Journal of Ethnopharmacology 131 (2010) 522–537
Contents lists available at ScienceDirect
Journal of Ethnopharmacology
journal homepage: www.elsevier.com/locate/jethpharm
Review
Piper umbellatum L.: A comparative cross-cultural analysis of its medicinal uses
and an ethnopharmacological evaluation
Carles M.F.B. Roersch a,b,∗
a
Instituto de Medicina Dominicana, P.O. Box 160, Santo Domingo, Dominican Republic
Instituto de Ciencias Fisiológicas y Medicina Experimental Dr. “Dr. José de Jesús Álvarez Perelló”, Universidad Nacional Pedro Henriquez Ureña, Av. J.F.Kennedy Km 6½, Santo
Domingo, Dominican Republic
b
a r t i c l e
i n f o
Article history:
Received 18 February 2010
Received in revised form 21 July 2010
Accepted 21 July 2010
Available online 1 August 2010
Keywords:
Piper umbellatum
Piperaceae
Medicinal plant
Traditional medicine
Pharmacological activity
Cross-cultural uses
Dominican Republic
a b s t r a c t
Aim of the study: This review assesses the botany, traditional medicinal uses, phytochemistry, pharmacology and toxicology of P. umbellatum.
Materials and methods: Information on P. umbellatum was gathered via the internet (using Scirus, Google
Scholar, CAB-Abstracts, MedlinePlus, Embase, Scielo, and Web of Science) and libraries. Additionally,
previously unpublished work on the traditional uses of P. umbellatum from our National Study of the
Medicinal Plants of the Dominican Republic has been included.
Results: Piper umbellatum is a Neotropical plant species widely distributed in Mexico, Central America,
South America and the West Indian Islands. It has also been introduced to Africa and South-East Asia.
Traditional uses for this plant are recorded in 24 countries in three continents, America, Africa and Asia for
a wide range of ailments such as kidney, women diseases, diarrhea, skin affections, burns, rheumatism,
malaria, intestinal parasites, inflammation and fever. We have analyzed the cross-cultural agreement
among traditional uses in different countries and found a high degree of consensus for the indications
kidney/diuretic, stomachache and wounds. Phytochemical studies of P. umbellatum have demonstrated
the presence of terpenes (mainly found in the essential oil), alkaloids, flavonoids, sterols and other classes
of secondary metabolites. The extracts and pure compounds derived from P. umbellatum show a wide
spectrum of pharmacological activities including antibacterial, anti-inflammatory, analgesic, antioxidant,
cytotoxic, antimalarial, antileishmanial, and antitrypanosomal activity. A first commercial product is in
development, based on the plant’s protective characteristics against UV irradiation.
Conclusions: The interesting biological activities of P. umbellatum need further research in in vivo experiments and clinical studies. The outcome of these investigations will determine the possible development
of drugs from P. umbellatum.
© 2010 Elsevier Ireland Ltd. All rights reserved.
Contents
1.
2.
3.
4.
5.
6.
7.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Botany . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Traditional medicinal uses of P. umbellatum in a cross-cultural context . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Phytochemistry . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Pharmacology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
5.1.
Antifungal activity: . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
5.2.
Antioxidant activity and skin protection . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
5.3.
Antimalarial activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
5.4.
Other biological activities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
5.5.
Pharmacological activities versus traditional medicinal uses . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Toxicology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
∗ Tel.: +809 568 7570; fax: +809 568 7570.
E-mail address: croersch@imd-medicina-dominicana.org.
0378-8741/$ – see front matter © 2010 Elsevier Ireland Ltd. All rights reserved.
doi:10.1016/j.jep.2010.07.045
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Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 535
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 535
1. Introduction
Since 1978, the World Health Organization has promoted the
development of Primary Health Care (PHC) and the importance of
the involvement of traditional health care systems, including the
use of medicinal plants (Anonymous, 1979, 1988; WHO, 1978).
Several authors have described ways in which medicinal plants
could be a part of PHC (Farnsworth et al., 1985; Le Grand and
Sri-Ngernyuang, 1989; Wondergem et al., 1989). Our own experience in Peru and the Dominican Republic has demonstrated that
PHC will fail if traditional medicine, including medicinal plants, is
not taken into account (Hoogte and Roersch, 1984, 1988; Roersch,
1994; Roersch and Hoogte, 1987).
In the Dominican Republic, two medical systems can be distinguished: the formal medical system and the informal medical
system. The formal medical system is based on the Western
conventional medical system (in which the biomedical model predominates) and involves hospitals, clinics, drugstores, insurance
companies and teaching facilities (universities). The informal medical system can also be called the Traditional Dominican Health
System (TDHS), which is based on ancient concepts and practices
in the Dominican culture. These concepts and practices have several
origins, including the slaves, who contributed a polytheistic African
cosmology (Deive, 1981, 1992); the Spaniards, with their medieval
cosmology, including spiritualism and alchemy (Kuschick, 1995);
and elements of the Taina culture (the original inhabitants of the
island) (Davis, 1987). Locally, the following terms are used: ‘medicina de farmacia’ (‘drugstore medicine’) for the formal health system
and ‘plantas (‘matas’) de la tierra’ (‘plants of the earth’) for the
informal health system (Roersch, 1995). Medicinal plants play an
important role in the Traditional Dominican Health System. Medicinal plants and other ingredients of this traditional medical system
are offered at local markets, on street corners and in special stores
(boticas). In a study concerning the market for medicinal plants,
we found that in the capital, Santo Domingo, the annual sales total
for medicinal plants amounts to $702,000 USD (Roersch, 1999).
Publications about the use of medicinal plants in the Dominican
Republic are not abundant, and most are descriptions of popular uses (Cordero, 1986; IMD et al., 1994a,b,c, 1997, 1999a,b,c,d;
Liogier, 1990; Mañon et al., 1992; Peguero, 2002; Peguero et al.,
2001; Polanco et al., 1998); some include experimental data (phytochemistry and biological characteristics) (Bonnelly et al., 1985;
Germosén-Robineau, 1995). Recently, studies have been undertaken to determine the relation between the uses of medicinal
plants by Dominican immigrants in New York and their country of
origin (Ososki et al., 2007; Reiff et al., 2003; Vandebroek et al., 2007).
However, there has been no extensive, systematic research on the
use of medicinal plants in the Dominican Republic. For the integration of medicinal plants in the official health system and for the
development of a national policy on alternative and complementary health practices, it will be necessary to have a broad knowledge
of the uses of the medicinal plants within the TDHS. As stated by the
WHO (WHO, 2002), it is necessary for a country with an active traditional health system, to formulate a national health care policy,
to have a broad knowledge of traditional health practices. Therefore, the Instituto de Medicina Dominicana (IMD, or the Dominican
Institute of Medicine) formulated a project for this purpose, calling it the National Study of the Medicinal Plants of the Dominican
Republic. In 2000, together with the Pan-American Health Organization (PAHO), a questionnaire was developed. With the help of
students from the Universidad Nacional Pedro Henriquez Ureña
(UNPHU), we have thus far conducted more than 5000 interviews
with about 1000 persons in each of the provinces of the Dominican
Republic. With the outcome of these interviews, an ethnopharmacological database has been constructed. P. umbellatum appears to
be an important plant in the treatment of, among other conditions,
leucorrhoea, locally known as ‘vaginal flow’. This disorder is very
common in the Dominican Republic. A first step in the validation
of this ethnopharmacological application is the assessment of the
existing literature on this plant. The presented review is the result
of this process and includes previously unpublished work.
2. Botany
Piper umbellatum L. (Piperaceae, syn. based on Tropicos: Pothomorphe umbellata (L.) Miq., Lepianthes umbellata (L.) Raf., Heckeria
umbellata (L.) Kunth., Peperomia umbellata (L.) Kunth) is a perennial
scrambling shrub or woody herb, 1–2.5(−4) m tall. Stems numerous, succulent, ribbed, forming a dense clump, rooting at the nodes,
main roots woody. Leaves alternate, almost circular to reniform,
5–40 cm × 5–40 cm, blade dark green above, grayish below, base
deeply cordate, apex shortly acuminate to rounded, margins entire
or crenulate, sparsely to densely hairy on the veins on both sides,
venation palmate, 11–15 veins, petiole 6.5–30 cm long, dilated
and sheathing basally. Inflorescence 5.5–15 cm long, 2–8 together
in false umbels, peduncle 3–12 cm long, 1–3 peduncles together,
peduncular bracts narrow, 6–8 mm long, white, soon falling. Flowers small, bisexual; floral bracts triangular to rounded, 0.5–0.8 mm
wide, subpeltate, margins fimbriate, white, cream or yellow; perianth absent; stamens 2; ovary superior, 1-locular, stigmas 3. Fruit
a drupe, obpyramidal, 3-angled, 0.6–1 mm × 0.4–0.6 mm, brownish
seed globose (Schmelzer, 2001).
