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Journal of Ethnopharmacology 70 (2000) 143 – 149

www.elsevier.com/locate/jethpharm

Cytotoxicity of some medicinal plant extracts used in


Tanzanian traditional medicine
Appolinary Kamuhabwa a, Charles Nshimo b, Peter de Witte a,*
a
Laboratorium 6oor Farmaceutische Biologie en Fytofarmacologie, Faculteit Farmaceutische Wetenschappen,
Katholieke Uni6ersiteit Leu6en, Van E6enstraat 4, B-3000 Leu6en, Belgium
b
Department of Pharmacognosy, Faculty of Pharmacy, Muhimbili Uni6ersity College of Health Sciences,
Dar es Salaam, Tanzania
Received 7 June 1999; received in revised form 30 August 1999; accepted 6 September 1999

Abstract

Using the ethnomedical data approach, some Tanzanian plants that are used in Tanzanian traditional medicine for
cancer or non-cancer diseases were collected and evaluated for cytotoxic activity. The antiproliferative effect of the
methanolic extracts (10 and 100 mg/ml) of 47 plants was evaluated in vitro on three human cell lines (HeLa, cervical
carcinoma; HT29, colon adenocarcinoma; and A431, skin carcinoma). From the nine plants that are used to treat
cancer, two plants (22%) exhibited pronounced cytotoxic effect ( B 25% cell proliferation) at least in one of the tested
cell lines. For the 38 plants that are used to treat non-cancer diseases, 14 plants (37%) exhibited pronounced cytotoxic
effect (B25% cell proliferation). Cell type cytotoxic specificity was observed in some extracts. Overall, the A431 cells
were much more sensitive to most of the extracts than the other cell lines. For the plants that are used as anticancer
herbal drugs, our results indicate that there is no correlation between the reported use of these plants and their
cytotoxic activity obtained in this study. However, plants that have shown pronounced cytotoxic activity will be
evaluated further for the possible isolation of active antitumor compounds. © 2000 Elsevier Science Ireland Ltd. All
rights reserved.

Keywords: Cytotoxic; Traditional medicine; Plant extracts; Ethnomedical data

1. Introduction pounds (Cragg et al., 1994). Indeed there have


been worldwide efforts to discover new anticancer
It is well established that plants have been a agents from plants. There are different ap-
useful source of clinically relevant antitumor com- proaches for the selection of plants that may
contain new biologically active compounds
(Cordell et al., 1991; Schwartsmann and Work-
man, 1993). One of the approaches used is the
* Corresponding author. Tel.: + 32-16-323432; fax: + 32-
16-323460. ethnomedical data approach, in which the selec-
E-mail address: peter.dewitte@farm.kuleuven.ac.be (P. de tion of a plant is based on the prior information
Witte) on the folk medicinal use of the plant. It is

0378-8741/00/$ - see front matter © 2000 Elsevier Science Ireland Ltd. All rights reserved.
PII: S 0 3 7 8 - 8 7 4 1 ( 9 9 ) 0 0 1 6 1 - 0
144 A. Kamuhabwa et al. / Journal of Ethnopharmacology 70 (2000) 143–149

generally known that ethnomedical data provides methanolic extracts were obtained after removing
substantially increased chance of finding active the solvent by evaporation under reduced pres-
plants relative to random approach (Chapuis sure. Dry methanolic extracts were then dis-
et al., 1988; Cordell et al., 1991). However, as solved in dimethyl sulphoxide (DMSO) to give
for cancer, the disease is complicated and hetero- the desired stock solutions of the extracts.
geneous, which makes it difficult to be well
diagnosed, especially by traditional healers. The 2.3. Cell lines and culture medium
ethnomedical information obtained for a plant
extract that is used to treat cancer might there- HeLa (cervical carcinoma, human), HT29,
fore not be reliable (Cragg et al., 1994). (colon adenocarcinoma, human) and A431 (skin
Traditional Tanzanian medicinal herbs have carcinoma, human) cell lines obtained from the
been used in the treatment of different diseases American Type Culture Collection (Rockville,
in the country for centuries. There have been MD) were used in this study. All cell lines were
claims that some traditional healers in Tanzania grown at 37°C in humidified 5% CO2 and 95%
can successfully treat cancer using herbal drugs. air atmosphere in minimum essential medium
Indeed, some traditional healers who were inter- (MEM) with Earle’s salt containing 2 mM L-glu-
viewed recently in the country stressed that they tamine, non-essential aminoacids (100× ), peni-
have successfully treated patients presented with cillin (100 IU/ml), streptomycin (100 mg/ml),
cancer or cancer related diseases. tylocin (60 mg/ml), amphotericin B (0.25 mg/ml)
In the course of our screening studies for and 10% fetal calf serum (FCS). MEM, L-glu-
the antitumor compounds from plants, we under-
tamine, non-essential aminoacids, penicillin,
took the present study to evaluate the in vitro
streptomycin, tylocin, amphotericin B, FCS and
cytotoxic activity of nine plant extracts that
phosphate-buffered saline (PBS) were obtained
are used in Tanzanian traditional medicine as
from Gibco BRL (Paisley, UK).
anticancer herbal drugs. Using three human
Dilution of stock solutions was made in cul-
cell lines (HeLa, HT29 and A43), another 38
ture medium yielding final extracts concentra-
plant extracts that are used for the treatment
tions of 10 and 100 mg/ml with a final DMSO
of other diseases in the country were also evalu-
ated. concentration of 0.1%. This concentration of
DMSO did not affect cell viability.

