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. Author manuscript; available in PMC: 2024 Oct 1.
Published in final edited form as: Am J Gastroenterol. 2023 Aug 22;118(10):1829–1840. doi: 10.14309/ajg.0000000000002478

Effect of Behavioral Interventions on the Uptake of Colonoscopy for Colorectal Cancer Screening: A Systematic Review and Meta-analysis

Stephanie Yakoubovitch 1, Timothy Zaki 2, Sanya Anand 3, Jillian Pecoriello 4, Peter S Liang 5,6
PMCID: PMC10592067  NIHMSID: NIHMS1925913  PMID: 37606070

Abstract

Background:

Screening decreases colorectal cancer (CRC) incidence and mortality, but uptake in the United States remains suboptimal. Prior studies have investigated the effect of various interventions on overall CRC screening and stool-based testing, but the effect on colonoscopy—the predominant screening test in the US—has not been fully examined. We performed a systematic review and meta-analysis to assess the effect of behavioral interventions on screening colonoscopy uptake.

Methods:

We searched PubMed, EMBASE, and Cochrane databases through January 2022 for controlled trials that assessed the effect of behavioral interventions on screening colonoscopy uptake. All titles, abstracts, and articles were screened by at least two independent reviewers. Odds ratios were extracted from the original article or calculated from the raw data. The primary outcome was the relative increase in screening colonoscopy completion with any behavioral intervention. We performed random effects meta-analysis, with subgroup analysis by type of intervention.

Results:

A total of 25 studies with 30 behavioral interventions were analyzed. The most common interventions were patient navigation (n=11) and multi-component interventions (n=6). Overall, behavioral interventions increased colonoscopy completion by 54% compared to controls (OR 1.54, 95% CI 1.26–1.88). Patient navigation (OR 1.78, 95% CI 1.35–2.34) and multi-component interventions (OR 1.84, 95% CI 1.17–2.89) had the strongest effect on colonoscopy completion among interventions examined in multiple studies. Significant heterogeneity was observed both overall and by intervention type. There was no evidence of publication bias.

Conclusions:

Behavioral interventions increase screening colonoscopy completion and should be adopted in clinical practice. In particular, patient navigation and multi-component interventions are the best-studied and most effective interventions.

Introduction:

Colorectal cancer (CRC) accounts for 8.2% of all incident cancers in the United States (US) and is the second leading cause of cancer death.(1,2) However, CRC incidence has been declining since the 1980s, and age-adjusted mortality has fallen from 21.5 per 100,000 persons in 1997 to 13.5 per 100,000 persons in 2017.(2)

Microsimulation modeling estimates that 50% of the observed reduction in CRC incidence and mortality can be attributed to screening.(3) However, screening uptake in the US remains suboptimal, and in 2018 only 68.8% of individuals aged 50 to 75 years were up to date with screening.(4)

Colonoscopy is the predominant screening modality used in the US and has been shown to reduce CRC incidence and mortality in the per-protocol analysis of a recent randomized controlled trial,(5,6) but the complexity of the bowel preparation process and invasiveness of the procedure pose a challenge for many individuals.(7) Undergoing colonoscopy for CRC screening is itself a healthcare-seeking behavior, but it is unclear whether behavioral interventions can increase colonoscopy uptake. Behavioral interventions such as patient navigation, text messaging, and active choice through the electronic health record (EHR) have been shown to be effective in promoting screening for breast and cervical cancer, as well as CRC.(8–10) We conducted a systematic review and meta-analysis to evaluate the effect of behavioral interventions on screening colonoscopy use.