This is a Neotropical species widely distributed in Mexico, Central America, South America and the West Indian islands. It has
been introduced to Africa and South-East Asia and is now broadly
naturalized (Domis and Oyen, 2008; Liogier, 2000; Saralegui, 2004;
Schmelzer, 2001).
3. Traditional medicinal uses of P. umbellatum in a
cross-cultural context
Besides the medicinal uses of P. umbellatum, the plant is also
used in medical-magic rituals in Cameroon (Agbor et al., 2005) and
Gabon (Akendengue and Louis, 1994). It is also used in Gabon as
a fetish to cause compassion (Domis and Oyen, 2008), to change
the sex of a child at birth in Cameroon (Jiofack et al., 2008), in
religious affairs in Brazil (Azevedo and Silva, 2006), as a fragrance
against ‘mal aire’ (bad air) in Ecuador (Pohle and Reinhardt, 2004)
and in Ghana as bait to attract fish (Domis and Oyen, 2008). In
the Dominican Republic, the leaves are used by farmers to protect themselves against the heat by putting the leaves under their
hats. In many countries, P. umbellatum is used as a vegetable or
condiment (young leaves and inflorescences eaten raw, boiled or
steamed) in people’s daily diets. In tropical Asia, the fruits are eaten
as a delicacy (Schmelzer, 2001). The Shuar in Ecuador use it as a
condiment (Pohle and Reinhardt, 2004). The nutritional values and
mineral contents of P. umbellatum (leaves) are as follows: ascorbic acid: 181 mg/100 g DM, carbohydrates: 3.8 g/100 g DM, protein:
3.9 g/100 g DM, moisture: 80% fiber: 2.2 g/100 g DM; and minerals:
Ca: 2.36, K: 4.1, Mg: 0.88, Na: 0.12, Fe: 0.05 mg/100 g) (Mensah et
al., 2008).
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In general, traditional, local uses of medicinal plants are the
starting point for the development of new drugs from the same
plants (Farnsworth et al., 1985; Farnsworth and Loub, 1983).
Numerous ethnopharmacological studies have been performed
all over the world in different cultures (Heinrich et al., 2009).
To determine the effectiveness of medicinal plants, Trotter and
Logan (1986) proposed a method known as the Informant Consensus. They argued that within and between cultural groups plants
with scientifically (i.e., pharmacologically) proven effectiveness are
more likely to be found, and will have a consistent pattern of usage.
Moerman (2007) stated that “consensus will identify plants with
significant and appropriate pharmacological properties”. This in
turn leads to the hypothesis that the same (or consensus) uses of a
plant in different cultures should have a scientific basis. We have
examined this cross-cultural agreement in the case of P. umbellatum.
The medicinal uses of P. umbellatum in traditional medicine
health systems are recorded in 24 countries across three continents.
In Table 1 , these uses are ordered according to the disease classification used in the modern Western biomedical system (Anonymous,
2007). It was necessary to extend this classification with categories
such as Women diseases, Liver and Fever, which are used in various traditional medicine health systems. A total of 94 traditional
medicinal uses for P. umbellatum are registered. In the American
continent information has been found for Brazil, Mexico, Jamaica,
Cuba, Dominican Republic, Haiti, Costa Rica, French Guyana and
Venezuela; in Africa, information was found for Nigeria, Cameroon,
Ivory Coast, Gabon, Zimbabwe, Liberia, Congo, Guinea, São Tomé
and Príncipe, Burundi, Comoros Islands, Guinea Equatorial and
Ghana; and in Asia, the Philippines and Malaysia are mentioned.
There are also references to the West Indies, to Africa as a whole,
and to East Africa, Central Africa, Southeast Asia and Indochina. In
this review, they will be considered a country. The country with
by far the most indications is Brazil (35), which also has the largest
number of authors (21). In the majority of these countries, literature
on this subject has just one author (14). In Asia, one author published a monograph on P. umbellatum within the PROSEA project for
Southeast Asia (Schmelzer, 2001). A similar project, called PROTA,
exists in Africa; in it, Domis and Oyen elaborated on a monograph on
P. umbellatum (Domis and Oyen, 2008). In the case of the Dominican
Republic, our own data, collected in our National Study, are added.
We have distinguished 13 categories of illnesses. The first one,
Urinary tract, has only two groups of traditional treatments, diuretic
and kidneys, but they are present in nine countries in three continents. The majority of the traditional uses in the category of Women
Diseases have their origin in Africa. Only leucorrhoea, accelerated
labor and emmenagogue are also treatments in the American continent. In the Digestive tract we see the same pattern as in Women
Diseases with the exception that two traditional uses are also mentioned in Asia, while in Women Diseases no application is found in
Asia. In Skin the three continents are present, with Asia only represented by one indication, abscesses. In the Respiratory tract, America
is represented by four treatments and four countries, Africa with
two indications and one country and Asia with just one indication
and one country. Liver is mentioned by 10 authors for Brazil. Fever
(and sudorific and febrifuge) is mentioned for Brazil, Gabon and
Africa. Eight different traditional treatments for Pain are recorded
in nine countries in two continents (if we include stomachache, up
to 13 countries in three continents). The plant is used as an antiinflammatory in Brazil, Mexico and Cuba and for inflamed tumors
in Africa. Also important are the Wound healing properties. This
category is found in six countries in the three continents. The category of Swellings, contusions is found in the three continents. These
last two more or less related categories have 11 diseases indications combined (including inflammation increases this number to
14). Rheumatism is mentioned in Africa and the West Indies.
From the 94 medicinal uses, 59 are uses for just one country in
one continent; 10 are uses for two or more countries in one continent, 21 are uses for two or more countries in two continents and
four are uses for four or more countries in three continents. In Fig. 1,
the traditional medicinal uses that occur in two or more countries
in one or more continents are ordered. Women diseases are represented by four traditional uses out of a total of 14 (Table 1); the
Digestive tract has three uses out of 17, Skin has three uses out of six,
Pain has four uses out of eight, the group Inflammation, Wounds and
Swellings, contusions has six out of 14 and Urinary tract has two out
of two. The cross-cultural uses with most consensus are kidneys,
diuretic, stomachache and wounds. These traditional medicinal
uses are present in more than four countries in three continents.
These uses, together with the categories Pain (with stomachache
used in three continents), Inflammation, Wounds, Swellings, Contusions (with wounds used in three continents) and Skin (with
three out of six disease indications mentioned in five countries in
two continents), can be categorized as highly indicated for further
investigation.
4. Phytochemistry
Phytochemical studies of P. umbellatum have demonstrated the
presence of terpenes (mainly found in the essential oil), alkaloids,
flavonoids, sterols and other classes of secondary metabolites. A
catechol, 4-nerolidylcatechol (Fig. 2), is considered the main bioactive compound. It is found in the whole plant (Bergamo et al., 2005;
De Oliveira and Akisue, 1984; Desmarchelier et al., 1997; Kijjoa et
al., 1980; Núñez et al., 2005; Tabopda et al., 2008; Viana et al., 2000).
From the branches, Tabopda et al. (2008) isolated some interesting new bioactive alkaloids, which they named piperumbellactams
A–D (Fig. 2). Another bioactive alkaloid, N-benzoylmescaline, was
found by Isobe et al. (2002) in the aerial parts of a Brazilian P.
umbellatum (Table 2).
Various studies have analyzed the composition of the essential oil of the leaves of P. umbellatum. Three studies were carried
out in Brazil, one in Costa Rica, one in Cuba and one in São Tomé
and Príncipe. Another study was done in Cameroon, and it detected
the presence of cadinene, caryophyllene and phellandrene (Chartol,
1964). This study is not included because the oil was extracted
from the leaves and flowers, while the other studies only used
the leaves. As one can see in Table 3, there are considerable differences between the presented essential oils. Most striking is the
contrast between the essential oil from Africa and the essential oils
from the American continent. In São Tomé and Príncipe, the main
constituents are the monoterpenoids ␣- and -pinene, while in
Brazil, Cuba and Costa Rica the sesquiterpenoids -caryophyllene
and germacrene D are the important elements. Within the American continent a salient feature is the singularity of the essential
oil of Cuba, where one component, safrole, is most significant
(48.7%). The essential oil of Costa Rica has (E,E)-␣-farnesene as
one of the three main constituents. This compound is only mentioned by Martins et al. (1998) in São Tomé and Príncipe. Mesquita
et al. (2005) present two series of data. One concerns a sample
collected in 1999 and the other one in 2001, both in the ‘Parque
Estadual do Rio Doce’ in the state of Minas Gerais. The main components are present in both samples, but the percentages are not
the same. Principal differences are in the presence of germacrene
D and trans-dihydroagarofurane. The last component was not even
detected in the sample of 2001! The recently elucidated role played
by -caryophellene to produce anti-inflammatory effects (Gertsch
et al., 2008) and the traditional uses of P. umbellatum related to
inflammation (Table 1) deserve more investigation. The presented
differences in the contents of the essential oils of P. umbellatum
make it very clear that for further comparison of experimental data,
C.M.F.B. Roersch / Journal of Ethnopharmacology 131 (2010) 522–537
525
Table 1
Cross-cultural medicinal uses of P. umbellatum.
