Abstract
The effectiveness of colonoscopy is directly affected by the quality of the patient’s bowel preparation. Patients with lower socioeconomic status (SES) are at increased risk of having suboptimal bowel prep quality. Patient navigators can play a key role in clarifying bowel prep instructions. The aim of the present study was to examine the quality of bowel prep and its predictors among individuals of low SES undergoing screening colonoscopy with patient navigation. Participants (N = 607) were individuals of low SES who completed a screening colonoscopy with patient navigation. Demographic information was collected after the participants received a primary care referral for a screening colonoscopy. After the colonoscopy was completed, medical charts were reviewed to document the colonoscopists’ bowel prep quality ratings. A total of 6.8% (41/607) of the sample had poor bowel prep, which significantly correlated with having a colonoscopy that did not reach the cecum. If fair preps were included, approximately 19.3% (117/607) of our cohort would be considered to have suboptimal bowel prep. Our suboptimal bowel prep rates were better than those reported from other low SES samples.
Keywords
In recent years, colonoscopy has become the preferred colorectal cancer (CRC) screening method in many parts of the United States because it permits for both the detection and removal of adenomas (Rex, 2007). The effectiveness of screening colonoscopy (SC), however, is greatly affected by the quality of the examination, a major component of which is dependent on the quality of patient’s bowel preparation. Previous research has found that suboptimal bowel prep correlates with decreased adenoma detection rates (Delavari et al., 2014; Lebwohl, Kastrinos, et al., 2011), increased time to complete the colonoscopy (Chan, Saravanan, Manikam, Goh, & Mahadeva, 2011), and increased hospital costs (Rex, Imperiale, Latinovich, & Bratcher, 2002). Furthermore, when patients present with suboptimal bowel prep, gastroenterologists are likely to recommend either a repeat colonoscopy or a shorter time interval for a follow-up colonoscopy (Ben-Horin, Bar-Meir, & Avidan, 2007; Clark, Rustagi, & Laine, 2014; Larsen, Hills, & Terdiman, 2011). Some studies have found that a substantial proportion of their patients had suboptimal bowel preps. For example, a study using the Clinical Outcomes Research Initiative national endoscopic database examined bowel prep quality and reported that, of the 93,004 cases examined, approximately 23% had suboptimal (i.e., fair or poor) bowel prep (Harewood, Sharma, & de Garmo, 2003).
Data suggest that patients with lower socioeconomic status (SES) are at greatest risk of having suboptimal bowel prep. In fact, one study found that 34% of patients with Medicaid (a proxy for low SES) had suboptimal (i.e., fair, poor, inadequate) bowel prep compared to 18% among non-Medicaid patients (Lebwohl, Wang, & Neugut, 2010). In that study, the vast majority (86%) of patients with Medicaid were Black or Hispanic. Additionally, other indicators of SES, such as low education, have also been predictive of suboptimal bowel prep quality (Chan et al., 2011).
Our group has been investigating the role of patient navigation (PN) to facilitate completion of SC among urban minorities of low SES. Patient navigators play a key role in helping patients complete their colonoscopy, and among their more important duties is providing and clarifying bowel prep instructions with patients. Overall, we have found PN quite efficacious for improving SC completion (Braschi, Sly, Singh, Villagra, & Jandorf, 2013; Jandorf et al., 2013). One study conducted by Lebwohl, Neugut, et al. (2011) reported that PN may also improve bowel prep quality ratings in this at-risk population. The primary aim of the present study was to build on this literature and examine the bowel prep quality in patients of low SES who received PN. The secondary aim was to add to the extant literature by examining the demographic (i.e., age, race, gender, education, income, insurance, marital status, language) and process (e.g., SC appointment wait times, amount of PN call attempts) predictors of bowel prep quality in patients with low SES receiving patient navigation.
