Rev Bras Farma; 24(2014): 110-115

Original article

Are ethnopharmacological surveys useful for the discovery

and development of drugs from medicinal plants?

Ulysses Paulino Albuquerquea,*, Patrícia Muniz de Medeirosa,b, Marcelo Alves Ramosa,c,

Washington Soares Ferreira Júniora, André Luiz Borba Nascimentoa,
Wendy Marisol Torres Avileza, Joabe Gomes de Meloa
aLaboratóriode Etnobiologia Aplicada e Teórica, Departamento de Biologia, Universidade Federal Rural de Pernambuco, Recife, PE, Brazil
bInstituto
de Ciências Biológicas e Desenvolvimento Sustentável, Universidade Federal do Oeste da Bahia, Barreiras, BA, Brazil
cDepartamento de Ciências Biológicas, Universidade de Pernambuco, Campus Mata Norte, Nazaré da Mata, PE, Brazil

ARTICLE INFO A B S T R A C T

Article history: Ethnopharmacological and ethnobotanical approaches are described in the literature
Received 15 November 2013 as efficient to identify plants of interest for phytochemical and pharmacological
Accepted 4 April 2014 studies. In the present work, we reflect on the quality of the data collected in ethno-
directed studies. In accordance to the problems identified in published studies, and
Keywords: their theoretical and methodological underpinnings, we believe that these studies are
Ethnobotany poorly suited to contribute to the advancement of research aimed at the development
Ethnodirected of novel drugs.
Ethnomedicine © 2014 Sociedade Brasileira de Farmacognosia. Published by Elsevier Editora Ltda. All rights reserved.
Traditional uses

Introduction and Hanazaki, 2006; 2009) both from a pharmacological point

of view and in the data collection of ethnopharmacological
Despite the richness of the ethnopharmacological surveys surveys. From the pharmacological side, many of the problems
performed worldwide, and the increase in knowledge of the are associated with limitations in the methods employed and
use of natural resources by local communities (Albuquerque et misinterpretations of the bioassay results (Houghton et al.,
al., 2012), particularly in Brazil, many of the collected data were 2007; Gertsch, 2009). Nevertheless, in order to characterize the
found not to be sufficiently sound for bioprospecting purposes. scenario we have to consider the affirmation of Gertsch (2009),
In fact, the ethnopharmacological/ethnobotanical approach which states that:
has been progressively losing its appeal as a tool for systematic “(…) in the last 20 years few significant discoveries have been
identification of novel pharmaceutical drugs because this made. This may in part be based on the fact that the many of most
approach has failed to locate new species that could represent relevant plant constituents, including the psychoactive, poisonous,
interesting candidates for further phytochemical and and antitumor natural products, have already been found and we
pharmacological studies (Gertsch, 2009). The reasons for this have to work harder to find yet another molecule that will change
failure include the poor quality of many studies (Albuquerque the world”.

* Corresponding author.
E-mail: [email protected] (U.P. Albuquerque).
0102-695X/$ - see front matter © 2014 Sociedade Brasileira de Farmacognosia. Published by Elsevier Editora Ltda. All rights reserved.
http://dx.doi.org/10.1016/j.bjp.2014.04.003
 Ulysses P. Albuquerque et al. / Rev Bras Farmacogn 24(2014): 110-115 111

