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North American Bioactive Plants for Human Health and Performance Maria Pontes Ferreira Wayne State University, [email protected]

North American Bioactive Plants for Human Health and Performance Maria Pontes Ferreira Wayne State University, Maria.Pontes.Ferreira@Fulbrightmail.Org

Wayne State University

Nutrition and Food Science Faculty Research Nutrition and Food Science Publications

11-1-2012 North American Bioactive for Human Health and Performance Maria Pontes Ferreira Wayne State University, [email protected]

Fidji Gendron First Nations University of Canada

Katrina C. McClure University of Kansas

Kelly Kindscher University of Kansas

Recommended Citation Ferreira M.P., Gendron F., McClure K. C., Kindscher K. (2012) "North American bioactive plants for human health and performance," Global Journal of Research on Medicinal Plants and Indigenous Medicine 1(11), 568-582, available at http://digitalcommons.wayne.edu/ nfsfrp/1/ Available at: http://digitalcommons.wayne.edu/nfsfrp/1

This Article is brought to you for free and open access by the Nutrition and Food Science at DigitalCommons@WayneState. It has been accepted for inclusion in Nutrition and Food Science Faculty Research Publications by an authorized administrator of DigitalCommons@WayneState. Global J Res. Med. Plants & Indigen. Med. | Volume 1, Issue 11 | November 2012 | 568–582

ISSN 2277-4289 | www.gjrmi.com | International, Peer reviewed, Open access, Monthly Online Journal

Review article

NORTH AMERICAN BIOACTIVE PLANTS FOR HUMAN HEALTH AND PERFORMANCE

Ferreira Maria Pontes 1*, Gendron Fidji 2, McClure Katrina C3, Kindscher Kelly 4

1Assistant Professor, Department of Nutrition and Food Science, Wayne State University, 5045 Cass Avenue, Science Hall 3009, Detroit, MI, USA, 48202 2Assistant Professor, Department of Science, First Nations University of Canada, 1 First Nations Way, Regina, Saskatchewan S4S 7K2 Canada 3Graduate Research Assistant, University of Kansas, Department of Geography, Lawrence, KS 66047 4Senior Scientist, Kansas Biological Survey, University of Kansas, 2101 Constant Avenue, Lawrence, KS 66047 USA *Corresponding Author: Email: [email protected] ; Phone: (313) 5775888; Fax: (313) 5778616

Received: 20/09/2012; Revised: 25/10/2012; Accepted: 31/10/2012

ABSTRACT

Native and naturalized bioactive plants of the Canadian and American temperate biome are examined for their health and performance enhancement properties. Some of these plants are now being used as natural health products, and many have a long history as traditional foods and/or medicines with indigenous groups. This paper reviews the medicinal/cultural uses and bioactive properties of selected families: the family (Aquifoliaceae) as stimulants, the Celery family () as normoglycemic aids and analgesics, the Ginseng family (Araliaceae) as energy boosting aids, the Sunflower family (Compositae) as antiinflammatory aids, and the Legume family (Fabaceae) and Nightshade family () as functional foods. These North American plants show promising avenues for innovative health and performance enhancement aids and it is concluded that they should be investigated further for their bioactive properties.

KEY WORDS: Athlete; botanicals; complementary & alternative medicine; dietary supplement; ergogenic aid; grasslands; functional food; indigenous; natural health product; prairie; phytotherapy

To Cite this article: Ferreira M P, Gendron F, McClure K C, Kindscher K (2012), NORTH AMERICAN BIOACTIVE PLANTS FOR HUMAN HEALTH & PERFORMANCE, Global J Res. Med. Plants & Indigen. Med. , Volume 1(11), 568–582

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Global J Res. Med. Plants & Indigen. Med. | Volume 1, Issue 11 | November 2012 | 568–582

