Ethnobotanical study of antimalarial plants in the middle region of the Negro River, Amazonas, Brazil

Etnobotânica de plantas antimaláricas no médio Rio Negro, Amazonas, Brasil

Bernardo TOMCHINSKY Lin Chau MING Valdely Ferreira KINUPP Ari de Freitas HIDALGO Francisco Célio Maia CHAVES About the authors

ABSTRACT

The middle Rio Negro region is an interesting place to seek novel antimalarial compounds because of the traditional knowledge of the Amazon population in conjunction with the high biodiversity of the region. The objective of this work was to study the use of antimalarial plants in Barcelos, state of Amazonas, Brazil. Fifty-two local specialists from eight different communities were interviewed over one year. The identified plants were collected with the assistance of local specialists, classified to species level and deposited in herbarium. In total, 55 antimalarial plants were identified in use in the region, of which 16 had not been previously reported in other published studies. Many factors could be involved with the use of antimalarial plants by the Barcelos population, such as the accessibility of these medicinal plants, efficiency and safety of using these plants, the accessibility to drugs or other medical treatments, plant bitterness, and the gender of the interviewees. Our results indicate that the population of Barcelos possesses an extensive knowledge on the use of a diverse array of antimalarial plants, and may contribute to the development of novel antimalarial compounds.

KEYWORDS:
malaria; ethnobotany; Amazonia; medicinal plants; traditional knowledge

RESUMO

O conhecimento tradicional da população amazônica, associado à grande biodiversidade da região, faz do médio Rio Negro um lugar propício para a pesquisa de novos remédios antimaláricos. O objetivo deste trabalho foi estudar o uso de plantas antimaláricas no município de Barcelos, Amazonas, Brasil. Ao longo de um ano foram entrevistados 52 especialistas de oito comunidades de Barcelos. As plantas indicadas foram coletadas com o auxílio dos especialistas, identificadas e depositadas em herbário. Foram mencionadas 55 plantas antimaláricas, das quais 16 nunca foram citadas em outros trabalhos previamente publicados. Muitos fatores podem estar associados ao uso destas plantas antimaláricas, tais quais o acesso a estas plantas, sua eficiência e segurança, o acesso a outros tratamentos médicos, o amargor das plantas e o gênero das pessoas entrevistadas. Nossos resultados indicam que a população de Barcelos é detentora de um rico conhecimento sobre o uso de plantas medicinais antimaláricas e pode contribuir para o desenvolvimento de novas drogas antimaláricas.

PALAVRAS-CHAVE:
malária; etnobotânica; Amazônia; plantas medicinais; conhecimento tradicional

INTRODUCTION

Malaria remains as one of the major tropical diseases worldwide (Bremen 2011). In 2015, 214 million cases and 438,000 deaths were reported, most of them children less than five years old (WHO 2015). Malaria is considered as one of the neglected diseases, which are usually present in poor populations in tropical areas, and which receive little attention from governments and the pharmaceutical industry (Krettli 2008Krettli, A.U. 2008. Grandes Endemias no Brasil. Gazeta Médica da Bahia, 78: 74-78.). Malaria is caused by an infection with protozoans of the genus Plasmodium, and is transmitted by female mosquitos Anopheles spp. Clinical symptoms of malaria include cycles of fevers, chills, and headaches, and infection can affect the liver, kidneys, and nervous system, causing brain damage, which can lead to serious complications in infected individuals and result in death (WHO 2010; WHO 2015).

Malaria has a large economic and social impact in its endemic areas in Brazil. In 2013, 143,000 cases and 30 deaths were reported in the country. The Amazon region concentrated 99% of malaria cases in Brazil. Plasmodium vivax is the most frequent infection agent in Brazil, identified in 84% of all cases, followed by P. falciparum, identified in 16% of cases (SVS 2015; WHO 2015). Although Brazil has a universal public health system, eradication of the disease across the country is difficult due to factors such as the incorrect administration of drugs, the presence of isolated populations in the forest, the movement of people, particularly in border areas, and the expanding colonization fronts in the Amazon region (Melo 1985; Coimbra 1998; Singer and Caldas 2001Singer, B.H.; Caldas, M.C. 2001. Agricultural colonization and malaria on the Amazon frontier. Annals of the New York Academy of Sciences, 954: 184-222.).

