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Interventions_for_increasing_c.PDF

RESEARCH ARTICLE

Interventions for increasing colorectal cancer

screening uptake among African-American

men: A systematic review and meta-analysis

Charles R. RogersID 1*, Phung Matthews1, Lei Xu2, Kenneth Boucher3, Colin Riley1,

Matthew Huntington 1 , Nathan Le Duc

1 , Kola S. Okuyemi

1 , Margaret J. Foster

4

1 Department of Family & Preventive Medicine, University of Utah School of Medicine, Salt Lake City, Utah,

United States of America, 2 Department of Health Education and Promotion, East Carolina University,

Greenville, NC, United States of America, 3 Cancer Biostatistics Shared Resource, Huntsman Cancer

Institute, Salt Lake City, UT, United States of America, 4 Medical Sciences Library, Texas A&M University,

College Station, TX, United States of America

* [email protected]

Abstract

Background

African-American men have the lowest 5-year survival rate in the U.S. for colorectal cancer

(CRC) of any racial group, which may partly stem from low screening adherence. It is imper-

ative to synthesize the literature evaluating the effectiveness of interventions on CRC

screening uptake in this population.

Materials and methods

In this systematic review and meta-analysis, Medline, CINAHL, Embase, and Cochrane

CENTRAL were searched for U.S.-based interventions that: were published after 1998–

January 2020; included African-American men; and evaluated CRC screening uptake

explicitly. Checklist by Cochrane Collaboration and Joanna Brigg were utilized to assess

risk of bias, and meta-regression and sensitivity analyses were employed to identify the

most effective interventions.

Results

Our final sample comprised 41 studies with 2 focused exclusively on African-American men.

The most frequently adopted interventions were educational materials (39%), stool-based

screening kits (14%), and patient navigation (11%). Most randomized controlled trials failed

to provide details about the blinding of the participant recruitment method, allocation con-

cealment method, and/or the outcome assessment. Due to high heterogeneity, meta-analy-

sis was conducted among 17 eligible studies. Interventions utilizing stool-based kits or

patient navigation were most effective at increasing CRC screening completion, with odds

ratios of 9.60 (95% CI 2.89–31.82, p = 0.0002) and 2.84 (95% CI 1.23–6.49, p = 0.01). No

evidence of publication bias was present for this study registered with the International Pro-

spective Registry of Systematic Reviews (PROSPERO 2019 CRD42019119510).

PLOS ONE

PLOS ONE | https://doi.org/10.1371/journal.pone.0238354 September 16, 2020 1 / 27

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OPEN ACCESS

Citation: Rogers CR, Matthews P, Xu L, Boucher K,

Riley C, Huntington M, et al. (2020) Interventions

for increasing colorectal cancer screening uptake

among African-American men: A systematic review

and meta-analysis. PLoS ONE 15(9): e0238354.

https://doi.org/10.1371/journal.pone.0238354

Editor: Joseph Telfair, Georgia Southern University,

UNITED STATES

Received: March 4, 2020

Accepted: August 7, 2020

Published: September 16, 2020

Copyright: © 2020 Rogers et al. This is an open access article distributed under the terms of the

Creative Commons Attribution License, which

permits unrestricted use, distribution, and

reproduction in any medium, provided the original

author and source are credited.

Data Availability Statement: All relevant data are

within the paper and its Supporting Information

files.

Funding: This study was supported by the National

Cancer Institute of the National Institutes of Health

(NIH) [grant number K01CA234319]. The content

is solely the responsibility of the authors and does

not necessarily represent the official views of the

NIH.

Competing interests: The authors have declared

that no competing interests exist.

Conclusions

Additional research is warranted to uncover effective, affordable interventions focused on

increasing CRC screening completion among African-American men. When designing and

implementing future multicomponent interventions, employing 4 or fewer interventions types

may reduce bias risk. Since only 5% of the interventions solely focused on African-American

men, future theory-driven interventions should consider recruiting samples comprised solely

of this population.

Introduction

African-American men and women in the United States (U.S.) have the highest rates of most

cancers in terms of both mortality and morbidity [1]. Despite being highly treatable when

detected early, colorectal cancer (CRC) remains the second leading cause of death in the U.S.

from cancers affecting both men and women, and the third deadliest among African Ameri-

cans [2]. African-American men are disproportionately affected by CRC, experiencing the

lowest 5-year survival rate of all racial and gender groups. Furthermore, African-American

men are 24% more likely to have CRC than white men [3]. Contributing factors to these CRC

incidence and mortality inequities among African-American men include a lack of health

insurance and limited access to early detection screening, in addition to socioeconomic disad-

vantages such as lower education levels and higher poverty rates [1, 2, 4, 5]. Other contributing

factors noted in the literature include lifestyle factors, existing chronic conditions, family his-

tory, tumor characteristics, a lack of social support, mistrust of medical systems, and percep-

tions of both racial discrimination and the African-American masculine role [3–14].

In June 2016, the U.S. Preventive Services Task Force (USPSTF), a panel of independent

national experts who provide recommendations about clinical preventive services, recom-

mended that all people, unless at heightened risk, should begin obtaining regular CRC screen-

ing at age 50 [15, 16]. In May 2018, the American Cancer Society (ACS) recommended that,

due to increasing rates of CRC in younger individuals, routine screening should begin at age

45 [17]. Evidence-based screening for CRC exists in the form of either stool-based laboratory

tests or camera-aided visual exams of the colon and rectum [17]. These options for asymptom-

atic individuals who are at average risk include the fecal immunochemical test (FIT) and

guaiac-based fecal occult blood test (FOBT), recommended yearly; the multi-targeted stool

DNA test every 3 years; a computed-tomography colonography or flexible sigmoidoscopy

every 5 years, or a colonoscopy every 10 years [17]. An estimated 50% reduction in CRC mor-

tality among the total U.S. population has been attributed to adherence to these guidelines

[18].

Although CRC screening rates have been improving since 2005, evidence suggests that

uptake remains low among African-American men and that screening is poorly understood in

this population [19, 20]. African Americans “in general” have lower screening rates than

whites (55.5% versus 61.5%) [1]. Recent research has identified several key factors associated

with lower CRC screening uptake in African-American men, including fear and anxiety, espe-

cially in regard to colonoscopy, and a lack of knowledge about the curability of early-stage

CRC [13, 21]. African-American men may also overestimate the risks associated with CRC

screening procedures [13]. In addition, the FOBT—that requires patients to avoid eating cer-

tain kinds of meat and vegetables before the collection of stool, has a lengthy testing time, and

necessitates patients handling their own fecal matter—has been associated with negative atti-

tudes among African Americans [22].

