THE RED SECTION
nature publishing group
see related editorial on page x
Underuse of Surveillance Colonoscopy in Patients at Increased Risk of Colorectal Cancer Caitlin C. Murphy, MPH1, Carmen L. Lewis, MD, MPH2, Carol E. Golin, MD3, 4 and Robert S. Sandler, MD, MPH1, 5 OBJECTIVES:
Colorectal cancer incidence and mortality have declined over the past two decades, and much of this improvement is attributed to increased use of screening. Approximately 25% of patients who undergo screening colonoscopy have premalignant adenomas that require removal and follow-up colonoscopy. However, there are few studies of the use of surveillance colonoscopy in increased risk patients with previous adenomas.
METHODS:
We conducted a cross-sectional study to examine factors associated with underuse of surveillance colonoscopy among patients who are at increased risk for colorectal cancer. The study population consisted of patients with previously identified adenomatous polyps and who were due for follow-up colonoscopy. Patients were categorized as attenders (n=100) or non-attenders (n=104) on the basis of completion of follow-up colonoscopy. Telephone surveys assessed the use of surveillance colonoscopy across domains of predisposing patient characteristics, enabling factors, and patient need. Mutlivariable logistic regression was used to identify factors associated with screening completion.
RESULTS:
Perceived barriers, perceived benefits, social deprivation, and cancer worry were associated with attendance at colonoscopy. Higher benefits (odds ratio (OR) 2.37, 95% confidence interval (CI) 1.04– 5.41) and cancer worry (OR 1.73, 95% CI 1.07–2.79) increased the odds of attendance at follow-up colonoscopy, whereas greater barriers (OR 0.49, 95% CI 0.28–0.88) and high social deprivation (≥2; OR 0.09, 95% CI 0.01–0.76) were associated with lower odds.
CONCLUSIONS:
Our results suggest that multilevel factors contribute to the use of surveillance colonoscopy in higher risk populations, many of which are amenable to intervention. Interventions, such as patient navigation, may help facilitate appropriate use of surveillance colonoscopy.
Am J Gastroenterol 2015; 110:633–641; doi:10.1038/ajg.2014.344; published online 11 November 2014
Background
Although colorectal cancer remains the second leading cause of cancer death among men and women in the US, both the incidence and mortality have declined over the past two decades (1). A substantial proportion of this improvement has been attributed to an increased use of screening (2). Data from the National Health Interview Survey (NHIS) from 2000 to 2010 suggest that most of the increase in screening has been due to increased use of colonoscopy (3). An estimated 11–14 million colonoscopies are performed in the US annually (4,5).
Approximately 25% of patients who undergo screening colonoscopy have premalignant adenomas that require removal and follow-up (i.e., surveillance) colonoscopy. These patients are considered to be at increased risk of colorectal cancer, and current guidelines recommend that they undergo a repeat exam in 3–5 years (6). However, there have been surprisingly few studies of surveillance colonoscopy in patients with previous adenomas. Underuse of surveillance colonoscopy remains an ongoing concern in this population (7). Appropriate use of surveillance colonoscopy may ultimately improve quality and reduce the cost and burden of colorectal
1 Department of Epidemiology, Gillings School of Public Health, The University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, USA; 2Department of Medicine, Division of General Internal Medicine, University of Colorado, Boulder, Colorado, USA; 3Department of Medicine, School of Medicine, The University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, USA; 4Department of Health Behavior, Gillings School of Public Health, The University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, USA; 5Center for Gastrointestinal Biology and Disease, The University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, USA. Correspondence: Robert S. Sandler, MD, MPH, Center for Gastrointestinal Biology and Disease The University of North Carolina at Chapel Hill, CB# 7555, 4157 Bioinformatics Building Chapel Hill, Chapel Hill, North Carolina 27599-7555, USA. E-mail: [email protected]
© 2015 by the American College of Gastroenterology
The American Journal of GASTROENTEROLOGY
633
634
THE RED SECTION
cancer. To address this research need, we examined multilevel factors contributing to underuse of surveillance colonoscopy among patients who are at increased risk for colorectal cancer. Understanding patterns of and factors associated with surveillance colonoscopy use is an important first step toward identifying effective strategies to promote appropriate use of colonoscopy.
