Vol. 9(6), pp. 179-192, 10 February, 2015
DOI: 10.5897/JMPR2014.5685
Article Number: 915206C50871
ISSN 1996-0875
Copyright © 2015
Author(s) retain the copyright of this article
http://www.academicjournals.org/JMPR
Journal of Medicinal Plants Research
Full Length Research Paper
Ethnobotanical survey and in vitro antiplasmodial
activity of medicinal plants used to treat malaria in
Kagera and Lindi regions, Tanzania
Ramadhani S.O. Nondo*1, Denis Zofou3, Mainen J. Moshi1, Paul Erasto2, Samuel Wanji4,
Moses N. Ngemenya3, Vincent P.K. Titanji3, Abdul W. Kidukuli1 and Pax J. Masimba1
1
Institute of Traditional Medicine, Muhimbili University of Health and Allied Sciences P.O.Box 65001,
Dar es Salaam, Tanzania.
2
National Institute for Medical Research P.O.Box 9653, Dar es Salaam, Tanzania.
3
Biotechnology Unit, University of Buea, P.O.Box 63 Buea, South West Region, Cameroon.
4
Research Foundation in Tropical Diseases and Environment P.O.Box 474, Buea, South West Region-Cameroon.
Received 10 November, 2014; Accepted 5 February, 2015
Tanzania has over 12,000 plant species, some of which are endemic and have potential to yield useful
medicines. This study seeks to document such plants used as traditional medicines for treatment of
malaria in Kagera region of northwestern Tanzania and Lindi region in south eastern Tanzania. The
study also reports on the antiplasmodial activity against chloroquine-resistant Plasmodium falciparum
(Dd2) strain of some of the documented plants using the parasite lactate dehydrogenase method. A total
of 108 plant species, among which the families Compositae (14; 12.96%), Fabaceae (12; 11.11%),
Euphorbiaceae (8; 7.41%), Melastomataceae (6; 5.56%) and Myrtaceae (4; 3.70%) were documented.
Sixteen (16; 44.4%) of 36 extracts from 31 plant species that were tested inhibited malaria parasites
growth by more than 50%. Bersema abyssinica stem bark extract was the most active with 86.67%
inhibition rate followed by Bridelia micrantha stem bark extract with 71.87% inhibition rate. These
results confirm the potential for plants used in traditional medicine to yield active antimalarial
compounds. Further in vitro and in vivo screening supported by bioassay-guided isolation of active
compounds from plants showing good safety margin is suggested.
Key words: Ethnobotanical survey, medicinal plants, malaria, treatment, in vitro antiplasmodial, Tanzania.
INTRODUCTION
Human malaria is caused by five Plasmodium species
namely; P. falciparum, P. vivax, P. ovale, P. malariae and
P. knowlesi, but Plasmodium falciparum is the most
widespread and virulent species (World Health
*Corresponding author. E-mail: nondo75@yahoo.com
Author(s) agree that this article remain permanently open access under the terms of the Creative Commons Attribution
License 4.0 International License
180
J. Med. Plants Res.
Organization (WHO), 2013; Cox-sigh and Singh, 2008).
Malaria in Tanzania is mainly caused by P. falciparum
with Anopheles gambiae complex being the main vector
United States Agency for International Development
(USAID, 2014). Tanzania has high malaria prevalence
and it is among six African countries that have many
reported cases of malaria, with an estimated 10 to 12
million cases and 60,000 to 80,000 malaria-related
deaths per year (USAID, 2014; WHO, 2012). Although
the Tanzania HIV/AIDS and Malaria Indicator Survey
(2011/2012) reported a decrease in the prevalence of
malaria in Tanzania, the trend remains unchanged.
Prevalence is still high in rural areas and the Lake
Victoria zone as compared to other parts of the country
Tanzania Commission for AIDS (TACAIDS, 2013).
Malaria is a curable disease that is treated by both
modern drugs and herbal medicines (Kinung’hi et al.,
2010; Gessler et al., 1995). However, the emergence of
P. falciparum strains resistant to almost all classes of
antimalarial drugs dictates that efforts be increased to
develop new antimalarial drug candidates (Dondorp et
al., 2009; Wongsrichanalai et al., 2002). Since most
antimalarial drugs that are currently being used like
quinine and artemisinin derivatives originate from
traditionally used medicinal plants (Wells, 2011), this
source has a great potential to provide new antimalarial
molecules.
Tanzania is estimated to have over 12,000 higher plant
species, of which 10% are used for medicinal purposes,
and may yield active antimalarial compounds (Mahunnah
et al., 2012). Previous reports confirm that some of these
plants are used in traditional medicine for treatment of
malaria (Gessler et al., 1995), and malaria is leading
among diseases that are popularly treated with medicinal
plants (Moshi et al., 2009; Mahunnah, 1987). Some of
these plants have been reported in previous studies
(Moshi et al., 2009; Gessler et al., 1995; Mahunnah,
1987), but many have not been documented and only a
few have been tested for antimalarial activity. Therefore,
this study reports plant species used for treatment of
malaria in Kagera and Lindi regions of Tanzania and
results of some of the plants that were screened for in
vitro antiplasmodial activity.
village in Misenyi district. The study in Lindi region was conducted
in July, 2012 in Mchakama village located in Kilwa district.
Information was collected from well known and experienced
traditional healers and herbalists who were informants in a previous
ethnomedical study (Moshi et al., 2009). Before collecting
information all the participants were informed about the study
objectives and agreed to participate by signing an informed consent
form. Vernacular names of the plants, part(s) used, method for
preparation, route of administration and possible signs of toxicity
were documented. Preliminary identification was done by a
Botanist, Mr. Haji. O. Selemani, in the field and further
authenticated in the Herbarium. Voucher specimens are deposited
in the Herbaria at Muhimbili University of Health and Allied
Sciences and at the Botany Department, University of Dar es
Salaam. The selection of the plants to be tested for antimalarial
activity was based on absence in the literature of previous
antimalarial testing, reported antimalarial use in other countries or
emphasis made by the traditional healers regarding efficacy for
malaria treatment. This study received ethical clearance (Ref. No.
