Antimalarial activity of methanolic extracts from plants used in Kenyan ethnomedicine and their interactions with chloroquine (CQ) against a CQ-tolerant rodent parasite, in mice.
Francis W. Muregia,c,* , Akira Ishiha , Toshio Miyaseb , Tohru Suzukia , Hideto Kinoa ,
Teruaki Amanod , Gerald M. Mkojic , Mamoru Teradaa
aDepartment of Parasitology, Hamamatsu University School of Medicine, 1-20-1 Handayama,
bDepartment of Pharmacognosy, School of Pharmaceutical Sciences, University of Shizuoka, Yada
cCentre for Biotechnology Research and Development, Kenya Medical Research Institute (KEMRI),
dEastern and Southern Africa Centre for International Parasite Control (ESACIPAC), Kenya Medical
Research Institute, P.O. Box 54840-00200, Nairobi, Kenya.
*Corresponding Author. Tel: +81-53-435-2338; Fax: +81-53-435-2337;
Email address: firstname.lastname@example.org (Francis Muregi)
Methanolic extracts from 15 medicinal plants representing 11 families, used traditionally for
malaria treatment in Kenya were screened for their in vivo antimalarial activity in mice against a
chloroquine (CQ)-tolerant Plasmodium berghei NK65, either alone or in combination with CQ. The
plant parts used ranged from leaves (L), stem bark (SB), root bark (RB), seeds (S) and whole plant
(W). When used alone, extracts from 7 plants, Clerodendrum myricoides (RB), Ficus sur (L/SB/RB),
Maytenus acuminata (L/RB), Rhamnus prinoides (L/RB), R. staddo (RB), Toddalia asiatica (RB)
and Vernonia lasiopus (RB) had statistically significant parasitaemia suppressions of 31.7-59.3%. In
combination with CQ, methanolic extracts of Albizia gummifera (SB), F. sur (RB), R. prinoides and
R. staddo (L/RB), Caesalpinia volkensii (L), Maytenus senegalensis (L/RB), Withania somnifera
(RB), Ekebergia capensis (L/SB), T. asiatica (L/RB) and V. lasiopus (L/SB/RB) gave statistically
significant and improved suppressions which ranged from 45.5-85.1%. The fact that these activities
were up to 5-fold higher than that of extract alone may suggest synergistic interactions. Remarkable
parasitaemia suppression by the extracts, either alone or in combination with CQ mostly resulted into
longer mouse survival relative to the controls, in some cases by a further 2 weeks. Plants, which
showed significant antimalarial activity including V. lasiopus, T. asiatica, F. sur, R. prinoides and R. staddo warrant further evaluation in the search for novel antimalarial agents against drug-resistant
Keywords: Antimalarial activity; Medicinal plants; Drug resistance; Plasmodium berghei NK65; Traditional medicine; Synergistic effects 1. Introduction
In view of the problems associated with antimalarial drug resistance, new drugs or drug
combinations are urgently required today for treatment of malaria. Preferably, the new drugs should
have novel modes of action or be chemically different from the drugs in current use (Phillipson and
Wright, 1991). Plants have always been considered to be a possible alternative and rich source of
new drugs and most of the antimalarial drugs in use today such as quinine and artemisinin were either
obtained directly from plants or developed using chemical structures of plant-derived compounds as
templates (Basco et al., 1994). Due to limited availability and/or affordability of pharmaceutical
medicines in many tropical countries, the majority of the populations depend on traditional medical
remedies ((WHO, 2002; Zirihi et al., 2005), mainly from plants. In ethnomedicine, same plants
and/or related species are used for the treatment of related ailments within the same region, or across
different regions of the world. For instance, whereas Maytenus senegalensis is used in many African
regions for the treatment of various ailments including chest pains, rheumatism, snakebites and
malaria, plants of the genus Maytenus are used to prepare decoctions in south America as anti-
inflammatory and analgesic remedies (Sosa et al., 2006; Ajaiyeoba et al., 2006). This is however not
surprising since malaria manifests itself with symptoms including fever, pains and immuno-
suppression and some plants may lack direct antiplasmodial activity but may possess antipyretic,
analgesic and immune stimulatory effects (Muregi et al., 2003). Among the plants we screened for
antimalarial activities, most of them find wide ethnopharmacological use among different Kenyan
ethnic groups either for similar or different ailments (Kokwaro, 1976; Beenjte, 1994). While
Vernonia lasiopus is used against malaria by Kikuyu of central Kenya, the Kamba of eastern Kenya
use it against scabies, the Luo of western Kenya against venereal diseases, and pounded leaves are
applied to sores by Maasai of southern Kenya (Beentjee, 1994). Toddalia asiatica is used
traditionally in Kenya by many communities for the treatment of malaria, fever, stomachache,
toothache, coughs as well as nasal and bronchial pains, and although all parts of the plant are claimed
to have medicinal value, roots are believed to be more potent (Kokwaro, 1976; Beentje, 1994).
