Journal of Ethnopharmacology 69 (2000) 139155

The search for natural bioactive compounds through a

multidisciplinary approach in Bolivia. Part II. Antimalarial
activity of some plants used by Mosetene indians
V. Mun oz
a
, M. Sauvain
b
, G. Bourdy
b
, J. Callapa
a
, I. Rojas
a
, L. Vargas
c
,
A. Tae
d
, E. Deharo
b,
*
a
Instituto Boli6iano de Biologia Andina (IBBA), Casilla 641, La Paz, Boli6ia
b
Institut de Recherche pour le De6eloppement (IRD), CP 9214, La Paz, Boli6ia
c
Herbario Nacional de Boli6ia, Campus Uni6ersitario, Calle 27 Cota-Cota, Casilla 303, La Paz, Boli6ia
d
Muchanes, Pro6incia Sur Yungas, Departamento del Beni, Boli6ia
Received 24 August 1998; received in revised form 17 May 1999; accepted 24 May 1999
Abstract
Forty-six different species collected in the Mosetene ethnia, dwelling in the Andean Piedmont of Bolivia, were
screened for antimalarial properties. Thirty-three extracts were screened for antimalarial activity in vitro on
Plasmodium falciparum chloroquine resistant strain (Indo), and forty-seven extracts were evaluated in vivo on the
rodent malaria P. 6inckei petteri 279BY. Only two plants are specically used in combination by the Mosetene against
malaria attack (Hymenachne donacifolia and Tesseria integrifolia), but they did not display any activity in vivo at 1000
mg/kg. The in vivo most active extracts were Swietenia macrophylla bark, Trema micrantha bark and Triplaris
americana bark, not all of them were used for antimalarial purposes by the Mosetene. The following extracts were
moderately active: Jacaratia digitata inner bark and Momordica charantia aerial part (both traditionally used as
febrifuge), Kalanchoe pinnate aerial part (used in inammatory processes), Lunania par6iora twigs and leaves,
Phyllanthus acuminatus (used as piscicide), Tynanthus schumannianus fruit (used against diarrhoea), Triumfetta
semitrilobata (used as febrifuge, to alleviate kidney and gynecological pain) and nally Solanum mammosum fruit
(used against scabies). We present here the results of this screening, emphazing on the in vivo antimalarial activity of
the selected plants. The antimalarial in vivo activity of the selected species, in relation with their traditional Mosetene
use is then discussed. 2000 Published by Elsevier Science Ireland Ltd. All rights reserved.
Keywords: Plasmodium; Antimalarial agents; Traditional medicine; Bolivia; Mosetene
www.elsevier.com/locate/jethpharm
1. Introduction
In the departments of Pando, Beni and part of
Santa Cruz situated in the Amazonian area of
Bolivia, all the characteristic for a high level of
* Corresponding author. Fax: +591-2-225846.
E-mail address: plantibba@megalink.com (E. Deharo)
0378-8741/00/$ - see front matter 2000 Published by Elsevier Science Ireland Ltd. All rights reserved.
PII: S0378- 8741( 99) 00096- 3
V. Munoz et al. / Journal of Ethnopharmacology 69 (2000) 139155 140
malaria transmission are present all year long, i.e.
a vector (Anopheles darlingi ), temperature, hu-
midity, rain, poverty, lack of basic hygiene facili-
ties and continuous migration. This plague
threatens 55% of the whole Bolivian population
and more than 45 000 cases were recently reported
(Ministerio de Desarrollo Humano, 1996). With
the purpose of nding new therapeutical alterna-
tives we studied the antimalarial potential of
plants traditionally used by the Mosetene (Vargas
Ramirez and Quintana Pen andra, 1995), a tribe
living in the north of Beni, in the Andean Pied-
mont (Department of La Paz, province of South
Yungas).
This study is a continuation of previously detailed
investigations performed in the Chacobo ethnia
(Mun oz et al., 1999).
Thirty-four extracts of plants were evaluated in
vitro on chloroquine resistant Plasmodium falci -
parum strains (Indo) and 47 extracts were tested
in the in vivo model on the rodent malaria Plas-
modium 6inckei petteri.
2. Materials and methods
The methodologies employed for the ethnob-
otanical survey, the vegetal samples treatment, the
biological tests and the phytochemical investiga-
tion are given in full details in a previous paper
(Mun oz et al., 1999).
We considered the following range of anti-
malarial activities in vitro:
% growth inhibition at 10 mg/ml: around
90%=excellent, around 50%=very good
% growth inhibition at 100 mg/ml: around
90%=good, around 50%=weak
In vitro assay standard drugs (data not
shown): at 0.4 mg/ml, the inhibition of Cinchona
calisaya stem bark extract was 100%, and the
Chloroquine displayed 100% inhibition at 148
ng/ml.
The in vivo results were classied as follows:
at the dose of 1000 mg/kg/day, when the
percent growth inhibition was higher than
50% the activity was considered moderate, in
other cases it was considered inactive. This
dose was taken into account to detect an active
product presented in small amount in the ex-
tract
at the dose of 500 mg/kg/day, if the extract
displayed a percent growth inhibition equal or
greater than 50%, the antimalarial activity was
also considered moderate
at the dose of 250 mg/kg/day, if the percent
growth inhibition was equal or greater than
50%, the antimalarial activity was considered
good
at the dose of 100 mg/kg/day if the per-
cent growth inhibition was equal to 50%,
the antimalarial activity was considered very
good.
In vivo assay standard drugs (data not shown):
the Cinchona calisaya bark extract, used as a
positive standard for these assays, displayed 91%
of inhibition at 250 mg/kg/day, while 5 mg/kg/day
of chloroquine inhibited 100% of the parasite
growth.
V. Munoz et al. / Journal of Ethnopharmacology 69 (2000) 139155 141
3. Selection of plants
Amongst the 150 different species indicated by
the Mosetene to cure different illness and/or as
useful, we decided to study 46 species.
