SYNTHESIS OF EVIDENCE SUBSTANTIATING POTENTIAL INTERVENTIONS

A Systematic Review of Barriers and Facilitators to Minority Research Participation Among African Americans, Latinos, Asian Americans, and Pacific Islanders

To assess the experienced

or perceived barriers and

facilitators to health research

participation for major US

racial/ethnic minority popu-

lations, we conducted a sys-

tematic review of qualitative

and quantitative studies

from a search on PubMed

and Web of Science from

January 2000 to December

2011.

With 44 articles included in

the review, we found distinct

and shared barriers and fa-

cilitators. Despite different

expressions of mistrust, all

groups represented in these

studies were willing to par-

ticipate for altruistic reasons

embedded in cultural and

community priorities.

Greater comparative un-

derstanding of barriers and

facilitators to racial/ethnic

minorities’researchparticipa-

tion can improve population-

specific recruitment and

retention strategies and

could better inform future

large-scale prospective quan-

titative and in-depth ethno-

graphic studies. (Am J Public

Health. 2014;104:e16–e31.

doi:10.2105/AJPH.2013.

301706)

Sheba George, PhD, Nelida Duran, RD, MS, and Keith Norris, MD

THE IMPORTANCE OF RACIAL

and ethnic minority participation in clinical research has been well established including, but not limited to, generalizability of research findings,1,2 equity in provision of health care,3,4 and accuracy of ethnicity-specific subgroup analyses.5,6 Despite a series of national-level initia- tives in the past 2 decades from the National Institutes of Health,7 the Federal Drug Ad- ministration (FDA),8 and the Centers for Medicare and Med- icaid Services,9 racial and ethnic minorities remain underrepre- sented in clinical research.10,11

Racial/ethnic minorities consti- tute more than 30% of the US population, but enrollment by race/ethnicity of National Can- cer Institute publicly funded cancer clinical trials (phase I---III treatment studies, January 1, 2003, through June 30, 2005) revealed that they represented less than 18% of clinical trial participants.12 Evelyn et al. reported that racial/ethnic mi- norities constituted only 17% of FDA clinical trial participants in 185 studies of new molecular entities over a 5-year period.13

Several barriers to participation of racial and ethnic minorities in clinical research have been iden- tified for both researchers and participants. For researchers, lack of knowledge about the cultural differences among ethnic minori- ties can result in ineffective com- munication strategies about health research at all stages, including

recruitment, enrollment, and re- tention. Because research has historically been conducted by White researchers and has tar- geted mostly White research par- ticipants, the “gold standards” with regard to research processes have tended to include incorrect assumptions about effectiveness when unquestioningly transferred to ethnic minority populations. For example, researchers’ inap- propriate use of recruitment strategies among racial/ethnic minority groups that were devel- oped for White participants and lack of knowledge about how to culturally and linguistically adapt recruitment materials have been noted concerns.1,14,15

Given the paucity of evidence- based strategies and practices in the literature regarding non-White populations, recruitment of mi- norities can require additional in- vestments of time and resources to learn what methods may work in distinct communities to im- prove community acceptance of clinical research and thus improve participation.14,16 Cultural and linguistic adaptation of recruit- ment strategies may include not only the selection of appropriate venues, methods, and topics of focus when addressing the gaps in knowledge about research among a particular minority group14,17,18

but also the translation of mate- rials into appropriate languages and the implementation of such strategies by culturally and lin- guistically competent research staff.19,20

In addition, many researchers fail to facilitate culturally sensitive and meaningful discussions about informed consent to ensure truly informed choices in the enroll- ment process21,22 For example, although obtaining consent from a research participant is often practiced as a 1-time occurrence, research indicates that consent should be considered an ongoing process—a dialogue—rather than a discrete act of choice that takes place in a singular moment in time, thus supporting participants in making informed decisions throughout the trial.23 Moreover, among many culturally diverse and immigrant populations, it may be important to include fami- lies and communities in a dialogue around research participation de- cisions because individual deci- sions to participate in research are frequently not independent of family and community involve- ment, benefits, and costs.2,24,25

Furthermore, once participants have been recruited and enrolled in studies, research success is more likely if culturally informed reten- tion strategies are used to engage such populations in research.2,26,27

Some suggested strategies focus on partnering with community orga- nizations, including investigators and staff from the same targeted communities as participants and retaining the same staff and in- terviewers over time to ensure continuity.20,28,29 Such efforts can increase likelihood of greater rap- port and trust building between study staff and participants and

SYSTEMATIC REVIEW

e16 | Systematic Review | Peer Reviewed | George et al. American Journal of Public Health | February 2014, Vol 104, No. 2

improved adherence to study protocol by participants.

For racial- and ethnic-minority participants, the concerns have ranged from psychosocial issues such as mistrust, fear, and lack of confidence to logistical con- cerns including childcare, sched- ule conflicts, lack of transporta- tion, and appropriate support to research-related factors such as lengthy consent documents and lack of adequate information about clinical research.1,2,10,30

Several studies raise questions about both overt and subtle forms of racism and discrimination at multiple levels that may lead to barriers and the underrepresen- tation of ethnic minority popula- tions in health research.31---34

Barriers to minority participation in health research resulting from such racism can occur at different levels, from institutional to inter- personal to internalized levels of racism.35

The continuing effects of slav- ery and colonization at a systemic institutionalized level have mani- fested in ongoing health inequal- ities through differential access to health care and poor health out- comes for racial/ethnic minorities in the United States.35---37 The US Public Health Services Syphilis Study at Tuskegee (Tuskegee Study) among African Americans and efforts to sterilize American Indians are some egregious ex- amples of a dark history of sys- tematic abuse and mistreatment both in health care and medical research for racial and ethnic mi- norities in the United States.38---40

As a consequence, mistrust of the medical establishment and of medical research has been well documented among minority groups and continues to be a formidable barrier to research participation among these popu- lations.1,31,32,41---43

Racism at the interpersonal level is often manifested in prej- udicial and discriminatory acts resulting in poor health care ex- periences and health outcomes for racial/ethnic minorities.42,44---47

Poor mental and physical health outcomes, delay or failure in seeking preventive services and treatment, and poor adherence behaviors have all been associated with reported experiences of dis- crimination among racial/ethnic minorities.46,48 Patients with such experiences are also less likely to participate in health research, contributing to the overall lower numbers of racial/ethnic minori- ties in clinical research.27,49,50

Finally, at the level of internal- ized racism, stigmatized popula- tions accept negative messages and stereotypes about their own abilities and worth, resulting in lower psychological health and lower self-esteem, which can then have a negative effect on health practices and outcomes. Internal- ized racism has been associated with psychological and physiolog- ical negative effects, ranging from emotional distress and alcoholism to increased risk of obesity, high blood pressure, and high fasting blood sugar.51---54 More relevant to the current topic of minority participation in research, internal- ized racism can also adversely affect the provider---patient relationship to potentially impede communication abilities of the patient, leading to discounting of information from the provider, delays, or failure to obtain needed medical care and lower levels of adherence.55

The same stereotypes and negative messages internalized by minorities may also shape providers’ and health care orga- nizations’ interactions with mi- norities. For example, in the case of African American women, a range of socially constructed

stereotypical images of “mammy, strong matriarch, welfare mother, female overachiever, etc.” can influence diagnoses and treat- ment choices made for African American female patients.56(p32)

Given that strong provider---patient relationships have been shown to be key to minority participation in research,57,58 these deleterious ef- fects of internalized racism on the provider---patient relationships may ultimately negatively affect deci- sions of minorities to participate in health research. Notwithstanding these barriers, some studies have suggested that minorities are not necessarily less willing than Whites to participate in clinical research, especially in cancer research studies.59,60

The literature on racial- and ethnic-minority participation in clinical research has burgeoned over the past decade, gauging by several systematic reviews on the topic.1,10,15,30 However, most of this scholarship has focused on African Americans,10,41 in light of a prevailing mistrust of clinical research in the Black community stemming from the historical abu- ses associated with the Tuskegee Study and related concerns of ethical misconduct.61---63 There are fewer studies that have included a range of racial and ethnic pop- ulations, resulting in less infor- mation about the barriers and facilitators to participation in clinical research for a variety of groups.10,41,64 A recent systematic review of the literature on re- cruitment interventions showed that African Americans were the most targeted group (82% of the studies) and Latinos were also likely to be targeted (46%), but specific information on other mi- nority groups was not included.15

Given the growing racial and eth- nic diversity in the US population and as Latinos are the largest

minority group and Asian and Pacific Islander populations are growing at a rate greater than any other group, such multiethnic analyses will become increasingly important.65

The existing literature reflects a trend of including 1 or 2 mi- nority groups, but few studies have compared across several groups. An exception is a study by Brown and Moyer who used a nationally representative sam- ple to compare predictors of awareness of clinical trials and feelings about the use of medical information for research across African American, Asian Ameri- can, White, and Latino popula- tions.66 The authors found that, relative to the White population, all other racial/ethnic minority participants were less aware of clinical trials and less positive about the use of medical infor- mation for research. Although this study identifies who is likely to participate in research, it does not identify specific barriers and facilitators for these different groups.

In a similar way, a collaborative research initiative entitled Project MICRO (Minority Involvement in Clinical Research Opportunities) is a multi-institutional (University of Hawaii, Charles Drew Univer- sity, Morehouse College, Meharry Medical College, University of Puerto Rico), multicultural (West Coast and Southern African American, Mexican, Puerto Rican, Filipino, Chinese, Pacific Islander, Somali, White), multilingual (En- glish, Spanish, Chinese, Samoan, Tagalog, Ilocano, Hawaiian, So- mali), and multigeographic Na- tional Institutes of Health (NIH)--- funded study that sought to identify predictors of research participa- tion by gaining a better under- standing of the factors that impede or enhance such participation

SYSTEMATIC REVIEW

February 2014, Vol 104, No. 2 | American Journal of Public Health George et al. | Peer Reviewed | Systematic Review | e17

among diverse racial/ethnic groups.41 This study was a first effort to address the need for comparative research about atti- tudes, beliefs, barriers, and facil- itators to minority research par- ticipation across racial/ethnic groups in multiple geographic regions.41,67 The qualitative findings from Project MICRO showed both distinct barriers and facilitators based on histori- cal and cultural factors specific to each of the groups and shared barriers and facilitators based on socioeconomic and environmen- tal factors that were shared among the 4 distinct racial/ethnic groups (African Americans, Latinos, Native Hawaiians, and Filipinos). There were several distinct bar- riers, but the only barrier that was shared by all the groups was lack of information about clinical research.67

With the growing rates of ra- cial/ethnic multicultural popula- tions come growing rates of health disparities and disease burden among them and, consequently, the increasing importance of their participation in clinical research. Without assuming that all such minority groups have the same barriers and facilitators, it is im- portant to identify context-specific culturally shared and distinct fac- tors that deter or enhance their participation in clinical research. When factors that are relevant across multiple racial/ethnic groups are identified, interven- tions that address common issues can then be developed on a broad platform and adapted to meet the particular specificities of targeted racial/ethnic groups. When such recruitment mate- rials resonate with racial/ethnic minority communities, they are more likely to participate effec- tively in clinical research. Fur- thermore, interventions can be

developed more efficiently and in a cost-effective manner by leveraging recruitment efforts across multiple groups and their shared barriers and facilitators.

