REVIEW article

Front. Pharmacol., 31 July 2020
Sec. Ethnopharmacology
https://doi.org/10.3389/fphar.2020.01160

Traditional Herbal Medicine in Mesoamerica: Toward Its Evidence Base for Improving Universal Health Coverage

  • 1Department of Biomedical Sciences, University of Cagliari, Cagliari, Italy
  • 2Biovision – Foundation for Ecological Development, Zurich, Switzerland
  • 3Botanical Garden, Institute of Biology, Universidad Nacional Autónoma de México, Mexico City, Mexico
  • 4Centro de Estudios en Salud, Universidad del Valle de Guatemala, Guatemala, Guatemala
  • 5Department of Epidemiology and Public Heath, Swiss TPH, University of Basel, Basel, Switzerland
  • 6Department of Life and Environmental Sciences, University of Cagliari, Cagliari, Italy
  • 7Pharmacognosy and Phytotherapy, UCL School of Pharmacy, London, United Kingdom

The quality of health care in Mesoamerica is influenced by its rich cultural diversity and characterized by social inequalities. Especially indigenous and rural communities confront diverse barriers to accessing formal health services, leading to often conflicting plurimedical systems. Fostering integrative medicine is a fundamental pillar for achieving universal health coverage (UHC) for marginalized populations. Recent developments toward health sovereignty in the region are concerned with assessing the role of traditional medicines, and particularly herbal medicines, to foster accessible and culturally pertinent healthcare provision models. In Mesoamerica, as in most regions of the world, a wealth of information on traditional and complementary medicine has been recorded. Yet these data are often scattered, making it difficult for policy makers to regulate and integrate traditionally used botanical products into primary health care. This critical review is based on a quantitative analysis of 28 survey papers focusing on the traditional use of botanical drugs in Mesoamerica used for the compilation of the “Mesoamerican Medicinal Plant Database” (MAMPDB), which includes a total of 12,537 use-records for 2188 plant taxa. Our approach presents a fundamental step toward UHC by presenting a pharmacological and toxicological review of the cross-culturally salient plant taxa and associated botanical drugs used in traditional medicine in Mesoamerica. Especially for native herbal drugs, data about safety and effectiveness are limited. Commonly used cross-culturally salient botanical drugs, which are considered safe but for which data on effectiveness is lacking constitute ideal candidates for treatment outcome studies.

Introduction

Access to adequate medical care is a basic human right (Article 25, Universal Declaration of Human Rights) and universal health coverage (UHC) is core to achieving Sustainable Development Goal three (SDG 3) of the UN Agenda 2030 (UN General Assembly, 1948; UN General Assembly, 2015). The World Health Organization (WHO, 2013) highlighted the need for integrating traditional and complementary medicine (T&CM) in national health systems in order to achieve UHC while respecting consumers’ choice. A comprehensive knowledge base is fundamental for establishing policies that allow people to “access T&CM in a safe, respectful, cost-efficient and effective manner” (WHO, 2013, p. 7). Lack of research data is seen as the number one challenge faced by member states for implementing the WHO’s T&CM strategy. The lack of systematic reviews of the available evidence on T&CM in Mesoamerica is reflected in insufficient policies and culturally sensitive health materials, representing critical barriers to care (Lozoya and Zolla, 1984; Nigenda et al., 2001; WHO, 2005; Caceres Guido et al., 2015; Mokdad et al., 2015). Recent emphases shifts in public health discussions stemming from debates around ‘Epistemologies of the South’ (De Sousa, 2011) propose that the route toward UHC in Mesoamerica is dependent on promoting “health sovereignty,” fostering a decolonial turn in favor of intercultural approaches that reflect the particular epidemiologies of the peoples (Basile, 2018). According to De Sousa (2010) and Laurell (2010) the neglected consideration of emic epistemologies in the shaping of public health policies should be contrasted with a turn toward an “ecology of knowledge-systems.” This perspective includes traditional medicine, particularly herbal medicine, which has been recognized as playing a key role toward providing culturally pertinent and accessible health coverage (Rocha-Buelvas, 2017) and is in line with the WHO’s guidelines, which pin-point acceptability as a factor fostering increased access to health provision services in diverse cultural settings (WHO, 2013).