We selected the species on the basis of their
traditional indications, and in case of medicinal
plants their way of administration: a higher prior-
ity was given to plants used internally above
plants applied externally.
Amongst the species mentioned by the
Mosetene, we retained species specically used
against malaria, species used to cure symptoms
with a possible relevance to a malaria attack, like
fever and digestive troubles, species used to cure
or alleviate symptoms with a relation with para-
sitic diseases i.e. leishmaniasis, scabies, species
that possibly have an effect on the immune sys-
tem, i.e. species used against inammation, and
species used against cutaneous affection. Anyway,
most of the selected species had a traditional
medicinal use not related with malaria. Finally a
few species with no claimed medicinal uses were
also selected. The species retained for biological
investigation are listed in Table 1.
4. Results and discussion
In order to highlight the potential antimalarial
activity of the species, we sorted our in vitro
results with the in vivo results, which are more
closely related with human physiological re-
sponses. Nevertheless, a good in vitro antimalarial
activity is also required for bioactivity-guided
fractionating, because the amount of drug ob-
tained is generally too low to perform direct in
vivo assays. Results are displayed in Table 2.
4.1. Species displaying a good acti6ity in 6i6o
Swietenia macrophylla bark extract displayed a
good activity in vivo (73% inhibition at 250 mg/
kg) and in vitro (78% inhibition at 100 mg/ml).
The use of bark by the Mosetene ethnia as a
dying agent was a hint to select this species,
because Vennerstom et al. (1995) and Atamna et
al. (1996) have shown the strong correlation be-
tween the dying properties of species and their
antimalarial activity. The genus Swietenia is
widely used for various purposes. Amongst them,
a decoction of seeds of S. macrophylla is reported
as an antimalarial remedy in Indonesia (Kadota et
al., 1990). The antimalarial activity of a S.
macrophylla methanolic seed extract was evidenci-
ated against P. falciparum (Soediro et al., 1990).
Nevertheless, it should be pointed out that the
seeds of this species are also reported to induce
uterine haemorrhage, eventually leading to death
(Bourdy, 1999), the same effect being described
for S. mahagony bark (Eldridge, 1975), thus mak-
ing its use dangerous. Considering this batch of
informations, we suggest that prior to any further
antimalarial investigation the possible toxicity of
S. macrophylla bark should be assessed, and it
should be determined if the antimalarial com-
pounds do not possess any toxic side-effect.
Trema micrantha stem bark was weakly active
in vitro (62% at 100 mg/ml), but displayed a very
good activity in vivo (81% inhibition at 100 mg/
kg). De Lucca and Zalles (1992) reported that
infusion of leaves is traditionally used in Bolivia
as antispasmodic while the bark is effective
against diarrhoea. In the West Indies, a decoction
made out from dried bark and leaves is used in
the form of a bath against skin eruption, and the
fresh sap is applied directly on aphtous ulcers
(Esposito-Avella et al., 1985). The biological eval-
uation of a leaf ethanolic and petrol ether extract,
administered by intragastric route at 500 mg/kg,
evidenciated analgesic activity, as well as an anti-
inammatory activity in the same experimental
conditions, at 1000 mg/kg (Barbera et al., 1992).
Triplaris americana bark extract displayed a
good activity in vivo (93% inhibition at 350 mg/
kg) and in vitro (83% inhibition at 100 mg/ml).
The bark of Triplaris americana is traditionally
used in Peru as a cure-all but was shown to be
inactive in an in vitro antitumor evaluation (Des-
marchelier et al., 1996). In the Mosetene nearby,
Tacana ethnia, the bark of this common species is
also used to cure a variety of ailments, such as
intestinal parasites, diarrhoea and leishmaniasis
(Bourdy, 1999).
V. Munoz et al. / Journal of Ethnopharmacology 69 (2000) 139155 142
Table 1
Traditional uses of Mosetene species selected for antimalarial investigation
Species, family Preparation, posology Traditional Mosetene use
Mosetene vernacular name (Vargas Ramirez et al., (Vargas Ramirez et al.,
1995) Voucher number 1995)
Dysentery, cough, intestinal The stem bark is boiled, in Anadenanthera macrocarpa
(Benth.) Brenan parasites, fever, and aphtas. order to obtain a decoction.
Mimosaceae This decoction is ingested. In
cases of aphtas, it is applied Bat n
LV1225 locally.
Diarrhoea A tea is made from the leaves Arrabidaea sp.
Bignoniaceae and is drunk. For small
Idytze children, leaves are squeezed
and the juice is mixed with LV1285
maternal milk and
administered.
Cana6alia beniensis Pieces of stem and leaves are Diarrhoea
boiled for a while in water. Aymard & Cuello
This preparation is ingested. Papilionaceae
Waje
LV1300
Cestrum sp. Leaves are crushed, mixed Bruises
with urine and applied in Solanaceae
form of a poultice on the Coh-cohs
GQP55 affected area.
(1) The leaves, together with the (1) Bites of insects or bites Chamaedorea angustisecta
of worms owers are mashed, in Burret
order to obtain a paste, which (2) Cicatrization of wounds Arecaceae
Ijtapahshi is applied on the skin.
GQP63 (2) Some leaves and pieces of
the trunk are mashed together
and applied in the form of a
poultice.
Eleutherine citriodora Rav. (1) The entire plant is (1) Vaginal discharge
Iridaceae (1) Homeostatic (wounds) boiled, and the preparation is
applied locally. Yuya (2) Dysentery
(2) The juice of the crushed LV1265 (2) Anaemia
bulb is drunk.
The latex is mixed with Intestinal parasites Ficus insipida Willd.
Moraceae water, the proportion upon
the age of the patient. Then Bihkj
LV1254 this preparation is drunk at
once. It is not recommended to
eat any salted or greasy food
the day of the treatment.