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Understanding and implementing evidence-based interventions that increase screening

uptake among African-American men is a challenge. Intervention studies have reported

mixed results about determining the most efficacious methods of increasing CRC screening

uptake overall, and few studies of this nature specific to African-American men have been con-

ducted. Furthermore, many of these trials are of low quality. Gee, Walsemann, and Brondolo

argue that such interventions should be grounded in a theoretical approach that includes cul-

tural and social factors as agents of change, as all too often healthcare interventions neglect the

importance of these aspects in patients’ healthcare decisions [23]. Accordingly, our research

team advocated for an assessment and evaluation of current evidence-based interventions that

target increasing CRC screening uptake in African-American men. To meet this goal, we con-

ducted a systematic review of the literature and a quantitative meta-analysis, with 2 aims: (1)

synthesize the evidence from published studies evaluating interventions to increase CRC

screening uptake among African-American men; and (2) quantitatively assess the evidence

from these published studies through meta-analysis to determine the most effective screening

uptake interventions for African-American men.

Rationale for systematic literature reviews

In recent decades, the amount of research on interventions to increase the uptake of CRC screen-

ing among African-American men has increased exponentially [24]. Consequently, it is more dif-

ficult for some researchers and medical professionals to digest current findings and directions in

the literature [24]. Systematic reviews thus fill an important role by providing an overview of the

current state of research on a particular topic, pointing out weaknesses and gaps in the literature,

and clarifying where disagreement or contradictions are reported, as findings from individual

studies may be inconsistent [25, 26]. Systematic methods must be used to conduct literature

reviews because nonsystematic or narrative reviews are difficult to properly assess [27]. The use of

a systematic approach also permits the researcher to create a set of parameters that allows for the

elimination of bias by excluding flawed studies from the ultimate analysis [27].

Rationale for meta-analyses

Single studies are informative for building the literature on a particular topic, especially when

evaluating treatments and interventions, but are prone to false positives and negatives [25]. A

meta-analysis provides a systematic approach for evaluating a series of studies in which those

with larger sample sizes carry more weight [25]. The strength of this technique also includes 1)

enabling researchers to provide a quantitative estimate for the effect of a treatment or interven-

tion, 2) helping researchers identify more precise estimates of intervention effectiveness or

other outcomes than any individual study in a pooled analysis [28]. Thus, by aggregating the

findings of many studies and correcting for potential error or bias, a meta-analysis helps to

identify the potential pitfalls within any single study as well as to identify studies with consis-

tent results [24]. Additionally, this technique enables researchers to identify the overall effect

of a particular treatment or intervention [25].

Materials and methods

Study selection

To be included in the review, studies had to be: (1) inclusive of African-American/Black adult

men 18 years of age or older; (2) focused on interventions for CRC screening uptake; (3) pub-

lished after 1998, 2 years before the initial publication of the American College of Gastroenter-

ology’s CRC screening guidelines [29]; (4) written in English and conducted in the U.S.; and

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(5) published, peer-reviewed, full-text journal articles. The (colorectal) cancer profile of Afri-

can-born Blacks differs from that of U.S. States-born Blacks and also varies by region of birth

[30], thus, our research team solely focused on U.S.-born African-American men. Studies

based on secondary analyses of data were excluded. Although potential for publication bias

remains, only peer-reviewed articles were considered as review for quality, relevancy, and

accuracy by multiple experts in the field provides a higher level of validity [31]. In addition,

because the research team was interested in interventions that proved to be effective in achiev-

ing increased screening completion, included studies had to report on actual CRC screening

uptake, as opposed to changes in CRC screening beliefs or intent to screen.

To determine an article’s eligibility, a team consisting of 3 systematic review screening-

trained co-investigators (authors CR, MH, and PM) performed 2 rounds of assessment. In the

first round, they reviewed potentially eligible studies by article title and abstract from the

results obtained in Rayyan QCRI, a web-based systematic-review platform that was created to

expedite the initial screening of abstracts and titles, and uses a process of semi-automation

while incorporating a high level of usability [32]. The databases Medline (Ovid), CINAHL

(EBSCO), Embase (Ovid), and Cochrane CENTRAL (Wiley) were individually searched, and

Rayyan QCRI was used to sort the retrieved manuscripts.

Last ran on January 14, 2020, the literature search combined 4 concepts: colorectal cancer,

screening, African American, and men. Each concept was searched using database thesaurus

terms and keywords as appropriate (see S1 Appendix). This method was based on the princi-

ples discussed in the Cochrane Handbook, including the combination of keywords and subject

headings [33]. Discrepancies between the 2 team members were adjudicated by the study Prin-

cipal Investigator (PI; first author CRR).

After this initial screening process, articles that potentially met all criteria, or the eligibility

of which was unclear, underwent a second round of screening in which the same 2 authors

again independently screened each article, and conflicts were resolved through face-to-face

meetings with the PI. The screening team also reviewed the references of included articles. As

a systematic review, this study did not require informed consent or institutional review board

approval as human subjects were not involved. Yet, the protocol was registered with the Inter-

national Prospective Registry of Systematic Reviews (PROSPERO 2019 CRD42019119510).

Data abstraction, risk of bias assessment, synthesis, and analysis

After articles had been accepted for the systematic review, the same 3 members of the research

team (CR, MH, PM) coded each paper individually by entering information into a standardized

Google form. Extracted data covered study characteristics such as sample size, demographics, and

eligibility criteria. Other data gathered from the accepted articles included statistical analyses used,

intervention type, theoretical background used, and limitations cited by the study authors. CR,

MH, and PM also abstracted data and met weekly to resolve any coding conflicts. Tables were con-

structed to qualitatively describe the study design and report the results of each included study.

In order to determine the potential risk of bias, each study was randomly assigned to 2 of 3

study members (CRR, PM, MF) who assessed the studies by applying the appropriate critical

appraisal criteria based on each study’s type independently. During this quality assessment

process, the two authors followed the blind review protocol [34]. In detail, Cochrane Collabo-

ration’s checklist was used to assess risk of bias for randomized control trials [35], as well as

Joanna Brigg’s checklist for quasi-experimental [36] and cohort [37] studies. All disagreements

were settled through discussions with a third member until consensus was reached.

For the meta-analysis, we first defined the values of I 2

statistics; our results showed that I 2

>75%, indicating that considerable heterogeneity was present [38, 39]. Next, substantial

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heterogeneity was investigated using meta-regression for intervention type (control interven-

tion, FIT or other stool-based screening test, printed education materials, or patient naviga-

tion) as recommended by Sharp [40] and Newton [41]. Control intervention denoted the

control group in the studies. For example, some studies reported usual care as a control group

while others mailed letters recommending CRC screening. Then, we conducted sensitivity

analyses to evaluate the effect of removing any 1 study from each meta-regression. To evaluate

for bias resulting from the absence of studies with negative or insignificant results (often

termed “publication bias”), we examined funnel plots visually for asymmetry and used the

method of Egger and colleagues to formally test for funnel-plot asymmetry [25]. The “meta-

prop” and "metareg” functions in R package “meta” and “metafor” were employed for statisti-

cal analysis, using a random intercept logistic regression model that was fitted using restricted

maximum likelihood (REML). We also used Clopper-Pearson exact binomial confidence

intervals to report, respectively, for individual studies on the funnel plots. These analyses were

conducted using R, and figures were produced using the meta package [42–44].