The ability of medical science advances to reach all Americans is predicated upon the participation of diverse study participants in an array of clinical trials and is ech- oed in the NIH’s call for trans- lational research over the past decade. Successful translational research requires not only inno- vative strategies for the recruit- ment and retention of diverse populations into research but also increased investments into com- munity education and the dissem- ination of results. However, there is little understanding of what are the key barriers and facilita- tors to address for which popula- tions or what the driving issues around recruitment and retention and general community education are as they relate to clinical research.

We present a systematic review of the existing literature of both qualitative and quantitative stud- ies that include multicultural racial/ethnic participant voices to identify the range of themes and papers and that take a compara- tive perspective in their assess- ment of barriers and facilitators to participation in health research. To the best of our knowledge, this is a first effort to do so. We have broadly defined “health research” as health-related research involv- ing human participants in clinical trials, clinical research, and be- havioral health interventions to be as inclusive as possible.

METHODS

The Preferred Reporting Items for Systematic Reviews and Meta- Analyses (PRISMA) statement consists of a 27-item checklist and

a 4-phase flow diagram to help authors improve the complete reporting and transparency of systematic reviews and meta- analyses.68 As necessary, some of the items on the PRISMA checklist may be modified.69 We conducted a systematic review in conformance with modified items of the PRISMA Statement to an- swer the following question: among major US racial/ethnic mi- nority populations, what are the experienced or perceived barriers and facilitators to participating in health research?

We chose the PubMed and Web of Science databases for their complementary content to con- duct the literature search. PubMed provides biomedical and health content related to the life sciences, behavioral sciences, chemical sci- ences, and biomedical engineer- ing, whereas Web of Science pro- vides multidisciplinary content on the sciences, social sciences, arts, and humanities. PubMed and Web of Science are proprietary databases for peer-reviewed jour- nal content that provide the ability to conduct transparent, controlled, and powerful searches.70,71 The decision to not conduct a search on Google Scholar limits the content of this review to peer- reviewed articles and inherently excludes gray literature and sub- sequently the results of recent studies presented at conference proceedings or institutional publi- cations. Furthermore, although Google Scholar may have allowed for greater inclusion of online and open-access journals in our search process,72 we excluded this search engine because repli- cability of searches, an extremely important factor for systematic reviews, cannot be ensured be- cause of the “constantly-changing content, algorithms and database structures” of Google Scholar.73(p214)

We selected titles, abstracts, and articles on the basis of the following eligibility criteria. We reviewed only English-language articles published in the United States between January 2000 and December 2011. We generally adhered to the norm of a maxi- mum time frame of 5 to 10 years in selecting the time frame for this review to ensure the most current and relevant articles.74 The target population of interest in the article had to include at least 1 of the following adult racial/ethnic mi- nority populations: African Amer- ican, Latino, Asian American, or Asian---Pacific Islander. We limited the search to the United States to account for the health care context that is unique to US residents, such as its particular history of racism with regard to health care provision and research, most infamously exemplified in the Tuskegee Study, and the lack of universal health care in the United States unlike most other devel- oped nations. The literature search related to the barriers (and facilitators) to health research participation perceived by adult African American, Latino, Asian American, and Asian and Pacific Islander populations. We did not include American Indians and Alaska Natives in this review because Indian Health Services presents a unique context for health care and research that is not available to other racial/eth- nic minorities.

Key terms used for the litera- ture search included racial/ethnic minority (e.g., African American, Latino, Pacific Islander, Asian American, or their derivative); health research study, clinical trial, and clinical research (or its derivative); and participation, ac- cess, recruitment, barriers, and facilitators (to health research). Examples of search strings

SYSTEMATIC REVIEW

e18 | Systematic Review | Peer Reviewed | George et al. American Journal of Public Health | February 2014, Vol 104, No. 2

included “research participation barriers among Latinos” and “African American AND research AND participation” as described in the search plan in Appendix 1 (available as a supplement to this article at http://www.ajph.org). In addition, the study’s method- ology had to be clear and at least 1 of the study’s aims had to use primary data to evaluate or assess the barriers or facilitators to par- ticipation in health research. We limited quantitative studies to those that surveyed self-reported factors that contributed to

barriers and facilitators, and in- dividuals’ attitudes, beliefs, and values related to health research participation. We excluded stud- ies with target populations youn- ger than 18 years. We also excluded articles that did not provide the barriers or facilita- tors to health research participa- tion from the perspective of the racial/ethnic---minority partici- pant. We focused on articles that provided a voice to racial/ ethnic---minority populations and, therefore, we excluded studies that reported the perspectives of

research staff, physicians, or in- stitutions.

We initially retrieved a total of 164 articles from the systematic literature search by using the search terms in Appendix 1 (available as a supplement to this article at http://www.ajph.org); 21 articles were duplicates (Figure 1). Duplicate articles occurred because articles appeared in both the PubMed and Web of Sciences databases, or when the articles with more than 1 target racial/ethnic minority population would appear in searches for each

individual racial/ethnic minority population. We screened the remaining 143 titles for their rel- evance to the research question of this review and we excluded 27 literature reviews, commentaries, and editorials. We reviewed the remaining unique full-text articles (n = 116) from the combined searches on PubMed and Web of Science and we excluded 72 for not meeting the inclusion criteria; thus, we included 44 articles in the review.

We abstracted data in a stan- dardized format and organized the data into tables that included the author’s names, title of the article, year of publication, target population, age of target popula- tion, methodology including whose perspective was being reported, and key findings related to the barriers and facilitators to participation in health research. We coded the studies for racial/ ethnic minority population, meth- odology (i.e., qualitative, quantita- tive, or mixed methods), distinct barriers and facilitators to partici- pation, and shared barriers and facilitators to participation, and grouping of themes across shared barriers and facilitators. Two au- thors (S. G. and N. D.) coded the findings of the barriers and facili- tators in an iterative process. The consistency between the coders was more than 90% and they resolved conflicts by using an it- erative process and discussion to reach consensus.

RESULTS

The articles presented in this review provide the perspectives of racial/ethnic minorities across age and socioeconomic status re- garding participation in health research. Of the 44 articles included, 23 used qualitative methods such as focus groups

Records identified through database searching (n = 164)

Sc re

en in

g In

cl u

d ed

El ig

ib ili

ty Id

en ti

fi ca

ti o

n

Records after duplicates removed (n = 143)

Records screened (n = 143)

Records excluded that were literature reviews,

commentaries, and editorials

(n = 27)

Full-text articles assessed for eligibility

(n = 116)

Full-text articles excluded: target populations resided outside the United States, were under 18 years, did not include at least 1 of

the racial/ethnic minority populations of interest or

their perspective (n = 72)

Studies included in qualitative synthesis

(n = 44)

Note. Adapted from Moher et al. 75

FIGURE 1—Flow diagram for systematic review of qualitative and quantitative studies regarding the

experienced or perceived barriers and facilitators to participating in health research for major US racial/

ethnic minority populations from a search on PubMed and Web of Science from January 2000 to

December 2011.

SYSTEMATIC REVIEW

February 2014, Vol 104, No. 2 | American Journal of Public Health George et al. | Peer Reviewed | Systematic Review | e19

and individual interviews, 16 ar- ticles used quantitative methods that statistically analyzed data collected through question- naires, and the remaining 5 arti- cles used mixed methods (Table 1). Sixteen studies were exclu- sively conducted among Afri- can Americans, 6 among Asian Americans, 3 among Latinos, and 1 among Pacific Islanders; the remaining 18 studies included a combination of at least 2 racial/ ethnic minority groups including White populations that were often used as the reference group. Asian Americans were primarily represented by peo- ples of East Asia and Southeast Asia, and Pacific Islanders were represented by Native Hawai- ians, Samoans, and Tahitians. Latinos were overwhelming rep- resented by Mexican Americans and immigrants from Mexico; also represented were peoples of Puerto Rico and Central Amer- ica. A number of studies did not

differentiate the country of origin of Latinos and Hispanics.

Many of the studies focused on women (14 of 44) or had an overrepresentation of women (66.5%; n = 5353), whereas only 1 study focused exclusively on men (Appendix 2, available as a supplement to this article at http://www.ajph.org). A few stud- ies (n = 11) utilized bilingual staff or translated materials for non--- English-speaking participants who immigrated from Latin America or Asia. Nonspecific health research studies (n = 14) dominated the literature, fol- lowed by cancer (n = 11) and HIV/AIDS (n = 11), and other health topics (n = 8; Table 2). The nonspecific health research was often referred to as medical research or hypothetical re- search. Other disease-specific studies included in this review focused on Alzheimer’s disease, kidney disease, and hyperten- sion, along with pregnancy and

genetic-related conditions. The results of the coded findings are summarized in the next section.

Shared and Distinct Barriers

and Facilitators

The terms shared and distinct represent the relatively commonly and uncommonly reported bar- riers and facilitators reported in the articles on the 4 racial/ethnic communities included in this re- view. The concordance of mes- sages across studies suggests that certain themes may be shared or distinct as a greater or lesser pri- ority for a particular community but they are not necessarily dis- tinct in the sense that those bar- riers or facilitators are exclusive to a particular community. It is im- portant to note that the shared and distinct barriers and facilita- tors presented were drawn from a comparison of the limited num- bers and types of studies included in this review and not from a comparison of the underlying

populations. As described in Ap- pendix 2 (available as a supple- ment to this article at http://www. ajph.org), the studies included in this review vary considerably in the extent to which they represent various populations. As a conse- quence, on the basis of the avail- able number and types of studies of a specific population, we can only present examples of mean- ings of a barrier or facilitator for a given population expressed in the set of studies included in this review but cannot say very much about the distribution or impor- tance of this barrier or facilitator in the defined population. Thus, observations are limited to the articles for this review and are not representative general statements about the populations under study and may allow us to make only explorative generalizations.

Both quantitative and qualita- tive research findings included in this review provided observations related to the shared barriers and facilitators, whereas the distinct barriers and facilitators were ex- clusively observed in the qualita- tive research findings. Further- more, the examples of shared and distinct barriers and facilitators presented in the tables are not exclusive to a group but rather illustrative of the observations made from the studies reviewed.

Shared Barriers

The shared barriers to health research participation that were

TABLE 1—Distribution of the Reviewed Articles by Method and Target Population Regarding Barriers and Facilitators to Health Research

Participation for US Racial/Ethnic Minority Populations From a Search on PubMed and Web of Science From January 2000 to December 2011

Article Type Total, No. (%) African American, No. (%) Asian American, No. (%) Latino, No. (%) Pacific Islander, No. (%) ‡ 2 Racial/Ethnic Groups, No. (%)

Qualitative 23 (52.3) 10 (22.7) 3 (6.8) 2 (4.5) 1 (2.3) 7 (15.9)

Quantitative 16 (36.4) 3 (6.8) 3 (6.8) 0 0 10 (22.7)

Mixed methods 5 (11.4) 3 (6.8) 0 1 (2.3) 0 1 (2.3)

Note. Total number of articles in the review was 44.

