adulteration of selected unprocessed botanicals in the u.s

7/28/2019 Adulteration of Selected Unprocessed Botanicals in the U.S.

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Adulteration of Selected Unprocessed Botanicals in the U.S.Retail Herbal Trade1

KAREN M. WALKER* AND WENDY L. APPLEQUIST

William L. Brown Center, Missouri Botanical Garden, P.O. Box 299St. Louis, MO 63166-0299,USA*Corresponding author; e-mail: [email protected]

Adulteration of Selected Unprocessed Botanicals in the U.S. Retail Herbal Trade.

Adulteration of botanical dietary supplements through the accidental or deliberate use of aplant species other than the one claimed to be present is a well-publicized concern. Recentsurveys of these products have found that some historically reported adulterations still occurdespite strict quality control regulations. For a few botanicals, the accidental inclusion of toxiclookalike species has caused consumer illnesses. Since most of the Western market, asmeasured by monetary value, consists of processed dietary supplements, relatively littleattention has been paid to the question of whether unprocessed bulk herbs sold to herbalistsand in herb stores are equally subject to adulteration. We hypothesized that adulterationssimilar to those seen in materials sold for use in dietary supplements would occur. Ninebotanicals were selected that had been previously reported to be adulterated, or weresuspected to be at risk of adulteration, and that could be distinguished from known or likelyadulterants by the morphology of parts in commerce. Samples were purchased from elevenvendors and authenticated by morphological examination. Most were correctly identified,and no toxic adulterants were found. Samples of Juniperus and Tilia commonly containedspecies other than those specified, and most samples of alleged Arnica montana were entirelycomposed of Heterotheca inuloides (false arnica). We conclude that the likelihood ofadulteration of crude botanicals in retail commerce is taxon-specific; while most species areconsistently correctly identified, a few are often confused. One implication is that botanicalspurchased for use in research should always be independently authenticated in some fashion.

Key Words: Adulteration, dietary supplements, herbal medicine, quality control.

IntroductionAdulteration of botanical dietary supplements

is a widely publicized problem. Contrary topopular myth, the manufacture and labeling ofbotanical supplements in the U.S. is subject tostrict regulations (Soller et al. 2012). However, asin other industries, some manufacturers illegallyadulterate these products either deliberately orthrough carelessness, occasionally with serious oreven fatal health consequences. Finished dietarysupplements have repeatedly been reported tocontain risky pharmaceutical drugs and druganalogs, with certain categories of product partic-

ularly likely to be adulterated (e.g., Chen et al.2010; Gryniewicz et al. 2009; Low et al. 2009);excessive heavy metal content is also a potential

concern for certain products (e.g., Cooper et al.2007; Saper et al. 2004).

At the stage when unprocessed botanicals arepurchased by wholesalers, the most likely form ofadulteration is the inclusion, in whole or in part,of undesired species. Substitution of toxic plantspecies for non-toxic species has occasionally beenreported, e.g., in the substitution of Atropabelladonna L. for Arctium lappa L. (Bryson et al.1978), Digitalis lanata Ehrh. for Plantago majorL. (Slifman et al. 1998), Illicium anisatum L. for

Illicium verum Hook. f. (Garzo Fernndez et al.2002; Johanns et al. 2002), and Aristolochiafangchi Y.C. Wu ex L.D. Chow & S.M. Hwangfor Stephania tetrandra S. Moore (Koh et al.

1 Received 10 April 2012; accepted 4 September2012; published online ___________

Economic Botany, XX(X), 2012, pp. 17 2012, by The New York Botanical Garden Press, Bronx, NY 10458-5126 U.S.A.


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2006). The inclusion of Teucrium species (ger-mander, probably hepatotoxic in some users) inScutellaria lateriflora L. (skullcap) products con-tinues to occur to this day (Sun and Chen 2011).