MU/DRP/AEC/Vol.XIII/01st August 2011) from the Muhimbili
University of Health and Allied Sciences Institutional Review Board.
Preparation of extracts
Dry powdered plant materials were macerated in 80% ethanol, at
room temperature, for 24 h and then filtered through cotton wool to
separate the liquid crude extracts from the solid materials. The solid
plant materials were macerated again in the same solvent for
another 24 h and the extracts obtained from the first and the
second extractions were mixed before drying. The liquid crude
extracts were concentrated under vacuo by using Heldolph® rotary
evaporator (Heldolph instruments GmbH, Schwabach, Germany) to
obtain viscous extracts which were further dried by using a freeze
drier (Edwards High Vacuum International, Crawley Sussex,
England).
In vitro antiplasmodial screening
Malaria parasites
Blood stage chloroquine-resistant P. falciparum Dd2 strains (Pf
Dd2; MRA-156 deposited by TE Wellems, Lot# 59443398) were
used. The parasites were donated to the University of Buea in
Cameroon by BEI-resources (MR4/ATCC® Manassas, VA, USA).
Malaria culture medium
RPMI-1640 (Lot# RNBC 8874) culture medium with L-glutamine
and 20 mM HEPES (Sigma®, Steinheim, Germany) was used.
MATERIALS AND METHODS
Documentation, identification and collection of the medicinal
plants used for treatment of malaria
Disease-specific ethnobotanical survey was conducted in six
villages in Kagera region (North-west of Tanzania) and one village
in Lindi region (South east of Tanzania). In Kagera region the study
was conducted in November, 2012 in Buzi Bukombe, Buzi Kishura
and Kwamkenge villages in Bukoba rural district, Buleza village in
Muleba disctrict, Rwambaizi village in Karagwe district, and Kashozi
In vitro culture of malaria parasites
P. falciparum Dd2 laboratory strains were maintained in culture
according to the method of Trager and Jensen (Trager and Jensen,
1976) with modifications (Zofou et al., 2013). The parasites were
grown in O+ red blood cells (RBCs) maintained in complete malaria
culture medium composed of RPMI-1640 medium supplemented
with 2 mg/ml NaHCO3, 10 µg/ml hypoxanthine, 2 mg/ml glucose,
1% albumax II as source of proteins, lipids and 10 µg/ml
gentamicin. The cultures were incubated at 5% CO2, 5% O2, 90%
Nondo et al
N2 in a humidified incubator set at 37°C (SHEL LAB® Sheldon Mfg
Inc, OR, USA). All materials were purchased from SIGMA (Sigma®,
Steinheim, Germany) except Albumax II (GIBCO™, Invitrogen) and
gentamicin (ROTEX MEDICA, Trittau - Germany) which were
supplied locally in Cameroon.
Preparation of plant extracts and standard drug
Stock solutions of 400 µg/ml for each crude extract was prepared
by first dissolving 4 mg of crude extract into 100 µl dimethyl
sulfoxide (Sigma®) followed by addition of RPMI-1640 medium to 10
ml. Artemether (Sigma®) was first dissolved in dimethyl sulfoxide
and then diluted with RPMI-1640 medium to 5 µg/ml. All solutions
were sterilized by using 0.22 µm syringe-adapted filters (Corning®,
NY, USA) and stored at 4°C until use.
In vitro antiplasmodial activity assay
In vitro antiplasmodial activity was assessed using the parasite
lactate dehydrogenase (pLDH) assay (Makler et al., 1993). Nonsynchronized 1% parasitized red blood cells (pRBCs) at 2%
181
haematocrit (hct) in 96 well cell culture plates (Costar®, Corning,
NY, USA) were incubated in triplicates with 100 µg/ml crude
extracts or with 1.25 µg/ml artemether. Wells with parasitized cells
but without extract or drug served as negative controls (100%
parasite growth) and wells without parasitized cells but with red
blood cells only at 2% hct served as blank controls. The plates were
incubated for 48 h at 37°C in a humidified incubator set at 5% CO2,
5% O2, 90% N2. After incubation for 48 h parasite growth was
confirmed by the aid of a light/UV fluorescence microscope
(TENSION®, China) with Acridine orange filter (λmax Abs = 490 nm;
λmax Em = 525 nm) and a counting device (Lennox Grain Analysis
NG NG21, SPI®, USA) before the plates were frozen overnight at 20°C. In the pLDH assay the plates were thawed at room
temperature to hemolyse red blood cells, and the 10 µL of malaria
culture were incubated with 50 µL Malstat solutions and 12.5 µL
nitroblue tetrazolium/phenazine ethosulfate for 1 h in darkness.
Parasite growth was determined by measuring the activity of pLDH
enzymes at 650 nm using a microplate reader (Emax-Molecular
Devices Corporation, California, USA) and the optical density (OD)
values obtained were used to calculate antiplasmodial activity. The
average OD value of the blank control (2%hct RBC only) was
subtracted from all OD values. The antiplasmodial activity was
expressed as percentage inhibition rate of parasites growth.
(OD negative control – OD treated)
%Growth inhibition rate (%IR) =
×100
OD negative control
(3%) and whole stem (1%) as shown in Figure 3.