Mesoamerica (from now on ‘MA’) is a term coined by Kirchoff (1943) and accepted by scholars to define a geographical region (Figure 1) inhabited by indigenous peoples that share several common cultural traits resulting from intense cultural interchange starting in the Early Preclassic period (Coe and Koontz, 2013). The advent of civilization in MA can be placed in the early second millennium BCE when the San Lorenzo Olmecs emerged in the region of today Veracruz (Mexico) and the Mokaya as the first socially stratified sedentary culture in the Soconusco region of Mexico and Guatemala on the Pacific coast (Clark, 1991, p. 13-26; Diehl, 2004, p. 129; Coe and Koontz, 2013). The common fundamental traits characterize the cultural area of MA and distinguish it from the rest of the Americas (Coe and Koontz, 2013, p. 9-10; Kirchhoff, 1943). Ranging from central Mexico to northern Central America, MA was home to several of the great civilizations of the Western Hemisphere, including the Olmecs, Maya, and Aztecs. Aztec medicine represented the culmination of a long cultural tradition uniting the different cultural groups of MA (Ortiz de Montellano, 1990). After the Conquest, the different health systems rapidly blended into a syncretic amalgamation combining indigenous and introduced elements (e.g., Ortiz de Montellano, 1975; Lozoya and Zolla, 1984; Ortiz de Montellano, 1990; Foster, 1994; Bye et al., 1995). Mirroring its outstanding cultural heritage, MA is also one of the world’s most biodiverse regions and among the most eminent centers of plant domestication (Vavilov, 1992; Smith, 1997; Myers et al., 2000; Ranere et al., 2009).

FIGURE 1
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Figure 1 Map of Mesoamerica (MA). The colored areas mark the geographic extent of the major linguistic groups: Mayan (green) in eastern MA and the Huasteca, Mixe-Zoque (blue) in the Isthmus of Tehuantepec region, Nahuatl (red) in central and western MA, Totonac (turquoise) in Veracruz, and Zapotec (yellow) in Oaxaca. The numbers 1–28 refer to the study codes in Table 1; the extents of the respective study sites are highlighted in white.

Epidemiology, Health Systems, and Integrative Medicine in MA

Mexico and Central America are undergoing a rapid health transition resulting in a “double burden of disease” as poverty related diseases coexist with modern lifestyle diseases (Frenk, 2006; Stevens et al., 2008; Puig et al., 2009; Gómez-Dantés et al., 2016).

As a result of a higher life expectancy, after the 1940s Mexico experienced a great demographic expansion going hand in hand with economic growth (Cabrera, 1994). Toward the end of the 1960s, however, concerns were raised about the economic sustainability of the soaring population (Cabrera, 1994) and in 1973 a new population policy was implemented (Alba and Potter, 1986). The Mexican Ministry of Health and Welfare (SSA) together with the Institute of Social Security (Instituto Mexicano del Seguro Social; IMSS) started to provide family planning counseling and contraceptive services free of charge through their national networks in 1973 (Alba and Potter, 1986). During the 1970s and until 1982 the political administrations expanded the Mexican health sector by increasing the number of hospitals, clinics and medical staff. This initiative included the establishment of over 3,000 rural health posts, 71 rural hospitals and trainee programs for community health workers including traditional midwifes. As a consequence, the family planning services reached communities and individuals that were not formally considered by the social security system (Alba and Potter, 1986). These measures resulted in a reduced population growth that was more accentuated in urban compared to rural areas and overall reduced poverty (Cabrera, 1994; Allen, 2007). In 1983 the IMSS started to monitor systematically the epidemiology in the marginalized rural communities. This data was used as a baseline for launching programs aimed at reducing morbidity and mortality culminating in a decrease of digestive infections, less malnutrition and better assistance during gestation, birth and postpartum period (Flores Alvarado and Morán Zenteno, 1989). In Guatemala in particular and Central America in general, emerging civil armed conflicts at the end of the 1960s, lasting into the 1990s, prevented health programs to comprehensively address the needs and reach out to the rural population, aggravating health disparities (Braveman et al., 2000; Flores et al., 2009).

Today, reduced burdens of infectious diseases are partially offset by the need for health care assistance caused by interpersonal violence and chronic illnesses (Stevens et al., 2008; PAHO, 2009; Acosta et al., 2011; Becerril-Montekio and López-Dávila, 2011; Bermúdez-Madriz et al., 2011; Gómez-Dantés et al., 2011a; Gómez-Dantés et al., 2011b; Gómez-Dantés et al., 2016). Despite promising effects of recent health system reforms, pronounced regional disparities in regard to health indicators within and between the countries of MA persist (Frenk, 2006; Stevens et al., 2008; Mokdad et al., 2015; Gómez-Dantés et al., 2016). Health inequities imply that infectious diseases – particularly diarrheal disorders and infections of the lower respiratory tract – and reproductive health still account for a considerable disease burden, particularly among marginalized, often indigenous, populations. Meanwhile, depressive and chronic diseases are becoming major health concerns (Frenk, 2006; Stevens et al., 2008; Mokdad et al., 2015; Gómez-Dantés et al., 2016). Especially type II diabetes mellitus and chronic kidney disease of unknown cause (CKDu), now also called epidemic of chronic kidney disease of nontraditional origin (CKDnt) pose increasing challenges to the health systems in the region (Barcelo et al., 2003; Barcelo et al., 2012; Kierans et al., 2013; Gómez-Dantés et al., 2016; Johnson et al., 2019; Wesseling et al., 2020). The endemic form of CKDu occurring in MA was previously called Mesoamerican nephropathy (MeN) and affects above all young male workers of the agricultural sector (Wesseling et al., 2013; Wijkström et al., 2013). The origin of CKDu (also MeN and CKDnt) seems to be primarily driven by occupational heat stress linked to dehydration (Wijkström et al., 2013; Wesseling et al., 2020).

