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Saturday 22 December 2018

Yaupon Holly: A North American Plant Source of Caffeine

Issue: 109 Page: 42-47 by Vicki Shufer HerbalGram. 2016; American Botanical Council Description and Distribution Yaupon (Ilex vomitoria, Aquifoliaceae) is an evergreen holly that is native to the southeastern United States. It grows wild in coastal areas from southeastern Maryland and Virginia, south to Florida, and west to the eastern half of Texas, spreading north to the Ouachita Mountains of Arkansas, where the species originates (Figure 1).1* Yaupon is in the same family and genus as yerba maté (I. paraguariensis), the leaves of which are the source of the popular national drink of Argentina that is exported at the rate of hundreds of tons each year.2 The genus also includes guayusa (I. guayusa), a lesser-known but increasingly popular caffeine-containing South American plant that is being introduced as a tea in the United States. The habitat for yaupon holly is varied and includes maritime forests, dunes, forest edges, pine flatwoods, and wet swamps. Yaupon is an understory tree or large shrub that forms thickets from horizontal roots that spread out. Leaves are simple, alternate, and a glossy green with rounded (crenate) teeth. The plants are dioecious, producing small, greenish-white, mildly fragrant male and female flowers on separate plants in early spring. Only the females produce the berries, which are shiny red drupes about a quarter of an inch in diameter, that ripen in late fall or early winter.3 Nomenclature Common names for I. vomitoria include yaupon, American tea plant, appalachine, cassine, Christmas-berry tree, coon berry, emetic holly, South-Sea tea, and variant spellings of some of these words.1 In 1753, Swedish botanist Carl Linnaeus first assigned the species the scientific name Ilex cassine var. β. The name Ilex vomitoria was given to the plant in 1789 by Scottish botanist William Aiton. This name was based on the Native American ritual that involved consuming a strong brew of yaupon, possibly combined with other herbs, resulting in ceremonial vomiting. This was often done after fasting for days and then singing and dancing.5 (“Black drink,” as this dark yaupon concoction is commonly called, was also consumed in other contexts, e.g., prior to battles.) Because cassine is one of the common names for yaupon, there has been confusion among some researchers who have attributed I. cassine (common name: dahoon) as the source of black drink. However, the methylxanthine alkaloids (caffeine, theobromine, and theophylline) have been shown to be more abundant in I. vomitoria than in I. cassine, supporting I. vomitoria as the most likely candidate for the source of the drink.6 Although high concentrations of caffeine may cause vomiting, research by Fuller et al. reveals no other properties of yaupon tea that would have an emetic effect.7 The confusion about yaupon being an emetic seems to have originated when English naturalist Mark Catesby called it an “emetick broth” in the 1700s.8 However, in 1564, French explorers visiting the east coast of Florida made observations and illustrations of the Timucua people, who were later depicted in a series of engravings, including one showing a group of men drinking from shell cups and vomiting.9 Maude Grieve, in A Modern Herbal, also writes that yaupon has emetic properties,10 although the leaves are not generally considered to have such activity.** Traditional Uses Yaupon was recorded as being used by many tribes of the Southeast and trans-Mississippi South in political, religious, and social contexts.9 Lack of documentation for many of these groups makes it difficult to determine how extensive its use was. However, some sources suggest that black drink was nearly ubiquitous among people in this region. For example, author Robin C. Brown wrote, “A potent beverage called cassina or black drink … was quite important to the prehistoric people of Florida.”12 The most complete information comes from the Creek Confederacy that dominated the Southeast. The earliest known reference was from Spanish explorer Cabeza de Vaca while traveling along the coast of Texas in 1542.9 Another early account was from John Lawson in his book A New Voyage to Carolina, printed in 1709.13 According to Lawson, yaupon was used by the Native Americans of the Carolina coast, and they “bore this plant in veneration above all the plants they are acquainted with.” It was