Journal of Ethnopharmacology 159 (2015) 43–48

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Research paper

Can organoleptic properties explain the differential use of medicinal plants? Evidence from Northeastern Brazil Patrícia Muniz de Medeiros a,n, Bárbara Luzia Santos Pinto a, Viviany Teixeira do Nascimento b a Universidade Federal do Oeste da Bahia, Centro das Ciências Biológicas e da Saúde, Estrada para o Barrocão, s/n, Morada Nobre, 47800-000 Barreiras-BA, Brazil b Universidade do Estado da Bahia, Campus IX. Rodovia BR 242, km 4, s/n, Loteamento Flamengo, 47800-000 Barreiras-BA, Brazil

art ic l e i nf o

a b s t r a c t

Article history: Received 9 September 2014 Received in revised form 30 October 2014 Accepted 1 November 2014 Available online 11 November 2014

Ethnopharmacological relevance: This study examined how people classify plants in terms of their taste and smell, and how those organoleptic properties influence the differential use of medicinal plants for treating different diseases. Methods: We conducted an ethnobotanical survey of household heads in the community of Sucruiu, located in Barreiras, Bahia, Brazil. The head of each family was questioned concerning their knowledge and use of medicinal plants, as well as the therapeutic indications (TIs), taste, and smell of each plant. We then tested for associations between the therapeutic indications and taste attributes of various plants using the Chi-squared test on a contingency table with Monte Carlo simulations. The same analysis was performed for associations between TIs and smell. Results: The study participants provided more details when classifying tastes than when classifying smells. We considered only the most cited TIs and attributes, and found significant associations between both taste and therapeutic indications (p o0.001) and smell and therapeutic indications (p o0.0001). Conclusions: Our results showed that the taste and smell of a plant can influence its differential medicinal use, since plants with certain tastes and smells prevailed in the treatment of distinct diseases. However, our results are valid only for the most popular TIs and organoleptic attributes. & 2014 Elsevier Ireland Ltd. All rights reserved.

Keywords: Ethnomedicine Traditional medicine Medicinal plant selection Brazil

1. Introduction One central interest of ethnobotanical research is to identify factors that influence a plant's selection and differential use by local communities (Medeiros et al., 2013 a, 2013b). Previous investigations have sought to understand whether factors such as a species' availability (Lawrence et al., 2005; Lucena et al., 2012), bioactivity (Omar et al., 2000; Araújo et al., 2008) or organoleptic properties (Leonti et al., 2002; Molares and Ladio, 2009) may explain its popularity and application for treating certain disorders. A plant's taste and smell can play an important role in its selection for medicinal use by local populations, and such attributes are directly associated with the presence of certain secondary plant metabolites. It is possible that some organoleptic attributes act as determinants of plant selection, clues of bioactivity, or serve a mnemonic function (Medeiros et al. 2013a), which

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Corresponding author. Tel.: þ 55 7736143113. E-mail address: [email protected] (P.M. de Medeiros).

http://dx.doi.org/10.1016/j.jep.2014.11.001 0378-8741/& 2014 Elsevier Ireland Ltd. All rights reserved.

enables people to have taste-based and smell-based information that can be used for experimenting and innovating traditional knowledge (Heinrich, 2003; Molares and Ladio, 2008). Some ethnobotanical studies have reported the importance of organoleptic attributes when distinguishing between medicinal and non-medicinal plants (Ankli et al., 1999; Leonti et al., 2002). Furthermore, we believe that the differential use of medicinal plants (use of different plants for distinct purposes) can be explained by attributes such as taste and smell. While previous investigators have found that certain diseases are mostly treated with plants that have specific tastes or smells (Ankli et al., 1999; Leonti et al., 2002; Heinrich, 2003), these reports have been limited to only a few diseases. Our current study examined the association between a plant's taste and smell, and its selection for treatment of a wide variety of diseases, with the goal of determining whether such an association can be generalized or is limited to particular diseases. We hypothesized that a plant's taste and smell influence its selection for treating specific diseases, and examined whether the differential use of medicinal plants be explained by their organoleptic properties.

