Herbal Medicine Research And Global Health: An Ethical .

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Herbal medicine research and global health: an ethical analysisJon C Tilburt a & Ted J Kaptchuk bAbstract Governments, international agencies and corporations are increasingly investing in traditional herbal medicine research.Yet little literature addresses ethical challenges in this research. In this paper, we apply concepts in a comprehensive ethicalframework for clinical research to international traditional herbal medicine research. We examine in detail three key, underappreciateddimensions of the ethical framework in which particularly difficult questions arise for international herbal medicine research: socialvalue, scientific validity and favourable risk–benefit ratio. Significant challenges exist in determining shared concepts of social value,scientific validity and favourable risk–benefit ratio across international research collaborations. However, we argue that collaborativepartnership, including democratic deliberation, offers the context and process by which many of the ethical challenges in internationalherbal medicine research can, and should be, resolved. By “cross-training” investigators, and investing in safety-monitoringinfrastructure, the issues identified by this comprehensive framework can promote ethically sound international herbal medicineresearch that contributes to global health.Bulletin of the World Health Organization 2008;86:594–599.Une traduction en français de ce résumé figure à la fin de l’article. Al final del artículo se facilita una traducción al español. . الرتجمة العربية لهذه الخالصة يف نهاية النص الكامل لهذه املقالة IntroductionTraditional herbal medicines arenaturally occurring, plant-derivedsubstances with minimal or no industrialprocessing that have been used to treatillness within local or regional healingpractices. Traditional herbal medicinesare getting significant attention in globalhealth debates. In China, traditionalherbal medicine played a prominentrole in the strategy to containand treat severe acute respiratorysyndrome (SARS).1 Eighty per cent ofAfrican populations use some formof traditional herbal medicine,2,3 andthe worldwide annual market for theseproducts approaches US 60 billion.2Many hope traditional herbal medicineresearch will play a critical role inglobal health. China, India, Nigeria,the United States of America (USA)and WHO have all made substantialresearch investments in traditionalherbal medicines.2 Industry has alsoinvested millions of US dollars lookingfor promising medicinal herbs andnovel chemical compounds.4,5 This isstill a relatively modest investmentcompared to the overall pharmaceuticalindustry; however, it raises interestingethical questions, some of which arenot faced in more conventional drugdevelopment.As attention and public fundingfor international traditional herbalmedicine research collaborationsgrows, more detailed analysis of ethicalissues in this research is warranted.Scant literature has addressed selectedissues such as informed consent andindependent review related to traditional herbal medicine research.6,7 Herewe apply a practical, comprehensiveand widely accepted ethical frameworkto international traditional herbalmedicine research.8 We examine in detail difficult questions related to socialvalue, scientific validity and favourablerisk–benefit ratio. We conclude withimplications for future research in thisarea, focusing on the importance ofcollaborative partnership.CaseA government agency from a developed country is conducting an HIVtreatment trial in Africa. A traditionalherbal medicine, Africa Flower, hasbeen used for decades to treat wastingsymptoms associated with HIV. Localtraditional medicine healers believeAfrica Flower is an effective antiviral.It is already widely used for immuneboosting in AIDS. In vitro pharmacokinetic studies suggest potentialinterference with vaccines, and animalmodels show liver toxicity at very highdoses. There are no systemic side-effectsreported for humans in the literature.A few case series have shown mixedresults. Local leaders are requesting thegovernment agency conduct a large,randomized controlled trial (RCT) ofAfrica Flower to test its efficacy as anovel adjunctive therapy to slow progression to AIDS.Ethical frameworkCases like these present challengingquestions related to the role of traditionalherbal medicines in public health.In general, international research ontraditional herbal medicines should besubject to the same ethical requirementsas all research related to human subjects.9An ethical framework previouslyoutlined by Emanuel et al. and revisedfor international research 8 offers a usefulstarting point for thinking about theethics of international traditional herbalmedicine research. This frameworkincludes eight ethical requirementsfor clinical research (Table 1). 8Department of Clinical Bioethics, National Institutes of Health, Bethesda, MD, United States of America.Osher Institute, Harvard Medical School, Boston, MA, USA.Correspondence to Jon C Tilburt (e-mail: bmitted: 2 April 2007 – Revised version received: 2 October 2007– Accepted: 25 October 2007 )ab594Bulletin of the World Health Organization August 2008, 86 (8)

