Journal of Ethnopharmacology 139 (2012) 155–163

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Journal of Ethnopharmacology

journa l homepage: www.elsevier.com/locate/jethpharm

Plants used as antidiabetics in popular medicine in Rio Grande do Sul, southern Brazil

a a a,b a,b,∗

M. Trojan-Rodrigues , T.L.S. Alves , G.L.G. Soares , M.R. Ritter

a

Pós-Graduac¸ ão em Botânica, Instituto de Biociências, Universidade Federal do Rio Grande do Sul. Av. Bento Gonc¸ alves 9500, Prédio 43433, Campus do Vale, 91501-970, Porto Alegre,

RS, Brazil

b

Depto. de Botânica, Instituto de Biociências, Universidade Federal do Rio Grande do Sul. Av. Bento Gonc¸ alves 9500, Prédio 43433, Campus do Vale, 91501-970, Porto Alegre, RS, Brazil

a r t i c l e i n f o a b s t r a c t

Article history: Ethnopharmacological relevance: are widely as antidiabetics. The study of these plants is essential

Received 27 July 2011

because many of them may have undesirable effects, such as acute or chronic toxicity; or their use may

Received in revised form 24 October 2011

even delay or discourage the adoption of the proper and effective treatment.

Accepted 26 October 2011

Materials and methods: The present study surveyed the that are popularly used to treat

Available online 2 November 2011

diabetes mellitus in the state of Rio Grande do Sul in southern Brazil. Sixteen ethnobotanical surveys

performed in the state were consulted, and the species used to treat diabetes were listed. For species

Keywords:

cited in at least two of the studies, scientific data related to antidiabetic activity were searched in the

Folk medicine

Ethnobotany ISI Knowledge database. The scientific binomial of each species was used as keywords, and data found in

review papers were also included.

Diabetes mellitus

South Brazil Results: A total of 81 species in 42 families were mentioned; the most important families were Aster-

aceae and Myrtaceae. Twenty eight species were cited at least twice as being used to treat diabetes in

the state. For 11 of these, no scientific data regarding antidiabetic activity could be located. The species

most frequently mentioned for use with diabetes were Syzygium cumini (Myrtaceae) and Bauhinia forfi-

cata (Fabaceae), in 12 studies each, followed by Sphagneticola trilobata (Asteraceae), in six studies; and

Baccharis trimera (Asteraceae), Bidens pilosa (Asteraceae), Cynara scolymus (Asteraceae), and Leandra aus-

tralis (Melastomataceae) in four studies each. Bauhinia forficata and Syzygium cumini have been studied

in more detail for antidiabetic activity.

Conclusions: A considerable number of plant species are traditionally used for the treatment of diabetes

melitus in the Rio Grande do Sul State. The majority of those plants that have been studied for antidiabetic

activity showed promising results, mainly for Bauhinia forficata and Syzygium cumini. However, for most

of the plants mentioned, the studies are not sufficient to guarantee the efficacy and safety in the use of

these plants in the treatment against diabetes.

© 2011 Elsevier Ireland Ltd. Open access under the Elsevier OA license.

1. Introduction WHO estimates that 30 million people had diabetes in 1985, and

this number increased to 171 million people in 2000. In that year,

Diabetes mellitus is a metabolic disease that currently affects an estimated 2.9 million people died of diabetes, representing 5.2%

250 million people around the world. Each year another 7 mil- of all deaths, probably the fifth largest cause of mortality in the

lion people develop the disease (International Diabetes Federation, world (Roglic et al., 2005). It is estimated that in 2030, people with

2011), resulting in a chronic state of hyperglycemia. The condi- diabetes will number 366 million, most of them from developing

tion is characterized by the body’s inability to transform sugar into countries, especially the among people from 45 to 64 years of age

energy, causing hyperglycemia. Hyperglycemia can cause retinopa- (Roglic, 2004).

thy, nephropathy, and cardiovascular damage (American Diabetes Marles and Farnsworth (1995) listed 1200 species of plants that

Association, 2007; Malviya et al., 2010). have been used to treat diabetes worldwide. They mostly belong to

the families Fabaceae, Asteraceae, and Lamiaceae.