V. Munoz et al. / Journal of Ethnopharmacology 69 (2000) 139155 143
Table 1 (Continued)
Traditional Mosetene use Species, family Preparation, posology
(Vargas Ramirez et al., Mosetene vernacular name (Vargas Ramirez et al.,
Voucher number 1995) 1995)
(1) Skin rash, scabies Gallesia integrifolia (1) Mashed leaves and
(2) Cough crushed bark are mixed with (Sprengel) Harms
(2) Vaginal discharge some water. The patient has to Phytolaccaceae
Shepiji (2) Irregular period bathe daily in this
preparation. LV1213 (2) Anaemia
(3) Stomach ache (2) The bark is boiled, then
the decoction is drunk.
(3) A tea is prepared witn the
leaves, and drunk.
All parts of plant can be Kidney pain Guarea guidonia (L.) Sleumer
Meliaceae Anaemia prepared in the form of a tea,
Yellow skin (hepatitis?) which is drunk. Oroson
GQP96 To induce abortion
The crushed bark is mixed Guettarda acreana (Krause) Scabies
with some water in order to Rubiaceae
Cotosi obtain a paste which is
LV1206 applied on the skin.
Gynerium sagittatum The soft pith of this giant Intestinal parasites
herb is prepared in the form (Aublet) Beauv. dysentery, diarrhoea
of a tea, or is squeezed with Poaceae
Shru water in order to obtain some
juice which is drunk. LV1256
(1) To facilitate birth Heliocarpus americanus L. (1) The bark is prepared in
form of a strong decoction, (2) Wounds Tiliaceae
Pahatshira which is ingested during child (3) Fever
birth. LV1267
(2) The leaves are mashed
with some fat then applied on
the wound.
(3) The leaves are mashed,
then applied in form of a
poultice on feet, groin, and
temples.
(1) A few drops of latex are (1) Intestinal worms Hura crepitans L.
diluted in water and absorbed (2) Piscicide Euphorbiaceae
in order to get rid of Conojto
GQP123 intestinal worms. But this
remedy can be dangerous.
(2) A basket, containing sand
impregnated with the latex, is
thrown away in calm water
and acts as an ichtyotoxic. The
poisoned shes can present
some toxicity for the people
eating them.
Hymenachne donacifolia Beauv. The whole plant is boiled in Malaria
water, with the leaves of Poaceae
Tessaria integrifolia and Thocoy
LV1257 termites eggs. This
preparation must be drunk
while hot.
V. Munoz et al. / Journal of Ethnopharmacology 69 (2000) 139155 144
Table 1 (Continued)
Species, family Preparation, posology Traditional Mosetene use
(Vargas Ramirez et al., (Vargas Ramirez et al., Mosetene vernacular name
Voucher number 1995) 1995)
Febrifuge The rasped soft inner bark is Jacaralia digitata (Poeppig &
boiled in water. This Endl.) Solms-Laub
Caricaceae preparation is drunk by the
Ashamba dere kanthy patient, and also is
administered in form of a LV1239
bath.
The whole plant is prepared Inammation and pain in the Kalanchoe pinnata Pers.
in the form of a tea, which is stomach. Crassulaceae
Inammation and pain in the Chsadyesiji tyidyesi drunk.
GQP89 uterus.
Lunania par6iora (1) For medicinal purposes, (1) Diarrhoea and vomits
a tea is prepared with the Spruce ex Benth (2) Used as a coca substitute
twigs and leaves, which is Flacourtiaceae
drunk. Cahnason
GQP145 (2) The leaves are chewed in
the same way as coca.
Intestinal parasites Mikania sp. The aerial part of the plant is
prepared in form of a tea, Asteraceae
which is drunk. San
GQP128
Mirabilis jalapa L. The whole plant is boiled in Fever
order to prepare a bath, in Nycktaginaceae
Orinaj which the patient submerges
himself. GPQ127
Fever The whole plant is boiled in Momordica charantia L.
water. Some small cups are Cucurbitaceae
Achocchi drunk, and the rest of the
preparation is administered LV1260
in form of a bath.
Ocimum micranthum Willd. (1) The raw leaves are eaten. (1) Stomach ache
(2) A handful of leaves is (2) Fever Lamiaceae
boiled in a big amount of Irepij
GQP30 water, and this preparation is
administered in the form of a
bath.
Pera benensis Rusby Crushed stem bark and Leishmaniasis
mashed leaves are mixed Euphorbiaceae
Apainichij together in order to obtain a
GQP133 paste, which is applied in the
form of a poultice on the
affected area.
(1) Fever in small children (1) The whole plant is boiled, Peti6eria alliaceae L.
Phytolaccaceae (2) Colds and the child must bathe in
the resulting preparation. (3) Diarrhoea Ere
LV1233 (2) A steam vapor is made out (3) Stomach-ache
of the plant. The vapour is (3) Teeth ache
inhaled.
(3) A tea is prepared with the
leaves, and is drunk.
V. Munoz et al. / Journal of Ethnopharmacology 69 (2000) 139155 145
Table 1 (Continued)
Traditional Mosetene use Species, family Preparation, posology
(Vargas Ramirez et al., Mosetene vernacular name (Vargas Ramirez et al.,
Voucher number 1995) 1995)
(1) Wounds, fungal infection Philodendron cf. megalophylum (1) The sap of the petioles is
of the skin, furunculosis applied on the affected area. Schott.
(2) Conjunctivitis (2) Some juice drop of the Araceae
Coyoj (3) Hair cosmetic crushed stem is instilled in
GQP157 the eye.
(3) The whole plant is boiled
in water. This water has to be
applied regularly on the
scalp.
Piscicide Leaves are crushed and Phyllantus acuminatus Vahl.
thrown away in calm water. It Euphorbiaceae
Qijtsij is said to be a powerful
ichtyotoxic. GQP7
Fever Phytolacca ri6inoides The whole plant is boiled in
water. Then the patient must Kunth and Bsache
Phytolaccaceae bathe in it.