Results

Sample

A total of 1,465 articles were initially identified from the 4 databases searched, 41 (2.79%) were

included in the final sample for the systematic review [45–85]. As recommended by the

PRISMA group [86], Fig 1 provides details regarding the identification, screening, eligibility,

and inclusion processes. S2 Appendix details the research team’s adherence to PRISMA’s

checklist—which helped improve the reporting quality for the current study.

Characteristics of included studies

Most interventions (73%) were performed in clinical or medical facilities. The remaining 11

(27%) studies that were not conducted in a clinical setting took place in a church (12%), busi-

ness (3%), or did not report their intervention setting (12%). Studies were published between

2000 and 2019, with most (n = 12) appearing between 2010 and 2012. Two authors published

more than 1 study on the topic (11%), namely, Blumenthal (n = 2), and Leone (n = 2) [50, 54,

68, 77]. Slightly more than half (56%; n = 23) of the studies included only participants aged 50

years and older, while five (12%) included participants starting at age 45 years, three (7%)

included participants younger than 45. Twelve of the studies (29.27%) reported demographics

specific to African-American men [50, 52, 56, 57, 59, 60, 63, 66, 71, 74, 82, 84]. In the studies

aimed at increasing CRC screening uptake among African-American men, the intervention

components most frequently employed (among 135 interventions types utilized) were tele-

phone encounters or education (18%; n = 25), mailed or electronically sent educational materi-

als (13%; n = 18), FIT or other CRC stool-based screening kits (mailed or administered in

person) (13%; n = 17), patient navigation (10%; n = 13), and printed materials given to individ-

uals in person (12%; n = 16). A matrix of the included studies, sorted according to their theo-

retical design and methodological features, is found in Table 1; these features are detailed

below.

Theory. Nearly half of the studies (39%; n = 16) did not report a theoretical framework,

while the remaining studies (61%; n = 25) used 1 to 3 frameworks. A theoretical foundation

built on 1 conceptual model was most common (56%; n = 14), with the Health Belief Model

the most utilized (28%; n = 7), followed by the Preventive Health Model (16%; n = 4) and the

Transtheoretical Model (also referred to as Stages of Change) (16%; n = 4). For example, in a

study grounded by the Preventive Health Model and input from a community advisory board,

Christy and colleagues tested the effectiveness of their self-created CRC photonovella booklet

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Fig 1. Selection of studies for inclusion in review and meta-analysis.

https://doi.org/10.1371/journal.pone.0238354.g001

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Table 1. Matrix of 41 reviewed studies, according to theoretical design and methodological features.

Study Theoretical

Framework

Study Design Most Advanced Statistical

Analysis

Validly and Reliably

Reported

Number of African-American Male

Participants Reported

Arnold et al. (2019) Explicit use RCT Multivariate evaluation Validity: No Reliability:

No

Not reported

Basch et al. (2006) No framework RCT Descriptive Validity: No Reliability:

No

Not reported

Bastani et al. (2015) Explicit use RCT Multivariate evaluation Validity: No Reliability:

No

Yes

Blumenthal at al.

(2005)

Explicit use Quasi-

experimental

Multivariate evaluation Validity: No Reliability:

No

Not reported

Blumenthal et al.

(2010)

Explicit use RCT Chi-square tests Validity: No Reliability:

No

Yes

Chen et al. (2008) No framework Cohort Chi-square tests Validity: No Reliability:

No

Not reported

Christy et al. (2016) Explicit use RCT Multivariate evaluation Validity: No Reliability:

No

Not reported

Cole et al. (2017) No framework RCT Multivariate evaluation Validity: No Reliability:

No

Yes

Davis S et al. (2017) Explicit use RCT Multivariate evaluation Validity: No Reliability:

No

Not reported

Davis T et al. (2019) Explicit use RCT Multivariate evaluation Validity: No Reliability:

No

Not reported

DeGroff et al.

(2017)

Explicit use RCT Multivariate evaluation Validity: Yes Reliability:

No

Not reported

Eberth et al. (2018) No framework Cohort Descriptive Validity: No Reliability:

No

Not reported

Fiscella et al. (2011) No framework RCT Multivariate evaluation Validity: No Reliability:

No

Not reported

Ford et al. (2006) Explicit use RCT Chi-square tests Validity: No Reliability:

No

Yes

Greiner et al. (2014) Explicit use RCT Multivariate evaluation Validity: No Reliability:

No

Not reported

Gupta et al. (2013) No framework RCT Chi-square tests Validity: No Reliability:

No

Not reported

Hendren et al.

(2014)

Explicit use RCT Multivariate evaluation Validity: No Reliability:

No

Not reported

Hoffman et al.

(2017)

Explicit use RCT Multivariate evaluation Validity: No Reliability:

No

Yes

Holt et al. (2011) Explicit use Quasi-

experimental

Multivariate evaluation Validity: No Reliability:

No

Not reported

Horne et al. (2015) No framework RCT Multivariate evaluation Validity: No Reliability:

No

Yes

Inadomi et al.

(2012)

No framework RCT Multivariate evaluation Validity: No Reliability:

No

Not reported

Jandorf et al. (2013) Explicit use RCT Multivariate evaluation Validity: No Reliability:

No

Yes

Kempe et al. (2012) No framework Quasi-

experimental

Multivariate evaluation Validity: No Reliability:

No

Not reported

Khankari et al.

(2007)

No framework Quasi-

experimental

Chi-square tests Validity: No Reliability:

No

Not reported

Lasser et al. (2011) Explicit use RCT Chi-square tests Validity: No Reliability:

No

Not reported

Leone et al. (2013) No framework Quasi-

experimental

Multivariate evaluation Validity: No Reliability:

No

Not reported

(Continued)

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plus a fecal immunochemical test (FIT) kit and the CDC’s standard “Screen for Life” brochure

(not targeted to African-Americans plus a FIT kit among 330 Black participants (308 African

Americans, 22 Caribbean/Haitians/Other) in Florida who were not current with CRC screen-

ing [5]. Fifty-two percent of this sample was male. The educational messages developed for the

CRC photonovella were based on the following theoretical constructs: barriers, self-efficacy,

CRC screening coherence and salience, response efficacy, and susceptibility of focus. Also,

noteworthy, a randomized control trial (RCT) by DeGroff and colleagues was the only study

driven by 3 frameworks: the Health Belief Model, Theory of Reasoned Action, and social learn-

ing theories [73]. This patient-navigation intervention aimed to address multilevel patient-

defined barriers to CRC screening completion among 840 patients who were referred for a

colonoscopy by primary care providers in Massachusetts. Eighty percent of participants were

either non-Hispanic Black (40%) or Hispanic (40%). Two bilingual lay navigators (1 male, 1

female) delivered the intervention primarily via telephone, while some activities were con-

ducted by mail or in person, with an average time of 44 minutes per patient. Both navigators

received additional training in motivational interviewing.