RESULTS
Documentation and identification of medicinal plants
used for treatment of malaria in Kagera and Lindi
regions, Tanzania
A total of 108 plants species distributed into 41 plant
families were documented and identified in six villages in
Tanzania (Table 1). Fourteen plant species (12.96%)
belonged to the family Compositae, 12 plant spp
(11.11%) belonged to Fabaceae, 8 plant spp (7.41%)
belonged to Euphorbiaceae, 6 plant spp (5.56%)
belonged to Melastomataceae and 4 plant spp (3.70%)
belonged to Myrtaceae. The families Anacardiaceae,
Graminae, Labiatae, Meliaceae and Rutaceae each had
3 plant spp (2.78%) while other families were represented
by 2 or 1 plant spp (Figure 1). The reported medicinal
plants were identified as trees (37%), herbaceous plants
(34%), shrubs (20%), climbers (5%), grass (2%) and
wood climbers (2%) as shown in Figure 2. In addition, all
the reported medicinal plants are administered orally,
mostly as decoctions. Boiling was the most common
method of preparation (Table 1). Leaves were the most
used part of the plants, representing 46% of all plant
parts reported followed by stem bark (19%), aerial parts
(15%), roots (8%), whole plants (4%), seeds (4%), fruits
In vitro antiplasmodial activity of the extracts
The results reported in Table 2 show that 16 (44.4%) out
of the 36 extracts of 31 plant species that were tested
inhibited the growth of the chloroquine-resistant Dd2
malaria parasite strains by more than 50%. The extract of
Bersema abyssinica stem barks was the most active with
86.67% inhibition rate followed by the extract of Bridelia
micrantha stem barks which inhibited parasite growth by
71.87%. The ethanol extracts of Anthocleista grandiflora
stem barks, Funtumia Africana stem bark and leaves, and
extracts from leaves of Vernonia glabra, Ipomoea rubens,
Pycnanthus angolensis, Eriobotrya japonica and
Oxyanthus speciosus were the least active with growth
inhibition rate of less than 30% against the chloroquineresistant Dd2 strains (Table 2).
DISCUSSION
The results of the current study support results of
previous ethnobotanical studies done in Tanzania and
outside Tanzania. In previous studies Abrus precatorius,
Adansonia digitata,
Azadirachta indica, Cassia
182
J. Med. Plants Res.
Figure 1. Distribution of plant species into different families
Figure 2. Percentage use of different types of plants. WC = wood
climber, G = grass, SH = shrub, CL = climber, T = tree, H = herbs
didymobotrya, Dombeya shupangae, Ethrina sacleuxii,
Lantana
camara,
Mangifera
indica,
Maytenus
senegalensis, Momordica foetida, Parinari excelsa,
Pseudospondias microcarpa, Psidium guajava, Syzygium
Nondo et al
183
Figure 3. Percentage use of different plant parts. L = leaves, F
= fruits, S = seeds, WP = whole plant, R = root, SB = stem
bark, ST = whole stem, AP = aerial part.
cordatum, Todalia asiatica, Vangueria infausta, Vernonia
amygdalina, and Zanthoxylum chalybeum were reported
to be used in the treatment of malaria in Tanzania and
some of them have shown good in vitro antimalarial
activity against multi-drug resistant P. falciparum K1
malaria parasites (Amri et al., 2012; Augustino et al.,
2011; Gessler et al., 1994; Weenen et al., 1990).
Similarly, Erythrina abyssinica, Markhamia lutea, Teclea
nobilis, Adansonia digitata, Lantana camara, Azadirachta
indica, Zynthoxylum chalybeum, Maytenus senegalensis,
Vernonia amygdalina, Momordica foetida, Mangifera
indica, Moringa oleifera, Leonotis nepetifolia, Maesa
lanceolata, Psidium guajava, Funtumia africana, Canna
indica, Cymbopogon citratus and Pycnanthus angolensis
are used in traditional medicine for malaria treatment in
Kenya, Uganda, Cameroon and Nigeria (Lacroix et al.,
2011; Nguta et al., 2010; Tabuti et al., 2008; Titanji et al.,
2008; Katuura et al., 2007; Odugbemi et al., 2007).
It is notable that some of the reported plants belong to
the families Compositae (13%), Euphorbiaceae (7.4%),
Fabaceae (11.1%), and Rubiaceae (9.2%) which are
known to contain chemical compounds with good
antimalarial properties (Ntie-Kang et al., 2014; Batista et
al., 2009). The study has provided useful information that
supports traditional healers’ claims for antimalarial activity
and earlier observations that plants used in traditional
medicine are a potential source of new antimalarial lead
compounds (Onguéné et al., 2013; Bero et al., 2009).
All the extracts tested for in vitro antiplasmodial activity
at 100 µg/ml inhibited the growth of malaria parasites to
different percentages. Bersama abyssinica, Bridelia
micrantha, Canarium schweinfurthii and Antiaris toxicaria
stem bark extracts; Aspilia natalensis, Aspilia
mossambicensis and Desmodium salicifolium aerial part
extracts; Maesa lanceolata and Rhytignia obscura leaf
extracts; Pycnanthus angolensis fruit and Hallea
rubrostipulata root extracts inhibited parasite growth by
more than 60%. The ethanol extract of B. abyssinica was
the most active with 86.67% inhibition rate against Dd2.
In a previous study Kassa et al. (1996) reported that the
ethanol extract of B. abyssinica stem bark exhibited good
in vitro antimalarial activity against P. falciparum tineFAC-2/ Ethiopia with IC50 = 11 µg/ml. Similarly, a study
done in Cameroon by Ngemenya et al. (2005) showed
that the methanol extract of B. abyssinica leaves
exhibited good in vitro antiplasmodial activity with an IC50
of 2.7 µg/ml. Meanwhile, the chloroform extract of M.
lanceolata was reported to exhibit very good antiplasmodial
184
J. Med. Plants Res.
Table 1. Medicinal plants used traditionally in the treatment of malaria in Kagera and Lindi regions, Tanzania
Preparation
Voucher number
SH
CL
Part (s)
used
R, L
WP
Decoction
Decoction
RN 01
RN 02
Omugorogoro
T
SB
Decoction
RN 03
Pseudospondias microcarpa (A. Rich) Engl
Omuziru
T
L
RN 04
Rhus vulgaris Meikle
Omukanja
SH
R, L, F
RN 05
Mangifera indica L.