Materials and Methods

Search Protocol:

We followed the Preferred Reporting Items for Systematic Reviews and Meta Analyses (PRISMA) guidelines to conduct the search and review. At least two authors (SY, SA, JP, TZ) independently searched the PubMed, EMBASE, and Cochrane Library databases. The search was conducted through January 2022 without date or language restriction, using predetermined search criteria. We used the following search terms: PubMed—(“colorectal neoplasms” AND screening AND behavior AND intervention); EMBASE—(screening and colorectal cancer and (intervention or trial)); Cochrane Library—(colorectal cancer screening and intervention). The search criteria terms were determined by a combination of literature review and previous work conducted in collaboration with a research librarian. Titles and abstracts were screened by at least two authors, and disagreements were resolved by the senior author (PSL). We only included controlled trials that reported the effect of behavioral interventions on screening colonoscopy uptake, and which included risk estimates or values necessary to calculate risk estimates. Studies that did not specify colonoscopy as the screening modality were excluded. There was no age restriction for participants.

Data Extraction:

At least two investigators independently extracted the following information for each study: author, year of publication, country of study, age range, study population, number of participants in intervention and control groups, intervention type, duration of follow-up, adjustment variables, risk estimate, and variance. If multiple publications reported on the same population, we used the most recent or complete data available. Any discrepancies in the data extraction were resolved by consensus. We also assessed risk of bias using the Cochrane tool and converted the results to the Agency for Healthcare Research and Quality’s (AHRQ) categories of good, fair, or poor.(11)

Statistical Analysis:

We used the Dersimonian and Laird random effects model to compute the odds ratio (OR) and 95% confidence interval (CI) for colonoscopy use in the behavioral intervention groups versus controls groups. We performed sensitivity analyses to assess whether the risk estimate differed for specific populations. The estimate of heterogeneity was derived from the Mantel-Haenszel model. We evaluated for heterogeneity using the I2 statistic and considered values of 25%, 50%, and 75% as low, moderate and high heterogeneity, respectively. Begg’s test, Egger’s test, and the funnel plot were used to assess for publication bias.(12) To evaluate whether results differed by study quality or duration of follow-up, we performed a random effects meta-regression based on risk of bias category and follow-up length, respectively. Statistical significance for all tests was set at P < 0.05. All analyses were performed with Stata/MP 16.1 (StataCorp, College Station, TX).

Results:

Description of Studies:

Figure 1 shows the study flowchart. We identified 8,704 titles using the search terms. After title and abstract screening, 441 papers were included for full text review. Twenty-five studies with 30 interventions were included in final analysis. Interventions were categorized into one of the following 10 types (Figure 2): letter, informational brochure, multi-component, patient navigation, telephone consultation, primary care provider (PCP) counseling, video, EHR, email, and financial incentives. Studies with two or more individual interventions were classified as multi-component.

Figure 1:

Figure 1:

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Flowchart

Figure 2:

Figure 2:

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Forest plot of colonoscopy uptake by behavioral intervention type

Table 1 shows characteristics of the 25 studies and 30 interventions, including a brief description of each intervention. A total of 30,064 participants were included, and the median duration of follow-up was 6 months. Twenty-one studies were randomized controlled trials and 6 were population-based.(13–18) Several studies focused on specific populations: 6 involved low-income or racial minority groups in the US,(19–24) 3 examined individuals with first-degree relatives with CRC,(17,18,25) and 1 studied persons with human immunodeficiency virus (HIV).(26) Six studies included patients younger than 50 years.(15,17,18,22,27,25) In terms of behavioral interventions, 3 interventions used mailed letters,(13,16,28) 3 used informational brochures, (24,29) 11 studied patient navigation,(17–21,23,25,30–32) 1 examined pre-procedural telephone consultations,(14) 1 studied PCP counseling,(33) 2 used videos,(22,26) 1 changed EHR settings,(10) 1 employed an email intervention,(34) and 1 used a financial incentive.(35) Six interventions studied the effects of multiple concurrent interventions.(15,27,28,34,36) Of the trials that combined multiple behavioral interventions, all but one combined a form of patient navigation with an additional intervention such as telephone calls, additional education, or mailed stool tests. One study offered financial incentives as part of a multi-component approach.