Special theme – Ethics public healthEthics and herbal medicine researchJon C Tilburt & Ted J KaptchukThese ethical requirements are universaland comprehensive but must be adaptedto the particular social context in whichthe research is implemented.8 Of these,fair subject selection, independentreview, informed consent, and respectfor enrolled subjects have been discussedpreviously in the literature on theethics of global health research andraise few issues unique to internationaltraditional herbal medicine research.8However, social value, scientific validity,and favourable risk–benefit ratio raisespecific challenges in international herbalmedicine research that have not beenadequately discussed.Social valueAll research should hold the potentialto achieve social value. Different entitiesmay view the social value of traditionalmedicine research differently. Publichealth officials are often eager to definethe safety and effectiveness of herbalmedicines for conditions such asmalaria.3 Conversely, harm can arisewith the unscrupulous use of herbssuch as Africa potato (various Hypoxisspecies).7 While some claim that suchmedicines have “stood the test of time”,they nonetheless pose serious challengesto investigators and regulators fromdeveloped countries, in which standardsof proof are closely linked to provenefficacy in RCTs. Accordingly, therehas been a serious investment in herbalmedicine research by public-healthbodies in many countries. Chinarecently launched a safety researchprogramme focusing on herbal medicineinjections from traditional Chinesemedicine. 10 South Africa recentlyincluded the need for investigatingtraditional medicines within its nationaldrug policy.11In the USA, the National Centerfor Complementary and AlternativeMedicine at the National Institutes ofHealth spent approximately US 33million on herbal medicines in fiscalyear 2005; in 2004 the National Cancer Institute committed nearly US 89million to studying a range of traditional therapies.12 While this scale ofinvestment pales in comparison to thetotal research and development expenses of the pharmaceutical industry,it nevertheless reflects genuine public,industry and governmental interest inthis area.Table 1. A comprehensive framework for research ethicsEthical rch leadership must include bilateral representation basedon mutual respect between equal partners with community advice.It includes a responsibility to invest in the scientific training andcapacity-building for ongoing research in a host country where suchresources are not well developed.Social valueKnowledge gained from the research should have the potential tolead to new generalizable knowledge or improvements in health.Partners should specify in advance to whom benefits will accrue andin what way.Scientific validityResearch should be designed to produce beneficial and generalizableknowledge. This includes designing research so that it can befeasibly implemented in the settings where it will be conducted.Fair subject selectionSubjects should be selected on the basis of scientific importance, notbased on convenience, vulnerability or bias.Favourable risk–benefit ratioThe potential benefits of individual participation should outweigh therisks of participation. Benefits to the community or population beingstudied should also be optimized. Compelling societal benefit canjustify risks to individuals in certain circumstances.Independent reviewTo maintain the integrity of the research, bodies not tied to theinvestigators must agree that the risks and potential benefits of theresearch are justified.Informed consentInvestigators must obtain valid permission for study participation fromsubjects in a manner that is sensitive to the cultural context in whichthe study is conducted.Respect for subjectsResearchers should have a plan for how the research results will bedisseminated; ensuring participants know their right to withdraw, andmonitoring the research for relevant adverse events.While public-health entities maybe concerned with defining the risksand benefits of herbal medicines already in use, entrepreneurs and corporations hope herbal medicines mayyield immediate returns from herbalmedicine sales, or yield clues to promising chemical compounds for futurepharmaceutical development. Theytest individual herbs, or their components, analysed in state-of-the-art highthroughput screening systems, hopingto isolate therapeutic phytochemicalsor biologically active functional components. In 2006, Novartis reportedthat it would invest over US 100 million to investigate traditional medicinein Shanghai alone.4,5Nongovernmental organizationsmay be primarily interested in preserving indigenous medical knowledge.One such organization, the Association for the Promotion of TraditionalMedicine (PROMETRA), based inDakar, Senegal, is “dedicated to preserving and restoring African traditionalmedicine and indigenous science”. 