Part used
Application*
Country
References
Not specified
Root
Not specified
Not specified
Brazil
Brazil
Leaf, root
Bark
Decoction, infusion
Decoction
Brazil
Brazil
Leaf
Leaf, root
Leaf, root
Fruit
Infusion
Not specified
Not specified
Not specified
Cuba
Dominican Republic
Haiti
Nigeria
Leaf
Leaf
Juice
Decoction
Africa
South-East Asia
Britto et al. (2007)
Brandão et al. (2008),
Hegnauer (1969)
Grandi et al. (1989)
Schultes (1980), in
Hammer and Johns (1993)
Pino et al. (2005)
Liogier (2000)
Liogier (2000)
Ndukwu and
Ben-Nwadibia (in press)
Domis and Oyen (2008)
Schmelzer (2001)
Inflorescence
Leaf
Root
Decoction
Decoction or infusion
Not specified
Brazil
Brazil
Brazil
Leaf
Leaf
Leaf and fruit
Leaf or root
Decoction
Maceration
Not specified
Decoction
Africa
Cameroon
Indochina
Dominican Republic
Not specified
Decoction
Ivory Coast
Aerial parts
Leaf
Leaf
Leaf, root
Not specified
Juice
Juice
Decoction, infusion
Ivory Coast
Africa
Brazil
Brazil
Whole plant
Decoction
Ivory Coast
Aerial parts
Not specified
Ivory Coast
Aerial parts
Not specified
Central Africa
Not specified
Not specified
Gabon
Women diseases
Leaf
Decoction
Guinea
Pain and abundant bleeding
during menstruation
Antihemorrhagic
Painful menstruation
Menstruation
Accelerate labor
Calms birth pains
Expulsion of the placenta
To clean the belly of women
after giving birth
Galactogogue
Leucorrhoea
Leaf
Maceration
Cameroon
Vasileva (1969), in
Hammer and Johns (1993)
Noumi et al. (1999)
Aerial parts
Leaf
Leaf or root
Not specified
Flower, leaf
Root (with Hyptis pectinata)
Leaf
Not specified
Maceration
Not specified
Decoction
Decoction
Decoction
Juice, as an enema
Ivory Coast
Cameroon
Africa
Mexico
Cameroon
Ivory Coast
Zimbabwe
Schmelzer (2001)
Noumi and Yomi (2001)
Domis and Oyen (2008)
Browner (1985)
Jiofack et al. (2008)
Kerharo et al. (1950)
Yamada (1999)
Leaf
Leaf or root
Leaf, root
Juice
Decoction
Decoction, infusion
Africa
Africa
Brazil
Domis and Oyen (2008)
Domis and Oyen (2008)
Grandi et al. (1989)
Vaginal flow
Leaf (with roots of Agave
sp., leaves of Momordica
charantia and Argemone
mexicana)
Leaf
Leaf (with leaves of
Momordica charantia)
Decoction
Dominican Republic
Roersch**
Infusion
Decoction
Dominican Republic
Dominican Republic
Roersch**
Roersch**
Root
Maceration and drunk with
white wine
Poultice, external
Brazil
Hammer and Johns (1993)
Mexico
Browner (1985)
Decoction
Decoction
Decoction
Maceration (with juice of
old banana spike)
Maceration
Africa
Africa
Africa
Cameroon
Domis and Oyen (2008)
Domis and Oyen (2008)
Domis and Oyen (2008)
Noumi and Yomi (2001)
Cameroon
Noumi and Dibakto (2000)
Medicinal use
Urinary tract
Diuretic
Kidneys
Women diseases
Emmenagogue
Anti–abortive
Digestive tract
Diarrhea
Leaf
Digestive
Dyspepsia
Constipation
Dysentery
Root
Root
Root
Leaf
Peptic ulcer
Leaf
Agra et al. (2007)
Santos and Lima (2008)
Rodrigues and Guedes
(2006)
Domis and Oyen (2008)
Chartol (1964)
Schmelzer (2001)
Roersch**
Bouquet and Debray
(1974), in Hammer and
Johns (1993)
Schmelzer (2001)
Domis and Oyen (2008)
Roig (1945)
Grandi et al. (1989)
Bouquet and Debray
(1974), in Hammer and
Johns (1993)
Schmelzer (2001), Domis
and Oyen (2008)
Schmelzer (2001), Domis
and Oyen (2008)
Bodinga-bwa-Bodinga and
Van der Veen (1993)
C.M.F.B. Roersch / Journal of Ethnopharmacology 131 (2010) 522–537
526
Table 1 (Continued )
Medicinal use
Part used
Application*
Country
References
Laxative for pregnant women
Not specified
Decoction
Guinea
Leaves with palm kernel oil
Boiled with local palm
kernel oil
Nigeria
Vasileva (1969), in
Hammer and Johns (1993)
Ndukwu and
Ben-Nwadibia (in press)
Edema (stomach)
Intestinal parasites
Leaf
Leaf
Leaf
Leaf
Leaf
Plant
Not specified
Tied on the stomach
Maceration
Not specified
Not specified
Not specified
Not specified
Not specified
South-East Asia
Cameroon
Central Africa
Congo
Guinea
French Guyana
Jamaica
Schmelzer (2001)
Noumi and Dibakto (2000)
Domis and Oyen (2008)
Domis and Oyen (2008)
Domis and Oyen (2008)
Schmelzer (2001)
Mitchell and Ahmad (2006)
Filariasis
Diarrhea with blood
Stomachache
Not specified
Leaf
Leaf
Root
Leaf
Leaf or root
Leaf
Not specified
Decoction
Decoction
Not specified
Infusion
Decoction
Infusion
Brazil
Mexico
Mexico
Brazil
Cuba
Africa
Nigeria
Leaf
Leaf
Not specified
Decoction
Nigeria
South-East Asia
Britto et al. (2007)
Robinson and López (1999)
Robinson and López (1999)
Brandão et al. (2008)
Pino et al. (2005)
Domis and Oyen (2008)
Ndukwu and
Ben-Nwadibia (in press)
Mensah et al. (2008)
Schmelzer (2001)
Colic
Leaf
Leaf and fruit
Infusion
Not specified
Liberia
Indochina
Domis and Oyen (2008)
Schmelzer (2001)
Emollient
Rectal prolapse
Piles
Nausea
Scurvy
Burps
Leaf
Leaf
Flower, leaf
Not specified
Seed (essential oil)
Leaf
Not specified
Crushed, as an enema
Decoction
Not specified
Oral
Decoction
Africa
Africa
Cameroon
Cameroon
West Indies
Dominican Republic
Domis and Oyen (2008)
Domis and Oyen (2008)
Jiofack et al. (2008)
Chartol (1964)
Chenu (1986)
Roersch**
Leaf
Decoction in poultice
Mexico
Leaf
Leaf
Poultice in water
Not specified
Brazil
São Tomé and Príncipe
Zamora-Martínez and Pola
(1992)
Hammer and Johns (1993)
Martins et al. (1998)
External ulcers
Abscesses
Leaf
Leaf
Leaf, root
Leaf
Decoction, infusion
Applied on the abscesses
Not specified
Not specified
Brazil
South-East Asia
Dominican Republic
Haiti
Grandi et al. (1989)
Schmelzer (2001)
Liogier (2000)
Liogier (2000)
Boils
Leaf
Leaf, root
Root
Not specified
Decoction, infusion
Not specified
Brazil
Brazil
Jamaica
Not specified
Leaf
Not specified
Poultice
Jamaica
Africa
Fenner et al. (2006)
Grandi et al. (1989)
Asprey and Thornton
(1954)
Mitchell and Ahmad (2006)
Domis and Oyen (2008)
Root
Leaf, root
Not specified
Not specified
Leaf
Not specified
Decoction, infusion
Sap
Sap
Poultice
Brazil
Brazil
Dominican Republic
Haiti
Africa
Brandão et al. (2008)
Grandi et al. (1989)
Liogier (2000)
Liogier (2000)
Domis and Oyen (2008)
Root
Root
Whole plant
Syrup
Syrup
Tea
Jamaica
Jamaica
Jamaica
Not specified
Leaf, root
Leaves with Piper auritum
Not specified
Decoction, infusion
Tea
Jamaica
Brazil
Costa Rica
Grieve (in press)
Grieve (in press)
Asprey and Thornton
(1954)
Mitchell and Ahmad (2006)
Grandi et al. (1989)
Hazlett (1986)
Bronchitis
Cough
Leaf, root
Leaves with Piper auritum
Fruit with Piper betle
Decoction, infusion
Tea
Chewed
Brazil
Costa Rica
Malaysia
Grandi et al. (1989)
Hazlett (1986)
Schmelzer (2001)
Breast infection
Angina
Lung indications
Flower, leaf
Not specified
Seed
Decoction
Not specified
Powder externally
Cameroon
Cameroon
West Indies
Jiofack et al. (2008)
Chartol (1964)
Chenu (1986)
Liver
Liver
Root
Not specified
Brazil
Desmarchelier et al.