446 consecutive patients (age.30 years) due for follow-up colonoscopy at UNC and sent appointment letters during July– September 2012
340 patients randomly selected as potentially eligible for study
Methods
Participants and procedures We conducted a cross-sectional study of factors associated with the use of surveillance colonoscopy among patients with a history of colorectal adenoma. Patients who underwent screening colonoscopy at the University of North Carolina (UNC) Hospitals (Chapel Hill, NC), with previously identified adenomatous polyps, and who were due for follow-up colonoscopy were eligible for the study. Endoscopy documentation software (ProVation® Medical, Minneapolis, MN) at UNC generates appointment letters that are sent to patients when the next colonoscopy should be scheduled. Letters are based on the interval recommended by the treating physician and entered into the database following the initial exam. Follow-up intervals are selected on the basis of the endoscopic findings and pathology reports. Patients who do not schedule an exam after receiving the appointment letter are sent up to two reminder letters. No further contact is made after both reminder letters are sent. To determine the use of surveillance colonoscopy, we generated lists of patients aged ≥30 years who were sent an appointment letter (i.e., required a follow-up exam) during a consecutive 3-month period (July–September 2012). We defined “attenders” as patients who completed a follow-up colonoscopy. Completion of colonoscopy was measured by electronic medical record and later verified by patient self-report. “Non-attenders” were patients who did not schedule a follow-up exam after 90 days of receiving a second reminder letter or did not complete a colonoscopy. Both patients who did not schedule an appointment and patients who scheduled an appointment but did not arrive were considered “non-attenders.” We randomly sampled 340 potentially eligible participants from the total list of attenders and non-attenders (n=446). Sampling probabilities were based on the distribution of age, sex, and race/ ethnicity of non-attenders. A research assistant reviewed the electronic medical record to exclude patients who were non-English speaking or with reasons for a follow-up exam other than adenoma (e.g., inflammatory bowel disease, cancer; n=51). The remaining eligible participants (n=289) were then sent an invitation letter and brochure describing the study. The letter also included a telephone number to request additional information or to opt out of the study. Of the eligible participants, 64 (22.1%) could not be contacted and 21 (7.3%) refused. Participants with undeliverable letters were replaced one-for-one until we achieved our target number of 100 interviewed participants in each group (Figure 1). Two weeks following any non-returned invitation letter (i.e., not returned because of wrong address or patient did not opt out), the research assistant called patients to describe the study and determine whether the patient was interested in participatThe American Journal of GASTROENTEROLOGY
51 patients excluded for the following reasons: • Non-english speaking • Follow-up exam for purpose other than adenoma (e.g., inflammatory bowel disease, cancer)
289 remaining eligible patients sent study invitation letter and brochure
64 patients could not be contacted
21 patients refuse to participate in study
204 patients participate in study and complete telephone interview
100 attenders
104 non-attenders
Figure 1. Process of participant selection into the study.
ing. Up to nine call attempts (with three voicemail messages) were made to reach the participants. Once a participant was reached, the research assistant explained the purpose of the study, verified receipt of the appointment letter (>80% of study participants recalled receiving the letter), and administered an interview survey to willing participants. The study invitation and survey were most often conducted in a single telephone call (median, 1; range, 1–4). Telephone calls were an average duration of 20.4 min (range 8–59 min). Participants were sent a $20 gift card, as compensation for completing the survey. Measures We developed the telephone interview survey on the basis of a conceptual framework derived from Andersen’s Behavioral Theory of HealthCare Utilization (8), which suggests that a patient’s use of health services is a function of their predisposition to use services, factors that enable or impede use, and their need for care. All items and measures included in the telephone survey are listed in the Appendix 1. Predisposing characteristics. Predisposing characteristics included demographic factors (e.g., age and sex), social structure (e.g., education, employment, race/ethnicity), and health beliefs VOLUME 110 | MAY 2015 www.amjgastro.com
THE RED SECTION