Method
Data were collected as part of a prospective study examining the efficacy of PN on SC completion (Braschi et al., 2013; Jandorf et al., 2013). The institutional review board approved the parent study and subsequent analyses. In the parent study, 611 participants received PN from our study staff and subsequently completed the SC. Four medical records were missing data on bowel prep quality leaving a total of 607 participants who were included in the data analyses. Eligibility for the parent study included asymptomatic for CRC, average-risk for CRC, at least 50 years old, and receipt of a physician referral for a SC. In accordance with the American Cancer Society, U.S. Multi-Task Force on Colorectal Cancer, and the American College of Radiology joint guidelines, primary care physicians referred average risk patients over the age of 50 for CRC screening, such as SC. Patients with active gastrointestinal symptoms, significant medical comorbidities, and/or a history of CRC or inflammatory bowel disease were excluded from the study.
Participants were recruited in the primary care clinic immediately after they received a physician recommendation and referral for a SC. Primary care physicians and medical staff referred eligible patients to the study. Interested patients met with a research assistant in a private exam room to provide informed consent. Then, consented participants completed a verbally administered questionnaire that assessed demographic information (i.e., age, education, gender, race, language, marital status, income, insurance type, employment status). All assessments were administered in the participants’ preferred language (English or Spanish). Then, participants received PN, which involved three phone calls: (a) a scheduling call (Time 1), (b) a call 2 weeks prior to the scheduled SC (Time 2), and (c) a call 3 days prior to the scheduled SC (Time 3). All Hispanic participants were paired with bilingual (Spanish/English) patient navigators so that the PN phone calls could be conducted in the participants’ preferred language.
A key component of the PN was to review the bowel prep instructions with the participants. The patient navigators mailed the bowel prep instructions to the participants immediately after they scheduled the SC (Time 1). The written instructions were provided in the participants’ preferred language. The instructions reviewed one of the three bowel cleansing regimens used at this institution: Half Lytley, Magnesium Citrate with Bisacodyl, or Miralax with Bisacodyl. Participants were instructed to eat a low-fiber diet 3 days before the SC and then a low-fiber breakfast the day of the procedure followed by only clear liquids (e.g., clear broth). In addition, the day before the procedure, the participants were asked to take their recommended doses of the prescribed laxative(s). Next, during the 2-week navigation call (Time 2), patient navigators reviewed the bowel prep instructions with the participants. Finally, during the 3-day reminder call (Time 3), participants were given the opportunity to ask the patient navigator any questions regarding the bowel prep. Throughout the study, the patient navigators documented the navigation process (i.e., total number of PN call attempts, number of complete navigation calls, minutes spent on navigation calls).
After the SC was completed, colonoscopists coded the bowel prep quality in the participants’ medical charts. In particular, when writing the endoscopy note, the colonoscopists were given the following prep quality options from a dropdown menu: poor, fair, good, excellent. There was no formal training to standardize bowel prep quality reporting. In our endoscopy unit, the quality of the bowel prep is rated as “excellent,” “good,” “fair,” or “poor.” Providers use “excellent” when minimal or no stool is present; “good” when clear fluid is in the lumen and requires suctioning; “fair” when semisolid stool is present and needs to be washed and suctioned; and “poor” when solid stool is encountered. After the SC was performed, endoscopy reports were reviewed to determine the bowel prep quality. No other information was gathered from the endoscopy reports.
Results
Data were analyzed using SPSS 20.0. Missing income data were imputed using the SAS procedure Multiple Imputation. Square route transformations were implemented to correct nonnormally distributed data for the process variables (i.e., total number of PN call attempts, wait times).
The average age of the 607 participants was 59.13 years (SD = 7.48 years). As shown in Table 1, participants were predominantly female (68.4%), single/living without a partner (69.4%), and English speaking (67.7%). Overall, 41.5% of the participants self-identified as African American, 49.6% as Hispanic, and 8.9% as “other.” With regard to indicators of SES, 66.6% of the sample had annual family income of less than $20,000 per year, 67.1% were unemployed, 52.2% had Medicaid insurance, and 27.0% had Medicare.
Demographic and Patient Navigation Process Data.
Note. Some percentages do not add up to 100% due to missing data.
As shown in Table 1, on average, the SC was completed 89.9 days (SD = 65.6) after the initial SC referral. On average, the navigators made 9.6 (SD = 6.3) call attempts and spent 55.4 (SD = 29.4) minutes completing the three navigation phone calls. Overall, the navigators were able to complete the majority of the navigation calls. In particular, 100% of the participants received the scheduling call (Time 1), 92.6% received the 2-week call (Time 2), and 88.1% received the 3-day reminder call (Time 3).