13Governments in developing countriesBulletin of the World Health Organization August 2008, 86 (8)may want to use traditional herbalmedicine research to expand the influence of their culture’s indigenousherbal practices in the global healthcare market. For instance, Nigeria’spresident recently established a nationalcommittee on traditional medicinewith the expressed desire to boostNigeria’s market share of traditionalmedicine. 14 In developed countries,the “need” for this research may be toprotect the public.The perceived need for the researchmay justifiably differ across countries,but without some basic agreement onthe primary source of social value forthe research it may be difficult to judgeits ultimate impact. In the Africa Flowercase above, before agreements to studya herbal medicine are decided, partnersmust fully discuss potential differences about the perceived “need” forthe research through public forums orstructured debates. Based on these frankdiscussions, partners can assess whetherthe social values of partner countriesare sufficiently compatible to warrant aresearch partnership.595

Special theme – Ethics and public healthEthics and herbal medicine researchScientific validityPart of ensuring the social value ofre s e a rc h i n c l u d e s d e v i s i n g a n dimplementing sound science. Althoughinternational collaborative research onherbal medicine is no exception,discussing scientific validity as anethical requirement raises some specificchallenges, including the meaning ofscientific validity, establishing inclusionand exclusion criteria, using appropriateoutcome measures, and determiningappropriate study designs.Balancing internal and externalvalidityBuilding a valid basis for knowledge inherbal medicine will require balancingtwo aspects of scientific validity: internaland external validity.15 Internal validitymeans the research must reliably testhypothesized relationships between anintervention and an outcome undercontrolled conditions. Internally validresearch will typically try to answer afocused research question that is salientwithin the vocabulary and methods ofthe scientific community at the timethe research is conducted. Externalvalidity refers to the applicabilityof the research results to a targetpopulation outside the experimentalconditions of the research study. Externalvalidity must always be weighed againstthe need for rigorous internally validresearch.This tension between internal andexternal validity can be illustrated by arecent herbal medicine trial of Echinacea angustifolia extract for preventionof parainfluenza virus infection.16 Thestudy was conducted under rigorousexperimental conditions, but manyherbalists pointed out that study conditions did not sufficiently reflect howthese medicines are actually used. Nulltreatment trial results like these promptquestions about the external validity(i.e. value and meaning) of the research.Was the herbal medicine truly ineffective, or did the experiment not reflectthe herb’s use in “real-world” practice?In herbal medicine there are oftenhuge variations in the way in which themedicines are used in herbalist practice,including herb source, preparation,dose and indication. Because traditional herbal medicine practitionersmay be unregulated and their productslacking in standardization, it may be596Jon C Tilburt & Ted J Kaptchukdifficult to generalize the results froma formal, structured and highly monitored trial to what will happen in thewidespread dissemination of the herbalmedicine. Nevertheless, herbal medicine research must endeavour to achievea balance between internal and externalvalidity.Inclusion and exclusion criteriaTo ensure that research results are externally valid, the inclusion and exclusion criteria for research participationshould fit with existing diagnostic categories in the target population specified by the research question. However,conceptualizations of health and illnesscan vary across medical systems andpopulations, making agreement onvalid inclusion and exclusion criteriafor international herbal medicine research collaborations more difficult toachieve.During the SARS epidemic, traditional Chinese medicine (TCM) practitioners involved in the care of SARSpatients characterized patients basedon nosological categories derived fromTCM including “deficiency of chi andyin” as well as “stagnation of pathogenicphlegm”.17 Designing clinical trials using these kinds of TCM categories asinclusion criteria would require significant additional effort and biomedicalflexibility to implement. If one wantedto test whether TCM works for populations in south-east Asia affected by aSARS-like illness, adapting the scienceto include traditional diagnostic categories may be critical for its ultimateexternal validity.If American researchers want totest a herb’s effects on heart failure, theymight use the New York Heart Association classification as part of the inclusion/exclusion