Omnembe, Mwembe
T
SB
Decoction
Root and leaf Decoction. Ripe fruits
eaten
Decoction
Apocynaceae
Funtumia africana (Benth) Staff
Holarrhena pubescens (Huch – Ham) G.Don
Mwezamaino, Omwelamaino
Nalupande
T
SH
L
R
Decoction
Decoction
RN 07
4665
Araliaceae
Bignoniaceae
Schefflera goetzenii Harms
Markhamia lutea (Benth) K. Schum
Olugogome
Omushambya
T
T
SB, L
SB
Decoction
Decoction
RN 08
RN 09
Bombacaceae
Adansonia digitata L.
Mbuyu
T
L, F
Leaves are eaten like vegetables.
Powder from dry fruits used to make
juice
RN10
Bulsaninaceae
Impatiens gomphophylla Bak.f
H
L
Decoction
RN 11
Burseraceae
Canarium schweinfurthii Engl.
Olwita mkole
Omubafu wa kike/muubani wa
kike
T
SB, L
Decoction
RN 12
Celastraceae
Salacia lovettii N. Hallé & B. Mathew
Maytenus senegalensis (Lam.) Exel
Omzindabikaka
Omunyaburiko
T
T
SB, L
SB, L
Decoction
Decoction
RN 13
RN14
Bidens schimperi Sch. Bip ex Walp
Orwongwa
H
AP
Aspilia mossambicensis (Oliv.) Wild
Eshurwa rusharila, Esisa
H
AP, WP
Gynura scandens O. Hoffm
Ekizimya mulilo
CL
L
Vernonia colorata (Wild.) Drake
Ekishura
SH
L
Family
Plant species
Vernacular name
Nature
Acanthaceae
Acanthus pubescens (Oliv.) Vatke
Thunbergia alata (Sims)
Amatoju
Wankula
Agavaceae
Dracaena steudneri Engl.
Anacardiaceae
Compositae
Fresh aerial parts pounded then mixed
with clean water, taken orally.
Fresh aerial parts pounded then mixed
with clean water, taken orally.
Fresh leaves squeezed to get juice.
Juice taken orally
Decoction
RN 06
RN 15
RN 16
RN17
RN 18
Nondo et al
Table 1. Cont’d
Convolvulaceae
Cucurbitaceae
Euphorbiace
Fabaceae
Vernonia amygdalina Delile
Omubilizi
T
L
Decoction
Crassocephalum mannii (Hook.f) Milne-Redh
Omugango
T
SB, L
Decoction
Crassocephalum vitellinum (Benth) S. Moore
Ekishenda
H
AP, L
Aspilia pluriseta (Schweinf)
Bidens pillosa L.
Lusharila eshurwa
Akakurura
H
H
AP
AP
Aspilia natalensis (Sond) Wild
Kanyamoisa
H
L
Melanthera scandens (Schum &Thonn) Roberty
Guizotia scabra (Vis.) Chiov
Omlela
Echihongosheija
H
H
L
L
Decoction or fresh leaves squeezed to
get juice, taken orally.
Decoction
Decoction
Decoction. Fresh leaves squeezed and
liquid obtained applied in the nose
Decoction
Decoction
Senecio spp
Ekikarabwe
H
L
Decoction
Vernonia glabra (Steetz) Vatke
Msangusangu
H
L
Decoction
RN 24
RN 25
Voucher not
collected
4664
Ipomoea rubens Choisy
Momordica foetida Schum.
Kataba
Orwihula
CL
SH
L
WP
Decoction
Decoction
RN 26
RN 27
Alchornea cordifolia (Schum & Thonn) Müell. Arg
Omujululuzi
SH
L
Sapium ellipticum (Hochst.) Pax
Omushasha
T
L, SB
Phyllanthus nummulariifolius Poir
Ricinodendron heudelotii (Baill) Pax
Croton macrostachyus Dell
Bridelia micrantha (Hochst.) Bail
Acalypha indica L.
Karungi
Kabaka njagala
Omwowa
Omushamako
Obweya
H
SH
T
T
H
AP
L
SB
R,SB
L, S
Canna indica L.
Maruru
H
S
Erythrina abyssinica D.C
Cassia didymobotrya Fress
Desmodium salicifolium (Poir) DC
Omulinzi
Omulembelembe
Batengeliange/Omukongoranwa
T
SH
H
SB
L
AP, L
Decoction or young fresh leaves
pounded then mixed with water, taken
orally
Decoction of leaves or stem bark. Fresh
leaves can be used to prepare cold
infusion
Decoction
Decoction
Decoction
Decoction
Decoction
Seeds grounded, powder used to make
warm infusion.
Decoction
Decoction
Decoction
RN 19
Voucher not
collected
RN 20
RN 21
RN22
RN 23
RN 28
RN 29
RN 30
RN 31
RN 32
RN 33
RN 34
RN 35
RN 36
RN 37
RN 38
185
186
J. Med. Plants Res.
Table 1. Cont’d.
Graminae
Labiatae
Loganiaceae
Lythraceae
Voucher not
collected
RN 39
Tephrosia aequilata Bak
Endalabugazi
H
WP
Decoction
Kotschya africana Endl.