Among the main natural hypoglycemic products are carbo-

hydrates, alkaloids, glycopeptides, terpenoids, flavonoids, and

Corresponding author at: Programa de Pós-Graduac¸ ão em Botânica, Instituto de

coumarins (Marles and Farnsworth, 1995; Negri, 2005; Cazarolli

Biociências, Universidade Federal do Rio Grande do Sul. Av. Bento Gonc¸ alves 9500,

et al., 2008).

Prédio 43433, Campus do Vale, 91501-970, Porto Alegre, RS, Brazil.

In Brazil, the use of plants as antidiabetics is very common, as

Tel.: +55 51 33087571.

E-mail address: [email protected] (M.R. Ritter). reported by Volpato et al. (2002), Barbosa-Filho et al. (2005), Negri

0378-8741 © 2011 Elsevier Ireland Ltd. Open access under the Elsevier OA license. doi:10.1016/j.jep.2011.10.034

156 M. Trojan-Rodrigues et al. / Journal of Ethnopharmacology 139 (2012) 155–163

(2005), and Borges et al. (2008). In Rio Grande do Sul, several eth- 3. Results and discussion

nobotanical studies established that the use of plants for metabolic

disorders such as diabetes is common (Simões et al., 1986; Ceolin, The ethnobotanical studies consulted mentioned 568 taxa with

2009). some medicinal usage, 84 of them used to treat diabetes. Among

According to Witters (2001), in the Middle Ages, Galega offic- these, only three were not identified to species level, and were

inalis L. (Fabaceae) was prescribed for polyuria, one of the most not counted in the final list. They are: Eucalyptus sp., Myrtaceae

common symptoms of diabetes. The active principle in Galega offici- (Marodin, 2000); Mentha sp., Lamiaceae (Marodin, 2000); and Ori-

nalis is known as guanidine. Although guanidine this and some of its ganum aff. vulgare, Lamiaceae (Soares et al., 2004). The species of

derivatives are overly toxic to treat diabetes, dimeric forms known these genera are admittedly difficult to delimit, in addition to the

as biguanides have been considered useful to treat the disease since occurrence of many hybrids.

the 1950s. The 81 species used for diabetes in the state of Rio Grande

About 66% of the Brazilian population has no access to com- do Sul (Table 1) are members of 42 botanical families. Species

mercial medicines, which means that the use of plants is their of the families Asteraceae and Myrtaceae were most often

only alternative for the treatment of their ills (Di Stasi, 2007). mentioned, comprising, respectively 29% and 15% of the occur-

In this context, ethnobotanical studies that have the main objec- rences. The relatively high number of species of the families

tive to catalogue knowledge about medicinal plants and cultural Asteraceae and Fabaceae agrees with the findings of Marles and

aspects of communities can serve as the basis to list species to Farnsworth (1995).

be studied as medicinal in order to validate the use, encour- These two families include species of great abundance and bio-

age the production of phytotherapeutics from these plants, or diversity in Brazil (Giulietti et al., 2005) and plants of these families

even the isolation and/or semi-synthesis of bioactive molecules also have a highly developed secondary metabolism. A considerable

(Elisabetsky and Coelho de Souza, 2007). The development of fraction of antidiabetic compounds belonging to species of these

medicines by the production of synthetic or semi-synthetic bioac- families have been described and tested for diabetes and its com-

tive molecules is based on the chemical diversity of plants plications (Marles and Farnsworth, 1995; Negri, 2005; Jung et al.,

(Phillipson, 2007). 2006). There is a predominance of species belonging to the “tannif-

This study surveyed the plant species mentioned for the treat- erous diagonal” which is a chemical group of families characterized

ment of diabetes in ethnobotanical surveys performed in Rio by the production of large amounts of tannins (commonly gallic

Grande do Sul, and evaluated the current status of scientific knowl- acid derivatives) and comprises the Cronquist‘s subclasses: Ham-

edge related to the antidiabetic activity of these plants. mamelidade, Dillenidae and Rosidae (Dahlgren, 1980; Kubitzki and