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2. Methods 2.1. Study area This study was conducted in 2012 in the rural community of Sucruiu (121120 29,0600 S and 451150 24,0300 W), located in the municipality of Barreiras, in the Western region of the state of Bahia, Brazil (Fig. 1). The municipality covers 7859.225 km2 (IBGE, 2010), and has seasonally dry vegetation. Its population of 136,427 inhabitants (IBGE, 2010) and the majority of economic activity are related to agribusiness. Although commercial large-scale agriculture has a substantial presence in Barreiras, it coexists with small-scale agricultural operations in local communities such as Sucruiu. Sucruiu is located 25 km from the nearest urban area, and has 21 households and 38 family chiefs. In terms of ethnicity, Sucruiu is constituted of mixing races, as its inhabitants are descendants of European, African and Indigenous people. Researchers commonly use the terms ‘setanejos’ or ‘cultura sertaneja’ (better translated as backcountry culture) to describe mixed race farming communities from seasonally dry Brazilian areas (Lütkemeier, 2014). However, the ‘sertanejos’ cannot be considered as culturally homogeneous, since differences can be found in their social organization and subsistence activities. Most men in Sucruiu are native to the community, while the women are mostly from neighboring communities, and migrated to Surruiu after marrying Scuruiu men. While the men are mostly dedicated to agricultural activities and the extraction of commercial forest products, women work in commerce, service, agriculture, and/or domestic activities. The community has a Catholic church (main religion in the area) and a public elementary public school. Students seeking higher academic degrees must travel to neighboring communities or the Barreiras urban area. In terms of access to public health, the community does not have a health center; however, health agents from the Barreiras urban area often visit community members.

In term of therapeutic options, the community presents a plural medical system, since traditional and official medicines coexist. Similar to other rural communities in Northeastern Brazil, young natives continuously migrate to urban centers, leading to their decreased numbers in Sucruiu. 2.2. Data collection This study was conducted in accordance with guidelines developed by the National Health Counsel by means of the Research Ethics Committee (Resolution 196/96), and the protocol was approved by that committee (CAAE 07488513.4.0000.5026). The community of Sucruiu was fully informed concerning the goals of this study, and members who agreed to participate were invited to sign a Free and Clarified Consent Term. We interviewed 21 family chiefs (men and women). This number of participants was reached because 17 individuals did not want to participate or were not located even after several attempts. We performed a free-listing of medicinal plants that each individual knew of and/or had used, including the parts utilized, their therapeutic indications, and their attributes of taste and smell. Species cited by the informants were collected and then identified by consultations with specialists and comparisons with herbarium material. The samples were deposited at the herbarium of the Universidade Federal do Oeste da Bahia, and the herbarium of the Universidade do Estado da Bahia (Campus IX). 2.3. Data analysis The relative importance (RI) of each plant was calculated by the method of Bennett and Prance (2000) using the following equation: IR ¼(NTIx/NTIVE) þ(NBSx/NBSVE), where NTIx is the number of therapeutic indications (TIs) for the species x; NTIVE is the number of therapeutic indications for the most versatile species; NBSx is the number of body systems of the species x, and NBSVE is

Fig. 1. Map of the study area emphasizing the state of Bahia, Western region and the municipality of Barreiras.

P.M. de Medeiros et al. / Journal of Ethnopharmacology 159 (2015) 43–48

the number of body systems for the most versatile species. The World Health Organization database was used to classify indications according to their body systems (WHO, 2010). The number of citations for each taste and smell was recorded. A citation was considered to be the ‘Species’-‘TIs’-‘Used part’‘Taste’ link, and the ‘Species’-‘TIs’-‘Used part’-‘Smell’ link. For example, if the interviewee 1 cited the bitter seeds of Pterodon emarginatus Vogel to treat influenza and the same interviewee cited the bitter bark of Pterodon emarginatus to treat influenza, we considered them as two different citations. Therefore, any kind of variation in the species, therapeutic indication, used part, and taste or smell led to a different citation. The Chi-squared test on a contingency table was used to test whether different therapeutic indications were treated with plants having distinct organoleptic properties (‘use’-‘taste’ association or ‘use’-‘smell’ association). As many values on the contingency tables were o5, we adjusted the p-Value with Monte Carlo simulations (10,000 simulations). This test was developed in four different models: (1) considering all cited therapeutic indications and all perceived tastes; (2) considering all cited therapeutic indications and all perceived smells; (3) considering only the therapeutic indications with 410 citations and tastes with 410 citations; (4) considering only the therapeutic indications with 410 citations and smells with 410 citations.