In an attempt to impede selection of drug resistance, use of monotherapy is being discouraged for
most parasitic diseases (WHO, 2000). In the case of malaria, for instance, not only are novel
combinations being tried, but also attempts are being made to enhance the potency and/or even
reverse resistance of conventional drugs such as CQ (Winstanley, 2000). Although several synthetic
molecules have been shown to restore CQ-sensitivity in resistant Plasmodium falciparum strains
(Oduola et al., 1998), there are almost no documented data on interactions of herbal remedies with
conventional antimalarial drugs such as CQ. In the present study, several medicinal plants used as
traditional remedies for malaria in Kenya were evaluated for antimalarial activity against a rodent
malaria parasite in mice, alone or in combination with the conventional antimalarial drug, CQ.
2. Materials and methods
Based on ethnomedical data, different plant parts (leaf, stem bark, root bark, seed, whole plant) of
15 plant species representing 11 families (Table 1) were collected in January 2004 from central
Kenya (Mount Kenya Forest) and southern Rift Valley (Nguruman Escarpment in Magadi). The
plants collected were identified by a taxonomic botanist from the East African Herbarium in Nairobi,
where voucher specimens were deposited. The plant samples were then catalogued, air-dried at room
temperature under shade, and ground into powder using an electric mill. The powder was packaged
into one kg-packs and stored in dry and well-ventilated room until use. Organic extraction was done
by refluxing 10g of plant material in 500 ml of methanol for one hour. The extracts were then filtered
and concentrated to dryness in vacuo.
For in vivo antimalarial assays of plant extracts, a CQ-tolerant Plasmodium berghei (strain NK65),
a rodent malaria parasite was used. The blood-stage CQ-tolerant-induced parasite, maintained at the
Parasite Bank of the Department of Parasitology, Hamamatsu University School of Medicine was
previously a kind gift from Professor Y. Wataya of Okayama University, Japan. A donor mouse to
the experimental mice, having 10-15% parasitaemia was sacrificed and bled by cardiac puncture. The
parasitaemia was adjusted downwards using physiological saline, and each of the experimental male
ICR mice, 7-week old weighing about 30 g (Japan SLC Inc., Hamamatsu, Japan) was inoculated
intraperitoneally with approximately 105 parasitisized erythrocytes in volumes of 0.2 ml (Ishih et al.,
2003). The inoculated mice were then randomized into 5 mice per cage and maintained in an animal
care facility on a commercial diet and water ad libitum.
Antimalarial activity of plant extracts either alone or in combination with chloroquine
In screening of the plant extracts alone, the 4-day suppressive method of Peters et al. (1975) was
used. Within 3 hours post-inoculation of mice with the parasite (i.e on day 0), treatment of the
experimental groups was initiated by oral administration of the test extract at a dose of 500 mg/kg
body weight and treatment was done twice a day (at 8-hour interval) for 4 days, up to day 3 post-
infection (p.i.). The untreated control group received distilled water only. Twenty-four hours after the
last treatment (i.e., on day 4 p.i.), parasitaemia of individual mouse was determined by microscopic
examination of Giemsa stained thin blood smears prepared from mouse-tail blood.
In assessing the in vivo interactions of CQ and the plant extracts, treatment was started on day 4
p.i. based on the method of Ishih et al. (2004). Infected mice were randomized into CQ/plant extract
treated groups [CQ, 20 mg/kg body weight, once a day for 2 days + plant extract, 500 mg/kg body
weight, twice a day for 4 days], a CQ-treated positive control group, and an untreated control group,
which received water only. For all mice before initial treatment on day 4 p.i., thin blood smears were
prepared, after which CQ dose followed by plant extract dose was administered by oral route.
In both studies, in vivo antimalarial activity of the test drugs was assessed by monitoring mouse
survival and parasitaemia, over a 30-day period. Handling of animals was done in accordance to the
Guide for the Care and Use of Laboratory Animals, Hamamatsu University School of Medicine.
Percentage suppression of parasitaemia for the plant extracts was calculated as: 100 - [(mean
parasitaemia treated/mean parasitaemia control) × 100] (Gessler et al., 1995). For comparison of
average parasitaemia, one-way ANOVA and 2-tailed Student’s t-test were used (Microsoft® Excel
2004), with P<0.05 being considered significant.