TABLE 2—Distribution of the Reviewed Articles by Health Condition Regarding Barriers and Facilitators

to Health Research Participation for US Racial/Ethnic Minority Populations From a Search on PubMed

and Web of Science From January 2000 to December 2011

Article Type Nonspecific Health Condition, No. (%) Cancer, No. (%) HIV/AIDS, No. (%) Other, No. (%)

Qualitative 7 (15.9) 8 (18.2) 5 (11.4) 3 (6.8)

Quantitative 5 (11.4) 3 (6.8) 5 (11.4) 3 (6.8)

Mixed methods 2 (4.5) 0 1 (2.3) 2 (4.5)

Total 14 (31.8) 11 (25.0) 11 (25.0) 8 (18.2)

Note. Total number of articles in the review was 44.

SYSTEMATIC REVIEW

e20 | Systematic Review | Peer Reviewed | George et al. American Journal of Public Health | February 2014, Vol 104, No. 2

reported across all 4 racial/ethnic groups included mistrust and lack of access to information (Table 3). Lack of access to information as reported in the studies reviewed among Asian Americans, Latinos, and Pacific Islanders pointed to language barriers as a key to per- ceived lack of access to informa- tion among these 3 groups. Other barriers included competing de- mands that conflicted with ability to participate in research, fear of unintended outcomes, stigma, and issues related to health insurance coverage and legal status, which were all reported in 2 or more groups. Mistrust. Mistrust was a reported

barrier across all 4 racial/ethnic minority groups and appeared in 77.3% (n = 34) of all articles in- cluded in this review (Table 3). Among the studies with African Americans, mistrust was frequently associated with the perception that research will benefit Whites or the research institution and not people of color.62,76,90---96 In a sim- ilar way, Native Hawaiians have reported a mistrust related to the researcher’s agenda not serving the community.97 Mistrust related to the fear of purposeful mistreat- ment and experimentation was often characterized as being treated like a “lab rat” or “guinea pig.”32,67,81,83,84,97---99 Mistrust with signing the informed consent was related to the perception that individuals are relinquishing their rights93 and providing the researcher with legal protection against any harm that may be inflicted onto the participants.91

Competing demands. Time98 and financial constraints related to the competing demands of working multiple jobs and needing to work, being the primary caretaker of children and or relatives, being the single head of household,90,93 and justifying the cost of participation

with the perceived high risk for a disease.85

Unintended outcomes. Unin- tended outcomes, such as the un- certainty of short- and long-term side effects or the uncertain effec- tiveness of the intervention under study may provoke participants to consider the benefits and risks to participation. The possible interfer- ence with current treatments92 or the lack of access to health care should injury100 or a disease di- agnosis90 arise were examples of unintended outcomes that weigh into the decision of participating in health research. More specific to the study of HIV vaccines was the fear of vaccine-induced HIV infection.82

Lack of access to information. A lack of informational access about research opportunities was a barrier that was reported across all 4 racial/ethnic minority groups and represented in 31.8% (n = 14) of the articles. The absence of bilingual research staff and informational material were reported to be barriers among non--- or limited---English-speaking racial/ethnic populations that have demonstrated an interest in participating in health re- search.41,67,78 Although research participation is viewed as unnec- essary among those who perceive their risk for disease as low, re- searchers warn that individuals may be misperceiving their actual risk85 or delaying access to health care until there is an urgent need.90 The misperceived risk may also result from a lack of information regarding their health and risk of disease. Stigma. Stigma is understood

to occur when labeling, stereotyp- ing, separation, status loss, and discrimination co-occur in the context of an unequal power situ- ation that permits stigma to oc- cur.101 Stigma was often related to

TA B LE

3 — E xa m p le s o f S h a re d B a rr ie rs

to H e a lt h R e se a rc h P a rt ic ip a ti o n a s O b se rv e d in

th e S tu d ie s R e vi e w e d F ro m a S e a rc h o n P u b M e d a n d W e b o f S c ie n c e

F ro m Ja n u a ry 2 0 0 0 to

D e c e m b e r 2 0 1 1

Ra ci al /E th ni c G ro up

O bs er ve d Ex am pl es

Ba rr ie rs

Ar tic le s, N o. (% )

Af ric an

Am er ic an

As ia n Am er ic an

La tin o

Pa ci fic

Is la nd er

M is tr us t

34 (7 7. 3)

Pe rc ei ve re se ar ch

w ill be ne fit W hi te s or th e

re se ar ch in st itu tio n an d no t pe op le of co lo r7 6

Co nc er ns

re la te d to si gn in g th e in fo rm ed

co ns en t7 7

Be lie ve m ed ic al ex pe rim

en ta tio n oc cu rs

w he n ac ce ss in g he al th ca re 6 7

N eg at iv e fe el in gs ab ou t th e pu rp os e

an d in te nt of re se ar ch 4 1

Co m pe tin g de m an ds

20 (4 5. 4)

In co nv en ie nc e6 2 ; co st of pa rt ic ip at io n3 4

La ck

of tim

e7 8 an d fin an ci al re so ur ce s7 9

Ti m e co nfl ic ts an d la ck

of ch ild ca re 6 7

U ni nt en de d ou tc om es

14 (3 1. 8)

Co nc er ns

ab ou t fu tu re lo ng - an d sh or t- te rm

si de

ef fe ct s8 0

U nc er ta in ty of ris ks , si de

ef fe ct s, an d

ef fe ct iv en es s of cl in ic al tr ia ls 8 1

Fe ar of va cc in e- in du ce d H IV in fe ct io n8 2

La ck

of ac ce ss

to in fo rm at io n

14 (3 1. 8)

M is co nc ep tio ns

ab ou t re se ar ch 8 3

Li m ite d kn ow le dg e ab ou t cl in ic al tr ia ls 8 4 ;

la ck of tra ns la te d m at er ia ls , in cl ud in g ke y

wo rd s or te rm s; fe el in g in tim id at ed

by En gl is h7 8

U na va ila bl e he al th in fo rm at io n in Sp an is h

an d la ck

of ac ce ss to Sp an is h- sp ea ki ng

st af f6 7 ; lo w pe rc ei ve d ris k of di se as ea ,8 5 ,8 6

In fo rm at io n ab ou t ac ce ss in g

re se ar ch

8 7 ; la ng ua ge

ba rr ie r be tw ee n

ho sp ita ls ta ff, re se ar ch er s, an d pa tie nt s4 0

St ig m a

12 (2 7. 3)

Re la te d to ge ne tic

or m en ta l ill ne ss re se ar ch

8 8

Re la te d to ju dg m en t fr om

hu sb an d or fa m ily

fo r pa rt ic ip at io n in he al th st ud y7 9

Re la te d to H IV -p os iti ve st at us 8 9

H ea lth

in su ra nc e

co ve ra ge

3 (6 .8 )

H av e ba si c he al th ca re or no

sp ec ifi c he al th

ca re ne ed s9 0 ; fe ar of di sc rim

in at io n8 8

La ck

of in fo rm at io n ab ou t in su ra nc e

co ve ra ge

fo r cl in ic al tr ia ls 7 7

Le ga l st at us

in

U ni te d St at es

2 (4 .5 )

Co nc er ne d im m ig ra tio n st at us

w ill be

af fe ct ed

am on g im m ig ra nt s7 9

Fe ar of de po rt at io n am on g im m ig ra nt s6 7

a L ow

pe rc ei ve d ris k of di se as e is a sh ar ed

ba rr ie r fo r Af ric an

Am er ic an s an d La tin os .

SYSTEMATIC REVIEW

February 2014, Vol 104, No. 2 | American Journal of Public Health George et al. | Peer Reviewed | Systematic Review | e21

the health condition of interest in the research study such as HIV infection or mental illness.82,88,89

In HIV-related research, there ex- ists the fear of the social reper- cussions of disclosing HIV sta- tus.82 Stigma was also coupled with privacy and confidentiality concerns related to the partici- pant’s medical condition, per- sonal health history, and genet- ics.34,77,79,93,102 The lack of acceptance and support from family members that may mani- fest itself in judgment for partici- pating in a study also contributed to stigma.79,81,94,103

Health insurance. African Americans reported a fear of dis- crimination from health insurance companies that may result from participating in health research that discloses their genetic health status,88 and shared with Latinos concern about health insurance coverage for participation in clini- cal trials.77 Among individuals who had no specific health care needs, there was a perception that participation in research is unnec- essary.90

Legal status. Immigrant Latinos have reported a fear of deporta- tion that may occur as a result of participating in health research,67

and Asian Americans of Filipino descent have reported their con- cern over their immigration status being affected.79

Shared Facilitators

The most commonly articulated facilitators to health research par- ticipation that were reported in the studies reviewed across all 4 racial/ ethnic groups included culturally congruent study designs and a range of benefits to participation such as receiving adequate remu- neration and access to health care resources. Altruism expressed as helping their family or community was the third most commonly

reported facilitator across the groups. Convenience of participa- tion and low risk in participation were shared facilitators reported in 3 of the 4 groups (Table 4). Cultural congruence. Having re-

search staff representative of the research participants’ racial/ethnic group was an important facilitator. Racial/ethnic participants pre- ferred research staff that they can relate to and communicate with in their own language and rhythm of expression67,96; among African Americans this act would give research the “personal touch” needed to encourage participation.93

African Americans and immigrant Filipino women were more likely to participate when invited by a recruiter or researcher that was personally known to them.79,94

Although familiarity and comfort with the clinical setting,108 re- cruiter, or researcher is helpful in enabling participation in health research, Brugge et al. caution that attention to the risk of ex- ploitation is necessary, as in their study of elderly Chinese immi- grants.109 The availability of language-appropriate materials and research staff was reported to be important to facilitating re- search participation among Asian Americans, Latinos, and Pacific Islanders.77,84,89,97,103

Benefits to participation. Mild monetary incentive,106,108 free lunch,107 or free health examina- tion85 may positively influence participation in health research. Research that allows people to help themselves, such as those wanting to lose weight41 and access health care, facilitates participation as well.67,89,91 In addition, receiving information about individual health and greater details about the study or clinical trial, such as risks and safeguards, were also observed as benefits to participation and poten- tial facilatators.41,81,82,91

TA B LE

4 — E xa m p le s o f S h a re d Fa c il it a to rs

to H e a lt h R e se a rc h P a rt ic ip a ti o n a s O b se rv e d in

th e S tu d ie s R e vi e w e d F ro m a S e a rc h o n P u b M e d a n d W e b o f

S c ie n c e F ro m Ja n u a ry 2 0 0 0 to

D e c e m b e r 2 0 1 1

Ra ci al /E th ni c G ro up

O bs er ve d Ex am pl es

Fa ci lit at or s

Ar tic le s, N o. (% )

Af ric an

Am er ic an

As ia n Am er ic an

La tin o

Pa ci fic

Is la nd er

Cu ltu ra l co ng ru en ce

27 (6 1. 4)

Co m m un ity

ed uc at io n at fr at er ni tie s an d

so ro rit ie s1 0 4 ; us e of cu ltu ra lly di ve rs e

st af f9 5

Cu ltu ra lly m at ch ed re se ar ch pe rs on ne la nd

in fo rm at io n in ap pr op ria te la ng ua ge 4 1

Re se ar ch st af ft ha t sp ea k Sp an is h an d ca n

re la te to pa rt ic ip an ts 1 0 3

Co m m un ity

in vo lv em en t pr er eq ui si te to

re se ar ch

fo r re se ar ch

st af f or us e of

in te rp re te rs an d tr an sl at ed

m at er ia l4 1

Be ne fit s to pa rt ic ip at io n

27 (6 1. 4)