Geography. Interventions were evaluated by geographic location, with 4 regions consid-

ered during coding: West, Midwest, South, and Northeast [87]. Interventions were conducted

in all 4 geographic regions: South (44%), Northeast (32%), Midwest (12%), and West (12%).

Table 1. (Continued )

Study Theoretical

Framework

Study Design Most Advanced Statistical

Analysis

Validly and Reliably

Reported

Number of African-American Male

Participants Reported

Leone et al. (2016) Explicit use RCT Multivariate evaluation Validity: No Reliability:

No

Not reported

Martin et al. (2017) Explicit use Quasi-

experimental

Descriptive Validity: No Reliability:

No

Not reported

Maxwell et al.

(2019)

No framework RCT Descriptive Validity: No Reliability:

No

Yes

Mehta et al. (2019) Explicit use Quasi-

experimental

Descriptive Validity: No Reliability:

No

Not reported

Miller et al. (2011) Explicit use RCT Multivariate evaluation Validity: No Reliability:

No

Not reported

Morgan et al.

(2010)

Explicit use RCT Multivariate evaluation Validity: No Reliability:

No

Yes

Myers et al. (2014) Explicit use RCT Multivariate evaluation Validity: No Reliability:

No

Yes

Philip et al. (2010) Explicit use Quasi-

experimental

Descriptive Validity: No Reliability:

No

Not reported

Pignone et al.

(2011)

No framework RCT Multivariate evaluation Validity: No Reliability:

No

Not reported

Resnicow et al.

(2014)

Explicit use RCT Multivariate evaluation Validity: No Reliability:

No

Yes

Reuland et al.

(2017)

No framework RCT Multivariate evaluation Validity: No Reliability:

No

Not reported

Schroy et al. (2012) Explicit use RCT Multivariate evaluation Validity: No Reliability:

No

Not reported

Siddiqui et al.

(2011)

Explicit use RCT Multivariate evaluation Validity: No Reliability:

No

Yes

Singal et al. (2017) No framework RCT Chi-square tests Validity: No Reliability:

No

Not reported

Zubarik et al.

(2000)

No framework Cohort Descriptive Validity: No Reliability:

No

Not reported

https://doi.org/10.1371/journal.pone.0238354.t001

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Most studies (90%; n = 37) reported that intervention delivery occurred in a single geographic

region, 2 articles reported delivery in 2 regions, and 2 articles did not report the location of

their interventions. For example, Leone and colleagues performed their intervention in both

Michigan and North Carolina, stating that the 2-state approach was as an effort to increase the

generalizability of their results [54].

Setting. Setting—where studies take place—is a highly influential factor for intervention

outcomes due to its potential impact on sample representation, intervention uptake, and sus-

tainability. Approximately 81% of studies implemented interventions in 1 primary setting, 7%

used multiple settings, and 12% did not report the intervention setting. For example, Blu-

menthal and colleagues delivered CRC education messages via radio, newsletters, public trans-

portation, health fairs, festivals, television programs, etc [68]. Blumenthal and colleagues used

community-based participatory research, which places the responsibility for intervention

design and delivery, including setting, in the hands of community partners [50, 68]. DeGroff

et al., Fiscella and colleagues, and Gupta et al. are examples of studies that used local resources

(i.e. established medical networks and safety clinics) to meet the disproportionate health needs

of largely minority areas [46, 58, 73]. Two studies used clinical/medical settings due to the

presence of an open-access endoscopy system, which was defined by Chen and colleagues as

providing direct referrals for CRC screening and thus bypassing additional gastroenterology

exams and decreasing the number of appointments that study participants needed to attend

[47, 49].

Interventions that took place outside of clinical or medical settings were conducted in

churches (12%), local businesses (5%), and other communal spaces (e.g., community centers,

social organizations) (~5%). Several studies justified using church-based settings because reli-

gion and faith are central themes of African-American culture; church settings are a natural

venue to introduce faith-based intervention materials; previous church-based interventions

have proven effective for addressing other health disparities in African-American populations;

and church settings may be able to reach those with limited access to healthcare [54, 60, 78].

Cole and colleagues, who conducted their intervention in New York City barbershops, empha-

sized the community-based approach, stating that––as is commonly seen among African-

American men––those with the greatest need are not accessing the healthcare system [57]. Set-

ting selection in our sample was likely also influenced by available resources, funding sources,

and population need. The effectiveness of interventions conducted in clinical versus commu-

nity-based settings should be further evaluated.

Post-intervention screening uptake. Reported screening uptake percentages among

study participants ranged from 8% to 90% [45, 76]. The intervention with the highest overall

screening uptake (81.9%) involved sending participants a culturally sensitive photonovella and

a free FIT kit [45]. Interestingly, however, this same study reported that 90% of their con-

trols––subjects who received a standard CRC screening brochure developed by the CDC,

along with the free FIT kit––also reported screening uptake [45]. Most, but not all, studies

reported higher screening uptake rates in the intervention group than in the control group.

Intervention types. Many of the studies evaluated used more than 1 intervention to

increase CRC screening (see Table 2). Often, 2 or more intervention arms were used, along

with a control arm. Intervention arms often included more than 1 component or type of inter-

vention. For example, 1 study compared patient navigation alone with patient navigation plus

motivational interviewing or a control group [57]. Another study combined a screening deci-

sion aid with patient navigation [62]. One intervention was a citywide messaging campaign

that included educational sessions at local community centers, yard signs, and messages in

newspapers [68]. Because of this heterogeneity, it was difficult to succinctly categorize studies

by the type of intervention used. However, we found that 43% (n = 16) of studies used some

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Table 2. Number of CRC interventions used in a sample of (41) reviewed studies.