3. Results Antimalarial activity of plant extracts alone
Table 2 shows a summary of parasitaemia suppression (%) for mice on day 4 p.i. and their
corresponding survival on day 9 p.i., when 100% mouse-mortality of the untreated control occurred.
Eleven extracts from 7 plant species showed significant parasitaemia suppressions (P<0.05) ranging
from 31.7-59.3%. These are C. myricoides (RB), F. sur (L/SB/RB), M. acuminata (L/ RB), R. prinoides (L/RB), R. staddo (RB), T. asiatica (RB) as well as V. lasiopus (RB). In contrast, other 14
extracts, C. volkensii (S), M. heterophylla (RB), M. senegalensis (RB), V. lasiopus (SB), A. remota
(W), E. capensis (L/SB/RB), A. indica (L), A. gummifera (L/SB), F. sur (L), R. staddo (L), and C. myricoides (L), had non-significant suppressions (P>0.05), which ranged from 9.8-37.0%. Three
extracts from C. volkensii (L), M. heterophylla (RB) and V. lasiopus (L) had no activity at all. Based
on day 9 p.i. relative to the untreated controls, 7 extracts gave a 40-60% mouse survival, in some
cases up to a further 2 weeks. T. asiatica (L) had a 60% and 40% mouse survival on day 9 and 16 p.i.
respectively. Although the extract had moderate suppression of 37.0% (P>0.05) on day 4 p.i., it is the
only extract that showed sustained effect on day 7 p.i. of 39.8% (P<0.05) relative to the untreated
controls. V. lasiopus (RB) gave a 60% survival of mice on day 9 p.i. and a 40% survival on day 11
p.i. C. volkensii (S) and A. gummifera (SB) had 40% survival on day 18 p.i., and 17 p.i. respectively.
Antimalarial activity of plant extracts in combination with CQ
In CQ/plant extract combination studies, the parasitaemia levels on day 4 p.i. (before initial
treatment) were not different (P>0.05) among all groups and microscopic examination of day 8 p.i.
smears detected no parasites. However, the recrudescent parasites reappeared by day 11 p.i., and
hence parasitaemia levels at day 11 p.i. were considered the most significant in assessment of
chemo-suppression. Table 2 summarizes the parasitaemia suppression (%) for mice on day 11 p.i.
and the corresponding survival on day 14 p.i., when all mice of CQ-treated control group died.
Seventeen extracts from A. gummifera (SB), F.sur (RB), M. senegalensis (L/RB), R. prinoides
(L/RB), R. staddo (L/RB), C. volkensii (L), E.capensis (L/SB), T. asiatica (L/RB), V. lasiopus (L/SB/
RB) as well as W. somnifera (RB) in combination with CQ gave parasitaemia suppressions that
ranged from 45.5-85.1% (P<0.05). The best activities were exhibited by CQ/A. gummifera (SB), CQ/F.sur (RB), CQ/R. prinoides (RB) as well as CQ/R. staddo (RB) with activities of 75.2, 79.3, 85.1
and 74.2% respectively. Nine extracts in combination with CQ including C. volkensii (S), Maytenus acuminata (L), M. acuminata (RB) and M. heterophylla (RB) showed non-significant (P>0.05)
activities of up to 45.5%, while 2 extracts, F. sur (L/SB) had no suppression at all (Table 2). Relative
to day 14 p.i., when 100% mortality of the CQ-alone treated controls occurred, mice in the groups
treated with CQ/R. staddo (RB) had the highest mouse survival of 80% at day 14 p.i., and 40%
survival on day 26 p.i. CQ/V. lasiopus (L) had 60 and 40% survival on day 14 and 26 p.i.
respectively. The 2 extracts had mice surviving longer by up to a further 2 weeks (day 28 p.i.)