Gottlieb, 1984a). The species placed in this chemical group are

often woody and tend to contain shikimate derivatives (Kubitzki

2. Materials and methods

and Gottlieb, 1984b). These compounds are also of great impor-

tance regarding antidiabetic activity known so far, because of their

Sixteen ethnobotanical studies performed in Rio Grande do Sul

antioxidant properties (Negri, 2005). Several species of the fam-

were consulted: Simões et al. (1986); Kubo (1997); Garlet (2000);

ily Myrtaceae are rich in tannins, flavonoids, and other phenolic

Marodin (2000); Possamai (2000); Garlet and Irgang (2001); Ritter

derivatives. Among these classes, some compounds with antioxi-

et al. (2002); Hass (2003); Leitzke (2003); Martha (2003); Sebold

dant activity have been isolated.

(2003); Löwe (2004); Soares et al. (2004); Vendruscolo (2004);

The family Lamiaceae occupies a significant place in many eth-

Barbosa (2005); Vendruscolo and Mentz (2006); Barros et al.

nobotanical surveys, because of its aromatic characteristics and

(2007), and Ceolin (2009). The papers consist of articles, mas-

high phytochemical diversity, but did not have great significance

ter’s dissertations, and monographs contributed by researchers

in this study. Importantly, hypoglycemic activities attributed to

in the state, and were found in databases or in university

flavonoids in the leaves of Origanum majorana L. and phenolic com-

libraries.

pounds from the leaves of Hyssopus officinalis L. have been found

The plants used for the treatment of diabetes mentioned in these

(Jung et al., 2006).

studies were selected by searching for terms such as “diabete”, “dia-

The species most frequently mentioned for use with dia-

betes” and “lower the blood sugar”.

betes were Syzygium cumini (Myrtaceae) and Bauhinia forficata

The popular names mentioned for these species, as they are

(Fabaceae), in 12 studies each, followed by Sphagneticola trilobata

given in the studies consulted, were compiled. For better under-

(Asteraceae), in six studies; and Baccharis trimera (Asteraceae),

standing, the information concerning the plant parts used in

Bidens pilosa (Asteraceae), Cynara scolymus (Asteraceae), and Lean-

preparations has been standardized. Terms related to preparation

dra australis (Melastomataceae) in four studies each.

form such as infusion and decoction have been standardized as

The monocots, although their metabolism has fewer secondary

“tea”, since these methods just differ in the extraction time and

metabolites, contain many polysaccharides, which also show hypo-

the temperature reached. The plants that were identified only

glycemic activity (Von Poser, 2007). In Saccharum officinarum, e.g.,

to are listed separately, and were not considered in fur-

the activity was found in the stems, where usually occurs the accu-

ther analyses. The valid names of the species and the authors

mulation of polysaccharides (Takahashi et al., 1985).

were confirmed using the databases Tropicos (2011) and The

The predominance of the use of teas agrees with the findings

Plant List (2011). However, it was decided to retain the names

of surveys for medical use in general. The use of tea has a strong

given to the species as Baccharis crispa, Baccharis trimera, Cynara

cultural appeal (Santayana et al., 2005). In the case of plants used for

scolymus and Eruca sativa because the new combinations are

diabetes, this is particularly important because the antioxidants are

not widely recognized currently yet. The botanical families were

commonly soluble in water. Furthermore, some reports described

updated based on the APG III classification system (Stevens,

a combination of plants such as compound teas, elixirs, and also

2011).

the use of the plant together with “chimarrão”, a drink made with

For species listed in two or more ethnobotanical studies, chem-

leaves of Ilex paraguariensis A. St. Hil., which is widely consumed in

ical data and data related to antidiabetic activity, found in studies

southern Brazil.

in the database ISI Web of Knowledge (2010) were searched. In the

Popular names such as “insulin” and “vegetal insulin” were

search for these data, the scientific binomial of the plant was used

repeatedly mentioned, for four species of two different families:

as the descriptor.