Table 1:

Characteristics of included studies and interventions

ID Author Year Country Age, years Female, % Total, n Intervention, n Control, n Intervention Target Follow up, months Description
1 Corbett 2004 Australia 55–74 50.9 392 206 186 Letter Patient n/a Invitation letter signed by general practitioner sent to patients in their practice (intervention) vs. letter without practitioner signature sent by electoral commission to residents (control)
2 Denberg 2006 US 50+ 61.8 781 386 395 Brochure Patient 4 Informational brochure about colonoscopy sent to patients in internal medicine practice (intervention) vs. usual care (control)
3 Ling 1 2009 US 50–79 55.1 257 133 124 Letter Patient 12 Tailored physician recommendation letter sent to primary care patients and nonenhanced office/patient management (intervention) vs. nontailored letter and nonenhanced management (control)
4 Ling 2 2009 US 50–79 55.1 276 152 124 Multi-component Patient/Physician/Office staff 12 Tailored physician recommendation letter sent to primary care patients and enhanced office/patient management (intervention) vs. nontailored letter and nonenhanced management (control)
5 Ling 3 2009 US 50–79 55.1 314 190 124 Multi-component Physician/Office staff 12 Nontailored physician recommendation letter sent to primary care patients and enhanced office/patient management (intervention) vs. nontailored letter and nonenhanced management (control)
6 Meng 2009 China 40–74 64.3 3288 1430 1858 Multi-component Patient 12 Patients at high risk for CRC based on questionnaire or stool test who received a barrier-focused intervention program (intervention) vs. those who did not (control)
7 Percac-Lima 2009 US 52–79 60.0 1223 409 814 Navigation Patient 9 Letter with educational material followed by phone or in-person contact by language-concordant health worker navigator (intervention) vs. usual care (control). Low-income, ethnically diverse primary care population
8 Lasser 2011 US 52–74 61.5 465 235 230 Navigation Patient 12 Letter with educational material signed by PCP followed by phone-based language-concordant navigation by health worker (intervention) vs. usual care (control). Low-income, ethnically diverse primary care population
9 Stoop 2012 Netherlands 50–75 51.5 6600 3302 3298 Telephone Patient 1 Telephone-based (intervention) vs. in-person (control) pre-colonoscopy consultation for regional residents
10 Braschi 2013 US 50+ 70.9 392 225 167 Navigation Patient 6 Culturally-targeted telephone navigation by health professional (intervention) vs. standard navigation (control) for Latino American primary care patients
11 Jandorf 1 2013 US 50+ 68.0 169 123 46 Navigation Patient 6 Culturally-targeted, racial-concordant telephone navigation by health care professional (intervention) vs. standard navigation (control) for African American primary care patients
12 Jandorf 2 2013 US 50+ 68.0 227 181 46 Navigation Patient 6 Culturally-targeted, racial-concordant telephone navigation by trained community member (intervention) vs. standard navigation (control) for African American primary care patients
13 Boguradzka 2014 Poland 50–65 69.7 600 300 300 PCP counseling Patient 6 PCP counseling (intervention) vs. information leaflet (control) in primary care setting
14 Kinney 2014 US 30–74 57.4 481 232 249 Multi-component Patient 9 Patients at high risk for CRC based on family history who received a mailed educational brochure and tailored visual aids/risk assessment/counseling/summary letter/reminder card (intervention) or mailed educational brochure only (control)
15 Ferron 2015 US 50+ 64.7 33 17 16 Video Patient 8 Educational video and decision aid (intervention) vs. usual care (control) for patients in HIV clinic