(1997), Rodrigues and
Guedes (2006)
Skin
Pimples and purulent
pimples
Skin irritation
Burns
Respiratory tract
Catarrhs
Cold
C.M.F.B. Roersch / Journal of Ethnopharmacology 131 (2010) 522–537
527
Table 1 (Continued )
Part used
Application*
Country
References
Root
Inflorescence
Not specified
Root
Leaves with almond oil
Brazil
Brazil
Brazil
Brazil
Brazil
Kijjoa et al. (1980)
Agra et al. (2007)
Britto et al. (2007)
Mentz et al. (1997)
Mentz et al. (1997)
Leaf
Leaf
Decoction
Decoction
Not specified
Decoction
Decoction, in lotion,
externally
Tea
Not specified
Brazil
Brazil
Leaf
Leaf, root
Root
Root
Macerate in water
Decoction, infusion
Not specified
Not specified
Brazil
Brazil
Dominican Republic
Haiti
Coelho and Silva (in press)
Coelho et al. (2002), Vieira and
Martins (2000)
Di Stasi et al. (2002)
Grandi et al. (1989)
Liogier (2000)
Liogier (2000)
Jaundice
Leaf or root
Leaf, root
Decoction
Decoction, infusion
Africa
Brazil
Domis and Oyen (2008)
Grandi et al. (1989)
Spleen
Root
Decoction
Brazil
Bile
Leaf
Not specified
Africa
Mentz et al. (1997), Rodrigues
and Guedes (2006)
Domis and Oyen (2008)
Fever
Sudorific
Fever, Febrifuge
Root
Leaf
Not specified
Decoction
Brazil
Brazil
Leaf
Leaf
Not specified
Leaf, root
Leaf
Brazil
Brazil
Brazil
Brazil
Gabon
Not specified
Eaten, fresh or dried
Body, rub
Not specified
Decoction, infusion
Pounded with water, as a
bath
Not specified
Leaf
Decoction, as a wash
Africa
Not specified
Leaf
Not specified
Infusion
Infusion
Not specified
Brazil
Brazil
Gabon
Stehmann and Brandâo (1995)
Di Stasi et al. (2002)
Bodinga-bwa-Bodinga and Van
der Veen (1993)
Inflorescence
Leaf
Leaf
Decoction
External, warm
Not specified
Brazil
Dominican Republic
Africa
Leaf
Not specified
Not specified
Tied on the head
Not specified
Not specified
Jamaica
Jamaica
Cameroon
Agra et al. (2007)
Roersch**
Domis and Oyen (2008),
Schmelzer (2001)
Asprey and Thornton (1954)
Mitchell and Ahmad (2006)
Chartol (1964)
Inflorescence
Leaf
Decoction
Massage
Brazil
Africa
Not specified
Not specified
Gabon
Leaf
Venezuela
Díaz and Ortega (2006)
Medicinal use
Pains
Body ache
Muscular pain
Headache
Migraine
Analgesic
Gabon
Brandão et al. (2008)
Hammer and Johns (1993),
Oliveira et al. (2003)
Hammer and Johns (1993)
Estrella (1995)
Britto et al. (2007)
Grandi et al. (1989)
Akendengue and Louis (1994)
Bodinga-bwa-Bodinga and Van
der Veen (1993)
Domis and Oyen (2008),
Schmelzer (2001)
Agra et al. (2007)
Domis and Oyen (2008),
Schmelzer (2001)
Bodinga-bwa-Bodinga and Van
der Veen (1993)
Leaf
Warm, placed on the
affected area
Not specified
Congo
Bioka and Abena (1990)
Toothache
Leaf
Maceration
Cameroon
Abdominal pains
Earache
Root
Leaf
Infusion
Juice, as drops
São Tomé and Príncipe
Africa
Noumi et al. (1999), Noumi and
Dibakto (2000)
Sequeira (1994)
Domis and Oyen (2008)
Root
Leaf
Brazil
Mexico
Desmarchelier et al. (1997)
Kashanipour and McGee (2004)
Leaf
Not specified
Wrapped around the
irritated area
Not specified
Cuba
Pino et al. (2005)
Not specified
Not specified
Brazil
Britto et al. (2007)
Root
Decoction in alcohol (dry
gin)
Decoction
Nigeria
Ndukwu and Ben-Nwadibia (in
press)
Domis and Oyen (2008)
Inflammation
Anti-inflammatory
Swelling and inflammation
of the legs
Inflamed tumors
Leaf or root
Africa
C.M.F.B. Roersch / Journal of Ethnopharmacology 131 (2010) 522–537
528
Table 1 (Continued )
Medicinal use
Wounds
Wounds
Antiseptic
Erysipelas
Swellings, contusions
Contusions, bruises
Part used
Application*
Country
References
Root
Leaf
Leaf
Leaf or root
Leaf
Leaf
Not specified
Not specified
Decoction, in bath
Not specified
Decoction
Fresh, applied on wounds
Decoction
Not specified
Brazil
Brazil
São Tomé and Príncipe
Africa
South-East Asia
Cameroon
Gabon
Brandão et al. (2008)
Rodrigues and Guedes (2006)
Martins et al. (1998)
Domis and Oyen (2008)
Schmelzer (2001)
Chartol (1964)
Bodinga-bwa-Bodinga and Van
der Veen (1993)
Leaf
Not specified
Not specified
Not specified
Africa
Brazil
Domis and Oyen (2008)
Britto et al. (2007)
Leaf
Leaf
South-East Asia
Brazil
Schmelzer (2001)
Hammer and Johns (1993)
Brazil
Estrella (1995)
Brazil
Hammer and Johns (1993)
São Tomé and Príncipe
Africa
Zimbabwe
Martins et al. (1998)
Domis and Oyen (2008)
Yamada (1999)
Brazil
Hammer and Johns (1993)
Leaf
Fresh, applied on wounds
Warm, placed on the
affected area
Poultice (with cow
intestines)
Warm, placed on the
affected area
Not specified
Poultice
Juice, rubbed on the
affected part
Warm, placed on the
affected area
Not specified
Nigeria
Ndukwu and Ben-Nwadibia (in
press)
Schmelzer (2001)
Leaf
Cuts and sprains
Leaf
Swellings
Leaf
Leaf
Leaf
Leaf
Dropsy
Leaf and fruit
Not specified
Indochina
Ascites
Leaf
Infusion
Nigeria
Ndukwu and Ben-Nwadibia (in
press)
Rheumatism
Rubefacient
Fruit
Not specified
Nigeria
Rheumatic pains
Fruit
Not specified
Nigeria
Rheumatism
Root
Decoction in alcohol (dry
gin)
Friction
Powder, externally
Nigeria
Ghana
West Indies
Ndukwu and Ben-Nwadibia (in
press)
Ndukwu and Ben-Nwadibia (in
press)
Ndukwu and Ben-Nwadibia (in
press)
Domis and Oyen, 2008
Chenu, 1986
Burundi
Polygenis-Bigendako (1990)
Burundi
Polygenis-Bigendako (1990)
Africa
Brazil
Domis and Oyen (2008)
Grandi et al. (1989)
Leaf
Seed
Sundries
Tonic
Leaf, stem
Kwashiorkor
Leaf, stem
Syphilis
Leaf or root
Leaf, root
Stems and leaves ashes on
scarification
Stems and leaves ashes on
scarification
Decoction
Decoction, infusion
Gonorrhea
Depurative
Conjunctivitis
Anemia
Against poisons
Hypertension
Leaf or root
Leaf, root
Leaf
Leaf and fruit
Root
Leaf
Leaf
Decoction
Decoction, infusion
Juice
Not specified
Not specified
Maceration
Decoction
Africa
Brazil
Philippines
Indochina
Jamaica
Cameroon
Comoros Islands
Domis and Oyen (2008)
Grandi et al. (1989)
Schmelzer (2001)
Schmelzer (2001)
Grieve (in press)
Noumi et al. (1999)
Kaou et al. (2008)
Diabetes
Malaria
Leaf
Leaf
Leaf or root
Leaf and root
Decoction
Nasal drops
Decoction
Not specified
Comoros Islands
Guinea Equatorial
Africa
Brazil
Kaou et al. (2008)
Akendengue (1992)
Domis and Oyen (2008)
Oliveira et al. (2003)
Epilepsy
Root
Root
Decoction
Not specified
Brazil
Brazil
Kijjoa et al. (1980)
Britto et al. (2007)
Aphrodisiac
Root
Decoction
East Africa
Infertility
Root
Not specified
Congo
Sedative
Tiredness (Asthenia)
Immunostimulant
Not specified
Root
Root
Not specified
Not specified
Not specified
Congo
Brazil
Brazil
Kokwaro (1976), in Hammer
and Johns (1993)
Nkounkou-Loumpangou et al.