INTRODUCTION well, this biome boasts a rich cultural diversity, including dozens of indigenous groups with a North Americans are avid users of long history of use of botanicals for food and complementary and alternative medicine medicine. Despite being one of the most human (CAM), such as dietary supplements and altered landscapes on the planet, due to natural health products (NHP), for health risk colonialism and agriculture, the grasslands reduction and performance enhancement. biome continues to be a source of functional Regarding performance enhancement, the foods and medicines for indigenous and non American Dietetic Association, Dietitians of indigenous people today (Kindscher, 1987, Canada, and the American College of Sports 1992). While CAM is not evidencebased, and Medicine have a joint position statement on the thus not part of allopathic medicine, this is use of supplements and ergogenic aids, due to changing. Increasingly, there is growing the popularity of their use amongst athletes and scientific evidence documenting the potential fitness enthusiasts (American Dietetic health and performance value of North Association et al., 2009). Regarding other American traditional foods and medicine consumer group use of botanicals, in 2007, products. For example, Echinacea species approximately 40% of surveyed USA adults (family Compositae) are wild perennials used used CAM, and 18% of these therapies are widely in by indigenous people dietary supplements (Barnes et al., 2008). In for a variety of health and performance Canada, 71% of adults surveyed in 2005 have purposes. Today, Echinacea species are one of used NHP (Ipsos, 2005). the most commonly utilized NHP by mainstream North Americans; as well, it is one CAM is a broad group of diverse medical of the most researched botanicals from the and health care systems (e.g., traditional / Americas (Price and Kindscher, 2007). indigenous medicine), various practices (e.g., sweat lodge, meditation), and products (e.g., The National Institutes of Health (NIH) functional foods, supplements, and NHP). invested nearly $90 million in mechanistic, pre Natural health products are naturally occurring clinical and clinical research studies of substances derived from organisms from the 5 botanicals through two rounds of the Botanical life kingdoms: plants, animals, microbes, Research Centers Program between 2000– fungi, and protists. These products come in a 2010. The center is currently in its third five variety of forms such as powders, extracts, year funding cycle. The Office of Dietary ointments, capsules, and tablets. They include Supplements and National Center for vitamins and minerals, botanical remedies, Complementary and Alternative Medicine zootherapies, ergogenic aids, probiotics, (both NIH entities) jointly orchestrate a homeopathic, and traditional medicines. Many network of interdisciplinary centers devoted to traditional/indigenous food and medicines the study of botanicals, with the Botanical inform the research and development of Research Centers Program being the largest relevant bioactive components into commercial (Coates and Meyers, 2011). In Canada, the NHP. Over 80% of Canadians believe that it is functional foods and NHP sector continues to important to respect the role that NHP play in grow, with total annual revenues of $3.7 billion some cultures (Ipsos, 2005). Thus, traditional CND, as estimated from the Functional Foods and indigenous knowledge systems continue to and Natural Health Products Survey 2007 have a broad impact on the use of CAM by (Statistics Canada, 2007). Growth of this mainstream consumers. Canadian sector is enhanced through the spending of $148 million CND (in 2007) for Across Canada and the USA, a large research and development by functional food 2 temperate grasslands biome (3 million km ) is firms and those producing and/or marketing host to a rich diversity of landscapes yielding a NHP. New developments of this wide range of variety of native and naturalized plants. As product lines (over 22,000) include extraction

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Global J Res. Med. Plants & Indigen. Med. | Volume 1, Issue 11 | November 2012 | 568–582 and processing of bioactive compounds to metabolites with significant plant growth and produce products with increased health and development roles (e.g., colour pigments, wellbeing benefits. hormones, and sterols), the vast majority are secondary metabolites with roles in plant In this paper we give a brief introduction to defense (e.g., essential oils and latex). Conifers the basic secondary metabolites in botanicals, and many flowering plants produce essential and how they may be used for health and oils rich in terpenes and terpenoids, which may performance enhancement. We will then have medicinal properties. The native North introduce selected native plants, organized by American hops ( Humulus lupulus L., family, that come from a variety of habitats Cannabaceae) are herbaceous perennial vines across the grasslands biome and have a history that grow in moist fertile soils in the prairie of utilization by indigenous people (past and/or bioregion. The female clusters are present). Ethnobotanical and evidencebased valued by indigenous people for their sedative information regarding the health and qualities and are used as an herbal analgesic performance properties of the plant will be and for insomnia. In the brewing industry, hops discussed with implications for future research. contribute antimicrobial, flavour, and aroma It is our hope that this multidisciplinary properties attributed in part to the terpene conversation regarding these plants will inspire compounds. Beer has been used by athletes for indigenous interest in higher education; its therapeutic qualities since recorded history; protection and appreciation of the varied yet in immoderate doses alcohol continues to habitats that occur in the North American be abused amongst athletes (Ferreira and grasslands biome; appreciation of the influence Willoughby, 2008). of traditional/indigenous knowledge on NHP use for health and performance; and scientific Polyphenols are a diverse, large group of study of these bioactive plants. simple or complex phenolic compounds derived from secondary metabolism of the SECONDARY METABOLITES aromatic amino acids. Downstream product groups include coumarin, lignin, flavonoids, Plants produce many metabolites from tannins, and alkaloids. Most of these secondary metabolism that may have clear compounds have a role in chemical defense, roles in plant physiology (Wink, 2010). These some are metabolic end products with unknown secondary metabolites are organic molecules function, and lignin is a major structural produced in response to influences such as component of cells. Lignin has developmental stage and environmental emerged as an important component of dietary assaults (e.g., maturation and insects). When fibre (undigested organic polymer) with applied externally or internally, some of these antioxidant potential and suppresses plant compounds have purported beneficial carcinogenesis in vitro (Fardet, 2010) likely by effects in mammalian physiology. For example, acting as an absorbent for potentially as medicinal agents in folk remedies, veterinary carcinogenic molecules in the digestive tract in medicine, and pharmacognosy, natural products vivo . The Academy of Nutrition and Dietetics continue to have significant medicinal, endorses consumption of a high fibre diet (e.g., economic, and ecologic functions (Hopkins and , vegetables, and whole grains) for good Huner, 2009). There are 4 major classes of health (American Dietetic Association, 2008). bioactive secondary metabolites: terpenes, phenolics, glycosides, and alkaloids. Glycosides are a class of compounds characterized by glycosidic bonds between a Terpenes are a diverse group of isoprenoid sugar molecule and another noncarbohydrate compounds with over 15,000 structures, thus molecule with a hydroxyl group. This feature forming one of the largest phytochemical gives the compound the property to act as a groups. While many terpenes are primary detergent with a role in plant defense (e.g., anti