M on ey or fr ee

m ed ic al se rv ic es 1 0 4 ; ac ce ss

to ne w , be tt er , or fr ee

m ed ic in es 1 0 0 ;

le ar n ab ou t th ei r ow n he al th 9 1 ; re ce iv e

ad eq ua te in fo rm at io n ab ou t th e pu rp os e

of st ud y1 0 5

N o ou t- of -p oc ke t co st s8 4 ; no

ot he r

ef fe ct iv e tr ea tm en t av ai la bl e8 4 ; m or e

in fo rm at io n ab ou t cl in ic al tr ia ls 8 1

M on et ar y co m pe ns at io n8 2 ; ac ce ss to

m ed ic al se rv ic es 8 9 ; su ffi ci en t or

ap pr op ria te st ud y in fo rm at io n pr ov id ed

8 2

Pe rs on al ne ed an d al lm ed ic al bi lls pa id 4 1 ;

im pr ov ed

m ed ic al fa ci lit ie s fo r th e

co m m un ity 4 1 ; co m pl et e di sc lo su re of

ris ks an d sa fe gu ar ds 4 1

Al tr ui sm — he lp in g fa m ily or co m m un ity

24 (5 4. 5)

Co nt rib ut io n to fu tu re ge ne ra tio ns

an d

co m m un ity 9 1 ,1 0 6 ; in cr ea se sc ie nt ifi c

kn ow le dg e1 0 4 ; pe rs on al or fa m ily hi st or y

of th e di se as e8 0 ,1 0 6

W an t to he lp fa m ily m em be r or As ia n

Am er ic an

co m m un ity

in ge ne ra l7 8 ; ca re

ab ou t th e pu rp os e of th e re se ar ch 1 0 7

H el p ot he rs 8 9 ; ad va nc e m ed ic al

kn ow le dg e1 0 3 ; bu rd en

of di se as e on

fa m ily or co m m un ity 6 7

Cl ea r co nt rib ut io n to fu tu re ge ne ra tio ns

an d co m m un ity 4 1

Co nv en ie nc e of pa rt ic ip at io n

8 (1 8. 2)

H av in g w or kp la ce

su pp or t9 0

Tr an sp or ta tio n co m pe ns at ed

1 0 7

Ch ild ca re pr ov id ed

6 7

Lo w ris k in pa rt ic ip at io n

5 (1 1. 4)

N at ur al tr ea tm en t or no ni nv as iv e9 5

Ta ke

m ed ic at io ns

w ith

kn ow n ef fic ac y8 4

Lo w ris k of to xi ci ty a, 8 5

a Pr ef er en ce

to pa rt ic ip at e in re se ar ch

w ith

a lo w ris k of to xi ci ty is sh ar ed

am on g Af ric an

Am er ic an s an d La tin os .

SYSTEMATIC REVIEW

e22 | Systematic Review | Peer Reviewed | George et al. American Journal of Public Health | February 2014, Vol 104, No. 2

Altruism. Altruism, articulated as helping family members and the community in the present and future, was an observed facilitator in the studies reviewed. Among studies that included African Americans and Latinos, advancing medical knowledge was a form of altruism and motivation for participation. Convenience of participation.

Addressing the logistics that make participating in health research convenient includes employer support to take time off to attend appointments,90 childcare,67 and transportation provisions.107 Ef- forts that make participation con- venient may help address the aforementioned barriers related to competing demands. Low risk in participation. Lastly,

a preference for studies that are perceived to have the least risk of discomfort or invasiveness, such as completing a survey or an education intervention,34 may also enable participation.110 Ex- amples of studies with the least risk that were articulated in the articles reviewed include inter- ventions with natural treatment

or taking medications with known efficacy and low risk of toxicity.

Distinct Barriers

Distinct barriers represent those barriers that are not neces- sarily unique to each of the groups but rather more commonly voiced and emphasized in the articles for this review. This understand- ing is also applied to the distinct facilitators. Again, these “distinct” barriers and facilitators are meant to be examples of the those factors that were uncom- monly reported in other groups relative to the group where the barrier or facilitator was com- monly reported and not meant to suggest that these barriers or facilitators were exclusively reported in only 1 group. Legacy of mistrust for African

Americans. Five themes appeared as distinct barriers among African Americans (Table 5). The legacy of the Tuskegee Study and lack of research integrity were each rep- resented in 13.6% (n = 6) of the articles, followed by the legacy of racism and discrimination. Ad- ditional themes contributing to

distinct barriers in participation included mistrust of the health care system and concerns related to the research process. African Americans’ negative personal ex- periences with the health care system, such as racism, differential treatment, and feelings of mistrust, may create distinct barriers to re- search participation.67,93,106

Social context for Asian Americans. Among Asian American groups, 2 distinct themes emerged in the limited literature available—namely, lack of social support that would encourage participation in health research84 and acculturation among elderly Chinese.109

Misrepresentation for Pacific Islanders. Native Hawaiians reported their concern over mis- representation of their community particularly in Hawaii where other Pacific Islanders and racial/ethnic groups also reside, and these latter groups may be inadvertently in- cluded in the findings for Native Hawaiians.97

Latinos. The lack of distinct barriers and facilitators for Latinos can be attributed to the limited articles exclusively focused on

Latinos and the greater reporting of their shared experiences with other immigrants. Also, less de- tailed information on Latinos may have resulted from their inclu- sion in 61% (11 of 18) of the articles with multiple racial/eth- nic groups that may have limited the attention to the nuances dis- tinct to Latinos.

Distinct Facilitators

Design and logistics for African Americans. Four themes observed in the studies reviewed that may facilitate African Americans’ par- ticipation in health research are having safety assurances, trust in the researcher and reputation of the research institution, having treatment options, and the inclu- sion of diverse racial and ethnic groups (Table 6). In the studies reviewed, African American par- ticipants wanted not only reputa- ble researchers, but also the as- surance that researchers will put African Americans’ best interests ahead of the study’s objectives.91

Although having treatment op- tions is contrary to the validity of randomized clinical trials,

TABLE 5—Examples of Distinct Barriers to Health Research Participation as Observed in the Studies Reviewed From a Search on

PubMed and Web of Science From January 2000 to December 2011

Racial/Ethnic Group, Barrier Articles, No. (%) Observed Examples

African American: legacy of mistrust

Legacy of the Tuskegee Study 6 (13.6) Belief in the perceived conspiracy in the United States to harm Black people 34 ; knowledge of the Tuskegee Study has

negative impact on willingness 111

Lack of research integrity 6 (13.6) Concerns related to data use 34 ; improper treatment of research participants

32,88 ; questionable ethical practices related to

cloning, reputation of researcher or institution, 74,88

consent forms, 91 and disclosure

100

Legacy of racism and discrimination 3 (6.8) Perception that researchers do not value Blacks62

Mistrust of health care system 2 (4.5) Direct or indirect experience of the disregard for cultural norms among health care or research staff74

Concerns with the research process 2 (4.5) Lack of choice over treatment in clinical trials95

Asian American: social context

Lack of social support 2 (4.5) Lack of family’s support of the decision to participate in health research 84,107

Acculturation 1 (2.3) Acculturation in elderly Chinese reduced the likelihood of participation 109

Latino: None

Pacific Islander: misrepresentation of community 1 (2.3) Concerns related to the use of data to benefit the researchers and not the community, and the extrapolation of data that

may overgeneralize Native Hawaiians41

SYSTEMATIC REVIEW

February 2014, Vol 104, No. 2 | American Journal of Public Health George et al. | Peer Reviewed | Systematic Review | e23

leveraging the importance of choice in participation may en- able African Americans’ partici- pation in research. Finally, want- ing to see White people also enrolled in a study along with African Americans was moti- vated by the perception that African Americans are not valued by researchers and the belief that if White people are enrolled, researchers are less likely to deliberately harm the partici- pants.34

Family for Asian Americans. In the studies reviewed, among Asian Americans, having family mem- bers, such as a spouse or sibling, support the decision to participate in health research or being asked by a son or daughter to engage in health research have been reported to facilitate participa- tion.78,81,109

Community for Pacific Islanders. Likewise, in the studies reviewed, among Pacific Islanders, particu- larly Native Hawaiians, the inclu- sion of family members was most relevant to elders who rely on youths to interpret information and thus increases access to in- formation about research oppor- tunities.87 The community’s in- volvement in being informed of

the results and subsequently aid- ing in the interpretation of the results to a larger audience were key mediation strategies to in- crease trust and facilitate partici- pation among Native Hawaiians in Hawaii.41

DISCUSSION

Our review of the literature between January 2000 and De- cember 2011 revealed several key experienced or perceived barriers and facilitators to partici- pating in health research across studies that focused on 1 or more of the major US racial/ethnic mi- nority populations, namely Afri- can Americans, Latinos, Asian Americans, and Pacific Islanders. In our review, we found trends in the similarities and differences in perceptions and experiences across the 4 groups, presented in tables. In this section, we consider both the limitations of our findings and the implications of the shared and distinct (commonly and uncommonly reported) barriers and facilitators for the recruitment and retention of these 4 racial/ethnic groups in the studies reviewed for health research and for future

large-scale prospective quantitative studies and in-depth qualitative ethnographic studies.

Shared and Distinct Barriers

Key shared (commonly reported across groups) barriers included (1) mistrust and conse- quent fear of participation, (2) stigma related to research par- ticipation, and (3) competing de- mands. The distinct (uncom- monly reported across groups) barriers for these groups were sometimes variations on the shared barriers, but expressed with greater intensity or with reference to a specific context by the particular racial/ethnic group.