Incorrect use of drugs and the evolution of Plasmodium spp. contribute to the development of increasing resistance to currently available antimalarial drugs, which creates an urgent need to identify novel therapeutic antimalarial compounds (Alecrim et. al. 1999Alecrim, M.G.C.; Alecrim, W.; Macedo, V. 1999. Plasmodium vivax resistence to chloroquine (R2) and mefloquine (R3) in Brazilian Amazona Region. Revista da Sociedade Brasileira de Medicina Tropical, 32: 67-68. , Krettli 2008Krettli, A.U. 2008. Grandes Endemias no Brasil. Gazeta Médica da Bahia, 78: 74-78., WHO 2010; WHO 2015). Ethnobotanical research of medicinal plants remains as one of the most important means for the identification of new, efficient, and safe compounds for the control of malaria (Ginsburg and Deharo 2011Ginsburg, H.; Deharo, E. 2011. A call for using natural compounds in the development of new antimalarial treatments - an introduction. Malaria Journal 10(S1): S1. (http://www.malariajournal.com/content/10/S1/S1)
http://www.malariajournal.com/content/10...
; Graz et al. 2011Graz, B.; Kitua, A; Maledo, H.M. 2011. To what extent can traditional medicine contribute a complementary or alternative solution to malaria control programmes. Malaria Journal 10(S1): S6. (http://www.malariajournal.com/content/10/S1/S6)
http://www.malariajournal.com/content/10...
; Willcox et al 2010Willcox, M.; Benoit-Vical, F.; Fowler, D.; Bourdy, G.; Burford, G.; Giani, S., et al. 2010. Do ethonobotanical and laboratory data predict clinical safety and efficacy of anti-malaria plants? Malaria Journal, London 10(S1): S7. (http://www.malariajournal.com/content/10/S1/S7)
http://www.malariajournal.com/content/10...
).

The populations that live along the Negro River, in the western Brazilian Amazon, use a wide variety of plants for the treatment of numerous diseases (Silva et al. 2007Silva, A.L.; Tamashiro, J.; Begossi, A. 2007. An ethnobotany of the riverine population from the Rio Negro, Amazonia (Brazil). Journal of Ethnobiology, 27: 46-72.). The Negro River region is suitable for the survey of novel drugs, because the region has a conserved forest, several endemic plant species, and the largest indigenous population of Brazil, comprising 24 ethnic groups (Sufredine and Daly 2001).

Therefore the objective of this study was to profile the use of antimalarial plants by traditional communities in the municipality of Barcelos, in the middle Negro River, Amazonas, Brazil.

MATERIALS AND METHODS

For this study, approval was obtained from all the involved communities, from the Ethics Research Committee (CEP) of São Paulo State University (UNESP/FMB no 3425-2010) and from the Brazilian National Genetic Heritage Council (CGEN no111 / 2012).

The fieldwork was carried out between July 2012 and July 2013 in eight communities in the municipality of Barcelos, state of Amazonas, Brazil (Figure 1), on the margins of the Negro River, the largest blackwater river of the Amazon basin, that originates in the Colombian Andes and crosses Amazonas from its northwestern border to the capital city of Amazonas, Manaus, where it joins with the Amazonas River. Barcelos is located in the middle region of the Negro River, 496 km upriver from Manaus.

Figure 1
Location of the municipality of Barcelos, Amazonas, Brazil. Numbers indicate the communities surveyed in this study: Barcelos (1), Ponta da Terra (2), Santa Inês (Bulixu) (3), São Luís (4), Cumaru (5), Baturité (6), Bacabal (7), and Romão (8). This figure is in color in the electronic version.