16 Hoffman 2016 US 49–75 67.4 89 59 30 Video Patient 3 Culturally-tailored patient decision aid video about CRC screening (intervention) vs. video about hypertension for African American primary care patients
17 Ingrand 2016 France 17–75 48.0 304 160 144 Navigation Patient/Sibling 12 Nurse-led telephone-based tailored intervention (intervention) vs. standard screening information given to sibling (control) for patients at high risk for CRC based on sibling history
18 Patel 2016 US 50–74 63.2 2224 967 1257 EHR Physician/Staff 6 Active choice alert in electronic health record to accept or cancel a colonoscopy order (intervention) vs. usual care (control) in primary care
19 Pisera 2016 Poland 55–64 50.4 967 488 479 Letter Patient 6 Reinvitation letter with prespecified colonoscopy date and reminders (intervention) vs. invitation to educational meeting (control) for patients who did not previously respond to invitation to participate in a screening colonoscopy trial
20 DeGroff 2017 US 50–75 56.9 843 429 427 Navigation Patient 6 Primarily telephone-based navigation delivered by lay navigators (intervention) vs. usual care (control) in racially diverse, low income primary care setting
21 Green 2017 US 50–74 54.6 4653 3490 1163 Multi-component Patient 60a Over 5 years, a combination of stepped increases of support consisting of an automated mailing program, plus telephone assistance if needed, plus nurse navigation if needed (intervention) vs. usual care (control) for patients in an integrated health care organization primary care setting
22 Mehta 1 2017 US 50–64 74.0 1497 748 749 Email Patient 3 Email with active choice to opt in or opt out (intervention) vs. email containing telephone number for scheduling (control) for health system employees
23 Mehta 2 2017 US 50–64 74.4 1497 748 749 Multi-component Patient 3 Email with active choice to opt in or opt out plus a $100 incentive (intervention) vs. email containing telephone number for scheduling (control) for health system employees
24 Bauer 2018 Germany 28–75 64.4 261 125 136 Navigation Patient 1 Nurse-led telephone-based counseling plus informational materials and invitation to colonoscopy (intervention) vs informational materials and invitation to colonoscopy (control) for patients with high risk for CRC based on family history
25 Temucin 2020 Turkey 50–70 65.5 110 55 55 Navigation Patient 6 Nurse-led navigation (intervention) vs. usual care (control) at a family health center
26 Mehta 3 2020 US 50–64 77.0 1977 990 987 Financial incentive Patient 3 Risk assessment, direct access colonoscopy scheduling, $10 loss-framed incentive to complete risk assessment, and $25 incentive for colonoscopy completion (intervention) vs. risk assessment and direct access colonoscopy scheduling (control) for health system employees
27 Duhamel 1 2020 US 50–85 62.2 182 116 66 Brochure Patient 12 Telephone-based patient navigation plus standard CDC print materials (intervention) vs. patient navigation (control) for Latino primary care patients
28 Duhamel 2 2020 US 50–85 62.2 188 122 66 Brochure Patient 12 Telephone-based patient navigation plus culturally-targeted print materials (intervention) vs. patient navigation (control) for Latino primary care patients
29 Paskett 2020 US 25–75 56.7 271 139 132 Navigation Patient 14 Patient navigation plus website with personal screening recommendation (intervention) vs. website recommendation (control) for patients at high risk for CRC based on family history
30 Abuelo 2020 US 50–74 51.0 251 126 125 Navigation Patient 6 Telephone-based or in-person patient navigation by health worker (intervention) vs. usual care (control) for patients with mental illness and/or substance abuse disorder
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Abbreviations: n/a, not available; EHR, electronic health record; CRC, colorectal cancer; PCP, primary care provider