used for rituals and ceremonies, village councils, and other important meetings. It was also used as a social drink and to show friendship.9 Cups made of whelk, a sea snail whose shells are found along the Atlantic and Gulf coasts, were frequently used, and, among some groups, were served to the men in descending order of importance.14 Ceremonies in which large quantities were consumed were followed by vomiting. Throughout the Southeast, it was a symbol of purity and used for peaceful purposes; therefore, some Native Americans in this region referred to the tea as “white drink.”15 In an account by Jonathan Dickinson, who encountered the St. Lucian people on the east coast of Florida, only important men were given the black drink, which was strictly forbidden for other men, women, and children.9 It seems that most southeastern Native American groups used the black drink only for special occasions and not as an ordinary tea that could be consumed at any time. For many, it was used only for male activities. Lawson claims that from the Carolina coast, yaupon was sent westward and sold at a “considerable price.”13 It was also traded or transplanted in areas of the Southeast where it did not grow naturally.9 Trading of yaupon has been traced back to more than 500 years ago by a team of archaeologists who were excavating in Greater Cahokia, near present-day St. Louis, Missouri. A chemical analysis of organic residues from pottery found at the site revealed “theobromine, caffeine, and ursolic acid, biomarkers for species of Ilex.”16 Cups from marine shells and ceramic effigies of such shells at the site indicate early contact with coastal groups from where yaupon would have grown. Preparing the tea, by most accounts, involved boiling the parched leaves in water. According to Lawson, the leaves were first bruised in a mortar until they became black.13 They were then placed in an earthen pot over a fire and stirred until they were “cur’d.” Others would put the bruised leaves in a bowl with live coals, cover the contents of the bowl with yaupon leaves, and turn those leaves until they finished smoking. The yaupon leaves were then spread upon mats to dry in the sun and stored for use. The encyclopedic Native American Ethnobotany (Timber Press, 1998), written by ethnobotanist Dan Moerman, PhD, refers to yaupon tea’s use as an emetic among the Alabama, Cherokee, Creek, and Natchez.17 The Alabama and Creek also used it for purification purposes. Use by European Settlers The Spaniards arrived in St. Augustine, Florida, in 1565 and soon afterwards adopted the yaupon drink from the Timucua tribe. Later, the English colonists learned of its use, and by the early 1700s, it was widely used as a breakfast drink in coastal North Carolina. It was also used medicinally and was recommended by a Carolina physician to a friend in London for the treatment of smallpox. Yaupon leaves were boiled to help purify drinking water, as well.18 During the Great Depression in the 1930s, and during wartime and other periods when tea (Camellia sinensis, Theaceae) and/or coffee (Coffea spp., Rubiaceae) were unavailable or difficult to obtain on the Outer Banks (a chain of long islands off the North Carolina coast), yaupon was the main substitute, and, according to some, the only available source for caffeine-containing beverages. The preparation method was similar to the method used by Native Americans, only instead of using an earthen pot, they used an iron kettle over a slow fire and then pounded the roasted leaves in a mortar and let them dry. The leaves were then stored in glass bottles. On Knotts Island in North Carolina, near the Virginia border, farmers were said to have a patch of yaupon from which they would put up a barrel or so every year. Twigs were gathered in the spring, chopped up with leaves, and dried rapidly with artificial heat until they were scorched.18 Yaupon in the Marketplace Yaupon had found its way into the American colonial marketplace by the 1700s. From Kinnakeet (modern Avon) on the Outer Banks, yaupon was exported to northern cities and even to some European countries until the mid-1800s. It appeared in 18th century markets in Europe, where it was called “Carolina” tea and Appalachina in France.19 One of the Bankers, as inhabitants of the Outer Banks were called, gave an account in the 1890s of gathering yaupon stems and leaves, which were cured by drying and parching in pots or ovens. Cured yaupon was sold for 50 cents per bushel.20 