Aspilia montevidensis and Sphagneticola trilobata (Asteraceae); and

M. Trojan-Rodrigues et al. / Journal of Ethnopharmacology 139 (2012) 155–163 157 in

activity, 2004,

of

al.,

diabetes

al., The et

glucosides

); et

butanol to

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decreased simulation ethyl

antidiabetic leaves Chang 2002

( ) );

hyperglycemia showed

of by

from 2009

achyrofuran

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the Oliveira

(

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found found found found attributed Th1-mediated

parts

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origin,

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158 M. Trojan-Rodrigues et al. / Journal of Ethnopharmacology 139 (2012) 155–163 oil al.,

of

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) effect

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of );

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animals al.,

were

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et );

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Cazarolli

metformin-like (

kaempferol-3-neohesperidoside

2006 studies diabetic

);

and

Volpato al., on ( related

insulin

2008 et

related

) al., like activity

effect

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et activity activity

(

to 2009

effect

diabetic

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leaves

anti

Cechinel, Antioxidant – – Antidiabetic – – – – – – – – – – – – – No Hypoglycemic attributed mimetic – – – 2009; ( from hypoglycemic antidiabetic

(2001) (2001) (2001) (2001)

Mentz Mentz Mentz Mentz

and and and and (1986)

(2004) (2004)

(2002) (2002) (1997)

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al. (2000)

al. al.

(2000)

al. al.

(2003) et (2003) (2003) (2003)

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et et (2009) (2009)

and and and and

et et

(2004) (1997) (1997) (1997) (1997)

(2003)

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of

and

with with

burned wine,

bergamota

mouthwash, fomentation gargle,

leaves

alcoholature tea tea

with

macerated

and

for for with

sugar tea,

tea

úcar

hull ¸ water

part

tea

form

in

leaves

brown

alcoholic compound chimarrão, dye alcoholature, syrup compound

aerial

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parts Tea parts fruits

parts

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aerial

parts parts – leaves; leaves leaves;

leaves; part Prepare

pod

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L. Native Aerial L.

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Mart.

L. Mart. Link Native

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L.

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(Jacq.)

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ferrea applii Macbr. officinale vulgare macrophylla

giganteum

x

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edule

J.F. minuta

officinalis illinoinensis sativa

Reissek

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Continued (

1

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M. Trojan-Rodrigues et al. / Journal of Ethnopharmacology 139 (2012) 155–163 159 in

in the

in in );

) in

); effect extract

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either 2005

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Bopp al., ); of hypoglycemic

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et

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(

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prepared treatment

antihyperglycemic pharmacologically

Teixeira showed

extract

1997 (

al., leaf showed

Gupta, mice

patients the

and

Teixeira

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al.,

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extract extract and extracts

˜ of

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nor

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( (

Villase

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Teixeira et cumini ethanolic from

( the

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of ethanolic

2010 hyperglycemic rats rats detectable S. with );

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al., );

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none et

activities

the Teixeira neither

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uptake

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( hypoglicemic

and anti

not

vitro patients al.,

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(2001) (2001) Mentz Mentz Mentz Mentz

and and and and (1986) (1986)

(2004) (2004) (2004) (2004) (2004) (2007)

Irgang Irgang

al. al. (2000) (2000) (2000) (2000) (2000)

al. al. al. al. al. al.

(2000) (2000)

(2005)

(2003) et et (2003) (2003) (2003) (2003) (2003)

(2003) (2003) (2003)

et et et et et et (2009) (2009)

and and

(2004) (1997)

(2003) (2003) (2003)

Leitzke Possamai Possamai Leitzke Soares Soares Barbosa Ceolin Hass Marodin Possamai Vendruscolo Vendruscolo Soares Possamai Hass Leitzke Simões Sebold Leitzke Barros Garlet Simões Vendruscolo Ceolin Garlet Hass Kubo Leitzke Löwe Marodin Martha Possamai Sebold Soares Vendruscolo Sebold Soares (2006) (2006) (2006) (2006)

