Ethnomedicinal plants used for the treatment of dermatological affections on the Purépecha Plateau, Michoacán, Mexico

Flora etnomedicinal utilizada para el tratamiento de afecciones dermatológicas en la Meseta Purépecha, Michoacán, México

Roberto Esquivel-García

Universidad Michoacana de San Nicolás Hidalgo, Mexico

Emmanuel Pérez-Calix

Instituto de Ecología, Mexico

Alejandra Ochoa-Zarzosa

Universidad Michoacana de San Nicolás Hidalgo, Mexico

Martha-Estrella García-Pérez

Universidad Michoacana de San Nicolás Hidalgo, Mexico

Skin diseases have been considered as the fourth leading cause of nonfatal disease burden worldwide (Hay et al., 2014). These conditions are widespread, being one of the most prevalent and disabling diseases and a source of considerable loss of life quality of patients. In rural populations, they are supposed to be one of the most common ailments (Policepatel and Manikrao, 2013). Skin affections have been related to clinical depression, anxiety and suicidal ideation, which represent a major additional problem with a significant negative impact for health systems (Dalgard et al., 2015).

Although in Mexico there are no extensive studies about the prevalence of skin diseases, the main reasons for dermatological consultation in the country are related with acne vulgaris, followed by psoriasis and melasma (HGM-SSA, 2012). In rural zones, the most frequent skin diseases are parasitic, viral and fungal infections as well as dermatitis and eczema (Paek et al., 2012).

Low adherence to treatments has been described for skin ailments (Storm et al., 2008; Augustin et al., 2011). Consequently, people frequently use natural products, mainly in undeveloped areas in which traditional herbal medicines play an important role in the management of these conditions (Sharma et al., 2014). In addition, many dermatological diseases have no cure (psoriasis, melanoma, pemphigus, etc.), so it is important to identify promising plants used in traditional medical systems to develop new therapeutic candidates. The ethnomedical studies remain very important in the discovery of new drugs and in the development of improved herbal preparations for use by local people (Heinrich and Gibbons, 2001).

The state of Michoacán, bordered by the states of Colima, Jalisco, Guanajuato, Querétaro, México and Guerrero is one of the regions of Mexico with the greatest diversity of plant species, many of which used for medicinal purposes (Medina, 2003). In pre-Hispanic times, this region was the home of the Purépecha Empire, which was centered on the Pátzcuaro lake basin. At that time, the Purépechas used copper agricultural tools in an exceptional way, compared to other Mesoamerican cultures (Amézcua Luna and Sánchez Díaz, 2015). They had a social stratification represented by the king, followed by knights, priests, and communities of farmers, fishermen, artisans and merchants (Amézcua Luna and Sánchez Díaz, 2015). Nowadays, the Purépecha people live mostly in the highlands of Central Michoacán, with a very important number of them on the Purépecha Plateau. The Purépechas preserve their language, traditions and customs, including an excellent ancestral knowledge of medicinal plants to treat various human health problems (INEGI, 2004).

The Purépecha Plateau is a rich reservoir of biodiversity which includes woody and herbaceous plants, the most important belonging to the genera Quercus L., Salvia L., Gnaphalium L., Senecio L., Eupatorium L., Bidens L., Tagetes L., Stevia Cav., Pinus L., Cirsium Mill., Adiantum L. and Dalea L. (Bello-González et al., 2015). Today, the participation of traditional Purépecha therapists in health services in this region is very important, mainly in those places where the public health system is still deficient (BDMTM, 2009).

Despite the importance of folk medicine by Purépechas, no ethnopharmacological studies are available about the use of plants for the treatment of dermatological conditions by this population. Therefore, it is considered that the documentation of Purépecha ethnomedicinal knowledge is required to identify promising plants for developing new therapeutic candidates or improved herbal preparations in the future.

Keeping the previously mentioned facts in mind, the present study was undertaken to scientifically enumerate medicinal plants and herbal preparations used by inhabitants of the Purépecha Plateau for the treatment of dermatological affections. Additionally, the ethnomedicinal studies performed on these plants are discussed to know whether other communities worldwide use the plants here reported for treating skin conditions, to estimate the contribution of this investigation to the global ethnopharmacological knowledge. Additionally, this study allows for the identification of plants to treat skin pathologies, which opens new perspectives for performing future phytochemical, toxicological and pharmacological investigations with extracts or pure compounds from natural origin.