(2005)
Bioka and Abena (1990)
Brandão et al. (2008)
Brandão et al. (2008)
*
**
If not specified, decoction, infusion, juice and maceration are used orally.
Data from our National Study.
C.M.F.B. Roersch / Journal of Ethnopharmacology 131 (2010) 522–537
529
Table 2
Chemical constituents of Piper umbellatum.
Component
Plant part
References
Alkaloids
N-Benzoylmescaline
N-Hydroxyaristolam II
Piperumbellactams (A–D)
Potomorphine
Aerial parts
Branches
Branches
Leaves
Isobe et al. (2002)
Tabopda et al. (2008)
Tabopda et al. (2008)
Hegnauer (1969)
Flavonoids
Acacetin 6-C--D-glucopyranoside
Acacetin 3-O--D-[6′ -dodecanoyl]-glucopyranoside
Acacetin 3-O--D-glucopyranoside
Apigenin 8-C-neohesperidoside
Uvangoletin
Wogonin
Branches
Branches
Branches
Branches
Aerial parts
Aerial parts
Tabopda et al. (2008)
Tabopda et al. (2008)
Tabopda et al. (2008)
Tabopda et al. (2008)
Isobe et al. (2002)
Isobe et al. (2002)
Sterols
Campesterol
-Sitosterol
Aerial parts
Aerial parts
-Sitosterol
Stigmasterol
Leaves, roots
Aerial parts
Sacoman et al. (2008)
Isobe et al. (2002), Sacoman et al. (2008), Tabopda
et al. (2008)
Kijjoa et al. (1980)
Sacoman et al. (2008)
Terpenes
-Amyrin
Bicyclogermacrene
Branches
Essential oil* , leaves
Cadinene
␦-Cadinene
Essential oil, leaves
Essential oil, leaves
-Caryophyllene
Essential oil, leaves
Caryophyllene oxide
␣-Copaene
␣-Cubebene
Cubebol
10-epi-gamma-Eudesmol
Epizonarene
(E,E)-␣-Farnesene
Friedelin
␣-Humulene
Germacrene D
Essential oil, leaves
Essential oil, leaves
Essential oil, leaves
Essential oil, leaves
Essential oil, leaves
Essential oil, leaves
Essential oil, leaves
Branches
Essential oil, leaves
Essential oil, leaves
Limonene
Linalool
(E)-Nerolidol
Essential oil, leaves
Essential oil, leaves
Essential oil, leaves
(E)--Ocimene
(Z)--Ocimene
Phellandrene
Phytol
␣-Pinene
-Pinene
Spathulenol
Essential oil, leaves
Essential oil, leaves
Essential oil, leaves
Essential oil, leaves
Essential oil, leaves
Essential oil, leaves
Essential oil, leaves
Trans-Dihydroagarofurane
-Elemene
-Gurjunene
␣-Acorenol
Essential oil, leaves
Essential oil, leaves
Essential oil, leaves
Essential oil, leaves
Others
4-Nerolidylcatechol
Roots, whole plant, leaves
Dillapiol
E-3-(3,4-dihydroxyphenyl)-N-2-[4hydroxyphenyletyl]-2-propenamide
Heneicosane
N-p-Coumaroyl tyramine
N-trans-Feruloyl tyramine
Safrole
Cinnamic acid
2-(4′ ,8′ -dimethylnona-3′ 7′ -dienyl)-8-hydroxy-2methyl-2H-chromene-6-carboxylic methyl
ester
*
Only the main components of the essential oil are mentioned (>1.0%).
Tabopda et al. (2008)
Luz et al. (1999), Mesquita et al. (2005), Pino et al.
(2005)
Chartol (1964)
Luz et al. (1999), Mesquita et al. (2005), Pino et al.
(2005)
Luz et al. (1999), Maia and Andrade (2009),
Martins et al. (1998), Mesquita et al. (2005), Pino et
al. (2005), Vogler et al. (2006), Chartol (1964)
Luz et al. (1999), Mesquita et al. (2005)
Luz et al. (1999)
Luz et al. (1999)
Luz et al. (1999)
Mesquita et al. (2005)
Luz et al. (1999)
Vogler et al. (2006)
Tabopda et al. (2008)
Luz et al. (1999)
Luz et al. (1999), Maia and Andrade (2009),
Mesquita et al. (2005), Pino et al. (2005), Vogler et
al. (2006)
Martins et al. (1998)
Martins et al. (1998)
Maia and Andrade (2009), Martins et al. (1998),
Mesquita et al. (2005), Pino et al. (2005)
Martins et al. (1998)
Martins et al. (1998)
Chartol (1964)
Martins et al. (1998)
Martins et al. (1998)
Martins et al. (1998)
Luz et al. (1999), Mesquita et al. (2005), Pino et al.
(2005)
Mesquita et al. (2005)
Mesquita et al. (2005)
Luz et al. (1999)
Luz et al. (1999)
Leaves
Branches
Bergamo et al. (2005), De Oliveira and Akisue
(1984), Desmarchelier et al. (1997), Kijjoa et al.
(1980), Núñez et al. (2005), Tabopda et al. (2008),
Viana et al. (2000)
Bernhard and Thiele (1978)
Tabopda et al. (2008)
Essential oil, leaves
Branches
Branches
Essential oil, leaves
Leaves
Branches
Maia and Andrade (2009)
Tabopda et al. (2008)
Tabopda et al. (2008)
Pino et al. (2005)
Chartol (1964)
Núñez et al. (2005)
C.M.F.B. Roersch / Journal of Ethnopharmacology 131 (2010) 522–537
530
Fig. 1. Traditional medicinal uses in two or more countries in one or more continents.
the chemical identification or the use of fingerprints in the extracts
must be taken into account.
5. Pharmacology
The extracts and pure compounds derived from P. umbellatum show a wide spectrum of pharmacological activities, including
antibacterial, anti-inflammatory, analgesic, antioxidant, cytotoxic,
antimalarial, antileishmanial, antitrypanosomal and other activities (Table 4). Pharmacological activities in in vitro and in vivo
experiments are taken as starting points for the development of
clinical studies. The concentrations by which these activities occur,
whether expressed in IC50 , MIC, ED50 , etc., are crucial. Lately, efforts
have been undertaken to obtain a more coherent, standardized
approach. Adequate concentrations for anti-infective bioassays
should be less than 100 g/ml for extracts and mixtures and below
25 M for compounds (Cos et al., 2006). Gertsch (2009) goes even
References see Table 1.
further and proposes 50 g/ml for extracts and 5 M for compounds. For in vivo experiments, Gertsch (2009) questions if doses
of 200 mg/ml or more are of any practical use. Inclusion of controls
in bioassays is very important and determines the effective dose
order of the extract or isolated compound. In the following assessment of the various pharmacological activities of P. umbellatum,
these criteria will be applied.
5.1. Antifungal activity:
In the case of the Dominican Republic, it is very interesting to
know whether antifungal activity is demonstrated for P. umbellatum. In our study, the main traditional use is vaginal flow (locally
called ‘flujo blanco’ or ‘flor blanca’), which is frequently caused
by a Candida albicans infection. Tabopda et al. (2008) tested three
secondary metabolites, Piperumbellactam D, N-hydroxyaristolam
II and 4-nerolidylcatechol, which showed high activity against a
Table 3
Comparison of the essential oils of P. umbellatum in different countries.