(e.g., attitude, values, norms). Health beliefs were assessed by 20 items that measured psychosocial constructs related to colorectal cancer screening: perceived barriers, perceived benefits, and selfefficacy to be screened. Items and scales were adapted from colorectal cancer screening intervention trials (9–11) and have been validated in diverse settings (12–17). Perceived barriers measured negative aspects of screening (10 items, α =0.68), and perceived benefits measured positive aspects (7 items, α =0.76). Self-efficacy assessed a participant’s confidence in their ability to perform certain aspects related to screening (4 items, α =0.77). Barrier items were measured on a 5-point scale ranging from “1” for “strongly disagree” to “5” for “strongly agree”, and benefits and self-efficacy items were measured on a 4-point scale ranging from “1” for “strongly disagree” to “4” for “strongly agree”. Enabling factors. Enabling factors must be present for a patient to effectively use health services (8). We assessed health insurance, insurance type, regular source of care (i.e., usual primary care physician), difficulty understanding the appointment letter, out-of-pocket costs, and social deprivation. Social deprivation was based on an index of socioeconomic deprivation developed by Power et al. (18) to predict colorectal cancer screening intention and attendance. The index combines dichotomous answers (i.e., yes/no) to questions on education, home ownership, and car ownership to create a scale from 0 (low deprivation) to 3 (high deprivation). Patient need. Patient need factors considered how participants viewed their own health and functional state, as well as how they experience symptoms of illness, pain, and worries about their health. Health status variables included comorbidity, recent inpatient hospitalizations (within last year), smoking history, and functional status. Patient comorbidity was measured using an adapted version of the Charlson Comorbidity Index based on self-report (19). Functional status was measured using the selfreported Instrumental Activities of Daily Living scale (20) and a single 5-point item from the SF-12 (“How would you describe your general health for someone your age?”) (21). We also measured cancer worry and perceived susceptibility with previously validated scales adapted from colorectal cancer screening trials (12). Cancer worry measured negative effects related to the threat of colorectal cancer with four items (α =0.63) and perceived susceptibility measured subjective personal risk of colorectal cancer or polyps with three items (α =0.78). All items were measured on a 4-point scale, where higher scores correspond to higher levels of the variable being measured. Statistical analysis Pearson’s χ 2 or Fisher’s exact tests were used to compare categorical characteristics of attenders and non-attenders, and Student’s t-tests or Wilcoxon rank-sum tests were used to compare continuous characteristics. To build a multivariable model, we first calculated Spearman’s correlation coefficient among scales and covariates to assess collinearity of potential correlates. Participants’ age and race were © 2015 by the American College of Gastroenterology
included as a priori correlates of attendance at follow-up colonoscopy. Other variables were selected if they were significantly associated with attendance in the univariable analysis (P
nature publishing group
see related editorial on page x
Underuse of Surveillance Colonoscopy in Patients at Increased Risk of Colorectal Cancer Caitlin C. Murphy, MPH1, Carmen L. Lewis, MD, MPH2, Carol E. Golin, MD3, 4 and Robert S. Sandler, MD, MPH1, 5 OBJECTIVES:
Colorectal cancer incidence and mortality have declined over the past two decades, and much of this improvement is attributed to increased use of screening. Approximately 25% of patients who undergo screening colonoscopy have premalignant adenomas that require removal and follow-up colonoscopy. However, there are few studies of the use of surveillance colonoscopy in increased risk patients with previous adenomas.
METHODS:
We conducted a cross-sectional study to examine factors associated with underuse of surveillance colonoscopy among patients who are at increased risk for colorectal cancer. The study population consisted of patients with previously identified adenomatous polyps and who were due for follow-up colonoscopy. Patients were categorized as attenders (n=100) or non-attenders (n=104) on the basis of completion of follow-up colonoscopy. Telephone surveys assessed the use of surveillance colonoscopy across domains of predisposing patient characteristics, enabling factors, and patient need. Mutlivariable logistic regression was used to identify factors associated with screening completion.
RESULTS:
Perceived barriers, perceived benefits, social deprivation, and cancer worry were associated with attendance at colonoscopy. Higher benefits (odds ratio (OR) 2.37, 95% confidence interval (CI) 1.04– 5.41) and cancer worry (OR 1.73, 95% CI 1.07–2.79) increased the odds of attendance at follow-up colonoscopy, whereas greater barriers (OR 0.49, 95% CI 0.28–0.88) and high social deprivation (≥2; OR 0.09, 95% CI 0.01–0.76) were associated with lower odds.
CONCLUSIONS:
Our results suggest that multilevel factors contribute to the use of surveillance colonoscopy in higher risk populations, many of which are amenable to intervention. Interventions, such as patient navigation, may help facilitate appropriate use of surveillance colonoscopy.