With the partial exception of Belize, the national health systems throughout MA have a similar structure and suffer from considerable degrees of fragmentation and segmentation (Homedes and Ugalde, 2009; Puig et al., 2009; Acosta et al., 2011; Becerril-Montekio and López-Dávila, 2011; Bermúdez-Madriz et al., 2011; Gómez-Dantés et al., 2011a; Kierans et al., 2013; Mokdad et al., 2015). Typically, public sectors in MA countries are composed of the respective ministries of health, social security institutes, and up to seven additional service providers. While formal employees benefit from social security, the majority of the populations rely on the – at least theoretically – free healthcare provided by the ministries of health. Notwithstanding the constitutional guarantee of affordable healthcare to all, a considerable proportion of the population of each country has no de facto access to healthcare provision from the public sector; a deficit partially compensated for by a multitude of civil society organizations operating in the most marginalized areas, but perhaps more importantly, by traditional healers embedded in long-standing ethnomedical systems.

In Guatemala it is estimated that public investments cover only 40% of the costs for accessing healthcare services, and that most of these funds are centralized in urban and peri-urban areas (World Bank, 2016; Gomez et al., 2017). This exemplifies how marginalized communities in rural settings have to rely on a plurimedical system, where practitioners of traditional Maya medicine play a key role in providing affordable services (Ceron, 2010; Berger-González et al., 2016b; CMMM, 2016). Comprehension of this situation prompted the development of the Model for Inclusive Health in 2004 (Fort et al., 2011). This model implements the parallel coordination of patients between specialists in traditional medicine such as ajkum (~ herbalists), ajiyom (~ midwives), ajq’omaneel (~ physicians) and biomedical staff in the first and second levels of attention those working at community health posts and district health centers. The Inclusive Health Model required the implementation of new protocols of attention including ‘cultural syndromes’ such as susto (fright) ojeado (evil eye) or wuqub’ siwan (disease of the seven ravines; Taquira et al., 2016), and an understanding of associated botanical drug based therapies, so that the medical staff could be trained in coordinating safe patient care with Maya health specialists. For example, in the Cuilco health district alone, located in the western highlands of Guatemala, 360 traditional medicine practitioners coordinated interventions with 78 medical health staff (ISIS, 2019). The Inclusive Health Model was strongly promoted by the Ministry of Public Health between 2016 and 2017, which led to the inclusion of 40 plants into the “Norms for the Attention of the First and Second Levels” of the Ministry of Health (MSPAS, 2018, p. 835-863). In spite of this initial effort, the lack of evidence about the safety and efficacy of medicinal plants and associated botanical drugs employed by practitioners of traditional medicine are a limiting factor in the translation of these intercultural protocols.

Finally, a growing for-profit private sector offers care to the urban socio-economic elites. Each of these service providers has its own infrastructure and, despite recent efforts to harmonize service provision, the coordination between different health institutions is limited. Within the respective national health systems, the Ministry of Public Health plays the stewardship role, including the formulation of T&CM policies as well as integrating and regulating T&CM products and practitioners in the formal health systems (WHO, 2005; Homedes and Ugalde, 2009; Puig et al., 2009; Acosta et al., 2011; Becerril-Montekio and López-Dávila, 2011; Bermúdez-Madriz et al., 2011; Gómez-Dantés et al., 2011a; Kierans et al., 2013; Mokdad et al., 2015). Inefficiency in the public sector as well as the lack of cultural competency results in unsatisfactory perceived quality of care (Puig et al., 2009; Mokdad et al., 2015). In Mexico, the health-care delivery clinics in rural areas are run by the IMSS and the Mexican Ministry of Health and Welfare (SSA). Usually they are staffed with recent medical graduates who spend their obligatory year of postgraduate social service as well as with community health workers. This situation is, however, not the best basis for achieving quality, consistency, cultural sensitivity, and ultimately, patients’ confidence (Berlin and Berlin, 1996, p. 6) and is one of the reasons why traditional medicine has retained its important role in rural areas. For marginalized people, experiencing excessive financial, physical, or cultural barriers to care, traditional medicine often presents the only accessible healthcare option. Meanwhile herbal products provide popular treatment alternatives for urban socioeconomic elites and Latin American migrant communities (Lozoya and Zolla, 1984; Taddei-Bringas et al., 1999; Waldstein, 2006; Loera et al., 2007; WHO, 2013; Ladas et al., 2014; Alonso-Castro et al., 2017a). However, integrative efforts and official recognition of Mesoamerican Traditional Medicine are limited. Several countries lack national policies and programs on T&CM and Mexico is the only country in MA with a national pharmacopeia (WHO, 2005; Caceres Guido, 2015). Yet, from the 129 herbal drugs listed in the Mexican Herbal Pharmacopoeia only around 36 are native (FEUM, 2013). With respect to Guatemala, the National Vademecum on Medicinal Plants (Cáceres, 2009) containing validated information on 101 herbal drugs of which 42 are native, got the endorsement of the University of San Carlos and the Ministry of Public Health and was later adopted as a reference by the Central American Technical Regulation.