Intervention Type (n = # of studies) Study

Telephone encounter/ education (n = 25) Arnold et al (2019) Eberth et al. (2018) Lasser et al. (2011) Reuland et al. (2017)

Basch et al. (2006) Fiscella et al. (2011) Leone et al. (2013) Siddiqui et al. (2011)

Bastani et al. (2015) Ford et al. (2006) Leone et al. (2016) Singal et al. (2017)

Chen et al. (2008) Gupta et al. (2013) Martin et al. (2017) Zubarik et al. (2000)

Christy et al. (2016) Hendren et al. (2014) Maxwell et al (2019)

Cole et al. (2017) Jandorf et al. (2013) Mehta et al (2019)

DeGroff et al. (2017) Kempe et al. (2012) Myers et al. (2014)

Mailed/electronic version of education materials (n = 18) Christy et al. (2016) Hendren et al. (2014) Leone et al. (2016)

Cole et al. (2017) Jandorf et al. (2013) Pignone et al. (2011)

Davis T. et al (2019) Kempe et al. (2012) Resnicow et al. (2014)

DeGroff et al. (2017) Lasser et al. (2011) Siddiqui et al. (2011)

Fiscella et al. (2011) Leone et al. (2013) Singal et al. (2017)

Gupta et al. (2013) Myers et al. (2014) Zubarik et al. (2000)

FIT/iFOBT/Stool test kit (n = 17) Christy et al. (2016) Gupta et al. (2013) Leone et al. (2016) Siddiqui et al. (2011)

Cole et al. (2017) Hendren et al. (2014) Martin et al. (2017) Singal et al. (2017)

Davis T. et al (2019) Inadomi et al. (2012) Mehta et al. (2019)

Fiscella et al. (2011) Kempe et al. (2012) Myers et al. (2014)

Greiner et al. (2014) Lasser et al. (2011) Reuland et al. (2017)

Patient Navigation (n = 13) Chen et al. (2008) Fiscella et al. (2011) Lasser et al. (2011) Reuland et al. (2017)

Cole et al. (2017) Ford et al. (2006) Leone et al. (2013)

DeGroff et al. (2017) Horne et al. (2015) Martin et al. (2017)

Eberth et al. (2018) Jandorf et al. (2013) Myers et al. (2014)

Printed Materials (n = 16) Arnold et al. (2019) Christy et al. (2016) Inadomi et al. (2012) Miller et al. (2011)

Bastani et al. (2015) Davis S et al (2017) Khankari et al. (2007) Morgan et al. (2010)

Blumenthal at al. (2005) Davis T et al (2019) Leone et al. (2016) Philip et al. (2010)

Blumenthal et al. (2010) Holt et al. (2011) Maxwell et al. (2019) Reuland et al. (2017)

One-on-One Education (n = 13) Arnold et al. (2019) Fiscella et al. (2011) Inadomi et al. (2012) Reuland et al. (2017)

Blumenthal et al. (2010) Hendren et al. (2014) Maxwell et al. (2019)

Davis S et al. (2017) Holt et al. (2011) Martin et al. (2017)

Eberth et al. (2018) Khankari et al. (2007) Philip et al. (2010)

Decision Aid (n = 6) Hoffman et al. (2017) Miller et al. (2011) Reuland et al. (2017)

Leone et al. (2013) Pignone et al. (2011) Schroy et al. (2012)

Group Education (n = 5) Blumenthal at al. (2005) Holt et al. (2011) Morgan et al. (2010)

Blumenthal et al. (2010) Leone et al. (2016)

Community Outreach (n = 4) Blumenthal at al. (2005) Leone et al. (2016) Martin et al. (2017) Morgan et al. (2010)

DVD/Video (n = 4) Hoffman et al. (2017) Leone et al. (2016) Martin et al. (2017) Morgan et al. (2010)

Educate/Train Clinical Staff (n = 4) Martin et al. (2017) Pignone et al. (2011) Schroy et al. (2012) Zubarik et al. (2000)

Case Management (n = 1) Ford et al. (2006)

Financial Assistance (n = 1) Blumenthal et al. (2010)

Financial Incentive (n = 1) Mehta et al. (2019)

Interactive Kiosk (n = 1) Greiner et al. (2014)

Open Access Colonoscopy (n = 1) Eberth et al. (2018)

Peer Counselors (n = 2) Leone et al. (2016) Maxwell et al (2019)

Resource Sheet (n = 1) Leone et al. (2016)

Online Risk Assessment (n = 1) Schroy et al. (2012)

Sigmoidoscopy Program (n = 1) Zubarik et al. (2000)

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form of tailored educational material; 32% (n = 12) included patient navigation; 22% (n = 9)

included some form of group or 1-on-1 education; 22% (n = 9) gave subjects free FIT or

immunochemical fecal occult blood test (iFOBT) kits; 9% (n = 4) employed telephone out-

reach; and 3% (n = 1) intervened at the physician level.

The intervention that performed best compared with controls was in a study by Reuland

and colleagues that incorporated a screening decision aid along with patient navigation; 68% of

participants in the intervention arm reported screening uptake compared with 27% of controls

[62]. Unfortunately, this study did not break out its screening-uptake results by race; thus, it

cannot be determined how much this intervention affected African Americans specifically.

Among African Americans specifically, the intervention that resulted in the highest screening

uptake compared with controls mailed a free FIT kit to participants, 43% of whom returned the

kit, compared with 15% of controls who engaged in some other form of screening [58].

The 2 interventions that most commonly reported significant differences in screening

uptake among African-American participants compared with controls were patient navigation

and free FIT or iFOBT kits. Tailored materials, such as culturally sensitive brochures or videos,

and education, whether in person or in a group setting, also had positive outcomes, but not to

the extent of patient navigation or free screening kits. Interestingly, Mehta and colleagues

approached CRC screening uptake by providing financial incentives via 3 arms: unconditional,

conditional, and lottery [81]. The unconditional arm was given a $10 gift card along with the

FIT kit, while those in the conditional arm received the $10 gift card after completion of the

FIT testing if within 2 months. Participants randomized to the lottery arm were afforded the

opportunity to win a $100 gift card–with a 1 in 10 chance of winning—if the FIT test were

completed and returned within the 2 months mark [81].

Intervention delivery. Interventions were most commonly implemented by the study

researchers themselves, medical personnel, or public health workers (as was the case among

patient navigation interventions). Some studies enlisted the help of local community members,

including churches, barbershops, and other local businesses [57, 68, 78, 82]. Besides the use of

patient navigators in general, there was no observed trend in CRC screening uptake related to

who implemented the intervention. For example, standard patient navigation resulted in

higher CRC screening uptake (80%) compared with peer–patient navigators (African-Ameri-

can community members who were specially trained to be patient navigators) (74%) or pro–

patient navigators (healthcare professionals who were trained to deliver culturally sensitive

patient navigation) (76%) [60].

Limitations of interventions. Most studies recognized a lack of generalizability in their

results due to the subject population or the geographic region in which the study was con-

ducted. For example, 1 study reported that “participants were recruited from healthcare pro-

viders in large urban settings, consisted of 75% females and had regular contact with a

healthcare provider, and thus are not representative of the African American community in its

entirety [67].” Another reported issue regarding generalizability relates to the potential for

selection bias, especially in studies in which the main intervention was a free FIT/iFOBT kit.

These studies first contacted the individuals to see if they were willing to participate in the

study, and then the subjects received the free kits. Because the participants were already willing

to participate in research, they may have been more likely than other members of the general

public to use and send back the FIT kits.

In many studies, especially those that used patient navigation or provided free FIT/iFOBT

kits, cost was often cited as problematic for wide-scale implementation of the intervention. A

study of 2 citywide interventions that implemented various intervention strategies reported

that radio and TV were the most effective media used, but recognized these are expensive

options that may not be financially feasible for others [68]. However, if granted financial

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incentives, Mehta et al. found the incentive amount of $10 might have been too small to pro-

mote any increase in FIT kit completion [81].