Munhina
LV1245
Picramnia sellowii Hook. (1) Wounds and infected (1) Leaves are mashed with
some water, and the resulting pimps Simaroubaceae
preparation is applied on the Itsij (2) Used as a blue-violet dye
for cotton threads GQP107 skin.
(2) Leaves and fruits are
mashed with water. The
thread is left in this water
overnight, with lime juice, in
order to x the colour.
Furunculosis, wounds, and The whole plant is crushed, Piper peltatum L.
and applied in form of a skin ulcers Ulcers (eventually Piperaceae
Iwaj iwaj poultice on the affected area. related with leishmaniasis)
LV1229
Leishmaniasis The whole plant is mashed, in Polybautria caudata Kuntze
order to form a paste applied Dryopteridaceae
Yijyij as a poultice on the affected
area. GQP156
Used to improve dogs hunting Renealmia sp. The plant is crushed, mixed
with some water, and this ability Zingiberaceae
preparation is rubbed all Nhaca nhaca
GQP83 over the dogs body.
Pieces of trunk bark and Fever Rheedia gardneriana Pl. and Tr.
Guthferae leaves are boiled together.
Biwei This preparation is drunk.
GQP150
Fever Salix humboldtiana Willd. Few leaves and pieces of bark
of this tree are boiled Salicaceae Diarrhoea
together for a while. Then this Jibuin
preparation is administered LV1226
in the form of a bath, and also
is drunk by the patient.
V. Munoz et al. / Journal of Ethnopharmacology 69 (2000) 139155 146
Table 1 (Continued)
Species, family Preparation, posology Traditional Mosetene use
Mosetene vernacular name (Vargas Ramirez et al., (Vargas Ramirez et al.,
1995) Voucher number 1995)
(1) Stomach ache (1) The whole plant is Scoparia dulcis L.
Scrophulariaceae prepared in form of an (2) For the small children to
walk infusion, and drunk when Simih-simih
LV1223 thirsty.
(2) The plant is boiled in a
lot of water. The child must
bathe in this preparation.
The leaves are crushed and Piscicide Serjania deltoidea Radek
thrown away in small ponds of Sapindaceae
Waishi water.
GQP64
Sida rhombifolia L. (1) A decoction is prepared (1) Fever
with the whole plant. When Malvaceae (2) Diarrhoea
cold, it is administered in (3) Hair cosmetic Biehky
form of a bath. GQP115
(2) A tea is prepared with the
leaves, and is drunk.
(3) The whole plant is
crushed with the toasted seeds
of Attalea phalerata palm.
Then, some water is added to
the preparation, and this
paste is applied regularly on
the scalp.
Piscicide Socratea exorrhiza The adventitious roots are
crushed and set in a basket, (C. Martius) H.A. Wendl.
which is thrown in the calm Arecaceae
Wijri water of ponds.
LV1244
Solanum cf. americanum Fever The aerial part of the plant is
Miller boiled for a while in water.
When cold small cups of this Solanaceae
preparation are administered Chichipa
LV1266 to the patient.
The fruits are mashed and this Scabies, furunculosis, rashes Solanum mammosum L.
paste is rubbed over the Solanaceae
Torito affected area.
GQP132
Spondias 6enosa C. Martius Scabies, to get rid of the A wash is prepared with the
leaves, applied all over the Anacardiaceae Dermatobia larvae,
body or on the affected part of incrustated under the skin Moco
the skin. LV1258
V. Munoz et al. / Journal of Ethnopharmacology 69 (2000) 139155 147
Table 1 (Continued)
Traditional Mosetene use Preparation, posology Species, family
(Vargas Ramirez et al., (Vargas Ramirez et al., Mosetene vernacular name
Voucher number 1995) 1995)
(1) A decoction is prepared Swietenia macrophylla King (1) To induce abortion
Meliaceae with the crushed seeds, and is (2) To heal wounds and
drunk. Ityalmaj various ailments of the skin
(2) The crushed seeds are GQP104 (2) To alleviate skin allergy
in children mixed with Attalea phalerata
(3) To dye cotton threads in seed oil and applied in form of
a poultice on the skin. brown.
(3) The bark is boiled until
the water has a strong color.
The thread is then immersed
few hours in this bath.
Talinum triangulare Crushed leaves are applied on Furunculosis
the abscess, in order to (Jacq.) Willdenow
Portulaceae accelerate its maturation.
N0 u-nuy
LV1232
Tessaria integrifolia (1) Leaves of this species are (1) Malaria
boiled with Hymenachne Ruiz and Pav. (2) Stomach ache
(2) Diarrhoea Asteraceae donacifolia and some termites
Shita (2) Intestinal parasites eggs. This preparation must be
(3) Leishmaniasis drunk while hot. LV1255
(2) The leaves are boiled in
water in form of a tea, which
is drunk.
(3) Juice from the stem and
leaves is mixed with oil, then
applied on the skin.
Trema micrantha (L.) Blume (1) A decoction is made out of (1) Cough
Ulmaceae (2) Wounds the bark of this species, then
Dhotyo drunk.
GQP62 (2) The bark is crushed and
applied in from of a poultice
on the wounds.
(1) Leaves and bark of this Triplaris americana L. (1) Inammation of the
Polygonaceae species are boiled in water. throat
Tsij The resulting preparation is (1) Cough
(2) Measles, wounds drunk. GQP93
(2) The resulting
preparation is applied locally.
The leaves are prepared in the Fever Triumfetta semitrilobata
Kidney pain form of a tea, which is drunk Jacq. Tiliaceae
by the patient, when he is Patsine Gynecological pain
LV 1059 thirsty.
Pieces of stem and some fruits Diarrhoea Tynanthus schumannianus
(Kuntze) A. Gentry are boiled in water. This
Bignoniaceae preparation is drunk, as a tea.