The emphasis on introduced taxa in formal phytotherapy in Latin America is due to an often lacking evidence base for native botanical drugs (Caceres Guido et al., 2015; Valdivia-Correa et al., 2016; Alonso-Castro et al., 2017b) and the relative good documentation of effectiveness and safety issues of herbal drugs present in the European and the US Pharmacopoeia (Lozoya and Zolla, 1984; Caceres Guido et al., 2015; Martins et al., 2019).

Medical concepts and health beliefs regarding disease etiology, diagnosis, and treatment show striking similarities throughout MA, notwithstanding the uniqueness of each cultural group’s ethnomedical system and individual case to case variations (Lozoya and Zolla, 1984; Weller et al., 2002; Groark, 2005; Kleinman and Benson, 2006; Balick et al., 2008; Berger-González et al., 2016a; Geck et al., 2017). Efforts to integrating traditional practitioners and practices into the formal health system have been met with limited success [but see Chary et al. (2018) and Hitziger et al. (2017)], partially due to a limited understanding of ethnomedical concepts and rural medicine as well as an a priori disesteem toward traditional medicine by formal health institutions and physicians (Lozoya and Zolla, 1984; Nigenda et al., 2001; Bye and Linares, 2015; Colon-Gonzalez et al., 2015). Formal health professionals in Mexico regularly prescribe and use herbal products yet lament the lack of T&CM-specific education and training material (Taddei-Bringas et al., 1999; Romero-Cerecero and Tortoriello-García, 2007; Alonso-Castro et al., 2017a). Meanwhile traditional healers rarely find successors and acculturation is changing patterns in transmission of traditional and local knowledge (Comerford, 1996; Balick et al., 2008; García-Hernández et al., 2015; Geck et al., 2016). Consequently, written sources of knowledge as well as popular media are increasingly shaping the medical systems of local and indigenous communities (Leonti, 2011; Geck et al., 2016).

Previous Cross-Cultural Comparisons and Compilations of Mesoamerican Herbal Medicine

Several national and regional compilations of medicinal plants exist in Mexico, covering over 3,000 botanical taxa (Argueta and Zolla, 1994; Bye et al., 1995). Unfortunately, these often demonstrate serious methodological deficits, particularly in regard to taxonomic identification and interpretation of ethnomedical data (Bye and Linares, 2015, p. 396-397). Further, the lacking quantification of traditional uses limit the utility of these compilations for the identification of cross-culturally salient taxa.

The first over-regional research program in the area aimed at the evaluation of the traditional use of botanical drugs in order to improve the quality of health care of marginalized populations was Tramil (Program of Applied Research to Popular Medicine in the Caribbean; Weniger, 1991; Boulogne et al., 2011). Tramil’s exclusive focus on the Caribbean implied that only very minor parts of MA were covered (Boulogne et al., 2011). Several studies compared the medicinal floras and ethnomedical concepts of closely related cultural groups within the same linguistic family (e.g., Berlin and Berlin, 1996; Leonti et al., 2003; Geck et al., 2016; Hitziger et al., 2016). Heinrich et al. (1998; 2014) conducted the most comprehensive cross-cultural analyses to date yet focused exclusively on gastrointestinal ailments. Additionally, several reviews exist on the treatment of emerging health concerns, specifically anxiety and depression, colorectal cancer, diabetes, and obesity (Alonso-Castro et al., 2015a; Cruz and Andrade-Cetto, 2015; Andrade-Cetto and Heinrich, 2016; Giovannini et al., 2016; Jacobo-Herrera et al., 2016; López-Rubalcava and Estrada-Camarena, 2016).

Objectives of This Analysis

T&CM contributes significantly to the health coverage of the population of MA, particularly in poor and underserved indigenous communities (WHO, 2013). Similarly, to the situation in MA, in most regions of the world, a wealth of information on T&CM has been recorded. Yet these data are often scattered, making it difficult for policy makers to regulate and integrate herbal products into primary health care. Despite over 400 million estimated regular users of T&CM in Latin America, systematic approaches to integrate T&CM in formal health systems are widely lacking (Caceres Guido et al., 2015). Given the shared cultural history, harmonizing regulations between different nations of MA is recommended (WHO, 2013, p. 41). A lack of pharmacological and toxicological data on even the most commonly used herbal drugs is often considered the principal limitation to integrative medicine in MA (Caceres Guido et al., 2015; Alonso-Castro et al., 2017a). National and international efforts have been conducted in Guatemala in order to establish integrative medicine at academic and public health levels and although official acceptance is limited, national interest and expectations are high (Cáceres, 2019). Further, there is a strong need to integrate T&CM into formal health education (Romero-Cerecero and Tortoriello-García, 2007; Alonso-Castro et al., 2017a). Hence, creating quantitative regional databases based on internationally published literature can be an effective means for advancing the integration of evidence-based T&CM and therefore contribute to achieving UHC.