In ethnopharmacological surveys, the problems include plants selected using the ethnodirected approach elicited such
inadequate design for data collection, and the misinterpretation properties, while only 42% of the randomly selected plants did.
of the role medicinal plants play in the medical systems of Similarly, Slish et al. (1999) found that four out of 31 plants
local and indigenous communities (Etkin, 1993; Moerman, selected in Belize using the ethnobotanical approach exhibited
2007; Albuquerque and Hanazaki, 2006; 2009). For instance, vascular smooth muscle relaxant activity, while none among
our current database relative to the local uses of the the 32 randomly collected ones exhibited this property.
Brazilian medicinal flora is quite large, but it exhibits various However, the interpretation of the results might lead to
methodological biases that limit our power of interpretation, divergent conclusions on the efficiency of the ethnodirected
as shown by Medeiros et al. (2013a,b). Furthermore, other approach as an indicator of promising plants. For instance,
authors have mentioned the fragility of taxonomic information Khafagi and Dewedar (2000) found that the random approach
for the species studied in ethnopharmacological studies led to the identification of a larger percentage of species
(Bennett and Balick, 2014; Rivera et al., 2014). Considering the with strong antimicrobial activity (13.9% versus 8.3%)
problems mentioned, the present manuscript focuses on issues even though the ethnobotanical approach allowed for the
associated with ethnobotanical/ethnopharmacological data identification of a larger number of plants with antimicrobial
collection of medicinal plants, a topic that has been neglected activity. Thus, one of the lessons we could draw from this
in the ethnopharmacological literature (Etkin, 1993; Reyes- example is that, in some cases, finding a small number of
García, 2010). plants that exhibit a property of interest to a high degree
One should bear in mind that not all records resulting from might be more relevant than finding a larger number of
ethnopharmacological surveys of medicinal plants can be plants with lower levels of activity. Therefore, even in cases
validated from the medical point of view for several reasons: in which the ethnopharmacological approach seems to
1. Data collection does not take into consideration the full stand out, our enthusiasm might lead us to reach unsound
scope of the particularities of the local medical systems; 2. conclusions regarding its actual relevance for the search of
Records include a maladaptive culture trait (i.e., therapeutic new drugs. Case et al. (2006) reported on the limitations of the
indications that do not seem to be biologically effective); ethnopharmacological approach in their study on drugs used
and 3. Records include traits exclusively adapted to the for the treatment of respiratory diseases in Manus province,
studied population. Therefore, to promote a debate on the New Guinea. These authors selected the informant consensus
ethnopharmacological/ethnobotanical approach with respect model to identify the plants with potential pharmacological
to bioprospecting, henceforth designated as ethnodirected, the activity, but found that their underlying assumptions were
present article discusses the main weak points of this approach inadequate to predict antimycobacterial activity. Hence, they
and possible alternatives to overcome its limitations, based warn that ethnodirected approaches should be considered
on experiences from our research group. The topics discussed limited while wider-scoped studies are needed to elucidate
here include sampling issues, the selection of plants relevant their relevance or incompatibility.
for bioprospecting based on their popularity and versatility, Although the results from an ethnodirected approach will
and the omission of information indispensable for efficiently overlap with those of a random approach, studies indicate
testing the plants. that there is no full agreement between the two methods in
In this manuscript we are do not consider that some cases. Examples can be found in the search for novel
bioprospecting and ethnopharmacology have the same anticancer agents. Spjut (2005) reported that active species
meaning, but rather we are critically reflecting on the direction were detected more frequently (1.4- to 2.6-fold greater rate)
commonly adopted by ethnopharmacological studies that seek from the group of medicinal and poisonous plants in relation
to increase knowledge for the discovery of new drugs from to a plant species screened at random. Gyllenhaal et al. (2012)
natural products. The following considerations aim to lead to found that for many cancer cell lines, the random approach
a reflection on the tools that are currently used by researchers returned better results than the ethnomedical selection
who explicitly aim to collaborate on the above-mentioned approach; as occurred with MCF-7 (human breast cancer) for
issues. which the random approach success rate was higher than the
ethnomedical. The authors relativize their findings by arguing
that the results could be due to the much higher sampling for
Efficiency of the ethnodirected approach random collections. However, according to the authors:
“The overall analysis suggests that plants collected based on
With respect to the search for new drugs, some studies have ethnomedical use may in fact have a somewhat higher rate of
compared ethnodirected to other approaches, the random positive bioassays on a per-species or per sample basis, although
approach in particular, which consists of randomly collecting a portion of these assay results may be due to ubiquitous bioactive
plants for phytochemical and pharmacological screening compounds. Ethnomedical collections in general may nevertheless
(Balick and Cox, 1996; Khafagi and Dewedar, 2000; Oliveira play a useful role in drug discovery programs due to this elevated
et al., 2011; Slish et al., 1999; see also Cragg and Newman, rate of bioactivity”.
2003; 2005). In several instances the results of ethnodirected In the last two decades, few significant discoveries have
investigation are best compared to a random search for plants been made in the field of ethnopharmacology (Gertsch, 2009).
for specific therapeutic purposes. Khafagi and Dewedar (2000) Some candidate compounds identified by the bioprospecting
investigated plants with antimicrobial activity that grow research-based ethnomedical approach, as developed by
spontaneously in Sinai (Egypt) and found that 83% of the Shaman Pharmaceuticals, have failed, which leads to the
112 Ulysses P. Albuquerque et al. / Rev Bras Farmacogn 24(2014): 110-115