a

Colonoscopy completion was assessed on a yearly basis over the 5 year study period

Effect of Behavioral Interventions on Colonoscopy Uptake:

Overall, behavioral interventions increased colonoscopy uptake by 54% compared to controls (OR 1.54, 95% CI: 1.26–1.88, Figure 3). Patient navigation (OR 1.78, 95% CI: 1.35–2.34) and multi-component interventions (OR 1.84, 95% CI: 1.17–2.89) exerted the strongest effect on colonoscopy completion for interventions that were examined in multiple studies (Figure 2). The single PCP counseling intervention had a strong effect but a wide confidence interval (OR 5.33, 95% CI 3.55, 8.00). The single telephone intervention resulted in lower colonoscopy uptake compared to controls (OR 0.87, 95% CI: 0.77–0.98). No other intervention type was associated with a statistically significant change in colonoscopy completion.

Figure 3:

Figure 3:

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Forest plot of the overall association between behavioral interventions and colonoscopy uptake

In sensitivity analyses, we examined the effect of excluding trials that focused on specific populations. When excluding studies that involved low-income or racial minority groups in the US,(19–24) the effect of overall interventions (OR 1.71, 95% CI 1.35–2.18) and patient navigation (OR 2.38, 95% CI 1.90–2.98) increased and the effect of informational brochures (OR 1.68, 95% CI 1.25–2.26) and videos (OR 5.28, 95% CI 1.20–23.32) both became significant. Without individuals who had first-degree relatives with CRC,(17,18,25), the effect of overall interventions (OR 1.48, 95% CI 1.20–1.83) and patient navigation both decreased (OR 1.62, 95% CI 1.14–2.30). Removing the single study that focused on individuals with HIV did not appreciably change the effect of interventions overall or by subtype (26).

Heterogeneity was high overall (I2=87.9%, P<0.001) and for multi-component interventions (I2=93.4%, P<0.001), and was moderate to high for patient navigation (I2=62.0%, P=0.003). Neither the Egger test (P=0.06) nor the funnel plot (Figure 4) showed evidence of publication bias. Based on AHRQ standards for risk of bias, 17 of the 25 studies were considered good quality, 8 were fair, and none were poor. Meta-regression showed results did not differ for good and fair quality studies. Data on duration of follow-up was available for 29 interventions. Green et al. had by far the longest follow-up (60 months),(37) as its definition for follow-up differed from other studies. Meta-regression, both including and excluding the Green et al. study, showed no association between duration of follow-up and effect size.

Figure 4:

Figure 4:

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Funnel plot to assess publication bias

Discussion:

In this systematic review and meta-analysis of 25 studies with 30 interventions and 30,064 participants, we found that behavioral interventions increased screening colonoscopy participation by 54%. Specifically, multi-component and patient navigation interventions were the most consistently effective for improving uptake. PCP counseling was highly effective in a single study, but the result requires confirmation.

To our knowledge, this study is the first to examine the effect of behavioral interventions on colonoscopy specifically, although others have evaluated interventions for CRC screening overall. We excluded trials whose primary endpoint was completion of any CRC screening test, rather than specifically colonoscopy. A survey showed that after thorough side-by-side comparison of the fecal occult blood test (FOBT) and colonoscopy, 53% of participants preferred FOBT over colonoscopy because of factors such as convenience, comfort, cost, and preparation and procedure times.(38) However, data from the 2018 National Health Interview Survey indicated that 91% of individuals aged 50 to 75 who were up-to-date with screening had undergone a colonoscopy.(5) Therefore, the lack of a systematic review summarizing the evidence for behavioral interventions for screening colonoscopy uptake is a major gap in the literature.

Dougherty et al. showed that fecal occult blood testing (FOBT) outreach (RR 2.26, 95% CI: 1.81–2.81) and patient navigation (RR 2.01, 95% CI, 1.64–2.46) were most strongly associated with increased CRC screening relative to usual care in randomized clinical trials conducted in the US.(39) Similarly, we found a significant association between navigation and screening colonoscopy after assessing 11 interventions in 10 studies. Overall, our results support and extend these previous findings to colonoscopy, which remains by far the most popular screening modality in the US.(5) Since the invasive nature of colonoscopy presents different barriers for patient acceptance compared to stool testing,(7) it is reassuring that similar interventions appear effective across CRC screening modalities.

Patient navigation has improved CRC screening in several contexts, such as stool testing and follow-up after abnormal stool tests,(19) in minority groups with language barriers,(23,24) groups with mental illness,(32) and low-income and underinsured populations.(31,39) In the 11 interventions that investigated patient navigation alone, we observed substantial heterogeneity with respect to both the backgrounds of the navigators and the format of the navigation. Navigators included lay persons,(21,23) nurses,(17,18,30) and other health workers.(19–21,31,32) The interventions introduced by the navigators also varied, ranging from scripted to individualized prompts and in-person versus telephone-based communication (Table 1). Five of the 11 interventions did not result in increased screening, although 3 of these tested culturally-targeted navigation compared to standard navigation rather than usual care in the absence of navigation.(20,21) For the remaining studies that used control groups without navigation, there was no navigator type or patient population for which navigation appeared consistently ineffective. Despite the heterogeneity in navigation programs, our findings suggest that if the principle of patient-centered care is observed, there can be many effective ways to perform patient navigation and the approach can be both flexible and tailored to a specific population. These data strongly support the implementation of various forms of patient navigation.