Mistrust was the most common barrier appearing in 73% of the studies across the qualitative and quantitative research articles we reviewed. The expressions of mis- trust regarding health research varied across all 4 groups, partly on the basis of context and expe- riences. Some groups expressed their mistrust of researchers and fear of participation in research in terms of community and com- munal experiences. For example, both African Americans and Native Hawaiians consistently

emphasized the importance of community and shared a mistrust of research related to the belief that research may not benefit their communities. Such mistrust seemed to be rooted in histori- cal communal experiences includ- ing slavery and colonialism and their legacy of racism and dis- crimination and from specific experiences such as the Tuskegee Study for African Americans, a finding that is consistent with previous reviews on barriers to participation in clinical research.1,113 Although 1 article reported the potential for simi- lar Latino mistrust associated with negative associations with research connected to oral con- traceptives that had been con- ducted in the 1960s among His- panics,114 we did not find any other references to mistrust con- nected to this experience among Latino research participants in contrast with African Americans, among whom there were re- peated references to the infa- mous Tuskegee Study. It was in- teresting that belief in the AIDS Origin Conspiracy Theory may contribute to mistrust but was not found to decrease participa- tion in biomedical research.115

TABLE 6—Examples of Distinct Facilitators to Health Research Participation as Observed in the Studies Reviewed From a Search

on PubMed and Web of Science From January 2000 to December 2011

Racial/Ethnic Group, Facilitator Articles, No. (%) Observed Examples

African American: design and logistics

Having safety assurances 3 (6.8) Guarantee compensation if participant is disabled or killed as a result of participating in the study 76 ; communicating study

process 112

and results with participants 88 ; having control in decision to participate or decline

100

Trust in researcher or reputation 2 (4.5) Trust researchers to put the participants’ best interest first 91 ; trust in researcher and reputation

76

Having treatment options 1 (2.3) Having choice of treatment in randomized clinical trials 92

Inclusion of diverse racial/ethnic groups 1 (2.3) Seeing White people also recruited in the study34

Asian American: endorsement from family 3 (6.8) Family involved in decision-making process among Chinese and Vietnamese81; if asked by son or daughter among elderly

Chinese109 or spouse among Chinese and Vietnamese women78

Latino: None

Pacific Islander: Community mediation 2 (4.5) Community has input over how research findings are used and reported; findings are reported back to the community 41 ; study

information is culturally tailored and directed to families 87

SYSTEMATIC REVIEW

e24 | Systematic Review | Peer Reviewed | George et al. American Journal of Public Health | February 2014, Vol 104, No. 2

Perceptions of mistrust regard- ing 3 specific aspects of research participation included (1) fear of purposeful mistreatment, (2) fear of unknown research procedures, and (3) fear of unintended conse- quences. One example of an un- familiar research process that led to some fear and mistrust was the informed consent process, about which participants expressed such fears as “Am I signing away my free will?” In addition to fear and mistrust related to unintended consequences, participants feared finding out that they had a disease that they did not know about. Other groups also talked about unintended consequences but did not express similar fears concern- ing participation. A distinct barrier reported among Native Hawai- ians, which may have stemmed from mistrust connected to their experiences of colonization, was expressed specifically as a fear of their community being misrepre- sented in the outcomes of re- search.

A second key shared barrier across all groups was competing demands, which included both time and financial challenges as- sociated with participation in re- search. The participants in many of these studies consistently appeared to be concerned about issues such as maintaining cur- rent jobs or needing to find work or holding multiple jobs to make ends meet. They also expressed concerns about being responsible for the care of children and other relatives, particularly when they were single parents. For such participants, a long-term com- mitment to a research study could be a very difficult barrier to overcome if appropriate retention strategies were not implemented.

Although stigma, another key shared barrier to participation in

research studies, may have been related to the mistrust and fear of participation, for most of the participants of the studies we reviewed, stigma seemed to be associated more with the clinical condition or topic being researched rather than with participation in research itself. For example, partic- ipation in both mental illness--- and genetic research---related studies was cause for stigma among Afri- can American participants in the studies reviewed. HIV-related studies were cause for stigma among Latino study participants. By contrast, in the 1 Asian American study where stigma emerged as a barrier, the cause of stigma was judgment from family members for participating in research. Lack of social sup- port, particularly from family members, was a distinct barrier to research participation for Asian Americans, underlining the likely importance of family in- volvement and likely reflecting stigma in this group.

Shared and Distinct

Facilitators

Despite the presence of these barriers, Katz et al. reported no difference in self-reported willing- ness to participate in biomedical research among African Ameri- cans, Latinos, and Whites.99 This finding suggests that, although barriers to participation can be significant across these popula- tions, there are also facilitators that result in a willingness to partici- pate among these groups, espe- cially for select medical conditions. Key shared facilitators included culturally congruent research pro- cesses, benefits of participation, and altruism toward and involvement of family or community.

A key facilitator for these study participants seemed to be the use of community-based, linguistically

appropriate, and personalized re- cruitment and retention practices in the research process. Partici- pants preferred having the re- cruitment processes based in community settings, with cultur- ally matched research personnel running the studies and study materials in the appropriate lan- guages. Furthermore, they pre- ferred being recruited in a more personal way, “face-to-face” such as by their physicians or others they knew. In fact, there were several interrelated facilitators re- lated to community and culture, which all underscored the interest expressed by multicultural popu- lations to learn about research and their willingness to participate when research processes were contextualized in community pri- orities and using culturally con- gruent practices. For example, a theme that resonated very strongly in the reviewed literature was the role played by altruism— construed as helping family and community—in facilitating partici- pation among these populations. As mentioned earlier, in the stud- ies reviewed, African Americans and Pacific Islanders, and specifi- cally Native Hawaiians, were each articulate about their mistrust of research related to the belief that such efforts would not benefit their communities; however, at the same time, participants from both communities expressed a commit- ted desire to help their future generations or community through research.

Participants from all groups expressed a desire for community contextualization and cultural congruence, but there were some distinct variations voiced among the groups. For example, Pacific Islanders, specifically Native Ha- waiians, additionally emphasized community mediation as a facili- tator to research participation,

where they desired trusted com- munity liaisons to take a more active role and for both facilita- tors and barriers to research to be mediated at the community level as opposed to the individual level. Therefore, whereas Afri- can Americans wanted follow-up and study results reported to in- dividual participants, Native Ha- waiians wanted results reported to families and communities. Studies on Asian Americans from multiple subgroups reported that endorsement of research from a trusted and known individual, such as a family member, was a distinct facilitator for research participation for members of this group.

Adequate remuneration for re- search participation was another key shared facilitator that was raised in almost half the studies reviewed. Study participants wanted to not have any “out of pocket” expenses and wanted all the medical care associated with the research to not be an addi- tional expense for them. In addi- tion to monetary remuneration, some study participants, across racial/ethnic groups, expressed preference for payment in direct health care, such as health screenings and other clinical ser- vices, which maybe otherwise unavailable to them. This may be particularly true for the poor, the underserved, and recent immi- grants who may not have access to regular sources of health care.

Limitations

A major limitation to our re- view was the lack of equivalent amounts of data across the 4 racial/ethnic groups. Our find- ings are consistent with previous scholarship in this area that rela- tive to the studies available on the research participation of African Americans and Whites,

SYSTEMATIC REVIEW

February 2014, Vol 104, No. 2 | American Journal of Public Health George et al. | Peer Reviewed | Systematic Review | e25

there is little comparable re- search on Latinos, Asian Americans, and Pacific Islanders.10,40,116 With regard to this review, the availabil- ity of relatively more information on African Americans allowed for a better understanding and a more nuanced grasp of the barriers and facilitators to research participa- tion present for this group. How- ever, the absence of a similar range of scholarship for the other 3 groups has limited our ability to identify and compare barriers and facilitators with the same level of specificity across all 4 groups.

Furthermore, we found that there were other social categorical distinctions across the groups that were rarely represented in the literature. For example, the ma- jority of the research articles that we reviewed included mostly fe- male participants and few male participants. We found only 1 study that focused on African American men. In addition, dis- tinctions such as immigrant versus nonimmigrant, English-speaking versus non---English-speaking, documented versus undocu- mented, and generational differ- ences were seldom reflected in the literature. The exclusion of research participants younger than 18 years limits the ability of our findings to be generalized to younger persons where a unique interaction of child or adolescent and parent will likely introduce new considerations for participation that may also be disease-specific. Because of the limited number of articles in the review, our analysis did not distin- guish between the internal diversity among Latino, Asian American, and Pacific Islander subgroups, which could limit generalizations to select ethnic communities.

The decision to exclude searching on Google Scholar

limited the content of this review to peer-reviewed articles and in- herently excluded gray literature such as conference proceedings or institutional publications.

Finally, this article presents a systematic review of the existing qualitative and quantitative stud- ies that focus on participants’ voi- ces to identify the range of themes and papers but cannot provide a truly quantitative comparative perspective. As already discussed in the Results section, although we have made comparative state- ments about the studies we have reviewed, we cannot make any definitive statements about the distribution or importance of bar- riers or facilitators in the defined populations represented in the studies. However, we believe it is the rigorous compilation of par- ticipant voices and expressions that lays the foundation to move future studies forward in a guided manner.

Implications for Recruitment

and Retention

Given our findings, enhancing research participation might be viewed through 2 interdependent lenses: (1) addressing barriers that hinge to a large degree on a his- tory of exclusion and vulnerabil- ity, which can be leveraged to appeal to most people’s desire to access trials as treatment of them- selves or their community, and (2) addressing facilitators through the implementation of community- based participatory research (CBPR) strategies to ensure that individuals and communities are more fully engaged in health research projects from conceptualization to design and implementation.117---119

Because social and structural factors such as mistrust, stigma, and lack of adequate health knowledge impede participation, it is clear that social or structural

interventions such as sensitivity training for community and aca- demic researchers and research staff will be among important strategies to enhance participation of a diverse constituency. The overwhelming presence of mis- trust of research in all 4 racial/ ethnic groups is such a shared barrier that might be mitigated by increasing the health and health research literacy120 of these groups in a cost-effective manner to be leveraged across multiple racial/ ethnic groups, given their similar range of mistrust issues. However, it will also be necessary to tailor such efforts to address the distinct bar- riers and leverage the distinct facil- itators related to mistrust for particular groups. For example, educating African American and Native Hawaiian populations may include acknowledging the historical context of their mis- trust and providing a venue where causes of mistrust can be discussed openly. Furthermore, providing reassurances such as (1) opportunities to learn and ask questions about the research process, (2) verifiable assurances of human participant protection measures to address fears of be- ing experimented on, and (3) explicitly addressing concerns about unintended consequences may be helpful for all multicul- tural groups with little previous exposure to research.

Such efforts may be more ac- ceptable to many of these study populations if they were incul- cated in a CBPR approach using a culturally congruent manner, in community settings, with cultur- ally matched research personnel, linguistically appropriate mate- rials, and a personalized recruit- ment process with endorsement from trusted community fig- ures.118,120---122 A more robust ap- proach to the consent process

should be developed to better address participant concerns.123

Whereas many CBPR practices involve community members from the research question devel- opment to design and interpreta- tion of results, few include partic- ipants or community in the conceptualization, development, and implementation of the consent form.124 Having representative study participants or community members involved in the consent process should be considered as a new standard for clinical trials. Furthermore, with Native Hawai- ian populations, additional efforts could be made to understand and address concerns about commu- nity misrepresentation resulting from research participation and to leverage the role of community liaisons as mediators of research participation.

An exception to community- based recruitment may be in the case of clinical studies involving conditions that are considered stigmatizing. For studies related to these conditions, recruitment of multicultural populations may become a challenge if they are based in the community because participants may be concerned about becoming stigmatized if their participation becomes com- mon knowledge. But effective community engagement can over- come even these concerns as demonstrated in depression re- search.125 We found stigma to be a consistent concern across differ- ent cultural groups, but the genesis and impact of stigma differed across groups. Especially when conducting studies involving con- ditions that are considered stig- matizing in particular communi- ties, researchers may need to use stigma-reduction strategies and interventions, which range from the intrapersonal to governmental levels, with the most effective

SYSTEMATIC REVIEW

e26 | Systematic Review | Peer Reviewed | George et al. American Journal of Public Health | February 2014, Vol 104, No. 2

strategies being multitargeted and multilevel, using counseling, ed- ucation, and personal contact, particularly targeting individual and community levels.126

Finally, when a study is recruit- ing multicultural populations, there may be a need to pay special attention to competing demands, particularly with regard to time and money, for the poorer and underserved segments of these populations. Providing adequate remuneration, particularly in the form of clinical services, may be a facilitator that would be attrac- tive to potential research partici- pants from these groups. To the extent that such clinical services are otherwise unavailable to par- ticipating members of these pop- ulations, researchers must be vigilant to reduce the possibility that participants may agree to onerous research requirements to obtain the necessary clinical ser- vices. There are several other such social justice---related issues that arise in the context of CBPR given the potentially inherent differ- ences in power, expectations, and priorities between research and historically disadvantaged com- munity partners. These can result in ethical challenges all along the research spectrum from research processes such as informed con- sent and participant selection to addressing the risk---benefit ratio of doing research to the owner- ship, sharing, and decision-making around findings.123,127

Future Directions

The findings from this review point to the urgent need to con- duct more research focusing on some groups such as Latinos, Asian Americans, and Pacific Is- landers about whom there is a dearth of information regard- ing their experiences and per- ceptions of health research.