Waje
LV1271
V. Munoz et al. / Journal of Ethnopharmacology 69 (2000) 139155 148
Table 2
Antimalarial activity of selected plants in vitro and in vivo
Family Part tested In vitro Scientic name In vivo Voucher num-
ber
Conc. mg/ml % inh.
a
Dosis mg.kg % inh.
per 4D
Mimosaceae Bark 10 LV1225 98 Anadenanthera 1000 Tox.
b
macrocarpa
Leaves Arrabidaea sp. 1000 Bignoniaceae 24 LV1285
Papilionaceae Cana6alia beniensis Stem and LV1300 1000 29
leaves
GQP55 Solanaceae Leaves 100 84 1000 Tox. Cestrum sp.
Arecaceae Leaves, stems 100 83 Chamaedorea angus- 1000 GQP63 44
tisecta
Entire plant 10 100 1000 0 LV1265 Eleutherine citriodora Iridaceae
Bark 10 99 Moraceae 793 Ficus insipida 26 LV1254
Phytolaccaceae Gallesia integrifolia Leaves 10 99 775 31 LV1213
Bark GQP96 1000 Guarea guidonia Tox. Meliaceae
Bark 100 99 Rubiaceae 1000 Guettarda acreana Tox. LV1206
Poaceae Gynerium sagittatum Stem 10 100 522 11 LV1256
LV1267 Tiliaceae Heliocarpus ameri - Leaves 10 99 1000 0
canus
Poaceae Entire plant 10 Hymenachne 99 LV1257 1000 0
donacifolia
GQP123 Euphorbiaceae Latex 854 26 Hura crepitans
LV1239 Caricaceae Bark 10 99 743 76 Jacaratia digitata
Entire plant Crassulaceae 1000 GQP89 63 Kalanchoe pinnata
Twigs and Lunania par6iora 10 85 880 GQP145 59 Flacourtiaceae
leaves
Aerial part Mikana sp. 765 Asteraceae 31 GQP128
GQP127 Nycktaginaceae Entire plant 10 94 1000 11 Mirabilis jalapa
Aerial plant 10 100 LV1260 904 Momordica charantia 70 Cucurbitaceae
Entire plant Lamiaceae 1000 Ocimum micranthum 37 GQP30
Euphorbiaceae Pera benensis Bark 1000 Tox. GQP133
Phytolaccaceae Peti6eria alliaceae Aerial part 10 90 1000 41 LV1233
Araceae Sap 10 57 GQP157 1000 Philodendron cf. 13
megalophylum
GQP7 Phyllanthus acumina- Euphorbiaceae Leaves 1000 52
tus
LV1245 Phytolaccaceae Aerial part 10 98 966 29 Phytolacca ri6inoides
Leaves Simaroubaceae 1000 GQP107 6 Picrammia sellowii
Aerial part 10 LV1229 97 Piper peltatum 854 47 Piperaceae
GQP156 Aerial part 10 73 Dryopteri- 812 Polybautria caudata 26
daceae
GQP83 Zingiberaceae Aerial part 1000 3 Renealmia sp.
Aerial part 10 77 GQP150 1000 Rheedia gardneriana 0 Guttiferae
Leaves 10 99 Salicaceae 1000 Salix humboldtiana 32 LV1226
Scrophulariacea Scoparia dulcis Aerial part 10 95 1000 0 LV1223
GQP64 Sapindaceae Aerial part 1000 44 Serjania deltoidea
Entire plant 10 54 Malvaceae 1000 GQP115 42 Sida rhombifolia
Arecaceae Socratea exorrhiza Roots 100 98 966 29 LV1244
LV1266 Solanum cf. ameri - Solanaceae Aerial part 10 100 931 9
canum
V. Munoz et al. / Journal of Ethnopharmacology 69 (2000) 139155 149
Table 2 (Continued)
Scientic name Family Part tested In vitro In vivo Voucher num-
ber
Conc. mg/ml % inh.
a
Dosis mg.kg % inh.
per 4D
Solanaceae Fruits 814 62 GQP132 Solanum mammosum
Anacardiaceae Leaves 10 Spondias 6enosa 99 LV1258 637 10
Swietenia macrophylla GQP104 Meliaceae Bark 100 78 250 73
Portulacaceae Leaves 10 LV1232 98 Talinum triangulare 701 0
Asteraceae Leaves 10 Tessaria integrifolia 100 LV1255 1000 16
Tessaria integrifolia GQP120 Asteraceae Roots 10 84 1000 66
Ulmaceae Bark GQP62 100 Trema micrantha 62 100 81
Polygonaceae Bark 100 Triplaris americana 83 GQP93 350 93
Triumfetta semitriloba LV1059 Tiliaceae Leaves 100 84 850 57
Tynanthus schumanni - Bignoniaceae Fruit 10 LV1271 98 510 49
anus
a
% inh., percentage of inhibition.
b
Tox, death of all animals.
4.2. Species displaying a moderate acti6ity in 6i6o
Jacaratia digitata inner bark extract inhibited
76% of the parasite development at 743 mg/kg on
P. 6inckei and 99% at 10 mg/ml in vitro. In the
Tacana ethnia, this species is also widely used as
remedy against high fever associated with urinary
disease (Bourdy, 1999) and the fresh roots of a
closely related species, Jacaratia corumbensis
Kuntze were also reported for the treatment of
stomach-ache, abdominal pain and vomits in
Paraguay (Arenas, 1987).
Kalanchoe pinnate entire plant extract presented
a moderate activity as it inhibited 63% of the
parasite growth at 1000 mg/kg in vivo. In a large
botanical survey, Esquimel et al. (1986) reported
that this plant was amongst the most frequently
used against dermatological diseases in Mexico.