In accordance with the strategic objectives outlined in the Traditional Medicine Strategy of the World Health Organization (WHO, 2013), we aim at establishing a consensus-driven knowledge base on herbal drugs used in Mesoamerican traditional medicine. The focus is on plants used as medicine by traditional healers in rural indigenous communities. The quantitative nature of the review will allow for the prioritization of taxa for pharmacological and clinical studies. The pharmacological evidence for the safety and efficacy of the cross-culturally most salient taxa is reviewed and important knowledge gaps are indicated. The review is intended as a baseline of evidence for regulators, health professionals, and consumers for making informed decisions on herbal drugs and phytomedicines. Hence, this review and the MAMPDB is seen as an essential first step for an improved integration of traditional medicine into the national health systems of Mexico and Central America.

Methods

The linguistic scope of this cross-cultural comparison is limited to the five groups that can be most closely linked to the cultural evolution of MA: Maya, Mixe-Zoque, Nahuatl, Totonac, and Zapotec (Kirchhoff, 1943; Campbell et al., 1986). Likewise, the geographic scope is limited to MA proper, excluding the frontier areas of northern Mexico and Central America, as these only temporally participated in MA (Coe and Houston, 2015: 13; Kirchhoff, 1943; Figure 1).

Published ethnobotanical and ethnopharmacological field studies related to the five linguistic groups were sought that met the minimum inclusion criteria of methodological transparency regarding data sampling, study location, population and taxonomic identification based on voucher specimens collected in situ. A comprehensive search on the online databases Medline (PubMed) and Scopus as well as the Swiss library network (swissbib) and the dissertations database ProQuest was conducted with the following search terms: ethnobotany OR ethnopharmacology OR “traditional medicine” OR “medicinal plants” OR “herbal medicine” AND Mesoamerica OR Mexico OR “Central America” Guatemala OR Belize OR “El Salvador” OR Honduras OR Maya OR Mixe OR Zoque OR Nahua OR Nahuatl OR Aztec OR Totonac OR Zapotec. Thus, 28 studies published between 1975 and 2016 were identified that met the geographic, linguistic, and methodological inclusion criteria to be considered by the MAMPDB (Table 1)1. Names and classification of linguistic groups follow glottolog 2.7 (Hammarström et al., 2016).

TABLE 1
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Table 1 Studies included in the Mesoamerican Medicinal Plant Database (MAMPDB).

All plant taxa with medicinal uses mentioned in the 28 studies were incorporated into the MAMPDB after verifying their taxonomic identity with www.theplantlist.org (accessed 06.06.2016). Family affiliations of angiosperms follow the more up-to-date APG IV (The Angiosperm Phylogeny Group, 2016). In case several members of the same genus are used interchangeably under the same vernacular name for the same purpose, the taxon is denoted Genus sp. Infraspecific taxa are not specified.

The medicinal uses were classified according to the second edition of the International Classification of Primary Care (ICPC; Table 2). The ICPC allows for classification of ethnomedical uses into 17 symptom-based categories, not requiring detailed diagnostics (WICC, 2004; Staub et al., 2015). The only modification made to the ICPC system refers to toothache, which was classified as a neurological rather than a digestive system disorder.

TABLE 2
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Table 2 Overview of the distribution of taxa and use-records of the Mesoamerican Medicinal Plant Database in the 17 International Classification of Primary Care (ICPC) categories.

For the species cited in at least nine studies (one third taken as an arbitrary threshold value) a comprehensive literature review of pharmacological data was conducted based on a literature search with the online databases Medline (PubMed), Scopus, and the Cochrane Library (Table 3). Preclinical and clinical data obtained with botanical drugs derived from the 98 medicinal plant species cited in at least nine studies are reported in correspondence to the predominant traditional uses (use-records). As an arbitrary threshold value predominant uses are defined here as those recorded in the same ICPC category by at least seven independent studies or alternatively, those most frequently recorded in an ICPC category in case no category was recorded in at least seven studies. A use-record is defined as a reported use per taxon and ICPC category in one study. Studies lacking methodological transparency or using doses unrealistically high from a therapeutic perspective were excluded from this review. We evaluated the available pharmacological and preclinical data in order to extrapolate on the safety and efficacy of clinical applications. We took the mode of application into account and considered the importance of cultural factors for the perceived effectiveness, which is to be distinguished from efficacy (Ortiz de Montellano, 1975; Last et al., 2001, p. 57-58; Moerman and Jonas, 2002; Witt, 2013). Therefore, we evaluated as potentially safe and effective also applications of herbal drugs for which no negative toxicological reports were available. Despite the human influence on the current distribution of plant taxa is not always exactly known we categorized the 98 species into natives and exotics, judging those species native which, due to their cultural importance, obtained a wide distribution range over South and MA prior to European conquest and colonization (e.g., Bixa orellana and Petiveria alliacea) as well as the pantropic species (e.g., Cissampelos pareira and Cocos nucifera).