These adulterations are almost always uninten-tional, unless the two species are consideredunder some traditional approach to be substitut-able, as for Stephania versus Aristolochia. Muchmore common, and more often deliberate, areeconomic adulterations with cheaper or moreeasily obtained species that, though not known tobe toxic, are sometimes likely to be less effective.Many or most of these adulterations could bedetected by careful inspection at the time ofpurchase of unprocessed materials.

In todays market, most botanicals are pro-cessed into powders or extracts before sale to themanufacturers of finished products, who often donot themselves handle unprocessed botanicals andhave no opportunity to authenticate them bymorphology. Most recent studies relating toadulteration have therefore dealt with chemicalmethods of authenticating processed botanicals,

whether finished products on store shelves orwholesale material purchased by manufacturers.However, some unprocessed or moderately pro-

cessed (e.g., cut and sifted) botanicals are divertedto the retail market, where they are available atspecialty herb shops and through Internet sales.Bulk herbs may be preferred by some consumersfor their lower price, quality, unaltered composi-tion, and/or flexibility of use. Access to these rawbotanicals is essential for an herbalist or otherknowledgeable consumer who wishes to make amixture or product type that is not commerciallyavailable. Researchers studying medicinal plantsalso sometimes purchase crude botanicals so thatthey can make their own extracts using known,controllable, and replicable methods, which theybelieve will provide some guarantee of quality intheir test substances. This raises questions about

whether the authenticity of unprocessed bulkherbs in the U.S. retail market can be relied upon.

We therefore sought to determine whetheradulterations previously reported from the sup-plement market would be found in unprocessedbotanicals sold directly to consumers. It is notclear whether the bulk herbs available to consum-ers and herbalists through retail venues are more

or less likely to be adulterated than those that areused in highly processed commercial products.Because this market is small and marginalized inthe U.S., compared to the market for dietary

supplements, the question of material quality hasattracted relatively little interest. The hypothesisof the present study was that errors similar tothose previously reported in the wholesale herb

market and in commercial products would alsoaffect whole herbs in the retail market. Contrarily,one might suppose that adulteration would be lesslikely, as some botanicals are sold in a readilyrecognizable form, and many of their purchasers(including herb shop owners and practicingherbalists) would be knowledgeable enough aboutbotanicals to notice and complain about conspic-uous errors.

The present study therefore sought to identify,in unprocessed herbs in the retail market,

adulterations comparable to those previouslyreported in the botanical industry. Its purposewas not to estimate the overall rate or frequencyof adulteration in this market across all plantspecies, but to find instances of adulteration asefficiently as possible, presuming that they werethere to be found. The study design deliberatelymaximized the likelihood of observing adultera-tion by not surveying the many botanicals that

would have been identifiable by morphology butlacked known or likely adulterants. Results are

therefore not generalizable to the entire retail herbmarket.

Material and MethodsTo facilitate identification of potential botan-

ical adulterants, a short list of botanicals for studywere selected according to the following criteria:(1) intact material of the parts used in commerceretains enough morphological characters to ade-quately authenticate the species; (2) the species

was available in an unprocessed or minimallyprocessed form from multiple vendors; (3) thespecies has been reported to be adulterated, orrelated species that could potentially be confused

with it are used commercially or occur in thesame region where it is wild-harvested. Becauseplant species are defined by morphology, mor-phological identification is the most rigorouspossible means of identification, if the availablematerial suffices to permit it. Also, examination ofmorphological and organoleptic characters (e.g.,taste, fracture) is the only means of authenticatingpurchased material that is available to herb stores

and herbalists. However, some isolated plant partscannot be unambiguously identified by morphol-ogy; for example, many roots or barks are notidentifiable to the species level, and if they are

ECONOMIC BOTANY [VOL XX


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finely cut, admixture of a second species can bevirtually impossible to detect. This study exclud-ed botanicals with known adulterants that we didnot believe we would consistently be able to

distinguish from the genuine article.Nine botanicals were ultimately selected for

sampling (Table 1). Botanicals identified by acommon name may encompass more than onespecies, with different species being permitted incommerce in different countries. Since material

was purchased on the U.S. market, the circum-scription favored in the U.S. was used (Standard-ized Common Names are given in Table 1following McGuffin et al. 2000). Eleven herbvendors were chosen, including two shops in the

state of Missouri that were physically visited andnine in other states that offered online sales.Geographic distribution of the latter representedseveral regions of the U.S., with home statesincluding Arizona, California, Colorado,

Kentucky, Minnesota, New Hampshire, Oregon,and Pennsylvania. Retailers were assigned codenumbers so that reported results would not beassociated with a specific retailer. All selected

species that were available were purchased fromeach retailer.