suggestion that an ethnodirected approach is not feasible for the Camou-Guerrero et al., 2008). In such cases, the social actors
development of novel drugs (Clapp and Crook, 2002). By contrast, who provide us information ought to be accurately identified
the random approach has made effective contributions to the to increase the success of selecting plants for bioprospecting
development of drugs, many of which are still available for the purposes. For instance, investigators who focus on gender and
treatment of various diseases. One example is the search for new age tend to emphasize the role of women and elders because
anticancer drugs conducted by the National Cancer Institute they are considered to possess greater knowledge on medicinal
(NCI) of the United States. They employed the random approach plants. According to such authors, the reason that women
in a program developed in the 1960s, resulting in several agents possess such knowledge is attributed to their role in home
of clinical relevance such as “taxanes and camptothecins, but their and family care, and in the case of the elderly the reason is
development into clinically active agents spanned a period of some attributed to their longer interaction with the environment
30 years, from the early 1960s to the 1990s” (Cragg and Newman, (Begossi et al., 2002; Voeks and Leony, 2004; Silva et al., 2011).
2005). Between 1960 and 1982 the NCI investigated about 35,000 Such patterns must not be misinterpreted and then be used
plants before the program was suspended (Beutler et al., 2012). as criteria for informant selection in later studies. Indeed,
According to Cragg and Newman (2005): some authors have shown that the “stock of knowledge” of
“This plant collection program was terminated in 1982, but the individuals from different age ranges might differ and that the
development of new screening technologies led to the revival of knowledge of older individuals might actually be in decline
collections of plants and other organisms in 1986, with a focus on (Silva et al., 2011). As a consequence, the assumption that older
the tropical and sub-tropical regions of the world”. individuals are systematically better “informants” for studies
The examples described above raise a question: why of medicinal plants might be mistaken because people appear
do scientists still assert so strongly the benefits of the to employ different repertoires of medicinal plants according
ethnodirected approach versus the random one when its to their age.
application in practice does not lead to significant advances As regards to gender, some studies, such as the one
in the development of particular drugs? Why do they keep conducted by Voeks and Leony (2004) in Brazilian rural
on conducting studies aimed at making lists of species and communities, have emphasized the role of women because
therapeutic indications? We cannot give definite answers to they are considered to possess greater knowledge of medicinal
these questions but we hypothesize that the ethnodirected resources compared with men. However, other studies, such
approach is perhaps only useful for particular types of diseases. as the ones by Giraldi and Hanazaki (2010) and Poderoso et
Only well-conducted and rigorous ethnopharmacological/ al. (2012), conducted in communities in Southeastern Brazil,
ethnobotanical studies might clarify these issues. have shown that such differences might not occur. Authors
who have found differences suggest that they are associated
with the role women play as homemakers, which place them
Influence of sampling and informant selection in charge of the family’s basic healthcare, while men focus on
other activities.
Ethnodirected studies of medicinal plants quite often exhibit Based on the roles the various social actors play and
sampling problems causing bias in their results. During the their knowledge of health care, we formulated the following
review of studies conducted in Brazil, Medeiros (2012) found suggestions for sample selection to optimize bioprospecting
that most of them had patent sampling flaws, the most strategies: 1. Researchers should clearly establish the goals
frequent being the following: 1. lack of information on the they aim to attain, e.g., “Do I want to study one single and well-
universe (U) or sample (N) on which the survey of the human defined therapeutic activity, or the full range of knowledge of the
communities was grounded; and 2. lack of information on the local medical system?”; 2. Consideration of age, gender and social
U or N of a specific group (e.g., folk healers), in intentional function of individuals particular relevance in the selection
samples based on specialists from the studied communities. of the informants who might effectively supply the expected
Therefore, studies seeking to investigate the knowledge information; and 3. Although thorough knowledge of the
possessed by “local specialists” (e.g., folk healers) must existing international literature on the subject is necessary
establish with full certainty that they are truly dealing with to give support to the study design, investigators should be
such. Contrariwise, when there are no well-defined criteria careful not to restrict the sample as previous patterns detected
for intentional selection the results might not reflect the in the literature. At times, time and financial restrictions
investigators’ desires. Similarly, studies that rely on the induce us to look for faster strategies without taking into
informants’ consensus as an indicator of the most significant consideration that such behavior might impair the power of
or popular species must take care to ensure an appropriate inference for the data.
application of that model and select truly representative
samples of the community. Conversely, non-representative
samples might point certain plants as the most popular or Searching for the most popular plants as a
versatile therapeutic indications when they are actually not. bioprospecting tool
In addition, many studies have shown that the local
knowledge on medicinal plants is not homogeneous, but rather Most ethnodirected studies identify the plants mentioned
it varies among the actors of a local community according by the largest number of individuals, the most versatile
to their age, gender, income, social role and intra-cultural plants (the ones with many potential therapeutic uses), or
acculturation differences (Voeks and Leony, 2004; Voeks, 2007; a combination of both criteria as the most interesting for
 Ulysses P. Albuquerque et al. / Rev Bras Farmacogn 24(2014): 110-115 113