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Global J Res. Med. Plants & Indigen. Med. | Volume 1, Issue 11 | November 2012 | 568–582 fungal). The four main groups of glycosides are habitual users are likely due to a reversal of saponins (have foaming properties), withdrawal symptoms (James and Rogers, glucosinolates (antioxidants in cruciferous 2005). vegetables), cyanogenic glycosides (contains cyanide group), and cardiac glycosides (used to According to a systematic review of the treat heart conditions). Although not native, the literature by Tarnopolsky (2010), has common dandelion, ( Taraxacum officinale demonstrated adrenaline/noradrenaline receptor Webb, Compositae) is used in Mexican and antagonistic effects upon skeletal muscle, Native American traditional medicine for a adipose, and central nervous system tissues. variety of ailments and health benefits Based upon his expert assessment of the (RodriguezFragoso et al., 2008). Glucosides currently available evidence, dietary doses of (glucosederived glycosides) from this plant caffeine consumed prior to (2–6 mg/kg) or have been shown to exhibit in vitro anti during (0.75–2 mg/kg) endurance exercise inflammatory action as well as antioxidant result in improved performance. While a action (RodriguezFragoso et al., 2008). reduction in central fatigue is a wellestablished benefit upon caffeine administration during Alkaloids are a diverse group of chemically endurance activities, caffeine does not unrelated nitrogenous organic compounds with significantly affect performance in high high biological activity. Herbaceous dicots intensity or strength activities. (flowering plants) are rich in alkaloids, and many are repellant to vertebrates and HOLLY FAMILY (AQUIFOLIACEAE) invertebrates, likely due to their bitter taste. Many commercially important drugs are The presence of xanthines (caffeine, alkaloids, and most interfere with , and methylxanthine) is restricted neurotransmitters (Hopkins and Huner, 2009). to a few species of the Ilex genus in the Thus, they often function as painkillers, muscle Americas. Indigenous groups consume mate ( I. relaxers, and also as moodaltering substances. paraguariensis A. St.Hil. ), guayusa ( I. Caffeine, an alkaloid xanthine derivative, is one guayusa Loes.), and yaupon ( I. vomitoria of the most widely used nutraceuticals in the Aiton). The first two are native to South world; and its use amongst athletes is similarly America, and the latter to North America. Mate widespread and wellstudied (Tarnopolsky, is used by the South American Guarani for 2010). socializing, mental and physical stimulation, and in herbal remedies. In southern South Common dietary sources of caffeine American culture, the consumption of mate include coffee (typically L. and rivals that of coffee as a mainstream stimulant. C. canephora Pierre ex A. Froehner, Of the 3 , mate has been subject to the Rubiaceae), mate (Ilex paraguariensis A. St.– most scientific scrutiny and found to have Hil., Aquifoliaceae), tea ( (L.) compelling chemical profiles with important Kuntze , Theaceae), cocoa ( Theobroma cacao health implications (Heck and de Mejia, 2007). L., Malvaceae), and energy drinks. Currently Guayusa is anecdotally used by the Amazonian not a banned substance by the International Runa people as a balanced stimulant that Olympic Committee, caffeine is well energizes the body and mind while promoting established as a potential aid to physical and restful sleep with lucid dreams. Consumed in mental performance. However, not all people social ceremony, the Runa appreciate mate’s are caffeine responders, and the effects of capacity to decrease bodily pain and to increase dietary caffeine are contingent upon whether a mental clarity. Yaupon, or the yaupon holly person is a habitual or a ‘naïve’ user. Studies (also cassina) was used by Southeastern USA that appropriately control for confounding bands where it grew, and by plains bands factors indicate that psychomotor and mood who traded for it (Browne, 1935; Havard, enhancement benefits of caffeine use in 1896). Records indicate that it was used as a