Likewise, some groups, such as Latinos, and Asian Americans, Pacific Islanders, have a great deal of internal diversity among them, which is not represented in the sparse literature that is cur- rently available. Again, inclusion of a greater representation of subgroups within larger groups is an important factor for future studies to consider when they are recruiting multicultural popula- tions for health research. Such differences may be important in obtaining a more accurate re- flection of barriers and facilita- tors to research participation, particularly among racial/ethnic groups with immigrant and non- immigrant contingents with dif- ferent language abilities and documentation statuses. It may be helpful to conduct a similar review exploring the literature on the health research experi- ences and perspectives of Amer- ican Indians within the context of the Native American Research Centers for Health supported by the Indian Health Services and NIH to help tribes and tribal organizations expand research infrastructure in culturally con- gruent ways. Future studies that explore the factors influencing research participation also need to consider whether having a greater gender balance among study participants may be im- portant to study outcomes and result in the identification of a distinct set of barriers and facilitators to research participa- tion for men versus women among these groups.

Data on the perspectives of patients with diverse health con- ditions and their preferences with regard to type of clinical research are limited. Given that the majority of studies are focused on cancer and HIV, there are limited data available on other health conditions

that allow for the examination of the nuances that influence the par- ticipants’ decision and willingness to participate in varying types of clinical research, especially chronic diseases not typically associated with a high risk of immediate mor- tality. Understanding the prefer- ences for observational studies compared with intervention stud- ies, and within interventions studies the preference for noninvasive compared with invasive interven- tions, may facilitate the better de- sign of effective recruitment and retention methods. Data on US minority participation in clinical trials suggests an overrepresenta- tion of minorities in phase I clinical trials and a continued underrep- resentation in phase III clinical trials.128 Thus, although partici- pants’ perspectives are integral in designing recruitment and reten- tion strategies, additional studies are needed to fully understand the breadth of factors that facilitate and impede minority participation in all phases of clinical trials.

Furthermore, it is imperative to conduct further study on con- texts of and approaches to re- cruitment and retention of minor- ity populations. For example, when participation in clinical trials is the only avenue to receiving clinical care, there are likely to be higher rates of recruitment from across diverse populations, par- ticularly in phase 1 trials.129,130

This is particularly true for cer- tain diseases, such as cancer, which have relatively higher rates of minority participation in clinical trials. Such differences in the context of participation raise questions about how recruitment and retention under dire circum- stances compares with other re- cruitment contexts, where partici- pants may have multiple treatment and care options. Furthermore, approaches to engaging diverse

populations in research vary considerably in terms of the level of community participation. In a recent systematic review ex- amining the effectiveness of CBPR to enhance clinical trials in racial/ethnic minority groups, the authors found that trials using CBPR had “very high success rates in recruiting and retaining minority participants and achiev- ing significant intervention effects.”131(p1363) With the expan- sion of CBPR approaches, com- munity---research partnerships have an opportunity to overcome many of the key barriers and leverage key facilitators to in- crease racial/ethnic minority participation in research. Future studies need to address a range of approaches to community en- gagement, including projects identified and driven by commu- nities and the varying impact on the recruitment and retention of multicultural populations in research.

Finally, researchers may be able to use the findings of this study to inform and motivate future large-scale prospective quantitative studies to make truly quantitative comparisons of bar- riers and facilitators across groups. We also need additional in-depth, ethnographic research in these communities to assess more accurately the shared and relatively distinct nature of bar- riers and facilitators, because quantitative surveys, qualitative focus group, and individual in- terview studies are limited by what participants are able or willing to share and articulate. In many instances, when barriers and facilitators are based in cul- tural practices, they occur at a subconscious level and may not be articulated by participants in responses to direct questions. Ethnographic studies, which

SYSTEMATIC REVIEW

February 2014, Vol 104, No. 2 | American Journal of Public Health George et al. | Peer Reviewed | Systematic Review | e27

involve observation of practices in community settings, are es- sential to identifying such not so easily articulated cultural varia- tions in barriers and facilitators among these groups.

Conclusions

Our review of the literature points to the need to learn more about and refine our understand- ing of barriers and facilitators to research participation among Af- rican American, Latino, Asian American, and Pacific Islander groups. Mistrust and competing demands, as well as stigma and consequent fear of participation, were notable challenges to re- search participation among the racial and ethnic minorities in the studies reviewed. Furthermore, our review also identified several facilitators that resonated across groups including the importance of contextualizing recruitment and retention strategies among these populations within specific com- munity priorities and using cul- turally congruent practices, where research is seen as altruism toward family and community, and ade- quate benefits for participation. Community-based participatory research approaches including in- volvement in the consent process may hold particular promise. Leveraging and integrating infor- mation about such shared barriers and facilitators into the develop- ment of recruitment and retention materials and practices are likely to result in more effective and ethical strategies to increase num- bers of multicultural participants in health research and meet the translational research challenge of moving scientific discovery to practice for all Americans. j

About the Authors Sheba George is with the Center for Biomedical Informatics, Charles R. Drew

University of Medicine and Science, and the Department of Community Health Sciences, University of California Los Angeles (UCLA) Fielding School of Public Health, Los Angeles. Nelida Duran is with the Department of Community Health Sciences, UCLA Fielding School of Public Health. Keith Norris is with the Division of General Internal Medicine and Health Services Research, David Geffen School of Medicine at UCLA, Los Angeles. Correspondence should be sent to Sheba

George, Department of Community Health Sciences, UCLA Fielding School of Public Health, Room 36-071, PO Box 951772, Los Angeles, CA 90095-1772 (e-mail: [email protected] ). Reprints can be ordered at http://www.ajph.org by clicking the “Reprints” link.

This article was accepted September 21, 2013.

Contributors S. George originated the project, led the writing, and, along with N. Duran, reviewed studies, developed the coding scheme, and conducted the analysis. N. Duran developed and managed the database used to summarize the data, retrieved and coded the relevant articles, conducted the analyses, and cowrote the article. K. Norris co-originated the project and cowrote the article.

Acknowledgments This work was supported by the Na- tional Center for Research Resources, National Institutes of Health (NIH; grant U54RR022762), with co-funding from the National Institute for Minority Health Disparities, NIH (grant U54MD007598, formerly U54RR026138), the National Center for Advancing Translational Sciences, NIH (grant UL1TR000124), and by the National Cancer Institute, NIH (grant 3U54CA153499-04S1).

The authors also wish to thank the reviewers and responsible editor for their insightful comments and suggestions, which have greatly improved this paper.

Note. The findings and conclusions in thisreportarethoseoftheauthorsanddonot necessarily represent the views of the NIH.

Human Participant Protection Institutional review board approval was not obtained because human participants were not involved and only published data were reported.

References 1. Hussain-Gambles M, Atkin K, Leese B. Why ethnic minority groups are under-represented in clinical trials: a review of the literature. Health Soc Care Community. 2004;12(5):382---388.

2. Yancey AK, Ortega AN, Kumanyika SK. Effective recruitment and retention of

minority research participants. Annu Rev Public Health. 2006;27:1---28

3. Davis S, Wright PW, Schulman SF, et al. Participants in prospective, ran- domized clinical trials for resected non- small cell lung cancer have improved survival compared with nonparticipants in such trials. Cancer. 1985;56(7): 1710---1718.

4. Heiat A, Gross CP, Krumholz HM. Representation of the elderly, women, and minorities in heart failure clinical trials. Arch Intern Med. 2002;162 (15):1682---1688.

5. Miranda J, Nakamura R, Bernal G. Including ethnic minorities in mental health intervention research: a practical approach to a long-standing problem. Cult Med Psychiatry. 2003;27(4): 467---486.

6. Satcher D. Mental health: culture, race, and ethnicity—a supplement to Mental Health: A Report of the Surgeon General. Rockville, MD: US Department of Health and Human Services, National Institute of Mental Health; 2001.

7. National Institutes of Health. NIH policy and guidelines on the inclusion of women and minorities as subjects in clinical research. Available at: http:// grants.nih.gov/grants/funding/women_ min/guidelines_amended_10_2001. htm. Accessed May 15, 2009.

8. Food and Drug Administration. Mod- ernization Act of 1997. Available at: http:// www.fda.gov/drugs/guidancecomplianc eregulatoryinformation/guidances/uc m065012.htm. Accessed October 21, 2013.

9. Medicare clinical trial policies. Available at: http://www.cms.hhs.gov/ ClinicalTrialPolicies. Accessed May 15, 2009.

10. Ford JG, Howerton MW, Lai GY, et al. Barriers to recruiting underrepre- sented populations to cancer clinical tri- als: a systematic review. Cancer. 2008; 112(2):228---242.

11. Bolen S, Tilburt J, Baffi C, et al. Defining “success” in recruitment of un- derrepresented populations to cancer clinical trials. Cancer. 2006;106(6): 1197---1204.

12. Williams JE. Eliminating Disparities in Clinical Trials (EDICT) Project. Avail- able at: http://minorityhealth.hhs.gov/ templates/content.aspx?ID=5046&lvl= 3&lvlID=361. Accessed October 21, 2013.

13. Evelyn B, Toigo T, Banks D, et al. Participation of racial/ethnic groups in clinical trials and race-related labeling: a review of new molecular entities ap- proved 1995---1999. J Natl Med Assoc. 2001;93(12 suppl):18S.

14. Banda DR, Germain DS, McCaskill- Stevens W, Ford JG, Swain SM. A critical review of the enrollment of Black patients in cancer clinical trials. 2012. Available at: http://meetinglibrary.asco.org/content/ 88-114. Accessed October 21, 2013.

15. UyBico SJ, Pavel S, Gross CP. Recruiting vulnerable populations into research: a systematic review of recruit- ment interventions. J Gen Intern Med. 2007;22(6):852---863.

16. MacEntee MI, Wyatt C, Kiyak HA, et al. Response to direct and indirect recruitment for a randomised dental clinical trial in a multicultural population of elders. Community Dent Oral Epidemiol. 2002;30(5):377---381.

17. Banda DR, Libin AV, Wang H, Swain SM. A pilot study of a culturally targeted video intervention to increase participation of African American patients in cancer clinical trials. Oncologist. 2012;17(5):708---714.

18. Lai GY, Gary TL, Tilburt J, et al. Effectiveness of strategies to recruit un- derrepresented populations into cancer clinical trials. Clin Trials. 2006;3(2): 133---141.

19. Larkey LK, Gonzalez JA, Mar LE, Glantz N. Latina recruitment for cancer prevention education via community based participatory research strategies. Contemp Clin Trials. 2009;30(1): 47---54.