2. Materials and methods 2.4. Antiproliferati6e assay

2.1. Plant materials Cells were seeded onto 96-well tissue microtitre
culture plates (Falcon, NJ, USA) at 5 ×103 cells
All plant samples were collected from different per well, and incubated for 24 h at 37°C. The
parts of Tanzania and their respective voucher medium was replaced with fresh medium con-
specimens are deposited at the Department of taining different concentrations of extracts (100,
Pharmacognosy, Faculty of Pharmacy of the 10 mg/ml) or the vehicle. The cells were then
Muhimbili University College of Health Sciences, incubated at 37°C for 72 h. Afterwards the ex-
Dar es Salaam, Tanzania. tract containing medium was removed and cell
proliferation determined by quantification of the
2.2. Preparation of extracts cellular protein content using naphthol blue
black (Acros, Beerse, Belgium), as reported
For each plant sample, plant materials were (Palombella and Vicek, 1989). Experiments were
dried at room temperature and grounded. Dry performed in triplicate and the results were ex-
powdery plant samples were exhaustively ex- pressed as cell proliferation as the percentage of
tracted with methanol by maceration. Dry control.
A. Kamuhabwa et al. / Journal of Ethnopharmacology 70 (2000) 143–149 145

Table 1
List of tested plant species with their used parts and known medicinal uses or pharmacological actions

Plant species (Family) Part Common uses or actions Ref.