Component (% in samples) Country
-Caryophellene
Germacrene D
Heneicosane
(E)-Nerolydol
-Pinene
␣-Pinene
Bicyclogermacrene
␦-Cadinene
(E,E)-␣-Farnesene
-Elemene
Trans-dihydroagarofurane
Safrole
*
Brazil (Maia and
Andrade, 2009)*
Brazil (Luz et al.,
1999)
Brazil (Mesquita et al.,
2005)
Costa Rica (Vogler et Cuba (Pino et al.,
al., 2006)*
2005)
São Tomé and Príncipe
(Martins et al., 1998)
37.5
11.9
1.2
9.1
–
–
–
–
–
–
–
–
14.8
27.4
–
0.7
–
–
11.5
13.3
–
–
–
–
12.6/10.2
8.6/27.4
–
7.0/7.9
0.1
Trace
10.1/8.8
–
–
6.7/6.4
6.6/–
–
28
17
–
–
–
–
–
–
15
–
–
–
9.8
–
–
12.4
17.6
26.8
–
0.1
0.7
–
–
–
Only the main constituents were mentioned.
4.6
7.9
–
1.1
0.2
0.1
3.7
5.6
–
–
–
48.7
C.M.F.B. Roersch / Journal of Ethnopharmacology 131 (2010) 522–537
531
Fig. 2. Structures of some chemical constituents of P. umbellatum.
series of fungi, including C. albicans. The first two demonstrated
an even higher activity against S. flavus and T. longifusus than did
amphotericin B. The authors suggested that the presence of the
methylenic carbon in methylenedioxyphenyl (MDP) is more able to
form a stable carbene under oxidation. However, further research
is needed in in vivo and in clinical studies to confirm these initial
findings. A classification system that was apparently proposed by
Aligiannis et al. (2001) is used in the literature and is based on
MIC values (for extracts), as follows: strong inhibitors – MIC up to
0.5 mg/ml; moderate inhibitors – MIC between 0.6 and 1.5 mg/ml;
weak inhibitors – MIC above 1.6 mg/ml. However, the indicated
reference proposes anything but a classification. These concentra-
532
C.M.F.B. Roersch / Journal of Ethnopharmacology 131 (2010) 522–537
tions are much higher than those suggested by Cos et al. (2006) and
Gertsch (2009).
5.2. Antioxidant activity and skin protection
The extracts of various parts of P. umbellatum and several
isolated compounds show interesting antioxidant activities. It is
known that one of the traditional medicinal uses with consensus
is in the treatment of wounds, and antioxidants play a well-known
role in wound healing (Sen et al., 2002; Soneja et al., 2005). Thus,
we have indirectly confirmed our hypothesis. We recommend that
further research be pursued in this area. Some problems need to
be taken into account, however. It is observed that the extract
shows a higher value compared to 4NC, which could imply the presence of other antioxidant compounds in the extract (Desmarchelier
et al., 1997). The free and total antioxidant capacity of several
Piper sp. (methanolic leaf extract) were studied, using two different methods, the Folin–Ciocalteu reagent (Folin) and the ferric
reducing antioxidant power (FRAP). There was no significant correlation between the Folin and FRAP free oxidant capacity, though
there was a highly significant correlation between the Folin and
FRAP total antioxidant capacity. It was concluded that the results of
antioxidant activity using different methods should be interpreted
carefully (Agbor et al., 2005). In Brazil, this antioxidant activity
was the starting point for studying the effect of the root extract
of P. umbellatum on skin damage produced by UV radiation. Prolonged UV exposure can cause severe depletion of skin antioxidants
(like ␣-tocopherol), which could lead to skin cancer and photoaging. The depletion of ␣-tocopherol was avoided by applying a gel
with the ethanolic extract of the roots of P. umbellatum on the skin
of hairless mice exposed to UV-B radiation (Ropke et al., 2003).
Also, after chronic exposure to UV-B radiation, these hairless mice
were clearly protected from skin wrinkling. This means that the
plant can be used as a photoprotective agent (Ropke et al., 2005).
Investigating the possible underlying mechanism of the prevention of photoaging by P. umbellatum, Ropke et al. (2006) looked
at the relationship between the root extract of P. umbellatum and
matrix metalloproteinases (MMP), specifically MMP-2 and MMP-9.
The ethanolic extract was able to inhibit MMP-9 activity in vitro as
well as in vivo. The effect of the extract was stronger than that of
4NC (Ropke et al., 2006). The synthesis of these MMP is upregulated
by the exposure of human skin to UV radiation. Possible application of the gel of the ethanolic extract of the roots can endanger
the existence of the species. Therefore, Almeida et al. (2008) investigated the photostability of the ethanolic extract of the leaves of
P. umbellatum, which contain 30% less 4NC. The outcome was that
the extract is stable under UV-B radiation and inhibits the MMP-2
and MMP-9 activity of hairless mice in vitro. In the USA and other
countries, Barros and Ropke have patented the effects of P. umbellatum on the skin (Anonymous, 2004). Optimization of the emulsion
concerning the appearance, centrifuge stability and permeation has
already been performed (Noriega et al., 2008).
(normally the day when antimalarial activity is evaluated). Intravenously infected animals did not show this effect. The presented
studies show that it is important to consider the particular strain of
Plasmodium falciparum. Andrade-Neto et al. (2007) and Kamanzi
Atindehou et al. (2004) have positive results at very interesting
concentrations using strain K1. On the contrary, Kaou et al. (2008)
consider the dichloromethane, methanol and methanol/water (1/1)
extracts (aerial parts) as having no activity against the chloroquineresistant strain W2 of P. falciparum. A comparable finding is given
by Bidla et al. (2004) concerning the chloroquine-sensitive F32
strain. Unfortunately, the promising result of the active principle,
4-nerolidylcatechol, concerning the chloroquine, pyrimethamine
and cycloguanil resistant P. falciparum strain K1 (Andrade-Neto et
al., 2007), has not been evaluated so far in vivo.
5.4. Other biological activities
There are several biological activities investigated for P.
umbellatum, which show positive effects at interesting concentrations. These studies demonstrated potential cytotoxic and
anti-tumoral activity (Anonymous, 1976; Brohem et al., 2009;
Kamanzi Atindehou et al., 2004; Sacoman et al., 2008; Werka et
al., 2007), antibacterial activity (Isobe et al., 2002), antileishmanial
activity (Braga et al., 2007) and antitrypanosomal activity (Kamanzi
Atindehou et al., 2004). These studies are still at an initial stage and
need to be reproduced and confirmed. No follow-up research has
been reported so far.
5.5. Pharmacological activities versus traditional medicinal uses
In traditional medical systems P. umbellatum covers a wide
range of medicinal uses (Table 1). Comparing these uses with the
existing pharmacological literature (Table 4) shows us that the
majority of the traditional uses lack a pharmacological basis. Some
traditional uses are being investigated, like malaria, which caught
the interest of several authors (see Section 5.3), and vaginal flow
(see Section 5.1). Analgesic and anti-inflammatory activity has been
shown for the water and water–ethanolic extract of P. umbellatum.
However, these effects are registered at relatively high concentrations. The traditional uses with consensus for P. umbellatum are
kidney, diuretic, stomachache and wounds. Also, skin affections are
mentioned in many countries. Up to now, pharmacological experiments directly dealing with these traditional uses have not been
performed. The proposed hypothesis – the same (consensus) uses
of a plant in different cultures should have a scientific basis – has
not been confirmed. However, in the case of wounds (see Section
5.3), there is indirect proof for this hypothesis. It would be challenging to see if these claimed traditional uses with consensus indeed
have a pharmacological justification. One can argue that the world
is not waiting for a new diuretic, but validating this broadly diffused medicinal use will be important for the incorporation of P.
umbellatum as a diuretic in Primary Health Care in many countries.