Another commonly reported limitation was the nature of the intervention follow-up. In

general, follow-up to check CRC screening status ranged from 3 to 12 months. However, it is

possible that participants obtained screening after these follow-up points and thus their data

were missed. Along with follow-up time, the ability to contact participants at follow-up was

also reported to be problematic. This was especially true in low-income populations. In 1

study, patient navigators were unable to follow up with 23% of participants [55]. This problem

was avoided in studies that had access to electronic health records where screening status

could easily be verified. However, not all studies had such capability.

Study design was also commonly mentioned as a potential limitation. Though most studies

were RCTs, few incorporated any kind of blinding because of the nature of the interventions

used (patient navigation, free FIT kits, culturally tailored brochures).

Risk of bias

Studies were allocated into 3 categories to assess for biases: Randomized Controlled Trials

([RCTs], Fig 2), Cohort (Fig 3), and Quasi-Experimental (Fig 4). Twenty-nine studies [45, 46,

48, 50–52, 54–66, 69, 71, 73–75, 77, 79–81, 83, 84] in the RCT category were largely rated as

unclear risk, yet 20 of the studies had low risk on random sequence generation (i.e., descrip-

tion of randomization procedure) [50–52, 56–63, 69, 74, 75, 79–81]. The majority of the stud-

ies (n = 13) did not explain or detail if any blinding of the participants and/or personnel in group allocation occurred, which included 18 studies with an unclear risk on allocation con-

cealment [48, 50, 52, 54, 55, 57, 63–66, 71, 74, 77, 79, 80, 83]. Either listed as a supplement in

the manuscript or published elsewhere, only 5 studies [50, 57, 58, 61, 80] reported their study

Fig 2. Risk of bias graph for RCTs.

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protocol. Overall, 26 RCTs did not account for blinding of outcomes while 6 RCTs [45, 48, 50,

56, 57, 63] received a high bias rating due to their report of additional biases. Moreover, studies

with the highest numbers of interventions (n = 9, Leone et al. 2016 [54], n = 7, Martin et al. 2017 [72], and n = 6, Reuland et al. 2017 [62]) demonstrated risk of bias scores ranging from unclear to high risks. Multicomponent studies with the lowest risk bias utilized 4 or fewer

types of interventions.

Next, 9 of the studies were classified as quasi-experimental [49, 53, 67, 68, 70, 72, 76, 78,

82]. Although only 2 of these studies contained a control group [68, 76], a high bias risk was

yielded for the remaining 7 studies. All 9 studies revealed low bias risk for outcome measure-

ment appropriate statistical analysis use. Lastly, 2 studies were considered for the cohort design

[47, 85], with both having similar ratings for low bias risk.

Meta-analyses

Meta-regression was used to compare the 4 intervention types (Table 3). The endpoint for the

meta-analysis was intervention effectiveness, defined as the proportion of participants that

obtained CRC screening during or after the intervention. Interventions that used a FIT kit or

patient navigation were significantly better than the print and control intervention at increas-

ing CRC screening uptake among African-American men, with odds ratios (ORs) of 9.60 (95%

CI 2.89–31.82, p = 0.0002) and 2.84 (95% CI 1.23–6.49, p = 0.01), respectively. Meta-analysis

results were reported for each intervention type separately (see Figs 5–7). Interventions that

used print materials were not significantly better than control interventions. To directly

Fig 3. Risk of bias graph for cohort studies.

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compare pairs of interventions, additional models were fitted restricting the studies to a pair of

interventions. In these models, FIT interventions were not superior to patient-navigation (PN)

interventions (OR = 3.42, 95% CI 0.75–15.62, p = 0.11), FIT interventions were superior to

print interventions (OR = 5.01, 95% CI 1.87–13.67, p = 0.001), and PN interventions were not

significantly different from print interventions (OR = 1.52, 95% CI 0.59–3.90, p = 0.38). There

was evidence of substantial statistical heterogeneity (range of I 2

between 93% and 98% for the

4 interventions, all p < 0.01) for combined ORs across categories. No single study significantly

influenced the meta-regression results.

Publication bias analysis

As depicted in a symmetric funnel plot (see S1 Fig), no publication bias was found in this

study [88]. Moreover, no evidence of bias was detected by Egger and colleagues’ test (bias = –

1.17, SE = 3.18, P = .72) [89].

Fig 4. Risk of bias graph for Quasi-experimental studies.

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Table 3. Random effects meta-regression results.

Variable Coefficient SE Odds Ratio Z P-value

Est. Lower 95% CI Upper 95% CI

Intercept -1.13 0.31 0.32 0.18 0.59 -3.66 0.0003

Arm

Control Intervention� (reference)

FIT 2.26 0.61 9.6 2.89 31.82 3.69 0.0002

PN 1.04 0.42 2.84 1.23 6.49 2.46 0.01

Print 0.63 0.46 1.87 0.76 4.62 1.35 0.18

�Control Intervention denoted the control group in the studies.

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Discussion

Findings overview

The purpose of this systematic review and meta-analysis was to ascertain which interventions

were most effective in increasing CRC screening uptake among African-American men. In

our qualitative analysis of the extant literature examining the various types of interventions,

patient navigation and the distribution of free stool-based test kits, including FIT and iFOBT

kits, emerged as the most consistently effective interventions. Print and other educational

materials were the most common interventions, but their results were mixed, with some stud-

ies reporting increased screening rates compared with controls, while others reported similar

or lower screening rates compared with control groups. Through using the Cochrane risk of

bias tools to assess the eligible studies in our review, we found that most RCTs failed to provide

any details about the blinding of the participants recruitment method, the allocation conceal-

ment method, and/or the outcome assessment. Future RCT research should focus on enhanc-

ing the research design quality in these specific areas, particularly in the implementation and

evaluation stages. In addition, most of the quasi-experimental studies lacked control groups in

Fig 5. Meta-analysis for control and FIT (fecal immunochemical test) interventions. Events: number of participants with screening outcomes in the arm of

the study; Total: number of participants in the arm of the study; Proportion: the ratio between Events and Total.

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their study design. Therefore, the ability to make group comparisons among participants was

challenging and it was nearly impossible to compare the interventions’ effectiveness. Statistical

evidence with both clearly defined controls are needed in future studies.

Heterogeneity of the findings made it challenging to determine which intervention was

most effective and should be considered for future studies focused on African-American men

as recommended by Kwaan and Jones-Webb [90]. Due to the diversity of settings, geographic

Fig 7. Meta-analysis for print interventions. Events: number of participants with screening outcomes in the arm of the study; Total: number of participants in the arm

of the study; Proportion: the ratio between Events and Total.