TABLE 3
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Table 3 The cross-culturally most salient medicinal plant species in Mesoamerica (MA).

Results and Discussion

The Mesoamerican Medicinal Plant Database (MAMPDB)

The MAMPDB includes a total of 12,537 use-records for 2188 taxa (Table 2), including 1929 species and 259 taxa identified to the genus level only (Table 4.1 in the Supplementary Material), 995 genera (Table 4.2 in the Supplementary Material), and 185 families (Table 4.3 in the Supplementary Material). For more than half of the species (1,100; 57%) no cross-cultural consensus does exist and 36% of the genera are only recorded in one of the 28 studies incorporated into the database.

In the different ICPC categories herbal medicine and pharmaceuticals are not considered to the same extent appropriate solutions for the treatment of the various health problems. Therefore, the number of taxa and use-records associated with these categories do not directly reflect the epidemiological situation in rural MA but can provide some information. Several categories are poorly recognized in ethnomedical systems such as “B” (blood, blood forming organs and immune mechanism), “K” (Cardiovascular) and “T” (endocrine/metabolic and nutritional) while “Z” (social problems) is unlikely to be treated with medicine. Typically, the broad categories “digestive” (D) and “skin” (S) are among those with the highest number of associated medicinal plants and use-records (Table 2). Musculoskeletal ailments (L) are often treated with massages by traditional healers called ‘sobadores’ or ‘ajpamaj’ (Ankli et al., 1999; Leonti et al., 2001; Berger-González et al., 2016b; Geck et al., 2016) while midwifes give massages for problems of the lower female organs (X) (Weimann and Heinrich, 1997; Ankli et al., 1999; Michel et al., 2016). Measures for family planning (W) are provided by the IMSS in collaboration with MEXFAM. For treating and preventing several ailments of the urological system (U) it is important to drink copiously and flush the urinary tract. This means that ailments and interventions with respect to the categories B, L, K, T, U, W, X, and Z are probably more frequent than suggested by the number of use-records related to botanical drugs.

The many species of Asteraceae (226), Fabaceae (194), Euphorbiaceae (85) and Lamiaceae (79) reported for medicinal purposes in the 28 studies (Table 4.3 in the Supplementary Material) reflect the floristic representation of these plant families in the region (see Bye and Linares, 2015, p. 394). The use consensus of Asteraceae is on digestive (D; 54% spp./19.5% use-records) and inflammatory skin disorders (S; 47.8% spp./12.8% use-records) but the characteristic presence of cytotoxic sesquiterpene lactones in this family can lead to allergenic reactions (Siedle et al., 2004). The family with the highest share of species for skin disorders in the MAMPDB are the Solanaceae (66.2% spp./20.8% use-records) and the Euphorbiaceae (64.7% spp./24.7% use-records.), the latter notorious for their proinflammatory properties (Evans and Taylor, 1983). The family showing the highest share for A ‘unspecified’ are the Solanaceae (61.8% spp./18.6% use-records), Lamiaceae are most frequently used for digestive problems (D; 73.4% spp./20% use-records) and Fabaceae for skin disorders (S; 51% spp./15.6% use-records).

Consensus Analysis

The consensus of those 98 species, for which a therapeutic use has been documented in at least nine (one third taken as an arbitrary threshold value) of the 28 independent studies is presented in Table 3 together with a critical evaluation of the pharmacological and toxicological evidence based on existing literature. It highlights the most frequently cited taxa in the MAMPDB, which have roots in Olmec, Maya, Zapotec and Aztec as well as traditional Mediterranean medicine. Most of the 98 herbal drug species are either grown in home-gardens or thrive in the vegetation surrounding the villages and are thus easily available. Several are also sold on local markets for food purposes, including spices, herbs, vegetables and fruits. Of the 98 species 68 are native to MA (Table 3). Of those 22 considered effective and safe for skin problems (S) 17 are native to MA while of the 13 considered effective and safe for respiratory ailments (R) only 3 are native. For digestive (D), skin (S) and respiratory (R) problems as well as for the category ‘general and unspecified’ (A) among the 98 species a range of effective and safe herbal drug-based treatment options exist (Table 3).