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Global J Res. Med. Plants & Indigen. Med. | Volume 1, Issue 11 | November 2012 | 568–582 mildly stimulating infusion for frequent use, or flavanols (quercetin and kaempferol more famously, as part of the emetic ‘black glycosides) (MertensTalcott et al., 2011). drink’ associated with ritual purging (Havard, 1896). Regarding the potential scientific merits of this plant for use as an ergogenic aid or Yaupon (Spanish: Acebo de Yupon ) nutraceutical, further work is encouraged. Yaupon holly has been analyzed by high Yaupon, or cassina, is a native North pressure liquid chromatography (Edwards and American member of the Holly family. This Bennett, 2005; MertensTalcott et al., 2011; evergreen perennial is native to the Palumbo et al., 2007), and discerned to have a southeastern coastal plains of North America number of phenolic compounds, as well as and the piney woods and postoak savannah of alkaloid xanthenes (Edwards and Bennett, Texas (Smith and Rechenthin, 1964) and 2005; Palumbo et al., 2009). Principal naturalized west to central Texas. It may be compounds identified by mass spectrometry are native or naturalized to some parts of . alkaloids and some phenols (MertensTalcott et It is a dioecious or small with a al., 2011). Many of these secondary height of 3–6 m, and distributed across a metabolites likely protect the plant against variety of soil types and light intensities. bacterial and fungal microbial overgrowth. However, it prefers moist acidic soil and has intermediate shade tolerance. Aerial plant parts There are no scientific reports on the health (e.g., roasted ) are caffeinerich and were properties of yaupon for humans; but Noratto used by indigenous groups in ceremony (e.g., and colleagues (2011) indicate anti as the ‘’ decoction) and as a phyto inflammatory and antioxidant activity for the medicine (e.g., as an infusion). Natives called I. polyphenol (quercetin and kampferol vomitoria Aiton , “cassina” (derived from the glycosides) extractions of the plant in vitro . Timucua language) and I. cassine L. They demonstrated that yauponderived (commonly known today as dahoon holly) as flavanols inhibit human colon cancer cell “yaupon” and the black drink may have viability in vitro through reduced inflammation involved a mix of several species of Ilex by induction of endogenous antioxidant (Power and Chestnut, 1919; Edwards and systems and through reduced activation of pro Bennett, 2005). The tangled nomenclature has inflammatory genes. While yaupon holly has an been resolved, although confusion persists in intriguing profile of bioactive compounds, the older literature (Edwin, 1963). In when used as a NHP, the antitumour, anti comparing the xanthine profiles of the two inflammatory, and antioxidant properties have species, it has been demonstrated that caffeine yet to be demonstrated in humans. and methylxanthine concentrations are higher in the yaupon than in the dahoon holly CELERY FAMILY (APIACEAE) (Edwards and Bennett, 2005). It is also established that xanthine alkaloids (caffeine There are nearly 3,000 members in the and theobromine) are present in the leaves of Celery family (Apiaceae) worldwide (Bidlack yaupon tree dependent upon soil nitrogen et al ., 2010). These are mostly temperate plants content (Palumbo et al., 2007). Roasting the with softhollow stems and the leaves are leaves facilitates solubilization of caffeine, as usually alternate and pinnately or palmately does the steeping in hot water. Yet, published compound with white umbellate inflorescences. quantification of the caffeine content of ‘a cup The and form below the point of of yaupon’ is lacking, and cannot currently be origin of the petals and stamen; they vary in compared to a cup of coffee, mate, or tea. size and shape and many have culinary and/or Aqueous infusions of the plant are rich in medicinal uses. Commonly used seeds include: phenolic acids (dicaffeoylquinic acids) and dill (Anethum graveolens L.), (Coriandrum sativum L.), celery ( Apium