Crassulaceous plants of the genus Kalanchoe are
popularly known in Brazil for their efcacy in
healing wounds. Noleto et al. (1992) showed that
the crude extract of Kalanchoe pinnate is effective
in reducing leishmanial lesion growth and that
this effect is accompanied by suppression of the
immune response. Also, mice infected with Leish-
mania amazonensis and orally treated with a
Kalanchoe pinnate leaf extract, showed a delayed
onset of the disease (Da Silva et al., 1995).
Lunania par6iora twig and leaf extract dis-
played a moderate antimalarial activity, as it in-
hibited 59% the growth of the parasite at 880
mg/kg, but an excellent activity in vitro (85% at
10 mg/ml).
Momordica charantia aerial part extract pre-
sented a moderate activity on P. 6inckei infected
mice (70% at 904 mg/kg), and an excellent anti-
malarial activity in vitro (99% of inhibition at 10
mg/ml). However, Amorim et al. (1991) showed
that oral administration of crude ethanolic ex-
tracts of M. charantia dried leaves was ineffective
in lowering the parasitaemias of Plasmodium
berghei -infected mice at 500 mg/kg. The dis-
crepancy observed with our results may be ex-
plained by the different route of administration
and the rodent malaria species used in our study.
M. charantia is also widely used in the Caribbean
traditional medicine for a wide range of symp-
toms such as cold, hypertension, diabetes, diges-
tive troubles, intestinal worms, malaria, anaemia,
fever, etc. A lot of scientic work was focused on
this plant on a chemical and biological point of
view. Some of the traditional properties claimed
were demonstrated but some were not (Ger-
mosen-Robineau, 1995), thus indicating that M.
charantia is a species with interesting biological
potential.
V. Munoz et al. / Journal of Ethnopharmacology 69 (2000) 139155 150
Phyllanthus acuminatus leaf extract displayed in
vivo 52% of inhibition at 1000 mg/kg. An aqueous
extract of dried branches was shown to be inactive
in anti-viral test (Unander et al., 1995), while
various root extracts showed interesting antitu-
moral potential (Pettit et al., 1982, 1984). If the
ethnanolic leaf extract from this species also
shows antitumor activities, the hypothesis of a
correlation between the antimalarial activity ob-
served and the possible antitumoral activity could
be explained by the similarity in rapid replication
cycle of Plasmodium and cancer cells (Pouvelle et
al., 1994).
Solanum mammosum fruit extract presented a
moderate activity in vivo inhibiting the develop-
ment of the parasite by 62% at 814 mg/kg. The
traditional Mosetene use of this plant (against
skin affection) is also quoted in some Peru tribes
(Lacaze and Alexiades, 1995). Alzerreca et al.
(1981) demonstrated that a S. mammosum fruit
methanolic crude extract showed a good mollusci-
cidal activity on Lymnaea cubensis snails.
Triumfetta semitrilobata leaf extract displayed a
moderate activity in vivo (57% at 850 mg/kg) and
a good one in vitro (84% at 100 mg/ml). The leaves
of this species are also quoted by Dominguez and
Alcorn (1985) as used by the Huastec Mayans of
northeastern Mexico for relieving gastrointestinal
pain, the roots for fever, cough, gynecological
purpose, as well as for kidney pain. Both last
indications are similar to the Mosetene uses,
though the part of plant employed by the
Mosetene is different (leaves, instead of roots).
Tynanthus schumannianus fruit extract presented
a moderate activity in vivo (49% at 510 mg/kg)
and an excellent activity in vitro (98% at 10
mg/ml), while the leaf did not (data not shown). In
the vicinous Tacana community, the juice
squeezed out from the inner part of fruits of this
species is used against conjunctivitis (Bourdy,
1999).
In short, all these plants above mentioned merit
to be investigated further.
4.3. Species displaying a weak acti6ity in 6i6o
Chamaedorea angustisecta bark and leaf extract
were weakly active with 44% of inhibition at 1000
mg/kg in vivo and active in vitro (83% at 100
mg/ml). Leaves of Chamaedorea angustisecta are
also used in nearby amazonian Bolivian Tacana
ethnia to alleviate stingray bites (Bourdy, 1999),
and Dominguez and Alcorn (1985) reported the
utilisation of Chamaedorea elegans afnis Mart.
by Huastec Mayans of Northeastern Mexico for
rabid dog bites.
Ficus insipida bark extract had an excellent
activity in vitro (99% inhibition at 10 mg/ml),
but as it showed weak activity against P. 6inckei in
vivo (26% at 743 mg/kg), we did not continue
with further antimalarial investigations. It should
be pointed out that this species is widely used
in Amazonia as anthelmintic because of its
high latex cin contents (Bourdy, 1999; Schultes,
1969), therefore, justifying the Mosetene use
against intestinal parasites. The enzymolytic activ-
ity of the cin and its derivatives possibly
could explain the antimalarial activity observed in
vitro.
The in vitro antimalarial activity of Gallesia
integrifolia leaf extract was excellent (99% at 10
mg/ml), but the in vivo activity was weak (31% of
inhibition at 775 mg/kg). Gallesia integrifolia is
one of this species, which, despite its high
reputation in the Bolivian Amazonia, already
mentioned in Cardu s (1886), has received little
attention from the scientists. In Bolivia this
species is widely used in the fabrication of soap
with antiscabies properties, and the strong
garlic scented bark is used in form of a decoction
against intestinal worms, to alleviate related
symptoms as diarrhoea and stomach-ache
(Bourdy, 1999). Therefore the biological activity
of this species seems to be much more oriented
towards nematicidal properties, not justifying
further antimalarial investigations. The com-
pound(s) responsible for the claimed nematicidal
activity and antiscabies properties still need to be
isolated.
Hura crepitans latex extract was weakly active
against Plasmodium in vivo (26% at 854 mg/kg).
The antiprotozoal and anti-viral activities of Hura
crepitans were extensively studied with no positive
results (Fournet et al., 1994; Van den Berghe,
1984). Moreover, the latex of this species is well
V. Munoz et al. / Journal of Ethnopharmacology 69 (2000) 139155 151
known to have caustic properties that even
can cause blindness if accidentally introduced in
the eye (Bourdy, 1999; Germosen-Robineau,
1995).