bioprospecting purposes. The ethnobiological literature of the plant in the local medical system might have always
describes a wide variety of quantitative indicators to establish been low (restricted to a few families or individuals); or e, the
such indications (Medeiros et al., 2011), which are often used; low availability or the difficulty in accessing the plant in the
however, awareness of their limitations is appropriate. The environment.
first criterion has proven to be inadequate in some studies As a result, rarely mentioned plants might actually be
seeking to confirm the pharmacological activity of certain highly valuable from the bioprospecting perspective because
plants based on the traditional knowledge, as in the above- they bear the additional advantage of being less well-studied
mentionedstudy by Case et al. (2006). The authors used the and could serve as the basis for further systematic quests for
informants’ consensus to select species from New Guinea medicinal products. There is a necessity to test differences
of potential pharmacological interest for the treatment of in the pharmacological activity between the most and least
respiratory diseases; however, they did not find such activity popular plants.
in the plants with highest levels of consensus. Many of the
quantitative indicators suggested by the scientific literature
were proposed with the purpose of revealing plants important Problems related to data collection and recording
for a given culture. The authors that applied those indices therapeutic indications
to indicate potential species for bioprospecting efforts were
based on the idea that a plant relevant for a culture, with At times, testing of the biological activity of medicinal plants
great cultural consensus is more likely to present biological based on ethnodirected data is hindered by the lack of detail of
activities. Furthermore, most of these indices do not consider the information gathered from local communities. Superficial
the particularities of the plants used in mixtures. data collection and interpretation is a serious mistake that
The expectation in the use of the above-mentioned criteria one finds reproduced in many published studies. The lack of
is usually to obtain the same lists of plants as reported in attention usually paid to therapeutic indications is noteworthy
previous studies, oftenly highly popular exotic or native plants because it has a negative impact on the success of approaches
with wide local distribution. For that reason, paying attention requiring accurate and precise information. Many studies do
to plants that are mentioned less frequently might be relevant not distinguish among the plants that serve to cure a disease,
for bioprospecting because low popularity is not a synonym the ones that relieve its symptoms, and the ones that are
for lack of efficacy. The high presence and importance of a able to prevent its occurrence. That distinction, however, has
plant in a local medical system is not necessarily linked to its paramount importance in bioprospecting and thus should
pharmacological effect, but can be due several other factors. receive more attention.
Moerman (2007) discusses that a plant used for treatment Some studies have demonstrated the relevance of
can be widespread in a community and may not contain investigating the concept of disease held by the community
any biologically active compounds. Instead, the symbolic (Beiersmann et al., 2007; Reyes-García, 2010). The choice of
meaning of the treatment within the culture can alter the therapies by human groups is related to how they recognize
patient’s physiology, acting similar to a “placebo,” and appears and classify diseases (Reyes-García, 2010), so an accurate
effective because of the cultural validation and the local belief understanding of those features is key for the planning of
in its effectiveness. In addition, ecological factors, such as future bioprospecting strategies. One simple method to
environmental and seasonal availability, can influence the investigate the local perception of a given disease is to ask the
importance of medicinal plants. For example, Molares and informants how it is recognized. This strategy identifies the
Ladio (2009) mentioned that species located geographically symptoms that are directly associated with the disease. For
closer to a community may be used more oftenly, imparting instance, the activity of a plant mentioned in the treatment
greater importance to this group of plants. of various diseases mainly associated with the symptom pain
The data on less popular plants, inadequately disseminated might reduce the release of chemical mediators related to the
within a social group for several reasons, might provide production of pain.
valuable information for bioprospecting strategies. For More than a few studies have merely recorded the medicinal
instance, Reyes-García et al. (2008) observed that the low properties of plants without investigating the local notions of
prestige of a given community member providing observations disease, which might be widely divergent from Western ideas.
about plant species might directly interfere with the reception This situation is illustrated by the study by Ferreira Júnior et
and cultural acceptance of that information by other al. (2011), which investigated the plants from the Brazilian
community members. As a consequence, the dissemination of Caatinga used to treat inflammation. Although inflammation
some information might remain restricted due to of forces that is considered as uniform in the ethnobotanical literature, the
hinder its circulation (e.g., family secrets) or block its reception authors recorded 37 different categories of that condition as
(e.g., low prestige of the information source). perceived by the community, and characterized it as a result
On this view, such plants might be rarely mentioned for of 26 different symptoms. Interestingly, the plants used
reasons like: a, the plant might have recently entered the for the treatment of the various categories exhibited broad
local medical system (recent introduction); b, the plant is differences, thus showing that inflammation could not be
being excluded from the local medical system; c, the plant considered a homogeneous “category” and that the studies
is indicated for the treatment of diseases affecting specific might be strongly biased. Ferreira Júnior et al. (2011) also found
social actors (e.g., age- or gender-specific diseases) and thus, that some conditions identified as “inflammation” by the
it is not known by the overall population; d, the popularity investigated community were not thus understood in Western
114 Ulysses P. Albuquerque et al. / Rev Bras Farmacogn 24(2014): 110-115