tea

goiabeira branches

alcoholature

bark

three

food

pitangueira compound

dust and

drops) sete-capota

pau-ferro three

chimarrão, chimarrão juice, syrup, seed

(in

– branches Tea Tea, Tea Tea – – – Tea, Elixir Dye Tea – – – Tea Tea, “Three Elixir Tea – Tea Tea, Tea Tea – – Tea Tea Tea Tea, – Tea Tea Tea Tea – branches”” plus with

roots fruits

flowers flowers seeds fruits

plant

parts button; leaves

leaves; leaves; leaves

seeds Bark Seeds Leaves Leaves; – – Leaves Leaves Leaves – Bark; – Leaves Bark Leaves – Aerial Leaves Leaves; Leaves Seeds Seeds Leaves; Leaves Seeds Elixir Leaves – Buds; Leaves Leaves – Leaves; Floral Leaves Whole

Native Exotic Native Native Exotic Exotic Exotic Exotic Native Exotic Exotic Native Native Native Native Exotic Native Native Bark; Native ExoticExotic Bark; Leaves

DC. -Hil.

St.

Presl

Eichler J.

A.

Sabine

DC.

(Jacq.)

Mill. (Cham.) (L.)

DC.

Berg verum Berg

acutifolius Tiegh. vulgaris

O.

L. coromandelianum

O. L. globulus

argentea communis

cumini

australis cattleianum involucrata uniflora Pav.)

americana alba nigra

&

Garcke

Persea Struthanthus Bunchosia Waltheria Morus Morus Eugenia Psidium Labill. Cinnamomum Tripodanthus Malvastrum Leandra Campomanesia guazumifolia (Cambess.) (L.) Skeels Cogn. (Ruiz Campomanesia xanthocarpa Eucalyptus Eugenia Syzygium

Lauraceae Moraceae Lauraceae Loranthaceae Loranthaceae Malvaceae Malvaceae Melastomataceae Myrtaceae Myrtaceae Myrtaceae Myrtaceae Myrtaceae Moraceae Myrtaceae Myrtaceae

160 M. Trojan-Rodrigues et al. / Journal of Ethnopharmacology 139 (2012) 155–163 al.,

al.,

et

et

) Ferreira (

Cazarolli (

2004

al.,

diabetes et

of

Chau (

-fucopyranoside l treatment al.,

tissue

glucose

Ramesh ) et (

of

the

in of

and model and

in and

rats 2006

rat

glucose

leaves hypoglycemic al.,

active normal in Takahashi

et

(

Ramesh absorption in found found found blood diabetic

(

from

circulatory

apigenin-6-C-beta- diabetic

in

of showed the mice to

in

reestablishment rats )

showed were were were )

in

);

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activity )

parts Kotowaroo

2010 (

2007 significant

2009 activity umbelliferone

active

extract

diabetic al., studies studies studies 2000

al., attributed

al., by aerial

et )

are et al.,

umbelliferone et of

normalization

activity

hyperglycemic et showed

); by related related related

levels

Okoli

2007b ( hypoglycemic activity fibers alcoholic

vitro

activity

Adebajo extract antihyperglycemic in hypoglicemic

( leaves 2007a

rats

Teixeira of of of glucose of (

hydro

in diabetic diabetic diabetic glucose

dietary

showed of );

) ); Pugalendi,

anti anti anti

Figueroa-Valverde No Hypoglycemic No Absence Absence Methanolic Absence – – – – – – – – – – – – – Stalks Extracts Pugalendi, ( streptozotocin-induced reductions No – alloxan-produced levels and humans 2009a activity 1985 normal 2008 (2006) (2006) (2006)

(2001) (2001) Mentz Mentz Mentz

and and and (1986) (1986)

(2004) (2004) (2004) (2004) (2004) (2004) (2007) (2007)

(2002)

Irgang Irgang

al. al. (2000) (2000) (2000) (2000) (2000) (2000) (2000)

al. al. al. al. al. al. al. al.