relative to the controls. CQ/A. gummifera (SB) gave a 60% survival on day 14 p.i., but all the mice
died by day 17 p.i. It is remarkable that all the 3 groups had shown significant parasitaemia
suppressions of 74.2, 56.1 and 75.2% respectively. Although CQ/E. capensis (RB) maintained a 75%
survival up to day 23 p.i, and 50% survival on day 28 p.i., it is remarkable that the combination had
day 11 p.i. parasitaemia suppression of 37.9% which was not statistically significant (P>0.05). Three
extracts showed a considerably longer mouse survival than the controls; CQ/Azadirachta indica (L),
40% survival on day 25 p.i.; CQ/R staddo (L), 50% survival on day 30 p.i.; CQ/T asiatica (L ), 40%
4. Discussion and conclusions
When assayed alone against CQ-torelant P. berghei NK65, 38% of the 29 methanolic extracts,
representing 53% of all the 15 plant species screened, showed significant parasitaemia suppression
(P<0.05) on day 4 p.i. ranging from 31.7-59.3%, which may partially validate the ethnomedical use
of the herbs in management of malaria. The plants with considerable in vivo chemo-suppression
including V. lasiopus, F. sur, C. myricoides, R. prinoides and R. staddo had shown moderate to
significant in vitro antiplasmodial activities against both CQ-sensitive and -resistant P. falciparum
isolates in their water and/or organic fractions in a previous study of some Kenyan medicinal plants
(Muregi et al., 2003; 2004). The organic leaf extract of V. lasiopus had shown the highest in vitro
inhibition of parasite growth, with IC50 values as low as 1.0 μg/ml, which is consistent with the
findings of the present study, in which the methanolic extract showed a remarkable in vivo
parasitaemia suppression of 59.3%, albeit in its root bark extract. The presence and/or quantities of
bioactive compounds in plants are influenced by several factors including seasons, environment,
plant-part used, intra-species variations and plant age (Weenen et al., 1990), and this may explain the
discrepancies observed in in vitro and in vivo activities of plant parts used. Many Vernonia species
have been investigated chemically and found to contain several metabolites including triterpenes and
oxygenated sesquiterpenes, flavones and vernolic acid (Oketch-Rabah, 1996). Oxygenated
sesquiterpene lactones are the most abundant secondary metabolites of the genus Vernonia, and since
artemisinin, isolated from the Chinese herb Artemisia annua belongs to the same class of compounds
and has been widely used in the synthesis of semi-synthetic antimalarials effective against multi-drug
resistant strains of P. falciparum (Trigg, 1989; Oketch-Rabah, 1996), it is important to investigate
Vernonia species further. Two 5-methylcoumarins isolated from the roots of V. brachycalyx showed
in vitro antiplasmodial activity against both CQ-sensitive and –resistant P. falciparum isolates
(Oketch-Rabah et al., 1997). Methanolic extract of T. asiatica (RB) showed remarkable activity
(59.3%) in the present study, and was previously reported to possess high in vitro antiplasmodial
activity, with a mean 50% inhibitory dose of 0.98 μg/ml (Gakunju et al., 1995). Subsequent activity-
guided fractionation and isolation afforded fractions and an alkaloid, nitidine, active against both CQ-
sensitive and -resistant P. falciparum isolates. Subsequent chemical development of this compound
has further improved its potency against CQ-resistant P. falciparum isolates in vitro (Waigh, 2002).
Oketch-Rabah et al. (2000) reported that a coumarin derivative from T. asiatica (RB) had a moderate
in vitro activity of 8.8 μg/ml against P. falciparum isolates. Although not much has been reported in
literature about biological activity of F. sur, it is widely used in Kenyan ethnopharmacology as a
cough remedy, against stomachaches and toothaches to relieve pain (Kokwaro, 1976; Beenjte, 1994).
The fact that all the F. sur parts investigated showed a modest antimalarial activity underscores the
need for further investigation of the plant. R. staddo and R. prinoides are the only 2 Rhamnus species
that occur in Africa and the latter is widespread in many parts of eastern and central Africa (Abegaz
et al., 1999). In ethnomedicine, the 2 plants, especially their roots are used for treatment of malaria,
indigestion, venereal diseases and rheumatism among other ailments (Kokwaro, 1976; Beenjte, 1994).
Recent studies have shown that R. prinoides can serve as a commercial hopping agent in the brewery
industries and 20 compounds including 7 glycosides of emodin anthrone, 5 flavonoids and 3
naphthalenic derivatives were isolated from the plant (Abegaz et al., 1999). Emodin has been
reported to possess various pharmacological and biological activities including immunostimulation,
antiparasitic, anti-inflammatory and analgelsic effects, among others (Izhaki, 2002). In several cases,
remarkable suppression of parasitaemia by extracts translated into either a higher and/or a longer
mouse survival. However, V. lasiopus (RB) gave a 60% survival of mice on day 9 p.i. and a 40%
survival on day 11 p.i., which mean that high percentage survival on day 9 p.i. does not translate into
a considerably longer mouse survival. This may suggest that the bioactive compound in the plant
may have a short half-life, since some antimalarial drugs including artemisinin-based derivatives are
known to be fast acting, and to have a short half-life (Van Agtmael et al., 1999). In contrast, T. asiatica (L) gave a 60% mouse survival on day 9 p.i., and a relatively longer survival, with 40%
mouse survival on day 16 p.i. The extract is the only one which maintained similar suppression levels
on day 4 and 7 p.i., suggesting that the bioactive agent (s) in the plant may have a slow onset of
action, and/or that it is not fast acting. On the other hand, some extracts with mild parasitaemia
suppression (P>0.05) gave a long mouse survival. C. volkensii (SD) and A. gummifera (SB), with
40% survival on day 18 p.i., and 17 p.i. respectively are such extracts, implying that other than direct
parasiticidal effects, plants may possess other pharmacological benefits to the hosts, such as acting as
analgesics, antipyretics or as immune stimulators (Dahanukar et al., 2000).