Pterocarpus angolensis DC. (Papilionaceae) Root Anemia, venereal, kidney C. Nshimo (pers. comm.)a
diseases
Clerodendrum myricoides (Hochst.) (Verbenaceae) Root bark Analgesic, antipyretic, Iwu (1993), C. Nshimo (pers.
infections comm.)
Oxygonium sinuatum (Meisn.) Dammer (Polygo- Whole plant Skin infections, amebia- Iwu (1993), C. Nshimo (pers.
naceae) sis, cancer comm.)
Rhus natalensis Krauss (Anacardiaceae) Root Hernia, abdominal pain C. Nshimo (pers. comm.)
Acacia nilotica (L.) Del. (Mimosaceae) Root Cancer, sclerosis Johnson (1999)
Dombeya shupange Sprague (Sterculiaceae) Root bark Venereal diseases, insan- Iwu (1993)
ity
Parinari excelsa Sabine (Chrysobalanaceae) Stem bark Malaria, antiseptic C. Nshimo (pers. comm.)
Ximenia caffra Sond. (Olacaceae) Root Anthelmintic, chest pain C. Nshimo (pers. comm.)
Salacia madagascariensis (Lam.) DC. (Celastraceae) Root Hernia C. Nshimo (pers. comm.)
Cassia abbre6iata (L.) Det. (Mimosaceae) Root Stomach pains, infec- C. Nshimo (pers. comm.)
tions
Margaritaria discoidea (Baill.) Webster (Euphorbi- Root bark Fever, coughs, inflamma- Iwu (1993)
aceae) tion
Vangueria tomentosa Hochst. (Rubiaceae) Root Anthelmintic C. Nshimo (pers. comm.)
Markhamia hildebrandtii (Bak.) Sprague (Bignoni- Root Analgesic, difficult urina- C. Nshimo (pers. comm.)
aceae) tion
U6aria acuminata Oliv. (Annonaceae) Root Dysentery, painful men- C. Nshimo (pers. comm.)
struation
U6aria leptocladon Oliv. (Annonaceae) Stem bark Venereal diseases C. Nshimo (pers. comm.)
Annickia kummeriae Engl. and Diels (Annonaceae) Barks Antiseptic for wounds C. Nshimo (pers. comm.)
Entanda abyssinica A. Rich. (Mimosaceae) Root bark Hypotensive, analgesic, Iwu (1993), C. Nshimo (pers.
cancer comm.)
Ocotea usambarensis Engl. (Lauraceae) Root bark Swellings, stomach pains C. Nshimo (pers. comm.)
Zanthoxylum chalybeum Engl. (Rutaceae) Root Fever, bilharzia C. Nshimo (pers. comm.)
Pteleopsis myrtifolia (Laws.) Engl. and Diels (Com- Root Venereal diseases C. Nshimo (pers. comm.)
bretaceae)
Cassia didymobotrya Fres. (Leguminoceae) Leaves Anemia, laxative, an- C. Nshimo (pers. comm.)
thelmintic
Cana6aria rosea DC. (Papilionaceae) Seeds Skin diseases, constipa- C. Nshimo (pers. comm.)
tion, cancer
Fluggea 6irosa Baill. (Euphorbiaceae) Root bark HIV related diseases C. Nshimo (pers. comm.)
Thylachium africanum Lour (Capparidaceae) Leaves Toothache, fever Iwu (1993)
Gnidia kraussiana Meisn. (Thymelaeaceae) Root Skin diseases, bronchitis, Iwu (1993), C. Nshimo (pers.
cancer comm.)
Harissonia abyssinia Oliv. (Simaroubaceae) Root Fever, dyspepsia, cancer Iwu (1993), C. Nshimo (pers.
comm.)
Crinum papillosum Nordal (Amarylidacea) Whole plant Antiseptic C. Nshimo (pers. comm.)
Gloriosa superba L. (Liliaceae) Root Anthelmintic, cancer, Iwu (1993), Johnson (1999)
colic, malaria
Markhamia obtusifolia (Bak.) Sprague (Bignoni- Root Toothache, fever in chil- C. Nshimo (pers. comm.)
aceae) dren
Paullinia pinnata L. (Sapindaceae) Aerial parts Fever, bronchitis, Iwu (1993)
bruises, laxative
U6aria lucida Benth. (Anonaceae) Stem bark Gynecological problems C. Nshimo (pers. comm.)
Acacia polyacantha Willd. (Mimosaceae) Roots Sterility (women), water C. Nshimo (pers. comm.)
deficiency
Minopsis fraticosa Boj. (Sapotaceae) Roots Constipation, hernia, C. Nshimo (pers. comm.)
venereal diseases
146 A. Kamuhabwa et al. / Journal of Ethnopharmacology 70 (2000) 143–149

Table 1 (Continued)

Plant species (Family) Part Common uses or actions Ref.

Euphorbia quandrangularis Pax (Euphorbiaceae) Roots Back, ribs and chest pain C. Nshimo (pers. comm.)
Dichrostachys cinerea (L.) Wight and Arn. (Mi- Whole plant Analgesic, antiviral, Iwu (1993), C. Nshimo (pers.
mosaceae) asthma comm.)
Capparis sepiaris L. (Capparidaceae) Root bark Cancer, fever, swollen Johnson (1999), C. Nshimo
stomach (pers. comm.)
Ziziphus mucronata Willd. (Rhamnaceae) Root Tonic, cold, lumbago, tu- Iwu (1993), Johnson (1999)
mor
Lannea stuhlmanii Engl. (Anacardiaceae) Root Tonic, antifungal, pain re- Iwu (1993)
lief
Opilia celtidifolia Guill. and Perr. (Opiliaceae) Stem Sleeping sickness, diuretic, C. Nshimo (pers. comm.)
purgative
Keetia zanzibarica (Klotzsch) Bridson (Theophras- Root Chest pain C. Nshimo (pers. comm.)
taceae)
Bauhinia thoningii Schumach. (Leguminoceae) Stem bark Bilharzia C. Nshimo (pers. comm.)
Kigelia africanum (Lam.) Benth. (Bignoniaceae) Stem bark Measles, analgesic, fevers C. Nshimo (pers. comm.)
Strychnos innocua Del. (Loganiaceae) Root Inflammations, colic, laxa- C. Nshimo (pers. comm.)
tive
Harungana madagascariensis Poir. (Guttiferae) Leaves Dysentery, leprosy Johnson (1999)
Bridelia micrantha (Hochst.) Baill. (Euphorbiaceae) Root bark Cough, diabetes, laxative, Iwu (1993), C. Nshimo (pers.
cancer comm.)
Hymenocardia mollis Pax (Euphorbiaceae) Root bark Colic, sterility in women, C. Nshimo (pers. comm.)
cancer
Maeruarendichii Gilg and Bened (Capparidaceae) Root Cancer C. Nshimo (pers. comm.)