criteria. However, thisclassification makes little sense from aTCM perspective, in which heart failure may be viewed primarily as eithera heart yang chi deficiency or a kidneyyang deficiency.18 TCM practitionersmay prefer to categorize patients basedon pulses, tongue examination, andother elements of traditional diagnosis.Investigators have simultaneously usedboth biomedical entry criteria andstratified for TCM diagnosis.19 Such anapproach is scientifically ideal becauseof its ability to maximize the externalvalidity of results.Valid outcome measuresInternational herbal medicine researchmust use outcome measures that accurately capture the effects conferredby herbal medicines. However, constructs such as “physical functioning”or “psychological well-being” measuredby the SF-36 quality of life instrumentmake little sense within the terminology and ideas of TCM.20 Therefore toaccurately measure a TCM herb’s effectson quality of life, some investigatorshave constructed and validated analoguous measures that more faithfullydetect the effects of TCM interventions that make sense within that healing tradition. 20,21 Ideally, when newmeasures are introduced, they shouldoverlap with existing outcome measures, so that the research can adequately contribute to the existing bodyof knowledge.Determining research designWhile it is generally agreed that allhuman subjects research must maintainvalid study designs, questions ariseabout the characteristics of a validresearch design. Two extreme positionsare often defended. At one extreme,some researchers trained in biomedicalmethods of clinical investigation arguethat the only valid source of knowledgeregarding clinical efficacy must comefrom one type of research design, therandomized double blind, placebocontrolled trial. They argue that anydeviations from this gold standard ofscientific validity amount to worthlessscience.At the other extreme, critics ofbiomedical research conducted on traditional medicines charge that attemptsto evaluate traditional therapies withbiomedical methodologies may fail togenerate true knowledge, since thatknowledge itself depends on a scientificvocabulary that only makes sense fromwithin the concepts of biomedicine.22–24They worry that “standard notions of. experimental design criteria represent an imperialistic ‘western’ mode ofthinking”.22,24Research on herbal medicinesshould typically employ experimentalresearch designs such as the RCT. Evenif research tools (including the RCT)are imperfect,25 they are thus far thebest methods we have for furtheringour knowledge.9,15 Consider how RCTdesigns could be implemented in TCM,Bulletin of the World Health Organization August 2008, 86 (8)

Special theme – Ethics public healthEthics and herbal medicine researchJon C Tilburt & Ted J Kaptchukin which treatments are individualized to patients, often incorporatingseveral, or even dozens, of herbs in acustomized preparation. Despite thesecomplexities, investigators have successfully adapted double-blind RCTdesigns to complex individually tailored Chinese herbs. Bensoussan et al.conducted a three-arm trial in whichthey tested the comparative clinical efficacy of standard complex herbal medicines, customized therapy and placebo.26Standard and customized therapy werecomparably beneficial as compared toplacebo. In other instances, clusterRCTs can allow for practitioner variability, while still rigorously testing theefficacy of a therapeutic approach. Incross-cultural settings, researchers cannot merely adopt alternative designsin an ad hoc manner, but must reflecton and refine their research question,and find a design that best answers theresearch question within the given cultural context.In recent years, growing attentionhas been paid to a group of additionalimportant ethical issues surroundingpublication bias, financial conflicts ofinterest, and clinical trial registries. Inthe arena of traditional herbal medicine, these same issues apply, and whencross-cultural differences exist in thedefinitions of valid science, as is the casein traditional herbal medicine research,these questions compound. For instance,until recently, there was a tendency tosee only positive studies published inChina. It is, therefore, critically important to the long-term scientific credibility of international traditional herbalmedicine research that, at the outset,partners agree about the standardsof scientific conduct, the disclosure offinancial relationships, registration ofclinical trials, and adequate reportingof trial results.Favourable risk–benefit ratioIn international herbal medicine research, several practical challenges arisein making accurate risk–benefit determinations. Typically, in Americanpharmaceutical development, a stepwise process of drug testing occurs – acompound is isolated, tested in tissuecultures and animals, and then investigated in phase 1, 2 and 3 clinical trials.However, herbal medicines are alreadyin widespread use, are often used incombination, and are drawn from plantsources with