Ekyangwe ekiango
H
AP
Eriosema parviflorum E. Mey
Mshelere
H
L
Dalbergia malangensis E.P Sousa
Macrotyloma axillare (E. Mey) Verdc
Omugorora
Akaihabukuru
WC
CL
L
AP
Indigofera arrecta A. Rich
Omusoroka
H
AP
Abrus precatorius L.
Karigoligo
CL
L
Erythrina schliebenii Harms
Erythrina sacleuxii Hua
Mlindimila
Mlindimila
T
T
SB
SB
Decoction
Decoction or fresh leaves squeezed to
get juice, taken orally
Decoction
Decoction
Decoction or aerial parts pounded then
mixed with water, taken orally.
Fresh leaves pounded then mixed with
water, taken orally.
Decoction
Decoction
4661
4662
Pennisetum purpureum Schum
Vossia cuspidata (Roxb) Grift
Cymbopogon citratus L.
Olutete
Ekishararago
Mchaichai
G
G
G
L
L
L
Decoction
Decoction
Hot infusion
RN 45
RN 46
RN 47
Platostoma africanum P. Beauv.
Leonotis nepaetifolia (L.) R. Br
Nyanjaeyera
Ekitatelante
SH
H
AP
L
RN 48
RN 49
Ocimum kilimandscharicum Gürke
Kaswagara
H
S
Dry powder used to make warm infusion
Decoction
Powder from dry seeds used to make
warm water infusion
Anthocleista grandiflora Gilg
Mgabaigana
T
L, R, SB
Strychnos spinosa Lam.
Orurema
SH
L
Lawsonia inermis L.
Eina
H
L, S
Dissotis rotundifolia (Sm) Triana
Obwehehe/Obwee
H
AP
Melastomastrum capitatum (Vahl) A. & R. Fern)
Katuntun
H
AP
Melastomataceae
RN 40
RN 41
RN 42
RN 43
RN 44
RN 50
Decoction
Dry powder used to make warm infusion
or decoction bathed to children
RN 51
Voucher not
collected
Leaf decoction. Powdered seeds used
to make warm infusion
RN 52
Decoction or fresh aerial parts pounded
then mixed with clean water, taken orally
Fresh aerial parts pounded then mixed
with clean water. Dry aerial parts used
to prepare warm infusion
RN 53
RN 54
Nondo et al
Table 1. Cont’d.
Aerial parts pounded then mixed with
water, taken orally
Decoction or cold infusion.
Decoction
Fresh leaves squeezed then mixed with
water, taken orally.
Dissotis melleri Hook.f.
Ekituntun/Etuntun
H
AP
Melastomastrum segregatum (Benth) A.& R Fern.
Dissotis brazzae Cogn
Eitulu
Bulitulo
H
H
AP
AP
Pilea holstii Engl.
Omufura/Eimyo
SH
L
Trichilia emetica Vahl.
Omushunguti, Mushunguti
T
SB, L
Decoction
Pseudobersama mosssambicensis (Sim) Verdc
Omusiibi
T
SB, L
Decoction
Azadirachta indica A. Juss.
Mwarobaini
T
L
Decoction
RN 59
Voucher not
collected
RN 60
Melianthaceae
Moraceae
Bersama abyssinica
Antiaris toxicaria (Pers) Lesch
Omujalya
Omujuju
SH
T
R, SB, L
SB, L
Decoction
Decoction
RN 61
RN 62
Moringaceae
Moringa oleifera (Lam.)
Mlonge
T
L
Decoction. Dry powder used to make
warm infusion
RN 63
Myristicaceae
Myrsinaceae
Pycnanthus angolensis (Welw.) Warb
Maesa lanceolata Forsk
Omunonoba
Omuzilanyama/ Omuhanga
T
T
SB
RB, SB, L
Decoction
Decoction
RN 64
RN 65
Syzygium guineense (Willd.) DC
Omuchwezi
T
L
RN 66
Syzygium cordatum Krause
Omugege
SH
SB, L
Syzygium cumini (L.) Skeels
Mzambarau
T
SB, L, F
Psidium guajava L.
Mpera
T
L
Decoction
Fresh leaves or stem barks grounded
then mixed clean with water, taken orally
Decoction of stem bark or leaf. Ripe
fresh fruits eaten
Fresh leaves pounded then mixed with
clean water, used orally
Onagraceae
Ludwigia octovalvis (Jacq.) Haven ssp.
brevisepala (Brenan) P.H. Raven
Wejunge
H
L
Decoction
RN 70
Palmae
Raphia farinifera (Gaertn) Hyl.
Omubobo
T
ST, R
Decoction
Voucher not
collected
Meliaceae
Myrtaceae
RN 55
RN 56
RN 57
RN 58
RN 67
RN 68
RN 69
187
188
J. Med. Plants Res.
Table 1. Cont’d.
Decoction or aerial parts pounded then
mixed with water, taken orally.
Aerial parts pounded then mixed with
water, taken orally
Polygonum senegalense Meisn
Kinyanyanja
H
AP
Rumex abyssinica
Akanulilizi
H
AP
Punicaceae
Punica granatum L.
Omukomamanga
T
F
Outer part of the fruits dried then
powdered. Powder used to make warm
infusion
RN 73
Rosaceae
Eriobotrya japonica (Thunb.) Lindl
Musharazi/Omusharazi
T
R, SB, L
Root decoction. Powdered dry stem
barks and leaves used to prepare warm
infusion. Fresh fruits eaten.
RN 74
Spermacoce princeae (K. Schum) Verdc
Psydrax parviflora (afzel) Bridson ssp.