a
C. Nshimo, personal communication, Department of Pharmacognosy, Faculty of Pharmacy of the Muhimbili University College
of Health Sciences, Dar es Salaam, Tanzania.

3. Results activity of the 38 plants that are commonly used


in Tanzanian traditional medicine to treat non-
In order to evaluate the cytotoxic effect of 47 cancer diseases.
plant extracts that are used in Tanzanian tradi- Of the plants used to treat cancer diseases
tional medicine, an antiproliferative assay with (Table 2), the Entanda abyssinica extract exhibited
three human cell lines (HeLa, HT29 and A431) a pronounced cytotoxic effect (B25% cell prolif-
was performed. Table 1 presents the list of the eration at 100 mg/ml) on the three cell lines. On
investigated plants, the parts used and their the other hand, Capparis sepiaris extract exhibited
known medicinal uses according to the Handbook the least cytotoxic effect (\ 75% cell prolifera-
of African Medicinal Plants (Iwu, 1993), Ethnob- tion) at both concentrations on the three cell lines.
otany Desk Reference (Johnson, 1999) and direct The results in Table 2 indicate that out of the nine
information obtained by Dr Charles Nshimo (De- plant extracts, two (22%), four (44%), two (22%)
partment of Pharmacognosy, Faculty of Phar- and one (11%) plant extracts exhibited a cytotoxic
macy, Muhimbili University College of Health activity on cell proliferation between 0 and 25%,
Sciences, Dar es Salaam, Tanzania) through inter- 25 and 50%, 50 and 75%, and 75 and 100% cell
viewing local traditional healers. Table 2 shows proliferation, respectively, in one or more of the
the cytotoxic activity of the nine plant extracts three cell lines tested. In the group of plants that
that are commonly used in the treatment of can- are used to treat cancer diseases, there was no
cer or cancer related illnesses in Tanzanian tradi- active (\50% cell proliferation) plant extract at
tional medicine. Table 3 shows the cytotoxic the 10 mg/ml concentration.
A. Kamuhabwa et al. / Journal of Ethnopharmacology 70 (2000) 143–149 147

Table 2
Cytotoxic activity of plant extracts (10 or 100 mg/ml in the three cell lines) that are used in the treatment of cancer or cancer related
illnesses in Tanzanian traditional medicinea

Plant species Cytotoxicity (cell proliferation as the % of control)

HeLa (mg/ml) HT29 (mg/ml) A431 (mg/ml)

100 10 100 10 100 10

Hymenocardia mollis − − + − + −
Bridelia micrantha − − − − + −
Cana6aria rosea − − − − ++ −
Capparis sepiaris − − − − − −
Oxygonium sinuatum − − ++ − ++ −
Entanda abyssinica +++ − +++ − +++ −
Gnidia kraussiana + − + − ++ +
Harissonia abyssinia ++ − +++ − +++ −
Maeruarendichii + − ++ − ++ −

a
−, indicates 100–75%, +, 75–50%, ++, 50–25% and +++, 25–0% cell proliferation vs. control. The results are the average
of three independent experiments with less than 10% standard deviations.