Am J Gastroenterol 2015; 110:633–641; doi:10.1038/ajg.2014.344; published online 11 November 2014
Background
Although colorectal cancer remains the second leading cause of cancer death among men and women in the US, both the incidence and mortality have declined over the past two decades (1). A substantial proportion of this improvement has been attributed to an increased use of screening (2). Data from the National Health Interview Survey (NHIS) from 2000 to 2010 suggest that most of the increase in screening has been due to increased use of colonoscopy (3). An estimated 11–14 million colonoscopies are performed in the US annually (4,5).
Approximately 25% of patients who undergo screening colonoscopy have premalignant adenomas that require removal and follow-up (i.e., surveillance) colonoscopy. These patients are considered to be at increased risk of colorectal cancer, and current guidelines recommend that they undergo a repeat exam in 3–5 years (6). However, there have been surprisingly few studies of surveillance colonoscopy in patients with previous adenomas. Underuse of surveillance colonoscopy remains an ongoing concern in this population (7). Appropriate use of surveillance colonoscopy may ultimately improve quality and reduce the cost and burden of colorectal
1 Department of Epidemiology, Gillings School of Public Health, The University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, USA; 2Department of Medicine, Division of General Internal Medicine, University of Colorado, Boulder, Colorado, USA; 3Department of Medicine, School of Medicine, The University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, USA; 4Department of Health Behavior, Gillings School of Public Health, The University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, USA; 5Center for Gastrointestinal Biology and Disease, The University of North Carolina at Chapel Hill, Chapel Hill, North Carolina, USA. Correspondence: Robert S. Sandler, MD, MPH, Center for Gastrointestinal Biology and Disease The University of North Carolina at Chapel Hill, CB# 7555, 4157 Bioinformatics Building Chapel Hill, Chapel Hill, North Carolina 27599-7555, USA. E-mail: [email protected]
© 2015 by the American College of Gastroenterology
The American Journal of GASTROENTEROLOGY
633
634
THE RED SECTION
cancer. To address this research need, we examined multilevel factors contributing to underuse of surveillance colonoscopy among patients who are at increased risk for colorectal cancer. Understanding patterns of and factors associated with surveillance colonoscopy use is an important first step toward identifying effective strategies to promote appropriate use of colonoscopy.
446 consecutive patients (age.30 years) due for follow-up colonoscopy at UNC and sent appointment letters during July– September 2012
340 patients randomly selected as potentially eligible for study
Methods
Participants and procedures We conducted a cross-sectional study of factors associated with the use of surveillance colonoscopy among patients with a history of colorectal adenoma. Patients who underwent screening colonoscopy at the University of North Carolina (UNC) Hospitals (Chapel Hill, NC), with previously identified adenomatous polyps, and who were due for follow-up colonoscopy were eligible for the study. Endoscopy documentation software (ProVation® Medical, Minneapolis, MN) at UNC generates appointment letters that are sent to patients when the next colonoscopy should be scheduled. Letters are based on the interval recommended by the treating physician and entered into the database following the initial exam. Follow-up intervals are selected on the basis of the endoscopic findings and pathology reports. Patients who do not schedule an exam after receiving the appointment letter are sent up to two reminder letters. No further contact is made after both reminder letters are sent. To determine the use of surveillance colonoscopy, we generated lists of patients aged ≥30 years who were sent an appointment letter (i.e., required a follow-up exam) during a consecutive 3-month period (July–September 2012). We defined “attenders” as patients who completed a follow-up colonoscopy. Completion of colonoscopy was measured by electronic medical record and later verified by patient self-report. “Non-attenders” were patients who did not schedule a follow-up exam after 90 days of receiving a second reminder letter or did not complete a colonoscopy. Both patients who did not schedule an appointment and patients who scheduled an appointment but did not arrive were considered “non-attenders.” We randomly sampled 340 potentially eligible participants from the total list of attenders and non-attenders (n=446). Sampling probabilities were based on the distribution of age, sex, and race/ ethnicity of non-attenders. A research assistant reviewed the electronic medical record to exclude patients who were non-English speaking or with reasons for a follow-up exam other than adenoma (e.g., inflammatory bowel disease, cancer; n=51). The remaining eligible participants (n=289) were then sent an invitation letter and brochure describing the study. The letter also included a telephone number to request additional information or to opt out of the study. Of the eligible participants, 64 (22.1%) could not be contacted and 21 (7.3%) refused. Participants with undeliverable letters were replaced one-for-one until we achieved our target number of 100 interviewed participants in each group (Figure 1). Two weeks following any non-returned invitation letter (i.e., not returned because of wrong address or patient did not opt out), the research assistant called patients to describe the study and determine whether the patient was interested in participatThe American Journal of GASTROENTEROLOGY
51 patients excluded for the following reasons: • Non-english speaking • Follow-up exam for purpose other than adenoma (e.g., inflammatory bowel disease, cancer)
289 remaining eligible patients sent study invitation letter and brochure
64 patients could not be contacted
21 patients refuse to participate in study
204 patients participate in study and complete telephone interview
100 attenders
104 non-attenders
Figure 1. Process of participant selection into the study.