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Global J Res. Med. Plants & Indigen. Med. | Volume 1, Issue 11 | November 2012 | 568–582 graveolens L.), cumin ( Cuminum cyminum L.), native in Asia, are widely used in Chinese anise ( Pimpinella anisum L.), caraway ( Carum Traditional Medicine. carvi L.), parsley ( Petroselinum crispum (Mill.) Mansf.), and fennel ( Foeniculum vulgare Mill). As a root infusion, oshá is used to treat The root in many species is edible (e.g., diabetes (AndradeCetto and Heinrich, 2005). (Daucus carota L.), parsnip ( Pastinaca sativa Type 2 diabetes is the world’s most common L.), as well as the stems and leaves of celery , endocrine disorder, with an escalating parsley, cilantro, and ( Levisticum incidence especially amongst the Native and officinale L.). These plants are aromatic due to Latin American populations. A recent study essential oils rich in bioactive compounds that reports the hypoglycemic effect of oshá extract contribute to their use by people for food and in streptozotocin diabetic mice (Brindis et al., medicine. Caution should be utilized when 2011). Several compounds isolated from the wildharvesting members of this family extract utilized in that study proved to have because some are deadly poisonous (e.g., antihyperglycemic activity in vivo , with the waterhemlock ( maculata L.). mechanism of action being undetermined or due to inhibition of intestinal alpha Oshá (Spanish: chuchupate ) glucosidase. One compound isolated from the extract has previously been shown to stimulate Oshá ( porteri, Apiaceae) and insulin secretion. Thus, the methanol root other Ligusticum species are herbaceous extract of oshá represents a normoglycemic perennials found from BritishColumbia and agent with bioactive compounds with differing further south into northern Mexico, at mechanisms of action, worthy of further elevations of 500–3,500m. It grows in moist scientific investigation. soils on the edge of wooded habitats, as well in drier, rocky soils. The roots are fibrous tubers Tincture made from soaking the oshá root with ‘hairy’ root crowns growing from a central in ethanol for months is commonly used as an rootstock. Below the dark brown outer ‘skin’, externally applied liniment for sore muscles. the offwhite inner root has a distinctive and The search for novel analgesics continues, aromatic ‘celery’ aroma. Animals and people because many common analgesics have adverse consume the leaves, seeds, and roots as food sideeffects. Botanical antinociceptive and medicine. Many indigenous and traditional substances recently discovered include people anecdotally refer to oshá as ‘Bear alkaloids, terpenoids, and flavonoids. While Medicine’, because bears utilize the root for chemical analysis of other Ligusticum species food and medicine (Andrews, 1992; Lipske, (e.g., Asian species) has indicated the presence 1993). of furanocoumarins, pyranocoumarins, and phthalides, a composite chemical profile on Currently, oshá is widely used by Latin and oshá , reported by Brindis and colleagues Native Americans, as well as by mainstream (2011), indicates the presence of NHP consumers. Cultivation of oshá has been phenylpropanoids, terpenoids, and phthalides. unsuccessful and is currently wildharvested. These phytochemicals have yet to be Overharvesting may be a concern, and is being specifically analyzed for antinociceptive studied by researchers at the Kansas Biological properties. However, orally administered Survey, University of Kansas, USA. Currently, methanolcholoroform extracts of oshá in mice it is sold in Canada, the USA, and Mexico in subjected to the writhing test study resulted in the form of tinctures, capsules, whole or ground significant decrement of painrelated behavior roots, and seeds. The roots and seeds have been (DecigaCampos et al., 2005). These infused as traditional and folk medicine, for a preliminary findings suggest a place for this variety of ailments; indigenous runners plant in analgesic discovery research. anecdotally chewed the root for stamina and power. Other species of the Ligusticum genus,

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GINSENG FAMILY (ARALIACEAE) a review by Bahrke and colleagues (2009), it is also reported that members of the genus Panax Panax species of the Ginseng family do not improve performance and recovery of Araliaceae are found native in Asia and North individuals undergoing exhaustive exercise. America. These perennials have woody or Asian ginseng supplementation taken one hour herbaceous species with umbel . The prior to exercise tests on a treadmill did not genus name, Panax is derived from the Greek affect the endurance running performance and word panacea. Panax is a part of the subfamily other selected physiological parameters in Aralioideae and the 3 species of the genus recreational runners (Ping et al., 2011). recognized as medicines are: Asian ginseng ( P. Senchina and colleagues (2009) conclude that ginseng C.A.Mey.), Japanese ginseng ( P. the benefits of taking Asian ginseng japonicas (T.Nees) C.A.Mey.), and American supplements on athlete immune system remain ginseng ( P. quinquefolius L.). The most largely unproven. commonly known family member is the Asian ginseng, which is used worldwide as a NHP. Small Spikenard (French: aralie à tige nue The indigenous people in New France used the (MarieVictorin, 1964) ; Anishnabe: jiisens American root to stimulate appetite and to treat ojiibikan gisēns, wenane ) rheumatism and dysentery. Colonists shipped this root to Asia, which proved to be profitable, Small spikenard ( Aralia nudicaulis L., as the Chinese considered the plant valuable Araliaceae), commonly referred to as wild (Messier, 1989). While harvest of wild sarsaparilla, is a characteristic feature of American ginseng is legal during state parkland groves and wooded ravines of the specified periods in the USA, it is illegal in prairie grasslands except the extreme South and Canada (COSEWIC, 2000). Southwest USA (Vance, 1999). This perennial member of the family Araliaceae, genus Aralia , The English name ginseng derives from its has single stalks, 15–30 cm in length Chinese name, rénshēn, meaning "man root" before dividing into 3 parts that then divide because the roots are often shaped like human again into leaflets. The greenish white flowers legs. Panax spp. contain over 150 ginsenosides, are borne on a flowering stalk, which is usually the bioactive compounds that are characteristic below the level of the leaves. The plant was of true ginseng. Ginsenosides are a subclass of used as a popular medicine in New France, but the triterpenoid saponin glycosides (Senchina et it was only during the Englishcontrolled al., 2009). Ginseng is commercially available period that the plant was harvested on a large as a NHP in dosage forms suited for oral scale. For example, it is reported that several administration. In a review by Senchina and thousands of pounds were sent to London colleagues (2009), it was found that, along with merchants in 1766 (Lessard, 1996). echinacea, ( Echinacea angustifolia DC., Compositae), Asian ginseng is the most popular Indigenous Elders from Saskatchewan often NHP used by athletes, with 3.2–15% of athletes refer to small spikenard as the energy plant, and using it. Athletes use NHP for health and also as rabbit root. Consistent with other performance more than other consumer groups. Ginseng family members, the wild sarsparilla root is used as a tonic and stimulant, although Athletes consume members of the genus not to the same extent as commercial Asian Panax for their alleged increase in energy and ginseng. The spongy root pith has a sweet physical stamina. Although members of the balsam aroma and flavour and indigenous genus Panax have been reported to increase people use the root and berries as a stimulating pulmonary function and exercise capacity and tonic on long journeys (Keane and Howarth, to reduce chronic fatigue in patients and elderly 2009). In Saskatchewan, some pubs still brew people, there is no evidence of these effects in sarsaparilla root beer, which is made from healthy, young athletes (Bahrke et al., 2009). In