3. Results 3.1. Taste and smell perceptions The study participants provided more details when classifying tastes than when classifying smells. ‘Bitter taste’ had the most citations (36.4%), followed by ‘good taste’ (22%), ‘no taste’ (21.8%), ‘bad taste’ (5.5%), and ‘sweet taste’ (2.7%); all these tastes had 410 citations. Tastes with r10 citations included ‘acid’ and ‘astringent’, as well as comparative tastes (‘orange-like taste’, ‘mint-like taste’, etc). Descriptions of smell were much less diverse, with 41.4% of the citations recorded as ‘no smell’, 31.5% as ‘good smell’, and 7.1% as ‘bad smell’. Furthermore, only those three smell attributes reached 410 citations. Among the less cited attributes were comparative descriptions such as ‘onion-like smell’, ‘mint-like smell’, ‘tick-like smell’, and ‘disease-like smell’. 3.2. More versatile species and their organoleptic attributes The species with the highest RIs were Melissa officinalis L. (2), Cymbopogon citratus (DC.) Stapf (1.92), Amburana cearensis (Allemão) A.C. Sm. (1.92), Aloe vera (L.) Burm. f. (1.58), and Pterodon emarginatus Vogel (1.58). Leaves were the most cited part for Melissa officinalis, Cymbopogon citratus, and Aloe vera, while seeds were most often cited for Amburana cearensis and Pterodon emarginatus.

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Regarding the attribution of tastes to the most cited parts of the most versatile species (Table 1) we found a strong consensus among the interviewee, given that at least 50% of them agreed on the plant's taste for all cases. For the attributes of smell some highly versatile species had 33% of agreement (Table 1). 3.3. Main therapeutic indications The therapeutic indications with 410 citations are listed in Table 2. Three of those indications are associated with inflammatory processes (inflammation in general, throat inflammation, and uterine inflammation). 3.4. Association between therapeutic indications and organoleptic properties When considering all cited therapeutic indications and tastes (model 1), the chi-squared test did not identify an association between TI and taste (χ2 ¼772.4; p 40.05). The same result was found for TI and smell in model 2 (χ2 ¼784.9; p4 0.05). However, when considering only the TIs and tastes with 410 citations (model 3), these two factors showed a significant association (χ2 ¼74.4; po 0.001), and a similar result was shown for TI and smell in model 4 (χ2 ¼58.6; p o0.0001). The association between TI and taste (for the most conspicuous TIs and tastes) was found because while plants classified as bitter dominated for some TIs, plants with good taste and no taste were more commonly used to treat other TIs (Fig. 2). In addition, plants with a ‘good smell’ predominated for some indications, while plants with ‘no smell’ were more often cited for other indications (Fig. 3).

4. Discussion 4.1. Taste and smell perceptions Previous studies have also shown a higher consensus on taste classification compared to smell classification (Molares and Ladio, 2008, 2009). In addition, other studies also gathered more detailed information for taste than for smell, given that attributes of smell are often less numerous than attributes of taste; and/or the attribute ‘no smell’ often has more citations than the attribute ‘no taste’ (Ankli et al., 1999; Leonti et al., 2002; Molares and Ladio, 2008, 2009). While some attributes of taste were well detailed for our study (e.g. bitter), others were restricted to ‘good’ and ‘bad’, with no further information. We believe that these two categories hide other taste attributes, such as sweetness, astringency etc., which are commonly cited in other studies (Ankli et al., 1999; Leonti et al., 2002; Molares and Ladio, 2008, 2009). The citation of plants classified as having both ‘no taste’ and ‘no smell’ in this study and many other investigations can mean two

Table 1 Attributes of taste and smell for the most cited parts of the most versatile (higher Relative Importance) medicinal plants of the community of Sucruiu, Northeasten Brazil. Species Melissa officinalis L. Cymbopogon citratus (DC.) Stapf Amburana cearensis (Allemão) A.C. Sm. Aloe vera (L.) Burm. f. Pterodon emarginatus Vogel