ing. Up to nine call attempts (with three voicemail messages) were made to reach the participants. Once a participant was reached, the research assistant explained the purpose of the study, verified receipt of the appointment letter (>80% of study participants recalled receiving the letter), and administered an interview survey to willing participants. The study invitation and survey were most often conducted in a single telephone call (median, 1; range, 1–4). Telephone calls were an average duration of 20.4 min (range 8–59 min). Participants were sent a $20 gift card, as compensation for completing the survey. Measures We developed the telephone interview survey on the basis of a conceptual framework derived from Andersen’s Behavioral Theory of HealthCare Utilization (8), which suggests that a patient’s use of health services is a function of their predisposition to use services, factors that enable or impede use, and their need for care. All items and measures included in the telephone survey are listed in the Appendix 1. Predisposing characteristics. Predisposing characteristics included demographic factors (e.g., age and sex), social structure (e.g., education, employment, race/ethnicity), and health beliefs VOLUME 110 | MAY 2015 www.amjgastro.com
THE RED SECTION
(e.g., attitude, values, norms). Health beliefs were assessed by 20 items that measured psychosocial constructs related to colorectal cancer screening: perceived barriers, perceived benefits, and selfefficacy to be screened. Items and scales were adapted from colorectal cancer screening intervention trials (9–11) and have been validated in diverse settings (12–17). Perceived barriers measured negative aspects of screening (10 items, α =0.68), and perceived benefits measured positive aspects (7 items, α =0.76). Self-efficacy assessed a participant’s confidence in their ability to perform certain aspects related to screening (4 items, α =0.77). Barrier items were measured on a 5-point scale ranging from “1” for “strongly disagree” to “5” for “strongly agree”, and benefits and self-efficacy items were measured on a 4-point scale ranging from “1” for “strongly disagree” to “4” for “strongly agree”. Enabling factors. Enabling factors must be present for a patient to effectively use health services (8). We assessed health insurance, insurance type, regular source of care (i.e., usual primary care physician), difficulty understanding the appointment letter, out-of-pocket costs, and social deprivation. Social deprivation was based on an index of socioeconomic deprivation developed by Power et al. (18) to predict colorectal cancer screening intention and attendance. The index combines dichotomous answers (i.e., yes/no) to questions on education, home ownership, and car ownership to create a scale from 0 (low deprivation) to 3 (high deprivation). Patient need. Patient need factors considered how participants viewed their own health and functional state, as well as how they experience symptoms of illness, pain, and worries about their health. Health status variables included comorbidity, recent inpatient hospitalizations (within last year), smoking history, and functional status. Patient comorbidity was measured using an adapted version of the Charlson Comorbidity Index based on self-report (19). Functional status was measured using the selfreported Instrumental Activities of Daily Living scale (20) and a single 5-point item from the SF-12 (“How would you describe your general health for someone your age?”) (21). We also measured cancer worry and perceived susceptibility with previously validated scales adapted from colorectal cancer screening trials (12). Cancer worry measured negative effects related to the threat of colorectal cancer with four items (α =0.63) and perceived susceptibility measured subjective personal risk of colorectal cancer or polyps with three items (α =0.78). All items were measured on a 4-point scale, where higher scores correspond to higher levels of the variable being measured. Statistical analysis Pearson’s χ 2 or Fisher’s exact tests were used to compare categorical characteristics of attenders and non-attenders, and Student’s t-tests or Wilcoxon rank-sum tests were used to compare continuous characteristics. To build a multivariable model, we first calculated Spearman’s correlation coefficient among scales and covariates to assess collinearity of potential correlates. Participants’ age and race were © 2015 by the American College of Gastroenterology
included as a priori correlates of attendance at follow-up colonoscopy. Other variables were selected if they were significantly associated with attendance in the univariable analysis (P