Yaupon continued to be used on the Outer Banks until the mid-1900s and was popular at Nags Head, North Carolina resorts. By 1973, it was served only at the Pony Island Restaurant on Ocracoke Island. With the arrival of regular tea and coffee, yaupon became the poor man’s tea and those who were seen out gathering it were called “yeopon-eaters” in a derogatory way.18 Recently, a blind taste-test study was conducted by Alisha Wainwright, an undergraduate student at the University of Florida, who found that yaupon’s descriptive scientific name may impact how well it is received by consumers. Wainwright prepared two separate teas from yaupon and yerba maté, and served each to the study’s 75 participants, asking them to rate which they preferred. To her surprise, most preferred the taste of yaupon. However, after being told its scientific name and traditional use among Native Americans, the number of tasters who indicated their interest in purchasing yaupon tea dropped considerably, from 16% to 7%.21 Even though the popularity of yaupon as a tea declined, it became a popular plant in the landscape of the southeastern United States, where cultivars are currently marketed. With glossy, evergreen leaves and berries that turn a waxy red just before the December holiday season, it is a favorite for decorations. The berries are also a source of food for birds that overwinter in areas where yaupon grows. Yaupon is therefore planted to help establish habitats for wildlife. Even though birds eat the berries, according to Schmutz and Hamilton, the berries of all hollies are reported to be poisonous to humans if eaten in quantity.22 High levels of theobromine in the berries may result in nausea, vomiting, and diarrhea.22,23 Phytochemistry Researchers at the University of Florida found that dry, unprocessed yaupon leaves contain 0.65-0.85% caffeine, which is somewhat less than that of coffee beans (1.1%) and tea leaves (3.5%). According to Steve Talcott, PhD, a food chemistry professor at Texas A&M University, yaupon’s caffeine levels vary, but they are comparable to Asian green tea and yerba maté. One study found that fertilization with nitrogen boosts the caffeine level several-fold in both wild and cultivated types of yaupon.2 Studies have also shown that yaupon contains high concentrations of antioxidant polyphenols, including chlorogenic acid, coumaric acid, and several flavonoids. Yaupon plants grown in full sun had higher concentrations of these compounds.2 In addition, yaupon contains nearly the same levels of antioxidants as its close relative, yerba maté.24 The plant also contains theobromine, a xanthine also found in cacao (Theobroma cacao, Malvaceae) and thus chocolate.24 Pharmacology Theobromine, theophylline, and caffeine are methylated xanthine alkaloids (methylxanthines) that stimulate the central nervous system (CNS), enhancing alertness and warding off drowsiness.25,26 Caffeine modulates the dopamine system, and it is thought to exert its stimulating effects by blocking adenosine A2A receptors (i.e., it acts as an adenosine-receptor antagonist).27 Caffeine’s performance-enhancing effects also arise from the intracellular mobilization of calcium and the inhibition of phosphodiesterase, which increases cyclic adenosine monophosphate (cAMP) in muscle and other tissues.28 However, caffeine, in therapeutic or high doses, can have adverse effects, including anxiety, nausea, vomiting, diarrhea, hypertension, and insomnia.26 It can increase heart rate and, in extreme situations, cause seizures and delirium. Over-the-counter and prescription medications can also interact with caffeine.29 Theobromine lacks the CNS effects that caffeine has.25 When theobromine was given to young patients with asthma, bronchodilation improved. This effect was strengthened when theobromine was combined with caffeine and theophylline.30 These chemicals open bronchial passages and help stop bronchospasms.31 In vitro studies with human colon cancer cells suggest that polyphenolic and flavonol compounds extracted from the yaupon leaves may have chemopreventive and anti-inflammatory activities. Quercetin and kaempferol 3-rutinosides were the main flavonol compounds identified in the investigation. An increase in activity of antioxidant enzymes protected colon cells against reactive oxygen species (ROS) in vitro.32 Yaupon berries are considered toxic and are the only part of the plant considered poisonous. They reportedly contain a compound called illicin,† possibly