Voucher numbera

Main part

%

Most cited taste

%

Most cited smell

%

b

Leaf Leaf Seed Leaf Seed

100 85.7 88.9 71.4 54.5

Good taste Good taste Bitter taste Bad taste Bitter taste

75 66.7 50 60 83.3

Good smell Good smell Good smell Tick-like smellNo smell No smell

87.5 83.3 50 33 33

BRBA 5.551 BRBA 5.484 b

BRBA 5.621

%¼ percentage of participants that indicated a plant part or organoleptic attribute for a given plant, considering only the participants that mentioned that plant. a b

Voucher numbers for the herbarium of the Universidade Federal do Oeste da Bahia. Plant identification in the field.

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things: (1) all of those plants were odorless and tasteless; (2) the low familiarity with less popular plants having only slight tastes and smells can lead to a lower distinction of their attributes, even if those low-popularity plants are offered for the interviewee to smell and taste at the moment of the interview. In fact, although some popular medicinal plants were considered as tasteless of odorless, most species with these attributes were low-popularity plants. The significance of a bitter taste among medicinal plants found in our study has been mentioned in other investigations (Ankli et al., 1999; Leonti et al., 2002; Heinrich, 2003), and a further discussion of this topic is found in Section 4.5 of this manuscript. However, other studies differed from ours concerning the importance of some attributes. For example, astringent taste was not commonly cited for Sucruiu plants, but was a very relevant attribute in other studies (Ankli et al. 1999; Leonti et al., 2002). 4.2. More versatile species and their organoleptic attributes The species with higher RI values in our study were often highlighted in other investigations conducted in Brazil and even throughout the world (Albuquerque et al., 2007; Negrelle and Fornazzari, 2007; Biswas et al., 2011; Medeiros et al., 2013b). Three of five species with the highest RI values are highly popular exotic species (Melissa officinalis, Cymbopogon citratus and Aloe vera), and two are native to Brazil and often used in the Brazilian Cerrado (Pterodon emarginatus and Amburana cearensis). Only a small number of studies have investigated the influence of organoleptic properties on the differential use of medicinal plants. Therefore, it is difficult to assess whether the tastes and smells as classified in Sucruiu are similarly classified in other geographic areas. Leonti et al. (2002) reported that a species identified as Aloe sp. was classified as having a ‘bad taste’ and a ‘bitter taste’, which partially agrees with the ‘bad taste’ classification for Aloe vera in Sucruiu. Finally, a study conducted in Argentinean Patagonia (Molares and Ladio, 2009) showed that interviewees had 100% agreement Table 2 Therapeutic indications with more than 10 citations in the community of Sucruiu, Northeastern Brazil. Therapeutic indication Indigestion Inflammations in general Influenza Stomachache Cicatrizing Throat inflammation Calming Gastritis Fever Uterine inflammation