The municipality of Barcelos covers an area of 123,000 km2 and has a population of 27,000 inhabitants, the majority of them (56%) being indigenous (IBGE 2016). The Human Development Index (HDI) of Barcelos is considered low (0,500) (IBGE 2016). The incidence of malaria in the city is high, with more than 100 cases per thousand inhabitants registered each year (Suarez-Muttis and Coura 2007Suárez-Muttis, M.C.; Coura, J.R. 2007. Mudanças no padrão epidemiológico da malária em área rural do médio rio Negro, Amazônia brasileira: análise retrospectiva. Cadernos da Saúde Pública, 23: 785-804.; SVS 2015). The surveyed communities were indicated by the Barcelos Municipal Health Office according to their incidence of malaria (Table 1). Fifty two persons from the eight target communities were identified by locals according to their knowledge of medicinal plants using the snowball method (Alexiades, 1996Alexiades, M. 1996. Selected Guidelines for ethnobotanical research: a field manual. The New York Botanical Garden, New York, 306p.). Semi-structured interviews were conducted in order to understand socio-cultural aspects, the comprehension of malaria, and the use of medicinal plants for treatment of the disease (Supplemental Material, Annex S1).

Table 1
Communities visited for the survey of antimalarial plants in the municipality of Barcelos, Amazonas, Brazil

The identified plants were collected with assistance of the local specialists, identified to the lowest possible taxonomic level and deposited in the herbarium of the Instituto Federal de Educação, Ciência e Tecnoclogia do Amazonas (EAFM/IFAM) (Manaus, Amazonas). The curator of the herbarium Valdely F. Kinupp identified all plant species. The geographical origin of the species (native or exotic to Amazonia), was determined in accordance with Flora do Brasil 2020 em construção (2017). We reviewed available information about the phytochemical composition of and biological essays carried out for each of the surveyed species in online databases BIOMED, Scopus, SciDirect and GoogleSchoolar, as well as in related literature (Milliken 1997Milliken, W. 1997b. Traditional anti-malarial medicine in Roraima, Brazil. Economic Botany, 51: 212-237. a).

RESULTS

The 52 interviewees were 18 women and 34 men, with an average age of approximately 52 years. In terms of ethnicity, 73% of interviewees considered themselves indigenous, including 26 (50%) Baré, three Tukano, two Baniwa, two Yanomami, two Kaxinawá, one Tariano, one Urubu Tapira, and one Arapaço.

Concerning the incidence of malaria, only three people reported that they never contracted the disease. All interviewees claimed that their last cases of malaria were contracted in other communities, particularly those in the urban zone of Barcelos. Regarding disease transmission, 53% of interviewees believed that transmission is via mosquitoes, known locally as carapanã, 6% believed that transmission is through the water, 25% believed that both water and mosquitoes facilitate transmission, and 16% claimed not to know how transmission occurs. Almost half of the interviewees (44%) reported they did not know any preventive method against contracting malaria. Most interviewees (67%) said they use pharmaceutical drugs in addition to medicinal plants to treat malaria, 18% said they only use pharmaceutical drugs, and 15% said they only use plants and natural remedies.

Our survey resulted in the identification of 55 species belonging to 29 botanical families that are used for the treatment of malaria (Table 2). Some plants referred locally by the same name have been classified by botanical specialists as distinct species. These included açaí (Euterpe spp.), which was later identified as three different species of the same genus; carapanaúba (Aspidosperma spp.), which turned out to be three different species; and sucuúba (Himatanthus spp.), which was represented by two distinct species. Herein these species were considered in accordance with their common local denomination, since species under the same local name belonged to the same genus and were morphologically similar.

Table 2
Antimalarial plants used in the municipality of Barcelos, Amazonas, Brazil. Species marked with an asterisc (*) were tested in biological essays. Voucher number refers to the identification of the EAFM herbarium. N citations=number of interviewed specialists that cited this plant followed by the percentage of total interviewees in parentheses; Other sources=other published works that cited the same use; NA=not available. N citations and rank for Aspidosperma, Euterpe and Phanera species are presented as one value because they were considered as only one species by the interviewees.