Some of these shops may have obtained bulkplant materials from the same wholesalers. Novendor was willing to tell us, when we identifiedourselves as researchers interested in purchasingherbs from multiple sources, who their whole-salers were. Thus, it is possible that a single sourceof adulteration could have given rise to multiplescored instances of adulterated samples receivedfrom stores that are widely separated geographi-

cally. If so, we believe that the results fairly reflectthe actual state of the market. Our interest is notin how many batches of adulterated material wereproduced, which was impossible to determine,but in how likely it is that a U.S.based researcher

Table 1. POTENTIALLY ADULTERATED, BOTANICALLY IDENTIFIABLE HERBS, WITH STANDARDIZED COMMONNAMES AND ALLOWABLE SPECIES FOLLOWING MCGUFFIN ET AL. (2000).

Botanical product Allowable species Potential adulterants

Arnica, flowering heads Arnica montana L. or North Americanspecies A. chamissonis Less.,A. cordifolia Hook., A. latifoliaBong., A. montana L.,A. sororiaGreene

Several species of Asteraceae, particularlyHeterotheca inuloidesCass. (Wichtl 2004)

Chamomile, floweringheads

Matricaria chamomilla L. Anthemis species, which are likely to beresponsible for most reports of allergicreactions (Hausen et al. 1984; Menzand Winkelmann 1987; Wichtl 2004;

Youngken 1943)Hawthorn, fruit Crataegus laevigata (Poir.) DC.,

C. monogyna Jacq., C. piperi Britton,C. rivularis Nutt.

Other species of Crataegus, including thoselegally sold in Europe or Asia as hawthornor sold in the U.S. under other commonnames (McGuffin et al. 2000; Wichtl 2004)

Juniper, pseudofruit Juniperus communis L. Other species of Juniperus (Wichtl 2004)Linden, flowers with

inflorescencesTilia cordata Mill, T. platyphyllos Scop.,

T. vulgaris HayneOther species of Tilia (Wichtl 2004)

St. Johns wort, herb Hypericum perforatum L. Other species of Hypericum (Wichtl 2004)Schisandra, fruit Schisandra chinensis (Turcz.) Baill.,

S. sphenanthera Rehder& E. H. Wilson

Potentially confusable with otherSchisandra species

Skullcap, herb Scutellaria lateriflora L. Teucrium canadense L. (Anonymous 1985;Sun and Chen 2011), a close relativeof which is hepatotoxic in some users(Larrey et al. 1992) and which is suspected

itself to be toxicStar anise, fruit Illicium verum Hook. f. Illicium anisatum L., which is toxic

(Garzo Fernndez et al. 2002; Johannset al. 2002; Small 1996; Wichtl 2004)

WALKER & APPLEQUIST: BOTANICAL ADULTERATION2012]


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or consumer purchasing one of these specieswould be supplied with adulterated material.

Botanical samples received were examinedmorphologically with the aid of a hand lens and

dissecting microscope to confirm the presence ofmorphological characters expected in the claimedspecies and the absence of characters that wouldbe expected only in known or potential adulter-ants. Morphological and organoleptic characterspertaining to the species of interest and reportedadulterants were determined by reference topharmacognostic compilations (Applequist 2006;

Wichtl 2004; Youngken 1943) and taxonomicliterature. Presence of more than a very smallamount of material having characters not consis-

tent with the stated identity was scored asadulteration; however, the proportion and taxo-nomic identity of adulterants were taken intoconsideration in evaluating the potential econom-ic or health effect of the adulteration. Statedidentity was defined by the text on the packagelabel. If only a common name was given, allspecies permitted to be sold under that Standard-ized Common Name in the U.S. according toHerbs of Commerce (McGuffin et al. 2000) wereacceptable for inclusion, whereas if a scientific

name was given, the material was expected tobelong to that species. Samples of all purchasedmaterials were retained at the Missouri BotanicalGarden (MO) to serve as vouchers.