The ethnomedicinal information on plants used to treat dermatological affections was collected from 86 individuals of the Purépecha Plateau; detailed information on these persons is shown in Figure 2. They mentioned 731 plant uses and the specimens of collecting plants corresponded to 97 species belonging to 87 genera and 47 families, which were documented for the first time for the treatment of dermatological conditions in this area. Families frequently used by Purépecha Plateau inhabitants were Asteraceae (20 taxa), Lamiaceae (13) and Solanaceae (5) (Fig. 3), with the genera Salvia (4 spp.), Tagetes (4), Allium L. (2), Artemisia L. (2), Euphorbia (2), and Solanum L. (2) the most represented.

Figure 3:
Family distribution of medicinal plants used on the Purépecha Plateau.

The dermatological conditions were classified into 19 categories according to the symptoms referred by participants as suggested by Sharma et al. (2014). These included blemishes, burns, calluses, cuts, fungal infections, hair fall, hematomas, infections with abscesses, skin inflammation, insect bites, pruritus, psoriasis, rash, skin bumps, skin care, superficial infections, varicella, varicose veins and warts. In this study, F_ic values were found to range between 0.14-0.75 (Table 1). The highest values were linked with hematomas (0.75), skin inflammation (0.73), varicose veins (0.73) and cuts (0.70), whereas lowest values were found for psoriasis (0.16) and blemishes (0.14). The highest numbers of plants were used for treating cuts (39 spp.), skin inflammation (36) and rash (36), whereas the treatment of warts (3) and calluses (2) was less reported among participants (Fig. 4).

Table 1:
Consensus factor values for different dermatological affection categories on the Purépecha Plateau.

Figure 4:
Number of plant species used for treating dermatological conditions on the Purépecha Plateau.

As revealed in Figure 5, the aerial parts which consist of a heterogeneous mixture of flowers, leaves and stems were preferred by participants (34.75%), followed by leaves (27.3%) and flowers (13.24%). In relation to the preparation modes, the most important were infusions (52.36%) and decoctions (15.13%). The present study also reports the use of common salt (sodium chloride) in small proportions for the preparation of pastes, particularly with the species Senecio salignus DC. and Sida kaenkeana C. Presl. Both plants are employed for treating cuts, hematomas, skin inflammation and skin bumps (Appendix).

Figure 5:
Plant parts and preparation modes used by inhabitants of the Purépecha Plateau for treating dermatological disorders.

Native and introduced plants (56.7 and 43.3%, respectively) are a valuable resource for local population for treating dermatological ailments (Appendix). According to the UV, the five most preferred plant species to treat dermatological disorders on the Purépecha Plateau were Heterotheca inuloides Cass. (0.53), Aloe vera (L.) Burm. f. (0.37), Oenothera rosea L'Hér. ex Aiton (0.21), Calendula officinalis L. (0.17) and Urtica subincisa Benth. (0.17) (Fig. 6).

Figure 6:
Plants with highest use values (UV) for treating dermatological ailments on the Purépecha Plateau.