No. of citations 57 49 40 20 15 14 13 12 12 11

on both the taste and smell of Melissa officinalis. Our study also showed high agreement on the taste and smell of this species, which supports the high perceptibility of these attributes for this species. 4.3. Main therapeutic indications Results of previous studies have shown certain similarities regarding the main therapeutic indications mentioned in ethnobotanical surveys. One of the most remarkable patterns is the prominence of digestive problems, in terms of citations or the number of plants used to treat these disorders (Felger and Moser, 1974; Heinrich et al., 1998; Novais et al., 2004; Giday et al., 2007; Zone et al., 2007; Jeruto et al., 2008; Giday et al., 2009; Teklehaymanot, 2009; Weckerle et al., 2009; Afroz et al., 2011; Bruschi et al., 2011; Rehecho et al., 2011). Respiratory disorders and inflammation are also prominently mentioned in ethnobotanical surveys (Heinrich et al., 1998; Bradacs et al., 2011; Rehecho et al., 2011; Calvet-Mir et al., 2008). Although inflammation is commonly treated as a homogeneous category in the ethnobotanical literature, it is incorrect to do so. Ferreira-Júnior et al. (2011) studied plants from the Brazilian semiarid region used to treat inflammation, and recorded 37 inflammation categories characterized by 26 different symptoms. Interestingly, they also found several differences concerning the plant-based treatment used for each type of inflammation. This further verified that inflammation could not be considered as a uniform disorder. Our finding that different plant tastes prevailed in distinct inflammation categories also supports the heterogeneity of these indications (e.g., ‘bitter taste’ for general inflammation and uterine inflammation, and ‘no taste’ for throat inflammation). 4.4. Association between therapeutic indications and organoleptic properties Our finding that therapeutic indications and organoleptic properties were only associated in models 3 (only the most cited TIs and tastes) and 4 (only the most cited TIs and smells) have the following implications: (1) taste and smell can only suggest a plant's medicinal use when it is a popular and characteristic taste or smell; (2) taste and smell can only suggest a medicinal plant's use in cases of popular diseases which frequently need treatment. Some associations between organoleptic attributes and therapeutic indications reported in previous studies were also found in our current investigation, and this was especially true concerning attributes of taste. One interesting example can be found in a study conducted by Leonti et al. (2002) among the Mexican Popoluca. Those study participants use a humoral classification in which plants are considered ‘hot’ and ‘cold’; thus hot plants can treat cold diseases and vice-versa (Leonti et al., 2002). Fever is a good example of a hot disease. For the Popoluca, bitter plants are considered as ‘hot’, and are only used to treat cold disorders

Fig. 2. Predominance (in terms of citations) of plant tastes for the most cited therapeutic indications in the community of Sucruiu, Northeastern Brazil (only tastes and indications with more than 10 citations). Therapeutic indications with wider bars were more cited than indications with narrower bars.

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Fig. 3. Predominance (in terms of citations) of plant smells for the most cited therapeutic indications in the community of Sucruiu, Northeastern Brazil (only smells and indications with more than 10 citations). Therapeutic indications with wider bars were more cited than indications with narrower bars.

(Leonti et al. 2002). Although there is no similar humoral classification used in the community of Sucruiu, we did notice that no bitter tasting plants were used to treat fever, while all other common diseases (410 citations) were treated by at least one bitter plant. 4.5. Bitter taste and its medicinal application The prevalence of a bitter taste among the medicinal plants identified in this study was not random. This taste is provided by a wide variety of chemical compounds with the potential to treat several disorders. Bitter taste is common in plants containing terpenoids (Brieskorn, 1990; Ankli et al., 1999), alkaloids (Drewnowski, 1997), and phenols (Brieskorn, 1990). Among the phenols, flavonoids are especially notable for their bitter taste, given that high molecular weight phenols (tannins) are commonly astringent (Noble, 1994; Drewnowski and Gomez-Carneros, 2000). The role which bitter taste plays in medicinal plant selection remains unclear. Studies focusing on food products suggest that this taste is directly related to toxicity, since most toxic compounds found in nature are bitter (Glendinning, 1994). Therefore, many animals (humans included) may have developed an adaptive response so as to reject ingesting bitter tasting resources (Glendinning, 1994; Kurihara et al., 1994). If the hypothesis of bitter-taste rejection as an adaptive response is valid, the preferential consumption of bitter tasting medicinal plants in the community of Sucruiu should be mostly related to cultural learning rather than a genetically fixed recognition mechanism based on sensorial markers. Therefore, bitter taste provides a clue to a plant's medicinal use rather than being a determinant of its use via chemical recognition.

5. Conclusion While the association between organoleptic properties and therapeutic indications cannot be considered valid for the entire medical system, it does apply for particular attributes and clinical indications, and especially for the most popular ones in the Sucruiu medical system. While we believe our results support the validity of this association, they are restricted to the studied community. Therefore, future studies should consider the entire medical system (all tastes, smells and therapeutic indications) in order to better understand the true role of organoleptic properties in the differential use of medicinal plants.

Acknowledgments We thank the community of Sucruiu for their kind reception and participation in this study. We especially thank Justino and

Claudina for their support and friendship. We also thank CNPq (141121/2010-6) for the grant given to the first author.

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Can organoleptic properties explain the differential use of medicinal plants? Evidence from Northeastern Brazil.

This study examined how people classify plants in terms of their taste and smell, and how those organoleptic properties influence the differential use...
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