Rubrocostata (Robyn) Bridson
Ekaiza nkoju
H
AP
Omushangati
T
SB, L
Tricalysia coriacea (Benth.)Hiern
Omushekera
SH
L, F
Vangueria infausta Burch
Mtugunda, Amabungo
SH
L
Decoction
Rytigynia obscura Robyns
Oxyanthus speciosus DC
Pentas bussei (K. Krause)
Pavetta lynesii Bridson
Chassalia umbraticola Vatke
Hallea rubrostipulata (K. Schum) J.F. Leny
Omulokola/Lulokola
Omwanikibira
Rusharila kibira
Orwingula, Omuingula
Mwataibare
Mchunguchugu
SH
T
H
SH
SH
T
L
L
AP
L
SB, L
SB, R
Decoction
Decoction
Decoction
Decoction
Decoction
Decoction
Zanthoxylum chalybeum Engl.
Omutaregwairungu
T
SB
Decoction
Toddalia asiatica (L.) Lam
Orukwatango
CL
L
Decoction
Teclea nobilis Delile
Omuzo
T
R
Decoction
Sapindaceae
Lecaniodiscus fraxinifolius Bak
Omwasha
T
L
Decoction
Voucher not
collected
Solanacaeae
Physalis peruviana L.
Kitutun kikubwa
H
L
Fresh leaves pounded then mixed with
water, used orally
RN 85
Polygonaceae
Rubiaceae
Rutaceae
Decoction
Decoction of SB or leaves. Fresh leaves
squeezed to get juice.
Fresh leaves pounded then mixed with
clean water or fresh leaves boiled
RN 71
RN 72
RN 75
RN 76
RN 77
Voucher not
collected
RN 78
RN 79
RN 80
RN 81
RN 82
4663
RN 83
Voucher not
collected
RN 84
Nondo et al
Table 1. Cont’d.
Datura stramonium L.
Ekitaigwa, Amalulu
SH
S
Decoction
RN 86
Sterculiaceae
Dombeya shupangae (K. Schum)
Omutangarara, Mtangarara
T
L
Ulmaceae
Trema orientalis Bullock
Omuhuwe
T
SB, L
Umbelliferae
Centella asiatica (L.) Urb
Mbatama
H
WP
Decoction
Dry powder used to prepare warm
infusion
Decoction
RN 87
Voucher not
collected
RN 88
Verbenacea
Clerodendrum cephalanthum Oliv
Lantana camara L.
Lantana trifolia L.
Ekishekesheke
Lukulata
Omuhuchi
WC
SH
SH
L
L
AP
Decoction
Decoction
Decoction
RN 89
RN 90
RN 91
Aframomum angustifolium (Sonn.) K. Schum
Orushasha
SH
L
Cold infusion
Costus afer Ker-Gawl
Ekigagi
H
R, AP
Decoction or eaten raw
Zingiberaceae
Voucher not
collected
RN 92
Plant part: R = root, ST = Stem, SB = Stem bark, AP = Aerial parts, L = Leaves, F = Fruits, S = Seeds, WP = Whole plant. Nature of the plant: SH = Shrub, H = Herb, T = Tree, CL = Climber,
WC = Wood climber, G = Grass
Table 2. In vitro antiplasmodial activity of 80% ethanol crude extracts at 100 µg/ml against P. falciparum Dd2 strains.
Plant Family
Plant species
Part tested
Acanthaceae
Acanthus pubescens (Oliv.)
R
Percentage growth inhibition rate (% IR) of crude extracts at 100 µg/ml
on P. falciparum Dd2 strain
41.50 ± 6.32
Apocynaceae
Funtumia africana (Benth) Staff
Funtumia africana (Benth) Staff
SB
L
17.51 ± 8.07
14.21 ± 2.74
Burseraceae
Celastraceae
Canarium schweinfurthii Engl.
Salacia lovetii N. Halle & B. Mathew
SB
L
61.94 ± 15.61
32.35 ± 3.50
Compositae
Guizotia scabra (Vis.) Chiov
Aspilia mosambicensis (Oliv.) Wild
Aspilia natalensis (Sond) Wild
Vernonia glabra (Steetz) Vatke
WP
AP
AP
L
49.09 ± 0.03
69.34 ± 7.05
65.23 ± 0.25
12.44 ± 1.18
Convolvulaceae
Ipomoea rubens Choisy
L
27.61 ± 1.83
189
190
J. Med. Plants Res.
Table 2. Cont’d.