5.3. Antimalarial activity
6. Toxicology
Several studies have been performed on the antiplasmodial
activity of P. umbellatum. The ethanolic extract of the leaves, applied
orally as well as subcutaneously in mice, has antimalarial activity against Plasmodium berghei (Amorim et al., 1988). However,
Ferreira-da-Cruz et al. (2000) found that mice infected intraperitoneally with P. berghei Pasteur is not a good test system to detect
the antiplasmodial activity. They discovered a ‘slow’ and ‘fast’ pattern of parasitemia. Some of the infected animals have a normal
(fast) pattern, in which parasitemia increases quickly from the day
of infection, and part of the animals have a low pattern, in which
the parasitemia only starts to increase at day four of the infection
Applied orally to mice, the ethanolic extract (70%, conc.:
500–2000 mg/kg) of the aerial parts did not produce any deaths
during the 72-h period in the acute toxicity test, which means
a LD50 higher than 2.0 g/kg (Perazzo et al., 2005). However, the
dichloromethane extract of the aerial parts, given intraperitoneally,
resulted in a LD50 of 533.71 mg/kg. The highest applied dose of
1000 mg/kg produced death (Sacoman et al., 2008). A water suspension of the dried root ethanolic extract was given, via catheter,
to rats in a concentration of 1, 2 and 5 g/kg. For 14 days the rats
were observed. No deaths or signs of intoxication were registered. Subchronic toxicity was determined by giving the rats, via
C.M.F.B. Roersch / Journal of Ethnopharmacology 131 (2010) 522–537
533
Table 4
Biological and pharmacological activities (in vitro and in vivo) of P. umbellatum extracts and pure compounds.
Extract/compound
ANTIBACTERIAL ACTIVITY
N-Benzoylmescaline (conc. 2.5 g/ml)
Essential oil (leaf, conc. 100 g/ml)
ANTIFUNGAL ACTIVITY:
Methanol extract of the leaves (conc.
100 mg/ml)
Piperumbellactam D (conc. 200 g/ml or
0.68 M)
N-hydroxyaristolam II (conc. 200 g/ml or
0.71 M)
4-Nerolidylcatechol (4NC) (conc. 200 g/ml or
0.64 M)
ANTIOXIDANT ACTIVITY
Methanolic extract of the roots
4-Nerolidylcatechol (4NC)
Ethanolic extracts of the root, stem and leaves
Methanolic extract and methanolic extract
with HCl of the leaves
Methanolic extract of the leaves
Piperumbellactam A
Piperumbellactam B
Piperumbellactam C
N-p-Coumaroyl tyramine (conc. 10 M)
CYTOTOXIC ACTIVITY
Water–ethanol extract of the stem
Dichloromethane extract of the aerial parts
Dichloromethane extract of the aerial parts
(conc. 100, 200, 300, and 400 mg/ml)
4-Nerolidylcatechol
Ethanolic extract of the stem and leaf
Essential oil (leaf, conc. 100 g/ml)
ANTIMALARIAL ACTIVITY
Ethanolic extract of the stem and leaf
Dichloromethane extract of aerial parts
Methanol extract of aerial parts
Methanol/water (1/1) extracts of aerial parts
4-Nerolidylcatechol
Chloroform/methanol extract (1/1) of the
leaves
Biological and pharmacological activity
References
In vitro antibacterial activity against Helicobacter pylori
Inhibition of the growth of Bacillus cereus (MIC = 1250 g/ml) and
Staphylococcus aureus (MIC = 156 g/ml)
Isobe et al. (2002)
Werka et al. (2007)
In vitro inhibitory activity against Candida albicans (MIC = 2.50
mg/ml) and C. neoformans (MIC = 625 g/ml) using the agar-well
diffusion assay with amphotericin B as positive control
Inhibition of radial growth of Trichophyton longifusus (73%),
Candida albicans (101%), Aspergillus favus (35%), Microsporum canis
(90%), Fusarium solani (63%) and Candida glabrata (101%) using the
agar tube dilution method (with miconazole and amphotericin B
as controls)
Inhibition of radial growth of Trichophyton longifusus (89%),
Candida albicans (108%), Aspergillus favus (51%), Microsporum canis
(87%), Fusarium solani (65%) and Candida glabrata (99%) using the
agar tube dilution method (with miconazole and amphotericin B
as controls)
Inhibition of radial growth of Trichophyton longifusus (50%),
Candida albicans (55%), Aspergillus favus (10%), Microsporum canis
(50%), Fusarium solani (49%) and Candida glabrata (78%) using the
agar tube dilution method (with miconazole and amphotericin B
as controls)
Braga et al. (2007)
In vitro antioxidant activity measured as total reactive antioxidant
potential (TRAP) and the total antioxidant reactivity (TAR) using
the luminol-enhanced chemiluminescence by peroxyl radicals
method and catechin as a standard (extract/4NC/catechin: TRAP
97.2 ± 10.8 M/33.6 ± 23.0 M/20.4 ± 9.0 M; TAR
0.6 ± 0.1 M/4.9 ± 0.2 M/3.1 ± 1.0. IC50 values were: 13.3 g/ml
(extract) and 4.9 g/ml (4NC))
In vitro inhibition of free radical-mediated DNA-sugar damage
induced by the presence of Fe(II) salts (extract/4NC: IC50 : 21 and
8 g/ml)
In vitro antioxidant activity in brain tissue auto-oxidation
evaluated by using malondialdehyde (MDA) and
chemiluminescence (CL). Q1/2 of the ethanolic extracts of the roots,
stems and leaves were 4.0, 19.3 and 38.5 g/ml, respectively
In vitro antioxidant activity in the Folin–Ciocalteu reagent (Folin)
and the ferric reducing antioxidant power (FRAP) method
In vitro scavenging effect on DPPH (1,1-diphenyl-2-picrylhydrazyl)
(79.8–89.9% at a dose level of 10 mg/ml), nitric oxide (85.1–97.9%,
dose level 10 mg/ml), the superoxide radical (47.1–51.6%, dose
level 8 mg/ml) and the hydroxyl radical (57–76.1%, dose level
5 mg/ml) and a 0.4–0.6 reducing power and a 88.3–93.9% metal
chelating activity at a dose level of 8 mg/ml
In vitro inhibitory activity in the DPPH radical scavenging assay
with caffeic acid as positive control (13.1%, 67.8%, 86.4% and 61.8%,
respectively, at a conc. of 10 M)
Desmarchelier et al. (1997)
In vitro cytotoxic activity against CA-9KB
In vitro antiproliferative activity against the human cancer cell
lines MCF-7, NCI-ADR/RES, OVCAR-3, PC-3, HT-29, NCI-H460,
786-O, UACC-62, K-56 (total growth inhibition, TGI, between 4.0
and 9.5 g/ml) and the leukemia cell line K-652 (TGI = 1.55 g/ml)
In vivo anti-tumor activity by intraperitoneal administration,
evaluated with the Ehrlich ascites tumor model in mice
In vitro cytotoxic activity against melanoma cell lines SK-Mel-28,
SK-Mel-103 and SK-Mel-147 (IC50 = 20–40 M)
In vitro cytotoxic activity against L-6 rat skeletal myoblast cells
(IC50 = 61.3 g/ml)
In vitro cytotoxic activity against Hep G2 (hepatocellular
carcinoma) (10% kill); no activity (0% kill) found against MCF-7 and
PC-3 human tumor cells
Anonymous (1976)
Sacoman et al. (2008)
In vitro antiplasmodial activity against Plasmodium falciparum
(strain K1, resistant to chloroquine and pyrimethamine)
(IC50 = 3.74 g/ml)
In vitro antimalarial activity against the chloroquine-resistant
strain W2 of Plasmodium falciparum (IC50 = >50, >50 and 50 g/ml,
respectively)
In vitro activity against the chloroquine, pyrimethamine and
cycloguanil resistant P. falciparum strain K1 (IC50 = 0.67 nM)
In vitro inhibition of chloroquine-sensitive F32 strain of P.
falciparum (70% inhibition at 40 g/ml)
Kamanzi Atindehou et al.
(2004)
Tabopda et al. (2008)
Tabopda et al. (2008)
Tabopda et al. (2008)
Barros et al. (1996)
Agbor et al. (2005)
Agbor et al. (2007)
Tabopda et al. (2008)
Sacoman et al. (2008)
Brohem et al. (2009)
Kamanzi Atindehou et al.