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Fig 6. Meta-analysis for PN (patient navigation) interventions. Events: number of participants with screening outcomes in the arm of the study; Total: number of

participants in the arm of the study; Proportion: the ratio between Events and Total.

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regions, interventions employed, and outcomes measured, factors other than the intervention

may have influenced CRC screening uptake. For example, most studies were conducted within

a medical clinical or hospital. This setting in and of itself may have increased CRC screening

uptake by increasing access to other resources (e.g., electronic health records, scheduling ser-

vices, screening materials).

Further, it should be noted that most of the interventions were implemented by healthcare

professionals, including physicians, public health workers (e.g., patient navigators), and the

researchers themselves. This may have influenced screening uptake rates as participants may

have had an implicit bias toward obtaining CRC screening to please researchers or doctors.

Conversely, medical mistrust—a common factor that significantly contributes to delays in

healthcare system utilization by African-American men—may have discouraged African

American study participants specifically from obtaining CRC screening [3].

Future directions

Only 2 of 41 studies reviewed (5%) focused exclusively on African-American males [57, 66].

Though each study included some African-American males, researchers rarely examined bar-

riers and enablers specific to this group, which continues to suffer the most from CRC inci-

dence and mortality [1]. The lack of understanding of CRC screening-completion barriers and

enablers among African-American men was exacerbated in our study by the lack of distinction

in the data reported for race and gender. Studies that segmented data by race or gender did

one or the other but not both, leaving the African-American male experience with CRC

screening further underrepresented in intervention studies. To achieve the goal of reducing

CRC-related inequities among African-American men, health promotion and prevention

interventions that centralize cultural identity and cultural empowerment should be developed

in order to better capture African-American men’s CRC screening experiences within a cul-

ture-specific context and their understanding of those experiences [91, 92].

Our inclusion criteria for the review required a study population that included African-

American men, and this specification may have been the cause of the geographic dispersion

among the interventions evaluated. The U.S. Census Bureau reports that a majority of the Afri-

can-American population of the U.S. is concentrated in the Southern and Northeastern

regions [93]. Additionally, African Americans experience greater CRC incidence, higher mor-

tality, and lower survival at all stages, when compared to their white counterparts, and several

articles mentioned that the geographical locations where interventions were implemented had

large populations of African Americans experiencing CRC disparities [3, 19, 49, 59, 78]. How-

ever, the majority of the studies (76%) is this review occurred in Eastern and Southern states,

with only 25% in Western and Midwestern states. The preponderance of data from the East

and South––while helpful for providing insight into regional barriers and enablers to CRC

screening uptake––is not equally applicable to all African-American populations. Given geo-

graphical variability in diet, culture, and intergenerational attitudes along with the effect of

these variables on CRC screening outcomes, more-specific regional information is required to

develop effective interventions in understudied areas. Western states, though included in only

12% of the studies evaluated, are home to the nation’s most ethnically diverse populations and

currently represent what is projected to be a nationwide shift in the ratio of ethnic-to-noneth-

nic residents [94, 95]. Specifically, the West encompasses 13 of the 25 most ethnically diverse

cities in the nation and the most ethnically diverse state, California, with a census-reported

population that is 39% Hispanic-white and 36% non-Hispanic white [94, 96]. As more regions

transform to resemble California’s demographic distribution, it is critical that future research

includes and emphasizes the barriers and enablers of CRC screening completion in minority-

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majority areas. More geographically dispersed studies occurring outside of the Southern and

Northeastern regions of the U.S. are needed. Moreover, with the unscreened populations in

these regions, subgroup differences for those experiencing CRC disparities are yet to be

identified.

It is noteworthy that slightly over 75% of the interventions aimed at increasing CRC screen-

ing uptake occurred in medical or clinical settings. Although many of these studies did not

provide a justification for choosing to provide the intervention in a clinical setting, this deci-

sion may have been due to ease of data access, convenience sampling, or community needs.

While many of the initiatives to promote CRC screening described in this review took place in

healthcare settings and have proved successful, it is likely that individuals who did not seek

routine medical care, did not have a regular healthcare provider, or lived with lower socioeco-

nomic status were excluded from the interventions [19]. In particular, the aforementioned sce-

narios have been demonstrated as potential barriers that prevent African-American men from

seeking or obtaining CRC screening [97–100]. Therefore, to reduce the pervasive CRC screen-

ing disparities faced by African-American men, it is important for future public health work-

ers, healthcare organizations, patient navigators, researchers, and physicians to consider

collaborating to design, evaluate, and implement interventions in non-healthcare settings.

In this review, 24% of the included studies formulated and conducted their CRC interven-

tion programs in churches, local businesses (e.g., barbershops), and other community settings

[47, 57, 68, 78, 101]. For example, Holt and colleagues discussed using church-based

approaches to promote CRC prevention behaviors through a series of community health advi-

sor–led educational modules [78]. However, results from the educational series suggested that

adding spiritual themes did not result in significant behavioral changes among attendees. This

might further validate the role of other contributing factors, such as lack of health insurance,

lack of access to early-detection screening, medical system mistrust, and socioeconomic disad-

vantages as mediators influencing early detection screening behavior changes among African-

American men, and thus, should be considered alongside the other well-documented barriers

to CRC screening [101, 102].

Furthermore, as highlighted in a previous systematic review by Rogers and colleagues, there

is a need to better understand the influence of sociocultural determinants that may influence

African-American men’s negative responses, reluctance, and apprehension associated with

CRC screening [103]. Culturally sensitive community-based interventions among African-

American men should be further developed and implemented. However, a few other cautions

should be considered by future researchers while designing Federally Qualified Health Center

(FQHC) non-clinically–based programs. Maxwell and colleagues noted that it remained chal-

lenging to implement and sustain their community-based programs to increase CRC screening

among Filipino Americans primarily due to (1) the need for program participants to seek

screening through their healthcare providers, (2) lack of funds to sustain the program, and (3)

lack of an adequately trained workforce to maintain program activities [104]. Similarly, it is

imperative to test the effectiveness of community-based interventions in an environment that

supports the sustainable growth of CRC screening promotion programs for African-American

men. Moreover, to ensure that African-American men receive the optimal benefits of early

detection screening for CRC, researchers must move beyond traditional practice-based set-

tings into community-based locations.

Lastly, from the research team’s observations, cost was a dominant concern or barrier in

implementing large-scale CRC screening interventions across the selected studies. Cost-effec-

tiveness strategies require an overall assessment of patient and provider barriers, the naviga-

tion system, and other potential inhibitors of CRC screening [105]. Because a significant

burden of CRC and observed disparities in CRC screening uptake still exists among African-

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American men, programs tailored to this population should consider how to effectively

enhance knowledge of the benefits of CRC screening, improve access to health care, and ele-

vate the related insurance services [15, 103–105]. In clinical settings, strategies to better utilize

patient navigation systems to emphasize the importance of screening and enhance educational

outreach for healthcare providers who provide routine care for African-American men could

conceivably aid in lowering the cost of promoting CRC screening, particularly among low-

income patients [105]. In community settings, interventions that could efficaciously dispel the

mistrust and ease the anxiety associated with screening are vital to promoting screening

among African-American men [19, 102]. According to Adams and colleagues in a recent sys-

tematic review, African-American men often face unique challenges and express substantial

fears about medical procedures associated with CRC [106–108]. Adams and colleagues

reported that higher mistrust scores correlated with lower CRC screening rates among Afri-

can-American men in most of the quantitative studies included in their review [96, 106, 109].