20. Skaff MM, Chesla CA, de los Santos Mycue V, Fisher L. Lessons in cultural competence: adapting research method- ology for Latino participants. J Commu- nity Psychol. 2002;30(3):305---323.

21. Norton IM, Manson SM. Research in American Indian and Alaska Native communities: navigating the cultural uni- verse of values and process. J Consult Clin Psychol. 1996;64(5):856---860.

22. Simon CM, Kodish E. “Step into my zapatos, Doc”: understanding and reduc- ing communication disparities in the mul- ticultural informed consent setting. Perspect Biol Med. 2005;48(1):S123---S138.

23. Corrigan O. Empty ethics: the prob- lem with informed consent. Sociol Health Illn. 2003;25(7):768---792.

24. Corbie-Smith G, Moody-Ayers S, Thrasher AD. Closing the circle between minority inclusion in research and health disparities. Arch Intern Med. 2004;164 (13):1362---1364.

25. Kuczewski MG, Marshall P. The decision dynamics of clinical research: the context and process of informed consent. Med Care. 2002;40(9):V-45---V-54.

26. O’Brien RL, Kosoko-Lasaki O, Cook CT, Kissell J, Peak F, Williams EH. Self-assessment of cultural attitudes and competence of clinical investigators to enhance recruitment and participation

SYSTEMATIC REVIEW

e28 | Systematic Review | Peer Reviewed | George et al. American Journal of Public Health | February 2014, Vol 104, No. 2

of minority populations in research. J Natl Med Assoc. 2006;98(5):674---682.

27. Swanson GM, Ward AJ. Recruiting minorities into clinical trials toward a participant-friendly system. J Natl Cancer Inst. 1995;87(23):1747---1759.

28. Parra-Medina D, D’Antonio A, Smith SM, Levin S, Kirkner G, Mayer-Davis E. Successful recruitment and retention strategies for a randomized weight man- agement trial for people with diabetes living in rural, medically underserved counties of South Carolina: the POWER study. J Am Diet Assoc. 2004;104(1): 70---75.

29. Davis RM, Hitch AD, Nichols M, Rizvi A, Salaam M, Mayer-Davis EJ. A collaborative approach to the recruitment and retention of minority patients with diabetes in rural community health cen- ters. Contemp Clin Trials. 2009;30(1): 63---70.

30. Mills EJ, Seely D, Rachlis B, et al. Barriers to participation in clinical trials of cancer: a meta-analysis and systematic review of patient-reported factors. Lancet Oncol. 2006;7(2):141---148.

31. Dula A. African American suspicion of the healthcare system is justified: what do we do about it? Camb Q Healthc Ethics. 1994;3(3):347---357.

32. Corbie-Smith G, Thomas SB, St George DMM. Distrust, race, and re- search. Arch Intern Med. 2002;162 (21):2458.

33. Earl CE, Penney PJ. The significance of trust in the research consent process with African Americans. West J Nurs Res. 2001;23(7):753---762.

34. Freimuth VS, Quinn SC, Thomas SB, Cole G, Zook E, Duncan T. African Americans’ views on research and the Tuskegee Syphilis Study. Soc Sci Med. 2001;52(5):797---808.

35. Jones CP. Levels of racism: a theo- retic framework and a gardener’s tale. Am J Public Health. 2000;90(8): 1212---1215.

36. Smedley BD, Stith AY, Nelson AR. Unequal Treatment: Confronting Racial and Ethnic Disparities in Health Care (With CD). Washington, DC: National Academies Press; 2009.

37. Williams DR, Mohammed SA, Leavell J, Collins C. Race, socioeconomic status, and health: complexities, ongoing challenges, and research opportunities. Ann N Y Acad Sci. 2010;1186(1): 69---101.

38. Davis SM, Reid R. Practicing partic- ipatory research in American Indian communities. Am J Clin Nutr. 1999;69 (4):755S---759S.

39. Washington HA. Medical Apart- heid: The Dark History of the Medical

Experimentation on Black Americans From Colonial Times to the Present. New York, NY: Random House Digital Inc; 2006.

40. Lawrence J. The Indian Health Service and the sterilization of Native American women. Am Indian Q. 2000;24 (3):400---419.

41. Gollin LX, Harrigan RC, Perez J, Easa D, Calderón JL. Improving Ha- waiian and Filipino involvement in clinical research opportunities: qualita- tive findings from Hawai’i. Ethn Dis. 2005;15(4 suppl 5):S5.

42. Shavers-Hornaday VL, Lynch CF, Burmeister LF, Torner JC. Why are Afri- can Americans under-represented in medical research studies? Impediments to participation. Ethn Health. 1997;2(1-2): 31---45.

43. Roberson NL. Clinical trial partici- pation: viewpoints from racial/ethnic groups. Cancer. 1994;74(9 suppl): 2687---2691.

44. Fong M, Braun KL, Tsark J. Im- proving Native Hawaiian health through community-based participatory research. Californian J Health Promot. 2003;1: 136---148.

45. Gee GC, Spencer MS, Chen J, Takeuchi D. A nationwide study of dis- crimination and chronic health conditions among Asian Americans. Am J Public Health. 2007;97(7):1275---1282.

46. Williams DR, Mohammed SA. Dis- crimination and racial disparities in health: evidence and needed research. J Behav Med. 2009;32(1):20---47.

47. Landrine H, Klonoff EA. The schedule of racist events: a measure of racial discrimination and a study of its negative physical and mental health con- sequences. J Black Psychol. 1996;22 (2):144---168.

48. Shavers VL, Fagan P, Jones D, et al. The state of research on racial/ethnic discrimination in the receipt of health care. Am J Public Health. 2012;102 (5):953---966.

49. Ellington L, Wahab S, Sahami Martin S, Field R, Mooney KH. Factors that influence Spanish- and English- speaking participants’ decision to enroll in cancer randomized clinical trials. Psy- chooncology. 2006;15(4):273---284.

50. Murthy VH, Krumholz HM, Gross CP. Participation in cancer clinical trials. JAMA. 2004;291(22): 2720---2726.

51. Blascovich J, Spencer SJ, Quinn D, Steele C. African Americans and high blood pressure: the role of stereo- type threat. Psychol Sci. 2001;12(3): 225---229.

52. Chambers EC, Tull ES, Fraser HS, Mutunhu NR, Sobers N, Niles E. The relationship of internalized racism to body fat distribution and insulin resis- tance among African adolescent youth. J Natl Med Assoc. 2004;96(12): 1594---1598.

53. Taylor J, Jackson B. Factors affecting alcohol consumption in Black women. Part II. Subst Use Misuse. 1990;25 (12):1415---1427.

54. Tull ES, Cort MA, Gwebu ET, Gwebu K. Internalized racism is associ- ated with elevated fasting glucose in a sample of adult women but not men in Zimbabwe. Ethn Dis. 2007;17(4):731.

55. Williams DR, Mohammed SA. Rac- ism and health I: pathways and scientific evidence. Am Behav Sci. 2013;20(10): 1---22 .

56. Taylor JY. Colonizing images and diagnostic labels: oppressive mecha- nisms for African American women’s health. ANS Adv Nurs Sci. 1999;21 (3):32---45.

57. Corbie-Smith G, Thomas SB, Williams MV, Moody-Ayers S. Attitudes and beliefs of African Americans toward participation in medical research. J Gen Intern Med. 1999;14(9):537---546.

58. Rivera-Goba MV, Dominguez DC, Stoll P, Grady C, Ramos C, Mican JM. Exploring decision-making of HIV-infected Hispanics and African Americans participating in clinical trials. J Assoc Nurses AIDS Care. 2011;22 (4):295---306.

59. Wallington SF, Luta G, Noone AM, et al. Assessing the awareness of and willingness to participate in cancer clin- ical trials among immigrant Latinos. J Community Health. 2012;37(2): 335---343.

60. Wendler D, Kington R, Madans J, et al. Are racial and ethnic minorities less willing to participate in health research? PLoS Med. 2006;3(2):e19.

61. Corbie-Smith G. The continuing legacy of the Tuskegee Syphilis Study: considerations for clinical investigation. Am J Med Sci. 1999;317(1):5---8.

62. Scharff DP, Mathews KJ, Jackson P, Hoffsuemmer J, Martin E, Edwards D. More than Tuskegee: understanding mis- trust about research participation. J Health Care Poor Underserved. 2010;21(3):879--- 897.

63. Katz RV, Green BL, Kressin NR, et al. The legacy of the Tuskegee Syphilis Study: assessing its impact on willingness to participate in biomedical studies. J Health Care Poor Underserved. 2008;19 (4):1168---1180.

64. Durant RW, Davis RB, St George DMM, Williams IC, Blumenthal C, Corbie- Smith GM. Participation in research

studies: factors associated with failing to meet minority recruitment goals. Ann Epidemiol. 2007;17(8):634---642.

65. US Census Data 2000. Available at: http: www.census.gov/main/www/ cen2000.html. Accessed October 21, 2013.

66. Brown M, Moyer A. Predictors of awareness of clinical trials and feelings about the use of medical information for research in a nationally representative US sample. Ethn Health. 2010;15(3): 223---236.

67. Calderón JL, Baker RS, Fabrega H, et al. An ethno-medical perspective on research participation: a qualitative pilot study. Medscape General Medicine. 2006;8(2):23.

68. Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. J Clin Epidemiol. 2009;62(10):1006---1012.

69. Liberati A, Altman DG, Tetzlaff J, et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interven- tions: explanation and elaboration. BMJ. 2009;339:b2700.

70. Mikki S. Google Scholar compared to Web of Science: a literature review. J Nordic Information Literacy Higher Educ. 2009;1(1):41---51.

71. Anders ME, Evans DP. Comparison of PubMed and Google Scholar literature searches. Respir Care. 2010;55(5):578--- 583.

72. Shultz M. Comparing test searches in PubMed and Google Scholar. J Med Libr Assoc. 2007;95(4):442---445.

73. Giustini D, Boulos MNK. Google Scholar is not enough to be used alone for systematic reviews. Online J Public Health Inform. 2013;5(2):214.

74. Cronin P, Ryan F, Coughlan M. Undertaking a literature review: a step- by-step approach. Br J Nurs. 2008;17 (1):38---43.

75. Moher D, Liberati A, Tetzlaff J, Altman DG, The PRISMA Group Pre- ferred Reporting Items for Systematic Reviews and Meta-Analyses: The PRISMA Statement. PLoS Med. 2009;6 (6):e1000097.

76. BeLue R, Taylor-Richardson KD, Lin J, Rivera AT, Grandison D. African Americans and participation in clinical trials: differences in beliefs and attitudes by gender. Contemp Clin Trials. 2006; 27(6):498---505.

77. Sadler GR, Gonzalez J, Mumman M, et al. Adapting a program to inform African American and Hispanic American women about cancer clinical trials. J Cancer Educ. 2010;25(2):142---145.

SYSTEMATIC REVIEW

February 2014, Vol 104, No. 2 | American Journal of Public Health George et al. | Peer Reviewed | Systematic Review | e29

78. Giarelli E, Bruner DW, Ethan N, et al. Research participation among Asian American women at risk for cervical cancer: exploratory pilot of barriers and enhancers. J Immigr Minor Health. 2011;13(6):1055---1068.