Appendix shows the fidelity levels (FL) for each plant recorded in the study. The FL indicates which species are mostly preferred for the study population to treat a given disease. In the present study, 39 species were determined to have the highest fidelity level (FL=100%) for different skin ailments (Appendix). For cuts these plants were Azadirachta indica A. Juss., Commelina diffusa Burm. f., Chenopodium ambrosioides L., Eriobotrya japonica (Thunb.) Lindl., Geranium seemannii Peyr., Leonotis nepetifolia (L.) R. Br., Piqueria trinervia Cav., Sonchus oleraceus L., Tagetes lucida Cav. and Tagetes remotiflora Kunze, for fungal infections Zea mays L., for hair fall Buddleja sessiliflora Kunth and Verbena carolina L., for infections with abscesses Ipomoea murucoides Roem. & Schult. and Lepidium virginicum L., for insect bites Iresine interrupta Benth. and Tanacetum parthenium (L.) Sch. Bip., for rash Ceiba aesculifolia (Kunth) Britten & Baker f., Euphorbia nutans Lag., Lactuca sativa L. Montanoa tomentosa Cerv., Origanum majorana L., Physalis pubescens L., Prunus persica (L.) Batsch, Psidium sartorianum (O. Berg) Nied. and Stevia serrata Cav., for skin bumps Euphorbia pulcherrima Willd. ex Klotzsch, Ficus carica L., Illicium verum Hook. f. and Sida haenkeana C. Presl, for skin care Salvia leucantha Cav., for treating skin inflammation Aloysia citrodora Paláu, Artemisia ludoviciana Nutt., Artemisia mexicana Willd. ex Spreng., Eryngium beecheyanum Hook. f. & Arn., Marrubium vulgare L. and Moringa oleifera Lam., and finally for superficial infections Argemone ochroleuca Sweet, Bursera bipinnata (DC.) Engl. and Eriobotrya japonica.

The literature review related to ethnopharmacological studies worldwide, focusing on dermatological conditions (96 published articles) and the information contained in the Digital Library of Traditional Mexican Medicine (Appendix), shows that several plants here reported (91.25%) are used by other populations for treating skin affections. Additionally, this study provides new ethnopharmacological information about plants used for treating skin ailments in the study area, as well as at national and global level, as no ethnomedicinal reports were found for Eryngium beecheyanum, Tagetes remotiflora, Tournefortia mutabilis Vent., Equisetum hyemale L. var. affine (Engelm.) A.A. Eaton, Clinopodium macrostemum (Moc. & Sessé ex Benth.) Kuntze, Salvia leucantha, Sida haenkeana and Urtica subincisa for managing dermatological conditions, which represent 8.25% of the reported plants (Appendix).

Mexico is considered one of the countries with the highest floristic richness in the world, only preceded by Brazil, China, Colombia and South Africa (Villaseñor, 2016). In this context, the study of ethnomedical systems, including the identification of herbal medicines, is of great importance in addressing health problems of traditional communities. On the Purépecha Plateau in the Mexican state of Michoacán, the knowledge about medicinal plants not only has an anthropological significance, it also allows that people with economic problems solve their health issues.

It is now recognized that the transmission of knowledge regarding the use of medicinal plants from old to new generations is declining (Calvo et al., 2011). This fact is also a reality in indigenous communities because of globalization and the use of orthodox medicine. Therefore, it is crucial to rescue this knowledge to prevent the loss of ethnomedical traditions, which is a precious scientific and cultural heritage for future generations.

The results indicate that among the inhabitants of the Purépecha Plateau, middle-aged people are the ones who best preserve the ethnopharmacological knowledge. It is suggested that there is a tendency towards the loss of these traditions among young persons of less than 30 years (Fig. 2). Juárez-Vázquez et al. (2013) noted that this is a common trend in Mexico. It is also striking that almost all knowledge about plants was obtained from women. This is related to the fact that based on the villager’s recommendations, most of the contributors to this study were female. This was not unexpected, because it has been previously reported that among Purépechas, there is a clear quantitative predominance of women engaged in activities related to the use of medicinal plants (Gallardo Ruiz, 2002; BDMTM, 2009).

The present investigation has revealed the medicinal plants for treating skin affections and their modes of preparation on the Purépecha Plateau, Michoacán, Mexico. The most prominent families were Asteraceae, Lamiaceae and Solanaceae (Fig. 3). These results agree with a previous study performed in the indigenous community of Nuevo Parangaricutiro, a municipality of the Purépecha Plateau, which reported Asteraceae and Lamiaceae as the most important families used for medical purposes in this region (Bello-González and Salgado-Garciglia, 2013). Other ethnomedicinal studies performed in Mexico have also suggested that Asteraceae are an important source of medicinal plants in the country (Andrade-Cetto, 2009; Alonso-Castro et al., 2012), probably due to the high diversity of its phytochemical constituents.