Ocimum micranthum entire plant extract was
weakly active against P. 6inckei (37% inhibition at
1000 mg/kg). It was shown (Godhwani et al.,
1987) that a methanol extract and an aqueous
suspension of Ocimum sanctum L. inhibited acute
as well as chronic inammation isolated rat liver
microsomes in vitro. Both the extract and suspen-
sion showed analgesic activity in mouse and re-
duced typhoidparatyphoid A/B vaccine-induced
pyrexia. That could explain the Mostene use of O.
micranthum against stomach ache if O. mi -
cranthum contains similar constituents, but this
needs to be conrmed. It should be also pointed
out that the traditional Mosetene use of this
species against fever, in form of a bath, is quite
common in Bolivia and Peru (Bourdy, 1999; La-
caze and Alexiades, 1995) and it can be assumed
that this treatment is effective, at least because of
its physical effect.
Peti6eria alliaceae aerial part extract displayed
in our in vitro antimalarial model an excellent
activity (99% at 10 mg/ml) and a weak one in vivo
(41% at 1 g/kg). This plant is widely used in Latin
America for a large panel of indications. In Brazil
the entire plant is used as abortive, antispasmodic,
diuretic, antirheumatismal, against sexual trans-
mission of disease and as insecticide (Gupta,
1995). In Colombia it is used as febrifuge, anal-
gesic, antiseptic, etc. In Panama as aphrodisiac,
against snake bite, inammatory process etc. But,
most of all, it was claimed to have potent anti-
cancer properties (Gupta, 1995). Scientic studies
could not demonstrate this afrmation. Neverthe-
less, the plant can stimulate the phagocytosis ac-
tivity of the reticulo-endothelial system (Gupta,
1995). This observation is probably related to the
weak activity observed in vivo against P. 6inckei,
but this assertion still has to be proved.
Aerial part extract of Piper peltatum presented
a weak activity in vivo (47% inhibition at 854
mg/kg), but was active in vitro (97% at 10 mg/ml).
Flores et al., (1988) demonstrated that a Piper
peltatum leaf ethanolic extract was ineffective in
lowering the parasitemia levels of Plasmodium
berghei -infected mice treated either orally (500
mg/kg) or subcutaneously (20, 100 and 500 mg/
kg). The discrepancy observed between the results
of Flores and ours could be explained by the
higher sensitivity of P. 6inckei compared to P.
berghei.
Serjania deltoidea aerial part extract inhibited
44% of the parasite growth at 1000 mg/kg. In a
previous paper (Mun oz et al., 1999) we reported
the activity of Serjania sp. collected in the
Chacobo community. The stem bark extract of
Serjania sp. was very moderately active in vivo on
P. 6inckei. at 1 g/kg (100%) and showed a rather
good activity (47%) on P. berghei at 250 mg/kg.
Moretti and Grenand (1982) reported the use of
Serjania species as ichtyotoxic in French Guyana
and associated their toxicity with the presence of
saponines responsible for respiratory troubles in
sh. This particular species, S. deltoidea does not
appear to be very interesting, but apparently the
genus Serjania might contain other species worth-
while of antimalarial investigations.
Salix humboldtiana leaf extract was weakly ac-
tive in vivo against P. 6inckei (32% at 1000 mg/
kg), while in vitro, it displayed an excellent
activity (99% inhibition at 10 mg/ml). Decoction
of Salix chilensis Molina and S. martiniana Ley-
bold barks are also used in Bolivia to cure diges-
tive troubles and administered against malaria. A
bark alcoholic maceration of theses species is also
used against rheumatisms as a rub on painful area
(De Lucca and Zalles, 1992). In Chile and Peru,
S. humboldtiana is also used as febrifuge and
against rheumatisms (Gupta, 1995, and Lacaze
and Alexiades, 1995). The well-known salicylate
derivatives responsible for the febrifuge and an-
tirheumatismal activity contained in the genus
Salix justify the traditional uses of this species,
but the poor activity displayed in our model does
not justify further antimalarial investigation.
Sida rhombifolia entire plant extract was weakly
active in vivo (42% at 1g/kg) but very active in
vitro (54% at 10 mg/ml). Sida rhombifolia is a
plant also used for a great variety of ailments, all
over South America and also all over the tropical
zone (Watt and Breyer-Brandwijk, 1962). Re-
cently, a work done by the Gupta (1995) related
its Honduran traditional use against diarrhoea by
V. Munoz et al. / Journal of Ethnopharmacology 69 (2000) 139155 152
evidenciating its antibacterial properties, therefore
corroborating one of the traditional Mosetene
uses of this species.
All these plants exhibit weak antimalarial activ-
ity, and are therefore not recommended for fur-
ther studies.
4.4. Species inacti6e in 6i6o but of traditional
interest
Scoparia dulcis aerial part extract was totally
inactive in vivo but reduced by 95% the Plasmod-
ium growth in vitro at 10 mg/ml. This plant is
widely use in Latin America as febrifuge (Lacaze
and Alexiades, 1995; Gupta, 1995), and was also
proposed in Colombia as antimalarial (Gupta,
1995). Because the strong traditional reputation
of this species, we think another effort should be
made to investigate the possible antimalarial ac-
tivity of S. dulcis, using the oral route, in order to
possibly highlight the activity of a compound
modied by digestive degradation.
Solanum cf. americanum aerial part extract was
very active in vitro (100% inhibition at 10 mg/ml)
but inactive in vivo. In Guatemala, a decoction of
leaves is used to make vaginal shower for abnor-
mal vaginal secretions while in Martinica, the
infusion is taken orally as an anti-inammatory.