Results and DiscussionResults are summarized in Table 2. For five of

the nine selected botanicals, no adulteration was

detected in any examined samples. These includethe species that were of most concern due tohistorical reports of toxic or potentially allergenicadulterants (Scutellaria lateriflora, Illicium verum,

and Matricaria chamomilla). The absence ofrepeatedly reported toxic or even poisonousadulterants in skullcap and star anise is certainlya positive finding. However, since a recent studyhas reported that four of 13 skullcap supplementscontained Teucrium canadense L. (Sun and Chen2011), and since the authors have seen a recentsample of commercial skullcap, not included

within this study, that was over 50 % Teucrium,it is evident that adulteration of Scutellarialateriflora does remain a serious concern and a

potential risk to health.A sixth botanical, schisandra, requires moredetailed interpretation. Two species, Schisandrachinensis and S. sphenanthera, are used inter-changeably in Chinese medicine (Chen and Chen2004; Pharmacopoeia Commission of PRC 1997)and both may be sold as schisandra in the U.S.(McGuffin et al. 2000). Our schisandra samplesdisplayed great variation in fruit size; the larger-fruited samples were identified as S. chinensis,

while four samples having very small, reddish-

brown fruits were consistent with S. sphenanthera.Three of the samples that fell into the lattercategory were labeled only, and appropriately, asschisandra, whereas one was additionally statedon the label to be Schisandra chinensis and wastherefore scored as being adulterated. Althoughthe bioactivity of the two species is not known todiffer, correct botanical identification may be

Table 2. AUTHENTICATION OF BOTANICALS OBTAINED FROM U.S.-BASED RETAIL OUTLETS. OK = IDENTITYCONSISTENT WITH CLAIMS ON PACKAGE; * = ADMIXTURE OF A MINORITY OF AN ADULTERANT; X = MOSTLY OR

ENTIRELY THE WRONG SPECIES (SEE TEXT FOR FURTHER DETAILS); N/A = BOTANICAL NOT AVAILABLE FROM THATVENDOR.

VENDOR Arnica Chamomile Hawthorn Juniper LindenSt. Johns

Wort Schisandra Skullcap Star Anise

1 X OK n/a * X OK OK OK n/a 2 X OK n/a * OK OK n/a OK OK 3 OK OK OK X X OK OK OK OK 4 X OK OK * X OK OK OK OK 5 OK n/a OK * X OK OK OK n/a 6 n/a OK OK OK OK OK OK OK OK 7 X OK OK OK X OK X OK OK

8 X OK OK X X OK OK OK OK 9 OK OK OK X OK n/a OK OK OK 10 X OK OK OK X OK OK OK OK 11 OK OK n/a n/a n/a n/a OK n/a OK



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important to some purchasers, e.g., those con-ducting pharmacognostic research, and labelclaims are legally required to be accurate.

For the three remaining botanicals in this

study, a majority of samples were adulterated atleast in part. Juniper frequently included someadmixture of fruits appearing inconsistent with J.communis. This is unsurprising, since juniper isoften collected from the wild, where it may occursympatrically with other species. It is likely thatinclusion of a small amount of some other speciesis consistent with longstanding traditional prac-tice and has little effect on quality. Linden flowerand inflorescence usually included material con-sistent with species of Tilia other than the

officially used three; a species having denselyhairy bracts was the most common adulterant.The most thorough European reference on thesubject indicates that both of these adulterationsare not uncommon (Wichtl 2004).