(2000) (2000) (2000) (2000)

al.

et et (2003) (2003) (2003) (2003) (2003) (2003) (2003) (2003) (2003)

et et et et et et et et (2009)

and and

et

(1997)

(2003)

Vendruscolo Marodin Garlet Possamai Soares Sebold Possamai Sebold Barros Simões Possamai Ceolin Marodin Garlet Vendruscolo Leitzke Leitzke Kubo Leitzke Soares Soares Leitzke Possamai Possamai Vendruscolo Simões Ritter Leitzke Hass Marodin Barros Soares Soares Sebold Marodin Soares Possamai Leitzke Possamai skin,

the

water,

the

food onion

in marcela

without

and

with

tea

and

tea

tea

chimarrão leaves soaking

baths use form References Antidiabetic

it

drops

the

chimarrão sitz let bath,

– – Internal lemon Tea Tea Tea Tea Tea, Tea Tea Tea, Tea Food Tea – – Maceration, Tea Tea, – – Salad Dye Tea – Blend – compound Tea, flowers margins

Knowledge.

fruits roots Tea flowersElixir

seeds, fruits, leaves of

plant Tea

leaves;

flowers parts; parts – parts

part Prepare bark

hulls, hull

Web

Leaves Leaves roots Seeds fruits Leaves Leaves; Leaves Leaves Leaves Leaves; fruit Leaves Fruits – – Leaves Leaves Roots; Flowers Leaves Leaves Leaves – fruit without midrib, Leaves Tea –– seeds, Aerial –– Leaves, Aerial Leaves, Roots Tea Leaves Alcoholature, Leaves; – Leaves Tea Aerial Leaves Leaves Tea Leaves ISI

in

Native Exotic Exotic Exotic Root Exotic Exotic Native Whole Exotic Native Native Exotic Exotic Native Native Exotic Exotic Native Native Native Exotic Native

reviewed

L.

GomesNative

L. de

Vahl not

Batsch Sw. Native

L.

Lam. Mart.

L.

(L.) (L.)

L.

(Pers.)

Sm.

Mill.

L. Jarvis

(L.)

Lam.

were

L. Exotic (Rich.) (Kaulf.) niruri

R.M.

C.E.

officinarum

(Ortega) japonica Swingle

jambos brasiliensis & verticillata carambola &

Lindl. australis paniculatum

sylvestris

zerumbet persica

Hassl. urens brasiliensis sicyoides verticillata which aurantifolia aurantium

arborescens lacryma-jobi

Burtt

Sota

Syzygium (Christm.) Meisn. (Thunb.) L. Averrhoa Phyllanthus Plantago Muehlenbeckia sagittifolia Prunus Richardia Stemodia Solanum Tropaeolum pentaphyllum Cissus Alpinia la Nicolson B.L. Alston (Mill.) Saccharum Casearia Aloe Coix Rubus Citrus Citrus Urtica Stachytarpheta cayennensis Cissus Microgramma squamulosa Eriobotrya plants

)

indicate

Continued ( (–)

1

FamilyMyrtaceae Species Origin Used Vitaceae Poaceae Polygonaceae Salicaceae Rubiaceae Oxalidaceae Phyllanthaceae Xanthorrhoeaceae Poaceae Rosaceae Rosaceae Rutaceae Rutaceae Scrophulariaceae Tropaeolaceae Urticaeae Verbenaceae Vitaceae Zingiberaceae Polypodiaceae Solanaceae Plantaginaceae Rosaceae Table Dashes

M. Trojan-Rodrigues et al. / Journal of Ethnopharmacology 139 (2012) 155–163 161

Cissus sicyoides and Cissus verticillata (Vitaceae). The adoption of Dr. Rumi Regina Kubo for their contributions to this paper, as well

names of medicaments for medicinal plants has been reported for Raquel Ludke for the information about additional surveys. This

some time, and indicates the occurrence of acculturation in the use research was carried out with financial support from the CAPES

of medicinal plants (Martins et al., 2005) This phenomenon is char- (Coordination for the Improvement of Higher Education Personnel

acterized by the abandonment of the traditional designation of one – Brazil).

plant for another name that corresponds to a medicine used with

the same therapeutic purpose (Di Stasi, 2007). In Rio Grande do Sul,

Kubo (1997) and Marodin (2000) reported this phenomenon for

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from Bidens pilosa can modulate the differentiation of helper T cells and pre-

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