, 2015). The extracts increased the volume of
urine excreted compared to the negative control at 250 mg/kg and
500 mg/kg oral doses after 5 and 18 h. Diuretics promote the
production and excretion of urine from the body. A. vogelii proved
to be a potent diuretic as it promoted the excretion of urine from
the rats, although the effect was not more than the positive control
(25 mg/kg of Furosemide). Thus, the traditional use of A. vogelii for
forced diuresis and hypertension is valid.
In the laxative studies, ethanol extracts of A. vogelii root bark
significantly increased the fecal output of rats compared to the
positive and negative control at 500 mg/kg oral dose after 8 and 16
hours (Anyanwu et al unpublished thesis, 2015). A. vogelii was
shown to be a potent laxative at 500 mg/kg, but not at 250 mg/kg
concentration of the extract. As common with all laxatives, A. vogelii increased bowel movement and loosened feces. Therefore, the
results supported its traditional use as a laxative or purgative.
Apart from A. vogelii, the diuretic and laxative effect of other
Anthocleista species has not yet been reported. The dose, that is,
500 mg/kg at which the diuretic and laxative effect of A. vogelii
was recorded seems high considering the use by humans, the
biodiversity of the plant will greatly be affected. Also, considering
that the diuretic effect of A. vogelii at 500 mg/kg was not more
than that 25 mg/kg of Furosemide, there is need to research the
bioactive component of the plant, possibly its effect may be
comparable or more than the available standard diuretic drugs.
6. Toxicity studies
There are several acute toxicity studies in different animals
showing different safety levels or varying LD50 of the different
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G.O. Anyanwu et al. / Journal of Ethnopharmacology 175 (2015) 648–667
parts of Anthocleista species. The acute toxicity study of aqueous
extract of the stem bark of A. vogelii did not provoke a death until
the dose of 20 g/kg p.o in mice (Mbianctha et al., 2013). The acute
toxicity (LD50) of the ethanol stem bark extract was estimated to
be 3162 mg/kg p.o in mice (Gboeloh et al., 2014). In another
toxicity study on pet ether leaf extract of A. vogelii, no lethality was
observed at 2000 mg/kg body weight i.p. in mice (Alaribe et al.,
2012). Sunday et al. (2014) reported the LD50 of A. vogelii ethanol
root extract as Z5000 mg/kg p.o in rats, while in an earlier study,
the ethanol extract of A. vogelii root bark revealed no lethality at
6400 mg/kg p.o in rats (Anyanwu et al., 2013).
The LD50 of the defatted ethanol root bark extract of A. nobilis
was 200 mg/kg, i.p. in mice (Madubunyi and Asuzu, 1996). The
acute toxicity study of the stem bark of A. grandiflora indicated that
extract did not cause mortality of mice up to 1000 mg/kg p.o.
(Okoye et al., 2014). Acute toxicity using a single dose of 2000 mg/
kg of aqueous extract of A. schweinfurthii bark administered orally
to mice showed neither death nor significant changes in the behavioral and morphological parameters after 14 days of observation (Christophe et al., 2015).
In a subacute toxicity study, the aqueous extract of the stem
bark of A. vogelii tested at the doses of 0, 250, 500 and 1000 mg/kg
p.o. once daily for 28 days revealed decreases in the body weight
and water consumption, and increases in food consumption
without any significant difference in the relative organ weight in
mice (Mbianctha et al., 2013). The serum and hepatic level of ALT
increased significantly, but that was not the case in the levels of
AST, proteins and creatinine in all the treated animals compared
with the animals of the group controls. Also, the aqueous extract of
A. vogelii showed reno-protective and hepatoprotective effect as
compared with the control following ethanol-induced toxicity in
rats (Ayoka et al., 2014).
Ogbonnia et al. (2011) reported the evaluation of the acute and
subacute toxicities of a Nigerian polyherbal tea remedy, prepared
with A. vogelii, Ficus exasperata and Viscum album in Swiss albino
mice and wistar rats of both sexes. The acute toxicity (LD50) of the
polyherbal tea was determined to be 8.970 g/kg p.o in mice. The
tea significantly reduced plasma glucose, LDL-cholesterol, AST and
creatinine levels, but increased HDL-cholesterol with no significant increase in the body weight and ALT levels. The subacute
toxicity of the aqueous extract of A. schweinfurthii bark at doses
250 mg/kg, 500 mg/kg and 1000 mg/kg showed no significant
variation in the evaluated parameters on male and female rats for
28 days (Christophe et al., 2015).