Of the 607 participants, bowel prep quality was reported as excellent in 60 (9.9%), good in 430 (70.8%), fair in 76 (12.5%), and poor in 41 (6.8%). Participants with a poor bowel prep quality were the most likely to have a colonoscopy that did not reach the cecum (r = 0.53, p < .001), when analyzing the data dichotomously (poor vs. other).
Univariate analyses (unadjusted) revealed that having lower income, speaking English (rather than Spanish/bilingual), being unemployed, and having more PN call attempts were all predictive (p < .10) of having poor bowel prep quality (Table 2). Significant predictors of poor bowel prep were entered into a logistic regression analysis. The multivariate (adjusted) model was significant, χ(5, N = 580) = 21.73, p < .01, and explained between 3.7% (Cox & Snell R2) and 9.6% (Nagelkerke R2) of the model. The model found that having lower income and speaking English (rather than Spanish/bilingual) remained statistically significant as predictors of poor bowel prep. There was a statistical trend (p = .09) between the number of total number of PN call attempts and the quality of bowel preparation, such that more call attempts were predictive of poorer bowel prep.
Adjusted and Unadjusted Predictors of Having Poor Bowel Prep Quality.
Note. OR = odds ratio; CI = confidence interval. p values greater than .10 are bolded.
Discussion
The present study analyzed bowel prep quality in average-risk individuals undergoing SC facilitated by PN. Participants were predominantly Black and Hispanic individuals of low SES seen in our primary care clinics. Approximately two thirds of the study population earned less than $20,000 per year, 79% had public health insurance, two thirds were unemployed, and 69% were single or living without a partner. One third was bilingual or spoke Spanish as their only language. Our previous data demonstrated that with patient navigation, between 74% and 81% of individuals completed their SC (Braschi et al., 2013; Jandorf et al., 2013). In the present study, we examined the quality of bowel preps in this population and what factors might predict poor preps.
We found that a small but substantial proportion (6.8%) of individuals in our sample had poor bowel prep quality. Not surprisingly, this correlated with having a colonoscopy that did not reach the cecum. Our poor bowel prep rates were comparable to the rates of other low-income samples that received PN. In particular, one study reported that 7% of a navigated sample of predominantly Blacks and Hispanics had poor bowel prep (Lebwohl, Neugut, et al., 2011). Similarly, a PN program in South Carolina with a predominantly Black sample reported that 7.9% of their participants had poor bowel prep quality (Xirasagar, Li, Burch, et al., 2014). If fair preps were included, as has been done in previous literature, approximately 19% of our cohort would be considered to have suboptimal bowel prep. Our suboptimal bowel prep rates (19%) were lower than those reported in other PN studies of 30.6% (Xirasagar, 2014) and 34% (Lebwohl, Neugut, et al., 2011).
Our suboptimal bowel prep rates were also better than those reported from other low SES samples that did not receive PN. For example, in previous studies, 34% of patients with Medicaid had suboptimal (i.e., fair, poor, inadequate) bowel prep (Lebwohl et al., 2010) and 44% of patients with less than a secondary education had suboptimal (i.e., poor) bowel prep (Chan et al., 2011). However, in our sample, when patients of low SES received language matched PN, their suboptimal bowel prep quality rates (19%) were comparable with the general population (23%; Harewood et al., 2003). These results build on the existing literature (Lebwohl, Neugut, et al., 2011) that suggests that PN may substantially improve bowel prep quality in patients of low SES. However, without a control group, we are unable to determine the exact impact PN has on bowel prep quality. A future randomized clinical trial could formally examine the impact of PN on bowel prep quality in a low-income, predominantly Black and Hispanic sample.
The second aim of the study was to identify predictors of poor bowel prep quality in this sample. Despite most participants reporting an income lower than $20,000, income level was still significantly associated with bowel prep quality. These findings are consistent with previous studies that have found that individuals of low SES are at greatest risk of having suboptimal bowel prep quality (Chan et al., 2011; Lebwohl et al., 2010). Other indicators of SES, such as education and insurance status, were not significantly related to bowel prep quality. Interventions are needed to help the lowest income patients improve their SC bowel prep.