The highest F_ic values were linked with hematomas, skin inflammation, varicose veins and cuts, whereas lowest values were found for psoriasis and blemishes (Table 1). It is considered that higher values of this factor are related to prevalent illness in the region, which lead people to exchange information about their knowledge concerning plant therapy for a longer time (Gazzaneo et al., 2005). As previously mentioned, among dermatological conditions, a high morbidity has been reported in the state of Michoacán for venous insufficiency (100.88 per 100,000 population) and wounds (DGE, 2015), which could explain the higher values obtained for the consensus factor in these categories. Lower F_ic values for psoriasis and blemishes indicate that plants used for these ailments were chosen randomly or no information about them was exchanged among participants (Neamsuvan and Bunmee, 2016).

According to the information referred by the participants, the higher number of reported plants was used for treating cuts, skin inflammation and rash (Fig. 4). Literature review, regarding ethnopharmacological studies worldwide for dermatological conditions, also shows that many plants are used for cuts, in comparison with other skin ailments (Sharma et al., 2014; Neamsuvan and Bunmee, 2016). A recent study performed among the Zoque indigenous people of Chiapas and Oaxaca, Mexico, also found that among dermatological conditions, most plant remedies are used for wound treatment (Geck et al., 2016). Another possible reason that could explain the preponderance of the use of plants in the region for cuts is the high incidence in Michoacán of morbidities associated with this ailment due to gunshots and dog bites (54.26 and 82.11 per 100,000 population respectively) (DGE, 2015).

Unexpectedly, some participants (mainly sellers and healers) referred during semi-structured interviews to the use of plants to treat specific diseases such as psoriasis (Fig. 4). Psoriasis is considered the second reason for dermatological consultation in Mexico (HGM-SSA, 2012). As it is an incurable disease, characterized by a low satisfaction of patients with treatments (García-Pérez et al., 2012), it is likely that the inhabitants of the Purépecha Plateau search natural alternatives for its treatment, leading to sellers and healers to know about this ailment. Unfortunately, no epidemiological studies were found about the incidence of this illness in this particular population.

For treating of dermatological disorders, the aerial parts were preferred by participants, followed by leaves and flowers (Fig. 5). This result agrees with previous studies which have reported the use of aerial parts to cure skin disorders due to their ease access in natural environments (Sharma et al., 2014; Neamsuvan and Bunmee, 2016). It is interesting to note that unlike other ethnopharmacological studies focusing on skin ailments (Njoroge and Bussmann, 2007; Abbasi et al., 2010; Afolayan et al., 2014; Sharma et al., 2014), Purépechas prefer the use of infusions and decoctions taken orally instead of topical administration, applying crushed plants, pastes and juices. This could be explained by the fact that among Purépechas there is a belief that dermatological disorders are manifestations of blood contamination (BDMTM, 2009). Therefore, they believe that cleansing the blood using herbal remedies by oral route would lead to improve skin problems. Another peculiar aspect to be highlighted is the fact that the population under study uses the “temazcal” (0.95%) for the treatment of cutaneous conditions. This is a steam bath of pre-Hispanic origin used in Mexico for curative, preventive, hygienic and religious purposes (Aparicio Mena, 2006). Its use is supported by the belief that the heat of the patient´s body is fundamental for healing, since the disease is eliminated through sweat (BDMTM, 2009). The present study also reports the use of common salt in small proportions for the preparation of pastes. Additionally, Sharma et al. (2014) found the same trend in a study focusing on the use of herbal preparations for dermatological disorders in India. These authors argued that the possible reason behind the use of salt would be related with the fact that it inhibits the activity of bacteria and fungi, thereby helping the skin to heal (Sharma et al., 2014).