While 26 out of the 38 plant extracts that are has been one of the common useful ways for the
used to treat non-cancer diseases (Table 3) discovery of biologically active compounds from
exhibited a cytotoxic effect resulting in less than plants (Cordell et al., 1991; Cragg et al., 1994).
50% cell proliferation at least in one of the three The big advantage of the ethnopharmacological
cell lines tested, the remaining 12 plant extracts information is that the extensive literature may
exhibit either minimum or no cytotoxic effect already allow for some rationalization with
( \50% cell proliferation). Of the 26 plant respect to the biological potential of a reputed use
extracts that exhibited a cytotoxic effect resulting (Cordell et al., 1991).
in less than 50% cell proliferation, 14 (37%) plant In this study, methanolic extracts (supposed to
extracts exhibited at least a cytotoxic effect contain mainly polar compounds) were used.
between 0 and 25% cell proliferation in one or Traditional healers who were interviewed on how
more of the three cell lines tested. In this group of they prepare the extracts before administering to
plants that are used to treat non-cancer diseases, the patients indicated that it was the water
five plant extracts were active (B50% cell decoction that was administered, meaning that it
proliferation) at the 10 mg/ml concentration in one is the polar compounds that were responsible for
or more cell lines (Table 3). Overall, the A431 the reported anticancer activity.
cells were much more sensitive to the cytotoxic Since it is known that different cell lines might
effects of the extracts than the other cell lines. exhibit different sensitivities towards a cytotoxic
compound, the use of more than one cell line is
therefore considered necessary in the detection of
4. Discussion cytotoxic compounds. Bearing this in mind, three
human cell lines of different histological origin
The present study was undertaken to evaluate were used in the present study. As can be seen
the cytotoxic activity of some Tanzanian from Tables 2 and 3, cell type cytotoxic specificity
traditional medicines that are used in the treat- is observed in some plant extracts. Cell type
ment of cancer and cancer related illnesses in the cytotoxic specificity of plant extracts is likely to be
country. Ethnopharmacological data (information due to the presence of different classes of
based on the medicinal traditional use of plants) compounds in the extract, as it has been
148 A. Kamuhabwa et al. / Journal of Ethnopharmacology 70 (2000) 143–149

documented in the case of known classes of com- extracts from both groups (plants used to treat
pounds (Cragg et al., 1994). cancer and cancer related illnesses and those used
The results of the present study indicate the to treat other diseases). While 37% of the plants
presence of cytotoxic activity in some of the plant for non-cancer disease purposes showed pro-

Table 3
Cytotoxic activity of plant extracts (10 or 100 mg/ml in the three cell lines) that are commonly used to treat non-cancer diseases in
Tanzanian traditional medicinea

Plant species Cytotoxicity (cell proliferation as the % of control)

HeLa (mg/ml) HT29 (mg/ml) A431 (mg/ml)

100 10 100 10 100 10

Pterocarpus angolensis + − + − ++ −
Clerodendrum myricoides ++ − +++ − +++ −
Rhus natalensis − − + − ++ −
Acacia nilotica + − ++ − ++ −
Dombeya shupange ++ − + − ++ −
Parinari excelsa +++ − + − ++ −
Ximenia caffra +++ − ++ − ++ −
Salacia madagascariensis +++ − +++ − +++ ++
Cassia abbre6iata − − + − ++ −
Margaritaria discoidea − − + + ++ ++
Vangueria tomentosa + − − − ++ −
Markhamia hildebrandtii − − − − ++ −
U6aria lucida ++ + +++ − ++ ++
U6aria acuminata +++ ++ +++ + +++ −
U6aria leptocladon +++ − +++ − +++ −
Annickia kummeriae ++ − +++ + +++ +
Ocotea usambarensis +++ − ++ − +++ −
Zanthoxylum chalybeum ++ + ++ − ++ ++
Pteleopsis myrtifolia + − +++ − +++ −
Cassia didymobotrya + − ++ − ++ −
Fluggea 6irosa + − +++ − +++ −
Thylachium africanum − − ++ − +++ −
Crinum papillosum +++ − +++ − ++ −
Gloriosa superba ++ +++ +++ ++ +++ +++
Markhamia obtusifolia − − − − ++ −
Paullinia pinnata ++ + − − + −
Acacia polyacantha − − − − − −
Minopsis fraticosa − − − − − −
Dichrostachys cinerea − − − − − −
Ziziphus mucronata + − + − + −
Opilia celtidifolia + − − − + −
Keetia zanzibarica − − − − − −
Bauhinia thoningii + − + − − −
Kigelia africanum − − − − − −
Strychnos innocua − − − − − −
Harungana madagascariensis − − − − + −
Euphorbia quandrangularis − − − − − −
Lannea stuhlmanii + − − − + −

a
−, indicates 100–75%, +, 75–50%, ++, 50–25% and +++, 25–0% cell proliferation vs. control. The results are the average
of three independent experiments with less than 10% standard deviations.
A. Kamuhabwa et al. / Journal of Ethnopharmacology 70 (2000) 143–149 149

nounced activity ( B 25% cell proliferation), only study but were not yet investigated by other
22% of the plants for cancer diseases exhibited the workers will therefore be evaluated further for the
same activity at the 100 mg/ml concentration. Due possible isolation of active antitumor compounds.
to the fact that there were only few active plant
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