79. Maxwell AE, Bastani R, Vida P, Warda US. Strategies to recruit and retain older Filipino-American immi- grants for a cancer screening study. J Community Health. 2005;30(3): 167---179.

80. Voytek CD, Jones KT, Metzger DS. Selectively willing and conditionally able: HIV vaccine trial participation among women at “high risk” of HIV infection. Vaccine. 2011;29(36): 6130---6135.

81. Nguyen TT, Somkin CP, Ma Y, Fung LC, Nguyen T. Participation of Asian-American women in cancer treatment research: a pilot study. J Natl Cancer Inst Monogr. 2005;(35): 102---105.

82. Brooks RA, Newman PA, Duan N, Ortiz DJ. HIV vaccine trial preparedness among Spanish-speaking Latinos in the US. AIDS Care. 2007;19(1):52---58.

83. Avis-Williams A, Khoury A, Lisovicz N, Graham-Kresge S. Knowledge, atti- tudes, and practices of underserved women in the rural South toward breast cancer prevention and detection. Fam Community Health. 2009;32(3): 238---246.

84. Tu SP, Chen HF, Chen A, Lim J, May S, Drescher C. Clinical trials: un- derstanding and perceptions of female Chinese-American cancer patients. Can- cer. 2005;104(12 suppl):2999---3005.

85. Veit CT. A single mathematical model predicts physicians’ recommenda- tions and postmenopausal women’s de- cisions to participate in a clinical trial to prevent breast cancer or coronary heart disease. Med Decis Making. 2004;24 (4):330---350.

86. Newman PA, Duan N, Roberts KJ, et al. HIV vaccine trial participation among ethnic minority communities: barriers, motivators, and implications for recruitment. J Acquir Immune Defic Syndr. 2006;41(2):210---217.

87. Ka’opua LS, Mitschke D, Lono J. Increasing participation in cancer re- search: insights from Native Hawaiian women in medically underserved com- munities. Pac Health Dialog. 2004;11 (2):170---175.

88. Murphy E, Thompson A. An ex- ploration of attitudes among Black Americans towards psychiatric genetic research. Psychiatry. 2009;72(2): 177---194.

89. Zúñiga ML, Blanco E, Martinez P, Strathdee SA, Gifford AL. Perceptions of

barriers and facilitators to participation in clinical trials in HIV-positive Latinas: a pilot study. J Womens Health (Larchmt). 2007;16(9):1322---1330.

90. Wyatt SB, Diekelmann N, Henderson F, et al. A community- driven model of research participation: The Jackson Heart Study participant recruitment and retention study. Ethn Dis. 2003;13(4):438---455.

91. Farmer DF, Jackson SA, Camacho F, Hall MA. Attitudes of African American and low socioeconomic status White women toward medical research. J Health Care Poor Underserved. 2007;18(1): 85---99.

92. Gadegbeku CA, Stillman PK, Huffman MD, Jackson JS, Kusek JW, Jamerson KA. Factors associated with enrollment of African Americans into a clinical trial: results from the African American study of kidney disease and hypertension. Contemp Clin Trials. 2008;29(6):837---842.

93. Herring P, Montgomery S, Yancey AK, Williams D, Fraser G. Understanding the challenges in recruiting Blacks to a longitudinal cohort study: the Adventist Health Study. Ethn Dis. 2004;14(3): 423---430.

94. Johnson VA, Edwards KA, Sherman SL, et al. Decisions to participate in fragile X and other genomics-related research: Native American and African American voices. J Cult Divers. 2009;16(3): 127---135.

95. Linden HM, Reisch LM, Hart A, et al. Attitudes toward participation in breast cancer randomized clinical trials in the African American community—a focus group study. Cancer Nurs. 2007;30 (4):261---269.

96. Smith YR, Johnson AM, Newman LA, Greene A, Johnson TR, Rogers JL. Perceptions of clinical research partici- pation among African American women. J Womens Health. 2007;16(3): 423---428.

97. Gollin LX, Harrigan RC, Calderon JL, Perez J, Easa D. Improving Hawaiian and Filipino involvement in clinical research opportunities: qualitative findings from Hawai’i. Ethn Dis. 2005;15(4 suppl 5):111---119.

98. Adeyemi OF, Evans AT, Bahk M. HIV-infected adults from minority ethnic groups are willing to participate in re- search if asked. AIDS Patient Care STDS. 2009;23(10):859---865.

99. Katz RV, Kegeles SS, Kressin NR, et al. The Tuskegee Legacy Project: willingness of minorities to participate in biomedical research. J Health Care Poor Underserved. 2006;17(4): 698---715.

100. Slomka J, Ratliff EA, McCurdy SA, Timpson S, Williams ML. Decisions to participate in research: views of underserved minority drug users with or at risk for HIV. AIDS Care. 2008;20(10): 1224---1232.

101. Link BG, Phelan JC. Conceptualizing stigma. Annu Rev Sociol. 2001;27: 363---385.

102. Floyd T, Patel S, Weiss E, Zaid- Muhammad S, Lounsbury D, Rapkin B. Beliefs about participating in research among a sample of minority persons living with HIV/AIDS in New York City. AIDS Patient Care STDS. 2010;24(6): 373---380.

103. Rivera-Goba MV, Dominguez DC, Stoll P, Grady C, Ramos C, Mican JM. Exploring decision-making of HIV-infected Hispanics and African Americans participating in clinical tri- als. J Assoc Nurses AIDS Care. 2011;22 (4):295---306.

104. Darnell KR, McGuire C, Danner DD. African American participation in Alzheimer’s disease research that in- cludes brain donation. Am J Alzheimers Dis Other Demen. 2011;26(6): 469---476.

105. Fouad MN, Partridge E, Wynn T, Green BL, Kohler C, Nagy S. Statewide Tuskegee alliance for clinical trials: a community coalition to enhance minority participation in medical re- search. Cancer. 2001;91(1 suppl): 237---241.

106. Byrd WM. An American Health Di- lemma: A Medical History of African Americans and the Problem of Race: Be- ginnings to 1900. Vol 1. New York, NY: Routledge; 2000.

107. Chao SZ, Lai NB, Tse MM, et al. Recruitment of Chinese American elders into dementia research: the UCSF ADRC experience. Gerontologist. 2011;51(suppl 1): S125---S133.

108. DeFreitas D. Race and HIV clinical trial participation. J Natl Med Assoc. 2010;102(6):493---499.

109. Brugge D, Kole A, Lu W, Must A. Susceptibility of elderly Asian immigrants to persuasion with respect to participation in research. J Immigr Health. 2005;7(2): 93---101.

110. Sengupta S, Strauss RP, DeVellis R, Quinn SC, DeVellis B, Ware WB. Factors affecting African-American participation in AIDS research. J Acquir Immune Defic Syndr. 2000;24(3):275---284.

111. Shavers VL, Lynch CF, Burmeister LF. Racial differences in factors that in- fluence the willingness to participate in medical research studies. Ann Epidemiol. 2002;12(4):248---256.

112. Dunlop AL, Leroy ZC, Logue KM, Glanz K, Dunlop BW. Preconsent edu-

cation about research processes im- proved African Americans’ willingness to participate in clinical research. J Clin Epidemiol. 2011;64(8):872---877.

113. Branson RD, Davis K, Butler KL. African Americans’ participation in clini- cal research: importance, barriers, and solutions. Am J Surg. 2007;193(1): 32---39.

114. Alanis AJ, Getz K. The pharmaceu- tical company/contract research organi- zation perspective. In: Increasing Minority Participation in Clinical Research: A White Paper From the Endocrine Society. Chevy Chase, MD: The Endocrine Society’s Task Force on Increasing Minority Participa- tion in Clinical Research; 2007:3---11.

115. Russell SL, Katz RV, Wang MQ, et al. Belief in AIDS origin conspiracy theory and willingness to participate in biomed- ical research studies: findings in Whites, Blacks, and Hispanics in seven cities across two surveys. HIV Clin Trials. 2011;12(1):37---47.

116. Des Jarlais G, Kaplan CP, Haas JS, Gregorich SE, Pérez-Stable EJ, Kerlikowske K. Factors affecting partic- ipation in a breast cancer risk reduction telephone survey among women from four racial/ethnic groups. Prev Med. 2005;41(3-4):720---727.

117. Minkler M, Wallerstein N. Community- Based Participatory Research for Health: From Process to Outcomes. Hoboken, NJ: Wiley.com; 2010.

118. Minkler M. Community-based re- search partnerships: challenges and op- portunities. J Urban Health. 2005;82(2 suppl 2):ii3---ii12.

119. Vargas RB, Jones L, Terry C, et al. Community-partnered approaches to en- hance chronic kidney disease awareness, prevention, and early intervention. Adv Chronic Kidney Dis. 2008;15(2): 153---161.

120. Shiu-Thornton S. Addressing cul- tural competency in research: integrating a community-based participatory re- search approach. Alcohol Clin Exp Res. 2003;27(8):1361---1364.

121. Christopher S, Watts V, McCormick AKHG, Young S. Building and maintain- ing trust in a community-based participa- tory research partnership. Am J Public Health. 2008;98(8):1398---1406.

122. Israel BA, Parker EA, Rowe Z, et al. Community-based participatory research: lessons learned from the Centers for Children’s Environmental Health and Disease Prevention Research. Environ Health Perspect. 2005;113(10):1463.

123. Chen DT, Jones L, Gelberg L. Ethics of clinical research within a community--- academic partnered participatory

SYSTEMATIC REVIEW

e30 | Systematic Review | Peer Reviewed | George et al. American Journal of Public Health | February 2014, Vol 104, No. 2

framework. Ethn Dis. 2006;16(1 suppl 1): S118---S135.

124. Quinn SC. Ethics in public health research: protecting human subjects: the role of community advisory boards. Am J Public Health. 2004;94(6): 918---922.

125. Chung B, Jones L, Dixon E, Miranda J, Wells K. Community Partners in Care Steering Council. Using a community partnered participatory research ap- proach to implement a randomized con- trolled trial: planning community partners in care. J Health Care Poor Underserved. 2010;21(3):780---795.

126. Heijnders M, Van Der Meij S. The fight against stigma: an overview of stigma-reduction strategies and interven- tions. Psychol Health Med. 2006;11 (3):353---363.

127. Minkler M. Ethical challenges for the “outside” researcher in community-based participatory research. Health Educ Behav. 2004;31(6):684---697.

128. Fisher JA, Kalbaugh CA. Challenging assumptions about minority participation in US clinical research. Am J Public Health. 2011;101(12):2217---2222.

129. Fisher JA. Medical Research for Hire: The Political Economy of Phar- maceutical Clinical Trials. New Bruns- wick, NJ: Rutgers University Press; 2008.

130. Fisher JA. “Ready-to-recruit” or “ready-to-consent” populations? In- formed consent and the limits of subject autonomy. Qual Inq. 2007;13(6): 875---894.

131. De las Nueces D, Hacker K, DiGirolamo A, Hicks LS. A systematic review of community-based participa- tory research to enhance clinical trials in racial and ethnic minority groups. Health Serv Res. 2012;47(3 pt 2): 1363---1386.

SYSTEMATIC REVIEW

February 2014, Vol 104, No. 2 | American Journal of Public Health George et al. | Peer Reviewed | Systematic Review | e31