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Global J Res. Med. Plants & Indigen. Med. | Volume 1, Issue 11 | November 2012 | 568–582 natural sarsaparilla flavour (indeterminately of thistle ( Cirsium canescens Nutt.). The edible wild sarsaparilla vs. nonnative source). tubers of Jerusalem artichokes contain a starch comprised of fructose polymers. Roasted Brussel (2004) also mentions its stimulant dandelion and chicory roots have been used as effect. Its high carbohydrate level might a coffee substitute. Sunflower, native to explain its energetic quality. In a study of 17 America, was widely used by indigenous species of plants growing in the southern edge people for their seeds. of the boreal forest in Ontario, Canada, small spikenard fruits showed the greatest total Yarrow (French: achillée millefeuille ; energy value (73.4 Kcal/100 g) and soluble Anishnabe: aadjidamowana waabanowashk carbohydrate based upon glucose (16.38%) zhagish kaandawens aanashic ) (Usui et al., 1994); the fat and protein composition of its fruits was 0.28% and 1.34%, Yarrow (Achillea millefolium L., respectively. While studies on the role of small Compositae) is one of the most abundant white spikenard as an energy source have been flowers growing upon the North American limited, its ethnobotanical history and prairie. It has white flower heads densely nutritional value suggests the need for further packed in a roundtopped terminal cluster. Its examination for its use as a NHP. woolly leaves are divided into many segments and grow from a branched rhizome. One Elder There have been several published and in Saskatchewan calls this species porridgeon ongoing mechanistic and clinical studies of astick and states that an infusion “made using ginseng and NHP. They show promise to be the entire top of the plant helps support the consistent, safe and effective in a variety of immune system and can be used for chest healthrelated areas of research. Regarding wild infection” (Gendron et al., 2009). Indigenous sarsaparilla, a small spikenard rhizome extract people in Saskatchewan use this plant for was found to have little antimycobacterial regulating body temperature, opening skin activity on its own but appeared to have some pores, stimulating perspiration, and treating synergistic activity with Bacillus Calmette– colds and fevers. Yarrow is also used to Guérin (tuberculosis vaccine) and regulate the menstrual cycle, heal tissues, and Mycobacterium avium when combined with to reduce inflammation (Keane and Howarth, Symplocarpus foetidus (Webster et al., 2010) . 2009). Rhizome extracts (hexane) were effective at eliminating 4 different human cancer cell lines Recently, it was found that methanol extract with cellular viability less than 6.8% (Huang et of yarrow inhibited human neutrophil elastase al., 2006). In a companion study, Wang and and matrix metalloproteinases MMP2 and 9 colleagues (2006) reported that hexane in vitro (Benedek et al., 2007). These enzymes extraction from the rhizome and the fruit of are proteases associated with the inflammatory small spikenard were more effective than stem degradation of the connective tissue and the and leaf extraction against human colon cancer, extracellular matrix proteins. Benedek and leukemia, and cervix cancer in cell lines. colleagues (2007) were unable to identify which flavonoids contributed the most to the SUNFLOWER FAMILY (Compositae) neutrophil elastase inhibition. The capacity of yarrow to reduce inflammation may be an The family Compositae has approximately interesting avenue to explore in regards to 20,000 species and is distributed worldwide mechanical stress associated with exercise. (Bidlack et al. , 2010). Wellknown members of Yarrow extracts exhibit bloodpressure this family include chicory ( Cichorium intybus lowering (in vivo & in situ ), vasodilatory (in L.), Jerusalem artichoke ( Helianthus tuberosus vitro ) and bronchodilatory (in vitro ) activities L.), Texas tarragon ( Tagetes lucida Cav.), (Khan and Gilani, 2011). sunflower (Helianthus annuus L.), and prairie

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Global J Res. Med. Plants & Indigen. Med. | Volume 1, Issue 11 | November 2012 | 568–582