Typically, many of the herbal drugs used against diarrhea (D) are rich in tannins and polyphenols (Heinrich, 1998), such as the bark of Byrsonima crassifolia, Guazuma ulmifolia, and Mangifera indica, leaves of Psidium guajava and Mangifera indica, unripe fruits of Musa × paradisiaca and fruit skin of Punica granatum. Those used altogether for gastrointestinal plain, cramps and diarrhea such as the leaves of Eryngium foetidum and Litsea glaucescens, the herb of Artemisia absinthium, the root of Cissampelos pareira and the zest of Citrus aurantiifolia are aromatic and/or bitter tasting drugs. Those herbal drugs effective and safe used for category ‘A’ fall under the sub-category of ‘general pain’, ‘weakness’ and ‘feeling ill’ (ICPC) and include those herbal species also used in ritual healing. These are often aromatic, essential oil-bearing plants such as Ocimum basilicum, O. campechianum, Tagetes lucida or Piper amalago. The ritual cleansing ceremony called “limpia” using aromatic herbs and lotions to brush away bad spirits from the patient is a typical therapeutic practice in MA (Zamora-Martínez and Pascual Pola, 1992). The leaves of Ocimum spp. are used either as an infusion or applied topically against headache (N) while the flowers and zest of Citrus sinensis and C. aurantium serve as infusions to treat anxiety and stress (P). The practice of using essential oil rich herbal drugs for treating the ICPC categories A, P and N remind of aromatherapy, which has been found effective in clinical trials focusing on stress and anxiety related disorders (Perry and Perry, 2006; Linck et al., 2010). There seems to be a lack of safe and effective diuretics as well as disinfectants of the urinary tract (only corn silk and fruits of Sechium edule (chayote) among Table 3). For muscular problems (L) nowadays often massages with commercialized balms are used and assistance during pregnancy, childbearing and family planning (W) is provided in Mexico by the IMSS in collaboration with trained local midwifes.

For several important medicinal species there is very limited evidence for either safety or efficacy or altogether, including but not limited to Tagetes erecta, Piper auritum, Byrsonima crassifolia, Bursera simaruba, Artemisia ludoviciana, Hyptis verticillata, Spondias purpurea Tradescantia zebrina Crescentia cujete, Parmentiera aculeata, Piper amalago, Baccharis inamoena, Bougainvillea glabra, Lepidium virginicum, Malvaviscus arboreus, Mimosa albida, Solanum lycopersicum, Cornutia pyramidata, Dorstenia contrajerva, Tagetes filifolia and Jatropha curcas (Table 3). This situation emphasizes the lacking knowledge base and the concerns regarding toxicity of native botanical drug species widely used in traditional medicine throughout MA (Caceres Guido et al., 2015; Valdivia-Correa et al., 2016; Alonso-Castro et al., 2017b).

According to the WHO guidelines for the assessment of herbal medicines (WHO, 1996, p. 181) a principle for the safety assessment of herbal medicines should be the traditional use of the product “without demonstrated harm” while “no specific restrictive regulatory action should be undertaken unless new evidence demands a revised risk-benefit assessment.” Yet even though a track record of traditional medical use can provide some evidence about the safety of herbal drugs and their applications it is necessary to point out that ‘natural’ is not to be confounded with safe, a common misconception among consumers of herbal drugs (WHO, 2013).

A well-studied case of toxic plant materials are aristolochic acids containing botanical drugs deriving from the Aristolochiaceae (Arlt et al., 2002; Michl et al., 2014). Aristolochic acids are nephrotoxic and carcinogenic and potentially contained in botanical drugs obtained from 14 different Aristolochia species present in the MAMPDB. The drugs obtained from Aristolochia spp. are often used for digestive problems and totaled 95 use-records in the MAMPDB (Table 4.1 in the Supplementary Material). The time lag between the onset of chronic intoxication and the manifestation of eventually lethal kidney disorders is the reason why the resulting pathology is difficult for the general population to associate with the consumption of Aristolochia spp. Clearly safety concerns prevail above all with systemic applications. Also the use of castor oil plant seeds as an emetic and purgative is risky (Aplin and Eliseo, 1997) and due to the high content of the hepatotoxic and carcinogenic safrole the leaves of Piper auritum, which are also widely used as a condiment for pork tamales (wrapped maize dough cakes), should be used in low doses when applied orally. Anthranoid rich material (bitterness as a proxy) of Aloe vera is regarded as unsafe upon prolonged oral applications and particularly during pregnancy as the resulting increased blood flow to the uterus can induce abortion (Schulz et al., 2012, p. 250). The leaves of Bryophyllum pinnatum contain cardiotoxic bufadienolids, the aromatic leaves of Lantana camara hepatotoxic metabolites, the leaves of Phyla scaberrima high amounts of neurotoxic camphor, and the aerial parts of Parthenium hysterophorus toxic sesquiterpenelactones and are thus all unsafe depending on the dose ingested. Also applying the latex of Argemone mexicana to the eyes, the latex of Asclepias curassavica to aching teeth and using Ruta chalepensis during pregnancy are to be regarded unsafe.