Finally, six of ten samples sold as arnica(including one implausibly stated to be Arnicamontana of Mexican origin) consisted wholly ofanother species identified as Heterotheca inuloides,

whose substitution for arnica is a persistentquality control problem (Pietta et al. 1994;

Wichtl 2004; Youngken 1943); genuine andadulterated samples are shown in Figs. 1a and b.Substitution may be economically motivated, asHeterotheca is a larger and, within its native range,more abundant and accessible plant, but honestconfusion might also play a role. Though theStandardized Common Name for H. inuloides inthe U.S. is false arnica (McGuffin et al. 2000), inits native Mexico it is usually called simplyarnica, and arnica is usually used to meanHeterotheca (Estrada Lugo et al. 1995; GonzlezElizondo et al. 2004; Martinez 1969; MorenoUribe 2004). The two genera have similartraditional uses, especially for bruises (EstradaLugo et al. 1995; Martinez 1969) but Heterothecais also consumed as a tea for internal inflamma-tions (Gonzlez Elizondo et al. 2004; MorenoUribe 2004) and lacks reported toxicity. Althoughmislabeling is illegal and unacceptable, knowledge-able consumers might rationally prefer false arnicaprobably safer, cheaper, and more sustainableto the genuine article. Perhaps this particularadulteration has been able to remain common for

generations in part because many buyers do notcare whether it occurs and would not bother tolook for it or to complain if they observed it. It is notknown whether the same frequency of adulteration

may be found in commercial arnica products atpresent. Although manufacturers of finished dietarysupplements often do not purchase botanicallyidentifiable material, they are legally required touse some means of authenticating their rawmaterials, and the two genera are readily distin-guished chemically.

We conclude that the likelihood of economicadulteration of bulk herbs in the retail market istaxon-specific. Some plants that have previouslyknown adulterants were never found to beadulterated, yet a few were frequently adulterated.

Accidental or deliberate admixture of relatedspecies may be most likely to persist amongspecies that are commonly wild-collected. Foreffective quality control of bulk herbs, retailersneed access to up-to-date information on whichspecies may be problematic, coupled with ageneral awareness that quality control by whole-salers cannot always be relied upon. Researchstudies using commercial herbs should always

supply some form of independent confirmation ofidentity or chemical composition. Voucher sam-ples for pharmacognostic studies cannot simplybe bagged and stored, but must be subjected to

Fig. 1. a. Authentic arnica (Arnica montana). b.Heterotheca inuloides sold as arnica.



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botanical identification, chemical fingerprinting,or some other means of authentication.

The potentially-adulterated botanicals exam-ined in this study were identifiable using tradi-

tional morphological methods which, along withorganoleptic methods (e.g., taste, odor, fracture),are the only methods accessible to herbalists orowners of herb shops. Such vendors also typicallyhandle some botanicals that cannot be definitelydistinguished from related species by appearanceand sensory characteristics, such as powderedherbs and many cut barks and roots. It is possiblethat, within the subset of botanicals that haveknown adulterants, such difficult-to-authenticatematerials could be more frequently adulterated

than those in this study, for which errors are moreeasily caught. If a morphologically unrecognizablebotanical is purchased for use in finished dietarysupplements, the manufacturer is required toperform (sometimes repeatedly) chemical ormolecular tests to confirm its identity, whereas ifit is sold to a retail vendor of unprocessed herbs,that vendor does not have similar tests performed,

which would intolerably inflate the retail cost ofbulk herbs. If a wholesaler is careless or dishonest,therefore, misidentified material directed towards

the retail herb market might be more likely toreach consumers than material that enters thedietary supplement processing stream. Thoughthe adulterations observed in this study were notdangerous, they do point out the risk thatinadequate concern for authentication of materialby vendors of bulk herbs could lead to theaccidental sale of potentially harmful herbs underthe wrong name.

AcknowledgmentsWe thank Dr. John Pruski for helpful advice

regarding identification of samples of Asteraceae,and Robert Fuqua for photographs of samples.

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