The cytotoxic activity of the crude methanol extracts obtained
from the stem, roots and leaves of A. djalonensis and three natural
plant constituents (djalonenol, sweroside (1) and djalonensone
(27) respectively) isolated from these extracts were evaluated in
vitro against ST-57 brain tumor transformed fibroblasts (Onocha
et al., 2003). Comparatively, the three crude extracts as well as
djalonenol and sweroside (1) exhibited low cytotoxicity (ED50 40–
70 μg/mL) while djalonensone (27) was not significantly cytotoxic
against the brain tumor transformed fibroblasts (Onocha et al.,
2003). The ethanol extracts of A. grandiflora showed little to no
toxicity to brine shrimps (Mosh et al., 2010). Similar, the activity of
A. djalonensis on brine shrimps lethality was not significant
(Awachie and Ugwu, 1997).
The effect of aqueous ethanol extract of A. vogelii leaves against
CCl4 induced toxicity in wistar albino rats restored the liver
function to near normal indicating the protection of hepatic cells,
also the extract increased the rate of erythropoiesis and antioxidant activity (Iroanya et al., 2015). The extract showed dose
dependent significant increase in the levels of catalase, glutathione
peroxidase, superoxide dismutase, reduced glutathione and glutathione-S-transferase with decrease in the level of MDA compared to the normal and toxin control groups. The administration
of 800 mg/kg of extract reduced the levels of ALP, AST and ALT
levels almost the same as Silymarin. Also, the extract stimulated
significant (p o0.05) increase in PCV, Hb, platelet and MCH levels
compared to the toxin control group.
The oral administration of 67 mg/kg of defatted ethanol root
bark extract of A. nobilis reduced pentobarbitone-induced sleep in
CCl4-poisoned mice, and effect was comparable to that of Silibinin
(Madubunyi and Asuzu, 1996). Elevation of serum ALT and AST
induced by CCl4 intoxication in rats were also significantly attenuated by the defatted ethanol root bark extract of A. nobilis
(Madubunyi and Asuzu, 1996). Overall, the Anthocleista species are
safe and not toxic at considerably high doses. The toxicity studies
revealed that the genus possess hepatoprotective, reno-protective,
free radical scavenging, and antioxidant properties. The above
findings imply and validate the safety and tolerability of the plant
various extracts in animals models. The 41 g/kg LD50 implies
drug safety and tolerability in animal models. Additionally, subacute toxicity studies have shown safety and tolerability attributable partly to the hepatoprotective and antioxidant effects of the
plant. The subacute toxicity studies have shown considerable
safety and tolerability on over all parameters of health and imply
safe usage, as practiced and experienced folklorically.
7. Conclusion
Six of the fourteen accepted species of Anthocleista have been
reported for their traditional medicinal uses in Africa. Scientific
studies on Anthocleista have given credence to their use by traditional healers or locals in the treatment/management of various
ailments such as diabetes, pain, inflammations, wounds, malaria,
hypertension, stomach disorders, infertility, obesity, typhoid and
worm infestations. However, its use as a contraceptive, antidote
for snake bite, ear and eye treatments or in the treatment of
asthma, STDs, jaundice, hemorrhoid, hernia, cancer, etc. had not
been scientifically researched or proven.
Forty chemical compounds were shown to have been isolated
belonging to the groups of secoiridoids, nor-secoiridoids, xanthones, phytosterols, triterpenes, alkaloids, and others. The chemical structures of 29 isolated chemical compounds were displayed. Majority of the studies on Anthocleista species were on
crude extract, few on fractions and very few on isolated compounds. There were no reports of mechanisms of action of the
extracts/fractions/compounds of these plants on any of the disease
conditions indicating that most of the studies were basic or preliminary and no clinical trial studies were found. Generally, the
plants of this genus are considered to be safe and non-toxic as
practiced and believed folklorically even at higher concentrations
and subsequently validated in experimental animals.
This review has provided for the first time a repository of
ethnopharmacological information while critically evaluating the
relation between the traditional medicinal uses, chemical constituents and pharmacological activities of the Anthocleista species.
Therefore, researchers have to move quickly and deeply in the
investigations of this species, particularly for antidiabetic and antimicrobial agents. Also, there is need for substantial advanced
research on their chemistry and pharmacological properties (both
in vivo and in vitro), the determination of the mode of action of the
active principles for new and already known pharmacological activities and commencement of clinical studies of some Anthocleista
species which will hopefully lead to newer, more effective and less
toxic drugs.
G.O. Anyanwu et al. / Journal of Ethnopharmacology 175 (2015) 648–667
Acknowledgments
We wish to thank The World Academy of Sciences (TWAS) and
COMSATS Institute of Information Technology (CIIT) for giving the
lead author the Award of 2014 CIIT-TWAS Sandwich Postgraduate
Fellowship in CIIT, Abbottabad, Pakistan. Thanks to Dr. Ethelbert
Chukwuagozie and Dr. Opeolu Ojo who assisted in sourcing some
materials for the writing of this paper.
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