The guidelines for the “Appropriate Use of Herbal Medicines” (WHO, 1998, p. 2) state that “it is necessary to make a systematic inventory and assessment (preclinical and clinical) of medicinal plants; to introduce measures on the regulation of herbal medicines to ensure quality control of herbal products by using modern techniques, applying suitable standards and good manufacturing practices; and to include herbal medicines in the national standard or pharmacopoeia.” A relatively cost-effective way for conducting clinical trials are retrospective treatment-outcome studies (RTO studies), which use questionnaires for the collection of information from a representative sample of the population (Graz et al., 2005; Graz et al., 2007). RTO studies assess retrospectively the effectiveness of herbal preparation and treatments for defined medical syndromes and clinical manifestations (Graz et al., 2005; Willcox et al., 2011). While the case of Aristolochia spp. derived products showcases that herbal drugs are not always safe, those with a traditional clinical track record and above all food items, usually considered safe, qualify for RTO studies (WHO, 1998; Willcox et al., 2011).

The quantitative approach and assessment of the 98 most frequently used medicinal taxa included in the MAMPDB highlights those herbal drugs with the highest intercultural acceptance as well as those applications potentially unsafe. The higher probability of exotic herbal drugs to be considered safe and efficacious (Table 2) is related to the better overall research situation of herbal drugs used in the European and the US Pharmacopoeia (Martins et al., 2019). However, Table 3 includes several native herbal drugs uses as food such as spices and culinary herbs and constitutes potential starting points for RTO studies. While the intercultural consensus can give some indications about the safety and perceived effectiveness, intriguingly Graz et al. (2005) found that the treatment of malaria in Mali showed no significant correlation between cultural consensus and the best patient progress, underlining the strength of RTOs being complementary to ethnopharmacological field studies.

The list of medicinal species reviewed in Table 3 constitutes a data collection that can be drawn on by the Mexican Herbal Pharmacopoeia Committee for increasing the Appendix VI (list of species with medical use in Mexico). Appendix VI is the prelude to the monographs of medicinal plants contained in the Pharmacopoeia and could be used to promote a better integration of native Mesoamerican species into that regulatory document. It should also be considered that knowledge about herbal remedies is increasingly shaped by literature and popular media, through which global trends in T&CM are introduced to local communities.

Conclusions

Through the evaluation of the MAMPDB we have highlighted a group of locally available medicinal plants, yielding products with a high inter-cultural consensus of use and track record of traditional use. However, the results from preclinical in vitro or in vivo studies are only a proxy for medical efficacy in humans. Especially for native herbal drugs data about safety and effectiveness is limited. Commonly used cross-culturally salient botanical drugs, which are considered safe but for which data on effectiveness is lacking are ideal candidates for treatment outcome studies. These could be conducted at local health clinics and in collaboration with the respective ministries of health and social security institutes. Retrospective treatment outcome studies constitute a valid tool for a culturally sensitive evaluation of traditional medicines including the psychosocial dimension of healing. Collaborations between the medical staff of local health clinics with local health workers and practitioners of traditional medicine have the potential to close cultural gaps and medical misconceptions that preclude the implementation of intercultural models of healthcare attention. It would facilitate an enhanced acceptance and integration of different medical thoughts and foster communication between traditional health practitioners, patients and health professionals trained in Western biomedicine. A closer collaboration between practitioners of biomedical and traditional medical systems has the potential to increase affordability, accessibility and cultural acceptability of health care.

Similarly, to the situation in MA, in most regions of the world, a wealth of information on traditional and complementary medicine (T&CM) has been recorded. Yet these data are often scattered, making it difficult for policy makers to regulate and integrate traditionally used botanical products while existing compendia are often outdated. Creating quantitative regional databases that are based on internationally published literature can serve as effective means in the advancement of the integration of evidence-based T&CM and contribute to achieving UHC. It also constitutes a tool for responding to changing epidemiological landscapes and consumer preferences.

Author Contributions

MG and ML designed the review. MG, MB-G, LC, SC, MH, and ML wrote the paper.

Funding

This project has received funding from the European Union’s Seventh Framework Program for research, technological development and demonstration under grant agreement no. 606895.

Conflict of Interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Supplementary Material

The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fphar.2020.01160/full#supplementary-material

Footnotes

  1. ^ Four studies (no. 15, 16, 20, 24) focus on a specific disease category, whereas medicinal uses are not detailed in study no. 17, due to concerns about intellectual property rights.

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Keywords: Mesoamerican traditional medicine, evidence-based phytotherapy, universal health coverage, medicinal plants, Mexico, Central America

Citation: Geck MS, Cristians S, Berger-González M, Casu L, Heinrich M and Leonti M (2020) Traditional Herbal Medicine in Mesoamerica: Toward Its Evidence Base for Improving Universal Health Coverage. Front. Pharmacol. 11:1160. doi: 10.3389/fphar.2020.01160

Received: 07 March 2020; Accepted: 16 July 2020;
Published: 31 July 2020.

Edited by:

Hung-Rong Yen, China Medical University, Taiwan

Reviewed by:

Armando Caceres, Universidad de San Carlos de Guatemala, Guatemala
Tinde Van Andel, Naturalis Biodiversity Center, Netherlands

Copyright © 2020 Geck, Cristians, Berger-González, Casu, Heinrich and Leonti. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Marco Leonti, marcoleonti@netscape.net; mleonti@unica.it

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