The results further revealed that participants who spoke monolingual or bilingual Spanish curiously enough had better bowel prep quality than participants who spoke only English. This finding stands in contrast to previous literature indicating that patients who require a translator are at greater risk of having suboptimal bowel prep (Nguyen & Wieland, 2010). Our language-matched PN model may have significantly helped non-English speaking participants prepare for the SC. In the parent study, all Hispanic participants were matched with native bilingual (Spanish/English) patient navigators who provided the PN, including the bowel prep instructions, in the participants’ preferred language. It is possible that, by overcoming language barriers, language-matched PN may improve the bowel prep quality ratings for non-English speaking patients. A formal randomized clinical trial is needed in order to definitively determine the effect of language-matched PN on bowel prep quality for bilingual/Spanish speaking patients.
We also found a trend suggesting that certain aspects of the PN process itself were related to bowel prep quality. In particular, participants who required more PN call attempts were more likely to have poorer bowel prep. Based on these results, patients who are more difficult to reach during PN may require more intensive and targeted interventions to help them better prepare for the SC.
A strength of our study is that all research participants underwent SC as part of a prospective clinical trial allowing us to both confirm their asymptomatic, average-risk status and ensure that all of the elements of PN took place as intended. In addition, we had almost complete data on colonoscopy prep quality in the procedure reports. Nonetheless, there are limitations to the study that should be considered when interpreting the results. For one, although our results suggest that PN may have improved bowel prep quality for patients of low SES, drawing definitive conclusions would best be done by a prospective randomized clinical trial. A second limitation is that the reliability and validity of the bowel prep quality ratings are unknown, and thus there may be interphysician variability in the ratings. In common clinical practice, a unified bowel prep quality rating system has not been universally adopted. At our institution as well as other clinical practices, colonoscopists rate bowel prep quality ranging from “excellent” to “poor.” However, the American Society for Gastrointestinal Endoscopy and the American College of Gastroenterology Taskforce on Quality in Endoscopy report that, in clinical practice, these ratings often lack well-accepted operational definitions (Rex et al., 2006). In an attempt to standardized bowel prep quality ratings, the Boston Bowel Preparation Scale (Calderwood & Jacobson, 2010; Lai, Calderwood, Doros, Fix, & Jacobson, 2009), Aronchick Scale (American Society for Gastrointestinal Endoscopy Standards of Practice Committee, 2015), and the Ottawa Bowel Preparation Scale (Rostom & Jollcoeur, 2004) have been developed. Although these scales have proven valid and reliable, they are underutilized in clinical practice. Future efforts are needed to standardize and operationalize bowel prep quality ratings in standard clinical care. A third limitation is that we did not collect data on other potential predictors of bowel prep quality such as compliance with the bowel prep regimen, history of poor bowel preparation, use of tricyclic antidepressants, and presence of medical comorbidities (e.g., obesity; American Society for Gastrointestinal Endoscopy Standards of Practice Committee, 2015). Such data could add to our understanding of the reasons why patients might still have poor bowel prep before a SC. A final limitation to our study is that the predictive effects, while positive, are relatively small, suggesting that other factors may better account for variability in bowel prep quality.
The results of this study can be used to inform clinical practice. They provide further support for the use of PN to not only improve SC completion but also to improve bowel prep quality, further strengthening the argument for integrating PN into standard clinical practice. This could decrease the need for repeat procedures and decrease both direct and indirect costs for CRC care, especially in an Accountable Care Organization system where populations are managed with limited funds. Furthermore, despite promising results, a small yet significant proportion of the sample still had poor bowel prep quality. Additional studies are needed in the population in order to determine what is missing from PN in order to improve bowel prep for this subgroup and offer all patients high quality colonoscopies.
Footnotes
Declaration of Conflicting Interests
The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding
Preparation of this manuscript was supported by the National Cancer Institute (R01CA120658) and the American Cancer Society (122931-PF-12-117-01-CPPB). The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Cancer Institute, National Institutes of Health or the American Cancer Society.