In combination with CQ, some of the extracts showed up to 5-fold better chemo-suppression as
well as longer mouse survival than that of CQ-alone treated controls, suggesting synergistic
interactions of the 2 drugs. As expected, high chemo-suppression in most cases led to a high mouse
survival at day 14 p.i., and subsequently a longer mouse survival, as in the case of the group treated
with CQ/R. staddo (RB). Some plant extracts such V. lasiopus (L) that lacked activity when used
alone, demonstrated both high as well as prolonged mouse survival when used in combination with
CQ. As earlier noted, this emphasizes the possibility of other pharmacological effects of plants being
involved, besides direct antiparasitic effects. Leaves and seeds of V. lasiopus and V. galamensis had
been reported to possess analgesic effects in rat models (Dahanukar et al., 2000). On the other hand,
some extracts including F. sur (L/ RB) which had significant activity when used alone showed little
or no suppression in combination with CQ. Antagonistic interactions among drugs as well as toxicity
cannot be ruled out in such cases, emphasizing the need to avoid simultaneous use of conventional
drugs with natural products before the safety and efficacy of such combinations have been
authenticated. The fact that about 50% of the 15 plants screened showed moderate to high in vivo
antimalarial activity when used alone, and that most of the extracts enhanced CQ activity forms a
basis of further detailed studies of the plants. This includes isolation and characterization of the
bioactive compounds with the ultimate objective of finding novel antimalarial compound(s), which
can be used in the fight against drug-resistant malaria.
We thank Mr. G. Mungai of the East African Herbarium (Nairobi) for his kind assistance in
collection and identification of plants. This work was supported by the Government of Japan through
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Table 1. Plant parts collected based on ethnopharmacological data and percentage yield of dry methanolic extract per 10 g of air-dried plant material used Plant Family
extract Caesalpinaceae Caesalpinia volkensii Harms
Celastraceae Maytenus acuminata (L.f.) Loes
M. heterophylla (Eckl. & Zeyh.) Robson
Compositae Vernonia lasiopus O.Hoffm.
Mimosaceae Albizia gummifera (JF Gmel.) C.A. Sm.
Rhamnaceae Rhamnus prinoides L’ Hérit
Rutaceae Toddalia asiatica (L.) Lam.
Solanaceae Withania somnifera (L.) Dunal
Verbenaceae Clerodendrum myricoides (Hochst.) Vatke
L, leaf; SB, stem bark; RB, Root bark; S, seed; W, whole plant
a some plant species may share vernacular names while others may have more than one name
Table 2. Parasitaemia suppression (%) on day 4 and 11 post infection (p.i.) for mice treated with plants’ methanolic extracts alone (from day 0 p.i.) and in combination with CQ (from day 4 p.i), and the corresponding survival (%) on day 9 and 14 p.i. respectively
0 L, leaf; SB, stem bark; RB, Root bark; S, seed; W, whole plant NS, no suppression; ND, not determined bstatistically significant (P<0.05)
National Board of Diving & Hyperbaric Medical Technology CHRN Study Guide Contents Introduction History of Undersea and Hyperbaric Medicine The Physical Aspects of Undersea and Hyperbaric Medicine The Physiological Aspects of Undersea and Hyperbaric Medicine Mechanisms and Theory of Decompression Therapeutic Associated with Hyperbaric Oxygen Exposure C
aDepartment of Psychiatry, University of Washington, 1959 Paciﬁc Street,bDepartment of Rehabilitation Medicine, University of Washington, 1959 Paciﬁc Street,The evolution of contemporary clinical pain care dates back to the pub-lication of Melzack and Wall’s gate control theory in the journal Science in1965 . Around that time, most of the attention was given to the ‘‘gate’’ inthis