Native (56.7%) and introduced (43.3%) plants were valuable resources for local population for treating dermatological ailments (Appendix). Although in the context of medicinal plants, both introduced and native plants are important, it has been reported that in rural areas of Mexico, practitioners depend on the natural environment rather than cultivated areas to obtain medicinal plants (Andrade-Cetto, 2009; Alonso-Castro et al., 2012). Indeed, 53.6% of the collected plants of this study were gathered from the wild. The extensive use of native species by Purépechas could not only be related to a higher availability of these plants through the seasons, but also to the inherited knowledge about their medicinal properties from the ancestors. In fact, it is known that among Purépechas the transmission of knowledge related to traditional medicine is performed in more than 50% by means of relatives (BDMTM, 2009). However, a non-neglectable amount of exotic plants was also reported in the study area. The contribution of these species is very important as they amplify the spectrum of therapeutic alternatives for treating dermatological conditions on the Purépecha Plateau, reinforcing the local plant formulary.

Five plants with the highest UV to treat dermatological disorders on the Purépecha Plateau were Heterotheca inuloides, Aloe vera, Oenothera rosea, Calendula officinalis and Urtica subincisa (Fig. 6). Heterotheca inuloides is known as Mexican arnica and is extensively used for dermatological problems in Mexico. Additionally, this plant is used alone or in combination with other herbs, for diminishing the pain associated to rheumatism, stomach ulcers and other painful conditions associated with inflammatory processes. It is also reported in the management of kidney disease, urinary infections, cough, lung diseases, vaginal infections, gastrointestinal disorders and cancer (Rodríguez-Chávez et al., 2017). According to the present study, Purépechas used this species for cuts, hematomas, infections with abscesses, skin inflammation, insect bites, rash, skin bumps, skin care, superficial infections, varicella, and varicose veins (Appendix). Its anti-inflammatory and antimicrobial properties in Purépecha traditional medicine are supported by pharmacological studies. Sesquiterpenes isolated from this plant exert activity against Bacillus subtilis var. niger Smith et al. (ATCC® 9372™), Brevibacterium ammoniagenes (Cooke and Keith) Breed (ATCC® 6872™), Propionibacterium acnes (Gilchrist) Douglas and Gunter (ATCC® 11827™), Staphylococcus aureus subsp. aureus Rosenbach (ATCC® 12598™), Staphylococcus aureus subsp. aureus (ATCC® 33591™), Streptococcus mutans Clarke (ATCC® 25175™), and Trichophyton mentagrophytes (Robin) Blanchard (ATCC® 18748™) with minimal inhibitory concentrations ranged from 6.23 to 12.5 mg/mL (Kubo et al., 1994). Infusions of Heterotheca inuloides inhibit the activity of cyclooxygenase enzyme by 40%, suggesting an anti-inflammatory effect of polar metabolites of this plant (Muñoz-Velázquez et al., 2012).

Aloe vera has been widely used for treating skin diseases across the globe. This plant is also very popular for managing cutaneous conditions in other Mexican states, such as Oaxaca and Chiapas (Geck et al., 2016). Aloe vera has demonstrated pro-cicatrizing effects by increasing collagen content in wounds and the degree of collagen cross linking (Heggers et al., 1996). Additionally, it possesses a protective effect against skin damage induced by radiation, anti-inflammatory activity, moisturizing and anti-aging effects (Choi and Chung, 2003). These pharmacologic properties justify its extensive use in traditional Purépecha medicine. Oenothera rosea is a native plant of Mexico that stimulates the proliferation of normal human fibroblasts in vitro (Takahashi et al., 2012), which could be related to its use for cuts by Purépechas. This species also reduces chronic and acute skin inflammation in rats (Villena and Arroyo, 2012), so it can function as anti-inflammatory agent, as referred by the population under study. Calendula officinalis has been employed in folk therapy for treating skin ailments worldwide. On the Purépecha Plateau, this plant is used for multiple skin affections including blemishes, burns, cuts, skin inflammation, insect bites, pruritus, psoriasis, rash, skin bumps and superficial infections (Appendix). Pharmacological studies suggest that extracts from this plant can protect skin against ultraviolet-induced damage (Fonseca et al., 2010). Moreover, this plant is highly effective for the prevention of acute dermatitis of grade 2, which occurs after postoperative irradiation for breast cancer, demonstrating its anti-inflammatory properties (Pommier et al., 2004). The extract of the flowers of this plant is also broadly recognized by its wound-healing promoting effects (Preethi and Kuttan, 2011). The multiplicity of pharmacological activities of this species on the skin agrees with its wide use on the Purépecha Plateau for dermatological conditions. Surprisingly, Purépechas frequently reported the use of Urtica subincisa for skin inflammation, skin bumps and varicose veins (Appendix). To the best of our knowledge, this native plant has not been previously reported neither in Mexico nor in the world for treating cutaneous disorders. Further phytochemical, toxicological and pharmacological studies with this species are required to establish its importance for treating skin ailments.