In addition, several dominant recurring themes such as “mistrust as a barrier to screening,”

“skepticism of provider motives,” and “mistrust of competence and quality of providers/sys-

tems” were identified in qualitative studies [74, 106, 110].

Future studies should thoroughly evaluate the effectiveness of different modes of interven-

tion—e.g., patient navigators, telephone outreach, and text messaging. For example, in an

effort to explore CRC screening among African-American church members using both quali-

tative and quantitative methods, the quality of patient-provider communication proved to be

the most influential factor in participants’ completion of CRC screening [111]. From the arti-

cles included in this review, we can conclude that it is debatable which CRC promotion modes

work best for African-American men. However, our meta-analysis results revealed that future

interventions utilizing FIT or enhancing patient navigation suited better than traditional

methods in increasing CRC screening uptake among this group. Traditional methods included

usual care as seen in the control groups of the study, and was significantly inferior to the FIT

(p = 0.0002) and patient navigation interventions (p = 0.01). Print interventions were also sec- ondary juxtaposed to FIT (p = 0.001). As recommended in the 2019 CRC screening messaging guidebook, promoting CRC screening via text messaging could be a cost-effective strategy to

improve interventions compared with traditional methods (e.g., mailings, printed materials,

telephone reminders) [112]. More research and evidence are warranted to identify more cost-

beneficial interventions focused on motivating unscreened African-American men to seek rec-

ommended CRC screening.

Limitations

Our study is not without limitations. First, although our publication bias analysis found no

such bias, it cannot be ruled out, as studies with negative findings were less likely to be pub-

lished. Secondly, a significant challenge with our meta-analysis was the heterogeneity of the

published data. Most of the studies we reviewed could not be included in the meta-analysis

because they did not provide sample or study-outcome data specific to African Americans,

especially African-American men, or because the interventions were too dissimilar to combine

with other studies. Moreover, since most studies had different inclusion criteria, it was impos-

sible to adjust for a confounder or covariate unless all levels of the covariate were available in

all studies. Since this resulted in difficulty teasing out which intervention components were

most effective, the meta-analysis results must be interpreted with caution. Next, due to the

small sample, aforementioned heterogeneity, and the notion that ‘the best CRC screening test

is the one that gets done’, the data captured for the meta-analysis focused on the proportion of

participants who completed CRC screening juxtaposed to specific types of screening. On

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account of the significant difference in the nature of CRC screening modalities, such as colo-

noscopy vs. FIT, separate analyses (both in future systematic review and meta-analyses) may

reveal different results regarding strengthening future interventions for increasing CRC

screening completion. Furthermore, since most clinical trials require 2–4 phases—potentially

causing minor to major percentage differences for CRC screening uptake based on the effects

of different intervention approaches, a more thorough systematic approach that compares

these differences as well as conduciveness of different CRC screening modalities in clinical ver-

sus community settings may be useful to detect the intervention outcomes. Nevertheless, our

findings highlight the lack of consensus in the literature regarding interventions for increasing

CRC screening uptake, especially among African-American males. Lastly, although our

research team made every effort to ensure our search yielded all applicable data and no publi-

cation bias was found in this study, it is possible that some articles were missed and the ability

of bias to distort results of future meta-analyses and systematic reviews should be considered.

Conclusions

In summary, this systematic review and meta-analysis examined the existing evidence for

interventions aimed at increasing CRC screening uptake among African-American men. Most

of the included studies used approaches such as patient navigation, telephone outreach, tar-

geted brochures, and other multicomponent promotion packages to enhance CRC screening

rates. Yet, our findings reflected a dearth of studies unambiguously focused on African-Ameri-

can men. Only 2 of the 41 studies in our review (5%) specifically explored the efficacy of CRC

screening-promoting initiatives among African-American men. Since half of the reviewed

studies were guided by 1 or multiple conceptual frameworks, a greater number of theory-

driven CRC screening interventions are needed. Since studies with the lowest risk of bias

employed 4 or fewer interventions, future multicomponent interventions should consider this

evidence when designing and implementing CRC screening completion-focused studies

among African-American men and other underserved populations. To achieve the National

Colorectal Cancer Roundtable’s challenge to attain screening rates of 80% or higher in every

community, further study is warranted that considers employing evidence-based, cost-effec-

tive, and culture-specific techniques targeting CRC screening completion among African-

American men outside of traditional clinic settings.

Supporting information

S1 Appendix. Search strategy syntax.

(PDF)

S2 Appendix. PRISMA checklist.

(PDF)

S1 Fig. Begg’s funnel plot with 95% confidence limits.

(PDF)

Acknowledgments

The research team extends appreciation to Eleanor Mayfield for editorial support. This study

was supported by Huntsman Cancer Institute’s Cancer Biostatistics Shared Resource at the

University of Utah and the National Cancer Institute of the National Institutes of Health

(NIH) [grant numbers K01CA234319 and P30CA042014]. All relevant materials discussed in

this study—registered with the International Prospective Registry of Systematic Reviews

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(PROSPERO 2019 CRD42019119510)—may be requested from the corresponding author free

of charge. The content is solely the responsibility of the authors and does not necessarily repre-

sent the official views of the NIH, Huntsman Cancer Institute, or the University of Utah.

Author Contributions

Conceptualization: Charles R. Rogers, Kenneth Boucher, Kola S. Okuyemi, Margaret J.

Foster.

Data curation: Charles R. Rogers, Margaret J. Foster.

Formal analysis: Charles R. Rogers, Phung Matthews, Kenneth Boucher, Colin Riley, Matthew

Huntington.

Funding acquisition: Charles R. Rogers.

Investigation: Charles R. Rogers.

Methodology: Charles R. Rogers, Phung Matthews, Kenneth Boucher, Margaret J. Foster.

Project administration: Charles R. Rogers.

Supervision: Margaret J. Foster.

Validation: Phung Matthews.

Writing – original draft: Charles R. Rogers, Lei Xu, Kenneth Boucher, Colin Riley, Matthew

Huntington, Nathan Le Duc, Kola S. Okuyemi, Margaret J. Foster.

Writing – review & editing: Charles R. Rogers, Phung Matthews, Lei Xu, Kenneth Boucher,

Colin Riley, Matthew Huntington, Nathan Le Duc, Kola S. Okuyemi, Margaret J. Foster.

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