The families identified most frequently for the treatment of malaria were Apocynaceae (41 times), Simaroubaceae (15 times), Asteraceae (14 times), Arecaceae (13 times), and Rhamnaceae (12 times). Regarding the origin of the identified species, 82% are native to the Amazon region and 18% are exotic.

Of the 52 plants identified for the treatment of malaria, 16 have not been previously described in other published works (Alternanthera sessilis, Himatanthus stenophyllus, Mikania pilostachya, Handroanthus barbatus, Phaseolus vulgaris, Doliocarpus magnificus, Poraqueiba sericea, Eschweilera sp., Plectranthus amboinicus, Plectranthus ornatus, Abuta imene, Iryanthera hostmannii, Paspalum gardnerianum, Solanum stramoniifolium, Cecropia ficifolia and Alpinia zerumbet) (Table 2). Only 25 of the plants identified in the present study have been characterized pharmacologically (Table 2).

The interviewees considered that approximately 65% of the plants reported for malaria treatment are bitter and eleven of the 12 most frequently identified plants for malaria treatment were considered bitter. A wide variety of plant parts were used, as well as several preparation methods (Table 2).

On average, the interviewed women identified eight antimalarial plants while men identified six. Among the plants indicated by women, 54% grow in intensively managed (domesticated) environments, such as backyards and small fields, while 61% of the plants indicated by men grow in wild environments, such as terra firme and floodplain forests.

DISCUSSION

More than 30% of interviewees believed that water was the sole or partial transmission agent of malaria. This association of malaria transmission with water can be explained by the higher incidence of the disease during the rainy season (November to March) (SVS 2015), when the breeding and consequent abundance of the Anopheles vectors increases significantly. The still widespread misconception about the transmission mode of the disease, as well as the widespread ignorance about preventative methods reflects the low effectiveness of awareness campaigns by local health officials, which makes the control of the disease more difficult. The use of medicinal plants may also be related to the ineffective coverage of health provision services. The majority of interviewees stated that they relay on pharmaceuticals for malaria treatment, and medicinal plants were used mainly for the treatment of malaria symptoms such as headache, fever, body aches, liver problems, and anemia. However, the use of plants for the treatment of the malaria infection in itself, occurred specially in communities with low access to conventional public health providers.

The most frequently identified species for the treatment of malaria in the present study were carapanaúba (Aspidosperma spp.), saracura-mirá (Ampelozizyphus amazonicus), açaí (Euterpe spp.), picão (Bidens pibinatifolia), sacaca (Croton crajucara), and quina (Quassia amara) (Table 2), which is in agreement with other similar studies carried out in the Amazon region (Brandão et al. 1992Brandão, M.G.L.; Grandi, T.S.M.; Rocha, E.M.M.; Sawyer, D.R.; Krettli, A.U. 1992. Survey of medicinal plants used as antimalarials in the Amazon. Journal of Ethnopharmacology, 36: 175-82.; Milliken 1997Milliken, W. 1997b. Traditional anti-malarial medicine in Roraima, Brazil. Economic Botany, 51: 212-237. b; Hidalgo 2000; Frausin et al. 2014; Ferreira et al 2015Ferreira, A.; Ming, L.C.; Haverroth, M.; Daly, D.; Caballero, J.; Ballesté, A. 2015. Plants Used to Treat Malaria in the Regions of Rio Branco-Acre State and Southern Amazonas State - Brazil. International Journal of Phytocosmetics and Natural Ingredients, 2015: 2-9. ; Kffuri et al. 2016Kffuri, C.W.; Lopes, M.A.; Ming, L.C.; Odonne, G.; Kinupp, V.F. 2016. Antimalarial plants used by indigenous people of the Upper Rio Negro in Amazonas, Brazil. Journal of Ethnopharmacology, 178: 188-198.). All of these plants have proven effective in the control of malaria Plasmodium (Milliken 1997a; Mariath et al. 2009Mariath, I.R.; Flacão, H.S.; Barbosa-Filho, J.M.; Sousa, L.C.F.; Tomaz, A.C.; Diniz, M.F. et al. 2009. Plants of the American continent with antimalarial activity. Brazilian Journal of Pharmacology, 61: 1401-1433.; Nunomura and Pohlit 2010Nunomura, S.M.; Pohlit, A.M. 2010. Alcalóides indólicos de casca de Aspidosperma vargasii e A. desmanthum. Quimica Nova, 33: 284-287.), except for B. bipinatifolia that has not yet been tested. Thus our results support the notion that the species more commonly used, and therefore empirically approved by more people, are also those proven to be efficient for disease treatment when tested scientifically.