Bridelia micrantha (Hochst.) Bail
Phyllanthus nummulariifolius Poir
Phyllanthus nummulariifolius Poir
SB
WP
WP
71.87 ± 1.53
38.88 ± 7.83
51.31 ± 12.84a
Erythrina schliebenii Harms
Dalbergia malangensis E.P Sousa
Dalbergia malangensis E.P Sousa
Macrotyloma axillare (E. Mey) Verdc
Desmodium salicifolium (Poir) DC
Erythrina sacleuxii Hua
SB
L
ST
AP
AP
SB
39.86 ± 13.97
39.78 ± 7.88
32.37 ± 8.49
33.21 ± 1.37
68.41 ± 13.33
42.08 ± 5.49
Labiatae
Leonotis nepaetifolia (L.) R. Br
AP
54.43 ± 9.07
Loganiaceae
Anthocleista grandiflora Gilg
SB
9.18 ± 6.77
Melastomataceae
Melastomatrum capitatum (Vahl) A. & R. Fern)
Dissotis brazzae Cogn
Dissotis rotundifolia (Sm) Triana
AP
AP
AP
39.06 ± 3.47
52.31 ± 0.55
33.64 ± 0.44
Moraceae
Antiaris toxicaria (Pers) Lesch
Antiaris toxicaria (Pers) Lesch
L
SB
34.72 ± 6.25
61.18 ± 2.02
Melianthaceae
Bersama abyssinica
SB
86.67 ± 11.32
Myristicaceae
Pycnanthus angolensis (Welw.) Warb
Pycnanthus angolensis (Welw.) Warb
Pycnanthus angolensis (Welw.) Warb
F
SB
L
65.43 ± 9.62
40.63 ± 8.10
28.63 ± 5.07
Myrsinaceae
Myrtaceae
Rosaceae
Maesa lanceolata Forsk
Syzygium cordatum Krause
Eriobotrya japonica (Thunb.) Lindl
L
SB
L
53.46 ± 1.86
55.46 ± 13.43
20.52 ± 3.35
Hallea rubrostipulata (K. Schum) J.F.Leny
Hallea rubrostipulata (K. Schum) J.F.Leny
Pentas bussei (K. Krause)
Oxyanthus speciosus DC
Rhytignia obscura Robyns
Artemether (1.25 µg/ml)
R
SB
AP
L
L
64.54 ± 7.56
53.22 ± 5.58
59.92 ± 4.41
29.19 ± 9.66
22.35 ± 5.42
91.98 ± 10.46
Euphorbiaceae
Fabaceae
Rubiaceae
a
WP= whole plant; L= leaves; SB= stem bark; ST= stem; AP= aerial parts (stem plus leaves); R= root; F= fruits = aqueous extract
Nondo et al
activity with IC50 = 1.6 µg/ml against P. falciparum
clinical isolates (Katuura et al., 2007). Most plants tested
in this study showed low parasite growth inhibition rate. It
is not easy to identify the specific reasons for low activity
but factors such as the solvent used for extraction, the
method of preparation, storage conditions, and variation
in the active constituents due to seasonal or geographical
and model of testing may also reduce the efficacy of the
extract (Weeneen et al., 1990). Furthermore, Chhabra et
al. (1993) reported that preparations of medicinal plants
can be used orally, rubbed into scarification, inhaled as
fumes, splashed on the eyes, poured into the wound or
sniffed. In this study we found that all preparations were
administered orally in the form of decoction (boiled water
extracts), infusion (hot water extract), juice or taken as
raw fruits. In the oral route, the bioactive molecules are
exposed to various barriers and enzyme systems before
reaching the systemic circulation. This causes some
bioactive molecules to be modified by metabolism thus,
either enhance or reduce their antiplasmodial activity
suggesting that the antiplasmodial activity of
metabolically activated compounds may not be evident in
in vitro assays.
Conclusion
This study reported 108 medicinal plants that are used in
the traditional medicine for treatment of malaria and
fevers in Kagera and Lindi regions of Tanzania. In vitro
assays revealed substantial antiplasmodial activities of
15 plants out of 31 plant species tested. Although
questionnaire based evidence suggested that decoctions
from these plants were not acutely toxic, further toxicity
testing will be required to establish their safety profile.
Meanwhile these findings support the use of these plants
for the traditional treatment of malaria. Further in vitro
and in vivo screening supported by bioassay-guided
isolation of active compounds of plants showing good
safety margin are suggested.
Conflict of interests
The authors declare that they have no competing
interests
ACKNOWLEDGEMENTS
This work was financed by Sida through MUHAS capacity
building grants. Authors are very grateful to Sida for the
financial support. We are grateful to Mr. Mohamedi
Ngalanga, Mr. Didas Ngemera, Mr. Dominic Mushwahili,
Mr. Buchadi Tibikunda and Mr. Papianus Rwechungura
for showing us the medicinal plants traditionally used for
191
treatment of malaria in their areas. We would like to
extend our gratitude to Mr. Haji.O. Selemani (Botanist) for
identification of the documented medicinal plants.
Extraction of the plant extracts was done at the Institute
of Traditional Medicine in Tanzania whereas in vitro
antimalarial study was done at the Research Foundation
in Tropical Diseases and Environment, and at the
Biotechnology Unit, University of Buea in Cameroon. We
are grateful to MR4/BEI-resources (Manassas, VA, USA)
for donating malaria parasites used for this work.
REFERENCES
Amri E, Kisangau DP (2012). Ethnomedicinal study of plants used in
villages around Kimboza forest reserve in Morogoro, Tanzania. J.
Ethnobiol. Ethnomed. 8:1
Augustino S, Hall JB, Makonda FBS, Ishengoma RC (2011). Medicinal
Resources of the Miombo woodlands of Urumwa, Tanzania: Plants
and its uses. J. Med. Plants. Res. 5:6352-6372.
Batista R, Silva Ade Jr J, de Oliveira AB (2009). Plant-derived
antimalarial agents: new leads and efficient phytomedicines. Part II.
Non-alkaloidal natural products. Molecules 14:3037-3072.
Bero J, Frederich M, Quetin-Leclerq J (2009). Antimalarial compounds
isolated from plants used in traditional medicine. J. Pharm.
Pharmacol. 61:1401-1433.
Chhabra SC, Mahunnah RL, Mshiu EN (1993). Plants used in traditional
medicine in eastern Tanzania. VI. Angiosperms (Sapotaceae to
Zingiberaceae). J. Ethnopharmacol. 39:83-103.
Cox-singh J, Singh B (2008). Knowlesi malaria: newly emergent and of
public health importance ?, Trends Parasitol. 24:406-410.
Dondorp AM, Nosten F, Yi P, Das D, Phyo AP, Tarning J, Maung K,
Ariey F, Hampithakpong W, Lee SJ, Ringwald P, Silamut K, Iwong M,
Chotivanich K, Lim P, Herdman T, An SS, Yeung S, Singhasivanon
P, Day NPJ, Lindergardh N, Socheat D, White NJ (2009). Artemisinin
Resistance in Plasmodium falciparum Malaria. N. Engl. J. Med.
361:455-467.
Gessler MC, Msuya DE, Nkunya MHH, Mwasumbi LB, Schar A,
Heinrich M, Tanner M (1995). Traditional healers in Tanzania: the
treatment of malaria with plant remedies J. Ethnopharmacol. 48:131144.