Thirty-nine plants were the most important, according to their FL (100%) for the treatment of 10 of the 19 dermatological conditions informed by the participants. These plants offer very interesting clues as to their pharmacological potential for the treatment of a specific skin ailment (Appendix). Additionally, this study provides new ethnopharmacological information about plants used for treating skin ailments on the Purépecha Plateau, Mexico and the world (Appendix). Apart from Tagetes remotiflora, all these plants are native of Mexico. Eryngium beecheyanum is a herbaceous plant which has been reported by peasants of the Sierra de Huautla, Morelos, Mexico, for kidney inflammation (Maldonado-Almanza, 1997). According to its fidelity level, it seems to be a promising candidate to treat skin inflammation (FL=100%). Tagetes remotiflora has been reported in the community of Nuevo Parangaricutiro by its antidiarrheic effect, as well as against vomiting, nerves and blood pressure (Bello-González et al., 2015). Its highest FL for cuts (FL=100%) indicates that it could also be employed for this affection. Tournefortia mutabilis has been reported to have antimicrobial properties (Sharma et al., 2017), which could be related to its use in superficial skin infections by Purépechas (FL=66.7%). In traditional Mexican medicine, Equisetum hyemale var. affine is mainly used for kidney conditions, pain, stomach inflammation, gastritis, ulcers and reproductive woman disorders (BDMTM, 2009). Although its use for treating skin conditions has not been reported, results obtained in this study indicate that it could probably be effective for hair fall and skin inflammation (FL=50.0%). Salvia leucantha is used in Mexico for stomach pain, respiratory ailments, reproductive disorders and diabetes (BDMTM, 2009; Romero-Cerecero et al., 2009). Our results point out that this species could also be used for skin care as the highest FL was obtained in this category. Although no reports were found regarding the use of Clinopodium macrostemum for dermatological disorders, its use for gastrointestinal affections and respiratory diseases has been documented in Mexico (INEGI, 2014). As its higher FL was obtained for skin inflammation (FL=83.3%), it would be interesting that further studies be performed to ratify this activity using in vitro and in vivo relevant models. To the best of our knowledge, Sida haenkeana and Urtica subincisa are reported for the first time as medicinal plants. According to their FL, Sida haenkeana seems to be a promising candidate to treat skin bumps (FL=100%), whereas Urtica subincisa was catalogued as anti-inflammatory agent (FL=80.0%). Traditional uses of the medicinal flora from the Purépecha Plateau can serve as a starting point for further scientific analysis, which may provide novel compounds or improved herbal preparations for treating skin diseases.

This study demonstrates that herbal remedies play an important role in healing skin by inhabitants of the Purépecha Plateau, state of Michoacán, Mexico. A total of 97 species were identified to treat 19 skin ailments. The quantitative analysis performed through the determination of the use value, fidelity level and the informant consensus factor allowed to identify plants as promising candidates for developing new dermatological formulations. This investigation is also a guide to the conservation of folk medicinal knowledge from indigenous people of Mexico, through a vision of sustainable use of natural resources. From the ethno-pharmacological point of view, it provides new information about plants whose medicinal properties for the skin had been unknown up to now. Additionally, it allows for dissemination of the inherited knowledge of Purépechas regarding herbal preparations for cutaneous diseases. The identification of plants used by this population to treat skin pathologies also opens new perspectives for performing phytochemical, toxicological and pharmacological investigations that allow the development of new herbal preparations or new drugs addressed to improve the quality of life of patients suffering from these diseases.

The authors are very grateful to traditional healers, sellers and local inhabitants from the Purépecha Plateau for providing the valuable information regarding medicinal plants for skin ailments and kindly sharing their ancestral knowledge with us.