The use of these medicinal plants was also influenced by their accessibility. For instance, saracura-mirá (Ampelozizyphus amazonicus), the second most frequently cited plant in this study, occurs only in specific places according to the interviewees, sometimes far from their home, and is only used when they have access to it. Some plants were rather used as substitutes for prefered plants, like paxiubinha (Socratea exorrhiza), that was used when the interviewees could not find carapanaúba (Aspidosperma ssp.).

Apocynaceae was the botanical family with the greatest number of species (six) used to treat malaria, followed by Arecaceae (five), Asteraceae (five), and Fabaceae (four), as has been observed in other antimalarial plant surveys in the Amazon region (Brandão et al. 1992Brandão, M.G.L.; Grandi, T.S.M.; Rocha, E.M.M.; Sawyer, D.R.; Krettli, A.U. 1992. Survey of medicinal plants used as antimalarials in the Amazon. Journal of Ethnopharmacology, 36: 175-82.; Hidalgo 2000; Frausin et al. 2014; Ferreira et al. 2015Ferreira, A.; Ming, L.C.; Haverroth, M.; Daly, D.; Caballero, J.; Ballesté, A. 2015. Plants Used to Treat Malaria in the Regions of Rio Branco-Acre State and Southern Amazonas State - Brazil. International Journal of Phytocosmetics and Natural Ingredients, 2015: 2-9. ; Kffuri et al. 2016Kffuri, C.W.; Lopes, M.A.; Ming, L.C.; Odonne, G.; Kinupp, V.F. 2016. Antimalarial plants used by indigenous people of the Upper Rio Negro in Amazonas, Brazil. Journal of Ethnopharmacology, 178: 188-198.). These families are among those with the highest species diversity in the Amazon region (Flora do Brasil 2020 em construção 2017). However, when considering the ratio of total species number by family to those of antimalarial value in traditional pharmacopeia, Simaroubaceae would be the most important plant family for the treatment of malaria, since 20% of all Simaroubaceae species that occur in the Amazon were reported to be used for the treatment of this disease, while only 3.4% of Apocynaceae species occurring in the region were reported as antimalarial (Milliken 1997Milliken, W. 1997b. Traditional anti-malarial medicine in Roraima, Brazil. Economic Botany, 51: 212-237. a; Mariath et al. 2009Mariath, I.R.; Flacão, H.S.; Barbosa-Filho, J.M.; Sousa, L.C.F.; Tomaz, A.C.; Diniz, M.F. et al. 2009. Plants of the American continent with antimalarial activity. Brazilian Journal of Pharmacology, 61: 1401-1433.; Flora do Brasil 2020 em construção 2017). The relatively high use of exotic species in popular pharmacopoeia is a result of population influx of other regions, which is common in northern South America (Bennet and Prance 2000Bennet, B.C.; Prance, G.T. 2000 Introduced plants in the indigenous pharmacopoeira of northerns South America. Economic Botany, 54: 90-102.) and in Barcelos (Barra and Dias 2013Barra, C.S.; Dias, C. 2013. Barcelos indígena e ribeirinha: um perfil socioeconômico. ASIBA/FOIRN/ISA, São Paulo, 82p.).