saponin glycosides, and triterpenoids, which can cause nausea, vomiting, and diarrhea. However, the berries also taste very bitter, thus preventing them from being eaten in large quantities.33 Future Outlook Caffeine is one of the world’s most sought-after psychoactive substances. More than a trillion cups of caffeinated beverages, including coffee, tea, and sodas, are estimated to be consumed worldwide each year.34 Tea is the second most consumed beverage in the world, second only to water. In 2014, the US imported 49.7 million pounds of green tea and 237.2 million pounds of black tea. Tea sales for yerba maté, both loose and in tea bags, were close to $10 million.35 Yaupon has the potential to become the next popular caffeinated beverage, despite its scientific name and its historical use as an emetic. The late ethnobotanist Dan Austin, PhD, author of Florida Ethnobotany (CRC Press, 2004), said the taste will be the make-or-break factor.36 Also, harvest of its leaves is labor-intensive, resulting in higher production costs than yerba maté, which is harvested in South America where labor costs are much lower. However, the agreeable taste and health benefits of yaupon may help reverse its undeserved bad reputation. These factors may also inspire people in areas where it grows to cultivate the plant or harvest it from existing patches. After a long period of obscurity, yaupon is once again starting to make its way back into the marketplace. Growers in Texas and Florida are producing yaupon leaves and beverages that are being sold online and in retail stores across the Southeast. Asi Yaupon Tea, a company in Georgia, was the first company to produce a ready-to-drink yaupon tea, flavored with native fruits that include muscadine grapes (Vitis rotundifolia, Vitaceae) and aronia berries (Aronia melanocarpa, Rosaceae), as well as wild mint (Mentha spp., Lamiaceae) and honey.37 A number of other companies are now selling yaupon tea online, including Cat Spring Yaupon Tea in Cat Spring, Texas. Yaupon has also appeared on the menu in several restaurants that focus on locally sourced food, including Dai Due and Odd Duck in Austin, Texas, and Commune in Virginia Beach, Virginia.38 People are becoming curious, especially those who have it growing on their property, where it often becomes invasive. With an increased interest in buying locally produced foods and teas, yaupon may very well become the next popular caffeinated beverage on the market. Vickie Shufer is a naturalist and herbalist with a master’s degree in therapeutic herbalism. She teaches classes on edible and medicinal plants, as well as outdoor education programs. Shufer is the author of several books, including The Everything Guide to Foraging (Adams Media, 2011), and was the editor/publisher of The Wild Foods Forum newsletter from 1994 to 2014. *A closely related plant — Ilex vomitoria subsp. chiapensis (Sharp) A.E. Murray — occurs in fragmented populations in Veracruz and Chiapas, Mexico.1 ** Per discussion in this article, there is no emetic activity associated with yaupon holly itself. Caffeine and other methylxanthines can act as emetics in relatively high doses: “The usefulness of xanthine bronchodilators in the treatment of asthma is often limited by the side effects of nausea and vomiting.”11 †An Internet search for the term “illicin” (also spelled “ilicin”) led to no credible information regarding its structure or pharmacology. The term appears to have originated from early chemical experiments on leaves from the genus Ilex conducted in the mid- and late-1800s. References Hu SY. The botany of yaupon. In: Hudson CM, ed. Black Drink: A Native American Tea. Athens, GA: The University of Georgia Press; 1979:10-39. Putz FE. Yaupon redeemed. The Palmetto. 2014;31(3):9-11. Little EL. National Audubon Society Field Guide to North American Trees. New York, NY: Alfred A. Knopf, Inc.; 1980. Ilex vomitoria Aiton: Yaupon. US Department of Agriculture website. Available at: http://plants.usda.gov/core/profile?symbol=ILVO. Accessed January 26, 2016. Putz FE. Yaupon tea has a bad name. The Gainesville Sun. April 8, 2010. Available at: www.gainesville.com/article/20100408/NEWS/100409426?tc=ar. Accessed January 26, 2016. Edwards AL, Bennett BC. Diversity of methylxanthine content in Ilex cassine L. and Ilex vomitoria Ait.: Assessing sources of the North American stimulant cassina. Econ Bot. 2005;59(3):275-285. Fuller HM, Arnold RJ, Murphy MK. Using chemistry to understand culture: Why did Native Americans vomit after drinking yaupon tea? J Undergrad Chem Res. 2002;1(1):47-51. Blanton WB. Medicine in Virginia in the Eighteenth Century. Richmond, VA: Garrett & Massie, Inc.; 1931. Available at: http://babel.hathitrust.org/cgi/pt?id=mdp.39015006706231;view=1up;seq=3. Accessed January 26, 2016. Merrill WL. The beloved tree: Ilex vomitoria among the Indians of the Southeast and adjacent regions. In: Hudson CM, ed. Black Drink: A Native American Tea. Athens, GA: The University of Georgia Press; 1979:40-82. Grieve M. A Modern Herbal. Mineola, NY: Dover Publications, Inc.; 1971. Howell RE, Muehsam WT, Kinnier WJ. Mechanism for the emetic side effect of xanthine bronchodilators. Life Sci. 1990;46(8):563-568. Brown RC. Florida’s First People: 12,000 Years of Human History. Sarasota, FL: Pineapple Press; 1994. Lawson J. A New Voyage to Carolina. London, UK; 1709. Milanich JT. Origins and prehistoric distributions of black drink and the ceremonial shell drinking cup. In: Hudson CM, ed. Black Drink: A Native American Tea. Athens, GA: The University of Georgia Press; 1979:83-119. Fairbanks CH. The function of black drink among the Creeks. In: Hudson CM, ed. Black Drink: A Native American Tea. Athens, GA: The University of Georgia Press; 1979:120-149. Crown PL, Emerson TE, Gu J, Hurst WJ, Pauketat TR, Ward T. Ritual black drink consumption at Cahokia. Proc Natl Acad Sci USA. 2012;109(35):13944-13949. Available at: www.pnas.org/content/109/35/13944.full.pdf. Accessed January 26, 2016. Moerman DE. Native American Ethnobotany. Portland, OR: Timber Press; 1998. Sturtevant WC. Black drink and other caffeine-containing beverages among non-Indians. In: Hudson CM, ed. Black Drink: A Native American Tea. Athens, GA: The University of Georgia Press; 1979:150-165. Hudson CM. Introduction. In: Hudson CM, ed. Black Drink: A Native American Tea. Athens, GA: The University of Georgia Press; 1979:1-9. Hill T. Materia medica indigenous to North Carolina. N C Med J. 1896;37(4):90-97. Wainwright AE, Putz FE. A misleading name reduces marketability of a healthful and stimulating natural product: a comparative taste test of infusions of a native Florida holly (Ilex vomitoria) and yerba maté (I. paraguariensis). Econ Bot. 2014;68(3):350-354. Schmutz EM, Hamilton LB. Plants That Poison: An Illustrated Guide for the American Southwest. Flagstaff, AZ: Northland Press; 1979. Helmenstine AM. Poisonous holiday plants. About Education website. Available at: http://chemistry.about.com/od/toxicchemicals/tp/poisonous-holiday-plants.htm. Updated December 2, 2014. Accessed January 26, 2016. Palumbo MJ, Talcott ST, Putz FE. Ilex vomitoria Ait. (yaupon): A native North American source of a caffeinated and antioxidant-rich tea. Econ Bot. 2009;63(2):130-137. Pengelly A. The Constituents of Medicinal Plants. 2nd ed. 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Flavonol-rich fractions of yaupon holly leaves (Ilex vomitoria, Aquifoliaceae) induce microRNA-146a and have anti-inflammatory and chemopreventive effects in intestinal myofibroblast CCD-18Co cells. Fitoterapia. 2011;82(4):557-569. Ilex vomitoria. North Carolina State University Cooperative Extension website. Available at: https://plants.ces.ncsu.edu/plants/all/ilex-vomitoria/. Accessed January 26, 2016. Klosterman L. Drugs: The Facts About Caffeine. Tarrytown, NY: Marshall Cavendish Benchmark; 2006. Keating B, Lindstrom A, Lynch ME, Blumenthal M. Sales of tea and herbal tea increase 3.6% in United States in 2014. HerbalGram. 2015 (105):59-67. Available at: http://cms.herbalgram.org/herbalgram/issue105/hg105-teamktrpt.html. Accessed January 26, 2016. Nordlie T. Native holly can provide caffeinated, antioxidant-rich beverage, UF experts say. University of Florida News website. Available at: http://news.ufl.edu/archive/2009/06/native-holly-can-provide-caffeinated-antioxidant-rich-beverage-uf-experts-say.php. Published June 25, 2009. Accessed January 26, 2016. Crane M. Yaupon, the only caffeine source native to the US, has potential to explode. Nutritional Outlook. May 13, 2015. Available at: www.nutritionaloutlook.com/sports-energy/yaupon-only-caffeine-source-native-us-has-potential-explode. Accessed January 26, 2016. Carpenter M. Here’s the buzz on America’s forgotten native ‘tea’ plant. NPR website. Available at: www.npr.org/sections/thesalt/2015/08/04/429071993/heres-the-buzz-on-americas-forgotten-native-tea-plant. Published August 4, 2015. Updated August 11, 2015. Accessed January 26, 2016.