The antimicrobial and antifungal activity was
conrmed in vitro against a panel of strains (Ger-
mosen-Robineau, 1995). As the in vivo antimalar-
ial activity of the species tested here was very low,
the claimed Mosetene reputation against fever
might be due to its antimicrobial activity, but this
still has to be conrmed.
Talinum triangulare leaf extract was inactive in
vivo but presented an excellent activity in vitro
(98% at 10 mg/ml). Talinum paniculatum (Jacq.)
Gaertn. was also reported for anti-inammatory
properties (de Lucca and Zalles, 1992). This spe-
cies does not present interesting antimalarial ac-
tivity in vivo but it should be interesting to try to
evidenciate a possible anti-inammatory activity.
Tessaria integrifolia leaf extract displayed an
excellent activity in vitro (100% inhibition at 10
mg/ml) but was inactive in vivo at 1000 mg/kg,
while the root extract presented a moderate activ-
ity in vivo (66% inhibition at 1000 mg/kg) and
excellent in vitro (84% at 10 mg/ml). It is impor-
tant to point out that the leaves of this species are
also valued by other amazonian tribes as an effec-
tiven antimalarial remedy (Lacaze and Alexiades,
1995). T. integrifolia leaves are also reported by
Peluso et al. (1995) to be traditionally used as
anti-inammatory properties. These authors
conrmed their in vitro activity on monocyte
migration and superoxide anion production. The
anti-inammatory properties of the leaves might
be correlated with a possible febrifuge activity,
therefore explaining the traditional Mosetene use
against malaria. Nevertheless the antimalarial
study of this species should focus on with the root
extract.
5. Conclusion
Of the 46 species tested for antimalarial investi-
gation, three species displayed a good activity in
vivo, eight a moderate activity resulting in 11
species displaying an interesting activity. Amongst
these extracts, one is reported to be toxic (Swiete-
nia macrophylla). Therefore, it is worthwhile ex-
amining ten species further.
The other species displayed a weak activity or
were totally inactive. Plants specically mentioned
by the Mosetene as useful against malaria belong
to these species, Tesseria integrifolia being also
prized by other amazonian tribes (Lacaze and
Alexiades, 1995). Nevertheless, only the roots of
this plant, though not used by the Mosetene,
presented in vivo activity, and we suggest to make
more investigation on this extract. Also, it might
be fruitful to prepare a similar extract to the one
used by the Mosetene, boiling the whole plant of
Hymenachane donacifolia with the leaves of Tes-
saria integrifolia, together with some termite eggs,
and evaluating its potential activity using the oral
route.
Six species were toxic at the dose tested (1000
mg/kg). We suggested that the dose has to be
lowered, especially for Anadenanthera macrocarpa,
and Spondias 6enosa, both species displaying a
good in vitro activity, and also, because in the
case of A. macrocarpa, its traditional Mosetene
indication (against fever, dysentery, diarrhoea,
V. Munoz et al. / Journal of Ethnopharmacology 69 (2000) 139155 153
taken internally) is very much related with a
possible antiprotozoal activity. After a close re-
view of the literature, it appears that one of these
species, Guarea guidonia (bark), does not warrant
further investigation.
Both plants used by the Mosetene against prob-
lems, related to an inammatory process and
ingested internally (Kalanchoe pinnate and
Triplaris americana) displayed, respectively, a
moderate and good antimalarial activity.
All plants used internally by the Mosetene
against stomach ache (Ocimum micranthum,
Gallesia integrifolia, Peti6eria alliaceae, Scoparia
dulcis) were found to be inactive, as well as plants
used against intestinal parasites (Ficus insipida,
Mikania sp., Hura crepitans), the latest pre-
senting toxicity. The same remark can be formu-
lated for the febrifugal species used in form of a
bath (Heliocarpus americanus, Mirabilis jalapa,
and Phytolacca ri6inoides), all of them being inac-
tive.
Amongst the species used internally to alleviate
fever, three of them displayed a moderate anti-
malarial activity (Jacaratia digitata, Momordica
charantia, Triumfetta semitrilobata), the rest being
inactive (Salix humboldtiana, Rheedia gardneriana,
and Solanum cf. americanum).
All species used against parasitically caused dis-
eases (as scabies or leishmaniasis) are employed
topically by the Mosetene, and all were found
inactive or toxic in vivo (Guettarda acreana,
Pera benensis, Philodendron cf. megalophylum,
Polybautria caudata, Spondias 6enosa), except
Solanum mammosum fruits, displaying a moderate
activity. On the whole of species used by the
Mosetene to cure local infections, as in-
fected wounds, furunculosis, also applied as top-
ics, only one species displayed a very good an-
tiprotozoal activity (Trema micrantha), while
Chamacdorea angustisecta, Picramnia sellowlii,
Piper peltatum, and Talinum triangulare were to-
tally inactive.
We retained ve species with no traditional
Mosetene medicinal uses (ichtyotoxic), or with no
medicinal use related with a malaria attack. All of
them were proved to be totally inactive or weakly
active in vivo, one of them toxic, (Cestrum sp.,
Renealmia sp., Socratea exorrhiza, Serjania del -
toidea), with the exception of Phyllanthus acumi -
natus, which displayed a moderate activity.
Acknowledgements
The project was nanced by FONAMA-EIA
Fondo Nacional para el Medio Ambiente, Cuenta
Iniciativa para las Americas, Bolivia), IRD (Iin-
stitut de Recherche pour le Developpement,
France), UMSA (Universidad Mayor de San An-
dres, La Paz, Bolivia), IBBA (Instituto Boliviano
de Biologia Andina, La Paz, Bolivia), the Min-
istry of French Foreign Affairs, and
IFS (International Foundation for Sciences). The
authors wish to thank Dr B. Weniger for kindly
help in the bibliographical search, and Rosy
Chavez de Michel and the National Herbarium of
Bolivia for helping in the management and deter-
mination of vouchers. We express our thanks to
the members of the Mostene communities who
were willing to share with us their knowledge of
plants.
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