Gessler MC, Nkunya MH, Mwasumbi LB, Heinrich M, Tanner M (1994).
Screening Tanzanian medicinal plants for antimalarial activity. Acta
Trop. 56:65-77.
Kassa M, Mohana R, Hunde A (1996). Antimalarial activity of Bersama
Abyssinica against Plasmodium Falciparum. Ethiop. Phar. J. 14:1621.
Katuura E, Waako P, Tabuti JRS, Bukenya-Ziraba R, Ogwal-Okeng J
(2007). Antiplasmodial activity of extracts of selected medicinal plants
used by local communities in western Uganda for treatment of
malaria. Afr. J. Ecol. 45(S3):94-98.
Kinung’hi SM, Mashauri F, Mwanga JR, Nnko SE, Kaatano GM, Malima
R, Mboera LE (2010). Knowledge, attitudes and practices about
malaria among communities: comparing epidemic and non-epidemic
prone communities of Muleba district, North-western Tanzania. BMC
Public Health 10:395.
Lacroix D, Prado S, Kamoga D, Kasenene J, Namukobe J, Krief S,
Brunois F (2011). Antiplasmodial and cytotoxic activities of medicinal
plants traditionally used in the village of Kiohima, Uganda. J.
Ethnopharmacol. 133:850-855.
Mahunnah RL (1987).Traditional plant medicines used by Hayas of
North-western Tanzania. J. Econ. Tax. Bot. 10:371-379.
Mahunnah RLA, Uiso FC, Kayombo EJ (2012). Documentation of
Traditioanal Medicine in Tanzania: A Traditioanal Medicine Resource
Book. Dar es Salaam University Press, Dar es Salaam – Tanzania. p.
8.
192
J. Med. Plants Res.
Makler MT, Hinrichs DJ (1993). Measurement of the Lactate
Dehydrogenase Activity of Plasmodium falciparum as an Assessment
of paraistaemia. Am. J. Trop. Med. Hyg. 48:205-210.
Moshi MJ, Otieno DF, Mbabazi PK, Weisheit A (2009). The
ethnomedicine of the Haya people of Bugabo ward, Kagera Region,
north western Tanzania. J. Ethnobiol. Ethnomed. 5:24.
Ngemenya M, Titanji V, Akam T, Yong J, Tane P, Fanso-Free S,
Berzins K (2005). Antiplasmodial activity and toxicity of extracts and
products from selected medicinal plants used in Cameroon. Acta
Trop. 96S:S1-S506.
Nguta JM, Mbaria JM, Gakuya DW, Gathumbi PK, Kiama SG (2010).
Traditional antimalarial phytotherapy remedies used by the South
Coast community, Kenya. J. Ethnopharmacol. 131:256-267.
Ntie-Kang F, Onguéné PA, Lifongo LL, Ndom JC, Sippl W, Mbaze LM
(2014). The potential of anti-malarial compounds derived from African
medicinal plants. Part II : a pharmacological evaluation of nonalkaloids and non-terpenoids. Malar. J. 13:81.
Odugbemi TO, Akinsulire OR, Aibinu IE, Fabeku PO (2007). Medicinal
plants useful for malaria therapy in Okeigbo, Ondo state, Southwest
Nigeria. Afr. J. Tradit. Compl. Alter. Med. 4:191-198.
Onguéné PA, Ntie-kang F, Lifongo LL, Ndom JC, Sippl W, Meva’a ML
(2013). The potential of anti-malarial compounds derived from African
medicinal plants. Part I: A pharmacological evaluation of alkaloids
and terpenoids. Malar. J. 12:449.
Tabuti JRS (2008). Herbal medicines used in the treatment of malaria in
Budiope county , Uganda. J. Ethnopharmacol. 116:33-42.
TACAIDS, ZAC, NBS, OCGS, IFC International (2013). Tanzania
HIV/AIDS and Malaria Indicator Survey 2011-12. Dares Salaam,
Tanzania: TACAIDS, ZAC, NBS, OCGS, and ICF International.
Titanji VP, Zofou D, Ngemenya MN (2008). The Antimalarial Potential of
Medicinal Plants used for the Treatment of Malaria in Cameroon folk
Medicine. Afr. J. Complement. Alter. Med. 5302-321.
Trager W, Jensen JB (1976). Human malaria parasites in continuous
culture. Science. 193:673-5.
View publication stats
United States Agency for International Development (USAID) (2014).
President’s Malaria Initiative: Tanzania Malaria Operational Plan FY
2014.
Weenen H, Nkunya MH, Bray DH, Mwasumbi LB, Kinabo LS, Kilimali
VA (1990). Antimalarial activity of Tanzanian medicinal plants. Planta
Med. 56:368-370.
Wells TN (2011). Natural products as starting points for future antimalarial therapies: going back to our roots ? Malar. J. 10(Suppl1):S3.
WHO (2002). Traditional Medicine Strategy 2002-2005. WHO Press,
Geneva, Switzerland. WHO/EDM/TRM/2002.1
Wongsrichanalai C, Pickard AL, Wernsdorfer WH, Meshnick SR (2002).
Reviews: Epidemiology of drug-resistant malaria. Lancet Infect. Dis.
2:209-218.
World Health Organization (WHO) (2012). WHO Global Malaria
Programme: World Malaria Report 2012. WHO Press, Geneva,
Switzerland.
World Health Organization (WHO) (2013). WHO Malaria Factsheet No
94 - 2013. WHO press, Geneva, Swirtzerland.
Zofou D, Tematio EL, Ntie-Kang F, Tene M, Ngemenya MN, Tane P,
Titanji VPK (2013). New antimalarial hits from Dacryodes edulis
(Burseraceae)- Part I: isolation, in vitro activity, in silico “druglikeness” and pharmacokinetic profiles. PloS One. 8:11