their own variability inspecies, growing conditions and biologically active constituents. They oftencome into use by a process of trial anderror, or over centuries. Accordingly, inclinical herbal medicine research thereis rarely a strong preclinical basis fordosing, and there are significant looming questions about product purity,quality, chemical stability and activeconstituents at the time herbal medicine trials are proposed.27,28Initiating large-scale research trialsin such circumstances raises questionsabout whether the risks and benefits ofresearch participation can be accuratelyascertained. Those reviewing protocolsshould factor in the uncertainty associated with product variability indetermining whether a herbal medicinetrial has a favourable risk–benefit ratio.However, protocol reviewers (i.e. institutional review boards) should not presume that because they are personallyunfamiliar with a herbal preparationthat there is no credible or valuablebackground evidence regarding safetyand potential efficacy. While researchers should provide such informationin protocol materials, reviewers mustremain aware of the role their own lackof familiarity may play in their ultimatejudgements of risks and benefits of theresearch.Researchers increasingly agree thatit is important to establish a rationalbasis for dosing and standardization ofbiologically active compounds beforeconducting large-scale treatment trials.29,30 These efforts can improve investigators’ ability to assess the risks andbenefits of participation in large-scaleherbal medicine trials. Likewise, morerigorous monitoring of adverse eventsand standardized reporting of researchresults for both safety and efficacy datawill improve long-term efforts to enhance risk–benefit ratio determinationfor trial participation.31Cultural factors also may influencejudgements of the risks and benefitsin herbal medicine research. For instance, a cultural familiarity with manytraditional Chinese herbal medicinesin China may promote a familiaritybias, accepting a widespread culturalassumption of safety, based on the historical use of herbal medicines.32 Theremay also be a cultural difference inemphasis placed on standardized adverse events reporting in China.33 Thesecultural differences make achievingBulletin of the World Health Organization August 2008, 86 (8)agreed-upon standards of favourablerisk–benefit ratio more difficult. Inorder for international collaborativeherbal medicine research to achieve itsobjectives, it will be important to establish standards of evidence for demonstration of safety before conductinglarge-scale clinical trials evaluating theefficacy of herbal medicines.Improving science throughcollaborative partnershipHow can international collaborativeherbal medicine trials achieve theethical requirements outlined above?Collaborative partnership, the firstrequirement for international researchethics, provides both the rationale andthe context for achieving appropriateapplication of the other ethical requirements. Partners in these collaborationsmust share vocabulary for all the requirements, especially for social value,scientific validity, and favourable risk–benefit ratio. How can agreed-uponlanguage be achieved? As illustratedhere, these challenges are significant. Inthe case presented earlier, investigatorsshould have reservations about implementing a large-scale clinical trial forAfrica Flower. Nevertheless, the localinterest in this substance may be validand deserve some additional preliminary investigation. Collaborative partnership displays a commitment by allparties in international research agreements to work together for commonlanguage and goals.To achieve collaborative partnership, parties can engage in structuredmethods of democratic deliberation todevise shared language and concepts forresearch. These methods have been usedto bring different parties together in asafe and collegial process of decisionmaking.34 Over time, collaborationscould “cross-train” basic and clinicalinvestigators to more fully appreciate theconcepts and practices of the traditionalherbal medicine traditions, and developing host countries would need to develop the basic literacy, knowledge andskills among traditional medicine practitioners so that they see the value ofrigorous clinical research.2 With a sustained investment like this, it will become increasingly possible to conductsound international scientific investigation on traditional herbal medicine.Furthermore, sustainable collaborativeresearch partnerships would benefit597