The predominance of bitter taste in plants used for malaria treatment was observed in other studies (Brandão et al. 1992Brandão, M.G.L.; Grandi, T.S.M.; Rocha, E.M.M.; Sawyer, D.R.; Krettli, A.U. 1992. Survey of medicinal plants used as antimalarials in the Amazon. Journal of Ethnopharmacology, 36: 175-82.; Hidalgo 2000). This may result from the relationship with the bitter taste of the real quina (Cinchona spp.) and its active component (quinine) that is used in the allopathic medicine, or with other antimalarial plants used by local populations that are considered bitter and have been proven effective in parasite control, such as sacaca (Croton cajucara), carapanaúba (Aspidosperma spp.), or quina (Quassia amara) (Milliken 1997Milliken, W. 1997b. Traditional anti-malarial medicine in Roraima, Brazil. Economic Botany, 51: 212-237. a; Mariath et al. 2009Mariath, I.R.; Flacão, H.S.; Barbosa-Filho, J.M.; Sousa, L.C.F.; Tomaz, A.C.; Diniz, M.F. et al. 2009. Plants of the American continent with antimalarial activity. Brazilian Journal of Pharmacology, 61: 1401-1433.).

Which plant part is used for treatment reflects the variety of growing habits of the species used. Commonly used materials from trees were bark and timber, while that from herbs were leaves. The plant part used largely determines the preparation method. Seeds and bark are usually decocted, while leaves are rather used in infusion. These aspects are important for the evaluation of the sustainable exploration of these plants, but should be considered on an individual case basis.

The generally higher number of antimalarial plants identified by women is probably due to the fact that, traditionally, women are responsible for the family’s health. In the northeast of Brazil women have been found to have more knowledge about the use of medicinal plants (Voeks 2007Voeks, R.A. 2007. Are women reservoirs of traditional plant knowledge? Gender, ethnobotany and globalization in northeast Brazil. Singapore Journal of Tropical Geography, 28: 7-20). The differential association of men and women with domesticated and wild medicinal plant species likely stems from the role partition between the genders. Men fish and hunt, having more contact with the wild areas around the communities, while women spend most of their working hours in backyards and farm fields (Ribeiro 1995Ribeiro, B. 1995. Os índios das águas pretas. Companhia das Letras, São Paulo, 270p.). The interviewees who identified a higher number of plants for malaria treatment had some form of written record of the use of medicinal plants, which suggests that the knowledge of medicinal plants should also be related to the memory of each person.

CONCLUSIONS

The knowledge of the use of antimalarial plants is well developed in communities of the Barcelos municipality at the middle Negro River, where the incidence of malaria is still high. We report 55 plants used to treat malaria infection, among them 16 species that had not been previously mentioned in other publications as antimalarial. Local women specialists cited more antimalarial plants than men, and cited more plants related to domestic environments, while men cited more plant species found in surrounding forests. Most antimalarial plants used by local people were bitter tasting. The exclusive use of plants for malaria treatment tends to be higher where conventional health providers are absent. Other factors could be involved with the use of antimalarial plants, but must be more studied, such as the accessibility of these plants and thei efficiency and safety. Of the 55 reported species, only 25 have been characterized through biological essays, which highlights the importance of ethnobotanical research for the identification of potential novel antimalarial drugs.

ACKNOWLEDGEMENTS

The authors are grateful to the population of Barcelos, and, in particular, to the Association of Indigenous Communities of Barcelos (ASSIBA), to the Foundation for Health Vigilance of Barcelos (FVS), to the Barcelos Health Secretary, and to the Special Secretary for Indigenous Health from the National Health Ministry (DSEI/Barcelos). This research was funded by Fundação CAPES, Fundação de Amparo à Pesquisa de São Paulo (FAPESP), and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq).

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Publication Dates

  • Publication in this collection
    Jul-Sep 2017

History

  • Received
    18 Apr 2017
  • Accepted
    08 June 2017
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