(2004)
Werka et al. (2007)
Kaou et al. (2008)
Andrade-Neto et al. (2007)
Bidla et al. (2004)
534
C.M.F.B. Roersch / Journal of Ethnopharmacology 131 (2010) 522–537
Table 4 (Continued )
Extract/compound
Biological and pharmacological activity
References
Ethanolic extract of the leaves
In vivo dose-dependent reduction in parasitemia (orally as well as
subcutaneously) in mice (conc. orally 250 and 1250 mg/ml;
subcutaneously 100 and 500 mg/ml)
Amorim et al. (1988)
In vivo analgesic effect in rats by intraperitoneal administration
(no concentrations given, abstract only)
Significant in vivo analgesic activity in rats by granulomatous
tissue induction and the writhing test by a daily oral
administration of 550 mg/kg extract
Bioka and Abena (1990)
ANALGESIC ACTIVITY
Water extract of the leaves
Water–ethanolic extract of the leaves
ANTIINFLAMMATORY ACTIVITY
Water–ethanolic extract of the aerial parts
OTHER PHARMACOLOGICAL ACTIVITIES
4-Nerolidylcatechol
4-Nerolidylcatechol
Water extract of the leaves
Essential oil of the leaves
Water extract of the leaves
Piperumbellactam A
Piperumbellactam B
Piperumbellactam C
Ethanolic extract of the root
Ethanolic extract of the root in gel containing
0.1% 4-nerolidylcatechol
Ethanolic extract of the root in gel containing
0.1% 4-nerolidylcatechol
Ethanolic extract of the root
Ethanolic extract of the root in gel containing
0.1% 4-nerolidylcatechol
Methanolic extract of the leaves
Ethanolic extract of the stem and leaf
Water extract of the leaves
Perazzo et al. (2005)
Significant in vivo anti-inflammatory activity by using
carrageenan-induced rat paw edema (ED50 = 550 mg/kg, orally)
Perazzo et al. (2005)
In vitro inhibition of myotoxin I, a phospholipase A2 of Bothrops
asper (IC50 = 987 M)
Significant in vivo reduction of myotoxic and edema-inducing
activities produced by Bothrops myotoxins in mice (preincubation
with 100 or 200 g 4NC)
Anti-crustacean activity (Artemia salina) (LD50 = 122.5 mg/ml)
Anti-crustacean activity (Artemia salina) (LD50 = 29.1 g/ml)
No significant inhibition in vitro of ␣- and -glycosidase (no conc.
given)
In vitro activity against ␣-glycosidase (IC50 = 98.07, 43.80 and
29.64 M, respectively)
Núñez et al. (2005)
In vitro dose-related reduction of MMP-2, pro-MMP-2 and MMP-9
in the cornea of the rabbit (dose 50, 100, 250 g/ml) (matrix
metalloproteinases, MMP, are related to the failure of the cornea to
re-epithelialize after injury)
In vivo prevention (100%) of ␣-tocopherol depletion in the skin of
hairless mice treated with P. umbellatum root extract gel after
UV-irradiation
In vivo photoprotective effect of P. umbellatum root extract gel
against UV irradiation-induced chronic skin damage (skin
wrinkling) in hairless mice
Strong in vitro inhibitory effect of P. umbellatum extract (100 g/ml
extract containing 7.09 g/ml 4NC) on MMP-2 and MMP-9
measured by gelatin zymography
In vivo inhibition of constitutive MMP-9 activity in mice sacrificed
2 h after UVB irradiation as measured by gelatin zymography and
histological analysis
In vitro antileishmanial activity against Leishmania amazonensis
and Leishmania chagasi with amphotericin B as control drug
(IC50 = 39 g/ml and IC50 = >250 g/ml, respectively)
In vitro antitrypanosomal activity against Trypanosoma brucei
rhodesiense (IC50 = 2 g/ml)
Hypothermic and tranquilizing activity; ataxia and reduction of
the spontaneous activity in rats by intraperitoneal administration
(no concentration given; abstract only)
Barros et al. (2007)
catheter, a water suspension of the dried root ethanolic extract
(conc. 500 mg/kg) for 40 days (5 days a week). No signs of intoxication or deaths were registered. The hematological parameters
(conc. hemoglobin, erythrocytes, leukocytes) showed no alteration;
concerning the serum biochemical parameters, the triglycerides
increased 39% in male rats and the AST activity decreased 24% in
female rats; serum proteins decreased in both sexes. There were
no alterations in the liver, spleen, kidneys and heart; also, no mutagenic activity was detected in the bone marrow micronucleus test
(Barros et al., 2005). Lajide et al. (1998) investigated the toxicity of
P. umbellatum to the maize weevil (Sitophilus zeamais Mots.). Maize
grains were treated with the plant powder at the rate of 0, 1, 5 and
10% by weight of maize grains and then infested with 10 adult weevils. P. umbellatum, at the 1% treatment level, gave 100% kill at 28
days of treatment. Chartol (1964) also described an effective action
of P. umbellatum as an insecticide, but of the essential oil from the
leaves.
Andrade et al. (2005) evaluated the mutagenic potential of the
water–ethanolic extract (70%) of the aerial parts. The extract was
given orally to Wistar rats at concentrations of 500, 1000 and
1500 mg/kg. This did not induce an increase in the average number
Núñez et al. (2005)
Hammer and Johns (1993)
Werka et al. (2007)
Hammer and Johns (1993)
Tabopda et al. (2008)
Ropke et al. (2003)
Ropke et al. (2005)
Ropke et al. (2006)
Braga et al. (2007)
Kamanzi Atindehou et al.
(2004)
Bioka and Abena (1990)
of DNA damage in the liver cells and in the micronucleus in the bone
marrow cells. There was, however, a significant increase in DNA
damage in peripheral blood cells. In the Salmonella/mammalianmicrosome assay, no mutagenic effect of the ethanolic extract
(plant parts not specified; conc. 50, 100, 250, and 500 g) was
observed (Felzenszwalb et al., 1987). The ethanolic extract of the
roots of P. umbellatum (dosis 50, 100 and 200 mg/kg/day, orally)
did not demonstrate a mutagenic effect in mice using the micronucleus test. On the contrary, there was a protective effect against
genotoxicity induced by cyclophosphamide. The effect of the isolated 4-nerolidylcatechol (dosis 12.5, 25 and 50 mg/kg/day, orally)
was even better (Valadares et al., 2007).
From the above, one may conclude that the different extracts of
P. umbellatum are not toxic and do not possess mutagenic effects,
and even better, show protective qualities. Nevertheless, in the
southwest of the Ivory Coast, in South-East Asia and in South America, Piper umbellatum is applied as a component of an arrow poison
to hunt monkeys and wild pigs. In Colombia, the scraped, boiled
bark of the lower part of the stem and root is used for this purpose (Domis and Oyen, 2008; Schmelzer, 2001; Schultes, 1980 in
Hammer and Johns, 1993; Schultes and Raffauf, 1990). This finding
C.M.F.B. Roersch / Journal of Ethnopharmacology 131 (2010) 522–537
and the fact that the pulverized plant and the essential oil of the leaf
have insecticidal activity make it necessary to do more research on
the toxicity of P. umbellatum.
7. Conclusions
P. umbellatum is a widely appreciated medicinal plant and has
cross–cultural uses in three continents. Traditional uses, on which
major consensus exists, are kidney/diuretic, wounds and stomachache. Indirectly, the traditional use for wounds is supported.
This interesting fact is the result of the demonstrated antioxidant
effect of the plant and the role antioxidants play in wound healing. In Brazil, the antioxidant activity has been the starting point
in the study of the effect of the root extract of P. umbellatum on
skin damage produced by UV radiation. The outcome of this study
is the formulation of a skin-protecting agent against UV radiation.
These findings have been patented and the development of a cosmetic product is in progress. Critical assessment of the biological
and pharmacological activities has shown that P. umbellatum may
have interesting clinical applications, but there is still a tremendous
distance between the existing pharmacological knowledge and any
clinical application. Most experiments are at an initial, in vitro stage.
There is an enormous shortage of in vivo studies, not to mention
clinical studies. Moreover, the existing pharmacological data show
differences in the activity of the extracts and the supposedly active
compound, 4-nerolidylcatechol. The recently discovered bioactive
constituents, piperumbellactams, indicate that much work still has
to be done on the phytochemistry of the species. The presented
differences in the contents of the essential oils of P. umbellatum
make it very clear that for further comparison of experimental data,
the chemical identification or the use of fingerprints in the extracts
must be taken into account. The incongruent information about the
toxicity of the species urges more research. This review indicates
that P. umbellatum has a potential as a therapeutic agent, but the
road to any clinical application is still very long.
Acknowledgments
I would like to thank the following persons for their support and their critical and constructive comments and corrections:
Michael Heinrich, University of London; Rob Verpoorte, University
of Leiden; Brent Berlin, University of Georgia; Norman Farnsworth,
University of Illinois at Chicago; Paul Maas and Tinde van Andel,
University of Wageningen; Arnaldo Bandoni, University of Buenos
Aires; Eduardo Garcia and Amelia Parra, UNPHU, Santo Domingo;
and Jacques van Rossum, University of Nijmegen. Also, I’m indebted
to my friend Jan Adriaanse for revising the English text and to
Juan Newton Ovalles Mella for drawing the chemical structures.
The Foundation of Pharmacological Systems Dynamics, the Pan
American Health Organization and the Academy of Sciences of the
Dominican Republic are acknowledged for their financial support.
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