Special theme – Ethics and public healthEthics and herbal medicine researchfrom robust and independent adverseevent reporting systems for herbalmedicines so that the risk–benefit ratiofor herbal medicine research can bemore clearly defined.Ethical challenges in internationaltraditional herbal medicine call for acomprehensive framework. Addressingthese challenges requires collaborativeJon C Tilburt & Ted J Kaptchukpartnership that implements soundresearch designs. So envisioned, international herbal medicine research cancontribute to global health. AcknowledgementsFranklin G Miller and Jack Killen generously read and offered helpful suggestions on earlier versions of this paper.Funding: TJK is a consultant for KanHerbal Company, Scotts Valley, CA,USA. Partial funding for TJK was provided by the National Center for Complementary and Alternative Medicineat the National Institutes of Health,Bethesda, MD, USA.Competing interests: None declared.RésuméRecherche en phytothérapie et santé dans le monde : analyse éthiqueLes gouvernements, les agences internationales et les entreprisesinvestissent de plus en plus dans la recherche en phytothérapietraditionnelle. Cependant, les difficultés éthiques de cetterecherche sont peu abordées dans la littérature. Dans cetarticle, nous appliquons les concepts d’un cadre éthiquecomplet à la recherche clinique en phytothérapie traditionnelleinternationale. Nous examinons en détail trois dimensions sousestimées et essentielles du cadre éthique, dans lesquelles seposent des problèmes particulièrement difficiles pour la rechercheinternationale en phytothérapie : la valeur sociale, la validitéscientifique et le ratio risque/bénéfice favorable. La définition deconcepts partagés pour la valeur sociale, la validité scientifiqueet le rapport risque/bénéfice favorable applicables à l’ensemblede la recherche en collaboration internationale se heurte à desdifficultés majeures. Nous affirmons néanmoins que le partenariatcollaboratif, et notamment la délibération démocratique, offrele contexte et le processus pouvant et devant permettre derésoudre beaucoup des problèmes éthiques rencontrés dansla recherche internationale en phytothérapie. Moyennant une« formation croisée » des chercheurs et des investissementsen infrastructures de surveillance de l’innocuité, l’identificationdes problèmes par ce cadre complet favorisera une rechercheen phytothérapie internationale valable sur le plan éthique etcontribuera à la santé dans le monde.ResumenInvestigación fitoterapéutica y salud mundial: análisis éticoGobiernos, organismos internacionales y empresas estáninvirtiendo cada vez más en la investigación de medicamentosherbarios tradicionales. Sin embargo, son escasas laspublicaciones que abordan los problemas éticos asociados aesas investigaciones. En este artículo aplicamos los conceptosmanejados en un marco ético amplio de regulación de lasinvestigaciones clínicas a las actividades internacionalesde investigación de medicamentos herbarios tradicionales.Examinamos en detalle tres dimensiones clave pero subestimadasdel marco ético en las que se plantean cuestiones particularmentedifíciles para la investigación internacional de esos medicamentos:valor social, validez científica y relación riesgo-beneficio. Elproceso de consenso en torno a lo que deba entenderse porvalor social, validez científica y relación riesgo-beneficio favorableen las investigaciones internacionales en colaboración entrañaretos importantes. Sin embargo, sostenemos que hay fórmulasde colaboración, en particular la deliberación democrática, quebrindan un contexto y unos procedimientos mediante los quese pueden, y se deben, resolver muchos de los dilemas éticosasociados a las investigaciones internacionales en materia demedicina herbaria. Formando de manera interdisciplinaria a losinvestigadores e invirtiendo en infraestructuras de vigilancia dela seguridad, las cuestiones identificadas mediante este marcointegral pueden fomentar la realización de investigacionesinternacionales de medicamentos herbarios éticamente válidasque contribuyan a la salud mundial. ملخص والنسبة بني املخاطر واملنافع يف جميع مستويات التعاون البحثي ، العلمية مبا يف ذلك املشاورات التي ، غري أن الباحثني يرون أن الرشاكة التعاونية . الدويل أن ، بل ينبغي ، توفر السياق والخطوات التي ميكن ، ُتجرى بطريقة دميقراطية ُيحل من خاللهام العديد من التحديات األخالقية يف البحوث الدولية يف مجال أن ، وميكن للقضايا التي يحددها هذا اإلطار الشامل للعمل . طب األعشاب والتي تسهم ، تعزز البحوث الدولية السليمة أخالقياً يف مجال طب األعشاب وذلك عن طريق التدريب املتعدد التخصصات ، يف تعزيز الصحة يف العامل . واالستثامر يف البنية التحتية لرصد السالمة ، للباحثني 598 تحليل للجوانب األخالقية : والصحة يف العامل ، بحوث طب األعشاب يتزايد إقبال الحكومات والوكاالت والرشكات الدولية عىل االستثامر يف بحوث غري أن القليل من الدراسات املنشورة تتصدى للتحديات . طب األعشاب ، ويف هذه الورقة يطبق الباحثون بعض املفاهيم . األخالقية يف هذه البحوث عىل بعض البحوث الدولية ، يف إطار عمل أخالقي شامل للبحوث الرسيرية ويدرس الباحثون بالتفصيل ثالثة أبعاد . يف مجال طب األعشاب التقليدي والذي ُتطرح فيه ، رئيسية لإلطار األخالقي ال تلقى ما تستحقه من التقدير القيمة : وهي ، أسئلة صعبة تدور يف مجال البحوث الدولية لطب األعشاب وتوجد . والنسبة بني املخاطر واملنافع ، واملوث

Medicine (PROMETRA), based in Dakar, Senegal, is “dedicated to preserv-ing and restoring African traditional medicine and indigenous science”.13 Governments in developing countries may want to use traditional herbal medicine research to expand the in-fluence of their culture’s indi