Yarrow’s high content of flavonoids makes breadroot scrufpea, is a perennial prairie plant it a potential candidate for chemoprevention found throughout the grasslands from Alberta research. Dried aerial parts of yarrow contain to Texas. The scientific name tells one it is the flavonoids, alkaloids, coumarins, saponins, esculent or edible species of the genus. It has a sterols, tannins, and terpenes. Infusions made chicken eggsized swollen root that appears with yarrow are a source of the flavonoids turniplike, but tastes more like a potato with a rutin, chlorogenic acid, and quercetin hint of peanuts. This was the most important (Dadáková et al., 2010). Yarrow has a high wild plant food collected by indigenous people amount of apigenin, a flavonoid associated with across the Great Plains of North America cancer prevention (Patel et al., 2007). Activities (Kindscher, 1987; Nabhan and Kindscher, identified for apigeninmediated cancer 2006). The roots are often braided by the tap prevention and therapy include: estrogenic/anti roots and are still traded and stored by the estrogenic; antiproliferative; cellcycle arrest Lakota and other indigenous bands. The long and apoptosis; antioxidation; detoxification lived plants have annual growth rings and are enzyme induction; immuneprotection; and cell found today only on native prairies. signal modulation (Patel et al., 2007). The Achillea genus also shows promising potential The plants occur in patches and historically, at reducing incidence of degenerative diseases, large prairie turnip patches were places where such as atherosclerosis, with its high anti people went to dig them during the early oxidant activity (Vitalini et al., 2006). summer before the tops dried up and blew away as tumbleweeds. The Omaha were known LEGUME FAMILY (LEGUMINOSAE) to determine the route of their summer buffalo hunts by where they could camp and harvest an The Legume family (also Fabaceae) is the abundance of prairie turnips (Fletcher and La third largest plant family, with over 19,000 Flesche, 1911). The harvest was an event for species (Bidlack et al., 2010). The family name the women and children, with the kids seeking Fabaceae refers to the fruit, which is also called new plants as a game while the women used a legume or pod. This large and economically digging sticks to harvest them from the hard important family is characterized by having prairie soil (Gilmore, 1977). Their abundance many species that form symbiotic relationships was evident as observed in 1858, as the Cree in with bacteria to fix atmospheric nitrogen, Saskatchewan were observed to harvest “many resulting in plants with rich nitrogen content, bushels” (Mandelbaum, 1940). Lewis and and hence in protein. The many important Clark recorded on May 8, 1805 in northern plants in the Legume family worldwide Montana that “this root forms a considerable include varieties of beans ( Phaseolus vulgaris article of food with the Indians of the L.), soybeans ( Glycine max (L.) Merr.), peas Missouri...they are esteemed good at all (Pisum sativum L.), cowpeas ( Vigna seasons of the year...are sought and gathered by unguiculata (L.) Walp.), peanuts ( Arachis the provident part of the natives for their winter hypogaea L.), chickpeas ( Cicer arietinum L.), store, when collected are stripped of their rind alfalfa ( Medicago sativa L.), and carob and strung on small throngs or chords and (Ceratonia siliqua L.). The largest genus is exposed to the sun or placed in the smoke of Astragalus with over 2,000 species; many of their fires to dry; when well dried they will which are medicinal while many others are keep for several years” (Thwaites, 2001). poisonous due to alkaloids, selenium accumulation, or both (Kindscher, 1987). The native harvesters of these plants came back to their prairie turnip patches repeatedly Prairie Turnip (Lakota: tipsin ) over the years, but not every year. Fortunately, when the plants are harvested, the seeds are The prairie turnip ( Pediomelum esculentum ripe, and traditionally these were scattered (Pursh) Rydb.), also called Indian bread root or across the disturbed soil as the tops of plants