Of the 6 multi-component interventions that we identified, 5 included patient navigation. Generally, most interventions combined patient navigation with additional reminders in the form of letters, phone calls, and emails. All of the interventions increased colonoscopy uptake except for the study by Green et al., in which patients who failed to schedule their colonoscopy were automatically mailed a stool test.(36) Overall screening increased with the multi-component intervention but the magnitude of the effect was largely due to stool testing, and the lack of improvement for colonoscopy can be likely attributed to the competing screening option. The positive effects of multi-component interventions further support the use of patient navigation in combination with additional types of reminders.

Boguradzka et al. published the only included study on PCP counseling,(33) and the observed strong positive effect compared to an information leaflet supports prior literature on the importance of physician recommendation for CRC screening.(40,41) For an invasive procedure like colonoscopy, physician counseling on the rationale and importance of the procedure may appear to be an obvious requirement—a foundation on which adjunctive interventions such as navigation can be added. This study serves as a reminder that the patient-physician interaction remains the central relationship for opportunistic screening colonoscopy.

Barriers to implementation of behavioral interventions for CRC screening include costs required to initiate and sustain programs, as well as underrecognition of the effectiveness of these interventions. However, cost-effectiveness analyses have shown that patient navigation—the most resource-intensive single intervention examined in this study—can yield a net financial benefit to health care institutions by increasing colonoscopy volume.(42,43) Studies such as ours will hopefully increase awareness among policymakers and health system leaders that investment in behavioral interventions will pay dividends for both patients and institutions.

A major strength of this study is the number of large population-based randomized controlled trials that included all or a representative sample of eligible participants within a region, which minimizes selection bias. In addition, although the majority of trials were conducted in the US, eight (32%) were international studies, which increases generalizability. We also acknowledge a couple limitations of the study. First, there was a moderate to high level of heterogeneity for the overall, multi-component intervention, and patient navigation analyses. This is not unexpected given the variations in study design and patient populations of the included trials. Second, the US Preventive Services Task Force has lowered the recommended CRC screening starting age to 45 years,(1) but since we did not have access to individual-level data, it is unclear whether the intervention effect differed by age in the 6 trials that included participants younger than 50 years. Although we have no reason to expect that these findings would not be generalizable to a slightly younger population, inclusion of younger adults in future studies would be necessary to confirm these results.

In summary, our systematic review and meta-analysis found that behavioral interventions, and in particular multi-component and patient navigation interventions, increase screening colonoscopy uptake. These results provide further support for the use of behavioral interventions in CRC screening overall. Additional studies are warranted to evaluate the most effective combination of interventions.

Study Highlights:

WHAT IS KNOWN

  • Behavioral interventions have been shown to improve participation in stool-based colorectal cancer screening.

  • The impact of behavioral interventions on screening colonoscopy uptake is unclear.

WHAT IS NEW HERE

  • In a systematic review and meta-analysis, behavioral interventions increased colonoscopy completion by 54%.

  • Patient navigation and multi-component interventions are the best-studied and most effective interventions.

Acknowledgement:

We thank Dr. Electra Paskett, Ms. Lina Jandorf, and their respective teams for providing additional information about their studies.

Funding:

PSL is supported by grant K08 CA230162 from the National Cancer Institute. The funding sources had no role in the analysis of data, preparation of the manuscript, or decision to submit the manuscript for publication.

COI/Financial Disclosures:

PSL has received research support from Epigenomics and Freenome and is on the advisory board for Guardant Health. The remaining authors have no disclosures.

Footnotes

Disclaimer: This material is the result of work supported in part by resources from the Veterans Health Administration. The content is solely the responsibility of the authors and does not represent the views of the U.S. Department of Veterans Affairs or the U.S. government.

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