conventional medicine. That finding makes the elucidation of (Albuquerque, 2013) on recent years. Therefore, a major lesson
local notions of disease even more relevant. Similarly, Oliveira to be learned from the discussion above is that researchers
et al. (2011) paid attention to local notions of disease. While must reconsider projects aiming at a mere elaboration of
investigating the plants used by Quilombola communities lists of species and their therapeutic indications. Such lists,
in the state of Pará (Northern Brazil) for the treatment of and the various sources of bias they include, are increasingly
respiratory diseases, the authors found that tuberculosis was showing their lack of relevance for bioprospecting purposes.
called “enfeeblement” and so the identification of the local The limitations pointed out in this study are not inherent to
notions had direct implications for ethnodirected studies. ethnopharmacological research, but rather happen due to the
Beiersmann et al. (2007) studied the plants used to treat lack of knowledge on the chosen tools. Every single scientific
malaria in seven villages in Burkina Faso and identified four method has limitations, which leaves the researchers the
variations of disease, each one having its particular treatment, responsibility for applying theoretical and practical knowledge
including the use of plants and/or conventional Western to make the most appropriate choices, as well as to draw
therapies. This finding further showed that studies that do not pertinent conclusions
include a thorough understanding of the diseases mentioned
by a given human group are at risk of collecting biased data
and of using the ethnodirected information incorrectly. In this Authors’ contributions
case, the researcher took notice of these differences and as a
result errors were minimized in the process of noting points UPA designed the study. All the authors contributed to critical
of convergence and divergence between local and biomedical reading and writing of the manuscript, and have read the final
systems. manuscript and approved the submission.
The procedures for collecting data on the medicinal plants
at a given site might exert a strong influence on the success of
pharmacological studies. The informants might apply several Conflicts of interest
criteria to the indication or use of a given species for medicinal
purposes, including a variable that is often omitted in studies, The authors declare no conflicts of interest.
the local perception of the efficacy of treatment (Ferreira Júnior
et al., 2011; 2012). The latter might supply valuable hints for
bioprospecting purposes because certain species might be Acknowledgments
preferentially reported as a function of their perceived efficacy.
Therefore, the investigations of these species increase the The authors thank CNPq for the productivity grant given to
odds of success in future studies. In addition, it is also worth UPA and financial support (Proc. 471989/2012-6), and CAPES
investigating the informants’ notion of the efficacious use of for the post-doctoral grant supporting JGM. They also thank
a plant for a given purpose (Etkin, 1988). the anonymous reviewers for their pertinent critics and
It must be considered that the issues we pointed out suggestions.
regarding the misinterpretation of the concepts of illnesses in
other cultures happen mostly on societies whose knowledge
has not still been decoded. One of the reviewers of this article R eferences
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