Global Journal of Research on Medicinal Plants & Indigenous Medicine || GJRMI ||

Global J Res. Med. Plants & Indigen. Med. | Volume 1, Issue 11 | November 2012 | 568–582 were returned to the hole from which they were reference to the inflated calyx, which forms the harvested. Research has shown that disturbance husk. The genus is a member of the surrounding prairie turnips increases the Nightshade family, Solanaceae, which includes numbers that are present (Castle, 2006) and tomatoes ( S. lycopersicum Lam.), potatoes ( S. helps justify the sustainability of traditional tuberosum L.), and tobacco ( N. tabacum L.). harvest and planting practices. All nightshades are considered somewhat poisonous and may contain toxins in some parts The nutritional profile of the prairie turnip of the plant, but many fruits in the family indicates that in addition to starch, it has high Solanaceae are edible, including wild levels of calcium, magnesium, and iron. Also (Kindscher, 1987). the prairie turnip is a good source of the amino acid lysine and is considered an “exceptionally The manyseeded berries of the genus range valuable dietary supplement” (Kaldy et al., from greenish to yellow to tangerine and are 1980). It would seem that the prairie turnip sometimes flushed with purple or red (Whitson could be suited as a functional food. It has been and Manos, 2005), thus explaining the use of difficult to cultivate, however, and it is not the common names “ground ” and “husk readily available in the commercial trade. tomato” with reference to Physalis (Castetter, 1935) . Wild tomatillos occur throughout the NIGHTSHADE OR POTATO FAMILY continental U.S. and into southern Canada and (SOLANACEAE) northern Mexico. Its habitat includes old fields, open woods, and prairies, but it thrives in The Solanaceae are well known as an disturbed sites, including roadsides. Plants form important group of plants that are used in food colonies through the spread of underground and medicine and contain alkaloids whose rhizomes. The widely distributed wild toxins range from very mild to very poisonous. is cultivated by Zuni women, who boil the ripe Phytochemical research has been occurring for red berries before grinding them with raw approximately 200 years. Members of this , chile, and coriander seeds in a mortar. family are particularly interesting for their The dish is regarded as a great delicacy competitive characteristics, high productivity, (Kindscher et al., 2012; Castetter, 1935). and a notable presence of secondary Ethnologist Walter Hough (1898) stated that in metabolites (Eich, 2008). Steroidal alkaloids or the “old times”, the berries were eaten by the alkamines are present such as tomatillidine Hopi. Hough (1898) also reported that the Zuni from Solanum tomatillo (Remy) Philippi f. dried and ground the berries to produce a meal (Eich, 2008). Tropane alkaloids are found in for making bread. the Physalis genera amongst others in the family. Steroidal and tropane alkaloids are non According to Matilda Cox Stevenson overlapping in taxa and are thus mutually (1915) the berries of the ivyleaf groundcherry exclusive (Wink, 2010). (P. fendleri A. Gray , now recognized as P. hederifolia A. Gray) had the same Zuni name Wild Tomatillos (Zuni: k’ia’potimo’we ) (Ke’tsitokia ) as this wild tomatillo (and is named for an insect that feeds upon the plant), The wild tomatillo, or groundcherry, indicating that these species may have been (Physalis longifolia Nutt.) is a lowgrowing used interchangeably. She reported that this perennial herb of weedy habitats. The papery plant grows wild on lowlands and is also husk that encloses the fruit of the wild tomatillo cultivated in the small gardens worked by is a distinctive characteristic of the genus women. In Frank Cushing’s (1920) Zuni Physalis , which includes cultivated species Breadstuffs , he states that: “Among the sandy such as husktomato ( P. philadelphica Lam.) defiles of the upper plains, mesas, and and Chinese lantern ( P. alkekengi L.). The mountains grow abundant low bushes bearing name Physalis is Greek for “a bladder,” a very juicy little yellow berries called k’ia’po

Global Journal of Research on Medicinal Plants & Indigenous Medicine || GJRMI ||

Global J Res. Med. Plants & Indigen. Med. | Volume 1, Issue 11 | November 2012 | 568–582 timo’we , or the “juicefilled fruitage.” These past, and now are the subject of much research berries were in high favour with the ancient as our colleagues have discovered 14 new Zuni as food. They were boiled or stewed to compounds in P. longifolia Nutt., including one make a sweet but acrid sauce, which although which has strong and significantly unique anti not quite so acidic, otherwise resembled the cancer properties (Zhang et al., 2011; Zhang et . The is still used as food at the al., 2012). Zuni Reservation. In Rita Edaakie’s (1999) “Idonaphshe ” let’s eat traditional Zuni foods” SUMMARY AND FUTURE DIRECTIONS she gives a recipe for the use of K’e:ts’ido’kya K’yalk’osenne or tomatillo paste in which the North American athletes and other store purchased husktomatoes or tomatillos ( P. consumer groups use natural health products philadelphica Lam.), are used to make a tasty (NHP) to improve health and performance. sauce which includes roasted chilis and green Many NHP and dietary supplements are onions, as an adaptation of the previous use of derived from indigenous/traditional knowledge native Physalis species. systems. The central region of North American is largely comprised of one of the largest Physalis seeds, which cannot be identified biomes in North America the grasslands as to specific species, occur commonly in well as a variety of physiographic regions rich archeological sites in the southwestern USA in ethnomedicine, past and present. For this (Kindscher et al., 2012). In fact, Physalis seeds reason, scientists in Canada and the USA are have been found in ruins dating from as early exploring the bioactive properties of plants as AD 298 at these archaeological sites in New from this region. Identified herein are several Mexico: LA 109100 on Ceja Mesa west of native and naturalized bioactive North Albuquerque (DelloRusso, 1999); at the American plants that could help improve the Basketmaker III/Pueblo I period (AD 650900) health and performance of athletes, and other site at River’s Edge west of the Rio Grande consumers, when used as NHP, functional River; and north of Corrales (Brandt, 1991). foods, and ergogenic aids. Bioactive plants and Nutritional data on the native Physalis species their compounds used for dietary supplements is lacking, but tomatillos are anecdotally and NHP require further study regarding: considered nutritious and these plants could identification, standardization, mechanism of provide an important source of additional action, toxicology. Future work should also vitamins and phytochemicals. Tomatillos elucidate plant compound benefits in human contain alkaloids, as is common in the physiology, when consumed in a whole food Solanaceae family (Whitson and Manos, 2005). matrix such as a functional food. Physalis species were used medicinally in the

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Global J Res. Med. Plants & Indigen. Med. | Volume 1, Issue 11 | November 2012 | 568–582

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Global Journal of Research on Medicinal Plants & Indigenous Medicine || GJRMI ||